‘04-- I A

THE COMPARATIVE MECROSCGNC
AMTQMY OF THE TRACHEAS OF
gas, CARA-AND om

 

Them for flu Dunno of M. 5..
RECHEGAN STATE UNLVER‘S'K’TY
Ciedith A. Miller. Jr.
1.963

THESIS

LIBRARY

Michigan State
University '

 

Frontispiece

A sketch of a typical section from a trachea showing

both cross-sectional and longitudinal views.

 

 

 

 

 

 

 

THE COMPARATIVE MICROSCOPIC ANATOMY
OF THE TRACHEAS 0F

BOS, CAPRA, AND OVIS

 

By

Cledith A. Miller, Jr.

A THESIS

Submitted to the College of Veterinary Medicine of Michigan
State University of Agriculture and Applied Science
in partial fulfillment of the requirements
for the degree of

MASTER OF SCIENCE

Department of Anatomy

1963

ACKNOWLEDGMENTS

The author wishes to express his genuine gratitude to his major
professor and friend, Dr. M. Lois Calhoun, Chairman and Professor,
Department of Anatomy, for her patience and excellent guidance during
the course of this investigation. Her contributions to this manuscript
have given meaning to the scientist's basic tool--exacting observation
and its conveyance to others that they, too, might share in the under-
standing and appreciation of the organized, living system.

The writer is indebted to Dr. C. W. Titkemeyer, Associate Professor,
Department of Anatomy, for his comments and suggestions on the prepara-
tion and manner of expression of anatomical concepts contained in this
work, and to Dr. Esther M. Smith, Associate Professor, Department of
Anatomy, for her skilled assistance in and invaluable contributions to
the preparation of the photomicrographs.

Thanks are due to Mr. Richard Witter, Misses Betty Mason, Pauline
Ho, and Effie Lou Ball, for they had performed the initial efforts in
this study. Their suggestions on technical methods proved beneficial
throughout this investigation.

That this manuscript is a reality is in large part the result of
the efforts and labors, as well as the constant encouragement of Miss
Margaret R. Kuxhaus. The author is deeply grateful to her for having
given so many hours to the preparation of this paper.

The writer wishes to express his heartfelt thanks to his parents,

who have made this undertaking possible. He is forever grateful to them.

ii

TABLE OF

Frontispiece

INTRODUCTION . . . .

REVIEW OF LITERATURE
Mucosa
Submucosa . . . .
Glands . .
Cartilage .
Annular Ligament .
Trachealis Muscle.

Adventitia . . .

Blood and Lymphatic Vessels

Nerves . . .
MATERIALS AND METHODS .
RESULTS AND DISCUSSION.

MUCOSA . . .

Epithelium. .

Bos . .
Capra. .
Ovis . .

 

 

CONTENTS

iii

Page

11
12
13
15
15
l7
l7
l7
19
21
21
21
23
23
23
23
23
23

23

Lamina Propria .

SUBMUCO$A . . . o

 

GLANDS .

CARTILAGE .

ANNULAR LIGAMENT .

TRACHEALIS MUSCLE. .

BLOOD AND LYMPHATIC VESSELS

NERYES . .

ADVENT ITIA O O O

COMPARATIVE HISTOLOGY

SUMMARY AND CONCLUSIONS

LITERATURE CITED.

iv

24
26
26
27
27
27
29
30
31
32
32
33
33
44

48

Table

LIST OF TABLES

Measurements (in microns) of microscopic
structures of the trachea of B03. . . . . .

Measurements (in microns) of microscopic
structures of the trachea of Capra . . . . .

Measurements (in microns) of microscopic
structures of the trachea of Ovis . . . . .

Comparison of the mean values (in microns)

of the structural dimensions of the tracheas
of B03, Capra, and Ovis at the dorsal, lateral,
and ventral regions . . . . . . . . .

Comparison of the mean values (in microns)

of the structural dimensions of the tracheas

of Egg, Ca ra, and Ovis at the cranial, middle,
and caudal levels. . . . . . . . . .

Comparison of the total mean values (in microns)
of microscopic structures of the tracheas of
303, Capra, and Ovis. . . . . . . . . .

Page

35

37

39

41

42

43

Plate

II.

III.

IV.

VI.

VII.

VIII.

XI.

XII.

LIST OF PLATES

Page
A comparison of cross-sectional views of the
bovine, caprine, and ovine tracheas; ventral
region, caudal level. . . . . . . . . . . . 52
Cross-sectional view of ovine tracheal epi-
thelium and its four cell types; ventral
region, cranial level . . . . . . . . . . . 53
Cross-sectional view of ovine tracheal mucous
membrane; lateral region, middle level. . . . . . 54
Polar view of basal cell during metaphase of
mitotic division; lateral region, middle level
of ovine trachea . . . . . . . . . . . . . 55

Cross-sectional view of pronounced mucosal folds
in dorsal region of middle level of bovine trachea. . 56

Cross-sectional view of ovine trachea showing
lymph nodule in submucosa and lymphocytic invasion
of epithelium; ventral region, middle level . . . . 57

Cross-sectional view of bovine trachea showing long
patent duct of mixed, sero-mucous gland; lateral
region, cranial level ., . . . . . . . . . . 58

Cross-sectional View of ovine trachea showing short
patent, branched duct of mixed, sero-mucous gland;
ventral region, middle level . . . . . . . . . 59

Cross-sectional view of ovine trachea showing gland
duct piercing the trachealis muscle; dorsal region,
caudal level . . . . . . . . . . . . . . 60

Mixed, sero-mucous glands in submucosa as seen in
a cross-sectional view of ovine trachea; ventral
region, cranial level . . . . . . . . . . . 61

Cross-sectional view of bovine tracheal glands;
ventral region, caudal level . . . . . . . . . 62

A field of mucous acini situated within the

trachealis muscle as seen in a cross-sectional

view of ovine trachea; dorsal region,

cranial level . . . . . . . . . . . . . . 63

vi

XIII. A field of serous acini situated within the
trachealis muscle as seen in a cross-sectional
view of ovine trachea; dorsal region,
cranial level . . . . . . . . . . . .

XIV. Cross-sectional view of intercartilaginous area
of caprine trachea; ventral region, middle level

XV. Cross—sectional view of caprine trachea depicting
glands both internal and external to cartilagi-
nous ring; ventral region, cranial level . .

XVI. Longitudinal view of intercartilaginous area of
caprine trachea; lateral region, caudal level

XVII. Glands of the intercartilaginous area enveloped
by annular ligament as seen in a longitudinal view
of caprine trachea; ventral region, caudal level

XVIII. Longitudinal view of three overlapping rings with
intervening glands in ovine trachea; ventral region,
cranial level . . . . . . . . . . . .
XIX. Cross-sectional view of bovine trachea showing

typical arrangement of layers; ventral region,
cranial level . . . . . . . . . . .

XX. Cross-sectional view of ovine trachea showing
insertion of trachealis muscle and "elastic
tendons"; dorsal region, middle level. .

XXI. Longitudinal view of bovine trachea showing
elastic character of hyaline cartilage; dorsal
region, middle level. . . . . . . . . . .

XXII. Cross-sectional view of bovine trachea showing

atypical location of two nerve trunks; dorsal
region, middle level. . . . . . .

vii

INTRODUCTION

The intent of this paper is to present a study of the normal
comparative microsc0pic anatomy of the tracheas of the bovine, caprine,
and ovine species. Because these three species comprise the ruminating
domestic animals, they were studied as a single group.

Since diseased conditions can be appreciated most fully in light
of the "normal" structural characteristics of a given organ, a demand
for the establishment of the normal microsc0pic anatomy of the tracheas
of the bovine, caprine, and ovine species has lead to this particular
investigation. It is hoped that a description of this type will serve
as a fundamental tool for the pathologist and the anatomist, as well as
for other individuals whose work and service entail an understanding of
the microscopic anatomy of the trachea.

As the multitude of contributions to veterinary medicine achieves
new peaks in medical science, this writer hopes that the results and
conclusions of his efforts will serve to add to the information that is

of practical value and application to the practitioner.

REVIEW OF LITERATURE

The authors of current histology textbooks have provided adequate
descriptions of the minute structures known to exist within the gross
confines of the human trachea. Trautmann and Fiebiger (1957) have
furnished a brief but inadequate account of the tracheas of domestic
animals.

Several notable investigations on various animals appear through-
out the available literature, namely: mouse (Andrew and Burns, 1947);
dog (Correll and Beattie, 1956, and Niewenhuis, 1961); cat (Macklin,
1929); pig, horse, and cat (Paul, 1913); cattle (Vacirca, 1961); mink
(Stowe and Calhoun, 1962); and rat (Schulz, 1959). With the exception
of the work done by Stowe and Calhoun, Niewenhuis, Paul, and Vacirca,
a majority of the investigators furnishing accounts of the histology of
the trachea gathered their data on only a few of the many microscopic
structures of the trachea. Many of the past studies on the trachea
include detailed reports of their respective subjects; however, with
a few noted exceptions, composite descriptions of the trachea of the

domestic animals are lacking.

Mucosa

Hayek (1960) stated that the tracheal mucous membrane consists of
three layers: 1) an epithelium; 2) a basement membrane; and 3) a membrana
propria, referred to by Rhodin and Dalhamn (1955) as the lamina propria.
According to Wilson (1859) the mucosa is pale, forms the internal lining

of this tubular organ, and exhibits the excretory tubes of numerous glands

Opening upon its surface. Vacirca (1961) described the bovine mucosa as
having sharp, low folds which have a longitudinal direction. Hayek (1960)
maintained these folds are the result of displacement by the loose, under-
lying submucosa.

