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SALMONELLA ENTERITIDIS INFECTION IN MICHIGAN (1995-2001):

INCIDENCE AND RISK FACTOR ANALYSIS

presented by
Muhammad Younus

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SALMONELLA ENTERITIDIS INFECTION IN MICHIGAN (1995-2001):
INCIDENCE AND RISK FACTOR ANALYSIS

By

Muhammad Younus

A THESIS

Submitted to
Michigan State University
in partial fulfillment of the requirements
for the degree of

MASTERS IN EPIDEMIOLOGY

DEPARTMENT OF EPIDEMIOLOGY

2006

ACKNOWLEDGEMENTS

I am indebted to my guidance committee members, their contribution made this
work possible. A special thank to my major advisor, Dr. Mahdi Saeed, for his
continuous intellectual advisement, encouragement, and financial support. He is a great
mentor, colleague, and friend.

Also, many thanks to Drs. Hossein Rahbar and Melinda Wilkins for serving on my
guidance committee. Their suggestions and feedback while conducting research and
writing my thesis were invaluable.

I gratefully acknowledge the staff of Communicable Disease Division, Bureau of
Epidemiology, Michigan Department of Community Health for their support. In
particular, I would like to thank Jennifer Beggs and Sally Bidol (Foodbome Disease
Epidemiologists, MDCH) for providing the data.

Many friends and colleagues at Michigan State University provided substantial advice
and encouragement during this project: Mokhtar Arshad, Sarah Miller, Amy Steffey,
Nicole Crisp, Alyssa DiFilippo, Najibah Rehman, Seongbeom Cho, Nasr Aref (National
Food Safety and Toxicology Center), Azfar Siddiqi, Alireza Sadeqhnej ad, Sangchoon
J eon (Department of Epidemiology) and Weixing Song (Department of Statistics).
Finally, I am thankful to my parents, brothers, and sisters for their continuous prayers,

encouragement, and support towards achieving this important milestone of my career.

III

TABLE OF CONTENTS

 

 

 

 

 

List of Ta les vi
List of Figures vii
List of Abbreviations viii
Foodborne Infections l
Salmonella Infection 3

Etiology 3

 

«Ii

Mode of transmission and clinical features

 

 

 

 

 

 

 

 

 

 

 

 

 

Serotypes 4
Salmonella serovar enterica serotype Enteritidis 6
Introduction 5

Study objective 8
Methods 9

Data source and collection 9

Data management and analysis 10
Ethical considerations 1 1
Results 12

Trends of Salmonella Enteritidis infection: Michigan and national estimates

12

Trends of Salmonella Enteritidis infection in Michigan compared with two large

egg-producing states and selected Great Lakes states 13

Stratified data analysis 13
Discussion 15
Conclusions 20

 

21

 

Financial Disclosure

 

 

 

 

Conflict of Interest 21
Figures 23
Tables 37
Appendices 42
References 50

 

LIST OF TABLES

Table 1. Reported outbreaks of Salmonella Enteritidis infection with confirmed vehicles
containing eggs as a principal ingredient

Table 2. Foodborne outbreaks, number of cases, hospitalizations, and deaths due to
Salmonella Enteritidis infection in the US, 1985-1999

Table 3. Common Salmonella serotypes in humans, Michigan, 1995-2001

Table 4. Food vehicles identified in selected foodbome outbreaks of Salmonella
Enteritidis in the United States traced to egg products

Table 5. Adjusted rate ratios (RRs) with 95% confidence intervals (CIs) for risk factors
of Salmonella Enteritidis infection in humans, Michigan 1995-2001.

Table 6. Michigan population by sex, 1990-2003

Table 7. Michigan Population by age groups, 1990-2003

Table 8. Michigan population by race, 1990-2003

Table 9. Michigan population by ethnicity, 1990-2003

Table 10. Michigan population by county, 2000-2004

VI

LIST or FIGURES

Figure 1. Salmonella Enteritidis infection incidence in the United States, 1970-2000
Figure 2. Transovarian transmission of Salmonella Enteritidis infection in laying hens
Figure 3. Transmission routes of Salmonella Enteritidis infection in humans

Figure 4. Surveillance of Salmonella infection in Michigan

Figure 5. Salmonella Enteritidis infection: Michigan and national estimates, 1977-1990
Figure 6. Salmonella Enteritidis infection: Michigan and national estimates, 1995-2001
Figure 7. Common Salmonella serotypes in Michigan, 1995-2001

Figure 8. Salmonella Enteritidis incidence by age group, Michigan, 1995-2001

Figure 9. Salmonella Enteritidis Infection incidence in children, Michigan, 1995-2001
Figure 10. Salmonella Enteritidis infection incidence: Comparison of Michigan and two
large egg producing states: Pennsylvania and California, 1995-2001

Figure 11. Salmonella Enteritidis infection incidence in the selected Great Lake States:
Michigan, Indiana, Illinois and Ohio

Figure 12. Number of Salmonella Enteritidis cases by months, Michigan, 1995-2001
Figure 13. Distribution of Salmonella Enteritidis cases by county, Michigan, 1995-2001

Figure 14. Salmonella Enteritidis infection incidence by county, Michigan, 1995-2001

VII

CDC

CDR

CI

FoodNet

FSIS

HACCP

[RB

LHD

MDCH

PHLIS

US FDA

USDA

LIST OF ABBREVIATIONS

Center for Disease Control and Prevention
Communicable Disease Rules

Confidence Interval

Foodborne Disease Active Surveillance Network
Food Safety Inspection Service

Hazard Analysis Critical Control Point
Institutional Review Board

Local Health Department

Michigan Department of Community Health
Public Health Information Laboratory System
Rate Ratios

United States Food and Drug Administration

United States Department of Agriculture

VIII

F OODBORNE INFECTIONS:

Globally, foodbome illnesses are a major public health concern. Infections spread
through food or beverages are a common, distressing, and sometimes life-threatening
problem for millions of people worldwide. The Centers for Disease Control and
Prevention (CDC) estimates 76 million people experience foodbome illnesses each year
in the United States, accounting for 325,000 hospitalizations and more than 5,000 deaths
(Meads PS, 1999). Known foodbome pathogens cause an estimated 14 million illnesses,
60,000 hospitalizations, and 1,800 deaths annually. More than 250 foodbome diseases
have been described so far (CDC, 2005). In the United States, the majority of foodbome
infections are caused by Salmonella, Campylobacter, and Escherichia coli (E. coli)

(CDC, 1996).

The symptoms of foodbome illnesses vary widely depending on the etiologic agent,
dosage, and immunologic status of the host. However, diarrhea, vomiting, and abdominal
discomfort are the most common symptoms. In the US, regulations for the control of
foodbome and waterborne illnesses have been in place from the early 1900’s.The CDC,
in partnership with state and local counterparts, has been responsible for investigation,

control, and prevention of diseases spread by food and water since 1961.

In 1996, the CDC established the F oodbome Disease Active Surveillance
Network (FoodNet) under the Emerging Infections Program. FoodNet collects data from
10 states on diseases caused by enteric pathogens transmitted commonly through food

(CDC, 1996). The project consists of active surveillance for foodbome diseases and

related epidemiologic studies designed to help public health officials better understand
the epidemiology of foodbome illnesses in the United States. FoodNet specifically targets
seven bacterial pathogens: Campylobacter, E. coli 0157:H7, Listeria, Salmonella,

Shigella, Vibrio, and Yersinia (CDC, 1996; CDC, 1997).

ENTERIC SALMONELLA INFECTIONS
Etiology:

The genus Salmonella consists of gram-negative rods belonging to the family of
Enterobacten'aceae. Salmonella are considered one of the most ubiquitous pathogens,
both in humans and animals (Velge, 2005).

