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THE HUMAN HEALTH ASPECTS OF THE
MYCOBACTERIUM BOVIS (BOVINE TUBERCULOSIS)
OUTBREAK IN MICHIGAN

presented by

MELINDA JEAN WILKINS

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5/08 K lProyAchres/CIRC/Daleoue Indd

THE HUMAN HEALTH ASPECTS OF THE MYCOBACTERIUM BOVIS
(BOVINE TUBERCULOSIS) OUTBREAK IN MICHIGAN

By

Melinda Jean Wilkins

A DISSERTATION
Submitted to
Michigan State University
In partial fulfillment of the requirements
for the degree of
DOCTOR OF PHILOSOPHY
Department of Large Animal Clinical Sciences

2008

ABSTRACT

THE HUMAN HEALTH ASPECTS OF THE MYCOBACTERIUM BOVIS
(BOVINE TB) OUTBREAK IN MICHIGAN

By

Melinda Jean Wilkins

The current outbreak of Mycobacterium bovis (bovine TB) in the white-tailed
deer (Odocoileus virginianus) and cattle populations of the northeastern portion of the
lower peninsula of Michigan offers a unique research opportunity to explore the health
impact of the outbreak on human health. Five independent research projects were
conducted, each focusing on a different aspect of how humans interact with deer and
cattle, potential exposure via pets, and examination of evidence of subclinical infection in
an analysis of TB skin test data from the affected counties.

The first project was a survey of deer hunters in both the bovine TB endemic and
non-endemic areas. The study determined that less than half were practicing basic health
precautions, such as wearing gloves, when handing potentially infected deer carcasses.

The second project summarized the human cases of M bovis infection reported in
Michigan from 1997 - 2007. Two of these patients were infected with the same genetic
strain of M. bovis circulating in the deer and cattle populations of Michigan, and both had
had exposure to deer in the endemic area.

The third project examined the role that domestic pets on infected cattle farms
might play in the transmission of M. bovis to both humans and non-infected livestock.
This study concludes that in Michigan, pets would expectedly play a minimal role in

disease transmission on the farm. This conclusion is based on a variety of factors, but

mainly due to a lack of evidence of infection in the pets, probably because the affected
cattle herds are detected in the early stages of infection.

The fourth project focused on the human “costs” of the disease control efforts in
cattle by measuring the incidence density of human injuries acquired while TB testing
livestock in 2001. Most of the injuries were found to be preventable, and
recommendations were made to decrease injuries in the fiiture.

The fifth project used risk factor exposure data for both M. tuberculosis and for
M. bovis paired with tuberculosis skin test (TDT) results from 12 local health
departments to determine if evidence is suggestive of the presence of subclinical
tuberculosis infections in persons with exposure risks. Being foreign born or a venison
processor were found to be significant risk factors for having a positive TST. This data
intimates that venison processors should be added to the list of groups targeted for public
health prevention messages for M. bovis.

These projects together elucidate distinct human health risks associated with the
Bovine TB outbreak in Michigan, and suggest that hunters, venison processors,
veterinarians, and owners of infected herds should receive targeted risk prevention
messages tailored to their specific routes of exposure to M. bovis. Surveillance efforts to
detect human cases of M. bovis should continue with thorough investigations to
determine likely sources of exposure, as M. bovis will likely remain endemic in this part

of Michigan for the foreseeable future.

This work is dedicated to my family, especially my partner, parents and siblings
who were continuous in their support and encouragement. I also dedicate this to
my children, in hopes that they will find passion and joy in the educational

process and enjoy both learning and teaching as much as I have.

iv

ACKNOWLEDGEMENTS

I would like to take this opportunity to acknowledge the contribution of
the many individuals who made the completion of this work possible. Without
your selfless contributions of time and knowledge this work would never have
been completed. First and foremost, I acknowledge the unending patience and
support of Dr. Paul Bartlett, my major professor. Dr. Bartlett’s quiet and
unhurried leadership made it possible for me to complete this Ph.D. on a timetable
compatible with the rest of my life and my many competing priorities. I also
acknowledge my other committee members, Drs. Matthew Boulton, John
Kaneene, Barbara Robinson-Dunn, Theresa Bernardo, and Ronald Erskine.
Together they have all unselfishly contributed time, knowledge and expertise to
my work, allowing me to mature as a researcher and an individual. I am honored
to have benefited from such a collective pool of wisdom. Dr. Corinne Miller also
deserves special mention for her role as a committee member (2001-2004) and her
willingness to serve as my external examiner.

I would like to thank Sarah Trembley, Jennifer Sexsmith, Chrysin Wood,
Drs. Kimberly Signs and Shelley Stoneciper for their help with on-farm data
collection, and Jennifer Dewitt and Melissa Gallego for help with data entry. A
special thanks to Dr. Kathy Schwarts and her staff at the Alpena Animal Hospital,
and USDA Veterinary Services and Wildlife Services for support with the pet

study. I also thank the staff of Health District #2, Health District #4, and

Northwest Michigan Community Health Agency for their participation in the
tuberculosis skin testing project.

I am grateful for the financial support I received from Dr. Bartlett for
assistance with tuition and student support, from the College of Veterinary
Medicine for the Dissertation Completion Fellowship, and especially for the
cooperative agreement support from USDA, APHIS. Without such support, this
project would not have been possible. I also would like to acknowledge the
scheduling flexibility offered by my supervisors at Michigan Department of
Community Health throughout this project period.

Finally, I would like to acknowledge my family’s contribution to this
work. They all contributed in so many large and small ways, past and present.

I hope that all who offered support and assistance at any point along the way will
know that I am truly grateful for you, and grateful for this wonderful opportunity
to learn and grow. I hope to make you proud, and I will take every opportunity to

assist the next generation of students and lovers of learning.

vi

TABLE OF CONTENTS

LIST OF TABLES .................................................................................. x
LIST OF FIGURES ................................................................................ xi
INTRODUCTION .................................................................................... 1
Setting ................................................................................................ 1
Purpose statement .................................................................................. 3
Importance of findings ............................................................................ 9
References .......................................................................................... 10
CHAPTER 1
LITERATURE REVIEW .......................................................................... 11
Michigan outbreak setting ........................................................................ 11
Human infection with M. bovis .................................................................. 15
General characteristics of M. bovis as an organism ................................. 15
Immune response ........................................................................... 15
Tuberculosis skin test (TST) .............................................................. l7
Pathogenesis and clinical manifestations in humans .................................. 18
Human exposure to M. bovis and populations at risk of infection ................... 22
Populations at risk of exposure ........................................................... 24
Injuries associated with veterinary practice ................................................... 25
References .......................................................................................... 27
CHAPTER 2

MY COBACT ERI UM BO VIS (BOVINE TB) EXPOSURE AS A RECREATIONAL
RISK FOR HUNTERS: RESULTS OF THE MICHIGAN HUNTER SURVEY—

2001 ................................................................................................... 35
Abstract ............................................................................................. 35
Introduction ........................................................................................ 36
Methods ............................................................................................. 41
Results .............................................................................................. 49
Discussion .......................................................................................... 52
Conclusion ......................................................................................... 57
References .......................................................................................... 59

vii

CHAPTER 3
HUMAN MYCOBACT ER] UM B0 VIS INFECTION ASSOCIATED WITH

THE BOVINE TB OUTBREAK IN MICHIGAN, 1994 -2007 .............................. 61
Abstract ............................................................................................. 61
Introduction ........................................................................................ 61
Case 1, 2002 ....................................................................................... 65
Case 2, 2004 ....................................................................................... 70
Conclusion .......................................................................................... 74
References .......................................................................................... 76

CHAPTER 4

ABSENCE OF M YCOBACT ERIUM BOVIS INFECTION IN DOGS AND CATS

RESIDING ON INFECTED CATTLE FARMS -- MICHIGAN, 2002 ..................... 78
Abstract ............................................................................................. 78
Introduction ........................................................................................ 78
Methods ............................................................................................. 81
Results .............................................................................................. 85
Discussion .......................................................................................... 88
Conclusion ......................................................................................... 91
References .......................................................................................... 93

CHAPTER 5

INJURIES ASSOCIATED WITH BOVINE TB TESTING LIVESTOCK IN

MICHIGAN, 2001. ................................................................................. 96
Abstract ............................................................................................. 96
Introduction ......................................................................................... 97
Methods ............................................................................................. 99
Analysis ........................................................................................... 102
Results ............................................................................................. 102
Discussion ........................................................................................ 1 16
Conclusion ....................................................................................... 120
References ........................................................................................ 122

CHAPTER 6

A COMPARISON OF RISK FACTORS FOR EXPOSURE TO M.

TUBERCULOSIS AND M. BOVIS IN NORTHERN MICHIGAN ......................... 124
Abstract ........................................................................................... 124
Introduction ....................................................................................... 125
Methods ........................................................................................... 127
Results ............................................................................................. 128
Discussion ........................................................................................ 131
Conclusion ....................................................................................... 135
References ........................................................................................ 136

viii

CONCLUSION ...................................................................................... 138

APPENDICES ...................................................................................... 144
Appendix A : Deer Hunter Health Survey .................................................................... 145
Appendix B : Injury Survey Tools ............................................................. 148

LIST OF TABLES

Table 2.1 : Summary of the public health content of newspaper articles containing
keywords “Bovine TB” collected by Michigan Press Reading Service, 1998-2000 ....... 39

Table 2.2 : Michigan Hunter Health Survey responses, total and per strata ................. 44

Table 2.3 : Characteristics of hunters associated with their likelihood of wearing
gloves while field dressing during the 2000 hunting season ............................................. 50

Table 2.4 : Characteristics of hunters associated with their likelihood of reporting
consuming venison from the 2001 hunting season as always cooked thoroughly ......... 51

Table 3.1 : Non-epidemiologically linked human M. bovis spoligotyping and MIRU

typing results, Michigan, USA ..................................................................... 64

Table 3.2 : Epidemiologically linked M. bovis spoligotyping and MIRU typing

results, Michigan, USA ............................................................................. 67

Table 4.1 : Summarized characteristics of study participants by species .......................... 86
Table 5.1 : Cause of injury while TB testing livestock ....................................... 104

Table 5.2 : Factors contributing to risk of injury while TB testing livestock in
Michigan, 2001 .................................................................................... 105

Table 5.3 : Characteristics of Study Population — Michigan veterinarians testing
five or more livestock herds for TB in 2001 .................................................... 107

Table 5.4 : Veterinary characteristics and associated rate ratios of risk of injury per
animal tested (incidence density) by veterinarians TB testing livestock in Michigan,
2001 ................................................................................................... 111

Table 5.5 : Bivariate analysis of risk factors found to be significant in the incidence
density analysis .................................................................................... 114

Table 6.1 : The time period of participation and number of completed TST records
received fiom each local healthjurisdiction.......................................................129

Table 6.2 : Chi-square analysis comparing positive and negative tuberculosis skin test
results by M. bovis and M. tuberculosis risk factors. ......................................... 130

LIST OF FIGURES

Figure 2.1 : Location of Stratum 1 counties (indicated by the “1”) and

Stratum 2 counties (indicated by the “2”) within the state of Michigan.

The shading counties within the enlarged area indicate counties in which

Bovine TB positive deer had been found, at the time of the survey ......................... 42

Figure 2.2 : Map of Michigan showing geographic areas of residence and
the number of survey respondents residing in each area ....................................... 48

Figure 3.1 : Photo of the chest cavity of the deer shot by Case 2, retrieved
after being buried for 9 weeks, displaying the classical nodular lesions of

M. bovis infection in deer .......................................................................... 73

Figure 4.1 : Flow diagram to show how participating farms were selected ................. 86

xi

INTRODUCTION
SETTING

Mycobacterium bovis (bovine TB) is an organism of great historical importance in
the United States. Due to its high prevalence in the nation’s cattle population, and the
transmission of the organism to humans via milk, it was a fairly common human
pathogen from its first recognition as a disease causing agent in 1882 (Koch, 1882) until
the 1920’s when it was a major impetus for the milk pasteurization laws. Afier
pasteurization of milk became commonplace, the human disease burden due to M. bovis
infection was substantially reduced (Grange, 1994). However, control of the disease in
cattle proved more difficult, and the prevalence in cattle remaining high until 1918, when
the Animal Industries Board (the precursor to United States Department of Agriculture)
initiated a national eradication campaign (Frey, 1995). Michigan gained (Bovine)
Tuberculosis Free status in 1979. M. bovis, in both cattle and humans, remained
quiescent for 20 years (Free ranging white-tailed deer, website).

In 1994, a white-tailed deer in Alpena County, Michigan was killed by a
physician who noticed tan nodules in the chest cavity. Suspecting, tuberculosis, the
animal was presented for testing (Free ranging white-tailed deer, website); M. bovis was
diagnosed. Animals from two captive cervidae herds within the immediate area of the
positive deer were tested, but no additional infected cervidae were found. In spring 1995,
all livestock (70 herds) within a 5 mile radius of the positive deer were tested, but no
infected herds were found. In 1995, 18 deer (of 403 tested) were found to be infected
with M. bovis; in 1996, 56 positive deer were found (of 4966 tested); in 1997, 73 positive

deer were found (of 3720 tested). In 1998, an Alpena County beef herd was found to be

infected. By the end of 1998, two more cattle herds were found to be infected, both in
neighboring Alcona County, Michigan (Summary of gross and histologic examination,
website).

In October of 2001, Senate Bill 1339 required the testing of all dairy herds and
other herds in the ‘high risk” areas to be completed within 12 months, and testing of all
cattle in non-high risk areas to be completed within three years. To meet the immediate
and large-scale demands for TB testing livestock, a cadre of private veterinarians was
recruited to conduct TB-herd testing and a high number of injuries to veterinarians were
anecdotally being reported to regulatory officials. Surveillance for M. bovis in the deer
population was primarily based on visual inspection, by Michigan Department of Natural
Resources check station personnel, of hunter-killed deer, and was geographically focused
in the counties in the northeast portion of the lower peninsula of Michigan.

By October, 2007, a total of 42 Michigan cattle herds have been diagnosed with
Bovine TB. Michigan lost its Federal TB Free Accreditation Status in 2000. Five
hundred and sixty-eight deer have been have been found infected (out of 153,740 tested)
and the disease now maintains itself in the wild deer population and is considered
endemic in the northeastern portion of the lower peninsula of Michigan.

In addition to deer and cattle, numerous other species have been found positive
for bovine TB, including; coyotes, raccoons, black bear, bobcat, red fox and opossum.
(Summary of Michigan wildlife bovine tuberculosis surveillance, website). These
species are believed to be “dead-end”, or spill-over hosts and not contributory to the
maintenance of the disease (Bruning-Fann, 2001). However, disease in these species

leads to the potential exposure to the organism by trappers and taxiderrnists.

Efforts to control the disease in the deer population have led to feeding and
baiting bans in affected counties. These bans, designed to reduce the congregation of
deer, have led to a decreased number of hunters frequenting these areas which in turn has
resulted in a substantial loss of income to hunting-related industries (deer crops, hotels,
restaurants, etc.). In addition, the testing requirements and loss of trade revenue has
placed a considerable burden on Michigan’s cattle and dairy industries.

Including 2007, the total amount of resources dedicated to control the disease in
Michigan now exceeds $90 million with the state government contributing $70 million,
and the federal government contributing $23 million, over the previous 12-13 years. The
majority of frmding was dedicated to the control of disease in cattle (M. Ankney, Bovine

TB Program Coordinator, personal communication, Nov 9, 2007).

PURPOSE STATEMENT

Since the discovery of M. bovis in Michigan’s cattle and flee-ranging white-tailed
deer, much attention, research and funding has focused on M. bovis control and
surveillance efforts, prevalence estimation, testing and diagnostic methodology.
Relatively little attention has focused on the role of M. bovis as a zoonotic disease. The
purpose of this dissertation is to explore the human health effects of the bovine TB
outbreak on Michigan residents, and includes both zoonotic and non-zoonotic affects on
the public’s health.

That Mycobacterium bovis is a zoonotic agent is not in question, nor is the
susceptibility of all warm-blooded animals to infection (de Lisle 2001; 2002). However,

the role of M. bovis as a zoonotic agent in the current outbreak setting, and the actual risk

of transmission to humans, has not been established. Historically, exposure to M. bovis
in the US. was via the gastrointestinal route (consumption of raw milk), via the
inhalation of aerosols from cattle with pulmonary infection, or by the cutaneous route
(prosectors and butchers) following exposure to infected carcasses. With M. bovis
infection endemic in the white-tailed deer population in Northeast Michigan, new routes
of exposure required assessment. With the re-emergence of bovine TB in cattle,
traditional or historical routes of exposure need to be re-visited and the lingering question
about the potential role of pets as reservoirs of infection for cattle or humans necessitated
examination in the current Michigan setting. In addition, exploring the rate of
veterinarian injury and the risk factors contributing to injuries will offer insight into the
“human costs” of large scale animal disease control efforts. Below, the research
questions and a short summary of findings are presented for each of the five projects

included in the dissertation.

Research questions and summary of findings

Project 1 - Mycobacterium bovis (bovine TB) exposure as a recreational risk for
hunters: results of the Michigan hunter survey - 2001.

Because M. bovis (bovine TB) is endemic in the white-tailed deer population of
northeastern Michigan, hunters may be exposed to M .bovis via cutaneous inoculation
while field dressing deer or by ingestion of undercooked venison. Michigan hunters have
heretofore received inconsistent messages about their risk of acquiring tuberculosis from

recreational exposure to deer. The most common health advice offered has been to wear

gloves while field dressing deer and to thoroughly cook venison meat products. The
objective of this study is to collect data to quantify the usage of these self-protective
activities and to characterize hunters practicing these activities. This data was collected
by surveying 1,833 hunters who had successfully harvested deer in or near Michigan’s
Bovine TB endemic area in 2000. The survey participation rate was 78%. Most hunters
(89%) reported field dressing deer, 43% of whom wore gloves. Most hunters (95%)
reported eating venison; 55% of whom reported their venison was always cooked
thoroughly. Several hunter characteristics including older age, female gender, higher
awareness level, and area of residence, were significantly associated with the practice of
these self-protective activities. The survey results suggest that hunters should receive
consistent advice encouraging the use of gloves while field dressing deer and the

thorough cooking of venison products before consumption.

Project 2 - Human Mycobacterium bovis infection associated with the Bovine TB
outbreak in Michigan, 1994 — 2007.

In the period between 1994 and October of 2007, M. bovis was found in 42 cattle
herds and 568 wild deer in Michigan. Based on genotyping analyses, the strain of M.
bovis circulating in Michigan’s deer and cattle remained genetically stable over this
duration. Although M. bovis is a zoonotic pathogen, this outbreak strain was not detected
in a human until 2002, with the occurrence of a human pulmonary isolate. In 2004,
cutaneous disease caused by M. bovis was documented in a hunter. This report
summarizes the epidemiologic and molecular investigation of these two human cases

who shared the deer/cattle outbreak strain of M. bovis. The results of this investigation

confirm recreational exposure to infected deer in Michigan as a potential, albeit low, risk

for acquisition of M. bovis infection in humans.

Project 3 - Absence of Mycobacterium bovis infection in dogs and cats residing on
infected cattle farms — Michigan, 2002.

A cross-sectional field study was performed to evaluate dogs and cats living on
farms with M. bovis (bovine TB) infected cattle. Our purpose was to determine pet
infection status and assess their risk to farm families and/or tuberculosis-free livestock.
Nine farms participated in the study. Data and specimens were collected from eighteen
cats and five dogs fiom nine farms. ELISA testing for M. bovis and M. avium was
conducted. Fifty-one biological samples were cultured; all were negative for M. bovis,
although other Mycobacterium species were recovered. No radiographic, serologic or
skin test evidence of mycobacterial infection was found. These negative results may be
due to the low level of bovine TB infection in the cattle and the infrequent exposure of
pets to cattle residing on the same farm. We found no evidence that pets residing on
bovine TB-infected Michigan cattle farms pose a risk to humans or bovine TB-free

livestock, however precautionary advice was provided.

Project 4 — Veterinarian injuries associated with Bovine TB testing livestock in
Michigan, 2001.

Determining the injury rate for working with cattle is difficult since a wide range
of persons perform a diverse assortment of procedures on cattle in highly variable

circumstances. There is also generally a lack of denominator data regarding the number

of cattle receiving each type of procedure. Testing all the cattle in an entire state with a
uniform procedure for each animal afforded an opportunity to relate human injury data to
a known number of animals handled while carrying out a standardized procedure. The
objective of this study was to capture the type and incidence density of injuries associated
with TB—testing a large number of cattle, bison and goatherds, and to delineate the
various factors contributing to the risk of injury. Additionally, two known mortality
events associated with bovine TB testing in Michigan are summarized. A survey was
mailed to all veterinarians (N=259) who had completed at least five official bovine TB
herd tests in Michigan in 2001. Collected data regarded basic demographics and health
status, work experience, veterinary specialty, and practice information. Veterinarians
were requested to complete a separate injury questionnaire for each injury received while
TB testing livestock in 2001. Risk ratios were calculated, based on the incidence density
of injuries per 10,000 animals tested, to compare the characteristics of the injured
veterinarians to the non-inj ured veterinarians. Accurate addresses were found for 247
eligible veterinarians, 175 of whom returned the survey for a participation rate of 71%
(175/247). Thirty-five veterinarians reported a total of 53 injuries (10 major, 12 minor
and 31 self-treated). Individual veterinary characteristics and the type, cause and location
of each injury are described. The overall incidence density of injuries was 1.9 per 10,000
animals tested. Female gender (RR=3.26), having less than 10 years of practice
(RR=1.81), being employed by the government (RR=4.54), smoking (RR=5.97) and
working 50 hours or less (RR=1.87) were found to be significantly associated with a
higher rate of injury per 10,000 animals tested. The human “costs” in terms of injuries,

must be considered when decisions are made to initiate large-scale livestock disease

control programs, although these costs are more difficult to measure than the financial
costs of a budgeted control program. Effort and resources must be allocated to reduce the
number and frequency of preventable injuries, and to monitor the public health impact of

ongoing disease control efforts.

Project 5 - A comparison of risk factors for exposure to Mycobacterium tuberculosis
and Mycobacterium bovis in northern Michigan.

First recognized in white-tailed deer in 1994, Mycobacterium bovis has since been
found in several cattle herds and is now considered endemic in the deer population of the
northeastern part of the lower peninsula of Michigan. Numerous additional species are
also infected, such as coyotes, raccoons, black bear, red fox, bobcats and opossum.
Because of the occurrence in wildlife and re-occurrence in cattle, persons in the affected
area deemed to be at an elevated risk of exposure include: hunters, trappers, taxiderrnists,
venison processors, beef or dairy producers and farm/ livestock workers. The health
departments covering 12 counties in the northeastern part of the lower peninsula of
Michigan participated in this study. A survey was administered which included a list of
M. bovis-specific exposure risk factors and a list of M. tuberculosis-specific exposure risk
factors. Each health department was asked to complete and attach the survey to each
tuberculosis skin test (TST) reporting form, and send the de-identified form to the
Michigan Department of Community Health. To measure the associations between each
risk factor and TST results, either a relative risk with 95% confidence intervals was used,
or the Fisher’s exact test when cell size was 5 5, as appropriate. Overall, there were 29

positive TST reactors, out of 1268 TST records submitted for a positivity rate of 2.29%

(29/1268). Being a venison processor was associated with a positive TST reaction
(p=0.047) and well as being foreign born (p=0.019). This finding suggests that venison
processors may benefit from targeted public health prevention messages to reduce

likelihood of exposure to M. bovis.

IMPORTANCE OF FINDINGS

The finding of this dissertation indicates that there are sub-populations of people
that may be at an elevated risk for infection with the outbreak strain of M. bovis in
Michigan. Additionally, personnel involved in the massive cattle testing programs are at
risk of physical injuries associated with TB testing livestock. These five projects are
independent fi'om each other, but each addresses a different aspect of the overall

question, “What are the human health effects of the bovine TB outbreak in Michigan?”

REFERENCES

Bruning-F arm CS, Schmitt SM, Fitzgerald SD, Fierke J S, Frieidrich PD, Kaneene JB,
Clarke KA, Butler KL, Payeur JB, Whipple DL, Cooley TM, Miller JM, Muzo

DP. Bovine tuberculosis in free-ranging carnivores from Michigan. J Wildl Dis.
2001;37:58-64.

deLisle GW, Mackintosh CG, Bengis RG. Mycobacterium bovis in free-living and
captive wildlife, including farmed deer. Rev Sci Tech Off Int Epizoot.
2001;20:86-111.

deLisle GW, Bengis RG, Schmidtt SM, O’Brien DJ. Tuberculosis in free-ranging

wildlife: detection, diagnosis, and management. Rev Sci Tech Off Int Epizoot.
2002;21:317-334.

F rec-ranging white-tailed deer. [homepage on the Internet] State of Michigan, Emerging
Disease Issues in Michigan (MI, USA). c2001 [cited 2007 Nov 6]. Available

from: hgpz/lwwwmichigan.gov/emergingdiseases/O,l607,7-186-25804 25811-
75803--,00.html.

Frey GH. Bovine tuberculosis eradication: the program in the United States. In: Thoen C,
Steele J, editors. Mycobacterium bovis infection in Animals and Humans, Ames:
Iowa State University Press; 1995. p. 119-129.

Grange JM, Yates MD. Zoonotic aspects of Mycobacterium bovis infection. Vet
Microbiol. 1994;40:137-151.

Koch R. Uber Tuberkulose. Berl Klin Wochenschr 1882;19:221-23 8.

Summary of Michigan wildlife bovine tuberculosis surveillance. [database on the
Internet] State of Michigan, Emerging Disease Issues in Michigan (MI, USA).
c2001 [updated 24 Apr 2007; cited 2007 Nov 6]. Available from:
http://www.michigan.gov/documents/emergingdiseasg/WildlifeTBSurveillanceS
ummarv_211947 7.pdf.