The tracheal mucosa contains respiratory epithelium (Edwards, 1956).
Lucas (1932), and Miller (1932) both agreed that this type of epithelium,
pseudostratified, ciliated, columnar, was composed of four types of cells:
1) basal cells; 2) non-ciliated cells; 3) ciliated cells; and 4) goblet
cells. Vacirca (1961) identified the epithelium of bovine trachea as
simple columnar with many layers of nuclei and with ciliated and mucous
cells. Miller termed the non-ciliated cells as "Ersatzellen" or inter-
mediate cells. The basal cells form the deepest layer and are situated
just above the basement membrane. Their nuclei, lying parallel to the
basement membrane, are either round or elongated. The basal cells are
the only cells of the epithelium not extending through the thickness of
the epithelium. The intermediate cells form the second layer of cells.
According to Miller, their various forms are due to pressure within
their proximity. They are usually spindle-shaped and often extend from
the basement membrane to the free surface.

The third type of cell described by various investigators is the
ciliated cell. This cell is columnar in shape and has on its outer free
end a cuticular border bearing cilia. Lucas (1932) cited Drasch (1879)
who found the nuclei situated at a higher level in the ciliated cells
than in the intermediate wedge-shaped, non-ciliated cells, due to the
greater length of the basal processes in the former. Lucas added that

in 1911, Loginoff determined that the length of the ciliated cells was

frequently greater than the height of the epithelium in domestic animals,
a fact attributable to the curvature of the basal ends of the cells.

The goblet cell or "chalice" cell is the fourth type of cell found
in respiratory epithelium. Attached to the basement membrane, the goblet
cell extends throughout the entire thickness of the epithelium. Its lower
end may be like a "foot" (Miller, 1932), may terminate in a pointed prolonga-
tion, or may end in a number of fine prolongations. The free end of the
goblet cell may be widely opened or it may be contracted like the neck of
a bottle. The nuclei of goblet cells are usually situated on the same
plane as those of the adjoining cells.

Rhodin (1959) reported the occurrence of a fifth cell type in the
simple columnar epithelium of the rat trachea. This cell has a dense
cytoplasm with small mitochondria scattered throughout the cell. The
numerous small extensions on the surface of the cell are similar in
appearance to the"brush border extensions"of the intestinal cells. Rhodin
maintained that judging from the similarity, one would expect that this
particular cell would have resorptive functions and actively participate
in regulating the viscosity of the mucous blanket. In cross section the
extensions appear to be forming cilia; consequently, the cell would then
be a newly formed ciliated cell.

In 1932, Lucas provided an extensive study and review of the litera-
ture concerning the ciliated epithelium in man. He noted the findings of
KBlliker and von Ebner in the middle and late 19th century, respectively.
These two investigators measured cilia in man ranging from 3.3 to 5.7
microns. Stowe and Calhoun (1962) derived an average length of 3.9 microns

for cilia in the ranch mink trachea. The average length of the cilia of

dog and cat tracheas measured 5.7 microns and 4.0 microns, respectively
(Niewenhuis, 1961). According to Lucas, Valentin and Purkinje, working
in the mid-19th century, counted from 10 to 22 cilia on each cell.

Investigators of the late 19th century denied the presence of a
cuticular border, but those of the early 20th century claimed it was
present in the ciliated tracheal cells of the rat and mouse, and was
regarded as a cell product or perhaps a derivative of the ciliary border
(Lucas, 1932). Lucas reported basal bodies, about 13 in number (as seen
in cross section), lying at the free border of the cell and forming a
single layer. Immediately below this layer is a narrow zone in which
the cytoplasm, free from granules and mitochondria, diSplays ciliary
rootlets.

Schulz (1959) reported that in the rat trachea the ciliated cells
have not only cilia but also filiform processes. He arrived at a figure
of 270 cilia per cell. Note the contrast with the report by Lucas (1932)
on the number of cilia per cell in man.

A study performed by Chambers and Rényi (1925) on the ciliated cell
of the frog's mouth demonstrated excellently the close relationship
between the viable state of the cell and the optical appearance of the
nucleus. If a ciliated cell be deformed or punctured with a needle with-
out causing any apparent change within the nucleus, the cilia will either
beat or can be made to beat upon stimulation. As soon, however, as the
nucleus is affected, the cilia st0p moving and disintegration of the cell
follows.

The most important mechanism of excretion is that of cilia and

secretion of mucus, for they extend over most of the respiratory tract

(Barclay, Franklin, and Macbeth, 1938). These investigators noted that
ciliated epithelium is distributed throughout the trachea and bronchi
down to the very fine bronchioles. In an earlier work, 1937, these same
investigators recognized the clockwise spiral direction (as viewed from
the oral end) of the ciliary movement in the cat.

The presence of leukocytes in the tracheal epithelium has been
reported by several investigators (Paul, 1913; Miller, 1932; Andrew and
Burns, 1947; Andrew, 1947; Hayek, 1960; and Vacirca, 1961). Perhaps
the most extensive of these reports is that of Andrew and Burns on the
large numbers of leukocytes in the tracheal epithelium of the normal
adult mouse. Of these leukocytes the predominant type is the lymphocyte,
but polymorphonuclear neutrOphils are also abundant. Rarely are monocytes
and eosinophils seen. The great majority of leukocytes in the trachea are
located either below or at the level of the layer of epithelial nuclei.
Relatively few appear to be in the process of continuing on through the
epithelium to the lumen. Lymphocytes which have reached the apical ends
of the epithelial cells generally show a marked pycnosis and decrease in
size. The polymorphonuclear leukocytes are more frequently fragmented in
this region. Andrew (1947) stated that pycnosis and fragmentation are
common in the intestinal epithelium but rare in the trachea. Andrew and
Burns (1947) added that while it seems clear that the great majority of
leukocytes in the tracheal epithelium lie between the cells, instances
have been found in which the leukocytes, particularly the lymphocytes,
actually are intracellular, the position which is very common for such

cells in the duodenum.

Paul (1913) reported having found leukocytes in the tracheal epi-
thelium of the pig, horse, and cat. In 1961, Vacirca identified lympho-
cytic invasion in the epithelium of bovine trachea. Miller (1932) and
Hayek (1960) asserted that scattered lymphocytes are commonly observed
in the human trachea.

Of the literature reviewed only one authority referred to mitotic
figures. Dawson (1948) affirmed the infrequent observation of mitotic
figures in the tracheal epithelium.

According to Miller (1932), the earliest accounts of stratified
squamous epithelium in the human trachea are found in papers published
by Griffini and by Baraban in the late 19th century. Baraban found areas
of squamous epithelium in the trachea of an executed criminal and thought
that the transition of ciliated epithelium into stratified squamous epi-
thelium is due to a low grade of irritation which leads to the loss of
the cilia and to the appearance of mucous cells. As was the case with
Griffini, all the instances in which Miller found stratified squamous
epithelium in the human bronchi were from tuberculous lungs.

Hilding (1932) described squamous epithelium in the upper respiratory
tract at the inactive areas (i.e., areas where the impact of air is not
so great). He mentioned an additional transitional form of epithelium in
proximity to the squamous epithelium. Both of these epithelial types are
non-ciliated. At the active areas there is pseudostratified,ciliated,
columnar epithelium. Because islands of squamous epithelium are commonly
found in the trachea, Hilding suggested that all such changes may be

caused by currents or eddies of air.

Hilding prOposed that the different forms of epithelium found in
the upper part of the reSpiratory tract are not fixed types, but are
more or less interchangeable, according to circumstances. When the
flow of air over the columnar epithelium of the nose is sufficiently
increased the lining changes to a form much like "squamous" epithelium.
Experiments indicate that the islands of similar epithelium found on
the turbinates and the patches of stratified squamous epithelium so
commonly found in the trachea are caused by eddies in the streams of
air which cause more forceful impact in these spots than the columnar
epithelium can tolerate.

The observations of Hilding on the replacement of pseudostratified,
ciliated, columnar epithelium by a "squamous" epithelium agree with the
findings of Ross (1961) that squamous metaplasia, the replacement of one
type of epithelium by squamous epithelium that is not normally present
in a given location, reflects chronic irritation of the respiratory tracts.
Koss stated that squamous metaplasia may be circumscribed or diffuse.

In contrast to the above mentioned reports by Hilding and Koss,
Correll and Beattie (1956) through their observations on the destroyed
epithelial lining of the trachea of the dog alleged that the epithelium
eventually regenerated is of the ciliated columnar type requiring 3-4
weeks to regenerate. Knowlton and McGregor (1928) noted similar circum-
stances in the maxillary sinuses of dogs.

R0pes (1930) presented evidence of phagocytosis, which is an activity
repeatedly denied for tracheal epithelium and which is a function of the

ciliated epithelial lining of the trachea and bronchi in rabbits.

He maintained that if particulate matter is suspended in a fluid medium,
the ciliated cells do not phagocytize; however, if the particulate matter
is inhaled under normal atmospheric conditions, then phagocytosis occurs.
Rapes listed the following phagocytic cells: 1) columnar or cuboidal,
ciliated cells; and 2) low columnar, cuboidal or rounded cells.

