Paper - The development of the rectum in the human embryo

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Johnson FP. The development of the rectum in the human embryo. (1914) Amer. J Anat. 16(1): 1-58.

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This historic 1914 paper by Franklin Paradise Johnson (1888-1943) describes the development of the rectum in the human embryo.

See Johnson's earlier paper on the mucous membrane of the gastrointestinal tract: Johnson FP. The development of the mucous membrane of the oesophagus, stomach and small intestine in the human embryo. (1910) Amer. J Anat., 10: 521-559.
See also Frederic Lewis's 1943 tribute to Johnson: Lewis FT. Clark ER. and Scammon RE. Franklin Paradise Johnson. (1943) Anat. Rec. 86: 1-7.

Modern Notes:

Recent papers on this topic.

YiChen Huang, Fang Chen, Xue Li Clarification of Mammalian Cloacal Morphogenesis Using High-Resolution Episcopic Microscopy. Dev. Biol.: 2015; PubMed 26485363

Sebastian C J van der Putte The development of the human anorectum. Anat Rec (Hoboken): 2009, 292(7);951-4 PubMed 19496155

P A de Vries, G W Friedland The staged sequential development of the anus and rectum in human embryos and fetuses. J. Pediatr. Surg.: 1974, 9(5);755-69 PubMed 4424274

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The Development of the Rectum in the Human Embryo

Franklin Paradise Johnson

The Anatomical Laboratory of the University of Missouri

Twenty-Five Figures (1914)


This is the third of a series of papers concerning the development of the mucous membrane of the digestive tract. The first two (Johnson '10 and '13) deal with the oesophagus, stomach, and small and large intestines. In this paper an account of the development of the rectum is given, particular attention being paid to the formation of the pars analis recti.

The upper portion of the rectum, that is, that part which goes into the formation of the ampulla recti, develops in a similar manner to the colon. In this region, ridges, folds, villi, and glands make their appearance in the order named, and, simultaneously with the further development of glands, the villi disappear. As these changes have already been described by stages, another account need not be given here. Attention, however, might again be called to the fact that the rectum is more precocious in its development than the other parts of the large intestine; thus we find in the rectum conditions which are always in advance of those higher up. It is to be noted also that the ridges and folds of the mucous membrane which precede the formation of glands and villi, at the level where these pass over into the anal region, are not longitudinal in direction, as found in the remaining portions of the large gut, but are transverse. In still another respect the mucous membrane of the ampulla recti of the embryo differs from that of the colon. One finds numerous epithelial gland cysts, which exist throughout a considerably long period of embryonic life, but which have disappeared before birth. These also have been described in the former paper.

Regarding the material used and the method of study employed very little need be said. Whole embryos, sectioned serially, have been used for stages up to 44.3 mm. From this stage upward, with the exception of an embryo of 65 mm. which was also sectioned whole, the pars analis recti, including a portion of the ampulla recti and the skin around the anus, was cut out of the embryos and made into serial sections, some cross, and some longitudinal. The serial sections of the whole embryos obtained from the Harvard Embryological Collection are designated, H.E.C.; those from the collection of the University of Missouri, H.

Wax models have been made to illustrate the conditions at various stages of development. Use was also made of gross dissections, and particularly of mid-saggittal sections through the whole pelvis. The models of the epithelial tube, except in case of older stages, have been made at a magnification of 145 diameters, and therefore allow easy comparison with those made of other portions of the digestive tube.

A difficulty which presented itself at the outset of this work was one concerning terminology. One finds in the literature varying descriptions of the rectum; the same terms being used to denote different portions. It was necessary, therefore, to review the literature concerning the anatomy of the adult rectum and determine upon the most generally accepted terminology. A brief review of the literature concerning the limits and subdivisions of the rectum is first given. To it are added certain topographical relations as described by various authors, for comparison with the observations noted in the section on developmental topography included in this paper.

Although but few observations have been made regarding the development of the plicae transversales recti, it was thought best for the sake of completeness, as well as for comparison with the observations made on the larger folds of the mucous membrane found in the small and large intestines, to include a brief description of them here. The Uterature regarding those of the adult, therefore, is briefly alluded to.

More attention, however, has been paid to the investigations bearing upon the embryology and histology of the pars analis recti. More complete re-views of the literature on this subject have been given by Braun ('01) and Zimmermann ('04). The following resume of the literature is taken up under separate headings.