Summary of gross and histologic examination and mycobacterial culture of tuberculosis
cases in cattle and captive deer in Michigan 1996 - 2007. [database on the
Internet] State of Michigan, Emerging Disease Issues in Michigan (MI, USA).
c2001 [cited 2007 Nov 6]. Available from:
http ://www.michigan. gov/documents/emergingdiseases/TBposTable_2-

07 FOR_THE WEB_167511 7 187838 7.doc.

10

CHAPTER 1
LITERATURE REVIEW

Because the topic area of “Mycobacterium bovis ” is so expansive, with a history
dating back to the domestication of cattle (4000-8000 BC), and a host range that includes
all warm-blooded animals, it is necessary to clearly delineate what will be covered, and
more importantly, what will not be covered in this literature review. Topics to be
covered include a brief history of the organism and a history of the disease status in cattle
and wildlife leading to a description of the setting in which the current Michigan outbreak
is occurring. Hmnan infection with M. bovis will be described in terms of clinical
manifestations (pulmonary, alimentary, and cutaneous), pathogenesis, latency, immune
response and detection using the tuberculosis skin test. Routes of exposure for humans,
as well as populations at risk of exposure will be covered. The role of dogs and cats in the
transmission of M. bovis and a summary of injuries associated with large animal
veterinary work will be covered as well. Topics that are outside the scope of this
dissertation, and therefore will not be covered by this literature review, include: vaccine
development in humans or animals, diagnostic techniques in humans (other than TST)
and animals, the microbiological or molecular characteristics of M. bovis, the role of co-
infection with HIV, and the animal disease control efforts in livestock or wildlife

populations.

MICHIGAN OUTBREAK SETTING - OUTBREAK HISTORY IN DEER, CATTLE,
AND OTHER SPECIES

ll

Although an association between a wasting disease in cattle and consumption in
humans had been suspected for many centuries, it was Robert Koch, who in 1882,
discovered the tubercle bacillus (Koch, 1882). Koch first believed that bovine and
human tuberculosis were caused by the same organism and named cattle as a source of
infection for humans. Koch later changed his opinion following research by Smith
(Smith, 1898) showing small but constant differences between bacilli of human and
bovine origin. Koch considered humans to be immune or only very slightly susceptible
to tuberculosis of bovine origin, and that control measures (in cattle) were unnecessary
(British Congress on Tuberculosis, 1901). Several groups of researchers were skeptical
of this conclusion and began a period of intensive research lasting form 1901 to 1911.
The most notable of these research groups was the British Royal Commission on
Tuberculosis which clearly established the risk of bovine tuberculosis to human health
and confirmed that milk was the principle route of exposure to humans (Frances, 1959).
The history of M. bovis is well summarized by Grange and Yates (1994), and Grange
(1995)

It was in 1917 that the United States Board of Animal Industries, officially began
the effort to eradicate tuberculosis in cattle. The disease was causing more losses than all
other livestock diseases combined. In humans, tuberculosis was also the number one
cause of incapacity and death, with many of these cases due to drinking raw milk from
tuberculous cows (Frey, 1995). In the first year of the program, 4.9% of the cattle were
reactors to the tuberculin skin test; in 1930 the percentage had dropped to 1.8%, and in
1940 to 0.5% (Frey, 1995). From 1959 to 1987, the reactor rate dropped from 0.2 to

0.01% (USDA, 1990). In the 1990’s, on the verge of eradicating the disease at the

12

national level, several new herds were detected in a handful of states (Frey, 1995). An
assessment was completed in which several new factors contributing to the persistence of
M. bovis in the cattle population were identified including: reliance on testing and
slaughter surveillance, the enzootic milkshed region of El Paso, TX, importation of
infected steers from Mexico, the finding of M. bovis in exotic hoofstock in zoos,
garneparks, auctions and other facilities and the presence of disease in camelidae (Bleem,
1993)

In 1994, in Alpena County, Michigan, a white-tailed deer (Odocoileus
virginianus) was killed. The hunter, who noticed tan nodules in the chest cavity,
suspected tuberculosis, and presented the carcass for testing; M. bovis was diagnosed
(Payeur, 2002). Animals from two captive cervidae herds within the immediate area of
the positive deer were tested, but no additional infected cervidae were found. In the
spring of 1995, all livestock (70 herds) within a 5 mile radius of the positive deer were
tested, but no infected herds were found. In 1995, 18 deer (of 403 tested) were found to
be infected with M. bovis; in 1996, 56 positive deer were found (of 4966 tested); in 1997,
73 positive deer were found (of 3720 tested). In 1998, an Alpena County beef herd was
found to be infected. By the end of 1998, two more cattle herds were found to be
infected, both in Alcona County, Michigan (Free ranging white-tailed deer, website).

Twenty years after obtaining the bovine TB Accredited-free status from the US
Department of Agriculture in 1979, Michigan lost that designation to become a Non-
Modified Accredited state on June 22, 2000, joining Texas as the only other US state that

did not have a Free status for bovine TB.

13

As of October, 2007, a total of 42 Michigan cattle herds were diagnosed with
bovine TB. Five hundred sixty-eight deer were found infected (out of 153,740 tested)
and the disease now maintains itself in the wild deer population and is considered
endemic in the northeastern portion of the lower peninsula of Michigan. The disease
pathology and transmission in deer in has been well described by Towar (1965) and more
recently by Schmitt (1997), Palmer (1999; 2000), and O’Brien (2001). The epidemiology
of the current outbreak in Michigan deer has likewise been well described (Schmitt,
1997; 2002; O’Brien, 2002).

In addition to deer and cattle, numerous other species have been found positive
including: coyotes, raccoons, blackbear, bobcat, red fox and opossum (Summary of
Michigan wildlife bovine tuberculosis surveillance, website). These species are felt to be
incidental, or spill-over hosts and not significant in the maintenance of the disease in the
wild (Bruning-Fann, 1998, 2001a).

A large amount of information can be found on the Emerging Infectious Disease
website {http://wwwmichigan.gov/emergingdiseases), under the heading of Bovine
Tuberculosis. Two chronologies are posted: “A Chronology of bovine TB in Michigan
since 1975”, and “History of Legislation and Regulation for bovine TB eradication in
Michigan’s wildlife”. In addition, two databases are maintained with current information
about new cases of bovine TB in both cattle and wildlife: “Summary for Michigan
Wildlife Bovine Tuberculosis Surveillance” and “Summary of gross and histologic
examination and mycobacterial culture of tuberculosis cases in cattle and captive deer in

Michigan 1996 — 2007”.

14

HUMAN INFECTION WITH M. BOVIS

General characteristics of M. bovis as an organism

Mycobacteriae are aerobic, non-spore forming, nonmotile, slightly curved or
straight rods. They have thick cell walls containing mycolic acids with free lipids making
them acid-fast stainers (gram positive) (Pfyffer, 2003). All Mycobacterium are able to
survive for weeks to months on inanimate objects if protected from sunlight, but are
easily killed by UV light and heat. They are more resistant to acids, alkalis, and some
chemical disinfectants than are most other non-spore-forming bacteria (Pfyffer, 2003).
M. bovis is a member of the M. tuberculosis complex, a complex related by a >99.9%
DNA-DNA homology (Gordon, 2001) sharing the characteristic of being human
pathogens, some more significant than others. They are all obligate pathogens with their

major ecological niche being the tissues of warm-blooded animals (Pfyffer, 2003).

Immune response

Even after over a century of study, very little is known about the virulence factors
of M. tuberculosis and M. bovis or how the protective immune response is triggered
within the infected host (Collins, 1994). Initial response to infection is by the unactivated
macrophage, in which the organism replicates without restriction until the macrophage
bursts. Lymphocytes, specifically sensitized T lymphocytes, cause the release of gamma
interferon. The liberation of gamma interferon causes the activation of the macrophages

(Todar, 2007). The immunologically activated macrophage induces a bacteriostasis,

15

which is usually sufficient to protect the host, but will not entirely eliminate the infection,
so that reactivation can occur whenever the cellular defenses are depleted (Collins, 1994).
Acquired immunity following mycobacterial infection usually develops within 4-6 weeks
and is associated temporally with the onset of delayed hypersensitivity to mycobacterial
antigens such as purified protein derivative (PPD). Acquired resistance is mediated by T
lymphocytes. Antimycobacterial antibodies, though present in many patients, do not play
a protective role in tuberculosis because infection with mycobacteria is intracellular, and
if extracellular, it is resistant to complement killing due to the high lipid concentration in

its cell wall (Todar, 2007; McMurry, 2007).

Tuberculosis skin test (TST)

The most common way to measure the prevalence of latent tuberculosis in a
population or an individual, is the use of a tuberculosis skin test (TST), most commonly
the Mantoux test. The Mantoux technique consists of an intradermal injection of 0.1 ml
of tuberculin purified protein derivative (PPD) (also known as 5 tuberculin units).
Interpretation of the Mantoux TST is based on the size (in mm) of induration measured at
48-72 hours post intradermal injection. The PPD reaction is based on the delayed-type
hypersensitivity reaction of a patient previously infected with mycobacteria, with the
positive reaction correlated histologically to the presence of mononuclear cells at the site
of injection (Huebner, 1993). Classification of the TST reaction is based on
epidemiological data, categories of potential risk factors for exposure to M. tuberculosis,
with cut-off points for positive reactions of 5mm, 10 mm or 15 mm, depending on the

risk factors of exposure. For a person with no known risk factors for exposure to

16

tuberculosis, an induration of greater than 15 mm would be required to have their
reaction classified as positive (CDC, 2005a). A TST will induce a positive reaction to
infection with M. tuberculosis or mycobacteriae other than tuberculosis (MOTT)
(including M bovis), although generally speaking, a tuberculin reaction caused by
infection with MOTT tends to be smaller than those elicited by infection with M.

tuberculosis (Dasco, 1990).

There is variability in the administration of the test, interpretation of the test and
among individual immune reactions to the test. There is little agreement on the
sensitivity and specificity of the procedure, multiple factors (both host and administrator)
lead to problems with false positive and false negative reactions (Huebner, 1993), and the
TST does not differentiate between infection with M. tuberculosis and M. bovis (Dasco,
1990). However, despite the variability and caveats associated with Mantoux testing, the
PPD has enormous clinical utility to detect latent tuberculosis infection in populations

considered to be at high risk for exposure and infection (Dasco, 1990).

The interpretation of the TST is based strictly on exposure to, and infection with,
M. tuberculosis. Infection with M. bovis would be expected to elicit a smaller reaction
than one caused by infection with M. tuberculosis because PPD is a mixture of antigens
derived from M. tuberculosis (Dasco, 1990). Individuals with M. bovis exposure risk
factors would only be considered positive if their TST induration were 15 mm or greater,
thus many latent cases of M. bovis infection may be missed using the current TST

interpretation guidelines (CDC, 2005b).

Pathogenesis and clinical manifestations in humans

17

The pathogenesis of mycobacteria depends on the site of infection. In pulmonary
tuberculosis, tuberculous mycobacteria enter the alveoli by airborne transmission of
droplet nuclei containing viable, virulent organisms. A portion of the infectious
innoculum resists destruction by the alveolar macrophages and persists, eventually
multiplying and killing the macrophage (McMurray, 2007). The accumulating
mycobacteria stimulate an inflammatory focus which matures into a granulomatous
lesion characterized by a mononuclear cell infiltrate surrounding a core of degenerating
epithelioid and multinucleated giant (Langhans) cells, eventually forming the primary
lesion or tubercle. The tubercle may become enveloped by fibroblasts and its center
often progresses to caseous necrosis. Liquification of the caseous material and erosion of
the tubercle into an airway may result in cavitation and the release of massive numbers of
bacilli into the sputum. In a resistant host, the tubercle eventually becomes calcified and
the infection latent (McMurray, 2007).

Early in infection, mycobacteria may be spread directly into circulation by erosion
of the tubercle into a pulmonary vessel, or indirectly through the lymphatics to the hilar
or mediastinal lymph nodes, and then via the thoracic duct, into the circulation. Erosion
of the arterial blood vessels resulting in the escape of blood into the air passages and the
coughing of sputum stained with bright red arterial blood (hemoptysis) is a common
feature of advanced, post-primary pulmonary disease in humans (O’Reilly, 1995). Other
organs may become seeded via the extrapulmonary hematogenous dissemination of the

organism (McMurray, 2007).

18

When exposure is by ingestion, the pathogenesis is similar, with the principle site
of involvement being the mesenteric lymph nodes with subsequent dissemination.
Tonsils may also be the port of entry for infection (Kakekhel, 1989). This alimentary
route of infection leads to extra-puhnonary forms of tuberculosis, where infection can
become established in the cervix, and less fi'equently in the axillary lymph nodes leading
to chronic skin tuberculosis (Moda, 1996). In countries where tuberculosis in cattle is
common, cervical lymphadenitis is the predominant clinical presentation in children
while pulmonary tuberculosis, and to a lesser degree, extrapulrnonary forms, are found in
adults (O’Reilly, 1995). In Canada, prior to the national bovine TB eradication
campaign, M. bovis accounted for 50 to 70% of cervical and 80% of abdominal
tuberculosis. Mortality rates were estimated to be between 10 and 30% primarily
attributed to secondary hematogenous spread (Panesar, 2002). In San Diego, California,
USA, Danker, (1993) reviewed 25 pediatric cases of M. bovis occurring from 1979 to
1992; 44% presented with cervical adenitis, 28% had abdominal manifestations and only
12% had puhnonary symptoms.

The last presentation of tuberculosis to be discussed is cutaneous. Cuntaneous
tuberculosis takes several different forms and clinical manifestations comprise a
considerable number of skin changes. Tappeiner and Wolfe (1993) use a classification
that distinguishes between exogenous infection and endogenous spread of M.
tuberculosis/bovis. Once in the host’s tissues, the mycobacteria multiply intracellularly
and the infection is characterized by the appearance of polymorphonuclear leukocytes,
and influx of mononuclear cells, and by the later development of epithelioid cells and

necrosis. The development of a certain type of skin tuberculosis depends on the

19

causative organism, the general condition and reactivity of the host, and the mode of
introduction of the bacteria into the skin. Cutaneous M. bovis and M. tuberculosis
manifestations are identical (Tappeiner, 1993). Exogenous infection can be classified as
primary inoculation tuberculosis (or tuberculous chancre), which is infection of the
nonimmune host, and tuberculosis verrucosa cutis (or warty tuberculosis), which is
infection of the immune host. Endogenous spread of existing infection can be classified
as lupus vulgaris, scrofuloderma, metastatic tuberculosis abscess, acute military
tuberculosis or orificial tuberculosis. Each form is well described by Tappeiner (1993).

Primary inoculation tuberculosis results from inoculation of mycobacteria into the
skin or less fi'equently into the mucosa. Some form of injury is mandatory as tubercle
bacillus cannot penetrate the normal intact skin barrier (Sehgal, 1990). Tuberculosis of
exogenous source is the most likely manifestation for persons who are exposed to
carcasses of M. bovis infected animals (farmers, butchers and knackers), with inoculation
through wounds or existing abrasions. Clinically, a papule develops into a ragged,
painless ulcer which may be accompanied by regional lymphadenopathy (Kakakhel,
1989). Lesions usually heal but may progress to lupus vulgaris, scrofuloderrna or rarely,
to military tuberculosis (Miller, 1955). In sensitized individuals, tuberculosis verrucosa
cutis (warty tuberculosis) starts as small, solitary, firm, syrnptomless reddish-brown or
purple indurated warty papule with an inflammatory halo. The papule gradually extends
to become a plaque that eventually results in atrophic scars. Regional lymphadenitis is
rare (Kakakhel, 1989).

Reactivation of old primary foci of infection with consequent clinical disease may

be triggered by immunodepression resulting from old age, co-morbidities, poor nutrition

20

and stressful life events (Tinker, 1959; Sauret, 1992). The most common sites of
secondary extra pulmonary involvement include the genitourinary tract, bones and joints,
and the central nervous system, and in adults often represent a reactivation of the disease
at the primary site(s) of childhood exposure (Gobels, 2000).

Before efforts to control M. bovis in cattle were initiated, contaminated milk was
the principle vector for the transmission of the disease to humans and the majority of the
lesions were extrapulmonary (Grange, 1995). Human pulmonary cases were considered
rare and were more prevalent in rural vs. urban areas (due to aerosol exposure to infected
cattle). After elimination of contaminated milk as a vector, the distribution of the
anatomical sites of disease changed considerably with the lung becoming the
predominant site, genitourinary disease becoming more prevalent, while lupus vulgaris
became rare (Grange, 1995). In the 1960’s with the control of the disease in the cattle
population of developed countries, the extra pulmonary presentations (due to reactivation
of latent infection) again became predominant and remain so today.

There are conflicting opinions in the literature regarding the severity of human
infection with M. bovis. Hedvall (1942) is often cited for claiming that in humans, cases
of pulmonary disease due to M. bovis and M. tuberculosis are indistinguishable,
clinically, radiologically, and pathologically. However, more recent work suggests the
pathogenicity of M. bovis may be less than that of M. tuberculosis (Enarson, 1995). Work
in both Denmark (Magnus, 1966a, 1966b, 1966c) and Sweden (Sjogren, 1974) suggests
that the relative risk of developing active tuberculosis, following infection with M. bovis,

was less than that following infection with M. tuberculosis.

21

Human exposure to M. bovis and populations at risk of infection

Humans can be exposed to M. bovis from infected domesticated livestock.
Although found in a wide range of wild and domesticated mammals (deLisle 2001; 2002)
cattle remain the primary reservoir species for M. bovis and thus the main source of
human infection. Of the domesticated animals, cattle, farmed buffalo and goats are
considered reservoir hosts of M. bovis, while pigs, cats, dogs, horses and sheep are
considered spillover, or “dead end” hosts. Infection of humans from cattle can occur via
inhalation of aerosols, direct contact with the animal (Baldwin, 1967), indirectly in an
abattoir setting (Robinson, 1988; Georghiou, 1989; Cousins, 1999), through the
consumption of infected milk or dairy products (Robert, 1999; O’Reilly, 1995; CDC
2005c), or by handling infected carcasses (Tappiener, 1993). A case of tuberculous
chancre in a 14 year old, subsequent to being gored by a bull, was described by Ara
(2000)

Scientific literature describing the role of domestic pets in the transmission of M.
bovis on the farm (livestock to pet, pet to livestock) is fairly limited and quite dated.
While uncommon in both dogs and cats, historic data suggests that dogs were more likely
to be infected with M. tuberculosis following exposure to infected humans, while cats
were more likely infected with M. bovis with exposure assumed to be related to the
consumption of contaminated animal products (Bim, 1965). Historically, farm cats and
dogs were at very high risk of acquiring M. bovis from infected cattle; 4 of 9 dogs and 24
of 52 cats were affected after exposure to positive cattle in a Pennsylvania study (Snider,

1971a). It is therefore feasible that pets could play a role in the maintenance of M bovis

22

on a farm (Greene, 1998), however, literature describing pet transmission to cattle is
hypothetical (McLaughlin, 1974) or limited to references from eastern Europe in the
1950’s and 60’s (Schliesser, 1957; Beinhauer, 1958; Milbrant, 1960; Pavlas, 1965).

Literature describing the role of pets in transmission of M. bovis to humans is also
very limited, although transmission would again be biologically plausible. Early
necropsy studies (1930-1965) revealed a tuberculosis prevalence ranging from 2.0 to 13%
in cats and 0.4% to 2.0% in dogs (Snider, 1971b). There is no evidence that dogs and cats
have transmitted M. bovis infection to humans; only one inconclusive cat-to-human
reference was found (Isaac, 1983).

In Michigan, wild carnivores and omnivores are considered dead-end hosts for M.
bovis. These animals are most typically exposed to infection via the consumption of
infected deer carcasses, thus resulting in a gastrointestinal clinical presentation with
limited potential for transmission to people or other animals (Bruning-Fann, 1998; 2001).
Humans have been infected by handling ill elk and infected elk carcasses in Canada
(Farming, 1991; Nation, 1999). In the US, one case is reported describing a hunter
infecting himself with a contaminated hunting knife while field dressing infected deer in
Michigan (Wilkins, 2008). In two zoos, humans have been infected by inhaling aerosols
generated while cleaning the pens of an M. bovis infected rhinoceroses (Dalovisio,1992;
Stetter, 1995). Seals have also been blamed for the aerosol transmission of M bovis to
human trainers (Thompson, 1993).

Until recently, human-to-human transmission was considered almost irrelevant
due to the preponderance of extrapulmonary infection with only anecdotal reports in the

literature (Griffith, 1937; Ruys, 1939; Hedvall, 1942; Sigurdsson, 1945; Wigel, 1972) and

23

lack of molecular subtyping techniques has made proof of such transmission difficult
(Grange, 1994). Nosocomial outbreaks of M bovis infection among HIV infected
patients, in Madrid, Spain from 1993-1998 are well described by Guerrero (1997),
Samper (1997) and Rivero (2001). The disease was spread via aerosol transmission.
More recently, a family cluster of M bovis cases in San Diego Califomia, was identified
that suggested human-to-human transmission (LoBue, 2004). In 2007, a cluster of six
cases of M bovis was identified in young adults in the United Kingdom, only one of
whom had zoonotic links to cattle or had consumed unpasteurized dairy products. One
patient died, and four had risk factors predisposing them to tuberculosis disease. This was
the first time in decades that human-to human transmission was documented in the
United Kingdom (Evans, 2007).

Although M bovis can survive for long periods outside an animal host, there are

no records of human infection by M bovis coming from a direct environmental source

(Biet, 2005).

Populations at risk of exposure

Various persons are considered at risk of exposure to and infection with M bovis
based on their occupation. Workers in the livestock industry, abattoir or rendering plant
workers, veterinarians and animal handlers are at greatest risk of infection with M bovis
(Collins, 1983; Liss, 1994; McKenna, 1996; Cousins, 1999) primarily via aerosol

transmission. In the past, primary inoculation tuberculosis caused by M bovis was known

24

as “butcher’s wart” and was considered an occupational disease of butchers, farmers and
knackers (handlers of poor quality or deceased livestock) (Tappiener, 1993).

M bovis has recently become established and endemic in the white-tailed deer
population in the northeastern portion of the lower peninsula of Michigan, with the
subsequent spill over into additional wildlife species. The outbreak situation has created
additional categories of persons at potential risk of exposure to M bovis including
hunters, trappers, and taxidermists, guides, wildlife conservation officers, venison
consumers and wildlife rehabilitators. Laboratory, veterinary and other regulatory
personnel examining deer carcasses as part of routine surveillance procedures may be
exposed to M bovis through direct contact with infected tissues and aerosolized particles
(Wilkins, 2003; 2008; USDA, 1996). During an outbreak in Canada involving elk, 8 of
30 of the veterinarians exposed to M bovis infected herds were TST positive compared to

l of 20 veterinarians not exposed (F arming, 1991).

INJURIES ASSOCIATED WITH VETERINARY PRACTICE

Veterinary practitioners are often classified as having a primary employment
focus in companion animal practice, large animal practice or a combination of both.
Regardless of their concentration, veterinary practice. presents occupational hazards fi'om
physical, biological and chemical agents (J eyaretnarn, 2000). An occupational hazard
survey found needle punctures, kicks and crush or handling injuries as the leading cause
of injury to veterinarians in large animal practices (Poole, 1999) while cat bites, dog bites

and needle punctures topped the list in companion animal practices (Poole, 1998). A

25

survey of AVMA members in Minnesota and Wisconsin found hands, shoulder/arm, leg,
head, back and feet to be the most frequently injured anatomic structures (Landercasper,
1988). Occupational injuries of zoo veterinarians have also been specifically studied
(Hill, 1998), as well as practice hazards unique to pregnant veterinarians (Moore, 1993).
In a large Minnesota study of all licensed veterinarians, factors found to increase the risk
of veterinary injury included smoking, lack of sleep, lifting heavy patients, inexperience,
and lack of availability of assistants. In contrast, participation in aerobic activities,

increasing age and male gender were found to decrease the risk of injury (Gabel, 2002).

26

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33

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Emerg Infect Dis. In press 2008.

34

CHAPTER 2
MYCOBACTERIUM BOVIS (BOVINE TB) EXPOSURE AS A RECREATIONAL
RISK FOR HUNTERS: RESULTS OF THE MICHIGAN HUNTER SURVEY—
2001.
ABSTRACT
Tuberculosis caused by Mycobacterium bovis (Bovine TB) is endemic in the

white-tailed deer population of northeastern Michigan. Hunters may be exposed to
Mycobacterium bovis via cutaneous inoculation while field dressing deer or by ingestion
of undercooked venison. Michigan hunters have received inconsistent messages about
their risk of acquiring tuberculosis from recreational exposure to deer. The most common
health advice offered has been to wear gloves while field dressing deer and to thoroughly
cook venison products. Data were collected to quantify these self-protective activities
and to characterize hunters practicing these activities. In 2001, we surveyed 1,833
hunters who had successfully harvested deer in or near Michigan’s Bovine TB endemic
area in 2000. The survey response rate was 78%. Most hunters (89%) reported field
dressing deer, 43% of whom wore gloves. Most hunters (95%) reported eating venison;
55% of whom reported their venison was always cooked thoroughly. Several hunter
characteristics including older age, female gender, higher awareness level, and area of
residence, were significantly associated with the practice of these self-protective
activities. The survey results suggest hunters should receive consistent advice
encouraging glove use while field dressing deer and the thorough cooking of venison

products before consumption.