Miller (1932) described the basement membrane as a clear, homogeneous,
structureless membrane having been derived from the subepithelial,elastic
layer or as made up of elongated cells, placed end to end. In contrast to
this Hayek (1960) asserted that the basement membrane is not homogeneous,
but rather a network of argerphilic fibers. According to Vacirca (1961),
the basement membrane appears distinct in the bovine trachea. Niewenhuis
(1961) found the basement membrane of the cat and dog to be indistinct.
Schulz (1959) measured the basement membrane of the cat trachea and found
it to be 6002 in thickness.

Rhodin and Dalhamn (1955) included as the main components of the lamina
propria of the tracheal mucosa of the rat the fibroblasts, the collagenous
and the elastic fibers. The collagenous fibrils, well separated from the
fibroblast by its cell membrane, are aggregated in bundles with 1000-2000
fibrils in each. The elastin occurs in dense fibers void of branching,
with a diameter of about 1-2 microns. Dawson (1948) reported the presence
of reticular fibers in the lamina propria.

According to Hayek (1960), the membrana propria, forming the deep
limit of the mucosa, contains a superficial layer with numerous cells and
a deeper one which is rich in fibers. The cells are mostly lymphocytes

which are found grouped especially about the glandular ducts. He stated

10

that not only does this layer contain the blood capillaries and lymphatic
vascular networks, but also a loose network of collagenous fibers. In the
deep layer there are numerous elastic fibers which laterally form a thin
layer and dorsally are condensed into thick bundles occupying the longi-
tudinal folds.

Macklin (1922) conducted an excellent investigation on the elastic
membrane, a component of the lamina propria. Macklin described the elastic
membrane as a "creamy white," Y-shaped band of elastic tissue, which when
stretched snapped back ”like a rubber band." He demonstrated the contrast
of the sharp recoil before removal from the trachea-bronchial tree and the
sluggish recoil after removal from the tree. A microscopic analysis by
Macklin showed the elastic fibers run parallel to the longitudinal axis
of the trachea, in agreement with Wilson (1859) and Sauser (1957), the latter
adding that this is the basic functional structure. Each fiber follows a
gently undulating course and branches frequently; thus, a meshwork of elastic
fibers, elongated longitudinally, is formed. Macklin noted a tendency for
the fibers to assemble into fasciculi, which themselves interbranch. The
elastic membrane forms a complete, extensible sheath for the epithelium of
the trachea.

Miller (1947) presented a correlation by Zuckerkandl between the longi-
tudinal folds of tracheal mucosa and the bundles of elastic fibers. The
elastic fibers appear in the form of bundles because of the folds having
been formed by the contraction of the trachealis muscle and the inherent
elasticity of the cartilages, and not by the bundles of elastic fibers.

Stowe and Calhoun (1962) determined the thickness of the elastic

membrane of the ranch mink trachea to be 7-10 microns. Niewenhuis (1961)

11

gave average values of 94.3 microns for the dog and 29 microns for
the cat.

Paul (1913) reported that in the trachea of the horse, cat, and
pig the elastic fibers may be interSpersed among the lobes of the
glands, which are frequently present in the lamina propria.

Dawson (1948), Trautmann and Fiebiger (1957), and Vacirca (1961)
reported the presence of lymphatic nodules in the lamina propria.
Trautmann and Fiebiger pointed out their frequent presence in sheep
tracheas. Vacirca recognized their common occurrence around the ducts

of glands.

Submucosa

According to Hayek (1960), Schaffer maintained the differentia-
tion of a submucosa as a true layer is justifiable-~contrary to von
Schuhmacher and Petersen, who did not recognize this layer--at least
in the region of the membranous wall, since the mucous membrane there
can be displaced and can lie in folds, a circumstance permitted by the
loose submucosa. Particularly in the region of the cartilage, the sub-
mucosa is lamellar in structure and passes without sharp demarcation
into the perichondrium of the cartilage.

Stowe and Calhoun (1962) reported the secretory portions of the
serous and mixed,sero-mucous glands and loose connective tissue com-
prise the major portion of the submucosaiin the ranch mink trachea.
Greep (1954) and Jordan (1952) noted loose fatty and areolar connective
tissue, small tubuloacinar mucous glands with mucous cells and serous

crescents, large blood vessels, and nerves in the submucosa of the

12

human trachea. The submucosa of domestic animals is rich in elastic

fibers (Trautmann and Fiebiger, 1957).

Glands

The glands of the trachea are found in the submucosa (Florey,
Carleton, and Wells, 1932), in the lamina propria (Ham; and Leeson, .
1961), external to the annular ligament, between the annular ligament
and the trachealis muscle, and in the substance of the annular liga~
ment between the cartilage rings (Wilson, 1859), and external to the
cartilaginous rings (Trautmann and Fiebiger, 1957).

Florey, Carleton, and Wells (1932) found acini of gland cells
lying in the submucosa of the cat trachea. These cell groups are
serous, mucous or mixed in type. Stowe and Calhoun (1962) reported
similar findings in the ranch mink trachea. Quain (1882) and Stirling
(1883) had described purely mucous glands. Bremer and Weatherford (1946)
reported the glands consisted of mucous cells with serous crescents.
According to Florey, Carleton, and Wells, gland cells which on a morpho-
logical basis would be termed "serous" often appear to be capable of
elaborating mucus, as evidenced by their histological reactions.

Paul (1913) reported the presence of glands in the whole course of
the trachea as well as the complete circumference. Although their main
site is in the submucosa, they are abundant, as well, in the lamina propria
(in agreement with Ham and Leeson, 1961). Paul described predominantly
complex tubular, particularly tubuloalveolar, glands in the pig. He also
reported that in the pig they are mucous in type and serous in the horse

and cat; mixed types are rarely present in any of these species.

13

Vacirca (1961) found tubuloacinous glands of a mixed type in the sub-
mucosa of the trachea of cattle.

Miller (1947) described glands of a tubuloacinar type situated in
the submucosa. They are more abundant in the anterior wall than in the
lateral wall of the human trachea. In the posterior membranous wall,
they are situated not only in the submucosa but also within and posterior
to the trachealis muscle with their ducts passing through the muscular
layer in order to reach the surface of the mucosa. Frequently the ducts

Open on the surface of the mucosa by a funnel-shaped enlargement.

Cartilage

The cartilaginous rings, which serve as the framework for the trachea,
are generally considered to be C-shaped (Bloom and Fawcett, 1962, and COpen-
haver and Johnson, 1958). Sauser (1957) described the rings as horse-shoe-
shaped. Straus (1931) cited variations of cartilage form among the primates,
ranging from complete to incomplete enclosure with the presence or absence
of overlapping rings.

In their review, Stowe and Calhoun (1962) presented the variations in
certain species regarding the number of rings and ring types. Among those
having incomplete rings are man, pig, dog, cow, cat, and horse. Complete
rings are found in the lemur and fowl. Of those species reviewed, the
number of rings varied from 18-20 (man) to 110-120 (turkey).

These same investigators found the margin of the tracheal rings in
the ranch mink to vary greatly from ventral to dorsal, if viewed in cross
section. They established an increase in ovoid elongation from ventral to

dorsal (i.e., the ventral cross sectional view may be considered oval,

14

whereas the dorsal cross sectional View may be considered spatulate). In
a longitudinal section through the trachea, the cross sections of the
individual rings show a flat, outside margin and a convex, inside margin
(Hayek, 1960).

With one exception, authorities (Bloom and Fawcett, 1962; Ham and
Leeson, 1961; and Copenhaver and Johnson, 1958) agree that the tracheal
rings are comprised of hyaline cartilage. Paul (1913) found, in some
cases, cartilage of an elastic character present in the trachea of the
horse and cat. In old age, the hyaline cartilages show fibrous degenera-
tive changes, and may become partly calcified (Bremer and Weatherford,
1946). Niewenhuis (1961) reported no significant amount of calcification
in the tracheal rings of either the dog or the cat.

Hayek (1960) asserted the perichondrium, thicker externally than
internally, consists principally of collagenous fibers which encircle
the trachea, and among which are inter-mingled a few elastic fibers.

Vacirca (1961) called attention to a ridge, extending the length of
the bovine trachea, formed by the opposition of the cartilage tips in the
dorsal region.

The site of bifurcation of the trachea is marked by the ”carina
tracheae" (Miller, 1904). From a study of 150 cat tracheas, Miller con-
cluded the carina is rarely membranous and the bronchial cartilages either
alone or in combination with the tracheal cartilage form the great majority
of the carinae.

In a later study (1947), Miller maintained if cartilage were present,
then it is classified accordingly: "When the cartilage was derived from a

bronchial crescent it might be either 'bronchial right' or 'bronchial 1eft,’

15

or when, as in some cases, both bronchial cartilages entered into the
carina, 'double bronchial.‘ Occasionally a fused tracheal and bronchial
crescent entered the carina; then called 'tracheo-bronchial' and like the

simple 'bronchial,’ it could be either 'right' or 'left'."

Annular Ligament

The cartilaginous, tracheal rings are held together by a strong
fibrous membrane, which is elastic and yielding to a certain extent, and
not only occupies the intervals between them, but is prolonged over their
outer and inner surfaces, so that they are, as it were, imbedded in the
membrane (Quain, 1882). Wilson (1859) had claimed this membrane to cover
only the outer surface of the rings as well as extending from one cartilage
tip to its opposing tip.