Salmonella are found worldwide in domestic and wild animals, including reptiles, birds,
and insects. Animals with salmonellosis may be asymptomatic carriers or symptomatic,
most commonly with diarrhea. Animals and their products, including meat, poultry, milk,

and eggs represent the principal sources of non-typhoidal Salmonella infection in human.

Salmonella have been recognized for over 100 years as the cause of illnesses ranging
from mild to severe gastroenteritis, bacteremia, septicemia, localized infections, and a
variety of long-term sequelae (Bell, 2002). From the time of first Salmonella isolation
from a diarrheic pig in 1885 by Salmon and Smith and the first laboratory confirmed
outbreak of salmonellosis due to contaminated beef in 1888 (Topley, 1929), Salmonella
have been considered one of the most important foodbome pathogens in the world. The
large number of foodbome outbreaks associated with Salmonella infection are testimony
to the importance of this bacterial genus.

In the United States, 1.4 million non-typhoidal Salmonella infections with 15,000
hospitalizations and 500 deaths are estimated to occur annually (Voetsch, 2004). The
economic impact of sahnonellosis in the United States is reported to be 2.3 billion per

year.

Mode of transmission and clinical features of Salmonella infection:

Salmonella is transmitted through the fecal-oral route. Ingestion of contaminated
food and water is the most important source of human infection. Although a large number
of bacteria are usually needed to cause infection, the bacteria grow well in most types of
food. In foods with a high fat content, such as chocolate and cheese, the infective dose is
very low and just a few bacteria may be sufficient to cause infection (Blaser, 1982). The
susceptibility to infection varies; the critical infective dose is lower in infants, the elderly,
and imunocompromised hosts (Miller, 2000). The onset of disease is often acute with
diarrhea, nausea, and vomiting (Saphra, 1957). An average incubation period is 1—3
(range <1—10) days. The carrier state is normally 4—6 weeks, but some may be
asymptomatic carriers for months or even years (Blaser and Newman, 1982; Buchwald

and Blaser, 1984). No vaccine is available against non-typhoidal salmonellosis.

Salmonella serotypes:

Using the Kauffmann-White scheme for antisera reaction to different bacterial O
and H antigens, more than 2,500 Salmonella serovars have been identified, with
prevalence patterns varying between different geographic locations of the world (Popoff,
2001). However, the majority of Salmonella infections are due to ten common serotypes
among which Typhimurium, Enteritidis, Newport, and Heidelberg are the most common,
Table 3. The degree of host adaptation varies between Salmonella serotypes and affects

the pathogenicity in humans and animals.

Although a great deal is already known about Salmonella, the organisms continue to pose

new challenges to food safety. This is due to the evolution and emergence of new strains

resulting from the acquisition of genes conferring characteristics such as virulence factors
and multiple antibiotic resistance.

Salmonella Enteritidis is the second most common Salmonella serotype and has shown
significant variation with respect to time, place, and age within the United States.
Analysis of Salmonella Enteritidis infection trends can help to strengthen Salmonella
infection control programs in defined geographical regions.

In this report, we described the epidemiology of Salmonella serotype Enteritidis in

Michigan, United States.

EPIDEMIOLOGY OF SALMONELLA ENTERICA
SEROTYPE ENTERITIDIS IN MICHIGAN

Introduction:

One of the major changes in the epidemiology of non-typhoidal salmonellosis in
the second half of the 20th century was the emergence of Salmonella Enteritidis (S.
Enteritidis) as a major foodbome illness (Velge, 2005). S. Enteritidis infection reached a
pandemic level and is now the second most common Salmonella serotype, responsible for
about 17% of all human salmonellosis in the United States (Patrick, 2004; CDC, 2005;
COX, 1995).
The epidemic of S. Enteritidis began in the late 1970s in the northeast region of the
United States and some areas of Europe (St. Louis, 1988). In 1976, 1207 S. Enteritidis
isolates were detected nationwide with an incidence of 0.6 cases per 100,000 population.
The incidence reached 2.4 cases per 100,000 by 1985. From 1980 to 1996, an increase of
S. Enteritidis isolation from 5% to 25% of all Salmonella cultures was reported (CDC,
2000). Figure 1 shows the overall incidence of S. Enteritidis infection in the United
States. According to the Centers for Disease Control and Prevention (CDC, 2000), 677 S.
Enteritidis-related foodbome outbreaks were reported between 1990 and 2001, resulting
in 23,366 illnesses, 1988 hospitalizations, and 33 deaths (CDC, 2000; CDC, 2003).
During 1994, 1995, and 1996, S. Enteritidis surpassed S. Typhimurium to become the
most common Salmonella serotype isolated in the United States (Oslen, 2001). Table 2
shows the foodbome outbreaks, number of cases, hospitalizations and deaths due to S.

Enteritidis infection in the United States between 1985-1999.

Epidemiological investigations of spOradic cases and outbreaks of S. Enteritidis
infections have demonstrated that contaminated eggs and egg-products are major risk
factors (Coyle, 1998; Mead, 1999; Patrick, 2000). Epidemiological studies have shown
that about 80-85% of all S. Enteritidis infection cases are attributed to consumption of
contaminated eggs or egg products. Table 1 shows reported outbreaks of S. Enteritidis
infection with confirmed vehicles containing eggs as a principle ingredient and Table 4
shows food vehicles identified in selected foodbome outbreaks associated with S.
Enteritidis infection traced to egg products in the United States.

The transmission of infection occurs in vivo, not from exterior cocmtamination of the
egg. Figure 2 shows the transovarian transmission of S. Enteritidis infection in laying
hens. Other implicated sources of S. Enteritidis infection in humans include poultry,
meat (Kimura, 2004), and raw almonds (CDC, 2004). Figure 3 shows the various

transmission modes of S. Enteritidis infection in humans.

The reason for the rise in S. Enteritidis in not completely understood. However, the shift
of S. Enteritidis from mice and rodents to laying hens has been cited as a possible cause
of the rise (Bafimler, 2000). Another reason mentioned is the eradication of avian adapted
Salmonella Gallinarium (S. Gallinarium), prevalent in the 19605, from commercial
poultry flocks. The inverse relationship between S. Gallinarium eradication and the rise in
S. Enteritidis infections prompted the hypothesis that S. Enteritidis filled the ecologic

niche vacated by the eradication of S. Gallinarium (Rabsch, 2000).

As a result of on-farm prevention and control initiatives, quality assurance programs, and
education of consumers and food workers regarding the risks of consuming raw or
undercooked eggs in the early 19905, the incidence of S. Enteritidis infection has
decreased significantly. From 1996 to 1999, the rate of culture-confirmed S. Enteritidis
infections declined by 49%, from 3.90 cases to 1.98 cases per 100,000 population
(Patrick, 2004). However, no significant reduction in infection was observed after 2000
and the rate of S. Enteritidis isolation has never returned to the baseline estimates of the
early 19805. In 2002, 5116 of 32,308 (15.8%) Salmonella isolates serotyped were S.
Enteritidis (CDC, 2004). The common S. Enteritidis phage types reported in the United
States are phage type 8 (48.2%), 13a (20.1%), 13 (7.8%), and 14b (7.8%) (Hickman-

Brenner, 1991).

Analyses of the epidemiologic data for S. Enteritidis infections detailing the trends in
different age groups, gender and place of residence, ethnicity and season have not been
reported before. The distribution of S. Enteritidis infection with respect to incidence and
demographic characteristics of reported cases in specific geographical regions is

imperative for evaluating control and prevention programs.

