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Variations in the wall of the large intestine and in the number and staining properties of the goblet cells.

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THE
ANATOMICAL RECORD
VOl. 11.
JULY, 1908.
No. 4
Variations in the Wall of the Large Intestine and in the Number and
Staining Properties of the Goblet Cells.
BY
RICHARD W. HARYEY.
From the Anatomical Laboratory of the University of California.
With Eight Figures.
The purpose of this paper is to describe some variations observed in
thickness of wall and in the depth and arrangement of the glands of
Lieberkuhn of the different regions of the large intestine in different
states of distension, and also to note some variations in the number
and staining properties of the goblet cells in the different regions. The
regions or parts of the large intestine considered are the caecum, ascending colon, transverse colon, descending colon, and rectum. Comparisons
are made first, between different regions in the same degree of contraction, and second, the same regions are compared, the contracted with
the distended condition. These comparisons comprise :
1. Variations in the thickness of the mnscular tunic in the dif€erent regions.
2. Variations in the shape of t h e intestinal (Lieberkuhn’s) glands in
the different regions.
3. Variations in the depth and cross section of the intestinal glands
in the different regions.
4. Variations in the depth and cross section of the glands and in
the thickness of the muscular tunic produced by distension.
5. Variations in the number and staining properties of the goblet
cells in the different regions.
2liaferial and Methods: Sections of human large intestine were
used in making the comparisons involving the staining qualities and
130
The Anatomical Record.
number of the goblet cells, and, in addition to the human, a dog's large
intestine was used in all comparisons involving measurements.
The human material had been obtained in an unusually fresh condition from the body of an executed criminal, and proved to be exceptionally good for the purpose in hand. Even the superficial cells of the
epithelium were remarkably intact and usually in no way disarranged.
At the time of obtaining the material, short lengths of the intestine
were distended with Zenker's fluid by means of a large syringe, each
piece being ligated so as to retain the fluid forced into it, then severed
from the rest of the intestine and immersed, distended as it was, in a
copious amount of the same fluid. Attempts were made, but roughly,
owing to the haste that was necessary, to use the same amount of
pressure in distending the different pieces. Other pieces of this intestine, in each case immediately adjacent to those distended, were clipped
off and, undistended, were dropped into the vessels containing the
corresponding distended pieces. These pieces became fixed, of course,
in a highly contracted condition. Unfortunately, both distended and
contracted pieces from each of the regions here considered were not
prepared at the time, and thus the necessary pieces for a complete comparison of the human material were not available for each region. The
pieces of human intestine which could be used may be described as
follows :
From the csecum-two pieces, one contracted, and the other distended.
From the ascending colon-one piece, somewhat contracted.
From the transverse colon-two pieces, one contracted, and one much
distended.
From the descending colon-two pieces, one contracted, and one distended.
From the rectum-two
pieces, one contracted, and one partly distended.
Obviously supplemental material was necessary to fill in the gaps in
the evidence obtained from the human material. The dog's large intestine was chosen for this purpose because of its slight resemblance to the
human large intestine, and also to determine the variations in the dog
itself. The supplemental material, in addition, made it possible to
compare variations of the dog's intestine with the human intestine.
The large intestine was removed from a freshly killed dog, and the
rectum tied off at its junction with the descending colon. A large rubber-bulb syringe containing normal salt solution was inserted at the
The Anatomical Record.
131
anus, and pressure applied to the bulb. When the intestine had reached
a presumably normal degree of distension the anal end was tied. The
distended rectum was then severed and placed in Zenker‘s fluid. Pieces
of the descending colon, transverse colon, ascending colon and caecum
were distended and fixed in the same way, the degree of pressure
exerted in each case being, as nearly as could be determined, the same
as in the rectum. The caecum was distended entire. When suf3ciently
hardened, the different pieces were slit open and the salt solution (now,
by osmosis, dilute Zenker’s fluid) emptied out, and the fixing fluid
replaced with fresh.