Stowe and Calhoun (1962) reported the presence of white fibrous
connective tissue and the absence of elastic fibers in the annular liga-
ment of the ranch mink trachea. Paul (1913) found elastic fibers in this
membrane in the pig and horse. Niewenhuis (1961) identified small amounts
of elastic fibers in the annular ligaments of the dog and the cat. If

elastic fibers are present, they have a longitudinal course (Hayek, 1960).

Trachealis Muscle

The mammalian trachealis muscle is located in the posterior membran-
ous portion of the trachea (Towers, 1953). Chauveau (1873) cited Leyh as
having described longitudinal fibers in the anterior wall of the human
trachea, between the mucous membrane and the cartilaginous rings.

Paul (1913) identified the circularly directed fibers in the horse,

pig,and cat. Stirling (1883) claimed to have observed longitudinally

16

directed fibers arranged in several bundles located outside the trans-
versely disposed fibers. Chauveau (1873) reported Kblliker had found
some longitudinal fibers passing across the transverse ones at the
posterior part of the trachea. Macklin (1929) identified a few longitu-
dinal fibers, scattered mainly in the region of the carina.

According to Miller (1920), Cuvier was the first to point out that
the musculature of the trachea in some animals is inserted on the outer
surface of the cartilages, in others on the inner surface. In agreement
with Meckel and Luschka, Miller (1913) found an external attachment in
all the examined carnivora. In monotremes and insectivora the attachment
is internal. As a rule, the attachment is internal in herbivora, e.g.,
ox. The rabbit is an exception to this rule. In man, an omnivore, it
is internal.

The trachealis muscle is inserted into the perichondrium by attach-
ments of elastic connective tissue (Paul, 1913). Hayek (1960) referred
to these elastic components as "elastic tendons.” According to Miller
(1913), Guieysse stated that in the smaller animals the insertion is
directly into the perichondrium, but in the larger animals an elastic
tendon is interposed between the muscle and the perichondrium. Niewenhuis
(1961) reported having observed transverse elastic fibers serving as attach-
ments for the trachealis muscle onto the outer perichondrium of the trachea
of both the dog and the cat.

According to Macklin (1929), the trachealis muscle exhibits a peri-
staltic wave resembling that of the digestive tract. Its length may reach
to 10 cm. Macklin claimed the speed of masses so propelled too rapid to

be accounted for by ciliary action. Bullowa and Gottlieb described the

17

peristaltic mechanism as "bellows-like,"

and Reinberg found it so marked
in the trachea as to suggest the designation "tracheal vomiting."

(Macklin, 1929).

Adventitia

In the cervical region of Equus, Bos, Ovis, Sus, and Qapig, the
adventitia of the trachea blends with the superficial layer of deep
fascia. A more intimate fascia propria forms a tubular sheath around
the trachea (Sisson and Grossman, 1959). In man, the adventitia is
continuous with the loose connective tissue of the mediastinum and
contains abundant blood and lymphatic vessels and both medullated and

non-medullated nerves (Greep, 1954).

'Blppg and Lymphatic Vessels

Blood and lymphatic vessels are found in both the lamina propria
(Hayek, 1960) and submucosa (Vacirca, 1961). According to Cover (1953),
the lamina propria of the turkey trachea is highly vascular. Jordan
(1952) maintained the submucosa was occupied by the larger blood vessels.
Trautmann and Fiebiger (1957) noted a submucous, a periglandular, and a
subepithelial plexus of blood vessels, as well as a deep and superficial

network of lymphatics in the tracheas of domestic animals.

Nerves

Nerves, located in the adventitia of the tracheas of domestic
animals, possess microsc0pic ganglia and consist of both myelinated
fibers and unmyelinated fibers, the latter ending on the smooth muscle

cells (Trautmann and Fiebiger, 1957). A large number of small ganglia

18

are found in the dorsal wall of the trachea of the mouse from the caudal
portion of the cricoid cartilage of the larynx to the bifurcation of the
trachea (Honjin, 1954). These ganglia form a chain and are connected
serially by nerves.

Elftman (1943) found two types of afferent nerve endings in the
tracheal wall of a four-day old puppy. One of these types terminated
in swellings or reticulations among the smooth muscle cells. The other
type of afferent ending in the trachea showed subepithelial branches
with swellings at their intersections and a ring termination. In addi-
tion, some of the branches continued up between the epithelial cells.
Lucas and Douglas (1935) found no motor innervation of the tracheal

epithelium.

MATERIALS AND METHODS

The data obtained for this study came from the tracheas of thirty-
six animals--twelve each of cattle, sheep, and goat. All of the speci-
mens exhibited no pathological disorders with the following exceptions:
one 6-month old cow with mastitis, a second 2-year old cow with peritoni-
tis, and one sheep with a mild inflammatory response in the respiratory
passages.

Upon obtaining each of the thirty-six tracheas, sections from three
levels of each trachea were procured for further study. The levels
resected were the following: first, tissue approximately three rings
below the cricoid cartilage; second, tissue approximately three rings
above the first bifurcating bronchus; and third, tissue at a level approxi-
mately midway between the anterior and posterior ends of the trachea.

The tissue of freshly killed or embalmed animals was placed in F.A.A.
(Lavdowsky's mixture, Guyer, 1949).

In order to dehydrate and infiltrate the tissue, the author used
the butyl alcohol method as prescribed by Johnson, g£_§l,, 1943.

Bioloidf served as the medium for imbedding the tissues.

Ten Specimens of each of the three species were utilized for cross-
sections, while two specimens of each species were used for longitudinal
sections.

A routine hematoxylin and eosin stain was performed to enable study-
ing, in general, the mucosa and submucosa. This stain also allowed

detailed observation of the epithelium. A Weigert-Van Gieson connective

 

* Will Corporation, Rochester, New York

19

20

tissue stain provided for the differentiation of collagenous and elastic
components of the mucosa and submucosa, as well as demonstration of the
nature of the cartilaginous tissue. A third stain, toluidine blue,
(Lillie, 1954), made possible the distinction between mucous and serous
cells of the glands, the enhancement of the outline of the goblet cells
of the epithelium, and the demonstration of the metachromatic nature

of mast cells.

As a result of these methods slides prepared from each of the thirty-
six tracheas represented the dorsal, lateral, and ventral regions at
each of the three levels.

With the aid of a calibrated ocular micrometer, measurements of
various structures were determined in microns and recorded. In order
that a range of numerical values might be derived, the author attempted
to evaluate the greatest and least magnitude, as well as intermediate,
representative magnitudes.

A list of the structures and characteristics that were measured
follows:

Epithelium - height

Cilia - length

Elastic membrane - thickness
Elastic fibers - diameter

Submucosa - depth

Cartilage - thickness
Perichondrium (inside) - thickness
Perichondrium (outside) - thickness

Trachealis muscle - thickness

RESULTS AND DISCUSSION

The tracheas of B05, Capra, and Ovis, both male and female, display
three major layers, namely, 1) a mucosa containing an epithelium, a base-
ment membrane, and a lamina propria; 2) a submucosa; and 3) a fibroelastic-

cartilaginous layer (Plate I).

MUCOSA
Epithelium

The mucous membrane of the tracheas of B08, Capra, and Qgip is
lined predominantly by a pseudostratified, ciliated, columnar epithelium
(Plates I and II) containing goblet cells. This type of epithelium is
present at each of the three tracheal levels examined, as well as the
dorsal, ventral, and lateral regions.

In several cases of each species patches of a non-keratinized, meta-
plastic, stratified squamous epithelium appears dorsally. The presence
of this type of epithelium in the trachea has been recognized by other
investigators, has been considered relatively common, and has been attri-
buted to an increase in attrition during both inhalation and exhalation.

Four cell types exist in the tracheal epithelium (Plate II) and are
readily identifiable in each specimen examined. The first of these cell
types, the goblet cell, is most abundant ventrally, less laterally, and
least dorsally. The base of the goblet cell rests on the basement mem-
brane while the apex of this cell reaches the lumen of the trachea. The

nuclei of the goblet cells, the product of which is a mucous secretion,

21

22

are situated within the vicinity of the adjacent intermediate and ciliated
cells. The size of the goblet cells appears to vary in preportion to the
degree of mucous content. In instances of abundantlnueus, cells adjacent
to the goblet cells appear laterally compressed.

The basal cells, perhaps the most readily identifiable of the four
cell types, are situated in a conspicuous row immediately above the base-
ment membrane. These cells do not extend to the lumen of the trachea, and
consequently possess no free border. The oval nuclei of the cuboidal
basal cells occupy most of the cellular cytoplasm.

The intermediate and ciliated cells of the epithelial lining present
a narrow and elongated profile. The former extend throughout most of the
thickness of the epithelium; frequently reaching the free surface of the
epithelium; whereas the latter extend from the basement membrane to the
lumen, their cilia obviously exposed to the overlying mucous blanket.

The cilia (Tables 1, 2, and 3) appear as hair-like projections, the
fixed ends of which are in contact with a distinct striated border (Plate
III). The striated border is continuous throughout the circumference (as
seen in cross section)of the mucous membrane and is interrupted only by
the apex of the goblet cells.

The fifth cell type (dense cytoplasm with scattered mitochondria and
small extensions on the surface) of the simple columnar epithelium of the
rat trachea described by Rhodin (1959) was not discerned.

Observation of mitotic figures is rare in the trachea of Bpp, Qgppg,
and'Qyip. Those identified were situated in the basal region of the

epithelium (Plate IV).

