Book - Contributions to Embryology Carnegie Institution No.50

ONTRIBUTIONS TO EMBRYOLOGY, No. 50.

STUDIES ON THE LONGITUDINAL MUSCLE OF THE HUMAN COLON, WITH SPECIAL REFERENCE TO THE DEVELOPMENT OF THE TAENIAE.

By Paul E. Lineback,

School of Medicine, Emory University, Georgia.

Eight text-figures.

The presence and arrangement of taeniae in the colon of some domestic animals, as well as of man, are striking and distinctive. The relationship between these bands and nutritional habits (i. e., kind of food eaten, manner in which it is taken and utilized, and type of feces discharged) attracts more than passing notice. For example, the horse and the cow eat the same kind of food; presuming that it goes into the caecum in the same state in both animals, the horse passes it through a colon having four taeniae, while the cow passes it through a colon having none, and the type of feces discharged by one is entirely different from that discharged by the other. Man and pig are omnivorous animals, having a broader range of food supply than any other types. Both will take and utilize animal and vegetable food, cooked or raw, and the types of feces are very similar; but the structure of the colon and the arrangement of the taeniae are quite different in the two species. The pig is supplied with only two bands in a long, double, spiral colon, whereas in man there are three bands in a rather simple loop of large bowel.

A further study of this relationship between the taeniae and the nature of the bowel-content might be carried on with interest. Especially would the physiological aspect of both the taeniae and the sacculations bear further investigation. But back of these peculiar phenomena with their physiological aspects is the problem of the production of taeniae, their origin, development, and nature. Since the human colon as a whole is more simple and primitive, ontogenetically, than the colon of domestic animals, a study of the taeniae here would seem to offer fewer difficulties and promise some definite results. At a meeting of the Anatomical Association in New Haven (1915), and again in New York (1916), I gave reports of work done on the colon and taeniae of the pig; and in 1916 I published in the American Journal of Anatomy (vol. 20, p. 483) an article on the development of the pig's colon. This paper is a report of further studies based upon these subjects, together with work done on the human colon.

Literature

The literature does not offer much in the way of setting forth the origin and development of the taeniae. Such references as are found, with a few exceptions, are mainly only a mention of the bands when the wall of the colon is discussed. Thus they are cited by Meckel (1817), Kolliker (1854), Barth (1866), and Brand (1877); but in 1882 Baginsky made a brief statement concerning them which has a definite embryological bearing. In Archivfur palhologische Analomie (vol. 89, p. 90) he wrote:

"Wahrend die aussere Muskelschicht nur eine diinne Lage darbietet, die an 3 Stellen einer dichten Anhaufung von Muskelfasern Platz macht. So ist schon deutlich die Anlage der Tanien des Colon markirt."

Following this, other citations are found, but only of a general nature, such as those made by Oppel (1897), Maurer (1902), Ellenberger and Baum (1909), and Nagy (1911-12). Then Broman (1911) gave a more detailed account of the growth of the taeniae. His statement is longer than Baginsky's and bears the added feature of setting forth the human taenia?, while. Baginsky dealt only with the lower animals. Broman's account in his Handbook (p. 352) is as follows:

"Bis zur Geburt bleibt gewohnlich auch im Colon die Langsmuskelschicht ringsum kontinuierlich. Bei der im extrauterinen Leben folgenden starkeren Ausdehnung des Colon wird aber diese Muskelschicht in drei parallelen Muskelbiindeln zersplittert, die durch immer grosser werdende Zwischenraume von einander getrennt werden. Die werdende Lage dieser Langsmuskelbtindel wird schon im vierten Embryonalmonat durch gef iisshalt ige Mesenchymverdickungen markiei t. ' '

More recent citations are made by F. T. Lewis (1912), F. P. Johnson (1913), and Sisson (1914). Sisson dealt with the taeniae in domestic animals only, and Johnson merely referred to them in his study of the mucosa of the human intestine. Lewis, however, has set forth their appearance very definitely. His account is found in Human Embryologij (Keibel and Mall, vol. 2, p. 396), in which he states:

"At 42 mm. it (the circular muscle) 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 tamiee are indicated. There is probably a thin layer of longitudinal muscle in the intervals between the teenise."

