Paper - Studies of the intestine and peritoneum in the human foetus - part 2

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Reid DG. Studies of the Intestine and Peritoneum in the Human Foetus: Part II. (1911) 45(4):406-15. PMID 17232897

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This 1913 paper is the second in this historical series describing human fetal intestine development. Note many of the terms introduced in this paper are historic terminology, no longer applied to describing the intestinal anatomy and some intestinal developmental concepts have been reviewed since this early series.

Other papers in this 6 part series by Douglas Reid:

  1. Reid DG. Studies of the Intestine and Peritoneum in the Human Foetus: Part I. (1911) J Anat Physiol. 45(2): 73-84. PMID 17232876
  2. Reid DG. Studies of the Intestine and Peritoneum in the Human Foetus: Part II. (1911) 45(4):406-15. PMID 17232897
  3. Reid DG. Studies of the Intestine and Peritoneum in the Human Foetus: Part III. (1912) 46(4):400-415. PMID17232936
  4. Reid DG. Studies of the Intestine and Peritoneum in the Human Foetus: Part IV. (1913) J Anat Physiol. 47(3): 255-267. PMID 17232956
  5. Reid DG. Studies of the Intestine and Peritoneum in the Human Foetus: Part V. (1913) J Anat Physiol. 47(3): 268-281. PMID 17232957
  6. Reid DG. Studies of the intestine and peritoneum in the human foetus: Part VI. (1913) J Anat Physiol. 47(4): 486-509. PMID 17232976

See also the historic paper Frazer JE. and Robbins RH. On the factors concerned in causing rotation of the intestine in man. (1915) J Anat Physiol. 50(1): 75-110. PMID 17233053
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Studies Of The Intestine And Peritoneum In The Human Foetus

By Douglas G. Reid, M.B., Ch.B. Edin., B.A. Trin. Coll. Camb.,

Demonstrator of Anatomy in the University of Cambridge.

Part II. The Root-Folds of Peritoneum

In a full-term foetus, in which the peritoneum of the intestinal loop has failed to adhere to the posterior abdominal wall, two distinct folds of peritoneum, which lie in line with one another, are seen projecting from the anterior aspect of the peritoneum of the loop. The left, and larger, of the folds contains the ileo-colic artery and vein ; and the right fold contains the anterior caecal vessels. The continuity of the free edges of the two folds is slightly interrupted at the point where the iliac branch of the ileo-colic artery leaves the right extremity of the left fold to enter the mesentery. But for this they would have formed a single fold extending from the middle line to the ileo-ceecal junction. In the younger foetuses (ranging from 12 to 22 cm. in vertex coccygeal length) these folds, which contain the blood-vessels just mentioned, are seen projecting from the peritoneum exactly along the line of attachment of the root of the mesentery. In the smallest foetus there is only a single fold (see fig. 1). This extends outwards from the middle line along the front of the third portion of the duodenum, and over the right kidney, to the ileo-caecal junction. Its free edge (except at the ileo—caecal junction) is directed upwards, and it forms, with the peritoneum of the posterior abdominal wall, a horizontal cleft more than 2 mm. deep.

In most cases there are two folds ( see fig. 2), each having its free edge directed downwards. Their direction varies with the position of the caecum. It is originally (in the smaller foetuses) transverse, but becomes more and more oblique‘ from above downwards as the caecum descends. The two folds may therefore be named the left or superior root-fold, and the right or-inferior root-fold. They bound in front fossae of variable depth——the left and right (superior ileo-ceecal) root-fossae.

It is at the place where the iliac branch leaves the left root-fold to enter definitely the substance of the mesentery (and to inosculate with the termination of the superior mesenteric artery) that the interruption occurs, in the continuity of the free edges of these folds. But sometimes the free edge of the left root-fold is continuous with that of the. right over the place where the iliac artery passes out of the left root—fold.

The right root-fold becomes relatively reduced in size and forms. the superior ileo-caecal fold (mesenterico-caecal fold of Jonnesco) of the adult.

Little has been said regarding the superior ileo-caecal fold in the foetus. Jonnescol has mentioned that the foetal superior ileo-caecal fossa is relatively large. But the facts, that the mesenterico-caecal fold lies along the right portion of the line of the root of the mesentery, and may be continuous with a similar fold extending from the middle line, and containing the ileo-colic artery and vein, have not previously been noted; indeed, the only fact mentioned regarding the vascular relations of the root of the foetal mesentery is that the peritoneum of the intestinal loop becomes soldered down along a line which corresponds to the trunk of the superior mesenteric artery (p. 920, vol. iV., Poirier’s Anatomy, 1905).