In choosing the bits for study, small squares of the human intestine
were cut from midway between the ttenis coli in each case. Two
similar areas of the dog‘s intestine were cut out, one from the distended
part and one from the contracted end of each piece, near the ligature.
No taenia! are dehitely differentiated in the dog‘s large intestine. I n
all cases, these bits taken were placed in separate vials, appropriately
labeled, and thus carried through the procedures necessary. The tissues
intended for measurements were embedded in celloidin and cut, and
the sections stained in hzemotoxylin and congo red. Measurements were
taken with an eye-piece micrometer whose spaces had been standardized
in microns.
h’ORIIAL
rTARIATIONS OF
DIVFERENT
REQIONSOF
THE
LARQEINTEETIRE.
The intestinal wall was found to be normally thinnest in the caecum
and gradually thickens as the anus is approached. In contraction the
mucosa forms folds to accommodate itsclf to the contracted muscular
wall, and the glands, therefore, are compressed within the crevices
between folds, and thus are frequently bent at a sharp angle with the
plane of the surface. In distension the folds are straightened out,
except in the rectum, the crevices disappear, and the glands stand
uniformly perpendicular to the surface.
The glands are closely packed together, here and there a lymph nodule
pressing them apart. They are straight tubular in shape. Those of
the cmum are short and thick, somewhat club-shaped, with a constriction a t the neck, and less thickly distributed than those further on in
the colon. In the ascending colon the glands are more closely packed
together than elsewhere, are much more long and slender than in the
cmum, are compressed against the muscularis mucosae at the fundus,
and are slightly constricted at the neck. In the transverse colon the
The Anatomical Record.
132
Depth of
Gland.
Region.
-
j
-~
:on. Dist
Dist.
--
-
373
302
324
-
--
474
317
58
--
-
98
33 1
__
599
58:
17
__________
~
68
62
-431
28)
~-
5
15
44
-
507
-
123
-
229
-
186
-
317
-
287
-
23f
* Separately stained preparation.
TABLE1. Recording average measurements showing in niicrons the rnri3tions in thickness of the wall of the large intestine in the different regions,
both human and dog, contracted and distended, and giving the number and
relatire depth of staining of the goblet cells.
The Ahatoinical Ilecord.
133
glancls are likewise long and slender. though they are shorter than tllosc
of the ascending colon, are less thickly distributed, and are more biilging
ilt the fundus. The glands of the dcsccnding colon, though longer than
those of the caecum, are shorter than those of the transverse colon, are
Aout equal to the latter in cross section, antl arc constricted at the neck.
They are closely packed together. and in places are much compressed
against the niuscularjs niucosw. The rectal glands are short and stout,
ncarly uniformly tubular, antl more sparacly distributed than in the
ctpcurn.
I n no region of the largc intestine was thcre seen evidence of branching as has been observed in tlic duodenum and jcjunum. Between the
folds of the mucosa of the rectum two or tlirce glands sometimes open
c';PCUlll
Asc. Colon
Transv. Colon
Desc. Colon
Rectum
FIG.1.
Curyes plotted from iiieiisiii'emeiits recorded i n Table 1, esprrssing the variations in thickness of t h e intestinal wall in the different regions
of the dog's large intestine, h when coiitracted, R when distended.
into a kind of yestibide; but this condition is probably due t o compression rather than being a persistent structure or a suggestion of
branching.
The accompanying table rccords measurements in microns averaged
from measurements of a number of different glands in each region of
the human and dog large intestine, affording data for the coinparison
of variations in depth and cross scction of glands, in thc interglandular
space, and in the thickness of the entire intestinal wall and of the
muscular tunic and the niuscularis mucosae. Measurements mere taken
from the cuticular border of the surface epithelium, or that directly
hounding the lumen of the intestine, to the outer margin of the tnnica
adventitia, except in the wction of transverse colon of the clog, the
The Anatomical Record.