Study objectives:
1. To examine the variation in S. Enteritidis incidence in Michigan by age, sex,
ethnicity, season, and area of residence so study results can be used for the design of a

better prevention effort.

2. To compare the incidence 0f S. Enteritidis infection in Michigan with estimates

on the incidences reported nationally and by selected Great Lake States.

Methods
Data sources and collection

Michigan's public health laws require the reporting of the occurrence or suspected
occm'rence of any disease or medical condition listed in the Communicable Disease Rules
(CDR). Salmonellosis is included in CDR a5 a notifiable disease. Physicians and
laboratories are required to report cases of salmonellosis to local health departments
(LHDs). LHDs investigate suspected cases of salmonellosis and collect patients’
demographic and food history data for submission to Michigan Department of
Community Health (MDCH). Figure 4 shows the surveillance of Salmonella infection in
Michigan. In addition to reporting to MDCH, LHDs also send patients’ clinical
specimens to the Bureau of Laboratories, MDCH for confirmation and serotyping. In this
study, culture confirmed S. Enteritidis cases of human origin from 1995 to 2001 collected
through passive surveillance were included. Data on the demographic characteristics of S.
Enteritidis cases including age, sex, ethnicity, date of reporting, and county of residence
were available for analysis. Age and sex population statistics from the 2000 census were
obtained for each Michigan county from the US Bureau of Census (MDCH, 2005).
Michigan’s S. Enteritidis estimates were compared with national figures, selected Great
Lakes states (Illinois, Indiana, and Ohio), and two large egg producing states (California
and Pennsylvania). Data from respective state health departments, the Public Health
Information Laboratory System (PHILS), and FoodNet were used for this purpose (Bean,

1992; CDC, 2004; CDC, 2005).

10

Data management and analysis:

We categorized age into five groups based on the variation in food exposure and
immunologic status. Because of a relatively lower incidence of S. Enteritidis infection
and the presence of immunocompetence in those aged 15-39 years, this age group was
used as a reference category to compute rate ratios (RRs) for other age groups. The
urban-rural continuum code developed by the US Department of Agriculture (USDA)
was used to categorize counties into urban and rural settings. This code forms a
classification scheme that distinguishes metropolitan counties by size and non-
metropolitan counties by degree of urbanization and proximity to metro areas.

Crude and stratum-specific (age, sex, place of residence, and year of infection) S.
Enteritidis incidences per 100,000 population were calculated using population
denominators reported by the US Bureau of Census. Differences in estimates among
Michigan counties and between urban and rural areas were assessed. Univariate analysis

was to examine associations between independent variables and S. Enteritidis infection.

Poisson regression analysis (Proc Genmod procedure/SAS) was performed to study
associations between S. Enteritidis infection and predictor variables and determine rate
ratios (RRs) adjusted for covariates along with their corresponding 95% confidence

intervals (CIs) (Kleinbaum, 1998).

11

Ethical considerations:

Data were coded and a group level analysis without any identification of study
subjects was performed to maintain the confidentiality of study subjects. The institutional
review board (IRB) for research involving human subjects at Michigan State University

approved the study protocol.

12

Results:

We examined the records of 1296 laboratory-confirmed cases of S. Enteritidis
infections reported during the study period and linked the epidemiologic and laboratory
data before analysis. Overall, the average annual incidence of S. Enteritidis between
1995-2001 in Michigan was 1.87 cases per 100,000 population (1296/68,951,346) with
an incidence of 1.91 cases per 100,000 population (685/35,200,682) in females and 1.81
cases per 100,000 population (611/33,750,664) in males. Among all Salmonella
serotypes, 20.6% (1296/6292) of salmonellosis cases were attributed to S. Enteritidis
infection.

Incidences of 2.04 cases of S. Enteritidis per 100,000 population in rural counties and
1.87 cases per 100,000 population urban counties were found. There was a higher
incidence of S. Enteritidis among children <5 years of age compared to the rate of

infection among other age groups.

Trends of S. Enteritidis in Michigan compared with national, two large egg-
producing States, and selected Great Lake States estimates

A significant reduction in S. Enteritidis incidence, from 4.0 cases per 100,000
population in 1995 to 1.9 cases per 100,000 population during 2001, was observed at the
national level. However, in Michigan, a relatively stable S. Enteritidis infection rate (1.9
cases per 100,000 in 1995 and 1.8 cases per 100,000 population in 2001) was reported for
the same period. Figures 5 and 6 show the comparison of Michigan estimates with
average annual national figures for S. Enteritidis infection.
When compared to Illinois, Indiana, Ohio, California, and Pennsylvania, Michigan had a

relatively lower incidence of S. Enteritidis infection for 1995-2001. Figures 10 and 11

13

show S. Enteritidis incidence in two large egg producing states and selected Great Lake
States, respectively. S. Enteritidis infection was the second most common Salmonella
serotype reported in Michigan during the study period (Figure 7). A higher incidence of
S. Enteritidis (2.6 cases per 100,000 population) was reported during the summer months
(June to August) compared to other months: September to November, 1.7 cases per
100,000 population; December to February, 1.4 cases per 100,000 population; and March

to May, 1.9 cases per 100,000 population (Figure 11).

Stratified analysis: Michigan

From 1995-2001, age-stratified analysis showed little fluctuation of the incidence rate in
children <1 year of age and in children 1-4 years of age. A higher incidence was found in
children <1 year of age compared to the 1-4 year age group (14.23 cases per 100,000
population versus 4.92 cases per 100,000 population: p<0.01). Further analysis of the <1
year age group revealed that the majority of cases are among children <4 months of age
(Figure 8 and 9).

A higher S. Enteritidis incidence rate was observed among Michigan children in the < 5
years age group when compared to the national estimates of the same age group between
2000-2002 (65/100,000 versus 42/100,000; p<0.01) [CDC, 2005].

The majority of S. Enteritidis cases (78.9%) were reported from urban areas, but when
the population denominators were considered, the overall incidence of S. Enteritidis
infection was found to be slightly higher in rural areas than urban regions (2.03 versus
1.84 cases per 100,000). This difference was not statistically significant (p=0.15). Figures

13 and 14 show the distribution and incidence of S. Enteritidis infection, respectively.

14

Univariate and multivariate analysis results for factors associated with S. Enteritidis
infection (age, gender, area of residence, and year of infection) are given in Table 5. The
final covariates-adjusted Poisson model revealed that children <1 of age [RR, 9.75; 95%
CI, 7.99 to 11.90] and children 1-4 years of age [RR, 3.37; 95% CI, 2.83 to 4.02] are at
higher risk of S. Enteritidis infection compared to adults aged 15-39 years. We did not
find a statistically significant difference for S. Enteritidis infection between sex [RR,
1.04; 95% CI, 0.92 to 1.98] or among cases reported from urban and rural areas [RR,
1.13; 95% CL, 0.99-1.29]. Overall, a higher relative rate of S. Enteritidis infection [RR,
1.55; 95% CI, 1.27 to 1.89] was reported in 1998 compared to 1995, 1996, 1997, 1999,

2000, and 2001.

15

Discussion

This study was carried out to assess the incidence and to identify the high-risk groups and
regions associated with S. Enteritidis infection in Michigan. Minimal fluctuation in the
incidence of S. Enteritidis infection was observed in Michigan compared to decreasing
national incidence over the study period. The nationwide declines in the incidence could
be attributed to several control measures implemented in 19905, including the US
Department of Agriculture's Food Safety Inspection Service (F SIS) Pathogen
Reduction/Hazard Analysis Critical Control Point (HACCP) systems regulations in meat
and poultry slaughter houses and processing plants. Additional interventions introduced
during the past several years to prevent foodbome diseases include egg quality assurance
programs for S. Enteritidis, increased attention to fresh produce safety through better
agricultural practices, introduction of HACCP in the seafood industry, regulation of fruit
and vegetable juice, new technologies to reduce food contamination, food safety
education, and increased regulation of imported food (CDC, 2002). Even with these
implementations, Michigan data suggest a stable S. Enteritidis incidence compared to a
decreasing national trend. This highlights a need to further strengthen Michigan’s control
and prevention programs against S. Enteritidis.