23

Leukocytic invasions of the epithelium are frequently seen in the
tracheas of B03, Capra, and Qggp. Lymphocytes are the outstandingly
predominant type of leukocyte; however, in a few isolated specimens of
each species, polymorphonuclear neutrophils can be identified. The
leukocytic invasions exhibited two architectural patterns. In one of
these patterns the leukocytes are aggregated into patches which extend
completely through the epithelium to reach the mucous blanket (Plate VI)
or to lower limits of the epithelium. The second pattern of leukocytic
invasions is one of a scattered or dispersed nature.

‘Bpg. The epithelium displays slight undulations with a general
uniformity in height.(Table l).

£2233. Pronounced undulations of the epithelium are apparent. As
in Egg the epithelium maintains a uniform thickness (Table 2) throughout
its course. Crypts are usually absent.

.Qgig. The intraepithelial crypts render a denticulate appearance to
the epithelium. The epithelium at the base of these crypts is of consider-
ably less height than the epithelium between any two crypts, as evidenced

by the range in height recorded in Table 3. (Plate X).

Basement Membrane

Bos, Capra, and Ovis. The methods employed in this investigation did

 

not provide for a critical examination of the basement membrane. However,
in each of the animals examined, a faint but discernible line can be observed
immediately adjacent to the lower limits of the cytoplasm of cells in contact
with this line, which appears somewhat more refractile than the cellular

membrane (Plate IV).

24

Lamina Propria

The deepest zone of the mucosa, the lamina prepria, consists of
white fibrous connective tissue, containing elastic and collagenous
fibers, acini of glands and their ducts, blood and lymphatic vessels
of a small caliber, connective tissue cells, lymphoid tissue, including
nodules, and mast cells.

The elastic fibers (Tables 1, 2, and 3) are organized into a clearly
delineated structure, commonly referred to as an "elastic membrane”
(Plate XVII). In a cross-sectional view of the trachea, the elastic
fibers manifest a longitudinally oblique deposition. Two of the ovine
tracheas examined contain a few scattered elastic fibers coursing cir-
cularly in the ventral region at the middle level.

Interspersed throughout the lamina propria are collagenous fibers
(Plate I), which are more densely distributed among the elastic fibers
of the elastic membrane. Their random deposition and irregular direction
provide a dense meshwork of white fibrous connective tissue. In Qpppg
and‘Qgip their concentration is greatest in the lower limits of the
elastic membrane. However, in.§p§ the collagenous fibers are equally
concentrated throughout the zone of the elastic membrane (Plate 1).

In longitudinal view the elastic and the collagenous fibers are
seen deviating from their usual direction in order to circumvent the
ducts and acini of the glands. The collagenous fibers, but not the
elastic fibers, establish contact with the epithelial cells of the glands
and ducts. A few collagenous fibers traverse between acini of the glands

producing an entwined character for the glands.

25

Cross-sectional views of the trachea of each species (Bos, Capra,
and.QZi§) reveal fasciculated aggregations of the elastic fibers. These
bundles are least conspicuous in.§p§ and Ca ra, but are quite evident in
the trachea ofiggip (Plate 1). The fasciculi of elastic fibers tend to
correspond with the mucosal undulations. In the dorsal region of the
trachea the relationship, as seen in cross section, is most apparent
(Plate V). The morphology of this elastic membrane-mucosal undulation
relationship leads one to deduce that the "wavy" surface of the epithelium
may be attributable to the fasciculation of the elastic membrane during
the exhalation phase of mechanical respiration or during a phase when
distention of the trachea is at a minimum.

Lymphoid tissue is commonly seen in the lamina propria of the bovine,
caprine, and ovine tracheas. In addition to the presence of a mild con-
centration of lymphocytes immediately below the epithelium of the ventral,
lateral, and dorsal regions at all levels, lymph nodules occur frequently
and may protrude into the submucosa (Plate VI). Although the nodules are
invested by collagenous fibers, lymphocytes are often situated in the
nearby connective tissue substance. '1

Connective tissue cells are scattered in moderate abundance through-
out the area of the lamina propria. Mast cells, the metachromatic nature
of which is demonstrated by the toluidine blue stain (Plate XII), are
frequently observed in the lamina propria and are usually within the

vicinity of or immediately adjacent to the small blood vessels.

26

SUBMUCOSA

White fibrous connective tissue and glands comprise the greater
part of the submucosa (Plate XIX). The depth of the reSpective sub-
mucosae in‘Bpp, Ca ra, and'Qpip decreases from the ventral to the
lateral region and is, in many cases, absent or shallow in the dorsal
region at all the levels. The white fibrous connective tissue, accom-
panied by varying amounts of adipose tissue confer a loose nature upon
the submucosa (Plate 1). The collagenous fibers of the submucosa, as
in the lamina propria, exhibit a random deposition with the exception
of those circularly directed fibers which blend with the perichondrium
of the inner surface of the cartilaginous ring. Circularly directed
elastic fibers are frequently intermingled with the collagenous fibers
which blend with the inner perichondrium (Plate XVIII).

Lymph nodules are seen less frequently in the submucosa than in
the lamina propria. When present they have the same characteristics
as those found in the lamina propria. As previously stated, lymph
nodules may be so large as to occupy both the lamina propria and the
submucosa. Lymphocytes, which presumably have migrated from these
nodules,are usually clustered at the peripheral margins of the ducts
of glands as the ducts proceed through the submucosa and mucosa to
reach the lumen of the trachea.

‘Bpp. The depths of the submucosae of £25 and‘Qggp are nearly
equal (Table 6). Relative to the thickness of the cartilage, the
submucosa of the bovine trachea is markedly more shallow than the

submucosa of Ovis.

27

Capra. The submucosa is approximately half as deep as those of
B08 and Ovis (Table 5).
Ovis. The depth of the submucosa is nearly equal in both the

lateral and ventral regions (Table 4).

arenas

The glands of the tracheas of Bpg,Ԥpppp, andIQgig are of the
branched,tubuloacinar type whose acini are most frequently mixed in
character (i.e., sero-mucous) (Plates VIII, X, XI, XIV). A few iso-
lated acini of a purely serous or purely mucous nature are observed
(Plates XII and XIII). In each of the three species, the glands are
most numerous ventrally, less abundant laterally, and least numerous
dorsally. No discernible gradation of quantity from the cranial level
through the middle level to the caudal level was established.

The glands are present in both the lamina propria and the sub-
mucosa, a majority of them situated in the latter. When located in
the lamina propria the acini of the glands tend to occupy the deeper
zone of this layer, while in the submucosa the acini are inclined to
reside in the upper limits of that layer (Plate XI).

The tracheal glands of Bpg, Ca ra, and'Qpip are, as a rule, located
in the lateral and ventral regions; however, in many cases the glands
are situated in the membranous area external to the dorsally fixed
trachealis muscle or within the muscle tissue (Plates IX, XII, and
XIII). In either case, the ducts of these glands pass through the

trachealis muscle in order to reach the surface of the mucosa.

28

In Qpppg, the glands are commonly implanted in the ventral or
lateral regions of the adventitia between the cartilaginous rings
(as seen in a longitudinal view) and may be enveloped, in part, by
the annular ligament (Plate XVII). In a cross-sectional view of
the ventral or lateral region of the caprine trachea, tubuloacinar
glands can be seen external to the cartilaginous rings (compare Plates
XIV and XV).

In both Qappp and.Qgi§ the tracheal glands (as seen in cross
section) appear as clusters or like a bunch of grapes. Inlfipp the
acini of the tracheal glands (as seen in cross section) appear to
be arranged like a string of beads (compare Plates X and XI).

In one ovine specimen, in the ventral region at the cranial level,
the glands are situated between three overlapping cartilaginous rings
(Plate XVIII). Such a location of tracheal glands is apparently uncommon.

The epithelial cells of the gland acini vary from low columnar to
cuboidal in all three species of domestic ruminants (Plate IX). No
pattern of distribution of the serous and mucous cells is discernible
with the exception that a single acinus may contain all serous or all
mucous cells or varying quantities of both cell types. Each of the
two cell types is either serous or mucous in character and displays
no serous or mucous crescents.

The nuclei of the serous cells possess an oval or round margin,
while those of the mucous cells are compressed toward the base of each
cell, depending on the amount of mucous content.

Epithelial cells of the ducts exhibit a gradation from low colum-

nar or cuboidal to tall columnar at the outlet on the surface of the

29

mucosa. Mucous cells frequently line the ducts.

Tall, ciliated, columnar cells are present in the ducts of glands
in.§2§,'gapp§, and Qgig as the ducts course through the pseudostratified
epithelium. The cilia of these columnar cells are directed toward the
outlet of the duct.

As previously stated, collagenous fibers and connective tissue

cells comprise the interstitial elements of the glands.

CARTILAGE

The dorsally incomplete cartilaginous rings, present in the tra-
cheas of Bos, Capra, and M91: are composed of hyaline cartilage, (Plates XXI,
XVI, XVII, XVIII and XX), incased by a thin inside and thick outside peri-
chondrium. The rings have a C-shaped form in sheep, goats, and young
cattle. However, in older cattle the tips of the rings oppose each other
to lie parallel, thus forming a dorsally located ridge, macroscopically
visible in an excised trachea. The cartilaginous rings of the tracheas
of Bos, Capra, and‘Qyip are thickest ventrally, thinner laterally, and
least thick dorsally (Table 4). Considered as a whole, the rings are
thickest in Egg, thinner in‘Qgig, and still thinner inquppg (Table 6).
Apparently the thickness of the tracheal rings of these three species
decreases consistently from the cranial level to the caudal level..

