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Grosser O. Lewis FT. and McMurrich JP. The Development of the Digestive Tract and of the Organs of Respiration. (1912) chapter 17, vol. 2, in Keibel F. and Mall FP. Manual of Human Embryology II. (1912) J. B. Lippincott Company, Philadelphia.

XVII. The Development of the Digestive Tract and of the Organs of Respiration: Introduction | Early Entodermal Tract | Mouth and Its Organs | Oesophagus | Stomach | Small Intestine | Large Intestine | Literature | Liver | Pancreas | Pharynx and its Derivatives | Respiratory Apparatus | Figures | Literature
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Intestine Development

The Development of the Large Intestine

Frederick Thomas Lewis
Frederick Thomas Lewis (1875-1951)

By Frederick T. Lewis


Early Development

In a 10 mm. embryo the large intestine consists of an epithelial tube, an undifferentiated layer of mesenchyma, and, except along the mesenteric attachment and near the pelvic termination, a layer of peritoneal epithelium. The entodermal epithelium shows nsnally two rows of nuclei. Mitotic figures are limited to the row next the lumen. The lumen is circular, and, though minute in places, it is continuous throughout. There is a marked local dilatation of the lumen in the region of the caecum, and a gradual enlargement downward in the rectal portion. The diameter of the colon is about equal to that of the lower portion of the small intestine, but it is less than that of the duodenum, the epithelium of which has begun to proliferate.


At 14.5 and 16 mm. the large intestine is still a round tube with a well-defined lumen, gradually enlarging from the colon toward the cloaca. At 22.8 mm. the lumen of the lower part of the rectum has become elliptical and the long axis is transverse. Passing upward the lumen gradually becomes circular. Near the caecum the inner surface of the epithelium shows some irregularities due to the varying height of the cells. Here, in cross section, the lumen is stellate or polygonal, but the circumference of the epithelium is circular. Patzelt (1883) has described the same condition in cat embryos of 25 and 33 mm.


In a 37 mm. embryo the lumen of the greater part of the ascending colon is pentagonal, but the circumference is circular. Toward the right (or hepatic) flexure the lumen becomes round, and so continues into the descending colon. Then it assumes a three-lobed form (in places four-lobed), but the circumference still remains nearly circular. After reaching the part of the rectum with a long transverse axis, the lumen shows additional lobes and the circumference becomes indented. Thus, in cross section, the lower part of the rectum shows five or six folds.


The transverse colon at 42 mm. is shown in Fig. 286, A. The cells at the bottom of the three outpocketings are lower than the others, and show a characteristic pearl or bud-like arrangement, suggesting the diverticula of the small intestine. They do not produce local pockets, however, but elongated ridges. Toward the rectum the epithelial irregularities are more marked. They are shown in longitudinal section in Fig. 286, B and in cross section in Fig. 286, C. Between the sheaf-like bundles of tall cells with superficial nuclei, there are concentric groups of short ones with basal nuclei. The latter appear to be growing outward, and by the shortening of the intervening cells the epithelium becomes folded. Thus in C there are three folds, but the places where two others will arise are clearly indicated, and lower down in the rectum five or six folds are found.


File:Keibel Mall 2 286.jpg

Fig. 286. — The epithelium of the large intestine in a 42 mm. embryo (Harvard Collection, Series 838). X[130 diam. A, cross section of the transverse colon. B, longitudinal section of the sigmoid colon. C, cross section through the upper part of the rectum.


There is no solid stage in the development of the large intestine. The atresia described by Kreuter (1905) at the beginning of the fifth week has not been found by Forssner (1907). There are no diverticula. Small vacuoles are found at 37 mm. in connection with the nests of low cells, and similar vacuoles have been observed in the stomach, but these are never conspicuous as in the oesophagus. The expansion of the epithelial tube occurs slowly, so that at 37 and 42 mm. the large intestine is very much smaller than the adjacent coils of the jejunum and ileum, in which villi are conspicuously present.


Villi and Glands

With the continued growth of the large intestine the out-pocketings bifurcate, and, as seen in cross sections, the number of elevations projecting toward the lumen increases. In a section of the transverse colon at 55 mm. there are five or six projections; at 73 mm. there are about ten; and at 99 mm. as many as twenty. A model of the transverse colon at 99 mm. shows that these elevations are true villi (Fig. 287). At their bases there are irregular epithelial clefts and pockets which give rise to the glands. The glands continue to grow downward, and they multiply through bifurcation. The cells at the bottom of the depressions are granular and dark, but the villi are covered with clear elongated cells, apparently containing mucus. Patzelt found occasional goblet-cells in a 75 mm. embryo, and he notes that the cuticular border is distinct. The relation between the dark cells below and the clear cells above is similar to that seen in the stomach and small intestine.