35

INTRODUCTION

Although cattle are the historical reservoir species for Mycobacterium bovis
(Bovine TB) in the United States, tuberculosis caused by M bovis has become endemic
in the wild white-tailed deer population in the northern lower peninsula of Michigan
(Schmitt, 1997). Identified initially in a young cow and a hunter-killed white-tailed deer
in 1994, the distribution within various animal populations has been explored by several
state and federal agencies. Prior to the October 2001 mailing date of this survey, 371
infected cervidae, carnivores or omnivores had been found in 12 of Michigan’s 83
counties: 342 wild white-tailed deer, one elk, 13 coyotes, four black bear, four bobcats,
two opossum, two raccoons, two red fox and one domestic cat (Michigan Department of
Natural Resources, 2001). Most of the infected wildlife and all of the infected farms
(including one captive white-tailed deer farm, 16 beef herds and two dairy herds) were
found within a five county area where the disease is considered endemic (United States
Department of Agriculture, 2001). The “endemic” area includes, Alcona, Alpena,
Montrnorency, Presque Isle, and Oscoda counties.

Infected cattle have been a source of infection for humans, via direct inhalation of
the organism and ingestion of unpasteurized dairy products from infected herds (Grange,
1994; Wigle, 1972). Abattoir workers have been infected during the processing of cattle
(Robinson, 1988; Cousins, 1999; Georghiou, 1989). Recently, cervidae have been
documented as the source of M bovis infection for humans; infection resulted from

exposure to live elk and the processing of cervidae carcasses (F anning, 1991).

Mycobacterium bovis in Michigan humans

36

Although M. bovis is a well-recognized zoonotic agent, available evidence has
shown no change in the incidence of M bovis infections in Michigan’s human residents
since the outbreak in deer was recognized. Since 1995, the expected incidence rate of M
bovis infection in Michigan residents is approximately one new case per year with a
range of 0-2 cases; the number of humans diagnosed with tuberculosis in Michigan has
ranged from 287 to 443 per year with <0.5% of these cases attributed to infection with M
bovis (Michigan Department of Community Health, 2002). At the time of the survey,
none of the human cases of M bovis in Michigan were related to the current outbreak of
Bovine TB in Michigan’s deer and cattle, based on epidemiologic case-investigations and
pulse-field gel electrophoresis (PFGE) analysis of M bovis isolates from humans and
deer completed by the Michigan Department of Community Health Laboratory

(Michigan Department of Community Health, 2002, unpublished data).

Mycobacterium bovis in Michigan deer

For deer, the most probable routes of exposure to M bovis are via inhalation or
ingestion, with the organism initially colonizing the tonsils before spreading to the cranial
lymph nodes and thoracic tissue (Schmitt, 1997; Palmer, 1999; 2000; O’Reilly, 1995).
The pulmonary form of infection is the most contagious to other mammals via coughing
and aerosolization of the organism (Sigurdsson, 1945). Likewise, for mammals,
exposure to M bovis via inhalation is more likely to lead to infection than exposure via
the gastrointestinal or cutaneous route (Whiting, 1994). Based on the 2000 deer harvest
survey data, an apparent prevalence estimate of 0.82% was generated for the five-county

endemic area (O’Brien, 2002).

37

While it is unlikely that hunters would be exposed to aerosolized droplets fi'om
infected deer, they often have close contact with the deer carcass during field dressing,
raising the possibility of cutaneous exposure. Primary inoculation tuberculosis
(tuberculous chancre, cutaneous primary complex) is very rare in developed countries
due to control efforts in cattle and humans (Kakakhel, 1989). In the past, primary
inoculation tuberculosis caused by M bovis was known as “butcher’s wart” and was
considered an occupational disease of butchers, farmers and knackers (handlers of poor
quality or deceased livestock) (Tappeiner, 1993). Cutaneous exposure to M bovis during
field dressing may occur when hunters cut themselves while field dressing or when
hunters field dress with an unprotected, open wound or abrasion on their hands or
forearms. Injury is required for infection, as tubercle bacillus cannot penetrate normal
intact skin (Kakakhel 1989; Sehgal, 1990). Field dressing a deer entails the removal of
all organs from the abdominal and chest cavity.

Hunters are also likely to consume venison products; therefore, exposure to M
bovis via the ingestion of undercooked, infected meat is a possibility. The infection of
humans via the consumption of infected meat has not been documented in scientific
literature. The severity of M bovis infection in humans is similar to infection with M
tuberculosis; both are highly dependent on the site of infection and immune status of the

individual (Cousins, 1999).

Bovine TB and health in the media

Literature in the form of brochures, newsletters, press releases, and intemet web

pages, has been distributed by state and federal agencies, Michigan State University, and

38

local health departments. From 1998 through 2000, the Michigan Press Reading Service
collected over 3000 newspaper articles with keywords “Bovine TB” (Table 2.1). Ten
percent of the articles state that humans are susceptible to M bovis infection. Of the
articles noting the zoonotic potential of M bovis, an average of 66% say the risk to
humans is none, negligible, or low, and offer no further advice on avoiding exposure to
the organism. The remaining articles do offer advice on avoiding exposure to the
organism that includes cooking venison thoroughly until the meat is no longer pink and

the juices run clear and wearing rubber or latex gloves while field dressing deer.

Table 2.1 : Summary of the public health content of newspaper articles containing

keywords “Bovine TB” collected by Michigan Press Reading Service, 1998-2000.

 

1998 1999 2000
No. (%) No. (%) No. (%)

 

Total articles referencing “Bovine
TB” in Michigan Press 790 1410 843

No. articles noting human
susceptibility to Bovine TB 79 (10.0) 119 (8.4) 104 (12.3)

Statements made or advice offered

No or negligible risk - no

advice 44 (55.7) 25 (21.0) 39 (37.5)
Low or small risk - no

advice 20 (25.3) 56 (47.1) 14 (13.5)
Cook meat thoroughly

(low risk) 11 (13.9) 27 (21.0) 14 (13.4)
Cook meat thoroughly

(low risk), skin test 0 O 7 (6.7)
Cook meat thoroughly

and wear gloves 2 (2.6) 8 (6.7) 5 (4.8)

39

Table 2.1 (cont’d)

Wash hands and wear

 

gloves 1 (1.3) 1 (0.8) 1 (1.0)
Have a TB skin test if

concerned 1 (1.3) 2 (1.7) 24 (23.1)
Total 79 (100.1) 119(100) 104 (100)

In Michigan, no evidence of transmission from deer to humans had been found at
the time of the survey, therefore the human health risk was considered only hypothetical
despite thousands of hurnan-deer interactions in the outbreak area. Consequently, a
concerted effort was made by all involved regulatory agencies to present the risk of
human acquisition of M bovis via recreational exposure as small, for two principle
reasons. First, controlling the Bovine TB outbreak in deer necessitates reducing the
number of deer in affected areas, a process that requires active hunter participation.
Second, the local economies of these sparsely populated areas are highly dependent on
the seasonal income provided by hunters.

Because information on the prevalence of preventive behavior by hunters was
lacking, the Michigan Departments of Community Health (MDCH) and Natural
Resources (MDNR) conducted the Michigan Hunter Health Survey (MHHS). It’s
primary purpose was to estimate the percentage of hunters taking measures to reduce
their exposure to M bovis and to determine which hunter characteristics are associated
with the practice of these self-protective measures. A secondary objective was to collect
information on the types of meat products made fi'om venison, hunter perceptions of the
risks posed by Bovine TB, and appropriate venues for disseminating future public health

information.

40

METHODS

Target population

The population target for this survey was hunters who successfully harvested at
least one deer during the 2000 hunting season in one of 11 counties in the northcentral
and northeastern portion of lower peninsula of Michigan as shown in the lower portion of
Figure 2.1. The sample frame consisted of hunters who responded to the MDNR’s 2000
Deer Harvest Survey (Frawley, 2000), which received surveys from 36,021 respondents

statewide who successfully took at least one deer during the 2000 hunting seasons.

41

 

Kalkaska

222

Mas-urea Roscommon Ogomaw

 

 

Figure 2.1 : Location of Stratum 1 counties (bovine TB found in animals) are indicated
by the “1” and Stratum 2 counties (no bovine TB found in animals) are indicated by the
“2” within the state of Michigan. The shading counties within the enlarged area indicate

counties in which bovine TB positive deer had been found, at the time of the survey.

Michigan Hunter Health Survey

42

The sample for the 2001 MHHS included all 1833 hunters who responded to the
2000 Michigan Deer Harvest Survey and harvested deer in the eleven counties of interest.
Stratum 1 counties, Alcona, Alpena, Presque Isle, Montrnorency and Oscoda, are
contiguous and were selected because the majority of positive deer and all the positive
farms (at the time of the survey) had originated from these counties. Stratum 2 consisted
of six counties, Charlevoix, Cheyboygan, Kalkaska, Missaukee, Ogemaw, and
Roscommon, chosen from the same geographic area as Stratum 1 counties, but no TB
positive animals had been found in these counties at the time of the survey (Figure 2.1,
enlarged portion) (Michigan Department of Natural Resources, 2001).

Questionnaires were sent to 884 to hunters harvesting in Stratum 1, and 949 to
hunters harvesting in Stratum 2. The first mailing occurred in mid-October and the
second in early November 2001. For hunters failing to return the questionnaire, two
follow-up phone calls were made with administration of the questionnaire over the phone
when possible.

In addition to the variables listed in Table 2.2, the hunter’s date of birth was
collected as well as whether they had ever had a TB skin test. The experience variable
measured the number of seasons hunted and was calculated using the hunter’s current age
minus age started hunting and multiplied by frequency of hunting variable. For example,
a 40 year old who started hunting at age 14 and reported hunting every other year {[(40 —
14) x 0.5] = 13} is Experience Level 3 (IO-19 seasons). Figure 2.2 defines areas of

hunter residence and the ntunber of respondents from each area.

43

Table 2.2 : Michigan Hunter Health Survey responses, total and per strata.

 

 

Responses Responses Responses
Total Strata 1' Strata 2*

Variable No. (%) No. (%) No. (%)
Total 1420 697 (49.1) 723 (50.9)
Gender

Male 1322 (93.1) 657 (94.3) 665 (92.0)

Female 98 (6.9) 40 (5.7) 58 (8.0)
Age category

14-19 81 (5.7) 43 (6.2) 38 (5.3)

20-29 108 (7.6) 56 (8.0) 52 (7.2)

30-39 273 (19.2) 124 (17.8) 149 (20.6)

40-49 404 (28.5) 204 (29.3) 200 (27.7)

50-59 290 (20.4) 131 (18.8) 159 (22.0)

60+ 264 (18.6) 139 (19.9) 125 (17.3)
Hunting frequency

Every year 938 (66.4) 459 (66.0) 479 (66.8)

Almost every year 412 (29.2) 210 (30.2) 202 (28.2)

Every other year 20 (1.4) 7 (1 .0) 13 (1.8)

Every 3-5 yrs 26 (1.8) 12 (1.7) 14 (2.0)

Every 6-10 yrs 4 (0.3) 1 (0.1) 3 (0.4)

Over 10 years between 12 (0.8) 6 (0.9) 6 (0.8)
Age first started hunting

4-14 726 (52.5) 360 (53.4) 366 (52.1)

15-17 295 (21.4) 147 (21.8) 148 (21.0)

44

Table 2.2 (cont’d)
18-24
25+
Experience level
1 (1-3 seasons)
2 (4-9 seasons)
3 (10-19 seasons)
4 (20-29 seasons)
5 (30-39 seasons)
6 (40+ seasons)
Field dress own deer
Yes
No. deer field dressed
1
2
3-4
5-9
10+
Wear gloves field dressing
Yes
Cut self field-dressing
Yes

Eat any venison
Yes

211 (16.0)

145 (10.1)

95 (6.9)
105 (7.7)
246 (18.0)
399 (29.1)
300 (21.9)
224 (16.4)

1256 (88.7)

589 (51.9)
354 (31.2)
148 (13.0)

33 (2.9)

18 (1.0)

541 (43.2)

60 (4.9)

1362 (96.6)

45

101 (15.0)

66 (9.8)

42 (6.3)

51 (7.6)
118 (17.6)
195 (29.1)
148(221)

117 (17.4)

618 (89.0)

289 (51.6)
168 (30.0)
74 (13.2)
18 (3.2)
11 (2.0)

275 (44.7)

30 (5.0)

665 (96.4)

110 (15.6)

79 (11.2)

53 (7.6)
54 (7.7)
128 (18.3)
204 (29.2)
152 (21.8)
107 (15.3)

638 (88.4)

300 (51.5)
186 (32.0)
74 (12.7)
15 (2.6)

7 (1.2)

266 (42.3)

30 (4.8)

697 (97.3)

Table 2.2 (cont’d)

Eat smoked venison
Yes

Eat venison jerky
Yes

Eat venison sausage
Yes

Cooked thoroughly
Never
Sometimes
Usually
Always

Bovine TB Awareness
Not aware of problem
Somewhat informed
lnforrned
Very informed

Threat to hunters in general
Not aware of problem
No threat
Small threat
Medium threat

Big threat

466 (34.8)

694 (51.2)

774 (54.5)

25 (1.8)
190 (14.0)
402 (29.7)
738 (54.5)

6 (0.4)
238 (17.0)
757 (54.1)
399 (28.5)

11 (0.8)
466 (33.4)
661 (47.4)
212 (15.2)

45 (3.2)

46

235 (35.9)

324 (48.9)

386 (58.4)

13 (2.0)

88 (13.3)
205 (31.0)
355 (53.7)

1 (0.1)

76 (11.1)
374 (54.5)
235 (34.3)

3 (0.4)
265 (38.9)
307 (45.1)

87 (12.8)

19 (2.8)

231 (33.8)

370 (53.3)

388 (56.0)

12 (1.7)
102 (14.7)
197 (28.4)
383 (55.2)

5 (0.7)
162 (22.7)
383 (53.6)
164 (23.0)

8 (1.1)
201 (28.2)
354 (49.6)
125 (17.5)

26 (3.6)

Table 2.2 (cont’d)

Risk to personal health

Not aware of problem 6 (0.4) 2 (0.3) 4 (0.6)
No risk 746 (53.3) 383 (55.7) 363 (51.0)
Small risk 550 (39.3) 262 (38.1) 288 (40.4)
Medium risk 85 (6.1) 35 (5.1) 50 (7.0)
Big risk 12 (0.9) 5 (0.7) 7 (1.0)

Discussed with health professional
Yes 135 (9.6) 79 (11.5) 56 (7.8)
Skin tested due to BTB concern
Yes 19 (1.4) 13 (2.0) 6 (0.9)
Preferred source BTB health infoI
Hunting Assoc. Newsletters 331 (23.3) 163 (23.4) 168 (23.2)
DNR Hunting/'1' rapping Guide 866 (61.0) 412 (59.1) 454 (62.8)
Hunting/Sports Magazines 560 (39.4) 273 (39.2) 287 (39.7)
Hunting/Sports TV programs 589 (41.5) 279 (40.0) 310 (42.9)
DNR Web page 365 (25.7) 174 (25.0) 191 (26.4)
Bovine TB Web page 208 (14.6) 106 (15.2) 102 (14.1)

 

*Alpena, Alcona, Presque Isle, Montrnorency, Oscoda.
ICharlevoix, Cheboygan, Kalkaska, Missaukee, Ogemaw, Roscommon.

1More than one answer possible, percentages do not equal 100.

47

    
  

Upper
Peninsula
N=6
.‘ '. Northeastern
Lower Peninsula
Northwestern N=421
Lower Peninsula
N=152

 

 

 

 

Southern Lower
Peninsula I I

N=435 f ’ GIG-8191'
Detrort Area
I I N=334

 

 

 

 

 

 

Figure 2.2 : Map of Michigan showing geographic areas of residence and the number of

survey respondents residing in each area.

48

ANALYSIS

Associations between both glove use or thoroughness of cooking and hunter
characteristics were assessed using relative risks for binomial variables and the Mantel-
Haenszel Chi square test for trend for ordinal variables. A linear test for trend compared
increasing age, experience, levels of awareness, perception of risk to personal health and
perception of threat to hunters in general with the likelihood of wearing gloves and with
thoroughness of cooking. The cooking variable was categorized as “always” cook
thoroughly versus “other” (never, sometimes, and usually cook thoroughly) for analyses.
Glove use, thoroughness of cooking, awareness level, risk perception and threat
perception of Stratum l and Stratum 2 hunters were compared. Resulting p-values of
$0.05 were considered significant. Data were analyzed using SPSS Version 10.0

software (SPSS Inc., Chicago, IL).

RESULTS

Survey response

The response rate was 1420/1808 (77.5%) after correcting for 25 undeliverable
mailing addresses. Phone numbers were found for 394 of 516 (76%) non-responding
hunters. An additional 44 surveys were completed over the phone. There was no
significant difference in response rate by gender (p<0.14) or Stratum 1 verses Stratum 2
(p<0.17). The average age of responders was significantly greater than non-responders
(46.1 years verses 39.5 years, p<0.001). Hunters residing in the southern lower peninsula

and Detroit area had a significantly higher response rate than hunters residing in the

49

northern lower peninsula (80.8% versus 71.3%, p<0.01). The responses to survey

questions are summarized in Table 2.2.

Glove use

Eighty nine percent of hunters field dressed their own deer in 2000. Of these,
43.2% reported wearing gloves while doing so. Characteristics of hunters and the relative
risk of wearing gloves are found in Table 2.3. Tests for trend showed a significant,
positive linear trend between increasing awareness level (p<0.03), increasing perception
of threat (p<0.03), and increasing perception of risk (p<0.05) with the use of gloves while

field dressing.

Table 2.3 : Characteristics of hunters associated with their likelihood of wearing gloves

while field dressing during the 2000 hunting season.

 

 

Binomial Variables Relative Risk 95% Confidence Level
Gender
Female vs. male 1.28 0.99 — 1.66

Hunting location
Stratum 1 vs. 2 1.06 0.93 — 1.20

Area of residence
Southern LP/Detroit vs.

 

Northeast/Northwest LP 1.38 1.19 - 1.59
Discussed TB Health concerns

with health professional 1.04 0.84 - 1.27
Ordinal Variables 98 test statistic' p-value for trend'r

 

Increasing levels of awareness
about Bovine TB 4.54 0.03

50

Table 2.3 (cont’d)

Increasing perception of Bovine

TB threat to hunters in general 4.99 0.03
Increasing perception of Bovine TB

risk to personal health 3.91 0.05
Increasing age categories 1.07 0.30
Increasing level of experience 1.42 0.23

 

'Tested using Mantel-Haenszel test for trend.

I Results in bold indicate statistical significance at the 050.05 level.

Thoroughness of cooking

Fifty-five percent of hunters reported consuming venison always cooked until it is
no longer pink and the juices run clear. Characteristics of hunters and the relative risk of
consuming venison always cooked thoroughly are found in Table 2.4. Tests for trend
showed a significant positive linear trend only between increasing age and thoroughness

of cooking (p<0.01).

Table 2.4 : Characteristics of hunters associated with their likelihood of reporting

consuming venison from the 2001 hunting season as always cooked thoroughly.

 

 

Binomial Variables Relative Risk 95% Confidence Level
Gender
Female vs. male 1.30 1.12 — 1.50

Hunting location
Stratum 1 vs. 2 0.97 0.88 — 1.07

51

Table 2.4 (cont’d)

Area of residence

 

Northeast/Northwest LP vs.

Southern LP/Detroit 1.20 1.09 - 1.32
Discussed TB Health concerns

with health professional 0.98 0.83 - 1.16
Ordinal Variables X2 test statistic' p-value for trend1

 

Increasing levels of awareness

about Bovine TB 2.76 0.10
Increasing perception of Bovine

TB threat to hunters in general 0.03 0.89
Increasing perception of Bovine TB

risk to personal health 0.13 0.72
Increasing age categories 8.37 <0.01
Increasing level of experience 2.01 0.16

 

'Tested using Mantel-Haenszel test for trend.

I Results in bold indicate statistical significance at the 050.05 level.
Location of hunter harvest

Survey results also indicated hunters harvesting deer in Stratum 1 were
significantly more likely to report being informed or well informed about the TB problem
than hunters hunting in Stratum 2 (p<0.01). Stratum 1 hunters were also significantly
more likely to consider the public health threat of Bovine TB to be small to none

(p<0.01).

DISCUSSION

Glove use

52

Our results indicate that nearly nine out of 10 (89%) respondents field dressed
their own deer with fewer than half (43%) wearing gloves while doing so. Approximately
30,730 deer were harvested within the five county endemic area (Stratum l) in 2000
(Frawley B, MDNR, personal communication). As the apparent prevalence of infected
deer for this area is 0.82%, approximately 252 positive deer were harvested. Our survey
results indicate that 55.3% of Stratum l hunters did not wear gloves while field dressing.
Therefore we estimate up to 139 (252 x .553) Stratum 1 hunters may have field dressed
positive deer without wearing gloves. Of potentially more concern are the 5.0% or 12 to
13 hunters (252 x 0.05) who reported cutting themselves enough to bleed while field
dressing these positive deer.

Although latex or heavy rubber gloves may not protect against a cut during the
field dressing process, gloves may lessen the severity of the cut, protect pre-existing
wounds from exposure to the organism, and decrease surface contamination of the hands
while handling internal organs. The average period of time between field dressing and
hand washing was 98 minutes, allowing many opportunities for hand-to-mouth contact to
occur.

Statewide, as hunter’s level of Bovine TB awareness increased, so did the
likelihood of wearing gloves while field dressing. Likewise, as the perception of threat to
hunters and risk to personal health increased, so did the likelihood of wearing gloves

while field dressing.

Gastrointestinal exposure

53

The probability of finding M bovis in the muscle tissue of bovines and cervids
with disseminated disease is poorly defined. In a 1999 study, 45% of TB positive
Michigan deer bore M bovis lesions outside of the cranial area (O’Brien, 2001).
Research on the dissemination of the organism and lesions in deer and cattle has focused
almost exclusively on tissue samples taken from the lymphatic and pulmonary systems,
liver, kidney and spleen. Only one recent study on the experimental transmission of M
bovis in deer reported the presence of M bovis in intercostals and diaphragm muscle
samples, but the study did not examine muscle tissues generally consumed by hunters
(Palmer, 2001). The acquisition of M bovis from the ingestion of infected meat has not
been documented in humans. However, infection following the consumption of infected
bovine or cervid carcasses has been reported in other mammalian species including
domestic and wild felids such as lions and bobcats, coyotes, raccoons, red fox, and black
bear (Isaac, 1983; Keet, 2000; Bruning-Fann, 2001). Humans generally avoid
consuming the pulmonary and lymphatic tissue most likely to harbor the organism and
usually cook meat before consuming it, firrther reducing the risk of ingesting large
numbers of organisms.

Venison processed in a licensed food establishment or processed for retail sale is
regulated by Michigan Department of Agriculture (MDA). MDA estimates less than
20% of all Michigan hunter-harvested venison is processed under state regulation (MDA,
Food and Dairy Division, 1998). The remainder is processed for home consumption by
unregulated and seasonal processors. Venison is often further processed into jerky and
sausage without regulatory oversight, making the inclusion of lymphatic tissue into

sausage mixtures or the surface contamination of steaks or roasts more likely. Smoking

54

of sausage and drying of j erky usually requires a long heating time at low temperature
and is often completed by unregulated processors or within the home. Outbreaks of
human disease caused by E. coli, Salmonella, and Trichinella have been linked to the
consumption of sausage and jerky made from beef or wild game (CDC, 1995a; 1995b;
1995c, 1996).

Because venison is very lean, it can become tough when thoroughly cooked,
consequently, there may be a tendency toward undercooking. It is difficult to assess the
risk of acquiring M bovis through consumption of undercooked venison. For solid
pieces of meat, the risk would likely be from surface contamination occurring during
gutting or processing. M bovis survived in wieners kept at 50°C (122°F) for 90 minutes
but was killed at a temperature of 60°C (140°F), held for six minutes (Merkal, 1980).
Most hunters are probably not at risk from consuming steaks, roasts or pan-fried
sausages. However, the hunting community needs education on the proper time and
temperature requirements for preparing smoked venison, venison sausages and venison
jerky. Proper knife sanitation, meat handling and adequate cooking temperatures will
substantially reduce the risk of human illness. State-wide, hunters with a high level of
awareness about Bovine TB, and hunters who perceived M bovis to be a public health
threat or personal health risk were more likely to report always cooking venison

thoroughly, although the trends were nonlinear.

Hunting location and hunter residence

Hunting in Stratum 1 versus Stratum 2 counties had no effect on the hunter’s

decision to wear gloves nor the likelihood of always cooking venison thoroughly. In

55

contrast, the hunter’s area of residence did impact their decision to wear gloves, with
hunters living in the northern lower peninsula counties being significantly less likely to
wear gloves but significantly more likely to always cook venison thoroughly than hunters
living in the southern lower peninsula and Detroit area. These strong associations are
likely due to cultural and hunting practice differences between the northern resident
hunters who hunt “locally” versus southern resident hunters who drive up for a long
weekend. Hunting is a way of life for many northern Michigan residents; many hunt and
consume a wide variety of wild game species. Perhaps in the northern counties, the
practice of thoroughly cooking game meat is simply ingrained in the population, just as
the practice of wearing gloves is not.

Compared with Stratum 2, Stratum 1 hunters considered themselves better
informed and also considered Bovine TB to be less of a threat to hunters in general and
less of a threat to their personal risk. This suggests an inverse relationship between level
of Bovine TB awareness and concern about the public health implications of Bovine TB
in the highest risk counties. Perhaps the efforts of the regulatory agencies to reassure
Stratum l hunters that their health risks are small have given Stratum 1 hunters a sense of
complacency. Message fatigue is another possibility, as much of the media focus has
been on the endemically infected counties of Stratum 1.