In a longitudinal view of the tracheas oflgpp,‘§§ppa, and‘Qgip,
the cross sections of the cartilaginous rings can be observed. A des-
cription of the margin of the rings is best served by the diagrams on

the following page.

30

ventral lateral dorsal

 

U

Ind
O
(n

O
F
ff
93

O
O 0 :3
CD

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Note: For orientation purposes the internal surface is at the
top of the diagram and the external at the bottom.

The perichondria, both internal and external, are composed of dense
white fibrous connective tissue containing collagenous fibers and cells
of an intermediate form between chondxwacytes and ordinary fibroblasts.
The perichondria are present throughout the circumference of the carti-
laginous rings, decreasing in thickness from the ventral to the dorsal
region of the ring. In all regions the thickness of the perichondria

appears enhanced by the adjacent collagenous fibers of the annular liga-

ment.

ANNULAR LIGAMENT

The annular ligament, composed of collagenous and elastic fibers
(Plate I), completely encompasses the cartilaginous rings of the tracheas
of Egg; Qgpgg, and.Qyi§. The annular ligament is best described as a
membranous, tubular structure extending the entire length of the trachea.
As seen in cross section, the annular ligament consists of two concentric,

.white fibrous connective tissue sheaths condensed into a single layer

31

dorsally between the ring tips, as well as throughout the perimeter of
the cylinder between two adjacent cartilaginous rings, as seen in a
longitudinal section. The cartilaginous rings are actually contained
within the annular ligament; consequently, the architectural relation-
ship of these two structures renders an externally corrugated appearance
to the trachea. Circularly directed collagenous fibers predominate
throughout the ligament, while circularly and longitudinally directed
elastic fibers are plentiful only in the condensed area between the
ring tips. The transversely directed elastic fibers extend for a short
distance along the internal and external surfaces of the cartilage.
Throughout the remainder of the annular ligament are isolated elastic

fibers having a random direction (Plate XDC).

TRACHEALIS MUSCLE
The trachealis muscle, composed of smooth musCle tissue, occupies

a dorsal position in the tracheas of Bos, Capra, and Ovis (Plates IX,

 

XII, XIII and XX). The smooth muscle fibers are circularly disposed

and attached to the inner perichondrium a short distance from the carti-
laginous ring tips. Several transversely arranged elastic fibers are
interposed between the smooth muscle fibers and the inner perichondrium

of the cartilage (Plate XX). The trachealis muscle is most expansive at
the dorsal mid-line of the trachea and tapers to narrower proportions
laterad. In.Bp§ the magnitude of the trachealis muscle increases from

the cranial to the caudal level; in‘Qyip, as in‘Qppgg, the magnitude
remains constant, but in the former the thickness increases slightly from
the anterior to the posterior end; in'gpppa the thickness of the trachealis

muscle is nearly equal at all levels (Table 5).

32

The trachealis muscle is frequently occupied by tracheal glands
and pierced by the ducts of these glands (Plates IX and XII).

No longitudinally disposed smooth muscle fibers were observed.

mmmammsae

The smallest blood vessels are found in large quantities through-
out the lamina propria. Numerous larger blood vessels are present in
the submucosa in the ventral and lateral regions; however, in the sub-
mucosa of the dorsal region, few blood vessels are present, and those
which exist are of a small caliber. Blood vessels of a diameter between
those of the lamina propria and the larger ones of the submucosa are
located within the vicinity of the tracheal glands.

The adventitia contains large blood vessels whose walls are the
thickest of any of the blood vessels seen in the trachea.

The membranous region external to the trachealis muscle is usually
well populated by blood vessels.

Lymphatic vessels are difficult to distinguish, but careful examina-
tion reveals small numbers of these collapsed vessels in the lower depths

of the lamina propria.

NERVES

Large nerve trunks are usually seen in the dorsal region in either the
adventitia or in the membranous area external to the trachealis muscle. In
older cattle possessing a ridge formed by the extended opposing ring types,
one and frequently two nerve trunks are seen in the adventitia whose medial
margin is marked by the ring tip having the greater curvature. An extreme

variation of this relationship is depicted in Plate XXII.

33

Smaller nerve trunks are, in many instances, situated laterally

in the adventitia. No nerve trunks are seen in the ventral adventitia.

ADVENTITIA

Peripheral to and completely investing the tracheas of Bpp, Ca ra,
and‘Qpip is a layer of loosely arranged collagenous fibers and adipose
connective tissue, the latter decidedly the most abundant component of
the adventitia (Plate XVI). Connective tissue cells are sparsely dis-
tributed throughout this investment. As previously stated, the adventitia

contains blood vessels, as well as nerve trunks.

COMPARATIVE HISTOLOGY

The aim of the veterinary histologist is to establish the general
histological criteria by which he can diagnose a given organ or its
counterpart peculiar to several species. The results of this investiga-
tion, as well as those of Niewenhuis (1961), appear in a chart (page 34),
which is a condensed presentation of those histological characteristics
considered the distinguishing features of the tracheas of 22p,‘ggpi§,

Capra, Felis, and Ovis.

34

 

 

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mm on n ms 00 H0 0m H0 00 00
mm 00 u He 00 05 am mm 00 Nm
Annmamnv
0m ~s.- oe om Na ow me as «N saeadauaam
umoz owcmm coo: owdmm coo: mwamm
o 0 m unpuopuum
Lmswo>oq

won 00 mosomua mo mousuosuum ownoomouoflz mo Amaouowa GHV muaofioupmmoz

H manna

36

Havana u o

maeeae - a
Hoaamuo u m as

Hmuuao> u >
HMHOUNH .- .H
Hmmuov u n s

 

 

 

Ammonxoanuv
ANN 0NmH mNN N~0 Nana mad N00 N00 0cm Q waves:
00 Nu «a He Nu 0H 00 mod 0N >
me ma Nm es ea em we as ea 4 Aaeedxoaeuv
Amusedav
mm 00 0H N0 00 0H mm 00 0H m asauwconofiuom
0HH 00H N0 00H 00H 00 mHH an 00 >
em mmH mm as sea as we HNH em a Aeaodaoaaev
AmwamuSOV
on H0 mm 00 00 N0 00 H0 oq n aswnwconowumm
0m0H mNmN HNOH 00mm 0500 HO0H 00mm 0000 «m0a >
mnma 0000 000 0HOH 0omN 000 m0na no0m H00 A
Ammonxoanuv
mam mos 0AA see aeoH aNH «mm seen HON a .ewaaauueo
00m 0mm HOH ooq 0mm 00 mO0 00¢H mHH >
000 000 55H ¢0~ 0N0 ma 0mm N00 0 A
. Aguadev
50H omN 0 now 0N0 0 mm 00m 0 n mmoopanpm
coo: owcmm :moz uMdmm cum: owamm
o 0 m ; scammed oupuopuum
inHot/ma

 

Aeosafiuaoov H aHan

37

Amvsmo u o

oAchE I A
AmAamuo n a Rs

Amuuuo> u >
AmuouwA a A
Ammuov a 0 s

 

 

 

0.A 0.A 0.0 A.A 0.A u 0.0 A.A 0.A 0.0
~.A 0.A 0.0 0.A 0.A u 0.0 A.A 0.A 0.0
AnoumEmAvv
N.A 0.A 0.0 N.A 0.A a 0.0 A.A 0.A 0.0 muonAm oAumoAm
5m mum 00 mm 005 1 N0 00A 05¢ 00
0AA mmN 00 00A 000 u 00 mNA 00m N5
Ammocxoanuv
A5A «00 00 00A 000 u 00 00A 000 N5 unmanauz afiummAm
0.0 N.5 0.0 0.0 N.5 a 0.0 0.0 N.5 0.0
0.0 0.5 0.0 0.0 N.5 a 0.0 0.0 «.5 0.0
Anuwaeflv
0.0 ~.5 0.0 5.0 N.5 a 0.0 0.0 «.5 0.0 «AAAU
00 00 mm 00 «5 a 00 00 «a As
An 05 N0 00 00 1 mm 00 N5 NN
Aunmfidnv
an no 0H an no - um am He ma eaaaeeuaau
coo: owdmm :moz swamm coo: wwwmm
o 0 m taOAwoM manuosuum
mkao>oA

 

mummo mo cocoons mo mouauophum camoomOHUAz_mo Annouoae aAv mucoaouamwoz

N oAan

38

Amvamo n o

mAvaE a n
AmAdeo n m st

Amuuao> a >
AmuoumA u A
Ammuov a 0 s

 

 

 

Assessoanuv
AmA 000 a N0 00A NNm N5 00A 050 A0 0 vomaz
0A N0 u 0 0A 00 0 AN 00 0 >
0N 00‘s 0 0N 00 0A 00 00 0A A ammoaonsuv
AowAmaAv
AA N0 us0 NA N0 0 0A 00 0 0 asAnvaosoAnom
00 A0 u 00 00 00A 00 A0 50 N0 >
mm Am - 0A Am AAA om me as em a AaaoexoaauV
AvamuaoV
0N 00 u 0 0N 00 0 0N 00 0 a a=AHUGOSUAHom
0N5 ANOA n 0A0 050 0NOA 005 000 05NA 000 >
ANO 050 u N00 050 AmmA 000 0N5 50AA 000 A
Aaamdxoaauv
AmN 000 u A0 0AN 00¢ ANA 00N 50¢ 00 0 owoAAuumu
00N 055 a 0AA AqN 000 0 00N 055 0 >
00A 000 u 00 00A 000 N5 00A 00¢ 00 A
AsuAdev
00 NqN n 0 55 AAe 0 50 00N 0 0 amounanpm
coo: «flag new: mama cam: madam
o n AWN atOAwom oupuupuum
msAo>oA