We found a relatively lower incidence of S. Enteritidis infection in Michigan compared to
the estimates reported for selected neighboring Midwest states (Illinois, Indiana, Ohio)

and two large egg producing states (Pennsylvania and California).

Nationally, a significantly higher incidence has been reported in children, elderly people,

and individuals with impaired immune systems (Hohmann, 2001). The higher incidence

16

is likely due to the irnmunocompromised status of these groups, making them vulnerable
to many infections including S. Enteritidis. Results of this study suggest that Michigan
children <1 year of age are at a 10 fold higher risk and children 1-4 years of age are at a 3
fold higher risk of acquiring S. Enteritidis infection compared to adults aged 15-39 years,
which is consistent with CDC ’5 FoodNet report (CDC, 1998). The majority of pediatric
cases (<5 years) were sporadic and the sources of infection were often unknown. In
general, pediatric cases account for most of the reported morbidity and mortality
associated with S. Enteritidis (Stutrnan, 1994; Hyams, 1980).

Furthermore, analysis of Michigan children <1 year of age revealed that the incidence is
much higher in children <4 months compared to those 4 months and older, corroborating
the findings of other investigators (Wilson, 1982). The limited variety of foods eaten by
these young children make contaminated food less likely as a source of infection. Person-
to-person transmission from infected family members, (Wilson, 1982; Delarocque—
Astagneau, 1998) ownership of pets, (Wells, 2003) and a contaminated home
environment (Rice, 2003; Schutze, 1999) were reported to be potential routes of
transmission in this age group (Haddock, 1986).

In comparison with national estimates reported by F oodN et, a significantly higher
incidence in Michigan children <5 years of age was found between 2000 and 2002. It is
important to note that the MDCH disease surveillance system collects salmonellosis data
passively, whereas FoodNet uses active surveillance methods for detecting foodbome
infection. Hence, the difference in S. Enteritidis incidence in young children between

Michigan and average national figures may be even higher than mentioned in this report.

17

Analytical studies are needed to identify risk factors for S. Enteritidis infection in
Michigan children. Serotype-specific Salmonella infection data for children <5 years of
age is available at the national level, but the data are not further categorized. Therefore,
data for children <1 year of age are not available for comparison with Michigan statistics.
The difference between incidence in young children and adults may partly be explained
because caretakers are more likely to seek medical treatment for young children who
become ill compared to older children. Similarly, adults with foodbome infection
symptoms are less likely to seek care. Pediatricians more often recommend stool
examinations for young children with diarrhea] symptoms when compared to adult care
physicians. Therefore, the higher reported incidence in young children may also in part
be a reflection of a higher rate of diagnosis.

Epidemiological investigations have shown that the elderly 265 are at higher risk of
acquiring infections, including Salmonella (CDC, 2001). However in our study, only a
marginally significant (p=0.08) difference was found when the 265 age group incidence

was compared tolS-39 year-old age group.

Information regarding race and ethnicity were missing for a significant proportion
(>40%) of cases and could not be analyzed as a potential risk factor for S. Enteritidis
infection. However, the missing data on ethnicity differed substantially by area. Most of
the reported cases were from Wayne and Oakland counties where the majority of the
population is Afiican—American. Food preference and preparation methods vary by race
and ethnicity and it has been reported that incidence of salmonellosis differs across ethnic

groups (CDC, 2005).

18

We did not find an overall difference in S. Enteritidis infection between male and female
populations (p=0.32), consistent with FoodNet report (CDC, 2005). However, age and
gender stratified analysis revealed that male children <1 year and 1-4 years of age had a
higher S. Enteritidis incidence (14.2 cases versus 12.9 cases per 100,000 population and
5.0 cases versus 4.7 cases per 100,000 population) compared to female children of similar
age groups. In adult age groups, incidence of S. Enteritidis infection in females 20-39, 40-
64, and 265 was higher (1.7 cases versus 1.4 cases per 100,000 population, 1.5 cases
versus 1.3 cases per 100,000 population, and 1.9 cases versus 1.6 cases per 100,000
population) than male adults of similar age groups. Perhaps this is because a higher
proportion of adult females than males are involved in cooking and food handling and
therefore are exposed to raw and possibly S. Enteritidis contaminated food.

We did not find a statistically significant difference in the rate of S. Enteritidis infection
between urban and rural dwellers. These findings suggest similar levels of exposure to
potential sources of S. Enteritidis infection among residents in urban and rural areas, such

as eggs, poultry, and vegetables.

Analysis of seasonal variation showed that the seasonal peak for S. Enteritidis infection
varies considerably by calendar year. The increase in S. Enteritidis incidence during the
summer months, June through August, may partly be explained by the hot and humid
weather, favoring survival and replication of the bacterium (Saeed, 1993).

In addition, outdoor cooking and handling of foods at events such as barbecues, picnics,

and camping trips increases during summer. Food safety measures are often inadequate in

19

these settings, placing individuals at higher risk of getting acquiring foodbome infections
including S. Enteritidis.

In Michigan, risk for S. Enteritidis infection was significantly higher in 1998 than during
1995. An increase in all Salmonella serotypes at the national level was also observed in

1998 (CDC, 2004).

Some limitations of the data should be considered when interpreting the results. We used
Michigan’s passively collected surveillance data, so the incidence figures are likely an
under-estimation of actual disease incidence in the population. Most foodbome disease
cases, including S. Enteritidis infection, are considerably under-reported (Mead, 1999;
Hardnett, 2004). A significant percentage of persons with S. Enteritidis infection are not
diagnosed or do not even seek treatment.

Since the last US census was done in 2000, the predicted estimates of population size
reported by the US Bureau of Census were used for 1995-1999 and 2001. It is important
to note that small numbers of cases could affect the calculated incidence rates and their
interpretation. Very few cases with small population denominators can produce high
disease rates and unstable, widely fluctuating disease trends. In our data, some counties
with low populations showed considerably higher S. Enteritidis infection incidence rates
(Figure 2).

The incidence of salmonellosis varies considerably among ethnic groups. However, the
association between race and ethnicity and risk of S. Enteritidis infection could not be

assessed due to the lack of this information in >40% of cases.

20

Conclusions:

Michigan children <5 years of age had an incidence rate of S. Enteritidis infection
that was significantly higher than the average national estimates, meriting immediate
public health attention. Between 1995 and 2001, little fluctuation in the incidence of S.
Enteritidis infections in Michigan was observed, except in 1998 when an increase in the
incidence in both Michigan and nationally was observed. Risk factors for S. Enteritidis
infection in Michigan children should be identified in order to devise effective control
and prevention measures. As an intervention, public education about food safety
measures against S. Enteritidis infection for mothers and other caregivers may help curb
infection in children. Mass media, especially during summer months, should be used to

provide food hygiene information to the general population.

21

Funding source: This research was supported by the NIH- Contract No. N01-AI-30058.
(Microbiology Research Unit, MSU), while supplemental funds were provided by the
Office of the Research Associate Dean of the College of Veterinary Medicine at

Michigan State University.

Conflict of interest: No conflict of interest is declared.