Boundaries and subdivisions of the rectum

According to Merkel, Sanson in 1817 described the rectum as beginning at the pelvic brim in the region of the sacro-iliac synchondrosis. The first of its three divisions, as described by Sanson, passes obliquely downwards from left to right, in which it describes a slight curve toward the right and finally reaches the mid-line against the third sacral vertebra. It is completely surrounded by a peritoneal fold called the mesorectum. The second part extends along the concavity of the sacrum to the end of the coccyx, where the third part begins. This turns backwards and ends in the anus. This description was accepted and used by most of the anatomists up until 1885 when Treves (according to Symington) modified it. Treves considered as the rectum only that part of the large intestine which is devoid of mesentery, which he says, begins at the level of the third sacral vertebra. That portion of the rectum previously known as the first part of the rectum he includes with the sigmoid flexure under the term 'sigmoid' or 'omega loop.'

Symington ('88) accepted this view of Treves in regard to the upper limit of the rectum, but regards only the second part of the rectum of the older anatomists as the rectum proper. The third part he calls the 'anal canal,' which he says, had previously been incorrectly described. It differs from the rectum in that it "exists normally as a longitudinal fissure." It is about an inch in length.

Merkel ('00) also regards the termination of the mesocolon as the upper Umit of the rectum, but divides it into two parts. The upper he calls the "pars ampullaris recti;" the lower, the "pars analis recti". He says :

”Zu dieser wichtigen Anderung im Verhalten des Bauchfelles kommen noch zwei Punkte in der Structur der Darmwand selbst, welche dem untersten Darmstiick eine besondere SteHung anweisen, erstens die betrachliche Verstarkung der Muskulatur unci zweitens die Neuordnung der Langsfaserschichte (Aufhoren der Tanien), Dieses Verhalten der Muskulatur ordnet das Rektum in die Reihe der Blasenbehalter ein, als Kotblase (Waldeyer), eine Annahme, welche durch haufig zu beobachtende spindelformig Erweiterung des Darmrohres (Pars ampullaris recti) (Pars pelvina, Waldeyer) gestiitzt wird. Dieser erste Teil des Mastdarmes reicht aber niemals bis zur Afteroffnung hin, sondern man findet das letzte Stiick immer, in gleicher Weise leer and zusammengezogen, so dass man dieselbe als zweiten Teil des Mastdarmes (als Pars analis recti) (Canalis analis, Symington) von der Pars ampullaris zu trennen hat.”
(To this important alteration in the behavior of the abdomen, there are two points in the structure of the intestinal wall itself, which indicate a particular condition to the lower intestine, first, the growth of the musculature, and the rearrangement of the longitudinal fibers. The rectum is placed in the row of the bladder vessels, as a bladder (Waldeyer), an assumption which is supported by the frequently observed spindle-shaped enlargement of the intestinal tube (Pars ampullaris recti) (Pars pelvina, Waldeyer). This first part of the rectum is never sufficient to reach the opening, but the last part is always found to be empty and contracted, so that the second part of the rectum of the rectum (Canalis analis, Symington) of the Pars ampullaris.)

In a paper regarding this subject, Paterson ('08) writes: "The superior rectal valve, though variable in its form, is, in my opinion so generally present that it may be looked upon as the true junction of the pelvic colon and the rectum."

Symington ('12) believes with Paterson that the superior rectal valve is a more reliable guide to the colo-rectal junction than the termination of the mesocolon, as this latter ends so gradually: "There is no reliable bony landmark serving as a guide to the colo-rectal junction, since while the empty and contracted rectum usually starts opposite the third sacral vertebra, when the rectum is distended this junction may rise as high or even higher than the sacral promontory. "