Materials and Methods

This study was confined essentially to the human colon and the results are applicable chiefly to this type. But in order to study as closely as possible some of the minute changes and variations attending early growth, especially the appearance of the longitudinal fibers, embryos of different animals were utilized. The most useful of these was found to be the pig, since an abundance of this material was at hand, and it was thus possible to collect a closely graded series and to vary its preparation. The best staining results were obtained by using Mallory's phosphomolybdic-acid preparation, which differentiated the muscle fibers with a good degree of definiteness. Human fetuses of the following stages of development were studied: 33 mm., 40 mm., 50 mm., 70 mm., 90 mm., 105 mm., 110 mm., 120 mm., 125 mm., 145 mm., 160 mm., 180 mm., 185 mm., 190 mm., 200 mm., and new-born. Several of the smallest were prepared whole, and from the others the colon was carefully removed and two sections, 6 and 8 mm. long respectively, were taken from the two ends (caecal and rectal). Three sections were taken from the older specimens, one each from the ascending, transverse, and descending portions. All were sectioned serially and stained by the Mallory method. In addition, the following series from the collection at the Carnegie Laboratory of Embryology, Baltimore, was also carefully studied, and these specimens will be referred to herein as C. C. (Carnegie Collection).

The entire collection was placed at my disposal through the generosity of Professor Streeter, and I wish at this time to express my sincerest gratitude to him for this great kindness. I wish also to express my indebtedness to Professor F. T. Lewis and Professor R. R. Bensley for encouragement and material aid, and to recall the delightful associations of their laboratories.

Home experimentation was done on the caecum of the guinea-pig, as this is a relatively large structure with an especially well-developed group of taenia?. A number of skiagrams were examined and a few fluoroscopic inspections were made of the human colon in the living state.

No.

mm.

No.

linn.

No.

mm.

782

26

135s

32

362

39

11!!!!

26

-111

35

886

43

756

27

15(11

36

96

50

75

30

1318

37

538

50

86

30

922

37

448

52

145

32

1101

37

Discussion

The production of taeniae may be divided into two phases, each dependent upon separate factors and attended by different phenomena: an early growth phase, characterized by the appearance of the bands and their growth up to a fixed state, and a functional phase, wherein the taeniae are accentuated and become especially distinct through the functioning of the sacculations.

The growth phase may be introduced by a brief consideration of the circular muscle. The study of a closely graded series of embryos reveals the circular muscle appearing much earlier than the longitudinal. This is true in the small intestine as well as in the large. It is also found that the muscle is first seen in the caudal end of the intestine, and that it can subsequently be traced throughout the entire length of the latter. Lewis states that " at 42 mm. it is found throughout the colon," with which my findings agree, although I should conclude that it reaches that state of completeness somewhat earlier. Fetus No. 75 C. C, 30 mm. (fig. 1), shows it only in the pelvic portion of the intestine; while in a 35-mm. specimen, No. 210 C. C, it can be seen throughout the entire length of the intestine. Evidently, its growth is upward from the caudal end of the tube and is quite rapid. These items are significant, in that they show that in its manner of growth the circular muscle exactly precedes the longitudinal, both in time of appearance and time of completion.

The zone just outside of the circular muscle is occupied by the myenteric plexus, capillaries, and embryonic cells. The plexus occupies almost the entire zone and is contained in rather poorly defined rounded and oval compartments, which become very distinct by the 50-mm. stage. It is on the outside of these, and in the angles between them, that the longitudinal muscle-fibers will make their appearance. In the younger stages, just following the formation of the circular muscle, these aggregations of nerves may be wrongly interpreted as the cut ends of the longitudinal fibers; but proper staining and careful study will reveal their true identity.

Fig. 1. — Sagittal section of a human embryo 30 mm. C R. length (No. 75, Carnegie Collection), showing the circular muscle-fibers in the pelvic portion of the colon. No longitudinal fibers are present.