Fig. 1. Foetus No. II. Note the absence of the right omental process, and the single long rootfold which contains the ileo-colic vessels.

  • 1 J onnesco et J uvara, “Anatomic des ligaments dc Pappendice vermiculaire et de la fossette iléo-appendiculaire,” Le Progrés Médical, tome xix., p. 321.

In my specimens, the root of the mesentery is attached along the line of the root-folds and the ileo-colic vessels.

From the examination of the secondary changes in relation of the root of the mesentery to the root-folds and their blood-vessels, I have come to the conclusion that the fold, which I have named genito-mesenteric, in association with the elongation of the ascending colon, and the descent of the genital gland, assists in lowering the root of the mesentery. The reasons for this conclusion I have given in another paper.

Fig. 2. Foetus No VIII. Note the summit of the omega loop lies behind the left root-fold, and the retro-colic position of the appendix associated with the presence of the genito-mesenteric fold.

Thus, whilst the caecum is still high up in front of the right kidney, and the root-folds are still transverse, I have found more than once that, in association with the presence of the genito-mesenteric fold, the left half, or more of the root of the mesentery may have already acquired its adult direction. In other words, the root of the mesentery passes downwards and to the right from the duodenum towards the position which is occupied in the adult by the ileum and caecum at their junction. It reaches the genito-mesenteric fold, and then passes upwards and to the right towards the ileo-caecal junction. The root thus lies at the sides of a triangular area whose base is above at the root-folds, which have retained their primitive position, and whose apex is below at the genito-mesenteric fold. The mesentery has manifestly adhered over the triangular area. to the peritoneum of the posterior abdominal wall owing to the presence of the genitomesenteric fold.

The left root-fold is sometimes of relatively large size and may resist headward growth of the pelvic colon, whose form it may also help to modify. Thus the summit of the large primary omega loop of intra-abdominally placed pelvic, or iliac-pelvic, colon may ascend to the level of the root of the mesentery, and, since this is overlapped by the left root-fold, comes to lie behind this fold, although separated from actual contact with it by the mesentery (see fig. 2). Headward. growth of the loop at right angles to the left root-fossa is thus, even if we leave the liver out of account, effectively resisted. In the foetus, therefore, the pelvic colon (unlike that of the adult) is unable to extend upwards beyond the root of the mesentery. The colon continuing to grow, a depression of the summit of the loop is produced, resulting in the formation of a secondary M-shaped pelvic colon.

Lying in contact with the anterior surface of the root-folds are coils of small intestine. In one case the convex border of one of these coils is overlapped by the left root-fold.

These root-folds may be subdivisions of a single continuous root-fold, such as is present in the smallest foetus.

If the free edge of the fold which is present in this foetus had moved downwards through an arc convex forwards, we would have obtained the condition seen in other foetuses in which, although two distinct root-fossae are present, the two folds, whose free edges are directed downwards, are still continuous with one another.

Later (see fig. 2) the fold becomes separated into two at the point where the iliac branch leaves the fold.

Still later the left root-fold becomes obliterated, and the right relatively reduced in size.

But it is doubtful whether the blunt ridge such as is present in another foetus, 6'7 cm. long, and which contains the ileo—colic vessels and is continuous with the sharp-edged right root-fold, usually gives rise to a definite fold whose free, well—defined edge is continuous with the free edge of the right root-fold. But it may sometimes do so.

It is also doubtful "if at first the free edge of the left root-fold is normally directed upwards.

This direction may sometimes be determined by a. piece of small intestine coming to lie, as in one of the foetuses examined, below the left root-fold, whose free edge it pushes upwards. 410 a Mr Douglas Reid

The Pelvic or Illac-Pelvic Colon

1. The Root of the Pelvic Mesocolon. The lower limit of the fusion of the descending mesocolon to the posterior abdominal Wall almost invariably corresponds to the line of a blood—vessel, and even, adjoining the colon, to the lines of the arcades formed by the inosculations of blood-vessels (see fig. 3). The approximately vertical or right portion of the root of the pelvic mesocolon is attached usually along the line of the superior haemorrhoidal artery (see fig. 3). The more horizontal portion of the root lies higher than in the adult, quite above the external iliac artery. It usually closely skirts or passes over the lower extremity of the left kidney, and, as just stated, it is attached along the line of a blood—vessel (either a sigmoidal branch of the inferior mesenteric or of the lower part of the left colic artery).

Fig. 3. Foetus No. XI.

The intersigmoid fossa is mostly present even in the smallest foetuses examined, and usually ascends for some distance along the inner border of the lower extremity of the kidney. Its orifice is bounded behind, as in the adult, by the left ureter. It is prolonged upwards along, or between, the lines. of blood-vessels, and is often determined by the adhesion of the descending mesocolon occurring along the line of a sigmoid artery arising (directly or indirectly) from the inferior mesenteric artery at an acute angle open downwards (see fig. 3).