Of the modern text-books of anatomy, Sobotta-McMurrich is the only one of those I have examined which still follows the description of Sanson, that is, considers three divisions of the rectum, the first of which begins at the sacral promontory. Cunningham regards as the rectum only that part of the digestive tube which lies between the third sacral vertebra and the pelvic floor. The 'anal canal' is treated separately. Other authors speak of two parts which lie between the third sacral vertebra or termination of the mesocolon, the pelvic floor or diaphragm, and the anus. The terminology, however, differs considerably. Thus the ampulla is considered as the lower part of the first portion of the rectum by Testut, Kopsch-Rauber, and Spalteholz. The terms 'pars pelvina' and 'pars perinealis' are employed for the two parts of the rectum by Waldeyer in Joessel's Lehrbuch. Poirier et Charpy use the terms 'rectum pelvien' and 'rectum perineal.' Morris and Gray apply no especial name to the first part. The former calls the second part the 'anal canal,' the latter the 'inferior' or 'prostatic' portion. Gray, like Spalteholz, Kopsch-Rauber, and others, regards only the lower widened portion of the first part as the ampulla recti. Corning considers as synonyms for the first part of the rectum the terms pars ampullaris recti, pars pelvina, and flexura sacralis, while for the second part, pars analis recti, pars perinealis, and flexura perinealis ; and says that the three sets of terms are applicable from the standpoints of physiology, topographic anatomy, and descriptive anatomy, respectively.

Likewise in the case of boundary lines between the pars analis recti and the ampulla recti one finds varying descriptions. Thus, the tip of the coccyx, the pelvic diaphragm, and the beginning of the pelvic floor are all given. It has also been described merely as the beginning of the narrower portion found below the widened ampulla. Still another line of division is given as the ano-rectal line, the point at which the simple columnar epithelium leaves off and a stratified columnar epithelium begins. However, these points do not exactly coincide. The ano-rectal line, even in late fetal stages, does not correspond to the beginning of the narrow portion of the rectum ; while the statement that it ends at the tip of the coccyx is indefinite.

The terms as found in the B.N.A. list are used consistently throughout this paper whenever possible. As regards the meaning of the term 'ampulla recti,' the work of Merkel and Corning is followed, designating the whole of the first portion of the rectum. By 'pars analis recti' will be meant that portion which has, under ordinary conditions a much narrower caliber than the ampulla. This portion which develops from a definite embryonic structure, does not have as its upper limit the histological ano-rectal line. Its upper boundary corresponds fairly closely, however, with the beginning of the pelvic floor.

Plicae transversales recti

Although the plicae transversales recti (valves of Houston), which are found in the ampulla recti, have attracted a great deal of attention from many anatomists, only a brief reference to the literature regarding them need be made in this paper. Most anatomists agree that Houston, after whom the plicae were named, was the first to describe them adequately. The name Kohlrausch, however, is often used in connection with the lower of these folds.

Baur ('60) made a careful study of the plicae and found that three are usually present. He also found indications of them in embryos of three, three to four, and four to five months, and at birth.

Vance (78) describes these folds in a number of adult subjects and emphasizes particularly the spiral arrangement of some of them. He asks: Is it not reasonable to suppose that both spiral folds and independent valves exist in the human rectum as rudiments, and that, when present in that organ, they must be looked upon as illustrations of the law of reversion?" In just what manner they are to be regarded as illustrations of this law, Vance does not state.

Otis ('87) finds the rectal plicae constantly present and states that there are either two or three of them, two of which are constant in position, and one of which is variable.

Pennington ('00) attaches particular importance to the folds from a clinical point of view, stating that they are often the cause of constipation. In describing their histological structure he states that some are composed of the mucosa and the submucosa alone, some have the circular muscle coat involved, while still others have a part or the whole of the longitudinal muscle coat.

Rectal columns, sinuses and valves

The longitudinal folds at the lower extremity of the rectum known as the column ae recti (columns of Morgagni) vary not only in size and number, but also in position. This conclusion is based not only upon the specimens I have myself examined, but upon the widely varying descriptions found in literature. Thus Ball ('94) describes the columns as lying; wholly within the ampulla, while on the contrary, Birmingham (in Cunningham's Text-book of Anatomy) shows them as lying wholly within the pars analis recti. Most authors, however, figure them as lying partly within the two portions of the rectum.

The same is true in regard to the descriptions of the valves of Morgagni and rectal sinuses (sinus rectales) . Some authors show them as very definite structures, closely resembling the valves of the aorta, with wide pockets behind and arranged regularly in between the bases of the rectal columns. Other authors state that they are inconstant and vary greatly in size and shape, and figure them as narrow clefts in between two adjacent columns.

The rectal columns and valves according to Bodenhamer ('88) were well understood and correctly described by Morgagni and Glisson, and by other early anatomists.