File:Keibel Mall 2 287.jpg

Fig. 287. — Model showing the villi of the transverse colon in an embryo of 99 mm. X 120 diam. (After F. P. Johnson.)


Meckel in 1817 described the villi of the large intestine at 3 months as much lower than those of the small intestine, but quite as numerous. In the fourth month he found that they are not only considerably smaller, but less club-shaped and more scattered. By the eighth month the villi have gradually given place to very low, slightly indented longitudinal folds, which produce irregularities on the inner surface of the intestine. Kolliker (1861) stated that at the fifth month the villi begin to fuse from their bases upward, around the gland outlets, and that this process is completed in the seventh month. Brand (1877) described the development of septa between the villi, beginning below and extending upward, transforming the spaces between the villi into prolongations of the glands. At the sixth month the tips of the villi are reached by the septa. Patzelt (1883) states that he can confirm the observations of Kolliker and Brand regarding the disappearanee of the villi. But Hilton (1902) has found that the villi shorten and disappear as the intestine enlarges, without forming outer portions of the glands. This accords with Meckel's original description and is apparently correct. The gradual disappearance, whereby the villi become slight elevations, probably accounts for the discrepancy in determining the time of their extinction (Meckel, during the eighth month; Kolliker, in the seventh month; Brand, at the sixth month). Even at 240 mm. the villi are quite low.


The Outer Layers

In embryos of 14.5 and 16 mm. the mesenchyma of the large intestine contains branches of the inferior mesenteric vessels. The circular muscle layer, which is present at this stage in the ileum, is still absent from the large intestine. It appears first in the rectal region and spreads upward. Thus at 22.8 mm. it is present only in the lower part of the large intestine, where it is in relation with branches of the pelvic sympathetic ganglia. At -42 mm. it is found throughout the colon. The longitudinal layer appears as a crescentic condensation along the mesenteric attachment of the transverse colon at 75 mm. In the transverse colon at 99 mm. the mesenteric taenia is still the most prominent part of the longitudinal muscle, but the other two taeniae are indicated. There is probably a thin layer of longitudinal muscle in the intervals between the taeniae. In the rectum at this stage the longitudinal layer is well defined. At 187 mm. the muscularis mucosae, is distinct in the rectum, but is apparently absent from the transverse colon. It is present there at 240 mm.


Lymphatic vessels are abundant along the mesenteric attachment of the rectum in early stages (37 mm.). At 120 mm. the lymphatic vessels in this region have extended into the submucosa, and lymph-glands are developing outside of the muscularis. At 187 mm. lymphoid tissue is present in the propria of the rectum, forming nodules and extending into the submucosa. Baginsky found developing nodules in the submucosa of the colon at 4 months. At birth the nodules are abundant.


The transverse folds of the rectum are seen in longitudinal sections at 120 mm. The haustra or sacculations of the colon, according to Meckel, are not present until the end of the fifth month and they first appear in the transverse colon. In this region they are distinct at 240 mm. Corresponding with the external indentation, which bounds the sacculation, there is a prominent internal fold of the mucosa. The appendices epiploiccc were found by Baginsky at 4 months. Meckel had said that they are distinct in the fifth month, although they contain quite as little fat as the omentum.


The Vermiform Process

At 16 mm. the vermiform process is an epithelial tube surrounded by undifferentiated mesenchyma. Its lumen is clear-cut and round. At 55 mm. the liunen has become lobed, resembling that of the colon in earlier stages. The circular muscle is present as a well-defined layer, but the longitudinal muscle has not yet appeared. At 120 mm. (about 4 months) villi are present, and between them there are bifurcating glands or pits. Brand (1877) found only villi at 3>< months, but at ± l / 2 months the glands had appeared. Some of them showed "lateral outpocketings" which Brand thought were perhaps concerned with the later increase in the number of glands. At 120 mm. the tunica propria, because of its crowded nuclei, is quite distinct from the underlying submucosa, and the contrast between them is greater than in the adjacent colon. At 140 mm. Stohr (1898) found small "groups of leucocytes" close beside blood-vessels, not only in the deep connective-tissue layer, but also within the villi. In the tunica propria they form compact masses of cells which are the beginnings of the nodules. At this early stage scattered leucocytes wander into the epithelium which covers the tips of the villi.


In the fifth month (170 mm.?) Stohr has found that the muscularis mucosa is indicated in the caecum but is absent from the vermiform process. Villi are still present. The glands of the vermiform process vary greatly in diameter and length, and some of them extend almost to the circular muscle. At this stage Stohr has described a degeneration of some of the glands, beginning with a characteristic thickening of the connective tissue which surrounds them. The goblet-cells at the neck of a degenerating gland first become flattened, and then give place to a solid epithelial strand. Later the strand ruptures, and the detached basal portion, after becoming cystic, undergoes involution. The last remnants of such a gland are small groups of epithelial cells, surrounded by thick connective-tissue capsules. Stohr finds that degenerating glands are relatively less numerous at six months, and he infers that the degeneration may be limited to embryonic stages.