Ahnost 10% of the hunters surveyed reported consulting with health professional
about the possibility of catching Bovine TB, suggesting concern within this community.
However, consultation with a health professional did not increase the probability these
hunters would choose to wear gloves or report consuming venison always cooked

thoroughly. This indicates needed improvement in regulatory agencies educating the

56

medical community, and the medical community educating hunters. This finding may be
a result of the conflicting public health messages conveyed to the public since the
outbreak began.

This survey has several limitations. Recall error may be a factor as hunters were
asked to recall events 10 to 12 months distant. Nonresponse bias is another possible
limitation as responders were significantly older and more likely to reside in the southern
part of Michigan than nonresponders. The 2000 Michigan Deer Harvest Survey was not
evaluated for the presence of bias. Any nonresponse bias present in 2000 Michigan Deer
Harvest Survey would carry over to the MHHS as the latter study population was selected
from the former. Finally, data detailing when and why hunters adopted the self-
protective measures of interest were not collected. Therefore the impact of public health

outreach efforts on hunter behavior cannot be evaluated.

CONCLUSION

The mixed results of this survey may reflect confusion from inconsistent public
health messages regarding risk of exposure and acquisition of Bovine TB. The best
approach to reduce the risk of transmission to hunters and venison consumers is to
prevent exposure. A simple and consistent public health message encouraging glove use
while field dressing deer and the thorough cooking of all venison products is needed.
This public health message should target several audiences including: hunters,
taxiderrnists, venison processors, venison consumers, medical personnel and the

regulatory/advisory community.

57

Hunters may be more receptive to public health advice in the future because of the
discovery, in February 2002, of a human case of M bovis. This case is genetically and
epidemiologically linked to the same strain of M bovis currently circulating in deer and
cattle, suggesting the zoonotic risk of transmission is no longer only hypothetical
(Michigan Department of Community Health, 2002). Also, the discovery of Chronic
Wasting Disease (CWD), a transmissible spongiform encephalopathy, in the free-ranging
deer of Wisconsin has raised concerns of Michigan hunters. Although evidence to date
does not indicate that CWD is a zoonotic agent, hunters will be looking to state agencies
for information and recommendations. This period of heightened awareness should be
utilized wisely to promote a simple and consistent public health message.

Specific recommendations should be provided to hunters regarding the best
practices for field dressing deer, aging and processing venison, and cooking venison and
other wild game. Based on survey results, the MDNR’s Annual Hunting and Trapping
Guide would be the best venue for distributing public health information to hunters.
Efforts are underway to expand the hunter health section of this popular publication. The
challenge will be to raise hunter awareness enough to persuade them to adopt basic
exposure prevention, without unduly inflating perceptions of risk and so dissuading them
from hunting in the areas where hunting is beneficial to the local economies and critical

for disease control and eradication efforts.

58

REFERENCES

Bruning-Fann CS, Schmitt SM, Fitzgerald SD et a1. Bovine tuberculosis in
free-ranging carnivores from Michigan. J Wildl Dis. 2001;37:58-64.

Centers for Disease Control and Prevention. Escherichia coli 0157:H7
outbreak linked to commercially distributed dry-cured salami — Washington
and California, 1994. MMWR. 1995a;442157-160.

Centers for Disease Control and Prevention. Community outbreak of
Hemolytic Uremic Syndrome attributable to Escherichia coli 01 11:NM —
South Australia, 1995. MMWR. 1995b;44:550-551,557-558.

Centers for Disease Control and Prevention. Outbreak of Salmonellosis
associated with beef jerky — New Mexico, 1995. MMWR. 1995c;44:785-788.

Centers for Disease Control and Prevention. Outbreak of Trichinellosis
associated with eating cougar jerky — Idaho, 1995. MMWR. 1996;45:205-
206.

Cousins DV, Dawson DJ. Tuberculosis due to Mycobacterium bovis in the Australian
population: cases recorded during 1970-1994. Int J Tuberc Lung Dis. 1999;31715-
721.

Fanning A, Edwards S. Mycobaterium bovis infection in human beings in contact
with elk (Cervus elaphus) in Alberta, Canada. Lancet. 1991;338:1253-1255.

Frawley, BJ. Michigan Deer Harvest Survey Report 2000 Seasons. MDNR/Wildlife
Report No. 3344. Michigan Department of Natural Resources, Lansing, Michigan,
2001.

Georghiou P, Patel AM, Konstantinos A. Mycobacterium bovis as an occupational hazard
in abattoir workers. Aust NZ J Med. 1989;19:409-10.

Grange JM and Yates MD. Zoonotic aspects of Mycobacterium bovis infection. Vet
Microbiol. l994:40;l37-151.

Isaac J, Whitehead J W, Adams MD, Coloe P. An outbreak of Mycobacterium bovis
infection in cats in an animal house. Aust Vet J. 1983;60:243-245.

Kakakhel KU, Fritsch P. Cutaneous tuberculosis. Int J Dermatol. 1989;28:355-362.

Keet DF, Kriek NPJ, Michel A. Tuberculosis and its geographical distribution in free-
ranging lions in the Kruger National Park. In: Proceedings of the Third
International Conference on Mycobacterium bovis, Cambridge, England, 2000.

59

Merkal RS, Whipple DL. Inactivation of Mycobacterium bovis in meat products. Appl
Enviro Micro. 1980;40:282-284.

O’Brien DJ, Fitzgerald SD, Lyon TJ, Butler KL, F ierke J S, Clarke KR, Schmitt SM,
Cooley TM, Derry DE. Tuberculosis lesions in free-ranging white-tailed deer in
Michigan. J Wildl Dis. 2001;37:608-613.

O’Brien DJ, Schmitt SM, Fierke J S, Hogle SA, Winterstein SR, Cooley TM, Moritz WE,
Diegel KL, Fitzgerald SD, Berry DE, Kaneene JB. Epidemiology of
Mycobacterium bovis in free-ranging white-tailed deer, Michigan, USA, 1995-
2000. Preventive Vet Med. 2002:54;47-63.

O'Reilly LM, Dabom CJ. The epidemiology of Mycobacterium bovis infections in
animals and man: a review. Tuber Lung Dis. 1995;76:1-46.

Palmer MV, Whipple DL, Olsen SC. Development of a model of natural infection with
Mycobacterium bovis in white-tailed deer. J Wildl Dis. 1999;35:450-457.

Palmer MV, Whipple DL, Payeur JB, Alt DP, Esch KJ, Bruning-Fann CS, Kaneene JB.
Naturally occurring tuberculosis in white-tailed deer. J Am Vet Med Assoc.
2000;216:1921-1924.

Pahner MV, Whipple DL, Walters WR. Experimental deer-to-deer transmission of
Mycobacterium bovis. Am J Vet Res. 2001;62:692-696.

Robinson P, Morris D, Antic R. Mycobacterium bovis as an occupational hazard in
abbatoir workers. Aust NZ J Med. 1988;18:701-703.

Schmitt SM, Fitzgerald SD, Cooley TM, Bruning-Fann CS, Sullivan L, Berry DE,
Carlson T, Minnis RB, Payeur JB, Sikarskie J. Bovine tuberculosis in free-ranging
white-tailed deer fi'om Michigan. J Wildl Dis. 1997;33(4):749-758.

Sehgal VN, Wagh SA. Cutaneous Tuberculosis: Current Concepts. Int J of Dermatol.
1990;29:237-252.

Sigurdsson J. Studies on the risk of infection with bovine tuberculosis to the rural
population. Acta Tuberc Scand. 1945;supp 1521-250.

Tappeiner G, Wolff K. Tuberculosis and other mycobacterial infections. Fitzpatrick TB,
Freedberg IM, Eisen AZ, Wolff K, Austen KF, Goldsmith LA, Katz SI. editors. 5th
edition. In: Dermatology in General Medicine. New York: McGraw-Hill, 1993: pp
2370-2391.

Whiting TL, Tessaro SV. An abattoir study of tuberculosis in a herd of farmed elk. Can
Vet J. 1994;35:497-501.

Wigle WD, Ashley MJ, Killough EM, Cosens M. Bovine tuberculosis in
humans in Ontario. Am Rev Resp Dis. 1972;528-534.

60

CHAPTER 3
HUMAN MYCOBACTERIUM BOVIS INFECTION ASSOCIATED WITH THE

BOVINE TB OUTBREAK IN MICHIGAN, 1994-2007

ABSTRACT

Mycobacterium bovis or bovine TB, is endemic in the white-tailed deer
population of the northeastern counties of Michigan’s lower peninsula. Between 1994
and February, 2007, M bovis was found in 41 cattle herds and 561 wild deer in
Michigan. Based on genotyping analyses, the strain of M bovis circulating in Michigan’s
deer and cattle has remained consistent for the duration of the outbreak. Although M
bovis is a zoonotic pathogen, this outbreak strain was not detected in a human until 2002,
with the occurrence of a human puhnonary isolate. In 2004 cutaneous disease was
documented in a hunter. This report summarizes the epidemiologic and molecular
investigation of these two human cases who share the deer/cattle outbreak strain of M.
bovis. The results of this investigation confirm recreational exposure to infected deer in

Michigan as a potential, albeit low, risk for acquisition of M bovis infection in humans.

INTRODUCTION

Historically, M bovis infection in humans has been associated with the
consumption of unpasteurized milk and dairy products (Enarson, 1995; Wigle, 1972) and
this remains the most important route of exposure in developing countries as well as US

populations exposed to unpasteurized dairy products imported from countries where M

bovis remains prevalent (Dankner, 1993; CDC, 2005). Before the US began

61

pasteurization of milk and implementation of a national control program in cattle, M
bovis reportedly accounted for 6%-30% of human tuberculosis cases (McKenna, 1995).
Exposure through dairy products was virtually eliminated in Michigan following
implementation of statewide milk pasteurization regulations mandated in 1948 (Michigan
Compiled Law, Act 291 No. 288.131, 1947). Cutaneous infection with Mycobacterium
species also became very rare in the US following the reduction of infection in both
humans and cattle (Tappeiner, 1993).

M bovis infection in humans is of particular concern to both public health and
animal health officials in Michigan due to the endemic nature of M bovis in the state’s
wild white-tailed deer population, and the subsequent discovery of infection in 41
Michigan cattle herds (Michigan Bovine Tuberculosis Eradication Project Activities
Report and Conference Proceedings, 2005). The presence of M. bovis infection in deer
presents several new possible occupational and recreational routes of exposure for
hunters, trappers, taxidermists, venison processors and venison consumers (Wilkins,
2003). To increase hunter awareness, the Michigan Department of Natural Resources has
included bovine tuberculosis (TB) information in their annual Hunting and Trapping
Guide since 1996 (NIDNR, 2006; D. O’Brien, personal communication; Michigan
Department of Natural Resources, 2007).

Although M bovis is a well-recognized zoonotic agent, available evidence
indicates no increase in the incidence of M bovis infections in Michigan residents since
the current outbreak began in 1994 (unpublished data, Michigan Department of
Community Health [MDCH], 2007). Since 1995, the incidence rate of M bovis infection

in Michigan residents has been approximately one new case per year (with a range of 0-3

62

cases), for a total of 13 cases. Less than 0.5% of all human cases of tuberculosis in
Michigan can be attributed to M bovis infection. No genetic or epidemiologic link to the
circulating deer/cattle outbreak strain circulating in northeastern Michigan has been
identified among 11 of the human M bovis cases identified in Michigan residents from
1995 through March of 2007. These findings were based on restriction fi'agment length
polymorphism (RFLP) analysis, spoligotyping or mycobacterial interspersed repeat units
(MIRU) typing (unpublished data, MDCH, 2007). Of these 11 cases, eight occurred in
recent immigrants; seven were from Mexico and one from Bosnia. The remaining three
cases were US-bom, instate residents, diagnosed at ages 74, 75, and 79 years; two of
whom reported a history of raw milk consumption in their youth. Table 3.1 shows the
diversity of spoligotyping and MIRU typing results from nine available human
specimens, unrelated to the deer/cattle outbreak. All genotyping of isolates mentioned in
this report was performed at the MDCH, Bureau of Laboratories, Lansing, MI, using
RFLP, spoligotyping and MIRU guidelines currently recommended by Centers for
Disease Control and Prevention (CDC) (Yang, 1998; Cowen 2002; 2004; Kwara, 2003).
Spoligotyping results were compared to the International M bovis Spoligotyping

Database (closed database, intemet).

63

.88 .8260 .3 68288 8e 52...... 8...: .88. 82899... 5888822 .2

30.692.33.53. 2 EB.— o_nm__m>m ”ommnfimo 0.509.on 320302.02: ..

 

 

 

 

 

 

 

 

 

 

 

 

888.898 9.300 88 2.. .8360 8.8.2
- -- «NSRSER 2900 88 2.. .8350 8.6.2
- 888.888 .980 88 2.. .8350 <0:
. ..... 888388 8800 88 53.80 8.6.2
- 288388 2900 88 2.. .8360 6.28m.
6.8.3.6 82 29% 82 553% 8.6.2
- -- ~88 388 9.500 82 888.. 8.... 8.8.2
-- 6.8.6.5 .62 5300 32 8.8 <0:
. - ....... 6.8.5.5 .62 29mm 52 2.. .8350 <0:
83.8..on +8.: 22.2 “3%.me 888%60 9.0 .o ammoo

 

$2 58.8.3. 8.3.2 825 9:3. as. 36828... .38 .2 882. .392... 2.88.98.28-82 . S. 3.2:.

64

The remaining two human cases of M bovis occurred in US-bom, Michigan residents
with epidemiologic and molecular links to the outbreak strain of M bovis circulating in
the deer and cattle of northern Michigan. The first case was diagnosed in 2002; the

second case was diagnosed in 2004. These two human cases are the focus of this report.

CASE 1, 2002
Clinical History

In January 2002, a male aged 74 years sought medical care for malaise, weakness,
anorexia, and fever of 389°C of one week duration. His past medical history was
significant for ischemic bowel disease, cerebral and peripheral vascular disease, partial
gastrectomy for peptic ulcer disease, and left upper pulmonary lobectomy for squamous
cell carcinoma (December 1999). He was placed on gatifloxacin for a possible urinary
tract infection but retumed one week later with no improvement and with additional
complaints of abdominal pain, nausea, and weight loss of 5 kg. He was maintained on
antibiotics and returned on February 1St when he was hospitalized with persistent fever,
non-productive cough and a chest radiograph revealing post-obstructive infiltrate
involving multiple segments of the left upper lobe. The infiltrate was felt to be consistent
with necrotizing pneumonia. A tuberculosis skin test (TST) was negative and a sputum
smear was negative for acid-fast bacteria (AFB) (Mycobacterium). He was started on
piperacillin/tazobactarn, and azithromycin. After five days of therapy the patient had not
improved clinically; chest radiograph revealed an increasing left side infiltrate and
diagnostic bronchoscopy was performed. This specimen yielded an AF B positive smear.

The patient was diagnosed with presumptive puhnonary tuberculosis and started on four-

65

drug therapy with isoniazid, rifampin, pyrazinamide, and etharnbutol. The patient
deteriorated clinically over the ensuing ten days, developing a right pneumothorax and
hypoxic bowel disease secondary to mesenteric thrombosis. Subsequently, he underwent
bowel resection; his post-operative outcome was complicated by septic shock, adult
respiratory distress syndrome and multi-organ failure. He expired on day 16 of his
hospitalization.

Laboratory confirmation of tuberculosis, speciation, and antimycobacterial
susceptibility testing were pending at the time of his death. Autopsy findings were limited
to the thoracic cavity. The cut surface of the left lung revealed diffuse areas of
parenchymal coagulative necrosis with a tan-gray-yellow fiiable appearance occupying
85% of the cut surface; only 25% nonnal-appearing lung tissue was present. There was
no coagulative necrosis noted grossly in the right lung. The histopathologic findings from
the autopsy report indicated numerous intracellular and extracellular Mycobacterium with
a beaded appearance which raised the possibility of atypical Mycobacterium avium
infection. No evidence of residual squamous cell carcinoma was found. The final culture
results from the bronchial specimen were reported by MDCH, Bureau of Laboratories,
Lansing, MI, as Mycobacterium bovis on April 11, 2002. Genotyping (RF LP) analysis
revealed the M bovis isolated from Case 1 shared the RF LP pattern of the predominant
deer/cattle strain endemic in northeastern Michigan. Further testing of this isolate
revealed spoligotyping and MIRU results matching the patterns of the circulating

deer/cattle strain (Table 3.2).

66

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............. - 888888 2.58 82 m 838
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67

Contact Investigation

Three close personal contacts of the patient and 133 potentially exposed hospital
staff were tested either immediately following Case 1’s presumptive TB diagnosis, and
again at 10 weeks post-exposure, or only at 10 weeks post-exposure. All personal
contacts and hospital staff had non-reactive tuberculosis skin tests and no person-to-
person transmission was detected.
Exposure History

In his youth, Case 1 resided in southeastern Michigan on a farm in an area
geographically distant fi'om that presently endemic for bovine TB. His current (second)
wife reported he drank unpasteurized milk as a youth but that he had not done so for
several decades. He was manied previously and his first wife was reportedly diagnosed
with tuberculosis following their divorce over 40 years before but this could not be
substantiated. He was not known to have any other exposure to an active TB case. Case 1
moved to the edge of Deer Management Unit (DMU) 452 in 1994. DMU 452 has been,
and continues to be, the focal area for the bovine TB outbreak in white-tailed deer. There,
he and his second wife ran a business with a buck pole on the property where hunters
displayed deer they had harvested. He and his wife fed deer on the property, a common
local practice, but stopped when feeding was banned in 1999 (O’Brien, 2006). Although
at one time he was an avid hunter, he had not hunted in at least ten years nor was he
known to have consumed venison over that period of time. However, in 2000 he helped
his brother and a friend of his brother's hang and transport a harvested deer that had been
shot on his property. This fiiend was subsequently TST positive at 20 mm induration,

although chest radiograph was negative, and he was placed on isoniazid for treatment of

68

latent (therefore noninfectious) TB infection. A review of this individual's history
revealed he had been exposed to an uncle with active TB many years previously. No
laboratory samples were available from either the fi'iend or his uncle for culture,
speciation or RF LP analysis.

Discussion — Case 1

This patient had several potential routes of exposure to M. bovis, including the
consumption of raw milk as a youth, exposure to an unconfirmed case of active TB in his
ex-wife over four decades earlier, hunting of white-tailed deer and consumption of
venison although not in the ten years before his death, handling a deer carcass from the
DMU 452 vicinity in 2000 and recreational feeding of white-tailed deer. The patient’s-
earliest possible exposures occurred during the initial years of TB control in Michigan’s
human and livestock populations. The state’s cattle population was not certified by
USDA as free of bovine TB until 1979. The address for the farm on which Case 1 resided
was not available, so the historical herd health records could not be retrieved, if they still
exist. Similarly, searching his ex-wife’s medical records would likely prove fi'uitless as
no laboratory culture would be available for DNA analysis and no differential tests were
available at that time. Lacking records or cultures, the probability of these two potential
routes of exposure cannot be further elucidated.

This patient was in poor health at the time of his death and suffered from both
acute and chronic illnesses. His poor health would have rendered him more susceptible to
infection with M. bovis, and more likely to progress from latent infection to clinical
disease. The pathology results from his lung resection in December, 1999 provided no

evidence of tuberculosis infection so infection was likely acquired subsequently. His

69

chest radiograph during final hospitalization and autopsy results showed severe
puhnonary involvement. The autopsy did not include abdominal findings and it is
unknown whether M. bovis was present in his mesenteric lymph nodes, which could
suggest exposure through consumption of infected milk or meat.

Case 1’s RFLP, spoligotyping and MIRU results matched that of the circulating
deer/cattle strain suggesting exposure to infected cattle or deer. The lack of recent
exposure to cattle suggests deer to be the more likely source of his infection. Information
about the patient’s exposure history was collected by proxy from the patient’s surviving
spouse and, therefore, relevant exposure details may have been missed. It is unlikely that
a conclusive route of exposure can be determined for this patient although one may be
reasonably inferred from the available clinical and epidemiological evidence.

CASE 2, 2004
Clinical history

Case 2 occurred in a 29 year old, previously healthy male with no significant past
medical history. On October 1, 2004, he shot a white-tailed deer in Alcona County,
Michigan, where M. bovis is endemic in the deer population. While field dressing the
animal, he sustained a small puncture wound to the base of his left index finger with a
hunting knife. He also noted tan nodules in the chest cavity classically associated with M.
bovis. Approximately 18 days post-injury, his lefi index finger became inflamed and
painful. He sought medical treatment from his family physician, who placed him on oral
antibacterial therapy (cephalexin). Based on his exposure to a deer, a tuberculin skin test
was administered and was read as negative. After approximately 10 days of antibacterial

therapy, the wound had not improved and the patient reported the abrupt onset of

70

increased pain and decreased mobility of the finger. He was referred to an orthopedic
specialist who diagnosed infectious tenosynovitis of the flexor tendon of the left index
finger. He was hospitalized and treated with intraveneous antibiotics (cephazolin). The
infected finger was incised and drained, and a wound culture was sent to the laboratory.
This specimen was received by MDCH on November 1, 2004. Microscopic examination
of this specimen did not reveal the presence of acid-fast bacilli. He was discharged after a
two-day hospitalization on cephalexin. He was readmitted to the hospital 12 days later
with subcutaneous infection at the initial puncture site, which did not appear to involve
the flexor tendon. The wound was again incised and drained, and he was treated with
intraveneous ampicillin/sulbactam for four days, and discharged on
amoxicillin/clavulanate. On November 23, 2004, a slide made of growth from the broth
culture medium was positive for acid-fast bacilli. Genetic probe results confirmed
Mycobacterium tuberculosis complex on November 24, 2004, and the submitting hospital
was notified. Case 2 was started that same day on the standard four-drug therapy for
Mycobacterium tuberculosis (isoniazid, pyrazinamide, etharnbutol, and rifampin). By
December 7, 2004, the culture was reported as resistant to pyrazinamide at 100mcg/ml,
suggesting M. bovis. At this point, pyrazinamide was dropped from the treatment
regimen. M. bovis was confirmed on December 21, 2004, based on susceptibility to
thiophen-2-carboxylic acid hydrazide (TCH) and detection of pyrazinarnidase activity.

A second skin test placed on January 7, 2005 (14 weeks post exposure) by the
local health department, was positive with a 6mm induration. Case 2 remained on
antibiotic therapy for nine months with no further complications involving his finger.

Contact Investigation

71

Tuberculosis skin testing results performed on Case 2’s immediate family
members were negative at 14 weeks post exposure (wife and child) and 27 weeks post
exposure (2"d test for child only), indicating no person-to-person transmission had
occurred.

Exposure History

At the time Case 2 field dressed the white-tailed deer, he immediately noted the
classic tan nodules in the chest cavity associated with bovine TB. Because he was in an
area he knew to be endemic for M. bovis transmission, he assumed the deer to be
unhealthy and promptly buried it. After undergoing treatment for his infected finger in
early December, he led Michigan Department of Natural Resources staff back to the site
of the buried carcass. The carcass was retrieved and the chest cavity was determined to be
heavily lesioned (Figure 3.1). Although the carcass had been buried for over nine weeks,
samples fiom the chest cavity were submitted to the MDCH laboratory for culture. After
numerous attempts using alternative decontamination techniques, a viable culture was
obtained on January 10, 2005, with pure grth on February, 28, 2005. Spoligotyping
and MIRU results of the isolate taken from the recovered deer carcass were identical to
the patterns of the strain recovered from the Case 2’s finger. In addition, these patterns
were identical to the M. bovis strain circulating in the deer and cattle in northeastern

Michigan as shown in Table 3.2.

72

 

Figure 3.1 : Photo of the chest cavity of the deer shot by Case 2, retrieved after being
buried for 9 weeks, displaying the classical nodular lesions of M. bovis infection in deer.
Photo: J S Fierke, DJ O’Brien, SM Schmitt Wildlife Disease Laboratory, Michigan

Department of Natural Resources.

Discussion — Case 2

The investigation of Case 2 provided strong evidence of transmission of M. bovis
infection from an infected deer to a human via percutaneous inoculation with a
contaminated hunting knife. The patient’s history of a hunting exposure was essential to

proper diagnosis and treatment of this very rare form of tuberculosis.

73

CONCLUSION

Because these two persons were infected with isolates with matching genotypes,
they are said to belong to the same genotyping cluster. Patients in the same genotyping
cluster who share known epidemiological links are said to belong to an epidemiologically
confirmed genotyping cluster as determined by protocols described by the National TB
Controllers Association and the CDC (CDC, 2004). Although the epidemiologic evidence
presented for Case 1 is not irrefutable, it is the opinion of the authors that both cases are
part of a cluster that is epidemiologically as well as genotypically confirmed.

The initial tuberculosis skin test was negative in both of these cases. For Case 1,
the test was negative most likely due to cutaneous anergy. For Case 2, the skin test was
administered too soon following exposure. He was tested prior to the 8-10 week period
required for his immune system to mount a detectable response. His second skin test was
appropriately interpreted as positive at 6 mm induration by staff from the local public
health department. However, a 6 mm induration would traditionally be classified as
negative based on his lack of standard risk factors used by CDC (CDC, 2006). In both
cases, initial negative skin test results made diagnosis problematic for the physicians
involved with healthcare.

Based on a 2001 survey of 1,833 hunters who had successfirlly harvested deer in
or near Michigan’s bovine TB endemic area, it was determined that 89% of hunters field
dressed their own deer, and only 43% of them wore gloves when doing so (Wilkins,
2003). Based on the 2001 prevalence estimate in the deer population and the survey
results, up to 139 hunters in the endemic counties may have field dressed positive deer

without wearing gloves and up to 12 hunters would cut themselves while field dressing

74

these positive deer (Wilkins, 2003). However, this is the only case that has come to the
attention of public health officials. Since the time of the survey, the apparent prevalence
of M. bovis infection in the white tailed deer population has been declining (Michigan
Bovine Tuberculosis Eradication Project Activities Report and Conference Proceedings,
2005) in the affected counties, but more counties now report positive deer. Cutaneous or
percutaneous exposure to M. bovis, while field dressing infected deer, continues to be a
potential risk for Michigan hunters.