Bodenhamer gives the credit to Glisson for the discovery of the columns, valves and sinuses. Braun ('01), on the other hand, while admitting that Glisson discovered the valves, states that the columns and 'Sinuositaten' (meaning the smaller secondary sinuses) were discovered and described by Morgagni (1719). Braun further states that Heister (1727) first described the transition zone between the mucous membrane of the rectum and the outer integument.

Chiari ('78) describes the rectal sinuses under normal and pathological conditions. He believes that by an outward and downward extension of these structures, fistulae are produced, and in support of his theory he gives several figures of the sinuses in different stages of fistulae formation. The same view is held by Bodenhamer ('88).

The first noteworthy attempt to describe accurately the mucous membrane of the anal region was made by Robin and Cadiat in 1874. In describing the junction of the ampulla and the pars analis recti, they state that the latter differs from the former only in that it is not provided with the intestinal glands. The upper limit of the pars analis recti is described as the line where the intestinal glands leave off ('hgne ano-rectale'), while the lower limit, the iigne sinueuse' lies at a distance of 5 to 8 mm. below the ano-rectal line. The zone marked off between these two Unes is broken and raised from place to place by the columns of Morgagni, between which are found the intercolumnar pits or depressions ('godets'). The semilunar valves are found at the inferior extremity of this zone. Two types of epithelia are present, but it is not clear from the descriptions just where these are to be found. In an accompanying figure, the limits of the two epithelia are definitely shown and the following description is based largely upon the figure and its accompanying legend. The first is the prismatic type of epithelium which, like that of the colon, extends from the ano-rectal line to the bottoms of the sinuslike depressions. The second, the stratified squamous type, lines the internal wall of the sinus, that is, the supero-external wall of the valve. Below the sinuous or true anal line" is described a region which is different from the skin proper, but which takes on more and more the structure of the skin when followed caudally.

This region which is 'termed the zone cutanee anale lisse, " extends down to where the hairs begin, a distance of 12 to 20 mm. below the sinuous line. It differs from the skin in that its cells are without pigment, only slightly cornified, the dermal papillae are small and few, and sebaceous and sweat glands are lacking.

Herrmann and Defosses ('80) state that the mucosa of the inferior extremity of the rectum is not directly continuous with the external integument, but that there exists at this level a circular zone, 6 to 12 mm. in height, corresponding to the muscular columns of Morgagni, and which represents a persistent part of the cloaca of the embryo. On the columns the epithelium is stratified polygonal, with superficial plate-like cells, while in the depressions it is of the stratified prismatic type.

Herrmann ('80) states that the anal mucous membrane is limited by the 'ano-rectale' and 'ano-cutanee' lines. The first he describes the position of definitely enough when he says here end the intestinal glands and the simple columnar epithelium of the colon, but his statement that it is to be found at the level of the upper borders of the anal valves and rectal columns is not clear.

The 'ano-cutaneous' line is drawn at the point where the anal epitheUum passes over the stratified squamous type (Robin and Cadiat's " Hgne sinueuse")- Below this line is the zone cutanee peri-anale" (zone eutanee lisse" of Robin and Cadiat). In agreement with the descriptions set forth by Robin and Cadiat, Herrmann says this region is deprived of hairs, sebaceous and sweat glands. Its epithelium is stratified polyhedral, composed of six to eight layers of cells, and differs from that of the skin by the absence of indented cells and a cornified covering, for although the superficial cells are somewhat flattened, they have not a lamellar form. The nuclei are clear and the cell bodies finely granular and stain the same as the underlying cells. Neither a stratum corneum nor stratum lucidum is present. â–  The anal mucous membrane proper, that is, the zone between the ano-rectal and ano-cutaneous lines, is thrown into folds (columns of Morgagni) between which lie rounded sinuses. Extending outward from these sinuses are recesses of a second type, narrow slit-like cavities which reach almost to the internal sphincter. A third type of sinus extends from the secondary type in the form of branched tubules. These, which he calls the intramuscular sinuses" ("special acinose glands") are dealt with below. The anal mucosa is covered by an epithelium which is made up of several layers of polygonal cells but the superficial cells are of the prismatic type. The protoplasm of these prismatic cells is transparent and only slightly granular and not readily staining.

He states further that it is a general rule that the stratified polygonal epithelium covers the more elevated parts (columns of Morgagni), while the prismatic type is found in the depths of the mucosa, in other words, "those parts which are not exposed to pressure and mechanical effects."