The investigation proceeded with the aim of noting the first muscle-fibers which could be unquestionably identified as such, and these were not found earlier than the 40-mm. stage. In a fetus of this size they are seen in the lower end of the intestine. In the extreme caudal end, near the anal canal, a complete layer, quite thin but well defined, completely surrounds the tube. Johnson has shown how they intermingle with the internal sphincter and levator ani muscles in older fetuses, a condition which is seen as early as this 40-mm. stage. A 46-mm. fetus, No. 95 C. C. (fig. 2), shows the whole muscle grown a little farther upward and its dorsal fibers

Fig. 2. — Sagittal section of a human fetus 46 mm. CR. length (No. 95, Carnegie Collection), showing the presence of longitudinal musclefibers (the circular muscle is not drawn). The ventral portion of the muscle extends only as far as the pelvic cavity, while the dorsal fibers extend well into the abdominal region.

extending well into the sigmoid region; no well-defined fibers can be detected in any of the regions higher up. In a 50-mm. fetus there is a distinct layer at the mesenteric attachment, the continuation of the dorsal fibers of the 46-mm. stage. The layer is well defined and extends throughout the length of the colon. Lewis noted this muscle and stated that in a 75-mm. fetus it was seen along the transverse colon, although he made no mention of it in other parts of the bowel.

Thus it is seen that the longitudinal fibers, as well as the circular, have their origin in the extreme caudal end of the intestine and grow rapidly upward toward the CEecal end. In the pelvis the muscle forms a continuous layer surrounding the tube, but as the more open region of the sigmoid is reached it extends only along the line of the mesentery attachment. Here it lies just over the plexus of nerves in a crescentic shape with its horns directed laterally. The remainder of the circle outside of the plexus is a zone of quite uniform thickness, where there are found cells generally of an indefinite type; some are fibrous and resemble the cut ends of the longitudinal muscle, but do not react as such to the Mallory stain. In a 52-mm.

fetus, No. 448 C. C. (figs. 3 and 4), this remaining portion is occupied by definitely formed muscle-fibers which are, however, loosely scattered in the zone, whereas those at the mesenteric arc are compact. This may cause the erroneous conclusion that the mesenteric arc is the only part of the muscle present at this stage, but a careful search reveals the scattered fibers as just mentioned. This state of the muscle continues unaltered for some time, no marked changes being noted until near the 90-mm. stage. At this time the entire circle of fibers becomes compact, with the mesenteric portion still prominent (fig. 5). This harmonizes with what Lewis stated concerning the arc, and also with Broman's statement about a continuous layer.

Fig. 3. — Sagittal section of a human fetus 52 mm. CR. length (No. 448, Carnegie Collection), showing both dorsal and ventral portions of the muscle extending into the abdominal region.

The important development up to the 90-mm. stage is the appearance of the longitudinal muscle in the rectum, where it is a complete layer entirely surrounding the tube. By rapid growth it extends to the caecal end, first along the fine of the mesenteric attachment, then (closely following this) the rest of the circle becomes occupied by muscle-fibers which are at first loosely scattered but soon become condensed into a well-defined layer. The condition in the pig is quite similar with the exception of a few minor differences. Shortly after the muscle appears in the pelvis it is also seen in the csecal end with apparently no muscle in the bowel between these regions. Growth then proceeds from both ends and, as in the human intestine, the muscle rapidly fills the entire length of the colon. Another peculiarity is that the two bands in the pig's colon have a striking position. Although the mesenteric arc is the first part of the muscle to develop, it does not grow into a taenia; but when the muscle entirely surrounds the tube, as in the human colon, two lateral thickenings appear, one on each side of the bowel equidistant from the mesentery, which become true taeniae (fig. 7). In the caecum, however, which is much longer than in man, a third taenia is present. It extends from the ilio-caecal junction to the tip of the caecum along the line of the meso-caecal attachment, corre-sponding to the mesenteric tseniae in man. The other two taeniae continue their lateral position also to the tip of the caecum.

The problem of the taeniae has been thus far suggested only by way of citing the mesenteric thickening and its relationship to the rest of the muscle. Lewis referred to this as the mesenteric lamia and stated that "at 99 mm. it is still the most prominent part of the longitudinal muscle"; and further, that "the other two taeniae are indicated." Broman stated that in the fourth month the primordia of the longitudinal muscle bundles are marked. One feels that both of these statements are incomplete, since one does not make it clear where or by what the taenia) arc indicated, and the other (that they are marked by "mesenchymal thickenings") is wide of the point, Thickenings are found scattered along at irregular intervals; these, upon cross-section, might be taken to indicate the developing taenia-, but they do not involve the muscle in any way. Indeed, when the taeniae appear they are quite distinct from these thickenings, which in reality are caused by large bloodvessels (fig. 5).