The confmnation of a hunter acquiring cutaneous M. bovis from an infected deer
supports the need for public health precautions for deer hunters. First, hunters should
wear heavy latex or rubber gloves while field dressing deer. Although latex or heavy
rubber gloves may not protect against a cut during the field-dressing process, gloves may
lessen the severity of the cut as well as protect pre-existing wounds from exposure to the
organism. Secondly, prior hunter education was critical in the second case, because the
hunter recognized the deer as infected, and specifically mentioned his exposure each time
he sought medical treatment. Thirdly, efforts to raise the index of suspicion of the
medical community regarding cutaneous and other occupational or recreational exposures
to bovine tuberculosis continues to be important, so that appropriate diagnoses can be
made. Finally, in both cases, the initial negative tuberculin skin test complicated the
diagnostic efforts. It is an ongoing challenge to ensure that both public and private

providers appropriately apply and interpret the tuberculin skin test.

75

REFERENCES.

Centers for Disease Control and Prevention. Tuberculin Skin Testing Factsheet.
[factsheet on the intemet]. Updated April 2006. [cited 2007]. Available from:
http://www.cdc.gov/nchstp/tb/pubs/tbfactsheets/Z50140.htm.

Centers for Disease Control and Prevention. Human tuberculosis caused by
Mycobacterium bovis - New York City, 2001-2004. MMWR. 2005;54;605-608.

Cowen LS, Mosher L, Diem L, Massey JP, Crawford J T. Variable—number tandem repeat
typing of Mycobacterium tuberculosis isolates with low copy numbers of 1861 10 by
using mycobacterial interspersed repetitive units. J Clin Microbiol. 2002;40(5):1592-
1 602.

Cowen LS, Diem L, Brake MC, Crawford J T. Transfer of a Mycobacterium tuberculosis
genotyping method, Spoligotyping, from a reverse line-blot hybridization, membrane-
based assay to the Lurninex multianalyte profiling system. J Clin Microbiol.
2004;42(1):474-477.

Dankner WM, Waecker NJ, Essey MA, Moser K, Thompson M, Davis CE.
Mycobacterium bovis infections in San Diego: a clinicoepidemiologic study of 73
patients and a historical review of a forgotten pathogen. Medicine. 1993;72:11-37.

Enarson DA, Rieder HL, Meslin FX, Cosivi O. The importance of Mycobacterium bovis
to the tuberculosis epidemic in humans. In Thoen CO and Steel JH, editors.
Mycobacterium bovis infection in Animals and Humans. Ames, Iowa: Iowa State
University Press;1995. p. xxii-xxv.

Kwara A, Schiro R, Cowan LS, Hyslop NE, Wiser MF, Harrison SR, Kissinger K, Diem
L, Crawford J T. Evaluation of the epidemiologic utility of secondary typing methods
for differentiation of Mycobacterium tuberculosis isolates. J Clin Microbiol.
2003;41(6):2683-2685.

McKenna MT, McCray E, Onorato I. The epidemiology of tuberculosis among foreign-
bom persons in the United States, 1986-1993. N Engl J Med. 1995;332:1071-1076.

Michigan Bovine Tuberculosis Eradication Project Activities Report and Conference
Proceedings. Proceedings of the Bovine Tuberculosis Eradication Project
Conference; 2005 June 7-8; Lansing, Michigan, p. 11. Available from:
http://www.michigan.gov/documents/MDA_2005_BTB_Report2_148 142_7.pdf.

Michigan Department of Natural Resources. 2006 Michigan Hunting and Trapping Guide
Bovine Tuberculosis Information. Lansing, MI. 2006. Available from:
ht_tp://www.mi.gov/emergingdiseases/O. l 607,7-1 86-25 804 25 81 1-126027--,00.html.

Mycobacterium bovis international database [database on the intemet]. Brighton, United
Kingdom: University of Sussex. c2005. Available from: http://www.mbovis.org.

76

National TB Controllers Association / CDC Advisory Group on Tuberculosis
Genotyping. Guide to the Application of Genotyping to Tuberculosis Prevention and
Control. Atlanta, GA: US Department of Health and Human Services, CDC; June
2004. Available from: http://www.cdc.gov/nchstp/tb/genotyping/toc.htrn.

O’Brien DJ, Schmitt SM, Fitzgerald SD, Berry DE, Hinkling GJ. Managing the wildlife
reservoir of Mycobacterium bovis: the Michigan, USA, experience. Vet Microbiol.
2006;112:313-323.

Tappeiner G, Wolff K. Tuberculosis and other mycobacterial infections. Fitzpatrick TB,
Freedberg IM, Eisen AZ, Wolff K, Austen KF, Goldsmith LA, Katz SI. editors. 5th
edition. In: Dermatology in General Medicine. New York: McGraw-Hill, 1993: p.
2370-2391.

Wigle WD, Ashley MJ, Killough EM, Cosens M. Bovine tuberculosis in humans in
Ontario: the epidemiologic features of 31 active cases occurring between 1964 and
1970. Am Rev Respir Dis. 1972;106:528-534.

Wilkins MJ, Bartlett PC, Frawley B, O’Brien DJ, Miller CE, Boulton, ML.
Mycobacterium bovis (bovine TB) exposure as a recreational risk for hunters:
results of a Michigan Hunter Survey, 2001. Int J Tuberc Lung Dis.
2003;7(10):1001-1009.

Yang Z, Barnes PF, Chaves F, Eisenach KD, Weis SE, Bates JH, Cave MD. Diversity of
DNA fingerprints of Mycobacterium tuberculosis isolates in the United States. J
Clin Microbiol. 1998;36(4):1003—1007.

77

CHAPTER 4
ABSENCE OF MYCOBACTERIUM BOVIS INFECTION IN DOGS AND CATS
RESIDING ON INFECTED CA'I'I'LE FARMS - MICHIGAN, 2002

ABSTRACT

A cross-sectional field study was performed to evaluate dogs and cats living on
farms with Mycobacterium bovis (bovine TB) infected cattle. Our purpose was to
determine pet infection status and assess their risk to farm families and/or tuberculosis-
free livestock. Nine farms participated in the study. Data and specimens were collected
from eighteen cats and five dogs from nine farms. ELISA testing for M. bovis and M.
avium was conducted. Fifty-one biologic samples were cultured; all were negative for M.
bovis, although other Mycobacterium species were recovered. No radiographic, serologic
or skin test evidence of mycobacterial infection was found. These negative results may
be due to the low level of bovine TB infection in the cattle and their infrequent exposure
to pets residing on the same farm. We found no evidence that pets residing on bovine
TB-infected Michigan cattle farms pose a risk to humans or bovine TB-free livestock,

however precautionary advice was provided.

INTRODUCTION

Causing disease in a wide range of mammals, M. bovis has the broadest host
range of the members of the M. tuberculosis complex (0’ Reilly, 1995) and is well
established as a zoonotic disease. Historically, milk-bome transmission has been
responsible for most human M. bovis infections. In developed countries, this route of

transmission was virtually eliminated following the widespread adoption of pasteurized

78

milk. M. bovis has recently become established in the wild white-tailed deer population
of the northeast portion of Michigan’s lower peninsula. Identified in 1994 in a hunter-
harvested white-tailed deer, Mycobacterium bovis has been found in 449 deer (out of
105,885 tested) through 2002. From 1996-2002, several additional species have been
tested and found positive for M. bovis infection in Michigan including: coyotes (19),
raccoons (8), black bear (7), bobcat (4), red fox (3), opossum (2) and elk (2) and one
semi-feral domestic cat (Summary of Michigan Wildlife Bovine Tuberculosis
Surveillance, 2007; Kaneene, 2002). At the time of this study (August 2202), 23 infected
cattle herds had been found (Summary of gross and histologic examination and
mycobacterial culture of tuberculosis cases in cattle and captive deer in Michigan 1996 —
2007, database on the Internet). The wide diversity of infected species suggests several

potential new routes of transmission for M. bovis from animals to humans.

Pet to Cattle, Cattle to Pet

Scientific literature describing the role of domestic pets in the transmission of M.
bovis on the farm (livestock to pet, pet to livestock) is fairly limited and quite dated.
While uncommon in both dogs and cats, historic data suggests that dogs were more likely
to be infected with M. tuberculosis following exposure to infected humans, while cats
were more likely infected with M bovis with exposure assumed to be related to the
consumption of contaminated animal products (Bim, 1965). Historically, farm cats and
dogs were at very high risk of acquiring M. bovis fi'om infected cattle; 4 of 9 dogs and 24
of 52 cats were affected after exposure to positive cattle in a Pennsylvania study (Snider,
1971). It is therefore feasible that pets could play a role in the maintenance of M. bovis

on a farm (Greene, 1998), however, literature describing pet transmission to cattle is

79

hypothetical (McLaughlin, 1974) or limited to references fiom Eastern Europe in the

1950’s and 60’s (Beinhauer, 1958; Milbrant, 1960; Pavlas, 1965; Schliesser, 1965).

Transmission from pets to humans

Literature describing the role of pets in transmission of M. bovis to humans is also very
limited, although transmission would again be biologically plausible. Early necropsy
studies (1930-1965) revealed a tuberculosis prevalence ranging from 2.0 to 13% in cats
and 0.4% to 2.0% in dogs (Snider, 1971). There is no evidence that dogs and cats have
transmitted M. bovis infection to humans; only one inconclusive cat-to-human reference
was found (Isaac, 1983). In Michigan, wild carnivores and omnivores are considered
dead-end hosts for M. bovis. These animals are most typically exposed to infection via
the consumption of infected deer carcasses, thus resulting in a gastrointestinal clinical

presentation with limited potential for transmission to people or other animals (Bruning-

Fann, 2001).

Clinical presentation

Clinical findings in dogs infected with Mycobacterium tuberculosis include:
anorexia, loss of body weight, lethargy, vomiting and leukocytosis; radiography revealed
pleura] and pericardial effusion, ascites, and hepatomegaly (Si-kwang, 1980). In cats, the
most common clinical sign associated with M. bovis infection was a moist skin lesion (de

Lisle, 1990). Additional clinical signs included lymphadenopathy (primarily the head

80

 

and mesenteric lymph nodes) and liver, spleen and lung lesions in generalized cases
(deLisle, 1990; Kaneene, 2004). It is also notable that in the Pennsylvania study,
tuberculosis infection frequently occurred without apparent clinical signs in the pets

(Snider, 1971).

Pets and the Control of bovine TB

The regulatory response following the detection of M. bovis infection in a herd of
cattle is to place the farm under quarantine. The herd is then either scheduled for
depopulation, or placed on a rigorous testing schedule to remove TB responders fi'om the
herd (USDA, 1989). Federal recommendations include removing other susceptible
livestock and pets fiom the farm during the cattle depopulation phase (Clifford, 2006).
However, regulatory officials in Michigan have not included pets in their depopulation
efforts.

This study assesses the potential role that dogs and cats may play in the
transmission of M. bovis to livestock and humans, and evaluates their possible role in the
epidemiology of the current Michigan outbreak. To accomplish this objective, we
evaluated the exposure and bovine TB-infection status of the dogs and cats living on
farms where cattle had recently been diagnosed with M. bovis. Pet owners on these farms
were also offered advice on how to prevent pet exposure to M. bovis and how to

minimize human exposure to potentially infected dogs and cats.

METHODS

Farm enrollment

81

From October, 1997 until August, 2002, 23 Michigan cattle farms were found to
be infected with M. bovis and were placed on a control program by the Michigan
Department of Agriculture. Our study took place in June and August 2002 and attempted
to include all recently or currently infected farms. All farms were located in the northern
portion of the lower peninsula of Michigan. Repeated attempts were made to contact the
owners of all 23 farms to invite participation in the study. Phone calls were attempted

initially, followed by several on—farm visits if phone contact was not successfirl.

Pet enrollment

A pet was considered eligible for inclusion in the study if it was >6 month of age
and resided on the farm when infected cattle were present. All cats including “barn”,
“feral,” and “indoor only” cats were eligible for the study. Written informed consent was
obtained from the pet owner for each specific pet and each clinical procedure. History
information obtained regarding each pet included age, gender, physical description, range
(cats - indoor only, indoor/outdoor, outdoor only; dogs - tied, loose, able to wander off
the farm), diet, raw milk exposure, time living on farm, exposure to cattle (share barn),
vaccination status and medical history. Live traps were used if necessary for outside cats.
If the owner desired, the pets were spayed or neutered as well. The pets were returned to
the farm within two days. If the owner did not wish to have the dog or cat returned to the

farm, consent for euthanasia was obtained.

Clinical exam and specimen collection

82

The clinical exam and sample collection took place at a local veterinary clinic.
Procedures were performed by a single veterinarian to ensure consistency. Sedation was
used at the clinician’s discretion. For both cats and dogs, the protocol included a physical
exam, radiographs of the chest and abdomen, fine-needle aspirate of any enlarged
superficial lymph nodes, the collection of rectal and oral swabs and a 5m] blood sample.
For cats, 3 combined F eLV and F IV ELISA test was done. Remaining serum was flown
and sent to Dr. C. Thoen’s Laboratory at the College of Veterinary Medicine, Iowa State
University, Ames, Iowa, USA for comparative ELISA (M. bovis and M. avium) (Thoen,
1980) testing. For dogs, 0.1 ml of 250 TU PPD was placed intradermally in the inner
surface of the pinna, with interpretation of the skin test made by the researcher within 48-
72 hours (Greene, 1998). If the owner consented to euthanasia of unwanted feral
animals, the above protocol was followed with the exception of the collection of the fine
needle aspirate and the fecal and oral swabs. The animals were euthanized at the clinic
and transported on ice the next day to the Michigan State University, Diagnostic Center

for Population and Animal Health, East Lansing, MI.

Necropsy protocol

Necropsies were performed the day following euthanasia. The necropsy included
gross examination of all tissues, and the collection of the following tissue pools for
mycobacterial culture: cranial (parotid, submandibular & retropharyngeal) and thoracic
(mediastinal and tracheo-bronchial) lymph nodes and lungs, abdominal lymph nodes
(mesenteric & ileo-cecal), abdominal viscera (spleen, liver, kidney), small and large

intestine. The following tissues were fixed in formalin and examined histologically:

83

brain, cranial lymph nodes, tonsil, trachea, lung, thoracic lymph nodes, heart, spleen,
kidney, liver, pancreas, adrenal gland, abdominal lymph nodes, small and large intestine.
Ziehl-Neelsen acid fast staining was applied only to slides exhibiting lesions suggestive

of mycobacteriosis on the histological exam.

Radiological exam

The radiographs were examined by a veterinary radiologist, Radiology
Department at the Michigan State University, College of Veterinary Medicine, for
evidence of mycobacterial infection. The radiologist was given only the animal’s age and
study identification number. The lung fields were to be examined for evidence of
mycobacterial infection, and the thorax and abdomen were examined for signs of

lymphadenopathy.

Microbiology and strain typing

Mycobacterial culture and identification was performed at the Michigan
Department of Community Health, Bureau of Laboratories, Lansing, MI. Recommended
procedures were followed for specimen digestion, concentration and examination (Kent,
1985). Sediment of concentrated specimens was examined microscopically for acid-fast
bacilli. Sediment of the specimens was then re-suspended by the addition of 1.5 mL of
PBS solution, and aliquots were inoculated onto a slant that contained Lowenstein-Jensen
medium (Lowenstein-Jensen BB20909, Becton-Dickinson, Sparks, MD), onto a slant that
contained a Middlebrook-based medium (Middlebrook 7H11S, Becton-Dickinson,

Sparks, MD) and into a vial that contained broth for microbial culture (Bactec 12B broth

84

vial, Becton-Dickinson, Sparks, MD). Media were examined for growth at least weekly
for 8 weeks. Acid-fast bacteria were tested by use of a genetic probe (Accuprobe, Gen-
Probe, San Diego, CA) (Reisner, 1994) to determine whether the bacteria were members
of the M. tuberculosis complex. Biochemical testing and high performance liquid
chromatography were used to differentiate M. bovis from other members of the M.
tuberculosis complex and to speciate other mycobacteria (Kent, 1985; Butler, 1991;

Metchock, 1995).

Determination of exposure period

We estimated the minimum period during which the dog or cat could have been
exposed to infected cattle as the difference between the first date when the cattle on the
farm tested positive for bovine TB using the caudal fold skin test results and the date
when the infected cattle were depopulated or the farm was placed on a herd testing and
removal plan. Next, the age of the pet at the time of study enrollment was used to
determine the number of months during which the pet and the infected cattle both resided
on the farm. This estimate is considered the minimum exposure duration, because the
cattle may have been positive for months to years prior to being tested and found to be
positive for bovine TB. The exposure period became progressively shorter as the bovine

TB eradication efforts in Michigan became more efficient at early detection.

RESULTS
Twenty-three farms had been identified as Bovine TB positive by August 2002.

After numerous attempts to contact each farm owner, 21 (91%) farm owners were

85

successfully contacted and invited to participate in the study. Nine (43%) of the 21
contacted farmers had no dogs or cats eligible for inclusion. Twelve (57%) had eligible
pets, of which nine (75%) agreed to participate (Figure 4.1). Eighteen cats and five dogs
were enrolled from these nine farms (7 beef, 2 dairy). Characteristics including age,

gender, diet, housing and exposure for enrolled dogs and cats are summarized in Table

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

  
     
   

 

4.1.
23 Bovine TB
positive farms*
21 Farms 2 Farms unable
contacted to contact
9 Farms _ No 12 Farms - Have
eligible pets eligible pets
9 Farms agree 3 Farms decline
to participate to participate

 

 

 

 

 

 

 

*Number of positive farms as of 8 August 2002

Figure 4.1 : Flow diagram to show how participating farms were selected

Table 4.1 : Summarized characteristics of study participants by species.

 

 

Characteristic Cats (N=18) Dogs (N=5)
Gender 11 Male (61%) 2 Male (40%)
Average age (yrs) 4.1 (range 1.0-12.5) 6.1 (range 2.0-11.5)
Routinely fed Yes n=15 (83%) Yes n=5 (100%)
Fed raw milk Yes n=5 (28%) Yes n=0 (0%)

86

Table 4.1 (cont’d)
Outdoor only Yes n=12 (67%) Yes n=4 (80%)
Known or likely to

have shared barn

with infected cattle Yes n=18 (100%) Yes n=0 (0%)

Average exposure
period* (mos) 2.3 (range 1.0 -7.0) 4.0 (range 2.0-8.0)

 

*Calculated as the minimum possible exposure period

Cats

Only four cats (22%) had ever been vaccinated (for any disease) and only one cat
was current on its vaccines. All cats were F IV negative; two (11%) cats were FeLV
positive. The two F eLV positive cats were euthanized and a full necropsy performed.
The 18 cats suffered fiom the expected range of barn cat ailments: earmites/otitis extema
5 (28%), bloated abdomen 3 (17%), missing hair/poor haircoat/scabby skin 3 (17%),
tracheitis 2 (11%), enlarged submandibular lymph nodes 2 (11%), conjunctivitis 2 (11%),
runny eyes, poor teeth, congestion of the lungs, and diarrhea (1 each). Sixteen oral swabs
and 16 fecal swabs were submitted for mycobacterial culture (two per live cat). In
addition, eight pooled organ samples were submitted for culture (four per each of the two
euthanized cats). All culture results were negative for M. bovis; one fecal culture was
positive for M. avium complex. Radiographs of the heart and lungs were found to be
unremarkable for all 18 cats; no signs of lymphadenopathy in the abdomen or thorax
were noted. Gross pathological and histological examination of the two euthanized cats

revealed no evidence of mycobacterial infection. Three cats tested positive for M. avium

87

at the 1:160 dilution, two of these cats also tested positive for M. bovis but at less than the

1:160 dilution and were assumed to be cross-reacting with M. avium.

Dogs

All dogs were allowed to run loose on the farm and presumably had substantial
contact with the cattle. No dogs showed noticeable or measurable TB skin test response
at 48 — 72 hours. An oral swab and a fecal swab from each of the five dogs were
submitted for mycobacterial culture (two per dog). All culture results were negative for
M. bovis. Two fecal cultures were positive for Mycobacterium species (Group IV
unclassified). Radiographs of the heart and lungs were found to be unremarkable for all
five dogs, comments include: mild right loss of cranial waist (n=1) and widened
mediastinum due to fat, loss of cranial cardiac waist, mild right heart enlargement (n=l).
No signs of lymphadenopathy in the abdomen or thorax were noted. We detected
negative responses on the ELISA test for all five dogs for the M. bovis and M. avium PPD

antigens.

DISCUSSION

The herds on the participating farms had a low prevalence of cattle infected with
M. bovis. Only 14 of the 869 (1.6%) cattle tested were either suspect or positive using
the comparative cervical test. Following necropsy of all comparative cervical suspect
and reactor cattle, an average of less than one gross lesion per bovine (1 1/14) was found
in the cattle on the participating farms, indicating the absence of advanced, heavily

diseased cattle with the potential to shed high numbers of infectious organisms. The low

88

 

prevalence of infection in the herd and low severity/early progression of infection in
individual animals may explain the apparent lack of transmission to the dogs and cats.

During the course of the outbreak in Michigan, the control and eradication efforts
by state and federal agriculture officials intensified. Positive farms were quickly
identified by contact tracing or by area testing, and the time between diagnosis and
depopulation was shortened. Thus, the period of time during which pets were exposed to
infected cattle became progressively shorter. The detection and control efforts also
decreased the likelihood of infected cattle progressing to a clinical stage of disease where
M. bovis would be transmitted via shedding into the milk.

The historic method of infection for cats with bovine TB has been through the
consumption of infected raw milk. Five of the study cats came from the two dairy farms.
Although these five cats (28% of 18) did routinely consume raw milk, it is highly
unlikely that any of the milk cows had infection that had progressed to the point of
shedding M. bovis in their milk. Only one animal was found positive by comparative
cervical testing per dairy farm and only one gross lesion was detected in each of these
positive cows. Furthermore, none of the positive cows had lesions in the supra-mammary
lymph nodes, further reducing the likelihood of shedding of organisms into the milk. All
of our study cats were likely to have slept in the barn with the infected cattle. However,
because the cattle were not heavily infected, exposure via aerosolized droplets was
unlikely.

Wild carnivores have acquired M. bovis infection in Michigan (Bruning-Fann,
2001) presenting as gastrointestinal infection presumably as the result of consuming gut

piles left from hunted infected deer, or by scavenging or hunting infected animals. In our

89

study population, all five dogs were routinely fed by their owners, decreasing the
likelihood that they would consume deer gut piles. According to the owners, the dogs
were routinely allowed to run loose on the farm, but did not often leave the farm premise,
so exposure to gut piles would expectedly have been rare. The study dogs did not sleep
in the barns with the infected cattle so aerosol transmission is also unlikely.

Transmission of Mycobacterium species from an infected dog has never been
documented. Carnivores are most likely to be infected via consumption of infected milk
or meat and present with gastrointestinal infection. Thus cats and dogs are generally felt
to be less likely to transmit the disease unless the disease progresses to a systemic
infection due to suppression of the immune system. Four out of five of our study dogs
were strictly outdoor dogs and all were in fair to good health, making them a very low
risk for clinical disease and shedding, even if they had become infected.

Cats pose a higher transmission risk to both humans and cattle than dogs for
several reasons: they have a closer relationship with both cattle (sharing the barn,
consuming raw milk) and with humans (more likely to be indoor/outdoor and sleep in
same bed as humans), they have recently been proven scavengers (Ragg, 1995) and they
are susceptible to common viruses, feline leukemia virus (F eLV) and feline
immunodeficiency virus (FIV), which specifically compromise their immune system. An
immunocompromised cat is more susceptible to infection in general, and a correlation
between FIV, M. bovis infection and clinical disease has been recently hypothesized
(Moines, 2000). Thus, cats infected with FeLV or FIV and exposed to M. bovis could

pose a much higher risk to human owners (and cattle) than an immuno-competent cat, as

90

the disease is more likely to progress clinically, increasing the likelihood of transmission
to others.

Diagnosis of M. bovis in live dogs or cats is very difficult, and our study protocol
included all non-invasive procedures available at the time. Only two cats were offered
for post-mortem exam; both were positive for FeLV, perhaps making them the best

candidates for M. bovis isolation if it were present.

CONCLUSION
In the final analysis, no evidence was found to indicate the transmission of M.

bovis from infected cattle to farm dogs or cats. The likelihood of dog and cat infection

 

Pl-I"

was judged to be minimal due to a low risk of cattle exposure, a low expected exposure
dosage and a relatively short duration of exposure to the infected cattle. In Michigan,
even if a farm dog or cat were to become infected, its potential to transmit infection to

humans or cattle is estimated to be very low.

Recommendations

Despite the low risk of infection of pets and transmission from pets, the following
prevention recommendations were made to pet owners on the farms infected with bovine

TB:
0 Do not feed pets raw milk.
0 Keep house cats strictly in the house and barn cats out of the house.

0 If barn cats are allowed into the house, keep them away from your face, especially

if they are ill.

91

0 Do not allow dogs to roam freely.

0 Keep pets healthy (fed and vaccinated) because an ill or weak animal is more
susceptible to infection with Bovine TB and more likely to progress to clinical
disease if infected.