Ball ('94) states that the "white line of Hilton" is the anorectal line of Herrmann, but since he says it occurs at the level of the semilunar valves, he undoubtedly means Herrmann's ano-cutaneous line. Birmingham ('09) uses the terms "white line of Hilton" and "ano-cutaneous line of Herrmann" synonymously.

Development of columns, sinuses and valves

Regarding the development of these structures very little has been written. The paper which deserves most credit is that of Herrmann ('80). His observations begin in an embryo of 85 mm. At this stage he states that the mucosa of the anal region forms a zone about 1 mm. in height, and contains on the sides excavations which are divided into several compartments by longitudinal folds. These folds of mucous membrane form the columns of Morgagni, and mark the places where the muscular columns are to develop. The epithelium is stratified prismatic, composed of two to three layers of cell's, and is about 0.025 to 0.030 mm. thick. The peri-anal cutaneous zone is covered by a stratified squamous epithelium of six to eight layers of cells, but shows no traces of hairs or glands. At 140 mm. the longitudinal folds are more numerous and in places are no more than 0.1 mm. from the internal sphincter muscle. In the epithelium of the peri-anal zone, in its outer part, hair follicles and sebaceous glands are beginning to appear. Sweat glands are present as tortuous cylindrical tubes of epithelium which are greatly swollen at their extremities.

In an embryo of 190 mm. the muscularis mucosa is present in the region of the rectal ampulla, but is absent from the anal region. In neither the rectal or the anal mucosa are solitary nodules present. At 210 mm. the anal mucosa has grown to a height of 2.5 mm. and has an epithelium of 0.04 to 0.05 mm. in thickness. At birth the anal region has a height of 3.5 mm. The muscularis mucosae is completely formed and is prolonged in several strands which extend down into the rectal columns. Finally in an infant of two years, he says, are to be found the identical disposition of all structures which are found in the adult, only with reduced dimensions.

Ball ('94) regards the semilunar valves as vestigial remnants. Re says: I think it may with tolerable confidence be asserted that the anal valves are vestigial remains of the anal plate, the rest of which has disappeared in the process of development." No evidence, however, is given in support of this assumption.

Birmingham states that both the columns of Morgagni and the rectal valves are distinct in embryos of four to five, six and nine months.


Gay ('71) describes an elliptical ring of glands in the form of a wreath around the anus. The ring he states is 1.25 to 1.5 cm. broad and the inner border of the zone 1 to 1.5 cm. from the anal opening. These 'circum-anal' glands have the structure of sweat glands but they are considerably larger, being even larger than the axillary glands. They are entirely absent in between the ring and the anus where only sebaceous glands are to be found.

Robin and Cadiat ('74) describe the manner in which the intestinal glands leave ofT at the lower extremity of the rectum. When seen in longitudinal section, the last four to six intestinal glands are more closely packed together and their cells stain more intensely. They emphasize the fact that there is a smooth zone (the zone cutanee lisse) below the ano-cutaneous line which has a stratified squamous epithelium, but which is lacking in hairs and glands. As soon as the sebaceous glands begin, they are relatively large.

Herrmann and Defosses ('80) describe another type of gland in the anal mucosa. They assert that at the bottoms of the sinuses limited by the semilunar valves, the epithelium prolongs itself in irregular canals which extend across the internal sphincter, in contact with which they are frequently enlarged, forming widened excavations. From these enlargements branch off several ducts which are quite similar to gland tubes. The tubes traverse the whole of the internal sphincter, and terminate in the connective tissue interposed between this muscle and the longitudinal layer of the muscularis.

Herrmann ('80) goes somewhat more into detail in the description of the glands found in the anal region. Several types are considered. 'Erratic glands' are intestinal glands which are found below the ano-rectal line in the region of the zona columnaris. They are few in number and are found only in a region a few millimeters below the ano-rectal line. 'Isolated goblet cells' are likewise found for a short distance be^ow the ano-rectal line and finally 'special acinous glands' which have already been referred to as the intramuscular glands. In regard to these last structures Herrmann states that he is not certain that they should be classified as glands. He was able to find no trace of secretory epithelium in them. He suggests that the term 'intramuscular sinus' would probably be more appropriate for them. He is nevertheless certain, because of their peculiar disposition that they correspond to the true acinous glands found in this region of the dog. Regarding the structure of the intramuscular glands Herrmann states that those in man are made up of polygonal cells which are similar to those of the epithelium from which they arise. They extend outward through the submucous layer, and, in contact with the internal sphincter muscle, the tube of epithelium presents a swelling which is lined with a cuboidal epithelium composed of one to two layers of cells. The branches arising from this swelling penetrate still further into the muscle and terminate in small caecums in between the iimer circular and outer longitudinal layers of muscle. Scattered along the tubes, and particularly about their terminal ramifications, are found masses of lymphoid tissue.