 

AedaeAuaoev N eAaeH

39

Amwsmo u o
dAeeAa - a

AmAcmuo n o rt

Annuao> n >
AmuoumA a A
Ammuov a 0 *

 

 

 

 

 

0.A 0.A 0.0 A.A 0.A 0.0 N.A ¢.N u 0.0 >
A.A q.N 0.0 N.A 0.N 0.0 0.A N.m u 0.0 A
AnouoEMva
A.A 0.A 0.0 N.A N.0 0.0 N.A «.N n 0.0 n mumnAm OAummAm
m5 0AA 00 AOA 00A 00 AAA NqN n «N >
50 55A N0 00A 00A 0N mNA mNN u 00 A
Ammoaonnuv
0AA «mm 00 00A 000 Nm 00A 000 a 0d 0 ocmunEoz UAummAm
N.0 N.5 N.0 0.0 N.5 N.m 0.0 N.5 a N.m >
0.0 N.5 N.0 0.0 N.5 N.m 0.0 N.5 u N.m A
Aaumeeav
0.0 N.5 N.m 0.0 N.5 0.N 0.0 N.5 u N.0 0 «AAAU
50 00 00 Am 00 N0 A0 00A n An >
A0 0AA A0 00 AOA «0 A0 00A a «0 A
AunwAmnv
00 00A «N 00 00 0 Am AOA a 5 0 BSAAonuAau
coo: mudmm coo: owdmm coo: swoon
o 0 w «WOAwum ouauopuum
o>oA
mA>o mo mosowuH mo moupuupuum oAnoomouon mo AnnoquE :Av muamaouammox

m mAQMH

40

Amwsmo a o

Annuao> u >

 

 

 

oAvaE n n AmumumA u A
AmAamuo u m as Ammuou u 0 %
A...aaaaaao
500 ANOA 00. 50N 000 50 00N 000 00 0 vomsz
0A N0 0 NN 05 5 0N 00 0.0 >
AA as a ma we a an oAA e.m A Aaeeaaeaan
onAmnAv
0A 00 0.0 AN 00 0 0N 00 0.0 0 asAuwconoAuom
05 ANA NN 00 00A N0 55 ANA 0N >
00 50 0A 05 0NA 0A A5 50 NN A Ammoaonnuv
AowAmu50v
00 N5 0A 00 N5 0A 00 50 0A 0 EpAuvaosoAuom
NOAA 00AA 0A5 00AA 500A NAO 0ANA 000A 000 >
000 NNqA 00m 500 NNqA 0N0 A50A 0NOA 000 A
Ammoaonnuv
000 000 00A N00 0N0 A0 N00 000 50A 0 owmAAuumo
A00 000 ANA 000 005 ANA 050 0N0 AOA >
00N A05 N5 0A0 005 05 000 055 50 A
Asuamev
00 0NN 0 05 NqN 0 «AA 000 0 0 mmooaanam
coo: omamm coo: mwcmm coo: uwdmm
o 0 m sakoom ousuonuum
nssAo>oA

 

AvopaAuGOOV 0 oAnma

41

Table 4

Comparison of the mean values (in microns)
of the structural dimensions of the tracheas of
Bos, Capra, and Ovis at the
dorsal, lateral, and ventral regions

 

 

 

Structure Region* Bos Capra Ovis

Epithelium D 50 37 50

(height) L 55 48 58

V 59 48 56

Cilia D 6.9 6 6 5.7

(length) L 6.8 6 6 5.8

V 6.8 6 6 5.9

Elastic Membrane D 281 164 134

(thickness) L 282 126 107

V 295 112 95

Elastic Fibers D 2.0 l 1 1.1

(diameter) L 2.0 l l 1.2

V 2.0 1.0 1.1

Submucosa D 134 58 92

(depth) L 306 180 394

V 431 236 391

Cartilage D 416 253 380

(thickness) L 1716 672 951

V 2479 879 1169

Perichondrium D 50 24 40

(outside) L 76 45 70

(thickness) V 112 62 82

Perichondrium D 33 13 20

(inside) L 61 26 26

(thickness) V 44 18 18

Muscle D 594 153 290
(thickness)

 

* D - dorsal
L - lateral
V - ventral

Comparison of the mean values (in microns) of the
structural dimensions of the tracheas of Bos,

42

Table 5

Capra, and Ovis at the cranial, middle, and caudal levels

 

 

 

 

B03. Capra Ovis
Level? a, b c a, b c a b c
Structure
Epithelium 53 55 56 43 43 47 58 51 56
(height)
Cilia 6.8 6.8 6.7 6.5 6.6 6.7 5.7 5.7 6.0
(length)
Elastic Membrane 272 1331 261 142 130 127 131 113 93
(thickness)
Elastic Fibers 2.1 2.1 1.7 1.1 1.1 1.1 L1.2 1.2 1.1
(diameter)
Submucosa 326 296 233 148 172 156 324 314 239
(depth)
Cartilage 1716 1612 1282 643 620 544 889 839 771
(thickness)
Perichondrium (out- 80 75 83 46 47 37 64 70 58
side) (thickness)
Perichondrium (in- 48 49 41 23 19 15 26 23 16
side) (thickness)
Muscle 432 622 727 159 168 131 265 297 307
(thickness)

 

*a - cranial
b - middle
c - caudal

43

Table 6

Comparison of the total mean values
(in microns) of microscopic structures of
the tracheas of Bos, Ca ra, and Ovis

 

 

Structure Bos Capra Ovis

Epithelium 55 44 ‘55
(height)

Cilia 6.8 6.6 5.8
(length)

Elastic Membrane 286 133 112.2
(thickness)

Elastic Fibers 1.9 1.1 1.1
(diameter)

Submucosa 290 158 292
(depth)

Cartilage 1537 591 833
(thickness)

Perichondrium 79 44 64
(outside)
(thickness)

Perichondrium 46 19 22
(inside)
(thickness)

Muscle 594 153 290

(thickness)

 

SUMMARY AND CONCLUSIONS

Routine histological staining methods were used to study the tracheas
of thirty-six animals--twelve each of §p§,.gap£a, and.Q!i§--including both
male and female specimens. A range and mean value (in microns) were estab-
lished for each structure measured.

The tracheas of Bos, Capra, and.Q!i§ display three major layers,
namely, 1) a mucosa containing an epithelium, a basement membrane, and
a lamina propria; 2) a submucosa; and 3) a fibroelastic-cartilaginous
layer.

The mucous membrane of the tracheas of B08, Capra, andlggig is lined
predominantly by a pseudostratified, ciliated, columnar epithelium contain-
ing goblet cells. This type of epithelium is present at each of the three
levels examined, as well as the dorsal, ventral, and lateral regions. Four
cell types exist in the tracheal epithelium and are readily identifiable in
each specimen examined. The goblet cell, most abundant ventrally, less
laterally, and least dorsally, rests on a basement membrane and extends
through the epithelial layer to reach the lumen of the trachea. The basal
cells are situated in a conspicuous row immediately above the basement
membrane. The intermediate cells may or may not extend through the mucous
membrane. The bases of the ciliated cells lay fixed on the basement mem-
brane, while the apices are covered by the mucous blanket of the lumen.

In.§pp the epithelium displays slight undulations with a general
uniformity in height. The epithelium of Qpppa exhibits pronounced undula-
tions with uniform thickness. In'Qxip, intraepithelial crypts are evident

and the height of epithelium is not uniform.

44

45

Leukocytic invasions of the epithelium are frequently seen in the
tracheas ofifip§,'gap£a, and gyip. Lymphocytes are the outstandingly
predominant type of leukocyte.

The longitudinally directed elastic fibers of the lamina propria
are organized into a fasciculated elastic membrane. The fasciculi are
least conspicuous in Egg and Qapga, but evident in.Qgi§.

Lymphoid tissue is commonly present in the lamina propria of the
bovine, caprine, and ovine tracheas. In addition to the presence of a
mild concentration of lymphocytes immediately below the epithelium, lymph
nodules occur frequently in the lamina propria and the submucosa. Lympho-
cytes are often situated in the nearby connective tissue substance.

White fibrous connective tissue and glands comprise the greater part
of the submucosa. The depths of the respective submucosae in Egg, Qappa,
and gyip decrease from the ventral to the lateral region and are, in many
cases, absent or shallow in the dorsal region at all levels. The depths of
the submucosae of Egg and.Qpi§ are nearly equal. The submucosa of the
trachea of Qapga is approximately half as deep as those of Bpp and‘Qgig.

The glands, present in both the lamina propria and submucosa of the
tracheas of Bos, Capra, and Qgip, are of the branched, tubuloacinar type,
the acini of which are most frequently mixed in character. In each of
the three species, the glands are most numerous ventrally, less abundant
laterally, and least ‘numerous dorsally. The glands may or may not be
situated posterior to the trachealis muscle. In Ca ra, the glands are
commonly implanted in the ventral and lateral regions of the adventitia
between the cartilaginous rings and are enveloped, in part, by the

annular ligament.

46

The epithelial cells of the gland acini vary from low columnar to
cuboidal. A single acinus may contain all serous’or all mucous cells or
varying quantities of both cell types.