134
surface epithelium of which was destroyed. Fig. 1 is plotted from the
tabulated measurements of the dog‘s intestinal wall contracted (A) and
distended (B). The ordinates are graduated in microns and the
ubscissze are equal spaces, representing the five different regions.
Under like conditions of contraction and distension the thicknesses
vary as follows: In contraction the greatest thickness is in the transverse and descending colons, the least in the rectum; in distension, the
greatest thickness is in the ascending colon, the least in the transverse
colon. The greatest diminution in thickness with distension occurs in
the transverse colon, the least in the rectum.
VARIATIONS IN
DEPTHOF THE GLANDS OF THE DIFFERENT
RFGIONS IN
CONTRACTED
AND DISTENDED
CONDITIONS.
THE
The depth of glands was measured from the basement membrane of
the surface epithelium to the basement membrane of the fundus; and,
in all cases, glands cut longitudinally throughout their length were
I
C:Pcnm
Asc. Colon
Transv. Colon
Desc. Colon
Rectum
FIG.2. Curves plotted from measuremeiits recorded in Table 1, expressing
variations in the depth of glands in the different regions of the dog’s large
intestine, A when contracted, B when distended.
FIG.3. Curves plotted from measurements in Table 1, expressing variations
in cross section of glands in the different regions of the dog’s large intestine,
A when contracted, B when distended.
selected, that the measurements might coincide with the Icngths of
their axes.
The contraction being approximately the same for each region, the
depths of the glands are found to vary as follows: Greatest in the
The Anatomical Record.
135
ascending colon, gradually diminishing to the least depth in the rectum.
Fig. 2, A is plotted for the contracted dog’s intestine from the measurements tabulated in the table above. The distension being approximately
the same for each region, the depth i n the distended pieces appears to
be greatest in the ascending colon, but least in the transverse colon
instead of in the rectum, and between these two extremes in the remaining regions. Fig. 2, B is plotted from the tabulated measurements of
the dog’s intestine distended. The greatest diminution in depth with
distension is seen to be in the transverse colon, the least in the ascending
colon. Mathematically expressed, the depth of the glands of Lieberkiihn
of the large intestine varies inversely as the distension. A comparison
made with the human caecum, but not taken into account i n plotting
the curres of variation shows variations which correspond with those of
the dog’s intestine.
7-ARI.iTIOXS IH CROSS SECTIONS OF TIIE GLAXDS IN DIFFEREXT
REGIOXSIN
TIIE
COXTRACTED
A N D DISTER’DED
CO~-DITIONS.
The cross section of the glands was determined by measuring the
distance between the basement membranes of the sides of each gland in
longitudinal section. It does not take into account the constrictions
and bulges, but is, as far as possible, the average diameter of a gland.
Cnder like conditions of contraction and distension the cross sections
or diameters of the glands are found to vary as follows: In contraction,
the greatest diameter is in the rectum, the least in the ascending colon,
between which is a gradual diminution, as shown i n the table and by
Fig. 3, A. In distension, the greatest cross section is in the rectum, as
in contraction, while the least is in the transverse colon instead of in
the ascending colon (Fig. 3, B) .
Comparing the contracted intestine with the distended, it appears
that distension produces a diminution in the diameter of the glands.
The greatest diminution i n the diameter of the glands occurs in the
transverse colon, the least in the ascending colon. Mathematically espressed, the diameters of the glands varv inversely as the distension,
just as do the depths of the glands. The human caecum contracted and
distended shows corresponding variations. This similarity i n the variation in depth and diameter indicates that distension, instead of compressing the glands against the muscular tunic and making them thicker,
as well as shorter, must result in stress upon the glandular epithelium
which produces a slight general decrease in the thickness of their epithe-
The Anatomical Record.
136
lium and in the diameter of their duct8, ancl which strcss, instead of
compression, must, to some extent, lend to the decrease in their dcpths.