22

 

Figure 1. Salmonella Enteritidis infection incidence in the United States, 1970-2000

 

.b

 

1

DJ

1

 

 

 

 

 

 

 

 

 

—

 

 

N
br—inNmmin-Am
: l '

 

 

O

 

 

O

S. Enteritidis incidence per 100,000 population

 

 

23

Figure 2. Transovarian transmission of Salmonella Enteritidis infection in
Laying hens (Source: A. M Saeed, 1999)

 

24

Figure 3. Transmission routes of Salmonella
Enteritidis infection (Saeed AM, 2006)

 

Reservoir
mice and other

rodents

 

 

Poultry flocks

Transovarian
transmission

Cross -
contamination

Poultry meat Eggs ___) Otherfoods

Egg-containing
foods

1

   
   

  

Humans
gastroenteritis

 

 

 

25

Figure 4. Surveillance of Salmonella infection in Michigan

 

Centers For Disease Control and Prevention

 

 

 

f

Michigan Department of Community

 

 

 

 

 

 

 

 

 

 

 

Health
Local Health Department
I 1
Physicians Laboratories

 

 

 

 

 

 

26

 

Figure 5. Salmonella Enteritidis infection: Michigan and average national
estimates, 1977-1990

 

 

 

 

 

 

 

 

 

lee—“Michigan State it

. —I— United States

 

Incidence per 100,000

 

 

 

 

fcf’nqSe‘qS‘rcb'betsfiebéeq’s’l
soaeeeeeeeeeeefi

Year

 

US: Chi square trend= 12785; p-value=< 0.01. Michigan:
Chi square trend= 218.953; p-value= < 0.01

 

 

27

Figure 6. Salmonella Enteritidis infection: Michigan and average national
estimates, 1995-2001

 

 

 

 

 

 

 

 

 

 

 

Incidence per 100,00

 

 

 

 

 

 

1995 1996 1997 1998 1999 2000 2001 2002

 

 

Year

 

 

l—o—United_fiStates—:_l_— Michiga:l _ VJ

 

 

 

28

Figure 7. Common Salmonella serotypes in Michigan, 1995-2001

4.0

3.5—--

3.0

S. Enteritidis incidence per 100,000
population
N
o

 

 

 

 

 

 

 

 

 

 

0-0 I I I F l
1995 1996 1997 1998 1999 2000 2001
Year case reported
+ S. typhinmrium + S. enlen'tidis S. lreidelberg + S. newport J

I
*_ __._._ _ _ _

29

Figure 8. Salmonella Enteritidis incidence by age group, Michigan, 1995-2001

 

16.0
14.0q — ___..." . _ M

 

 

 

 

12.0. ~_. . . f LL--- , m

 

 

 

 

...
5‘.
ts»
10 0 ~#
...
_ ‘._. .. __k . .!_ ___. _ 7, . -. ,M, -__
- 4:;
..
t...
7?:
5‘:
6
.
8 0 i it" —— if #—
..5 ___fi __, ___“ ,__ i_—, 7777 ,, » ___ 7, i4._7, 7 7 ,,,.
0 ‘i‘.
_.
.
-.
II.
if,
.

4.0 -

l

2.0 «

l

 

Average annual incidence of S. enteritidis
(per 1000 00 population)

 

 

 

 

   

o.o
bx 0.: Q) bx Co
6329 b9y6y§W$ofok 9963M; 09g}

Age group

30

Figure 9. Salmonella Enteritidis infection incidence in children, Michigan, 1995-2001

18.0
16.0 —
14.0 -
12.0 —
10.0 -
8.0 4
6.0 «
4.0 -
2.0 «
0.0 . . . -

1 995 1 996 1 997 1 998 1 999 2000 2001

 

Incidence per 100,000

 

 

 

Year

].‘;.’-2iy_é;{£ an ' " 144 years—0F

 

31

Figure 10. Salmonella Enteritidis infection incidence: Comparison of Michigan and two

large egg producing states, Pennsylvania and California, 1995-2001

 

 

 

 

 

 

 

 

 

 

 

___—___ ___ l

 

l 1995 1996 1997 1998 1999 2000 2001

 

L—O— California —I— Pansylvania -b.— Michigan! 1

l _.__

 

 

32

Figure 11. Salmonella Enteritidis infection incidence in selected

Great Lake States: Michigan, Indiana, Illinois, and Ohio

 

po
3"
O

l

l

l
4L

S. Enteritidis incidence per 100,000
pulatron

 

 

 

1995 1996 1997 I998 1999 2000 2001

Year of case reported

 

IMichigan Ulndiana Illlinois IOhioJl

 

33

Figure 12. Number of Salmonella Enteritidis cases by month, Michigan, 1995-2001

 

Number of cases
as
O
l
l
l
l

 

 

 

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Month

34

Figure 13. Distribution of Salmonella Enteritidis cases by county, Michigan, 1995-2001

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

One dot=l case

Wanye

35

Figure 14. Salmonella Enteritidis infection incidence by county, Michigan, 1995-2001

 

       

13-18 cases/100,000
19-13 cases/100.000

36

Table 1. Reported outbreaks of Salmonella Enteritidis infection with confirmed vehicles

containing eggs as a principal ingredient

 

 

Year No of outbreaks Outbreaks with Outbreaks with a confirmed
confirmed vehicle vehicle containing eggs

# # # (% )1:

1985 26 14 10 (71)

1986 47 22 15(68)

1987 58 28 21(75)

1988 48 25 20(80)

1989 81 30 19(63)

1990 85 30 24(80)

1991 74 29 20(69)

1992 63 35 31(88)

1993 66 40 31(77)

1994 51 29 22(76)

1995 56 22 15(68)

1996 47 26 21(81)

1997 46 22 19(86)

1998 49 18 15(83)

1999 44 19 15(79)

 

*Of all outbreaks with confirmed vehicle, % of outbreaks with a confirmed vehicle that contained eggs

37

Table 2. Foodborne outbreaks, number of cases, hospitalizations, and deaths due to

Salmonella Enteritidis infection in the US, 1985-1999

 

Year No. of No. ill Median no. of No. of No. of
outbreaks cases Hospitalization deaths
1985 26 1159 24.0 144 1
1986 47 1444 12.0 107 6
1987 58 2616 17.5 557 15
1988 48 1201 12.5 155 11
1989 81 2518 23.0 206 15
1990 85 2656 18.0 318 3
1991 74 2461 15.0 200 5
1992 63 2348 13.0 233 4
1993 66 2215 16.5 219 6 -
1994 51 5492 14.0 214 0
1995 56 1312 12.0 113 8
1996 47 1414 12.0 158 2
1997 46 1102 13.0 124 0
1998 49 744 10.0 93 3
1999 44 1080 15.0 63 0

 

38

Table 3. Common Salmonella serotypes in humans, Michigan, 1995-2001*

 

Serotype 1995 1996 1997 1998 1999 2000 2001 Total

Typhimurium 188(1) 259(1) 232(1) 311(1) 221(1) 200(1) 185(1) 1596(1)
Enteritidis 158(2) 161(2) 202(2) 247(2) 184(2) 189(2) 168(2) 1309(2)
Heidelberg 65(3) 80(3) 55(3) 67(3) 56(3) 72(3) 71(3) 466(3)
Newport 30(5) 32(4) 18(6) 25(8) 34(5) 32(6) 51(4) 222(4)
Java 24(8) 31(5) 13(9) 27(7) 21(9) 33(5) 29(5) 178(5)
Thompson 17(12) 23(6) 38(4) 31(6) 34 (5) 19(7) 16(8) 178(6)
Oranienburg 30 (5) 23 (6) 17(7) 45(4) 23(8) 18(8) 18(7) 174(7)
Agona 29(7) 16(9) 37(5) 40(5) 14(12) 10(11) 11(11) 157(8)
Muenchen 19(9) 13(12)17(7) 13(11) 50(4) 5(14) 13(10) 130(9)
Braenderup 12(14)14(10)11(11)8(15) 10(14) 58(4) 6(9) 119(10)
Saintpaul 18(10) 19(8) 6(14) 13(11)13(13)9(12) 26(6) 104(11)
Infantis 14(13)9(13) 11(11)12(14)29(7) 18(8) 8(14) 101 (12)
Montevideo 11(15)14(10)8(13) 18(9) 21(9) 18(8) 9(12) 99(13)
Stanley 55(4) 9(13) 4(15) 14(10)5(15) 5(14) 4(15) 96(14)
Javiana 18(10) 7(15) 12(10)13(11)15(11)7(13) 9(12) 81(15)
Unknown 14 21 20 35 29 31 58 208