The dorsally incomplete, cartilaginous rings, present in'gpp, Qappa,
and‘Qpip, are composed of hyaline cartilage. The rings have a C-shaped
form in the sheep, goats, and young cattle; however, in older cattle the
tips of the rings oppose each other to lie parallel for a short distance.
The cartilaginous rings of each species are thickest ventrally, thinner
laterally, and least thick dorsally. The thickness of the tracheal rings
decreases from the cranial to the caudal level. The internal and external
perichondria are composed of white fibrous connective tissue. The latter
is thinner than the former.

The annular ligament, composed of white fibrous connective tissue with
interspersed elastic fibers, completely encompasses the cartilaginous rings
of the tracheas of Bos, Capra, and'Qgig. The cartilaginous rings, therefore,
are actually contained within the annular ligament.

The trachealis muscle, composed of circularly directed smooth muscle
fibers, occupies a dorsal position and attaches to the internal face of
the cartilaginous rings by means of elastic tendons. The thickness of the
muscle is greatest at the dorsal mid-line, tapering to smaller dimensions
laterad. Glands frequently occupy the trachealis muscle.

The smallest blood vessels are found in large quantities throughout
the lamina propria. Numerous larger blood vessels are present in the sub-
mucosa. The adventitia contains blood vessels, the walls of which are the
thickest of any of the blood vessels seen in the tracheas. Blood vessels

are numerous in the dorsal, membranous region of all the tracheas.

47

Nerve trunks are present in the dorsal region in either the adventi-
tia or in the membranous area external to the trachealis muscle. Small
nerve trunks are situated in the lateral adventitia.

Peripheral to and completely investing the tracheas of‘Bpp, Qapga, and
.Qyig is a layer of loosely arranged collagenous fibers and adipose connec-
tive tissue comprising an adventitia. The adipose tissue is the most abun-
dant component of the adventitia.

Differences between male and female specimens of each species are not

observed in the trachea.

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49

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51

Plate 1. A comparison of cross-sectional views of
the bovine, caprine, and ovine tracheas; ventral
region, caudal level. Note the relative thicknesses
of each layer. Hematoxylin and eosin stain; x 140.

l. epithelium

2. elastic membrane

3. adipose tissue

4. submucosa

5. collagenous fibers

6. cartilage

 

52

 

r3“ '
3 .3
1 ’fl ‘

 

 

53

 

Plate II. Cross-sectional view of ovine tracheal epithelium
and its four cell types; ventral region, cranial level.

1, goblet cell; 2, intermediate cell; 3, ciliated cell;

4, basal cell; 5, lymphocyte; 6, blood capillary; 7, gland
duct. Hematoxylin and eosin stain; x 364.

54

      

. ,4; .
.‘h ifWfi’it-W' .

O
_ ‘vacm

Plate III. Cross-sectional view of ovine tracheal mucous
membrane; lateral region, middle level. Note the difference
in cell alignment at bottom of crypt and at corresponding

level of duct. 1, duct; 2, crypt; 3, cilia; 4, lamina pro-
pria. Hematoxylin and eosin stain; x 813.

55

 

Plate IV. Polar view of basal cell during metaphase of
mitotic division; lateral region, middle level of ovine
trachea. l, basal cell; 2, mitotic figure; 3, basement

membrane;4, lamina propria. Hematoxylin and eosin stain;
x 2067.

56

 

Plate V.

Cross-sectional view of pronounced mucosal folds in
dorsal region of middle level of bovine trachea.

l, mucosal
fold; 2, lamina propria; 3, trachealis muscle; Toluidine blue
stain; X 57 .

57

 

Plate VI. Cross-sectional view of ovine trachea showing
lymph nodule in submucosa and lymphocytic invasion of
epithelium; ventral region, middle level. 1, epithelium;
2, lymphocytic invasion; 3, lamina propria; 4,1ymph nodule;
5, scattered lymphocytes; 6, blood vessel. Hematoxylin and
eosin stain; x 126.

 

Plate VII.

long,patent duct of mixed, sero-mucous gland; lateral region,

Cross-sectional view of bovine trachea showing

cranial level. 1, epithelium; 2, duct containing glandular

secretion; 3, gland acini; 4, lamina propria; 5, submucosa.
Hematoxylin and eosin stain; x 156.

59

 

Plate VIII.

short,patent, branched duct of mixed, sero-mucous gland;

Cross-sectional view of ovine trachea showing

ventral region, middle level. 1, epithelium; 2, patent
duct of branched tubular gland; 3, lymphatic vessels in

lamina propria; 4, serous cells; 5, mucous cells.

Hema-
toxylin and eosin stain; x 220.

60

 

Cross-sectional view of ovine trachea showing

gland duct piercing the trachealis muscle; dorsal region,

Plate IX.

1, lumen; 2, duct; 3, trachealis muscle;

caudal level.

Hematoxylin and eosin stain; x.68.

4, gland acini.

61

Plate X. Mixed, sero-mucous glands in submucosa as seen
a cross-sectional view of ovine trachea; ventral region,
cranial level. 1, epithelium; 2, lower limit of mucosa;

3, branched, tubuloacinar, mixed, sero-mucous glands.
Toluidine blue stain; x 136.

 

in

 

 

Plate XI. Cross-sectional viewcfifbovine tracheal glands;
ventral region, caudal level. 1, epithelium; 2, lamina
propria; 3, branched, tubuloacinar, mixed, sero-mucous
gland; 4, submucosa. Toluidine blue; x 64.

 

Plate XII. A field of mucous acini situated within the
trachealis muscle as seen in a cross-sectional view of
ovine trachea; dorsal region, cranial level. 1, goblet
cells; 2, mast cell; 3, trachealis muscle; 4, mucous acini
of tubuloacinar gland. Toluidine blue stain; x 186.

64

 

Plate XIII.

A field of serous acini situated within the
trachealis muscle as seen in a cross-sectional view of
ovine trachea; dorsal region, cranial level. 1, epithe-
lium; 2, lamina propria; 3, trachealis muscle; 4, gland
duct; 5, gland acini. Hematoxylin and eosin stain; x 220.

 

Plate XIV. Cross-sectional view of intercartilaginous area
of caprine trachea; ventral region, middle level. 1, epithe-
lium; 2, gland acini in lamina propria; 3, gland acini in
submucosa; 4, annular ligament; 5, gland acini in adventitia;
6, adipose tissue. Toluidine blue stain; x 96.

66

 

Plate XV. Cross-sectional view of caprine trachea depicting
glands both internal and external to cartilaginous ring;
ventral region, cranial level. 1, epithelium with goblet
cells; 2, gland acini in lamina propria; 3, gland acini in
submucosa; 4, cartilaginous ring; 5, gland acini in adventi-
tia. Toluidine blue stain; x 74.

67

 

Plate XVI.

of caprine trachea; lateral region, caudal level.

thelium; 2, gland duct; 3, glands in submucosa; 4, hyaline

cartilage; 5, glands in adventitia; 6, adipose tissue.
Toluidine blue stain; x 101.

Longitudinal view of intercartilaginous area

1, epi-

68

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.\ A ‘ .. \:. V , . n -“ . A ‘ . ‘ , ‘. v "\y - 1“,»39“! ”8".“ .‘
‘ . Q ‘. ‘y. _ ‘ " ‘0
. .. _ I . ‘ v . C4K.‘“".ryor :1 r’o:“‘i
O . o. . .
‘ .

 

Plate XVII. Glands of the intercartilaginous area enveloped
by annular ligament as seen in a longitudinal view of
caprine trachea; ventral region, caudal level. 1, epithe-
lium; 2, elastic membrane (note longitudinal direction of
fibers); 3, gland acini enveloped by annular ligament;

4, annular ligament; 5, gland acini in adventitia. Weigert-
Van Gieson stain; x 111.

69

 

Plate XVIII. Longitudinal view of three overlapping rings
with intervening glands in ovine trachea; ventral region,
cranial level. 1, epithelium; 2, hyaline cartilage; 3, gland
acini; 4, elastic fibers. Weigert-Van Gieson stain; x 74.

 

Plate XIX. Cross-sectional view of bovine trachea showing
typical arrangement of layers; ventral region, cranial
level. 1, epithelium; 2, lower limit of lamina propria;

3, submucosa containing glands. Hematoxylin and eosin
stain; x 158.

71

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. ,|
' Q
q 0 I O
- a I
‘ .
')
7 g ’
' I". ’.
.1.
’ 6
CL- 1 '
I ‘ ‘

53:29

. .
a
s ”.4
4
3

Jk

 

Plate XX. Cross-sectional view of ovine trachea showing
insertion of trachealis muscle and "elastic tendons";
dorsal region, middle level. 1, epithelium; 2, elastic
membrane; 3, trachealis muscle (note its insertion on
outer face of the inner of two overlapping rings);

4, elastic tendon. Weigert-Van Gieson stain; x 63.

 

Longitudinal view of bovine trachea showing

elastic character of hyaline cartilage; dorsal region,

Plate XXI.

l, hyaline cartilage; 2, elastic fibers.

weigert-Van Gieson stain; x 394.

middle level.

73

 

Plate XXII. Cross-sectional view of bovine trachea showing
atypical location of two nerve trunks; dorsal region, middle

level. 1, cartilage ring tip; 2, nerve trunks; 3, adventi-
tia. Hematoxylin and eosin stain. x 85.

N32!" 2 i; 332:5