Braun ('01) states that in the transition zone (zona intermedia) can be found in some individuals, though not in all, free sebaceous glands. Because he was unable to find any of Herrmann's special acinous glands (intramuscular sinuses) he completely denies their presence. He describes and figures, however, tubelike structures (rohrenformige Anhange) which arise from the secondary sinuses ('Sinuositaten'). These, however, were found in the submucosa and did not pierce the internal sphincter muscle.

Although the glands of the anal region in man have attracted but little attention, those of the lower mammals have been more thoroughly studied. Herrmann uses the term 'anal glands' to denote the two large saccular glands of the dog. Besides these he describes large intramuscular glands, which, unlike those of man, open into the pars analis recti below the zona columnaris. These are true acinous glands lined with secretory epithelium.

Hebrant ('99) likewise describes under the term 'anal glands' of the dog, the two saccular glands found one on either side of the anal orifice, and which open by small ducts on the skin just lateral to the anus. He also describes 'sudoriparous' glands which apparently include both Herrmann's intramuscular glands and Zimmermann's 'circum-anal' glands. He also describes the close relation of the lymphoid nodules to the anal mucous membrane of the dog, and remarkis upon their close resemblance to the structure of the tonsils. With regard to this he says: "N'y a-t-il pas lieu ainsi d'admettre, de la part des glandes anales par les follicules clos qu'elles renferment, une action analogue a cette jouee par les amygdales a I'autre porte d'entree du tube digestif?"

Zimmermann ('04) has made a careful and complete stud}^ of the glands of the anal region of the dog. He divides the anal mucous membrane into three zones: the zona cutanea, which is composed of internal and external subdivisions, the zona intermedia, and the zona columnaris. All these regions are lined by a stratified squamous epithelium, which takes on more and more the structure of the skin when passing downward from one region into the next. The zona columnaris is characterized by columns, sinuses and valves. The sinuses are not always equally well formed and some 'Sinuositiiten' extend in the form of branched canals or crypts into the region of the lymphoid nodules. These structures, he speaks of as the 'anal tonsils.' The zona intermedia is characterized by its smooth epithelium and the ducts of the large 'reservoir glands.' The zona cutanea takes on more and more the structure of the skin when followed downward. The internal portion lies within the anal canal, the external without. This zone contains large sebaceous glands (which according to Zimmermann have incorrectly been called 'circum-anal glands') and sweat glands, both of which open into hair infundibuli in which hair shafts are lacking.

For an account of the anal regions of the domestic animals, the reader is referred to the work of Mladenowitsch ('07) who has studied this portion of the rectum of the horse, ox, sheep, goat, pig, dog, and cat. He finds that the columns of Morgagni, or rectal columns, and the rectal sinuses are constant structures. Blackman ('11) is referred to for an account of the anal glands of the skunk.

Development of the anal glands

Regarding the embryology of the anal glands in man, the work of Herrmann alone is known to the writer. He asserts that the intramuscular glands are present as small epithelial buds in an embryo of 140 mm. In an embryo.of 190 mm. they have penetrated the internal sphincter, in which they end in small ampullalike swellings. At this stage the glands are not provided throughout with lumens, but are in some places solid cords of cells. At 240 mm. they extend through the whole thickness of the internal sphincter muscle and are complete canals. In the region of their terminal swellings lymphoid tissue is already being laid down. At birth they are quite similar to those of the adult.


Early stages

Under this heading are arbitrarily grouped stages up to 22.8 mm. when the first evidences of the columns of Morgagni are seen. No attempt has been made to work out the early history of the formation of the hind-gut and cloaca, for this has already been thoroughly done by Keibel ('96), whose observations have been recently confirmed by Pohlmann ('11). These observers show clearly the relations of the hind-gut in its earlier stages to the allantois, and of the rectum to the cloaca, and the division of the cloaca into the rectum and the urogenital sinus.