Total 863 937 846 1097 898 846 805 6292

 

*Numbers in parentheses are ranks

39

Table 4. Food vehicles identified in selected foodbome outbreaks of Salmonella
Enteritidis in the United States traced to egg products

 

 

Year Food vehicles Reported number States
of cases
1990 Hollandaise sauce 169,42 CT, KY
Bread pudding (shell egg) 1100 IL
1991 Bread stuffing 393 NY
Caesar salad dressing 38 Not available
1992 Lasagna (shell eggs) 9 OH
Banana pudding with meringue 191 NJ
Egg batter 434 NY
Imitation crab meat pancakes (shell 118 MD
eggs) 27 PA
1993 Mayonnaise (shell eggs) 38 CA
Egg rolls (shell eggs) 130 TX
Hard boiled eggs 175 VT
1994 Hollandaise sauce 56 DC
1995 Rice pudding (shell eggs) 7 PA
Scrambled eggs 40 DJ
Caesar Salad dressing (shell eggs) 28 NY
1996 Eggnog (shell eggs) 5 NA
Chicken fried steak (shell eggs) 30 UT
French toast (shell eggs) 74 CA
1997 Beamaise sauce (shell eggs) 30 NJ
Pastries (shell eggs) 17 CT
Chopped boiled eggs 192 SC
1998 Chile rellenos (shell eggs) 50 MD
Ziti (shell eggs) 71 NV
2002 Bakery made cake 200 M1

 

40

Table 5. Adjusted rate ratios (RRs) with 95% confidence intervals (CIs) for risk factors
of S. Enteritidis infection in humans, Michigan 1995-2001.

 

Incidence Unadjusted RR Adjusted RR
Variables Cases Population (Per 100,000) (95% CI) (95% CI)

Age in years

<1 131 920,358 14.23 9.72 (796-1187) 9.75 (7.99-11.90)
1-4 188 3,817,594 4.92 3.36 (2.82-4.01) 3.37 (2.83-4.02)
5-14 171 1,028,7464 1.66 1.13 (0.95-1.36) 1.13 (095-136)
15-39* 366 2,500,3977 1.46 - -

40-64 291 2,043,1574 1.42 0.97 (0.83-1.13) 0.97 (0.83-1.13)
265 149 8,488,269 1.76 1.19 (1.00-1.45) 1.18 (0.98-1.43)

Gender
Male“ 611 3,374,8554 1.81 - -
Female 685 3,520,0682 1.95 0.93 (0.83-1.03) 0.92 (0.83-1.02)

Area of residence
Urban“ 1023 5,555,4746 1.84 — -
Rural 273 1,339,4490 2.03 1.10 (0.96-1.26) 1.13 (0.99-1.29)

Year of infection

1995* 157 9,676,211 1.62 - -

1996 161 9,758,645 1.65 1.01 (0.81-1.26) 1.02 (0.82-1.27)
1997 201 9,807,839 2.05 1.26 (1.02-1.55) 1.27 (1.03-1.57)
1998 245 9,847,044 2.49 1.53 (1.25-1.55) 1.55 (1.27-1.89)
1999 179 9,897,116 1.81 1.11(0.89-1.38) 1.13 (0.91-1.40)
2000 187 9,956,115 1.88 1.15 (0.93-1.43) 1.17 (O.95-1.45)
2001 166 1,000,6266 1.66 1.02(0.82-1.27) 1.04 (0.83-1.29)

 

1
Reference category (final Poisson regression model included age, gender, area of residence, and year of

infection)

41

Appendices:

Table 6. Michigan population by sex, 1990-2003

 

 

Year Male Female Total population
# % # %

2003 4,951,811 49.10 5,128,174 50.90 10,079,985
2002 4,934,223 49.10 5,1 16,223 50.90 10,050,446
2001 4,909,789 49.10 5,096,477 50.90 10,006,266
2000 4,882,431 49.00 5,073,684 51.00 9,956,115
1999 4,849,346 49.00 5,047,770 51.00 9,897,116
1998 4,819,883 48.90 5,028,059 51.10 9,847,942
1997 4,797,299 48.90 5,011,752 51.10 9,809,051
1996 4,768,273 48.90 4,990,372 51.10 9,7 5 8,645
1995 4,723,643 48.80 4,952,568 51.20 9,676,211
1994 4,680,552 48.80 4,917,185 51.20 9,597,737
1993 4,648,175 48.70 4,891,939 51.30 9,540,114
1992 4,613,264 48.70 4,865,801 51.30 9,479,065
1991 4,569,627 48.60 4,830,819 51.40 9,400,446
1990 4,521,575 48.60 4,789,744 51.40 9,311,319

 

42

Table 7. Michigan population by age groups, 1990-2003

 

Year .

2003

2002

2001

2000

1999

1998

1997

1996

1995

1994

1993

1992

1991

1990

Under 18 Years

#
2,538,920
2,570,264
2,573,235
2,575,677
2,587,289
2,582,413
2,582,841
2,576,910
2,564,834
2,541,302
2,527,010
2,503,024
2,487,028

2,461,093

%

25.20

25.60

25.70

25.90

26.10

26.20

26.30

26.40

26.50

26.50

26.50

26.40

26.50

26.40

18-44 Years

#
3,842,349
3,862,991
3,885,613
3,902,990
3,915,222
3,938,274
3,957,399
3,973,562
3,969,539
3,977,692
3,992,099
4,010,415
4,024,913

3,996,807

%

38.10

38.40

38.80

39.20

39.60

40.00

40.30

40.70

41.00

41.40

41.90

42.30

42.80

42.90

45-64 Years

#
2,462,215
2,385,271
2,320,660
2,256,095
2,180,031
2,114,822
2,058,413
2,001,756
1,945,502
1,896,665
1,852,492
1,814,839
1,758,168

1,744,01 1

%

24.40

23.70

23.20

22.70

22.00

21.50

21.00

20.50

20.10

19.80

19.40

19.20

18.70

18.70

265 Years

#
1,236,501
1,231,920
1,226,758
1,221,353
1,214,574
1,212,433
1,210,398
1,206,417
1,196,336
1,182,078
1,168,513
1,150,787
1,130,337

1,109,408

%

12.30

12.30

12.30

12.30

12.30

12.30

12.30

12.40

12.40

12.30

12.30

12.10

12.00

11.90

 

43

Table 8. Michigan population by race, 1990-2003

 

Year

2003

2002

2001

2000

1999

1998

1997

1996

1995

1994

1993

1992

1991

1990

White

#
8,282,727

8,269,209
8,246,254
8,217,699
8,186,898
8,166,073
8,150,817
8,123,578
8,068,832
8,020,513
7,988,856
7,954,555
7,902,325