Measurements show this to be true, and it may be seen in the outline
drawings in Big. 4. This figure shows that the funcli of the glands
only are occasionally affccted by coinprcssion against the grcatlg thinned
snlmiiicoaa ancl musculiir tunic.
EP.4
A
B
(':rc~ulu
;\sc. Colon
Traiisv. Colon
Desc. Colon
Rectuiu
Fiu. 4. Outline drawiiigs, iiiade with c'uiiiern luc'ida. all under the s:me
magnification, and corrected bj- micronieter measurements, showing the vnriations i i t the depth niid dinirreter of the glaiids arid in the intei*glniidnlnr
spares of the different regions of the indicated dog's large intestine, -4 in the
contr:icted, and B in the disteiiued contlition.
YARIATIOXS OF INTERGLASI)TI.AR SPAC'E IN DIFFERENT I<EQIONS 1 3 TIIE T W O
CONDITION
s.
The interglandular space mas measured from the basement membrane
of one gland to that of an adjacent gland, both glands being longitu-
dinally sectioned through their axes. The degree of contraction ancl
distension being the same for all regions, the measurements, recorded in
the table, show that the spaces vary as follows: Tn contraction, the
Tlic Anntcmical Recorcl.
137
grciitcd breadth of s.pace is bet\wcn the gliincls of the rectum, next the
transvcrsc colon, tlieii the ilewwling colon, ancl the least hrcwdth in
the ascending colon. That is, in n given contracted condition the glands
of the ascending colon appear to he niod tllickly distributed. Fig. 3
e i p r e w s thesc relations in the forni of a curve.
I n distension, the greatest space is in tlic transverse colon, diniinishing in the rectum, desccniling colon, ant1 cit'cuiii in the order giren, to
the least space wliich is found in the aFcending colon (Fig. ,5, R ) .
That is, in a given distended condition, as \wll as in the contracted,
ti0 5
r
Rectum
Transr. Colon
Desc. Coloii
FIG.3. Cnrres. cmatrnctrtl from tlie iiieasureueiits recorded in Table 1 ,
espreesing the rariatioiis in the breadth of the interglandular spaces of the
glands of the different regions of the dog's large intestine, A, when contract&,
(
':ww111
ASC. COlOll
aiid B. when distended.
tlie glands of the ascending colon are most thickly distributed. Mathematically expressed, the interglanilular space varies directly as the ilistension.
These observations indicate obviously that in all conditions the
mucosa of the ascending colon is more thickly stiidded with glands than
any other region of the large intestine. Further, the observation inade
above, that distension decreases the depth o f tlic glands, coupled with
the observation that it results in an increase in the breadth of the interglandular spaces, indicates that distension must increase the allsolute
ares of the superficial epithelium or of thnt glandular surface directly
exposed to the intestinal contents.
~ - A B L 4 T I O S S IN T I I I C K x E S S O F ~ f r S C I T . A R I S JfVCOsAE.
The thickness of the niuscularis miicosa: ~ v a smeasured from the inner
margin of the inner, circular layer, to the outer margin of the outer,
longitudinal layer. Contracted. the mnsciilaris niucosa: is thickest in
138
The Anatomical Record.
the rectum, diminishes in the descending colon and ascending colon, in
the order named, and is thinnest in the transrerse colon (Fig. 6 , A).
Distended, it is thickest in the caecum, diminishes in the ascending
colon, rectum, and descending colon, in the order named, and is thinnest
in the transverse colon (Fig. 6, B) .
,a.
,
tlB h
1‘
4
B’
Asc. Colon
Transv. Co1on
Dew. Colon
Rectum
FIG.G. Curves, constructed from the measurements recorded in Table 1,
expressing the variations in thickness of the muscularis rnucosle of the
different regions of the dog’s large intestine, A when contracted, and B when
distended.
Ciecum
FIG. 7. Curves, constructed from the measurenients recorded in Table 1,
expressing the variations in thickness of the tunica muscularis of the different
regions of the dog’s large intestine, A mheu contracted, and B when distended.