In addition, each farm owner is strongly encouraged to have family and employees skin
tested for possible Mycobacterium tuberculosis complex exposure on an annual basis.
Regulatory veterinarians should carefully assess the health status of pets on
infected cattle farms and seriously consider following the federal recommendations to
depopulate pets that have been heavily exposed to infected cattle. Cattle owners should
clearly understand that pets do pose a health threat, albeit remote, to their family and to
TB free livestock purchased to re-populate the farm. Because skin testing in both dogs
and cats is unreliable, and infected pets may be asymptomatic, the development and use
of reliable ante-mortem tests should be considered as an in—vivo testing alternative for
domestic pets on M bovis infected farms. In fact, a study by several of the authors is
currently under way evaluating several different ante-mortem assays for bovine

tuberculosis detection in cats.

92

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Beinhauer W. Cats as carriers of tuberculosis in a cow shed. Deutsch Tieraerztl Wschr.
1958;65:271.

Bim KJ, Clegg F G, Mason JA. Canine Tuberculosis. Vet Rec. 1965;77(45):1341-1342.

Bruning-Fann CS, Schmitt SM, Fitzgerald SD,Fierke J S, Friedrich PD, Kaneene JB,
Clarke KA, Butler KL, Payeur JB, Whipple DL, Cooley TM, Miller JM, Muzo
DP. Bovine Tuberculosis in Free-
Ranging Carnivores fi'om Michigan. J Wildl Dis. 2001;37(1):58-64.

Butler WR, Jost KC, Kilbum J O. Identification of Mycobacteria by high performance
liquid chromatography. J Clin Microbiol. 1991(29):2463-2472.

Clifford JR. Instructions and Recommended Procedures for Conducting Tuberculosis
Tests in Cattle and Bison. Washington, DC: United States Department of
Agriculture, Animal Plant Health Inspection Service, Veterinary Services, 2006.
Veterinary Services Memorandum No: 552.15

de Lisle GW, Collin DM, Loveday AS, Young WA, Julian AP. A report of tuberculosis
in cats in New Zealand and the examination of strains of Mycobacterium bovis by
DNA restriction endonuclease analysis. New Zealand Vet J. 1990;38(1): 10-13.

Greene CE, Gunn-Moore DA, Greene CE. Mycobacterial Infections: Tuberculous
Mycobacterial Infections. In: Infectious Diseases of the Dog and Cat.
Philadelphia: W.B. Saunders Company, 1998. p. 313-321.

Isaac J, Whitehead J, Adams JW, Barton MD, Coloe P. An outbreak of Mycobacterium
bovis infection in cats in an animal house. Aust Vet J. 1983; 60(8):243-245.

Kaneene JB, Bruning-Fann CS, Dunn J, Mullaney TP, Berry D, Massey JP, Thoen CO,
Halstead S, Schwartz K. Epidemiologic investigation of Mycobacterium bovis in a
population of cats. Am J Vet Res. 2002;63(11):1507-1511.

Kent PT, Kubica, GP. Public health mycobacteriology. A guide for the level HI
laboratory. Atlanta (GA): United States Department of Health and Human
Services; 1985.

McLaughlin AR, Moyle AI. An epizootic of bovine tuberculosis. J Am Vet Med Assoc.
1974;164(4):396-397.

Metchock BG, Nolte F S, Wallace J W, Jr. Mycobacterium. In: Manual of Clinical

Microbiology. Washington, DC: American Society for Microbiology Press,
1995:400-437.

93

Milbrant N, Roemmele 0. Cat as cause of tuberculosis reinfection of dairy herd. Deutsch
Tieraerztl Wschr. 1960;67: 17.

Moines RJ, Cranwell MP, Pahner N, Inwald J, Hewinson RG, Rule B. Bovine
tuberculosis in domestic cats. Vet Rec. 2000; 146:407-408.

O'Reilly LM, Dabom CJ. The epidemiology of Mycobacterium bovis infections in
animals and man: a review. Tuber Lung Dis. 1995;76 Suppl 1:1-46.

Pavlas MH, K. Vitkovic, L. Role of cats in the dissemination of tuberculosis amoung
cattle. Veterinarstve. 1965;15:389.

Ragg JR, Moller H, Waldrup KA. The prevalence of bovine tuberculosis (Mycobacterium
bovis) infections in feral populations of cats (F elis catus), ferrets (Mustelafuro)
and stoats (Mustela erminea) in Otago and Southland, New Zealand. New
Zealand Vet J. 1995;43(7):333-337.

Reisner BS, Gatson AM, Woods GL. Use of the Gen-Probe Accu-Probes to identify
Mycobacterium avium complex, Mycobacterium tuberculosis complex,
Mycobacterium kansasii and Mycobacterium gordonae directly from BACTEC
TB broth culture. J Clinical Microbiol. 1994;32:2995-2998.

Schliesser T, Bachmainer, K. Cat with bovine tuberculosis transmitted disease to cattle.
Mh Prakt Tierheilk. 1957;6z23.

Si-kwang L, Weitzman 1, Johnson GG. Canine Tuberculosis. J Am Vet Med Assoc.
1980;177:164-167.

Snider WR, Cohen D, Reif J S, Stein SC, Prier JE. Tuberculosis in canine and feline
populations. Study of high risk populations in Pennsylvania, 1966-1968. Am Rev
Respir Dis. 1971 ;104(6):866-876.

Snider WR. Tuberculosis in canine and feline populations. Review of the literature. Am
Rev Respir Dis. 1971;104(6):877-887.

Summary of Michigan wildlife bovine tuberculosis surveillance. [database on the
Internet] State of Michigan, Emerging Disease Issues in Michigan (MI, USA).
c2001 [updated 24 Apr 2007; cited 2007 Nov 6]. Available from:
http://www.michigmov/documents/emergjngdiseases/WildlifeTBSurveillanceS

ummm 211947 7.pdf.

Summary of gross and histologic examination and mycobacterial culture of tuberculosis
cases in cattle and captive deer in Michigan 1996 - 2007. [database on the
Internet] State of Michigan, Emerging Disease Issues in Michigan (MI, USA).
02001 - [cited 2007 Nov 6]. Available from:

94

http://www.michi gan.gov/docmnents/emergingdiseases/TBp_osLablg_2-
07_FOR_THE_WEB_16751 1 7 187838 7.doc.

Thoen CO, Mills K, Hopkins MP. Enzymne—linked protein A: an enzyme linked
immunosorbent assay reagent for detecting antibodies in tuberculous exotic
animals. Am J Vet Res. 1980;41:833-835.

United States Department of Agriculture. Bovine Tuberculosis Eradication: Uniform

Methods and Rules Effective February 3, 1989: US. Government Printing Office:
1992-621-485 (41699);l989.

95

CHAPTER 5
VETERINARIAN INJURIES ASSOCIATED WITH BOVINE TB TESTING

LIVESTOCK IN MICHIGAN, 2001.

ABSTRACT

Determining the injury rate for working with cattle is difficult since a wide range of
persons perform a diverse assortment of procedures on cattle in highly variable
circumstances. There is also generally a lack of denominator data regarding the number
of cattle receiving each type of procedure. Testing all the cattle in an entire state with a
uniform procedure for each animal affords an opportunity to relate human injury data to a
known number of animals handled while carrying out a standardized procedure. The
objective of the current study is to capture the type and incidence density of injuries
associated with TB-testing a large number of cattle herds, and to delineate the various
factors contributing to the risk of injury. Additionally, the two known mortality events
associated with bovine TB testing in Michigan will be summarized. A survey was mailed
to all veterinarians (N=259) who had completed at least five official bovine TB herd tests
in Michigan in 2001. Collected data regarded basic demographics and health status,
work experience, veterinary specialty, and practice information. Each veterinarian was
also requested to complete a separate injury questionnaire for each injury received while
TB testing livestock in 2001. Risk ratios were calculated, based on the incidence density
of injuries per 10,000 animals tested, to compare the characteristics of the injured
veterinarians to the non-injured veterinarians. Accurate addresses were found for 247
eligible veterinarians, 175 of whom returned the survey for a participation rate of 71%

(175/247). Thirty-six veterinarians reported a total of 53 injuries (10 major, 12 minor and

96

31 self-treated). Individual veterinary characteristics and the type, cause and location of
each injury are described. The overall incidence density of injuries was 1.9 per 10,000
animals tested. Female gender (RR=3.26), having less than 10 years of practice
(RR=1.81), being employed by the government (RR=4.54), smoking (RR=5.97) and
working 50 hours or less (RR=1.87) were found to be significantly associated with a
higher rate of injury per 10,000 animals tested. The human “costs” in terms of injuries,
must be considered when decisions are made to initiate large-scale livestock disease
control programs, although these costs are more difficult to measure than the financial
costs of a budgeted control program. Effort and resources must be allocated to reduce the
number and frequency of preventable injuries, and to monitor the public health impact of

ongoing disease control efforts.

INTRODUCTION

Twenty years after obtaining the bovine TB (bTB) Accredited-free status from the
US Department of Agriculture in 1979, Michigan lost that designation to become a Non-
Modified Accredited state on June 22, 2000 joining Texas as the only other US state that
did not have Free status for bTB. Michigan's loss of Free status for bTB was due to the
recent confirmation of Mycobacterium bovis (i.e. bovine TB) infection in seven cattle
herds in the northeastern portion of the lower peninsula of Michigan. To remain in
compliance with the federal Pasteurized Milk Ordinance and the Michigan Grade A Milk
Law of 2001 (Act 266 of 2001) all dairy herds in the state (~3000 herds, ~300,000 milk
cows) were required by the Michigan Department of Agriculture (MDA) to be TB tested

within 12 months. In addition, all beef cattle (~10,000 herds, ~700,000 cattle), bison and

97

goat herds in the state were required to be tested by the end of 2003 (2000; 2004). To
meet this large scale and immediate demand for TB testing, the MDA hired federally-
accredited private veterinarians on a fee-basis to supplement the existing state and federal
veterinary field staff. The fee-basis veterinarians were hired without selection for their
current practice focus. The purpose of this study is to capture the type and frequency of
injuries in veterinarians associated with TB testing a large number of cattle, bison and
goat herds, to delineate the various factors contributing to the risk of injury, and to
summarize two known mortality events associated with bTB testing in Michigan.
Veterinary practitioners are often classified as having a primary employment
focus in companion animal practice, large animal practice or a combination of both.
Regardless of their concentration, veterinary practice presents occupational hazards from
physical, biological and chemical agents (J eyaretnam and Jones, 2000). An occupational
hazard survey found needle punctures, kicks and crush or handling injuries as the leading
cause of injury to veterinarians in large animal practices (Poole et al., 1999) while cat
bites, dog bites and needle punctures topped the list in companion animal practices (Poole
et al., 1998). A survey of AVMA members in Minnesota and Wisconsin found hands,
shoulder/arm, legs, head, back and feet to be the most frequently injured anatomic
structures (Landercasper et al., 1988). Occupational injuries of zoo veterinarians have
also been specifically studied (Hill et al., 1998), as well as practice hazards unique to
pregnant veterinarians (Moore et al., 1993). In a large Minnesota study of all licensed
veterinarians, factors found to increase the risk of veterinary injury included smoking,

lack of sleep, lifting heavy patients, inexperience, and lack of availability of assistants. In

98

contrast, participation in aerobic activities, increasing age and male gender were found to
decrease the risk of injury (Gabel et al., 2002).

Unlike prior veterinary injury research focusing on practice specialty or
demographic characteristics such as age and gender, this study investigates injuries
associated with one particular task, the TB-testing of livestock. This study is part of a
larger effort to assess the human health risks associated with the current bovine TB

outbreak in Michigan (Wilkins et al., 2003, 2008).

METHODS
Animal testing

At the time of the study, cattle, bison and goats were screened for TB using the
caudal fold test (CF T) with intradermal placement of M. bovis antigen under the tail head.
A CFT is considered positive at 72 hours when skin thickness of the injection site is
measured at 4 mm or more. If positive, a comparative cervical test (CCT) was performed
by a state or federally employed veterinarian (hereafter referred to as “regulatory”
veterinarians), placing separate intradermal injections of M. bovis and M. avium 12.5 cm
apart on the neck. A CCT was considered positive if the skin thickness at the M. bovis
injection site is 4 mm greater than the M. avium site (Clifford, 2006).

To properly place and interpret both the CCT and the CFT test, the animal must
be adequately restrained, often requiring the use of veterinarian-supplied heavy
equipment such as portable chutes and panels. For an official test (CFT or CCT) each
animal must be handled twice, separated by 72 hours. For this study, an animal “tested”

means the animal was handled twice, and refers to both caudal fold and comparative

99

cervical tests. The term “herd test” is non-specific and may correctly refer to the testing
of a single animal or alternatively may refer to the testing of hundreds of animals
comprising an entire herd.

Study population

The study population included all veterinarians who had completed at least five
official TB herd tests in Michigan in 2001. The list of official herd tests was obtained
from US. Department of Agriculture, Animal and Plant Health Inspection Service,
Veterinary Services - Michigan. The mailing addresses for all veterinarians licensed in
Michigan were purchased fi'om the Bureau of Health Professions, Michigan Department
of Community Health. The lists were combined to create a mailing list for 259 eligible
veterinarians, who collectively performed 9,326 herd tests.

Data collection

The first survey instrument was mailed in September 2002. It was resent to non-
responders, with a new cover letter, three weeks later. Available addresses were
inaccurate for 12 veterinarians, so 247 received the survey. Of these, 175 veterinarians
returned the survey for a participation rate of 71% (175/247).

The survey was pilot-tested on 7 veterinarians to ensure the clarity of each
question and the availability of adequately descriptive answer options. The survey
questions were primarily close-ended or short fill-in-the-blanks. There was one open-
ended question to allow the veterinarian the option to “in your own words, describe the
circumstances leading to the injury and the injury itself ’. The survey took between 5 and

25 minutes to complete, depending on the number of injuries reported.

100

The following information was collected for each injury: severity, month of
occurrence, when in the course of the farm visit the injury occurred, availability of
assistants, location on body, type and cause of the injury, type of animal or equipment
involved, contributing factors (animal behavior, facilities, weather, assistants, personal
issues, whether the current injury was a re-aggravation of a prior injury, as well as the
preventability of the injury. Microsoft Excel and SPSS 12.0 (Chicago, IL) were used to
manage the data.

Classification of Injury

Veterinarians were asked to categorize their injuries as major, minor and self-
treated. Maj or injuries were defined as injuries that required immediate treatment
(hospitalization, outpatient visit to an emergency room or urgent care center) within 4
hours of incident and/or resulted in over 16 hours of lost work time. Minor injuries were
defined as requiring non-immediate treatment for the injury from a physician or human
health professional within seven days of the incident and/or 4-16 hours of lost work time.
The self-treated category included treatment provided to themselves or received from
their veterinary staff and resulted in <4 hours lost work time. Because the veterinarians
had such a propensity to self—treat -- even severe injuries (Landercasper et al., 1988), their
reluctance to seek human medical advice, and to continue working while injured
(indicated by our data), the injury categories were collapsed for the final analysis, making

our final definition consistent with prior work (Landercasper et al., 198 8).

101

ANALYSIS

Because the number of herds and number of animals tested did not follow a
normal distribution, the Mann-Whitney U test was used to compare responding
veterinarians to non-responders on the basis of the median number of herd tests
completed, and the median number of animals tested. The injury details and veterinarian
characteristics are reported by both number and percent. Because several veterinarians
reported more than one injury and because each veterinarian did not test the same number
of animals, incidence density (number of injuries per animal tested) was the most
appropriate epidemiologic measure to describe our results. To compare the
characteristics of the injured veterinarians to the non-inj ured veterinarians, a risk ratio
was calculated based on the incidence density of injuries per 10,000 animals tested, using
Epi Info 6.04b (Centers for Disease Control and Prevention, Atlanta, GA). Factors found
to be significantly contributing to the risk of injury in the incident density analysis were
included in a bivariate analysis using )8 testing to further examine inter-relationships
between risk factors. Additionally, a portion of these risk factors were examined to
determine their direct relationship with the likelihood of injury (as a binomial outcome),

as opposed to their contribution to the rate of injury (incidence density analysis).

RESULTS

Responders vs. Non-responders

Responding veterinarians tested a median number of 28 herds (5th percentile = 5; 95th

percentile = 84.4) compared to 20.5 herds (5th percentile = 5; 95th percentile = 66.7) for

102

non-responding vets; the difference was not found to be significant (p = 0.197 using
Marm-Whitney U test). Responding veterinarians tested a median of 1055 animals (5th
percentile = 32.7 ; 95 percentile = 4769.3) compared to 1006 (5th percentile = 28.5; 95
percentile = 3608.8) for nonresponders; the difference was not found to be significant
(p=0.434, by Mann-Whitney U test). No additional variables were available for

comparison.

Summary of Injuries

Thirty-six veterinarians reported a total of 53 injuries (10 major, 12 minor and 31
self-treated). Sixty-one percent of the injuries were caused by direct contact with
animals; the remaining 39% were caused by equipment use or failure. Only 13.3% of the
injuries were a re-aggravation of prior injuries, and the veterinarians thought 81.1% of
the injuries could have been prevented. During the course of the farm visit, the majority
(75%) of the injuries occurred when placing or reading the TB test or ear tagging the
animal, followed by preparing for/ setting up equipment for TB testing (15.4%) and
finally, disassembling or cleaning TB equipment (5.8%). Hands (28.6%), legs (21.4%),
thorax/ribs (15.7%) and arm/shoulder (12.9%) were the most common location of the
injury on the body followed by the head (5.7%), back, foot, abdomen/intemal organs
(4.3% each), nose and neck (1.4% each) with many veterinarians listing more than one
location for a single injury (n = 70). Strains/sprains (30.2%) and abrasion/contusion
(30.2%) were the most common types of injury reported, followed by open

wound/laceration (15.1%), fracture (11.3%), allergy/initant (5.7%), spinal cord injury,

103

internal injury, and “other” described as a hematoma behind the kneecap (1.9% each).
The injuries were most directly caused from being kicked (17.9%) or crushed/pinned by
animal (17.9%), pushed/head butted by animal (14.3%), or pinched/crushed by
equipment (10.7%) (Table 5.1). To capture the factors contributing to the injury,
veterinarians were encouraged to indicate as many contributory factors as needed to
describe the incident (n = 104). The main animal behavior factors include unusually
aggressive (7.7%) or unusually frightened behavior (7.7%) on the part of the animal.
Facility-related factors include inadequate animal restraint (10.6 %) or inappropriate
workspace (7.7%). The main weather-related factors include rain (4.8%), and cold
temperature (4.8%). The main assistant-related factors include too few (9.6%) or
inexperienced (8.7%) help. Personal issues include feeling rushed or in a hurry (7.7%) or
overly tired (2.9%) (Table 5.2). The primary animals (n=38) involved with the injury
include: beef cow (42.1%), dairy cow (29.0%), beef other (7.9%), beef bull, dairy other

(5.3% each), and dairy bull, bison bull, bison cow, and goat (2.6% each).

Table 5.1 : Cause of injury while TB testing livestock in Michigan, 2001.

 

 

N %
Kicked 10 17.9
Crushed/pinned by animal 10 17.9
Pushed/headbutted 8 14.3
Pinched/crushed by equipment 6 10.7
Needle stick 4 7.1
Lifting/moving equipment 4 7.1
Slip/trip/fall 4 7.1
Lifting/pushing animal 3 5.4
Allergic/irritant* 3 5.4
Repetitive motion 3 5.4

104

Table 5.1 (cont’d)

Motor vehicle accident 1 1.8
Total 56

 

*self injected tuberculin (n=2) hornets (n=1)

Table 5.2 : Factors contributing to risk of injury while TB testing livestock in Michigan,

 

 

2001.
N %
Animal Behavior
Unusually aggressive 8 7.7
Unusually frightened 8 7.7
Extremely unpredictable 5 4.8
Unusually protective 1 1.0

Facilities

Inadequate animal restraint 11 10.6

Table 5.2 (cont’d)
Inappropriate work space 8 7.7
Poor flooring 6 5.8
Poor lighting 3 2.9
Assistants*

Too few 10 9.6
lnexperienced 9 8.7
Poor animal handling skills 4 3.8
Unhelpful (poor attitude) 2 1.9
Too many 0 0.0

105

Table 5.2 (cont’d)

Weather
Rain 5 4.8
Cold temperature 5 4.8
Hot temperature 3 2.9
Snow 2 1.9
Ice 1 1.0
Personal Issues
In hurry/felt rushed 8 7.7
Over1y tired 3 2.9
lnexperienced 1 1 .0
Poor physical condition 1 1.0
Lacked adequate training 0 0.0
Total 104

 

*lncludes help provided by testing veterinarian and help provided by

producer.

106

Characteristics of Veterinarians

The characteristics of the study population (n = 175) detailed in Table 5.3 include:
gender, age, practice type, years of practice, number of hours spent in vehicle each week,
number of days worked per week, number of hours worked per week, number of hours of
sleep per night, percentage of time spent on-call, self-assessment of health, number of
times they exercised per month (defined as brisk aerobic activity lasting 20 minutes or
more), tobacco smoking, tobacco chewing, seatbelt use, body mass index (BMI) and

percentage of time doing TB work.

Table 5.3 : Characteristics of Study POpulation — Michigan veterinarians testing five or

more livestock herds for TB in 2001.

 

 

Characteristic N %
Gender n=75
Male 141 80.6
Female 34 19.4
Age n=168
26-35 27 16.1
36-45 53 31 .5
46-55 60 35.7
56-65 22 13.1
>65 6 3.6

107

Table 5.3 (cont’d)
Practice type

Private
Government
Other
Years of Practice
<5
5%)
10-19
20-29
30-39
>39
Hours in vehicle/wk
041
54)
10-14
15-19
20-24
>24
Days worked per week
(L3
4L5
6
7
Hours worked per week
0-29
30-49

50-59
60-69
>69

n=175

160
14

n=175
21
18
51
48
30

n=175

20
45

30
12
n=175

57

99

1 8
n=175

32

58
51
26

108

91.4
8.0
0.6

12.0
10.3
29.1
27.4
17.1
4.0

19.4
11.4
25.7
19.4
17.1
6.9

0.6
32.6
56.6
10.3

4.6
18.3

33.1
29.1
14.9

Table 5.3 (cont’d)

Hours sleep per night
5

6
7
8
>8
%Time on-Call
044
54)
10-19
20-49
50-99
100
Self health assessment
Poor
Fan
Good
Exceflent
No. times exercise/mo
0
1-10
11-20
>20
Smoke
No

Yes

n=172

32
85
42

n=174

1 8
43
42
24
12
n=169

87
75
n=175
48
70
39
18
n=175
166

109

4.1
18.6
49.4
24.4

3.5

19.5
10.3
24.7
24.7
13.8
6.9

0.0
4.1
51.5
44.4

27.4
40.0
22.3
10.3

94.9
5.1

Table 5.3 (cont’d)

 

Chew tobacco n=175
No 168 96.0
Yes 7 4.0
Body Mass Index n=174
Undewveight <18.5 1 0.6
Normal 18.5-24.9 58 33.3
Overweight 25-29.9 77 44.3
Obese >29.9 38 21.8
Seatbelt use while working n=175
Always 130 74.3
Usually 33 18.9
Sometimes 5 2.9
Rarely 4 2.3
Never 3 1.7
% Time doing TB work n=175
<5% 40 22.9
5-9% 50 28.6
10-19°/o 40 22.9
20-39% 25 14.3
40—99% 12 6.9
100% 8 4.6
Incidence Density

Overall, 1.9 veterinary injuries were found per each 10,000 animals tested, or
9.3 injuries per 1000 herds tested. To compare the rate of injury between different groups

of veterinarians, the incidence density was used to generate a rate ratio (relative risk).

110

The veterinarians were compared using several different grouping variables including
gender, years of practice (<10 years vs. 10 or more years), practice type (private vs.
regulatory), hours of work per week (50 or less vs. >50), percentage of time spent doing
companion animal work (> 50% vs. 50% or less), percentage of time spent on-call (20%
or more vs. <20%), working with assistants (always and usually vs. sometimes, rarely
and never), hours of sleep per night (<8 vs. 8 or more), tobacco smoking (users vs. non
users) and chewing habits (users vs. non users), seatbelt use (always and usually vs.
sometimes, rarely and never), BMI category (obese and overweight vs. normal and
underweight) and number of herds tested (<30 vs. 30 or more). Female gender
(RR=3.26), having less than 10 years of practice (RR=1.81), being a regulatory
veterinarian (RR=4.54), being a smoker (RR=5.97) and working 50 hours or less
(RR=1.87) were found to be significantly associated with a higher rate of injury per
animal tested. All variables and 95% confidence intervals are shown in Table 5.4. No

factors were found to be significantly protective.

Table 5.4 : Veterinary characteristics and associated rate ratios of risk of injury per

animal tested (incidence density) by veterinarians TB testing livestock in Michigan,

 

 

2001.
# # Injury Rate 95%
Characteristic N* Injuries Animals Rate/ Ratio Confidence
* Tested 10,000 Intervals
Animals
All Veterinarians 172 52 269,765 1.93
Gender
31 17 34,993 4.86 3.26 1.83-5.82
Female
Male 141 35 234,772 1.49

111

Table 5.4 (cont’d)

Years of Practice

<10 Years 39

10 or greater 136
Practice Type

Regulatory 11

Private 160
Hours of Work/wk

50 or less 73

> 50 99
%Time Spent SA

>50% 68

50% or less 92

% Time on Call

20% or more 79

<20% 92
Work With Assistants

Always/Usually 91

Sometimes/Rarely/ 80
Never

Hours Sleep/Night
<8 123
8 or greater 48

19
33

12
39

25
27

31

30
22

29
23

37
15

65,107
204,658

17,080
252,235

89,371
180,394

47,820
204,41 5

120,211
147,849

144,888
122,113

202,981
65.274

2.918
1.612

7.026
1.546

2.80
1.50

1.67
1.52

2.50
1 .49

2.00
1.88

1.82
2.30

1.81

4.54

1.87

1.10

1.68

1.22

1.03-3.18

2.38 - 8.68

1.08 - 3.22

0.51 - 2.40

0.97 — 2.91

0.71 — 2.09

0.793 0.44 — 1.45

 

*Excluded three veterinarians for whom number of animals tested was missing

(one of whom reported an injury).