7,844,171

%
82.20

82.30

82.40

82.50

82.70

82.90

83.10

83.20

83.40

83.60

83.70

83.90

84.10

84.20

#
1,490,546

1,484,848
1,475,580
1,467,272
1,455,082
1,441,513
1,428,471
1,416,589
1,401,822
1,382,963
1,364,873
1,345,171
1,325,382

1,302,647

%
14.80

14.80

14.80

14.70

14.70

14.60

14.60

14.50

14.50

14.40

14.30

14.20

14.10

14.00

#
72,497

73,104
73,638
73,689
71,513
69,623
67,978
66,463
64,432
62,545
61,193
59,991
59,01 1

57,434

0/0
0.70

0.70

0.70

0.70

0.70

0.70

0.70

0.70

0.70

0.70

0.60

0.60

0.60

0.60

Asian and
African American Native American Pacific Islander

#
234,215

223,285
210,794
197,455
183,623
170,733
161,785
152,015
141,125
131,716
125,192
119,348
113,728

107,067

%
2.30

2.20

2.10

2.00

1.90

1.70

1.70

1.60

1.50

1.40

1.30

1.30

1.20

1.20

 

 

44

Table 9. Michigan population by ethnicity, 1990-2003

 

 

Year # Hispanic % #Non-Hispanis/o
2003 357,339 3.60 9,722,646 96.50
2002 349,166 3.50 9,701,280 96.50
2001 337,088 3.40 9,669,178 96.60
2000 326,846 3.30 9,629,269 96.70
1999 307,670 3.10 9,589,446 96.90
1998 291,317 3.00 9,556,625 97.00
1997 276,535 2.80 9,532,516 97.20
1996 262,484 2.70 9,496,161 97.30
1995 247,532 2.60 9,428,679 97.40
1994 235,489 2.50 9,362,248 97.60
1993 226,421 2.40 9,313,693 97.60
1992 218,133 2.30 9,260,932 97.70
1991 211,302 2.30 9,189,144 97.80
1990 202,246 2.20 9,109,073 97 .80

 

45

Table 10. Michigan population by county, 2000-2004

 

 

County 2003 2002 2001 2000
Alcona 11,572 11,455 11,648 11,707
Alger 9,767 9,796 9,816 9,840
Allegan 110,331 109,336 107,877 106,113
Alpena 30,781 31,026 31,245 31,291
Antrim 24,094 23,809 23,478 23,267
Arenac 17,309 17,185 17,245 17,298
Baraga 8,782 8,694 8,745 8,740
Barry 58,774 57,943 57,454 56,909
Bay 109,452 109,672 109,694 110,122
Benzie 17,078 16,818 16,462 16,113
Berrien 162,766 162,285 162,026 162,629
Branch 46,414 46,189 45,849 45,871
Calhoun 138,854 138,375 138,175 138,085
Cass 51,385 51,284 51,273 51,161
Charlevoix 26,712 26,386 26,351 26,154
Cheboygan 27,405 27,072 26,831 26,566
Chippewa 38,822 38,898 38,530 38,564
Clare 31,589 31,686 31,364 31,378
Clinton 67,609 66,668 65,695 64,965
Crawford 14,808 14,734 14,544 14,345

 

46

 

Delta
Dickinson
Eaton
Emmet
Genesee
Gladwin
Gogebic
Grand Traverse
Gratiot
Hillsdale
Houghton
Huron

In gham
Ionia
Iosco
Iron
Isabella
Jackson
Kalamazoo
Kalkaska
Kent

Keweenaw

38,317
27,186
106,197

32,741

38,336

27,325

105,590

32,329

442,250 441,423

26,939
17,329
82,011
42,501
47,230
36,249

35,216

26,745
17,407
81,263
42,365
46,980
35,883

35,422

282,030 281,362

63,573
26,888
12,787
64,663
162,321
242,110
17,177
590,417

2,227

62,941
26,979
12,736
64,523
160,972
241,471
17,043
587,951

2,204

38,418
27,291
104,659
32,109
438,800
26,421
17,706
79,943
42,329
46,763
35,746
35,685
280,486
62,054
27,213
12,916
63,893
159,826
239,621
16,833
582,487

2,283

38,562
27,481
103,916
31,536
436,943
26,126
17,325
77,980
42,312
46,687
35,999
36,053
279,474
61,669
27,336
13,1 13
63,370
158,724
238,877
16,626
576,330

2,309

 

47

 

Lake 11,795 11,623 11,609 11,391
Lapeer 91,314 90,776 89,495 88,315
Leelanau 21,860 21,722 21,535 21,262
Lenawee 100,786 100,145 99,517 99,050
Livingston 172,881 168,862 163,712 158,459
Luce 6,919 7,027 7,059 7,010
Mackinac 1 1,470 1 1,505 11,713 1 1,924
Macomb 813,948 808,529 800,392 790,879
Manistee 25,317 25,082 24,801 24,639
Marquette 64,616 64,342 64,566 64,613
Mason 28,685 28,879 28,508 28,338
Mecosta 41,728 41,465 40,897 40,658
Menominee 25,084 25,109 25,231 25,293
Midland 84,492 84,1 19 83,780 83,017
Missaukee 15,189 14,950 14,741 14,551
Monroe 150,673 149,253 147,930 146,481
Montcalm 62,926 62,420 61,917 61,445
Montrnorency 10,492 10,560 10,517 10,376
Muskegon 173,090 171,765 171,166 170,521
Newaygo 49,271 49,013 48,738 48,024
Oakland 1,207,869 1,202,721 1,201,646 1,196,497
Oceana 28,074 27,650 27,181 26,975

 

48

 

Ogemaw
Ontonagon
Osceola
Oscoda
Otsego
Ottawa
Presque Isle
Roscommon
Saginaw

St. Clair

St. Joseph
Sanilac
Schoolcraft
Shiawassee
Tuscola
Van Buren
Washtenaw
Wayne

Wex ford

21,792
7,571
23,509
9,461
24,268
249,391
14,286
26,230
209,327
169,063
62,864
44,583
8,772
72,543
58,382

78,210

21,758
7,703
23,500
9,449
24,155
245,913
14,320
25,818
210,087
167,712
62,366
44,535
8,778
72,122
58,249

77,235

338,562 334,351

2,028,778 2,045,540

31,251

30,777

21,707
7,732
23,306
9,495
23,779
243,528
14,379
25,744
209,973
166,237
62,515
44,518
8,869
72,053
58,353
76,733
329,308
2,052,964

30,638

21,689
7,802
23,244
9,421
23,426
239,494
14,374
25,528
209,945
164,710
62,541
44,537
8,917
71,700
58,289
76,355
324,483
2,059,529

30,547

 

49

References:

Baumler A. An epidemic of food poisoning in the US. Environ Rev 2000; 7:2-5.

Bean NH, Martin SM, Bradford H. An electronic system for reporting public health data

from remote sites. Am J Public Health 1992; 82:1273-1276.

Bell C, Kyriakides A. Salmonella in foodbome pathogens: hazard, risk and control.

Edited by Blackburn CW and McClure PJ 2002; 307-335.

Binkin N, Scuderi G, Novaco F, et a1. Egg-related Salmonella Enteritidis, Italy, 1991.

Epidemiol Infect 1993; 110: 227-237.

Blaser MJ, Newman LS. A review of human salmonellosis: Infective dose. Rev Infect

Dis 1982; 4(6): 1096-1 106.

Buchwald DS, Blaser MJ. A review of human salmonellosis: Duration of excretion

following infection with nontyphi Salmonella. Rev Infect 1984; 6(3):345-56.

Buzby JC. Children and microbial foodbome illness. Food Review 2001; 24(2):32-37.

CDC. Summary of Notifiable Diseases - United States, 2001. MMWR 2003; 50(53);1-

108.