Observations on embryos of 7.5 mm. (H.E.C. 256) and 10 mm. (H.E.C. 1000) have already been reported (Johnson '13). In these stages the rectum has the form of a hollow tube, and in the 10 mm. embryo presents at its lower extremity a spindle-shaped swelling. The cloaca is present but closed off from the outside by the cloacal membrane. These observations are in accordance with those of Keibel and Pohlmann, who state that the cloaca is never open to the outside.

In an embryo of 13.6 mm. (H.E.C. 839) the rectum presents a large spindle-shaped swelling. At the lower end of this swelling the epithelial tube becomes much reduced in size, but just before the cloaca is reached, it gradually increases in size again. This lower widened portion, which is relatively short, joins the cloaca.

Separation of the rectum and urogenital sinus has taken place in an embryo of 16 mm. (H.E.C. 1322). The spindle-shaped swelling is more pronounced than before, and its epithelium now passes over into that of the outside skin. Just before the epidermis is reached, however, another slight swelling is seen, smaller and more flattened than the swelling above. The lumen of the rectum is continuous above with that of the colon, is larger in the swellings than in between them, and below opens to the exterior by an extremely fine opening. In a second embryo of 16 mm. (H. 133) the epithelial tube has a similar form. The lumen, however, is occluded at its lower end.

In embryos of 17 mm. (H. 58) and 19 mm. (H.E.C. 819) both swellings have increased slightly in size and are more flattened dorso-ventrally. Again the lumen does not open to the outside for at its lower extremity can be seen a mass of cells which fills the lumen.

At 22.8 mm. (H.E.C. 871) the epithelial tube presents a form as seen in figures 7 and 11. The two swellings are again present, the upper of which is much larger and more conspicuous. Both are again slightly flattened dorso-ventrally. A very shallow depression can be perceived running along the ventral surface of the upper swelling thus forming a small infolding of the epithelium into the lumen. This fold, the first of a large number to develop in the walls of the rectum, may be regarded as the earliest appearance of a rectal column.

Throughout all the preceding stages the epithelial tube is made up of a stratified epithelium of two to four laj'^ers of cul^oidal cells, without distinct cell boundaries, an epithelium quite similar to that found in the whole of the digestive tract in its early stages. In the region of the swellings the epithelial wall becomes correspondingly thicker.

Surrounding the above described epithelial tube of the rectum is seen loose mesenchyma. The circular layer of the muscularis was first seen in an embryo of 16 mm. It extends down only as far as the constriction in between the two swellings, a point to which Keibel calls attention. A lighter staining zone was seen just outside of the circular layer of muscle, probably the beginning of the nervous layer. At 17 mm. a faint indication of the longitudinal muscle coat is seen. In embryos of 19 mm. and 22.8 mm., both layers of muscle, with the intervening nervous layer, have become more distinct.

Apparently Keibel was the first to describe the two swellings of the rectum referred to above. He shows that they are present and distinct in embryos of 17.5, 18.5, and 25 mm. In the description of his figure 55 - a longitudinal section of the rectum from an embryo of 25 mm. - he says:

Wir sehen die Aftergrube, in welches sich die Deckschicht des Ectoderms fortsetzt. Es folgt weiter cranial eine kleine Anschwellung des Darmrohres, die aber mit der Aftergrube noch nicht in offener Verbindung steht. Die Grenze zwischen Ectoderm and Entoderm tritt ziemlich deutlich hervor. Auf die kleine Anschwellung des entodermalen Enddarmrohres folgt cranial eine stark ausgebildete Anschwellung, wie sie ja an den Zeichungen nach den Modellen und auf der Profilreconstruction klar genug zur Darstellung kommt.

Tourneux ('90) who studied the cloacal region of the sheep, does not refer to these two swellings so distinctly shown by Keibel, and Pohlmann ('11) apparently failed to find them in the human embryo.

Concerning a sagittal section through the rectum of a 22 mm. embryo, Lewis ('12) states that:

Just before the rectum reaches the anal membrane it forms a bulbous enlargement .... The terminal swelling extends beyond the muscle layers as recorded by Keibel . . . . In a 32 mm. specimen the anal membrane has disappeared. Along the dorsal wall there is a slight indication of a terminal bulbous enlargement but it seems clear that it is a transient structure. It is probable that the elongated swelling above it gives rise to the rectal ampulla of the adult.