At 240 mm. both the muscularis mucosae and the longitudinal muscle layer are present. The glands are branched and some of them are long enough to cause a local bulging of the muscularis mucosae. Occasionally they appear to penetrate it. In this specimen detached glands were not found. The propria contains diffuse lymphoid tissue and five nodules, of which the two most highly developed are near the distal end of the vermiform process.


At birth the glands are still branched. The number of lymphnodules has increased, and five were seen in a single longitudinal section of the distal third of a vermiform process 35 mm. long. Berry and Lock (1906) have stated that the lymph-nodules increase rapidly after birth, but these authors are in error in denying the presence of lymph-nodules at term.

Anomalies of the Large Intestine

It is generally agreed that the sigmoid colon is relatively long and freely movable at birth.

Bourcart (1863) has determined its course and form in 150 cases. Frequently in the adult the sigmoid colon is excessively long, forming two or three very large coils. According to Frommer (1902), Curschmann found an elongated colon in 15 of the 233 bodies which he examined, and he regarded it as a persistence of the infantile condition. Concetti (1899) recognizes three types of congenital cases, which cause habitual constipation : 1, those with simple elongation of the descending and sigmoid colon; 2, cases in which, in addition to the elongation, the colon is dilated and its walls hypertrophied ; 3, cases in which there is local dilatation of the lowest part of the colon, above which there is apt to be a region of compensatory hypertrophy. In the third group Concetti describes a case at 2 1-2 years, in which the longitudinal muscle was completely absent from the portion of the colon just above the rectum, and the transverse muscle was thinner than the muscularis mucosa?. The embryological factors which control the length of the colon are unknown.


Stenosis and atresia are less frequent in the colon than in the small intestine, but they present the same forms. They occur both as membranes and as complete interruptions of the intestinal tube, with blind ends more or less widely separated (Forssner, 1907). In the large intestine of the embryo there is ordinarily no occlusion such as occurs in the duodenum, and these cases are essentially abnormal. The same is true of the doubling of the cascum and colon described by Lockwood (1882).


Diverticula of the colon are frequent, but apparently they are acquired late in life. Hansemann (1896) finds that they are not limited to the mesenteric attachments, but may occur on the convex side of the intestine, sometimes projecting into the appendices epiploicse. Unlike the false diverticula of the small intestine with which they are sometimes associated, he states that the outpocketings of the colon often push the atrophic muscle before them and are "true dilatation diverticula." Hedinger (1904) has described a case of congenital diverticula of the vermiform process. In the distal third of the vermiform process of a new-born child there were numerous outpocketings, which either only reached the muscularis or extended nearly through it so as to produce an uneven serous surface. Hedinger considers that in his case alone, the congenital origin of a diverticulum of the digestive tube has been established.


Contents of the Intestine

When the glands of the digestive tract begin to secrete, their secretions together with desquamated and disintegrating entodermal cells are found in the intestinal tube. These become mixed with amniotic fluid, containing lanugo hairs and fatty material from the vernix caseosa, which has been swallowed. In early stages the fluid is yellowish in color, and at birth it is still light colored in the upper part of the intestine. Toward the rectum it gradually becomes dark brown or dark green, and is known as meconium (a Greek term for the juice of the poppy and for sepia). The color is due to bile pigments. Schenk (1896) states that in embryos of four months the meconium appears as a bright yellow or pale greenish fluid, and that it tills the entire large intestine in embryos of five months. In later stages it becomes dark brown. But, according to Tourneux ( 1909) . it does not pass the valve of the colon in embryos of five and months; it is only from the seventh to the ninth month that it passes into the large intestine, where it Incomes greenish brown. Bacteria are absent and there is no gas in the embryonic intestine.


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Grosser O. Lewis FT. and McMurrich JP. The Development of the Digestive Tract and of the Organs of Respiration. (1912) chapter 17, vol. 2, in Keibel F. and Mall FP. Manual of Human Embryology II. (1912) J. B. Lippincott Company, Philadelphia.

XVII. The Development of the Digestive Tract and of the Organs of Respiration: Introduction | Early Entodermal Tract | Mouth and Its Organs | Oesophagus | Stomach | Small Intestine | Large Intestine | Literature | Liver | Pancreas | Pharynx and its Derivatives | Respiratory Apparatus | Figures | Literature
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   Manual of Human Embryology II 1912: Nervous System | Chromaffin Organs and Suprarenal Bodies | Sense-Organs | Digestive Tract and Respiration | Vascular System | Urinogenital Organs | Figures 2 | Manual of Human Embryology 1 | Figures 1 | Manual of Human Embryology 2 | Figures 2 | Franz Keibel | Franklin Mall | Embryology History