50

Cox JM. Salmonella enteritidis: the egg and 1. Aust Vet J 1995; 72: 108-115.

Centers for Disease Control and Prevention. Preliminary FoodNet data on the incidence
of infection with pathogens transmitted commonly through food - 10 Sites, United States

2004. Morb Mortal Wkly Rep 2005; 54: 352-356.

Centers for Disease Control and Prevention. 1996 Final FoodNet surveillance report.

Atlanta, CDC 1998.

Centers for Disease Control and Prevention. Public Health Laboratory Information
System, CDC Salmonella surveillance summaries 1976—1999. Washington: US.

Government Printing Office, 2000.

Centers for Disease Control and Prevention. Outbreaks of Salmonella serotype Enteritidis
infection associated with eating shell eggs—United States, 1999-2001. J AMA 2003;

289:540-541.
Centers for Disease Control and Prevention. Outbreak of Salmonella serotype Enteritidis
infections associated with raw almonds--United States and Canada, 2003-2004. Morb

Mortal Wkly Rep 2004; 53:484-487.

Centers for Disease Control and Prevention. Public Health Laboratory Information

System surveillance data: annual Salmonella summaries, 1995-2002. Available at:

51

http://www.cdc.gov/noidod/dbmd/phlisdata/salmonella.htm. [Accessed 5 November,

2004)

Centers for Disease Control and Prevention. F oodNet presentation: Age, ethnic and racial
disparity in Salmonella serotype Enteritidis: FoodNet, 1998-2000. Available at:
http://www.cdc.gov/foodnet/pub/iceid/2002/marcus_r.htm. [Accessed on 22 March,
2005]

Centers for Disease Control and Prevention. The Foodborne Diseases Active Surveillance

Network, 1996. Morb Mortal Wkly Rep 1997; 46:258-261.

Centers for Disease Control and Prevention. Incidence of foodbome illnesses---FoodNet,

1997. Morb Mortal Wkly Rep 1998; 47:782-786.

Centers for Disease Control and Prevention. Preliminary FoodNet data on the incidence
of foodbome illnesses-selected sites, United States, 2001. Morb Mortal Wkly Rep 2000;

51:325-329.

Coyle EF, Palmer SR, Ribeiro CD, Jones HI, Howard AJ, Ward L, Rowe B. Salmonella
enteritidis phage type 4 infection: Association with hen's eggs. Lancet 1998; 2: 1295-

1297.

Delarocq’ue-Astagneau E, Desenclos J C, Bouvet P, Grimont PA. Risk factors for the
occurrence of sporadic Salmonella enterica serotype enteritidis infections in children in

France: A national case-control study. Epidemiol Infect 1998; 121:561-567.

52

Hardnett FP, Hoekstra RM, Kennedy M, Charles L, Angulo FJ. Emerging Infections
Program F oodNet Working Group. Epidemiologic issues in study design and data

analysis related to F oodNet activities. Clin Infect Dis 2004; 15:121-126.

Haddock RL, Malilay J. A search for infant salmonellosis risk factors on Guam.

Southeast Asian J Trop Med Public Health 1986; 17:38-42.

Health care professional’s guide to the Michigan communicable disease rules. Lansing:

Michigan Department of Community Health, 2001.

Hohmann EL. Nontyphoidal salmonellosis. Clin Infect Dis 2001; 15:263-269.

Hickman-Brenner FW, Stubbs AD, Farmer JJ. Phage typing of Salmonella Enteritidis in

the United States. J Clin Microbiol 1991; 29:2817-2823.

Hyams J S, Durbin WA, Grand RJ, Goldmann DA. Salmonella bacteremia in the first year

of life. J Pediatr 1980; 96:57-59.

Kimura AC, Reddy V, Marcus R, et a1. Chicken consumption is a newly identified risk
factor for sporadic Salmonella enterica serotype Enteritidis infections in the United

States: A case-control study in FoodNet sites. Clin Infect Dis 2004; 15:244-252.

53

Kleinbaum DG, Kupper LL, Muller KE, Nizam A. Applied Regression Analysis and
Multivariable Methods. 3rd ed. Duxbury Press: Brooks/Cole Publishing Company, 1998;

687-709.

Mead PS, Slutsker L, Dietz V, et a1. F cod-related illness and death in the United States.

Emerg Infect Dis 1999; 52607-625.

Miller SL, Pegues DA. Salmonella species, including Salmonella typhi. Mandel GL,
Bennet J E, Dolin R, eds. Principle and practice of infectious diseases, 5th ed. New York:

Churchill Livingstone, 2000; 2344-2359.

Michigan Department of Community Health. Population Trends. Available at:

http://www.mdch.state.mi.us/pha/osr/Index.asp?ld=17. [Accessed on 12 January, 2005].

Olsen SJ, Bishop R, Brenner F W, Roels TH, Bean N, Tauxe RV, Slutsker L. The
changing epidemiology of Salmonella: Trends in serotypes isolated from humans in the

United States, 1987-1997. Infect Dis 2001; 183:753-761.

Patrick ME, Adcock PM, Gomez TM, et a1. Salmonella enteritidis infections, United

States, 1985—1999. Emerg Infect Dis 2004; 10:1-7.

Popoff MY, Bockemuhl J, Brenner FW, Gheesling LL. Supplement 2000 (no. 44) to the

Kauffmann-White scheme. Res Microbiol 2001; 152(10):907-9.

54

Rabsch W, Hargis BM, Tsolis RM,et a1. Competitive exclusion of Salmonella enteritidis

by Salmonella gallinarum in Poultry. Emerg Infect Dis 2000; 62443-448.

Rice DH, Hancock DD, Roozen PM, et a1. Household contamination with Salmonella

enterica. Emerg Infect Dis 2003; 9: 120-122.

Saeed AM, Koons CW. Growth and heat resistance of Salmonella enteritidis in

refrigerated and abused eggs. J Food Protection 1993; 56:927-931.

Saphra 1, Winter J W. Clinical manifestations of sahnonellosis in man; an evaluation of
7,779 human infections identified at the New York Salmonella Center. N Engl J Med

1957; 256(24):1128-34.

Schutze GE, Sikes JD, Stefanova R, Cave MD. The home environment and salmonellosis

in children. Pediatrics 1999; 10321-5.

St. Louis ME, Morse DL, Potter ME, et al. The emergence of grade A eggs as a major

source of Salmonella enteritidis infections: new implications for the control of

salmonellosis. JAMA 1998; 259:2103-2107.

Stutman HR. Salmonella, Shigella, and Campylobacter: Common causes of infectious

diarrhea. Pediatr Ann 1994; 23:538-543.

55

Topley W, Wilson GS. The principles of Bacteriology and Immunity, Vol. 11.. Edward

Arnold and Co., London, 1929; 1037-8.

Velge P, Cloeckaert A, Barrow P. Emergence of Salmonella epidemics: the problems
related to Salmonella enterica serotype Enteritidis and multiple antibiotic resistance in

other major serotypes. Vet Res 2005; 36:267-288.

Voetsch AC, Van Gilder TJ, Angulo F J , Farley MN, Shallow S, et a1.. F oodNet estimate
of the burden of illness caused by nontyphoidal Salmonella infections in the United

States. Clin. Infect. Dis. 2004; 38(Suppl 3): 8127-34.

Wells EV, Boulton M, Hall W, Bidol SA. Reptile-associated salmonellosis in preschool-

aged children in Michigan, January 2001-June 2003. Clin Infect Dis 2004; 39:687-691.

Wilson R, Feldman RA, Davis J, LaVenture M. Salmonellosis in infants: The importance

of intrafarnilial transmission. Pediatrics 1982; 69:436-438.

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