The greatest diminution in thickness of the muscularis rnucosiz, due
to distension, occurs in the rectum, and the least in the ascending colon.
Mathematically expressed, the thickness of the muscularis mucosb varies
inversely as the distension.
VARIATIONS IN TEIICKNESS OF TUXICA hIUSCULARIS.
The thickness of the tunica muscularis was measured from the inner
margin of the inner circular layer to the outer margin of the outer
longitudinal layer, which latter in the dog forms a continuous sheath
instead of being partially assembled to form tzniae coli as in the human.
I n contraction, the thickness of the muscular tunic of the dog is greatest
in the descending colon, diminishes in the ascending and transverse
colons, in the order named, and is least in the rectum (Fig. 7, A).
The Anatomical Eecorrl.
139
Didelitled, the greatest thickness is in the ascending colon. It diminishes in the descending colon, caecum, and rectum, in the order named,
and it is least in the transrerse colon (Fig. ?, B). The greatest diminution in thickness, due to distension, is in the transverse colon, and the
least in the ascending colon. Rlathematically expressed, the thickness
of the tunica muscularis varies inversely as the distension.
YARIATIOXSIS GOBLET CELLS,
Method of staining : Maper's Muchaematein,' so effectively used by
BensleyYz though not absolute in its mncin reactions, yet furnishes
evidence as to the comparative staining properties of the goblet cells
in the different regions when the conditions of staining are exactly
alike. Bensley found that, by modifying Mayer's solutions, positive
results could be obtained. In fact, it is largely a matter of experiment
what strength of solution should be used and the time it should be
applied. The best results Irere obtained with a stock solution over a
Fear old, each 100 C.C. of which was diluted with 100 c.c 70 per cent
alcohol. This solution was applied for five minutes. To insure uniformity in application to the sections from different regions of the
intestine, all the slides bearing the thin pnraffine sections from the
different regions were clamped together in a Miller's multiples slideh ~ l d e r ,and
~ immersed together in a jar of the stain. A freshly prepared solution required a much longer time to give results which were
not nearly so good. The sections, still held in the slide-holder, were
washed simultaneously in distilled water, dehydrated by passing through
the alcohols, cleared in xylol, from which they were taken separately t o
be mounted in balsam. Several sets of sections were stained until
co-ordinate results were assured.
Counting the goblet cells is likewise largely a matter of practice and
the elimination of the personal equation. The glands selected for
counting were those cut longitudinally along their axes; and the goblet
cells counted were those lying in the nearest focal plane. To determine
the latter it was only neressary, while counting, to slightly turn the
fine adjustment and exclude all cells of s lower focal plane. It was
'P. JIayer, Mitth. a. d. Zool. Station zu Neapel, XII, pp. 303-30, Leipz.. 1899.
'R. R . Bensley. The Cardiac Glands of illammals. Am. Journ. Anat., Vol.
11. No. 1. 102, pp. 11&110.
F. Miller. A Multiplex Slide-Holding Device. The Johns Hopkins Hospital Bulletin, Vol. XVI, No. 169. April, 1905.
The Anatomical Xccord.
140
found impracticable to count by a plan of cell-ineasurement, assuiiiing
that the longest cells would be those lying in tlie sainc focal plane,
because the cells of the neck w r c found to be consiclerably Inrgcr than
those of the fundus.
\'.\R~ATIOXS
IN
R'uhrn~a OF GOBLET CELLS IN UIPFERENT R ~ s r o x s IS THE
])ISTENDED
CONUITION OF T H E
HUMANL.4RGE
INTESTISE.
l'he tabulated results of the counts, given with the measurements in
Table 1, are for the human intestine only. They are averages of the
number counted in the nearest focal plane of the longitudinal sections
of scveral glands of each region. The regions examined were approsimately equally distended, excepting the much distended transverse
colon and the somewhat contracted ascending colon. The results are
plotted in Fig. 8, the ordinates being the number of cells, and the
ahscissae the five regions of the intestine.