The mesentery of the primitive omega loop of pelvic colon (fig. 2) is rotated upwards about the vessels which lie along its root, so that the surface, which will become posterior when the pelvic colon enters the pelvis after birth, is now definitely anterior. I have seen cases in which both the superior haemorrhoidal artery and the artery which lies along the left part of the root of the pelvic mesocolon are separated above from the parietal peritoneum of the posterior abdominal wall by clefts. In other words, it appears as if the upward plication of the pelvic mesocolon about the blood-vessels is primary to the adhesion along these bloodvessels to form the root. This may help, along with the rigidity of the blood-vessels, to determine their position along the line of the root.

Pressure occurring during the movements of the pelvic colon may cause a secondary displacement of the root. ‘ ,

As has been noted, the superior haemorrhoidal artery lies along the right portion of the root. In one specimen this part of the root is attached, for ‘exactly the width of the colon, ‘to the right side of this artery. This has manifestly been brought about by a rotation of the right limb of the omega, which has brought it to press firmly upon the anterior surface of the pelvic mesocolon to the right of the superior haemorrhoidal artery, and has caused the part pressed upon to adhere to the posterior abdominal wall over an area corresponding exactly to the part pressed upon. .

In another foetus a similar displacement has been brought. about by the pressure which has obviously been exerted on the anterior surface of the pelvic mesocolon during the descent of the summit of the primitive omega to" form the secondary M-shaped pelvic colon (see fig. 3) which I shall presently describe. The original line of attachment is still indicated by a slight fold leading downwards from the intersigmoid fossa. ‘

In the light of these evident causes for the fusion, the displacement theory quite fails to account for the displacement of the root. Obviously two endothelial surfaces have been pressed together and have adhered to one another; and there are details, which have hitherto been overlooked, in the arrangement of the peritoneum of almost every one of the twenty smaller foetuses I have examined, that. point to the occurrence of adhesion together of normal peritoneal surfaces in this manner. 412 Mr Douglas G. Reid

2. The Form of the Pelvic O’olon.—In three out of the twenty foetuses the pelvic colon forms a large intra-abdominally placed, roughly omegashaped loop, the right limb of which descends usually without marked bend into the pelvic cavity. The left extremity of the loop in one case lies practically at the pelvic brim. In the other two it is placed distinctly above the brim, and in them, therefore, the loop is perhaps best named the iliac-pelvic omega.

The pelvic colon in the foetus, whilst the caecum is still at a high level, does not extend upwards beyond the root of the mesentery, and is always roofed over by the mesentery. ‘

In the adult, on the other hand, it may conceal the small intestines behind it as it ascends, rotating the mesentery upwards and to the right before it. It may even come to lie in front of the stomach, and may also compress the liver to a considerable extent, producing a groove on its visceral surface, and even a series of furrows on its parietal surface, as in a case I have noted (Journal of Anatomy and Physiology, vol. xliii.).1

In the foetus, headward growth of the primary omega is resisted not only by the large liver, but more directly, and very effectively, by the left root—fold behind which the summit of the loop may come to lie (see fig. 2). The loop may extend laterally into the region below the right root-fold. This extension is resisted by the genito-mesenteric sheet (see fig. 3), which probably helps to modify the form of the pelvic colon, and may be itself modified by the bowel. In five cases a particular modification of the loop has been produced in this manner.

As a consequence of the resistance above, the summit of the omega has been forced to descend. This subsidence, which occurs as a rotation downwards between two sigmoid arteries, results in the formation of an M-shaped loop of pelvic colon (see fig. 3 and fig. 4.-, iv.). The third stage in the development of the pelvic colon consists of changes which especially affect the left loop of the secondary M-shaped pelvic colon.

The plication of peritoneum associated with it becomes undone, and the loop is straightened out to form part (see fig. 4, iii.) or the whole of the iliac colon along with part of the pelvic colon. Or it may be entirely used to form part of the pelvic colon.

Therefore there are here three forms which may precede the development of the intra-pelvic colon. They are the primary omega—shaped pelvic or iliac-pelvic colon, the secondary M-shaped pelvic colon, and the tertiary colon (see fig. *4, iii.), in which the left loop of the M-shaped colon has dis ‘- An extreme case of ascent of the pelvic colon is described by Barclay Smith, Journal of Anatomy and Physiology, vol. xxxii. p. 341. Studies of the Intestine and Peritoneum in‘ the Human Foetus 413

appeared, leaving the right loop which ascends for a variable distance into the abdominal cavity.