Fig 4 —Cross-section of the colon of a human fetus 52 mm. CR. length, showing a well-defined tenia at the mesenteric arc. with a complete layer of loosely scattered fibers surrounding the tube.

Fig 5 -Cross-section of a human fetus 90 mm. CR. length, showing the fibers of the longitudinal muscle, loosely scattered in the 52-mm. stage, now compact, and only the mesenteric taenia present. Two enlargements are seen, one on each side of the tube, caused by the presence of blood-vessels. It will be noted that the muscle here is in no way involved.

At about 100 mm. there appear at two places in the muscle an accumulation of fibers which cause a marked thickening in the layer (fig. 6). These masses are crescentic in shape, resembling the mesenteric thickening, are located about equidistant from it and from each other, and extend the whole length of the bowel. They are accumulations of muscle-fibers within the layer at these two places and continue to enlarge until the 105-mm. stage, when they are distinctly formed and fixed in their triangular position. When traced for some distance along the bowel they are seen to vary in size and shape; at places they are broad and flat or narrow and thick, but are not effaced by subsequent growth in the general intestinal wall. They are actually permanent accumulations of muscle-fibers and not temporary migrations of fibers from the adjacent interspaces, since these spaces are entirely unaffected by them. This is somewhat at variance with Broman, who speaks of a splitting of the muscle by dilatation of the intestine which produces the three parallel bands. One may only conjecture what he considers produces the dilatation. That it is a filling of the intestine with meconium is a reasonable deduction, but the formation of the taeniae could hardly be explained on this basis. Meconium accumulates first in the rectum. In a 125-mm. fetus it fills the tube to distension only as far as the beginning of the sigmoid, but the taeniae are distinctly formed as early as the 105-mm. stage and in a region where no trace of meconium is found. Furthermore, in this rectal region, where there is marked distension with distinct taeniae, the interspaces are unbroken. In the new-born, distension with meconium may be found as high up as the caecal region, but the ring of longitudinal fibers remains unbroken ; hence a splitting process can hardly be considered. From his statement that "there is probably a thin layer of longitudinal muscle in the interval between the taeniae," it may be concluded that Lewis holds that the taeniae are present first, and that later the interspaces are filled in by extension from the edges of adjacent bands; but from a careful study of young series up to the 100-mm. stage I am led to believe that the muscle is first present as a continuous layer, probably having grown laterally from the horns of the mesenteric crescent — the first band — and that the other two taeniae develop within the layer as aggregations of muscle-fibers.

Fig. 6. — Cross-section of the ascending colon of a human fetus 105 mm. CR. length, showing the three tseniaj in a triangular position in the wall. Note their broad, flat shape and the presence of longitudinal fibers in the intervals.

Fig. 7. — Cross-section of a 200-mm. pig fetus, showing lateral position of the two teniae. Note blood-vessels passing just beneath the peritoneal layer to the vicinity of the bands.

The development thus far attained is fundamental, remaining unchanged in its essential features throughout subsequent variations in size, shape, and relationship of the colon. Changes may be noted in its form, as when contractions of the circular muscle produce saccules, or in its position and relationship, as when markedly filled by meconium; but the bands never lose their identity, nor do the intervals become entirely obliterated. In a region of the bowel where there is marked distension and the wall is smoothed out the taeniae remain distinct, and over the domes of the saccules there may be found a very thin layer of longitudinal fibers. It is generally stated that the taeniae become confluent in the lower end of the bowel, but cross-sections show that the three bands are still present as thickenings in the wall, distinctly separated from each other, although sacculations are absent.

The second phase of taeniae formation is ushered in by a factor which begins about the 150-mm. stage — i.e., the appearance of sacculations, the effect of which upon the taeniae is significant. Their formation and effect were studied experimentally in the guinea-pig; investigations were also made of skiagrams of the human colon and a few direct inspections in fife, through the fluoroscope. By these methods it was directly observed that the pouches are produced by the sharp contraction of narrow groups of circular muscle-fibers extending between adjacent taeniae. Apparently the circular muscle is more or less firmly attached by inter-muscular connective tissue to the longitudinal bands, which fact permits it to contract segmentally. The fluoroscopic inspections and the experiments on the caecum of the guinea-pigshowed waves of contraction passing down the bowel in three rows, between the three taeniae, which constantly changed its surface contour from a series of saccules to a series of clefts. The degree of contraction varied from a slight indentation of the saccule to its entire obliteration.