112

Bivariate Analysis of Risk Factors

Bivariate analysis of the factors found significant in the incidence density analysis
was conducted using )8 analysis. Four of the variables (gender, number of hours worked
per week, type of practice, and years of practice) were compared to each other, to
examine between-risk factor associations (Table 5.5). There was a strong association
between the type of practice and hours worked with private practitioners much more
likely to work 50 hours or more (61.5%) compared to regulatory veterinarians (7%) (OR
= 20.76;Cl = 2.72 — 890.81). Another significant association was found between gender
and practice type, with a higher percentage of females (57%) in regulatory positions
compared to private practice (16%) (OR 6.92; 95% CI 1.90 - 26.00). The association
between practice type and years of practice was also found to be significant with a higher
percentage of regulatory veterinarians (50%) having less than 10 years of practice
experience compared to private practitioners (20%) (OR=4.03; 95% CI 1.11-14.41).
Finally, having less than 10 years of practice was significantly associated with the female
gender (OR= 3.85; 95% CI 1.93 — 11.18). Gender and number of hours worked per
week, and years of experience and number of hours worked per week were not found to

be associated.

113

Table 5.5 : Bivariate analysis of risk factors found to be significant in the incidence

density analysis.

 

Variables Odds 95% Confidence
Ratio” Interval

Practice type by hours worked per week

<50 hrs 50 or more hrs
Government 13 1 20.76 (2.94 — 1390.131)T
Private 62 99
Practice type by gender

Female Male E
Gov/Regulatory 8 6 6.92 (1.90 — 26.00)T "
Private 26 1 35

Practice type by years of practice

<10 yrs 10 or more yrs
Gov/Regulatory 7 7 4.03 (1.11 - 14.41 )T
Private 32 129

Years of practice by gender
Female Male
<10 yrs 15 24 3.85 (1.93 — 11.18)

10 or more yrs 19 141

114

Table 5.5 (cont’d)

Hours worked per week by gender

Female Male
<50 Hrs 18 57 1.66 (0.73 - 3.76)
50 or more hrs 16 84

Hours worked per week by years of practice
<10 Yrs 10 or more Yrs
<50 Hrs 18 57 1.19 (0.55 — 2.58)

50 or more hrs 21 79

 

*ManteI-Haenszel odds ratio.

I Exact confidence limits used when expected cell size <5.

Stratified Analysis

The final step in the analysis included using x2 analysis to examine the
relationship between injury (injured yes or no) and gender, stratified by practice type, and
the relationship between injury and practice type, stratified by gender. For gender and
injury, the crude odds ratio was 2.66 (95% CI 1.07 — 6.58) with women more likely to be
injured than men. But, once stratified by stratified by practice type, the odds ratios
differed; for private practice OR = 2.87 (CI = 1.02 — 8.01), for regulatory practice OR =
1.6 (CI = 0.15 — 17.02) with women still more likely to be injured, but the association by
strata was barely, or no longer statistically significant. The adjusted odds ratio was 2.54
(95% CI 1.01 — 6.53). For practice type and injury, the crude odds ratio was 3.28 (95% CI

0.86 — 11.61) with regulatory veterinarians at higher risk of injury than private

115

practitioners. Stratified by gender, the odds ratios differed; for female regulatory
veterinarians the OR = 1.13 (95% CI 0.14 — 7.50), for males regulatory veterinarians the
OR = 5.43 (95% CI = 0.67 — 42.59), neither was statistically significant. Because gender
is an effect modifier, an adjusted odds ratio was not reported.

A closer look at the gender variable using )6 analysis revealed that females were
no more likely than males to report major injuries (odds ratio 1.04, p=0.96), but they
were more likely to report minor (OR 4.10, p=0.01) and self-treated injuries (OR 2.38,
p=0.05).

Mortality

Two mortality events associated with the current TB testing efforts in Michigan
occurred. Although not captured by the survey, they bear mentioning as they contribute
tremendously to the human cost of the control program. In September, 2000, a 60 year
old, male cattle producer was attacked and killed by a Holstein bull as he was separating
animals during the course of a routine TB herd test on his farm (Mcclellan, 2000). In
September, 2006, a 27 year old female USDA-employed animal health technician was
killed in a motor vehicle collision on her way to an early morning TB testing appointment

(Judge, personal communication).

DISCUSSION

Large-scale animal disease control and management efforts are necessary and
difficult tasks assigned to the US. Department of Agriculture and state Departments of
Agriculture. The solvency of many agribusinesses depends on the ability to export

livestock and livestock products. To maintain or expand export markets, the US must

116

obtain and maintain certain prevalence levels for diseases of international significance,
such as bTB. The “costs” for the needed disease control programs are often measured in
program expenses (state and/or federal appropriations) or in terms of markets lost or
restricted. Prior to 1997, the Michigan Department of Agriculture’s bTB eradication
efforts were supported by existing departmental resources. From 1997 to January 2001,
nearly $29 million in State resources had been newly appropriated; an additional $6
million in federal firnds was made available in fiscal year 2000-2001, specifically for the
control of bTB in Michigan (Thiel, 2001). A team fi'om Michigan State University
estimated the total economic costs of bovine TB to the Michigan livestock industry to be
$21.1 million in fiscal year 2000-2001 and then decrease to $17 million in FY 2009-10
(Wolf and Ferris, 2000). Among these large dollar amounts and the inevitable political
wrangling, the human cost in terms of injury and death of program-related personnel, can
be easily lost.

The direct public health impact of the current bovine TB outbreak in Michigan as
previously described (Wilkins et al., 2008) is perceived to have been minimal, with only
two outbreak-associated human cases reported. However, the public health impact of a
disease includes not only the direct effects of the disease itself but also the health costs
associated with the contrOl of the disease. For example, although foot and mouth disease
is not a zoonotic, the 2001 outbreak in Great Britain “is considered a human tragedy, not
just an animal one” (Mort et al., 2005) and has been blamed, by the media, for several
suicides (Champion, 2001; Dennis, 2001; Smith, 2001; Williams, 2001). In the case of
bovine TB, the true public health impact of the disease must include the health impact of

the control efforts. In this case, the decision to TB test the entire cattle population of

117

Michigan not only generated a direct economic cost, but also had negative health effects
on both veterinary staff and cattle producers. A simplistic comparison of morbidity and
mortality events suggests that the control of the disease has had a greater negative impact
on human health than did the disease itself (only two human cases). However, it must be
remembered that, unlike injuries, bovine TB is a transmissible disease. Left uncontrolled
in livestock, the number of human cases could escalate. The direct impact on human
health of handling and testing large numbers of cattle is one of the costs that must be
considered.

This study's estimate of 1.9 veterinary injuries per each 10,000 animals tested,
should be useful to regulatory veterinarians when estimating the total impact of future
disease control programs for bT B and perhaps for other diseases that require a similar
» type of individual animal restraint and handling.

The very high risk ratio for injuries among regulatory vs. private veterinarians is
not a surprising finding. Private veterinarians were paid $40.00 per herd visit and $8.00
per head, so private practitioners had a clear financial incentive to test the larger herds. In
Michigan, larger herds tend to be dairy herds, which generally have cattle that are more
used to being handled and are housed in better working facilities. The smaller herds,
primarily beef, were generally left for the regulatory veterinarians. Because of their
natural temperament, dairy cows are less dangerous to handle and test than are beef cows
and more restraining equipment is generally needed, and less is usually available, to
handle beef animals. In addition, only regulatory veterinarians can place a comparative
cervical test, which requires firmly restraining the animal’s head in order to access the

neck.

118

The bivariate analysis revealed strong associations between several of the factors
found to be contributing to the risk of injury in the incidence density analysis. These
associations are not surprising. That few regulatory veterinarians work over 50 hours per
week is not unexpected, since a 40 hour work week is the standard for government
practice. A 40 hour work week likely explains the strong female presence in the
regulatory work force, as these positions may offer women the better possibility of a
reasonable work/home-life balance than full-time private practice. During the initiation
of the state-wide testing effort, both USDA and MDA were hiring veterinarians. These
positions would be quite appealing to new graduates (with reasonable hours, good
benefits), explaining the high proportion of regulatory veterinarians with less than 10
years experience. Recent hiring would also contribute to the high percentage of female
veterinarians, since the classes graduating from Michigan State University, College of
Veterinary Medicine have been predominantly female for the last 20 years.

Female gender was significantly associated with an increased rate of injury in the
incidence density analysis. The association remains significant in the comparison
between gender and injury after controlling for the confounder of practice type (adjusted
OR = 2.54; CI 1.01 - 6.53), but only barely reaching statistical significance. Further, the
association between regulatory practice and injury remained elevated only for males,
upon stratification by gender, suggesting gender is an effect modifier in the relationship
between practice type and likelihood of sustaining an injury.

Our study included only veterinarians who tested five or more herds in 2001,
therefore excluding veterinarians with the least experience with TB-testing. Recall bias

may be a factor as the survey instrument was mailed in September of 2002, asking about

119

injuries occurring in 2001. Most major or minor injuries are memorable, but some of the
more minor injuries may have been forgotten. Any recall bias, would expectedly have
caused a bias toward the underreporting of the self-treated injuries. However, a reporting
bias may have occurred in that veterinarians with injuries to report may have been more
interested in the study and therefore more likely to return their questionnaire than those
who did not have injuries. Lastly, this study was limited to veterinarians and did not
include animal health technicians or other farm assistants. Although assistants do not
place or read TB tests, they are often responsible for moving the animals and setting up
the testing area, which may make them as likely as the veterinarian to be injured. Injuries
to non-veterinarians were excluded to better enable determination of an accurate

incidence density based upon a definable numerator (injuries) per 10,000 animals tested.

CONCLUSION

The study population reported that 81% of these injuries could have been
prevented, generally by slowing down enough to 1) calmly move animals instead of
rushing them, 2) properly restrain animals (especially using chutes instead of milking
parlors for dairy cattle and restraining even “tame” animals 3) properly maintaining
equipment 4) clearing work area of obstacles such as shovels and manure. The USDA.
and state Departments of Agriculture can better control the execution of on-farm testing
by developing on-farm standard operating procedures (SOPs) for animal
handling/restraint and require their own staff and fee-basis veterinarians to attend annual
training and review the SOPs regularly. In addition, regulatory employers should allow

herd tests to be scheduled with enough time to focus appropriately on safety and shift the

120

emphasis fi'om herd tests completed, to herd tests completed safely. Ongoing training
and monitoring of the safety and health of regulatory staff should be extended to privately
employed fee-basis veterinarians as well. This study determined the rate of injuries that
can be expected while TB testing livestock per animal tested and per herds tested.
Although the relationships are complicated, gender to some degree, and practice type, to
a greater degree, are the main risk factors leading to an elevated rate of injury and an

elevated likelihood of injury in this setting.

121

REFERENCES

Animal Industries Act of 2000. Act No. 323. Enrolled Senate Bill No. 1339. State of
Michigan 90th Legislature (Oct 31, 2000).

Champion M. Foot-and-Mouth Disease Takes Its T 011 on England's Communities. In The
Wall Street Journal (New York), 2001 March 23.

Clifford JR. Instructions and Recommended Procedures for Conducting Tuberculosis
Tests in Cattle and Bison. Washington, DC: United States Department of
Agriculture, Animal and Plant Health Inspection Service, Veterinary Services.
2006. Veterinary Services Memorandum No: 552.15.

Dennis S. Foot and mouth drove our son to suicide. Daily Record (Glasgow). 2001 June
1.

Gabel CL, Gerberich G, Gerberich SG. Risk Factors for Injury among veterinarians.
Epidemiol. 2002;13:80-86.

Grade A Milk Law of 2001. Act 266 of 2001. State of Michigan Legislature (Feb 8,
2002)

Hill DJ, Langley RL, Morrow WM. Occupational injuries and illnesses reported by zoo
veterinarians in the United States. J Zoo Wildlife Med. 1998;29:371-385.

J eyaretnarn J, Jones H. Physical, chemical and biological hazard in veterinary practice.
Aust Vet J. 2000;78:751-758.

Landercasper J, Cogbill TH, Strutt PJ, Landercasper BO. Trauma and the veterinarian. J
Trauma. 1988;28:1255-1259.

Mcclellan TD. Farmer dies in attack by bull. The Grand Rapid Press (Grand Rapids).
2000 Sept 19.

Moore RM Jr, Davis YM, Kaczmarek RG. An overview of occupational hazards among
veterinarians, with particular reference to pregnant women. Am Ind Hyg Assoc J.
1993;54:113-120.

Mort M, Convery I, Baxter J, Bailey C. Psychosocial effects of the 2001 UK foot and
mouth disease epidemic in a rural population: qualitative diary based study.
British Medical Journal. 2005;331:1234-1238.

Poole AG, Shane SM, Kearney MT,Rehn W. Survey of occupational hazards in
companion animal practices. I Am Vet Med Assoc. 1998;212:1386-1388.

122

Poole AG, Shane SM, Kearney MT, McConnell DA. Survey of occupational hazards in
large animal practices. J Am Vet Med Assoc. 1999;215:1433-1435.

Smith R. Cow Slaughter Made Farmer Hang Himself; Foot & Mouth Suicide No. 2. The
Mirror (London). 2001 April 23.

Thiel C. A summary of the resources and roles dedicated to the eradication of bovine
tuberculosis in Michigan. Senate Fiscal Agency. 2001. Available from:
http://www.senatemichigan.gov/sfa/Publications/Issues/Bovine/BovineTB. pdf.

United State Department of Agriculture. 2002. Census of Agriculture. National
Agricultural Statistics Service. 2004. Report No: AC-02-A-22.

Wilkins MJ, Bartlett PC, Frawley BJ, O'Brien DJ, Miller CE, Boulton ML.
Mycobacterium bovis (bovine TB) exposure as a recreational risk for hunters:
results of a Michigan Hunter Survey, 2001. Int J Tuberc Lung Dis. 2003;7: 1001-
l 009.

Wilkins MJ, Meyerson J, Bartlett PC, Spieldenner SL, Berry DE, Mosher LB, Kaneene
J B, Robinson-Dunn B, Stobierski MG, Boulton ML. Human Mycobacterium
bovis infection associated with the bovine TB outbreak in Michigan, 1994-2007.
Emerg Infect Dis. In press 2008.

Williams B. Killed By Foot and Mouth; Gun Suicide of farmer scared of an outbreak. In
The Mirror (London). 2001 Apr 3.

Wolf C, Ferris J. Economic Consequences of Bovine Tuberculosis for Michigan
Livestock Agriculture. In: A Summary of the Resources and Roles Dedicated to
the Eradication of Bovine Tuberculosis in Michigan, Thiel C, ed. Senate Fiscal
Agency. 2000. p. 3.

123

CHAPTER 6
A COMPARISON OF RISK FACTORS FOR HUMAN EXPOSURE TO M.

TUBERCULOSIS AND M. BOVIS IN NORTHERN MICHIGAN.

ABSTRACT

First recognized in white-tailed deer in 1994, Mycobacterium bovis has since been
found in 42 Michigan cattle herds and is now considered endemic in the wild white-tailed
deer population of the northeastern part of the lower peninsula of Michigan. Numerous
additional species have been found infected including: coyotes, raccoons, black bear, red
fox, and opossum. Because of the occurrence in wildlife and re-occurrence in cattle, a list
of M. bovis-specific risk factors for exposure was developed for residents of the
geographically affected area. The list includes being hunters, trappers, taxidermists,
venison processors, beef Idairy producers or a farm/livestock worker. The health
departments covering 12 counties in the northeastern part of the lower peninsula of
Michigan participated in this study. A survey was developed which included the list of
M. bovis-specific exposure risk factors and a list of M. tuberculosis-specific exposure risk
factors (from CDC). The health departments were asked to complete and attach the
survey to each tuberculosis skin test (TST) reporting form, then send the de-identified
form to the Michigan Department of Community Health. To measure the associations
between each risk factor and the TST results, a relative risk with 95% confidence
intervals, or a Fisher’s exact test was used. Overall, there were 29 positive TST tests, of
1268 TST records submitted, for a positivity rate of 2.29% (29/1268). Two risk factors

were found to be significantly associated with a positive TST, being a venison processor

124

RR=2.49; p=0.047) and being foreign born (RR=9.36; p=0.019). The positive
association found for being foreign born was expected, but the association between
having a positive TST and being a venison processor suggests that this population may
benefit from increased surveillance efforts and targeted public health prevention

messages to raise awareness about the risk of M. bovis exposure.

INTRODUCTION

First recognized in a white-tailed deer in 1994, M. bovis (bovine TB) has been
found in 42 cattle herds and is now considered endemic in the deer population of the
northeastern part of the lower peninsula of Michigan. Several other wildlife species
(coyotes n=19, raccoons n=8, black bear n=7, bobcat n=4, red fox n=3 and opossum n=2
(Summary of Michigan wildlife bovine tuberculosis surveillance, intemet) have also been
found infected with the deer/cattle outbreak strain of M. bovis. Due to the presence of
infected wildlife and cattle in this area, persons with exposure to these animals may be at
higher risk of exposure to M. bovis, a zoonotic organism with one of the broadest host
ranges of all known pathogens (O’Reilly, 1995).

The authors developed a list of Michigan-specific risk factors for residents which
includes being a: hunter, trapper, taxidermist, venison processor, beef or dairy producer
or farm/ livestock worker. According to CDC, persons at higher risk for exposure to or
infection with M. tuberculosis include: close contacts of persons known or suspected to
have TB, foreign-bom persons from areas that have a high TB prevalence, residents and
employees of hi gh-risk congregate settings, some medically underserved, low-income

populations as defined locally, hi gh-risk racial or ethnic minority populations, defined

125

locally as having an increased prevalence of TB, infants, children, and adolescents
exposed to adults in high-risk categories, persons who inject illicit drugs; any other
locally identified high-risk substance users, health care workers who serve high-risk
clients (CDC, 2005).

Data available to the Michigan Department of Community Health (MDCH) does
not indicate an increase in the number of human cases of M. bovis in Michigan, since
1994 (MDCH unpublished data). When humans are exposed to M. tuberculosis, 30-40%
of exposed close contacts become infected. If they do not progress to clinical disease,
they are considered to have latent TB infection (LTBI) (CDC, 2005). Approximately 5-
10% of latently infected individuals will develop active TB disease at some point in their
life, with the highest risk within the first two years of infection (CDC, 2005). In humans,
disease caused by M. tuberculosis is usually a pulmonary presentation, and transmission
is usually human-to-human via aerosol droplets. Data about the infection rate for persons
exposed to M. bovis are not available, but would likely be less because M. bovis infection
in the US is more likely caused by ingestion of raw dairy products which leads to a
gastrointestinal presentation, with human-to-human transmission rare. That said, once an
individual is infected with M. bovis, the likelihood of progression from latent infection to
clinical disease would be similar to that of M. tuberculosis.

The most common way to measure the prevalence of LTB1 in a population is the
use of the Mantoux tuberculosis skin test (TST). A TST will react positively to infection
with M. tuberculosis or Mycobacterium other than tuberculosis (MOTT) (including M.
bovis). Generally speaking, a tuberculin reaction caused by infection with MOTT tends

to be smaller than those elicited by infection with M. tuberculosis (Dasco, 1990).

126

Our objective was to determine if evidence existed to indicate the presence of
latent human infections with M. bovis. Our plan was to look at TST results in a region of
Michigan where M. bovis is endemic in the deer population and M. tb risk factors are
low. If skin tests results were found to be associated with exposure to the known animal
reservoirs of M. bovis, this would suggest that latent or undiagnosed M. bovis infections

might be occurring in the Michigan human population.

METHODS

The health departments covering 12 counties in the northeastern part of the lower
peninsula of Michigan were asked to participate in this study. A survey was developed
and printed on a sticker which was attached to each TST skin test reporting form. Survey
questions included a list of exposure risk factors for both M. bovis and M. tuberculosis.
Health department were asked to complete and attach the survey to each TST skin test
reporting form. Once the TST was interpreted and the survey completed, the report was
de-identified and mailed to MDCH. The 12 counties were in three different local health
jurisdictions, District Health Department No. 2 (Alcona, Iosco, Ogemaw, Oscoda
counties), District Health Department # 4 (Alpena, Cheboygan, Montmorency, Presque
Isle counties), and Northwest Michigan Community Health Agency (Antrim, Charlevoix,
Emmet, Otsego counties). The population of this area is approximately 256,548 (2000
Census) and the largest population center is Alpena (population 10,364). The study
began October 1, 2001 and continued through December, 2003. Each county began
participation at slightly different times, and continued participation for various lengths of

time. To better ensure comparability, and to avoid counting individuals more than once,

127

no more than 12 consecutive months of data was used from each county. The time period
for collection ranged from 9 to 12 months per county.

To measure the associations between each risk factor and TST results, the relative
risk with 95% confidence intervals, or Fisher exact test (when an expected cell size < 5),

was used to measure the strength and statistical significance of the association (EpiInfo

6.04, CDC, Atlanta).

TST Interpretation

Interpretation of the Mantoux TST is based on the size (in mm) of induration
measured at 48-72 hours post intradermal injection of 0.1 mm of tuberculin purified
protein derivative (PPD). Classification of the TST reaction is based on categories of
potential risk factors for exposure to M. tuberculosis (CDC, 2005) with cut-offs of 5mm,
10 mm and 15 mm used, depending on the risk factors of exposure. Although the TST
report usually included the measurement of induration for reactive TSTs, the researchers
did not have sufficient information to categorize each reactor. Therefore, the
interpretation (positive or negative) rendered by the public health nurse completing the

report was used in this study.

RESULTS

The number of completed TST records submitted to MDCH with the number of
months of participation for each local health jurisdiction is included in Table 6.1.

Overall, there were 29 positive TST reactors out of 1268 TST records, for a positivity

rate of 2.29% (29/1268).

128

Table 6.1 : The time period of participation and number of completed TST records

received from each local health jurisdiction.

 

 

Local Health Number of No. Completed No. of %

Jurisdiction Months of TB Skin Test Positive TB Positive
Participation Reports skin Tests TB Skin

Submitted Tests

Health District # 2 12.0 250 6 2.4

Health District # 4 10.7 541 8 1.5

NW Michigan

Community Health

Agency 10.8 477 15 3.1

Total 1268 29 2.3

 

For Health District # 4, risk factor data for exposure to M. tuberculosis was
missing from 130 records and risk factor data for exposure to M. bovis was missing from
34 records. These records were excluded from the risk factor analysis. Relative risk

results for each exposure risk factor are found in Table 6.2.

129

 

Table 6.2 : Comparison of tuberculosis skin test results by M. bovis and M. tuberculosis

exposure risk factors using relative risk analysis.

 

 

 

 

 

Relative
No. Positive TST No. Negative Risk (with
Results TST Results 95% C!) F. E. pvalue
Risk Factors for M. Bovis
Hunter
Yes 9 288 1.43
No 20 925 (066-31 1)
Trapper
Yes 0 18 N/A
No 29 1195
Taxidennist
Yes 0 2 N/A
No 29 1211
Venison Processor
Yes 5 91 2.49 0047*
No 24 1122
Beef or Dairy Producer’-
Yes 2 29 2.89 0128*
No 27 1884
Farm/Livestock Worker
Yes 2 35 2.41 0.161*
No 27 1 178
Risk Factors for M.
tuberculosis
Contact with known or
suspected case
Yes 0 42 N/A N/A

No 29 1075

130

Table 6.2 (cont’d)

Live or work in a
congregate setting

Yes 11 295 1-56
No 18 814 (0.73 - 3.48)

Health care worker
Yes 2 200 0.343 0064*
No 27 909

Foreign born
Yes 2* 7 9.358 0.019*
No 27 1 1 10

 

*Fisher’s exact p—value used because of small cell size

180th from Taiwan

DISCUSSION

The overall rate of TST positivity for this study was 2.3%, lower than the 3.3% to
5.2% rate expected based on an estimate of 9.6 -— 14.9 million persons residing in the US
with latent tuberculosis infection (Bennett, 2003) divided by the estimated US population
of 285,125,973 (July 2002, US Census data
http://www.census.gov/popest/states/tables/NST-EST2006-01.xls). This area of
Michigan is very homogenous with little racial or ethnic diversity. Afiican Americans
make up a small percentage the population in these 12 northern counties, 0.3 — 0.7%
compared to 14.3% for the state of Michigan as a whole, and 12.3% for the US.
Likewise, persons of Latino or Hispanic origin comprise only 0.6-1.4% of the 12 county
population, versus 3.8% of Michigan’s population and 14.4% of the US population.

Foreign-bom persons are underrepresented with 1.2 - 1.7% of the 12 county population

131

compared to 5.3% for Michigan, and 11.1% of the US (US Census Bureau, 2005). This
area was chosen because of the presence of M bovis in the deer and cattle population, but
also because it lacks several of the exposure risk factors for M. tuberculosis (such as high
rates of illicit drug use, foreign born persons, persons known or suspected to have TB,
and high-risk racial or ethnic minority populations) that drive the TST rates in more
diverse and urban settings.