There are other modifications of the primary pelvic colon, and the manner in which they have been brought about can usually be recognised by undoing the plications of the pelvic mesocolon which are produced during their formation.

FIG. 4.—The primitive iliac-pelvic colon. The. compressed and partly inverted omega. A small compressed omega, and the M-shaped iliac-pelvic colon from which in this case it has been formed.

Part of the ascending limb of the loop may be straightened out so as to form a direct continuation of the descending or iliac colon with which it is brought into line. In this way the two limbs of the loop maywbecome closely opposed, and what may be termed a compressed omega results. At the same time, or subsequently, owing to the resistance of the left root-fold, the summit of the loop may be turned downwards so that it comes to lie either (Ct) to the right of the descending limb of the loop ’ 414 ‘ . ' Mr Douglas G. Reid

(see fig. 4, ii., and fig. 5), or (b) to the left of the ascending limb of the loop. . .

In this manner what may be termed the compressed and incompletely inverted omega loop is produced (fig. 4, ii.). If the summit turn downwards on the right side, it may meet with the resistance of the genito-mesenteric fold (see fig. 3). This was beautifully seen in one case (see fig. 5). The

Czaslro-phrenic ligament Bare area of Stomach


V Outline Of spleen Sub-venous fold /

Ga5t,-o-hepatiC- Omemum i ll/ Abdominal wall (cut)

’ ‘ill Pre-splenic fold Inferior area of gastric ‘

adhesion ’ "7.i:Sub-splenic fold

_ . e ,1 (Superior surface) HeP3t°'C0"C "gamem * «  Phreno-colic ligament

Pyloro-colic fold|d

, Colon PelVlC Colon

Plica vascular-is

HYD0gastric artery Urinary bladder (Cut)

FIG. 5.—Foetus No. X. The spleen has been removed to show the upper surface of the sub-splenic fold, which is distinct from To1dt’s (“the suspensory ”) ligament. '

line of attachment of the genito-mesenteric fold lay considerably to the

right of the right spermatic vessels, along which it is primitively attached,

and its lower end was separatedby a considerable distance from the plica

vascularis. The genito-mesenteric fold and the plica vascularis lay each with its right surface turned and apposed to the posterior parietal peritoneum (fig. 5). On rotating the turned-down summit of the omega up wards into its primitive position, it just brushed over each of these folds. What had taken place was that the summit of the loop had glided downStudies of the Intestine and Peritoneum in the Human Foetus 415

wards upon the left surface of the genito-mesenteric sheet, pushing it, and with it the plica vascularis, over upon its right side. Moreover, it had caused, as a result of the pressure, the genito-mesenteric sheet to adhere by its right surface to the parietal peritoneum. This, of course, produced a diminution in the size of the fold, a displacement to the right of its line of attachment to the posterior abdominal wall, and a marked interruption in its continuity with the plica vascularis (see fig. 5). Here, again, is distinct evidence that two endothelial surfaces may adhere together apart from inflammatory causes. ‘

We must contrast the small size, due to apparent disappearance, the result of fusion, of the genito-mesenteric fold as presented here, with the still large size of the fold in these foetuses in which the M-shaped form of pelvic colon is present (see fig. 3). In these latter cases it is clearly the left root-fold which affords the chief resistance in the production of the M-shaped colon, and the genito-mesenteric fold is not pressed upon to any considerable extent. '

A compressed omega may also result from the straightening out of the left loop of the M-shaped pelvic colon (fig. 4, iii.).

A compressed and incompletely inverted omega may also be produced in a direct and simple way. Thus, in one foetus the right half of the primitive omega had rotated forwards, and to the left about a sigmoid artery and its convexity has been brought into complete and close apposition with the concavity of the left half of the loop.

This manner of modifying the omega may be especially associated with the resistance which may have been offered upon the right by the genitomesenteric fold which is present. ,

Sometimes the omega loop may turn forwards and downwards as a whole, and take at once the direction which is presented by the intra-pelvic adult pelvic colon. This is indicated in one foetus where the pelvic colon is small. ' . L

I have drawn attention to the following forms of pelvic colon :—

(1) The primitive omega loop (figs. 2 and 4) which in some cases may rotate downwards as a whole.

(2) The secondary M-shaped loop of pelvic colon (figs. 3 and 4) arising

I from (1).

(3) The compressed omega loop arisingfrom (1) or (fig. 4) from (2). (4) The compressed and incompletely inverted omega (figs. 4 and 5) loop arising from (1) or from (3).

(a) With the original summit of the omega turned downwards upon the left side, or

(b) Upon the right (genito-mesenteric) side (figs. 4 and 5).