I
~;IY~lllll
Asc. Colon
I
I- -
-_
Desc. Colon
Rectum
___
Trnnsv. Colon
FIG.8. Curve coustructed froin the results tabulated iii Table 1 of the
arernge 1iuiiil)er of goblet cells in tlie iienrest focal lame of longitudiiinl
sections of glands in the different regions.
Repinning with the cecun1, tlie number of goblet cells per gland
decrenses in the ascending colon ; and they are fewest in the transverse
colon. In the descending colon they increase in number, and are most
abundant in the rectum.
\'ARIATIONS
IN J ~ L ~ C O U HEACTIONS
S
OF THE
GOBLETCELLS IN
TIIE
DIFFERENT
RFGIONS.
Since the sections of different regions were stained sinidtaneonsly
any variations in the depth of stain are indicative of differences in
The dnatoinical Record.
141
mucous reactions, and not over- or under-staining ; the time discrepancy
is completely eliminated by the use of the slide-holding device. I n the
section of transverse colon, stained with the others, the stain showed
a coagulum in the goblet cclls, and the tissue itself took the stain. A
block from another piece of transverse colon was takcn and prepared in
the same way, but stained separately, though under the same conditions
of time and solution. The sections of this block likewise stained much
more dceplp than any of the others. The fact that this color reaction
was obserred with a separatcly stained preparation is taken into account.
Whether the deeper staining property of this region was due to any
extent to some abnormality of the region at the time the tissue was
obtained, or whether it was induced by some irrcgularity in the technique
prerious to the staining, is not so absolutely certain. The technique is
supposed to have been the same throughout for this region as for the
other regions. Including this preparation, it may be said concerning
the variations in staining that the goblet cells stain faintest in the
c;ecuiii, medium to faint in the ascending colon, heaviest of all in the
preparation of the transverse colon separately stained, dark in the
descending colon, and medium in the rectum. It is realized that variations in the mucous reaction map be explained as due to chemical differences of the stages in the cycle of iiiucous production in which the
cells are caught a t the time of fixation.
R v ~ ~ l A R s .
Comparative measurements of the contracted and distended large
intestine of the dog show that variations occur in the intestinal wall
and glands of the different regions, and that variations in those of the
same region are produced by distension. Thesc variations, observed
in the dog, are found to be true in the human intestine in the eases in
which contracted and distended sections of the same region of the same
intestine were available for this study.
1. The entire intestinal wall varies in thickness inversely with distension, most in the transverse colon and least in the rectum. It is
obvious that, i n the normal condition, the wall of the different regions
varies in thickness.
2. The depth and cross section of the glands in the different regions
vary inversely as the distension. The interglandular space varies
directly as the distension. These variations are least in the ascending
colon and greatest in the transverse colon. While they occur under the
142
The Anatomical Record.
conditions of both contraction and distension, they also occur normally
in the different regions, the longest, narrowest and most thickly distributed glands being in the ascending colon, and the shortest, thickest
and most thinly distributed in the rectum, the contracted cwum not
having been available for use in the comparison.
3. The resultant of the forces acting on the gland in distension is in
the direction of the lumen of the viscus, tending to pull the gland out,
and thus to decrease its depth and increase the actual area of glandular
surface exposed in the lumen of the intestine.
4. The greater epithelial surface thus exposed in distension is applied
directly to the intestinal contents, and therefore the area directly utilized for absorption and directly stimulated to secretion is increased in
the distended condition.
5. The number of goblet cells per gland varies in the different regions,
being greatest in the rectum and least in the transverse colon.
6. The chemical properties or stages in mucous production of the
glands vary in the different regions, indicated by the variations in
staining qualities under similar conditions.
I n conclusion, I wish to express my acknowledgment to Professor
Hardesty, at whose suggestion and with whose guidance and advice this
investigation was undertaken.
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