We do know that hunters are being exposed to M bovis by handling infected deer
carcasses. Based on a 2001 survey of 1,833 hunters who had successfully harvested deer
in or near Michigan’s endemic area, it was determined that 89% of hunters field dressed
their own deer, and only 43% of them wore gloves when doing so. Based on the 2001
prevalence estimate in the deer population and the survey results, up to 139 hunters in the
endemic counties may have field dressed positive deer without wearing gloves and up to
12 hunters would cut themselves while field dressing these positive deer (Wilkins, 2003).
Another recent paper (Wilkins, 2008) reported two human cases of M. bovis with
molecular and epidemiologic links to the outbreak in deer and cattle, with one hunter
infected after cutting himself as he opened the chest cavity of an infected deer. Abattoir
workers have been infected during the processing of cattle (Robinson, 1988; Cousins,
1999; Georghiou, 1989), and cervidae have been documented as the source of M bovis
infection for humans with infection resulting from exposure to live elk and the processing
of cervidae carcasses (Farming, 1991). Cutaneous infections can resolve without
treatment, but the infected individuals would respond positively to a TST.

Our study results showed an expected association between TST positivity and

being foreign born (and likely exposed, vaccinated with ECG, or both) (RR=9.36;

132

p=0.019). However, the statistically significant association between being a venison
processor (RR= 2.49, p=0.047) and TST positivity is new, but perhaps not unexpected.
In addition, the risk was found to be elevated if the individual was a beef or dairy
producer (RR= 2.89; p=0.128), or a livestock worker (RR=2.41; p=0.161) although these
finding were not statistically significant. Four of the five TST positive venison
processors were also hunters, as was one of the two beef or dairy producers and one of
the two farm/livestock workers, so their exposure, if it was to M bovis, could have been
recreationally associated with hunting.

Primary inoculation tuberculosis is rare in developed countries where tuberculosis
has been largely controlled in cattle populations. However, before state and federal
efforts to control the disease in cattle, it was much more prevalent and known as
“butcher’s wart” (Kakakhel, 1989). Venison processed in a licensed food establishment
or processed for retail sale is regulated by the Michigan Department of Agriculture
(MDA). According to the MDA, less than 20% of all Michigan hunter-harvested venison
is processed under state regulation (MDA, Food and Dairy Division, 1989).

These findings suggest that venison processors and anyone working with cattle in
the endemic area may benefit from targeted public health prevention messages to reduce
likelihood of exposure. Persons in these (potential) risk categories should also be
encouraged to receive an annual TST to enable the earliest possible detection of infection.
Latent infection with M tuberculosis is 90% curable, that is, the likelihood of progressing
from latent infection to clinical disease decreased from 10% to 1% following treatment
(Centers for Disease Control and Prevention, 2000). It would be reasonable to assume

the cure rate for latent M bovis infection would be similar.

133

There are several limitations in this study, the first being the TST itself. There is
variability in the administration of the test, interpretation of the test and among individual
immune reactions to the test. There are problems with false positive and false negative
reactions, and it does not differentiate between infection with M tuberculosis and M
bovis. This study focused on TSTs conducted by local health departments and did not
include TSTs performed in the private setting. Our study results represent approximately
25% of the TB testing occurring in this area on an annual basis (unpublished data, M.
Gallego, Michigan State University, 2007), thus limiting our ability to generalize the
results. The relatively small number of positive results (n=29) makes it difficult to
accurately measure associations.

Also of concern is that the interpretation of the TST is based strictly on exposure
to, and infection with, M tuberculosis. Infection with M bovis (MOTT) would be
expected to elicit a smaller reaction than one caused by infection with M tuberculosis
because PPD is mixture of antigens derived from M tuberculosis (Dasco, 1990). An
individual with only M bovis exposure risk factors would only be considered positive if
their TST induration were 15 mm or greater, thus many latent cases of M bovis infection
may be missed using the current CDC TST interpretation guidelines. In fact, the only
reported case of cutaneous tuberculosis caused by M bovis related to the current outbreak
had an initial negative TST followed by a 6mm reaction 14 weeks post exposure (MDCH

unpublished data).

134

CONCLUSION

It is safe to say that basic public health advice including the use of gloves when
field-dressing deer and the thorough cooking of venison, should continue to be offered to
all residents of the M bovis endemic area, with an extra effort to reach hunters and
venison processors. In addition, people exposed to deer or cattle should be advised to
receive annual TSTs. Targeted surveillance of venison processors should be considered,
using the TST and the newly available Quantiferon—gold blood (to help distinguish
between latent infection with M tuberculosis vs. other mycobacteriae) to better delineate
the unique risk factors for exposure in this population of Michigan. In addition, MDCH
(in conjunction with the Centers for Disease Control and Prevention) should strongly
consider adding M bovis-specific risk factors to the TST interpretation guidelines for

areas in which M bovis is present in animal populations.

135

REFERENCES

Bennett DE, Courval JM, Onorato IM, Agerton T, Gibson JD, Lambert L, McQuillan G,
Lewis B, Navin TR, Castro KG. Prevalence of TB infection in the US population,
1999-2000 [Abstract 67921]. In: Program and abstracts, 131St annual meeting of
the American Public Health Association, November 15-19, San Francisco,
California; 2003.

Centers for Disease Control and Prevention. Controlling tuberculosis in the United States:
recommendations from the American Thoracic Society, CDC and the Infectious
Disease Society of America. MMWR. 2005;54(No. RR-12):1-81.

Centers for Disease Control and Prevention. Targeted Tuberculin Testing and Treatment
of Latent Tuberculosis Infection : American Thoracic Societ/CDC Statement
Committee on Latent Tuberculosis Infection Membership List. MMWR.
2000;49(No. RR-6): 1-54.

Cousins DV, Dawson DJ. Tuberculosis due to Mycobacterium bovis in the Australian
population: cases recorded during 1970-1994. Int J Tuberc Lung Dis.
1999;32715-721.

Dasco CC. Skin Testing for Tuberculosis. 3rd ed. Walker HK, Hall WD, Hurst JW,
editors. London, Butterworth Publishers; 1990.

Farming A, Edwards S. Mycobaterium bovis infection in human beings in contact with
elk (Cervus elaphus) in Alberta, Canada. Lancet. 1991;338:1253-1255.

Georghiou P, Patel AM, Konstantinos A. Mycobacterium bovis as an occupational hazard
in abattoir workers. Aust NZ J Med. 1989;19:409-10.

Kakakhel KU, Fritsch P. Cutaneous tuberculosis. Int J Dermatol. 1989;28:355-362.

O’Reilly LM, Dabom CJ. The epidemiology of Mycobacterium bovis infections in
animal and man: a review. Tuberc Lung Dis. 1995;76 Suppl 1: 1-46.

Robinson P, Morris D, Antic R. Mycobacterium bovis as an occupational hazard in
abbatoir workers. Aust NZ J Med. 1988;18:701-703.

Wilkins MJ, Bartlett PC, Frawley B, O’Brien DJ, Miller CE, Boulton ML.
Mycobacterium bovis (bovine TB) exposure as a recreational risk for hunters:

results of a Michigan Hunter Survey, 2001. Int J Tuberc Lung Dis.
2002;7(10):1001-1009.

136

Wilkins MJ, Meyerson J, Bartlett PC, Spieldenner SL, Berry DE, Mosher LB, Kaneene
J B, Robinson-Dunn B, Stobierski MG, Boulton ML. Human Mycobacterium
bovis infection associated with the bovine TB outbreak in Michigan, 1994-2007.
Emerging Infec Dis. In press 2008.

United States Census Bureau, State and County QuickFacts. [factsheet on the
intemet] Available from: http://quickfacts.cg§us.gov/qfd/states/26000.html.

137

CONCLUSION

The purpose of this dissertation is to clarify the human health effects of the bovine
TB outbreak on Michigan residents. Each of five projects addressed an area of risk to
human health and used methodologies best suited to address that particular issue. The
studies characterized the risks in greater detail than what was previously available. As
with most field research, each study suffered fi'om limitations typically encountered when
working in the “real” world. Several new hypotheses were generated, ideas for further
studies proposed and public health prevention recommendations produced.

The Hunter Health Survey (Chapter 2) characterized the self-protective behaviors
practiced by 1,833 hunters in the northeastern comer of the Michigan’s lower peninsula.
Because hunters could be exposed to M bovis via the cutaneous or the gastrointestinal
routes, the survey focused on hand washing and glove use practices, as well as cooking
and venison consumption practices. The likelihood of foodbome exposure to M bovis
was found to be remote. However, exposure via the cutaneous route was found to be not
only possible, but expected at the rate of 12-13 cases per year. This conclusion was
supported by the documentation of the first cutaneous infection in a Michigan hunter in
2004. Based on the findings of this study, the Michigan Department of Natural
Resources Annual Hunting and Trapping Guide now encourages hunters to wear gloves
when dressing venison and to cook all game meat thoroughly.

Michigan residents diagnosed with M bovis infection from 1994-2007 are
described in the second project (Chapter 3). Two of these patients were infected with the

genetically identical strain of M bovis circulating in the deer and cattle populations

138

involved in the current outbreak in Michigan. The exposure history and clinical course of
these two patients are described in detail. The 2004 patient diagnosed with cutaneous M
bovis infection was indisputably infected via exposure to an infected deer, with the deer’s
lesion and the hunter’s wound yielding isolates with matching genotypic patterns. The
patient diagnosed in 2002 yielded the same strain of M bovis, from a puhnonary sample,
which genotypically matched the endemic strain in both deer and cattle in Michigan. M
bovis was identified post mortem on this patient, who had a number of potential routes of
exposure to M bovis, including hunting, residence on the edge of the epicenter of the
outbreak (Deer Management Unit 452), drinking raw milk in the 1930’s and close contact
with a family member with TB (60 yrs prior). Although his route of exposure will never
be definitively explained, the fact that his isolate matched the pattern of the outbreak
strain provides strong epidemiologic evidence of a recent exposure to an infected animal
(most likely deer) in Michigan. That his exposure history yielded no “smoking gun”
raises the possibility that additional and/or unexplored routes of exposure may exist.

The pet study (Chapter 4) evaluated 23 dogs and cats residing on farms with M.
bovis infected cattle. For 21 of the pets, only non-invasive methods were used to assess
their health and TB infection status. Two cats underwent full necropsy. All results were
negative for evidence of M bovis infection. Three cats tested positive for M avium at the
1:160 dilution, of which two also tested positive for M bovis at less than the 1:160
dilution. These results were therefore interpreted to be cross-reactions with M avium. In
addition, three rectal swabs from these animals yielded positive cultures for M avium or
Mycobacterium species (Group IV unclassified), suggesting that the non-invasive

protocol would likely have produced positive results if M. bovis was actively being shed

139

in feces at the time of the study. These negative findings were not surprising, given that
the average number of months these pets were exposed to infected cattle was only 2.3
months for cats and 4 months for dogs. In addition, the cattle herds in Michigan were not
heavily infected (few lesions per cow and a small number of cows per herd), the herds
were diagnosed very quickly, depopulation also took place quickly, and only two of the
farms were dairies, where raw milk was fed to pets. In Michigan, under the current
intensive bovine TB testing protocols for cattle, pets do not appear to play any role in
perpetuating M bovis infection on cattle farms, nor do they appear to pose significant risk
to their owners. However, the fact that a semi-feral cat living in the endemic area was
diagnosed with advanced M bovis disease in 2000 reminds us that cats certainly have the
potential to pose an exposure risk to the humans with whom they interact. In light of
MDA’s decisions to not depopulate domestic pets on infected farms along with the
removal of cattle, a list of recommendations for farm owners with pets was generated to
keep the risk to a minirmun.

Fifty-three injuries were reported among 175 veterinarians TB testing livestock in
2002 (Chapter 5). Veterinarians reported that animal behavior, poor working facilities,
weather, lack of availability and inexperience of assistants and personal issues all
contributed to the risk of injury. Over 80% of these injuries were reported to have been
preventable by slowing down enough to calmly move animals instead of rushing them,
properly restraining animals, properly maintaining equipment and clearing the work area
of obstacles. The estimated rate of injury (1 .9/10,000 animals tested) should be useful to
regulatory agencies planning any large scale animal disease control efforts that require

individual animal restraint. Two human deaths associated with the bovine TB control

140

effort in Michigan are also described. This project was important to elucidate the
“human costs” of animal disease control efforts, an issue easily overshadowed by
financial and political costs.

Exposure to risk factors for both M tuberculosis and M bovis were collected for
1,268 persons receiving tuberculosis skin test (TST) in the 12 counties of northern
Michigan. The TB skin test (TST) project (Chapter 6) yielded a background positivity
rate of 2.3% for the participating counties, which is well below the national estimate of 5-
10%. This low rate is expected, as the national TB rates are driven by two high-risk
populations, neither of whom are highly represented in the counties of northeastern
Michigan; homeless persons (with a history of injection drug use and or alcohol abuse)
and foreign born persons, primarily from Asia. Being foreign born and being a venison
processor were the two exposure risk factors proving to be a significantly associated with
a positive TST reaction. These results indicate that venison processors may be at
elevated risk of exposure to M bovis, and would therefore benefit from targeted M bovis
prevention information. Although the TST is a crude measure, which includes reactions
to both M tuberculosis and M bovis exposure, it none-the-less provides a starting point
for monitoring long-term trends in this rural, relatively homogenous population of
Michigan.

Based on the work presented in this dissertation, recommendations were
generated to decrease the risk of exposure to M bovis, and to reduce injuries associated
with the bovine TB control efforts in Michigan. Several of these recommendations have
already been adopted by appropriate regulatory agencies.

0 Develop educational materials specific for venison processors.

141

Develop educational material targeting hunters.

Develop educational materials for physicians regarding the clinical presentation
of cutaneous M bovis infections so that early and accurate diagnoses can be
made.

Continue to offer training to health care professionals on the proper
administration and interpretation of the TST .

Owners of cattle infected with bovine TB should be counseled by both human and
animal health officials that M bovis is a zoonotic organism and that precautions
can be taken to avoid infection.

Initial two-step tuberculosis skin tests, followed by an annual skin test should be
recommended for all veterinarians, livestock owners whose cattle have tested
positive, hunters, taxidermists and trappers.

The USDA and The Michigan Department of Agriculture should develop on-farm
standard operating procedures for animal handling/restraint with a focus on the

safety of the animal handlers.

The strength of these studies is their timeliness, as the questions about human

health risks only become more pressing as the bovine TB outbreak in Michigan

continues. A similar outbreak in Minnesota was detected in 2005. Each study had its

own limitations, which are addressed in detail within each chapter. The shortcoming

present in almost all studies was small sample size, which affected the study regarding

bovine TB farms with pets, TST positive reactors, injuries and human cases of M bovis

infection. Another limitation common to several studies is the ability to generalize the

142

results beyond the geographic area currently experiencing the M bovis outbreak in
wildlife and cattle in Michigan.

Several scientific advances could dramatically alter the quality of data available
for assessing human health risk from M bovis, including the availability of better in vivo
tests for M bovis in pets (under development), and the increased use of the interferon-
garnma test (QuantiFERON-TB Gold®) to detect M tuberculosis in humans, which could
help research efforts if used in series with the TST. Changes in the pattern of disease in
both cattle and wildlife, or changes in disease control efforts, would also change the
routes and frequency of human exposure to M bovis. Public health prevention messages
should be developed, delivered, and then their impact should be measured as a

continuation of the work presented in this dissertation.

143

APPENDICES

144

APPENDIX A

DEER HUNTER HEALTH SURVEY

145

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mmewmmdmmrmnm.mrm
Attn. Widllte Surveys: 99999-1422 &
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8. MWMMMMMMIM ‘D Yes ”D M (U‘No'mflnbfl)
A. Howmrydeerddyoufielddmslntyeafl door

8. Didyouwearmbberorlmxglovesmnfield- '1] Yes ‘D No 'EI 0mm
dresshgdeerlaatyear?

c. Didyoucutyomselltenougntodrawbloodwhle ‘D Yes 'D No '0 Ururrs
fielddreeehgdserbstyear?

D. I‘Iowmnyhourspamdbetwunflalddressim
deerandmhingyourhandslastyeafl

4. MflmWMMmd-arh ‘D Yes '12] No ’12] Unsure

Mmmammmw

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moundoerl‘astyaar)

6. Dflywmanyvufloontrundsorkllsdhm ‘EIYes ’E] NoflI'No'Zalrprola)
ADldyouoatanyamokedvenbonrmdeirorndoor ‘DYes 'DNo 'L'IUnsure

 

hours

 

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B. Didyoueatvonhonlorkymedofl'omdeerklad '0 Yes 'D No ”El Uncle
Iastyear?

c. Dldyoueatmmmmm ‘Cl Yes ‘D No ’1] Unsure
ldlledlactyear?

D. wummmmmommmrmmmmmmwm
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11.

Michigan?
'D Wasnotawareotapmblem
’ [:1 Somewhat “owned (aware otthe probbm)

’[j Informed (undorstandthescopeoftheproblem,typesofanlmals Involved, ellorlstooontrel
outbreak)

" Cl 3mm (avidly follow the issue and keep up-to-date on newt‘ndings and control

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doorbaptblichoolththnat?

'D Nothreat ’13 Small '12] Medium ‘1] Blgthreat I’CJ Wasnotawareofa
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147

APPENDIX B
INJURY SURVEY TOOLS

148

VETERINARY INJURY SURVEY - BASIC INFORMATION SHEET
(One per vet whether or not you were injured in 2001)
(Refonnatted for Dissertation)

 

[Please fill in the blank, or mark the box next to your answer for each question]

General Information

1. Year of Birth _ 2. Gender [:1 Male El Female
3. Year of graduation from Veterinary School

4. No. of years “working with or handling” large animals (including equine) prior
to vet school yrs

5. How many years have you been practicing veterinary medicine? yrs

Work Information for 2001 Only (Approximates are fine)

6. In what type of practice were you primarily employed during 2001?
1:] Private clinical practice [I Govemment/Regulatory
[:1 College/University [:1 Other (please specify)

 

7. How many hours per week did you spend In a work related vehicle (driving or

riding)? _hrs
8. How many days per week did you usually work? _days
9. How many hours per week did you usually work? _hrs
10. How many hours of sleep did you get per night during your average work
week? _hrs
11. What percentage of your work time was spent on emergencies coverage
(being on call)? %

 

12. What percentage of your work time was spent doing TB-related work?
%

 

Health Information for 2001

13. How many times/month did you participate In aerobic activity lasting 20 min or
more? lmo (examples - jogging, M walking, playing sports, working out,
aerobics, swimming, biking)

14. What was your body weight and height In 2001?

(lbs) __ft __in
15. How would you rate your overall health In 2001?
[:1 Excellent 1:] Good [:1 Fair El Poor
16. When working, how often do you wear your seatbelt?

[:1 Always [:1 Usually El Sometimes 1:1 Rarely 1:] Never
17. Did you regularly smoke? Cl Yes 1:] No or regularly chew tobacco? El Yes E] No

149

Practice Information for 2001

18. Please indicate the percentage of time you spent working on each species
(totaling 100%).

Beef Captive cervidae Dogs and cats
__ Dairy Swine Avian, reptiles, pocket pets
Equine Small ruminants Wildlife (excluding captive
cervidae)
__ Other

 

19. When TB testing livestock or cervidae, how often did you have technical or lay
personnel available to assist you?

Cl Always Cl Usually [I] Sometimes D Rarely [:1 Never

20. When TB testing livestock or cervidae In 2001, how often did you provide the
restraint equipment (chute, gates or panels)?

[:1 Always (:1 Usually El Sometimes 1:1 Rarely [:1 Never

Injuries in 2001
The definition of INJURY is: -“an acute traumatic event occurring as a result of TB
testing activities either on a client’s or employers premises, or during TB work-related
driving activities that resulted in:
0 Restriction of normal activities for at least four hours; and/or
0 Loss of consciousness, loss of awareness or amnesia for any length of
time; and/or
a The use of medical assistance (includes, suturing, antibiotics, splinting, x-
rays, surgery, and physical therapy whether obtained from others or
yourself).

This definition includes injuries associated with any TB-related work activities
such as interacting with animals, clients or staff, preparing for TB test
administration or reading, administering or reading TB skin tests, clean-up
and disassembly of testing equipment, administrative functions, and travel as
part of your TB-related work. Both intentional and unintentional events
(animal-inflicted or self-inflicted) are included in this definition.
It includes but is not limited to such injuries as:

o Bites, laceration, fractures, sprains, strains, skin punctures;

o Allergic reactions, including asthma and dermatitis;

- Ergonomic and repetitive motion injuries

20. Did you sustain at least one Injury associated with TB testing livestock or

captive cervidae in Michigan during calendar year 2001 according to the
definition given above?

150

[:1 Yes - Please complete one or more of the attached sheets, starting with Injury
Data Collection Sheet No. 1 for your most severe injury. Please return this page
and the data collection sheets in the postage paid envelope provided.

El No - Please return this page in the self-addressed postage paid envelope
provided.

Drawing

By completing and returning this page of the survey, you will be entered into the drawing
for a Michigan State University, College of Veterinary Medicine sweatshirt. If you
answered yes to Question No. 20 above, please fill out the appropriate number of Injury
Data Collection Sheets and return these as well.

If you win one of the five sweatshirts, what size would you prefer? Adult sizes: [:1
Small 13 Medium [:1 Large 13 X Large El XX Large

Thank you so much for your cooperation!

151

Injury Data Collection Sheet No. 1
(For your most severe injury in 2001)

Please fill out both sides for each injury sustained while TB testing livestock or cervidae In
2001. “TB testing” Includes placing the skin test (caudal fold, single cervical, or
comparative cervical) and reading the test as well as any blood collection for TB testing. If
you sustained more than 4 injuries in 2001, please complete the data collection sheets for
your four most severe injuries, starting with Sheet No. 1 for the most severe Injury.

1. Month in which injury occurred , 2001

2. Severity of Injury
D Major - required immediate treatment (hospitalization, outpatient visit to emergency
room urgent care center, within 4 hours of incident)
D Minor - required non-immediate treatment for the injury from physician or human health
professional within 7 days following the injury
3 Self treated - please specify treatment (such as simple first aid, antibiotics, suturing,
reduction of fracture) by self or veterinary staff

 

 

3. Number of days (or hours) of work time lost because of this injury
days or hours

4. When In the course of the farm visit, did the Injury take place? (Please check only one)
El Traveling to a TB testing (or reading) appointment

While preparing for or setting up equipment for TB testing (or reading)

While placing (or reading) TB tests

While disassembling or cleaning TB testing equipment

Filling out TB test charts (on farm or in vehicle)

Traveling from a TB testing (or reading) appointment

Other - please comment

UCIEIDCICI

 

5. Were other people working with you at the time of the injury?

a. Veterinarians, besides yourself? [1 No D Yes - If yes, how many? __

b. Animal health technicians or C] No [:1 Yes - If yes, how many? __
your own hired help?

0. Animal owner 1:] No D Yes

(I. Laborers provided by herd owner [II No [I Yes -- If yes, how many? _

(family members, farm help, neighbors)

152

6. Location of Inlug on Body ‘ 7. T of In u
(please Indicate primary site with a “1” (please check the best answer)
and secondary sites with “2’s” )

CI Eyes 1:] Fracture

C] Nose El Traumatic head injury
13 Teeth [:1 Spinal cord injury

El Head (other) Cl Dislocation

1:] Neck Cl Strain/sprain

CI Arm/shoulder E1 Internal injury

El Hand 1:] Open wound/laceration
1:1 Leg El Abrasion/contusion

[:1 Foot Cl Burn

[Z] Back [3 Toxic exposure
CIThorax including ribs El Allergy/Irritant

El Abdomen/intemal organs Cl SIip/trip/fall

CI Genitalla C] Other

Cl Other

 

 

8. Cause of Inlug

(please check the best answer)

[:1 Needle stick

[I] Lifting or pushing animal

[3 Kicked by animal

El Bitten by animal

Cl Pushed/headbutted animal
[3 Fallen on by animal

Cl Crushed/pinned by animal
El Lifting or moving equipment
[I Pinched/crushed by equipment
[:1 Motor vehicle accident

I: Allergic to/Irritated by:

 

El Other

 

9. Was the Injury caused by direct contact with an animal? DYBSEI No (If “no” skip to #11)

10. What kind of animal was involved?

Dairy l'_'l Cow [3 Bull El Other
Beef 1:] Cow El Bull El Other
Bison D Cow El Bull 13 Other
Elk D Cow D Bull D Other
Deer D Doe 1:] Buck [:1 Other
Small Ruminants El Goat D Sheep
Other

1:] Don't know or remember
1:] Don’t know or remember
El Don’t know or remember
1:1 Don’t know or remember
[I Don’t know or remember

 

11. Was the Injury caused by equipment (use or failure)? DYes El No (If “no” skip to #13)

12. Please briefly describe the type of equipment Involved and what happened to cause

the injury.

 

 

153

13. In your opinion which of the following factors contributed to your Injury?
(Mark as many factors as apply to this incident)

 

 

 

Animglgehavior Facilities Weather
Cl Unusually aggressive Cl Poor flooring El Rain
[:1 Unusually frightened El Poor lighting [:1 Snow
Cl Extremely unpredictable Cl Inadequate animal restraint 1:] Ice
1:] Unusually protective Cl Inappropriate work space [:1 Cold Temp
(cramped, couldn’t reach animal) D Hot Temp
Vet Techs or Hired Help Farm Help Personal Issues
Cl Too few 1:] Too little CI Overly tired
[3 Too many Cl Too much El lnexperienced
Cl lnexperienced 1:1 lnexperienced D You were in a hurry
Cl Unhelpful (poor attitude) 1:] Unhelpful (poor attitude) or felt rushed
Cl Poor animal handling skills El Poor animal handling skills El You lacked adequate
(spooked/rushed the animals) (spooked/rushed the animals) training
C] Your poor physical
condition

Other factors contributing to the injury incident
14. Was this the re-aggravatlon of a previous Injury? El No El Yes

15. In your opinion, could this Injury have been prevented? E] No C] Yes
If yes, how?

 

 

16. Optional — In your own words, briefly describe the circumstances leading to the Injury
and the injury Itself:

 

 

 

Thank You!

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