A marked feature noted was that the contraction waves were independent of each other; only rarely were two groups of fibers on opposite sides of taeniae in contraction at the same time. Most commonly a contracting segment was opposed by a saccule; thus the three rows of saccules are also independent of each other (fig. 8) . The saccules are in no way related to the bowel-content, as evidenced by the fact that they appear as early as the 150-mm. stage in a region of the colon where there is no meconium, and that where meconium is causing the distension the saccules are absent. For the production of both taenia' and saccules it is evidently necessary to seek further than meconium distension or stimulation caused by it. A basis for such a study might be found in the peculiar position of the pig's taeniae and their relationship to the mesenteric structures, nerves, blood-vessels, and lymphatics.

Recalling the position of the two taeniae, one on each side of the bowel with none at the mesenteric attachment, it is interesting to note that, instead of the mesenteric structures entering the intestinal wall at the mesenteric line, the majority of them

-Semi-diagrammatic figure of colon of a new-born infant, showing alternate arrangement of saccules on opposite sides of a tsenia.

pass just beneath the serous layer, around to the vicinity of the bands, before penetrating deeper (fig. 7). Usually, on the mesenteric side of each taenia and very close to it, there can be seen numerous branches of the nerves and blood-vessels passing in and out. If the proposition of an active growth for the production of taenia? be tenable, then, instead of a passive adjustment by a splitting process, it is essential to look for some causative factor back of this growth. The breaking up of mesenteric vessels into capillary plexuses in the region where the bands will later develop is fundamental. Numerous instances of this phenomenon were noted, but such a line of investigation requires further and more careful attention.

The effect of these segmental contractions is to accentuate the taeniae, causing them to stand out in marked distinctness, especially when the contractions are most active (fig. 8) . Previous to the appearance of the contractions the taeniae are poorly outlined to the unaided eye, but by their action the bands become sharply defined. This condition is noted in the adult as well as in the fetus. There are portions of the adult colon, when directly examined, in which there seem to be no taeniae and the content of which appears to have no effect upon this state of the wall; but where contractions and saccules are in an active state the taeniae are marked.

In the consideration of this fundamental factor in taenia? production another aspect of the bands proper presents itself — that of an added function. In addition to holding the colon in position and shortening it, the bands functionate as fixed and firm longitudinal cables between which the circular muscle-fibers are stretched and against which they may pull in segmental contraction. When one considers the more solid content of the colon, with its retarded progress and the necessity of more force in moving it, some such adjustment for only partial circular-muscle contraction would seem logical. This can be accomplished only by the development of strong, fixed, longitudinal bands, against which the segments of the circular muscle may pull. By such an adjustmentt here are three rows of counteracting segments which, working alternately, tend to gradually move the massive content along without violence to the wall.

Summary

An attempt has been made to give a more detailed account of the appearance, development, and nature of the taeniae than is found in the literature. In so doing a few features are noted in addition to and at variance with accounts already given.

1. The longitudinal muscle begins its growth in the caudal end of the intestine and rapidly extends to the caecal end; first, as a layer at the mesenteric attachment, followed shortly by the whole circle of the tube becoming incased in a complete layer of longitudinal muscle-fibers before taeniae are formed.

2. The mesenteric thickening becomes the first taenia, and the other two are developed in the already existing layer of muscle.

3. The production of taeniae, especially of the adult state, is due to an added factor, the segmental contraction of the circular muscle between the bands. These contractions are in turn dependent upon the taeniae, which functionate as cables against which the circular muscle may pull.

4. The whole aspect of taeniae production is based on active growth and functional factors rather than being the passive results of foreign elements.

44

STUDIES ON THE LONGITUDINAL MUSCLE OF THE HUMAN COLON.

Bibliography

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Maitrer, F., 1902. Die Entwickelung des Darmsystems. Hertwig's Handbuch der vergl. u. exp. Entwickelungslehr, Bd. 2, Teil 1, p. 109-252.

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v. Nazy, Ladislaus, 1912. Ueber die Histogenese des Darmkanals bei menschliehen Embryonen. Anat. Anz., vol. 40, p. 147-156.

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Sisson, Septimus, 1914. The anatomy of domestic animals: 2nd ed., Philadelphia.