Lewis accordingly has labelled the elongated upper swelling the 'ampulla recti.' Apparently, however, he disregards the accepted use of 'ampulla recti,' for he applies the term to the bulbous pars analis recti in the figure of a case of atresia ani cum fistula vulvari, copied from Mackenzie. The conjecture that the elongated swelling gives rise to the pars analis recti proves to be correct, but the term 'ampulla recti' is wholly inapplicable, as will be shown. At the time his article was written, Lewis realized the importance of further study upon this subject, and pointed out to me the desirability of following this swelling- throughout the later stages of the embryo.

The upper swelling persists as a definite swelling throughout stages up to birth. It is an embryonic structure quite similar to that found at the junction of the ileum and the colon, which the author ('13) designated by the term 'ampulla coli.' Originally it was likewise intended to use the term 'ampulla recti' for this embryonic structure in the rectum. From its position in the early stages of the embryo one would suppose that it was identical with the ampulla recti of the adult. However, such is not the case. With the growth of the embryo it becomes relatively shorter and shorter and gradually descends lower and lower in the pelvis. It eventually turns out to be a portion of the pars analis recti of the adult, principally the zona columnaris. As this structure has as yet received no definite name, the author proposes the term 'bulbus analis.'

With regard to the lower swelling it can be said that it forms the zona intermedia of the adult pars analis recti, although nothing can be definitely said with respect to its boundaries. It persists as a swelling only throughout the early stages.

The dorsal portion of the cloaca into which the rectum opens has been termed by Tourneux ('90) the 'vestibule anal.' In describing it he says:

L'extremite inferieure du rectum debouche maintenant dans un vestibule qui se prolonge en avant jusqu'au l:»ouchon cloacal, et qui represente le sommet meme de I'anse cloacal unissant primitivement le rectum au bouchon. Nous donnerons a ce vestibule le nom de vestibule anal, et a sa parol inferieure ou cutanee exclusivement formee de cellules ('pitheliales, le nom do UK^mhrane vestibulaire ou de membrane anale.

When the cloaca becomes divided into dorsal and ventral parts, whether it he by means of the down g owth of the perineal fold (as described by Tourneux) or b}^ means of a pushing together of the two lateral mesodermic folds (Retterer '90), it is evident that the dorsal half of the cloaca becomes incorporated with the rectum and forms its lower portion. It is also evident that the lower swelling' described in the 16 mm. and 19 mm. embryos, is formed from the old cloaca. This is what is taking place in the above described 13.6 mm. embryo, where the lower bulb is only partially formed. This conclusion seems justifiable not only because the constriction between the bulbus analis and the cloaca in the early stages is identical with the constriction between the bulbus analis and the lower swelling in the later stages, forming a definite boundary superiorly, but because of the constant and definite relation presented by the anal membrane. This membrane, which is identical with the posterior half of the cloacal membrane, forms the inferior wall of both the anal vestil)ule in the early stages and of the lower swelling in the later stages. The lower swelling, which develops from a part of the cloaca (Tourneux's 'vestibule anal') and which forms the zona intermedia of the adult pars analis recti, will be sj^joken of by the term 'bulbus terminalis.'

Late Stages

The form of the rectum of an embryo at 30 mm. (H.E.C. 913) is shown in figures 8 and 12. It is to be noted that the figures represent the basal surfaces of the epithelium, that is, those surfaces which are covered by mesenchyma. The grooves, therefore, which are seen on the outer surface are to be considered as folds of the mucous membrane turned into the lumen of the rectum. For clearness of description in the remainder of this paper, these folds of mucous membrane into the lumen will always be spoken of as 'in-foldings,' while the furrows in between them will be called 'out-foldings.' The side view shows that the dorsoventral curvature is slightly greater than at 22.5 mm. The bulbus analis is not well marked off from the intestinal tube above, but below, where it joins the bulbis terminalis there is a great diminution in its dorso-ventral thickness. The bulbus terminalis itself is only slightly thicker than the constriction. Viewed from in front the upper extremity of the bnlbus analis is again indistinctly marked, whilst below its lower boundary is quite sharp. The whole surface of the anterior wall of the bulbus analis is deeply furrowed by a single longitudinal groove. Two other well marked grooves are found, one on either side.

  • Since the 'bulbus analis', (he 'bulbus terniinalis,' and the swelling at the ileo-colic junction aic all similar embryonic- structures, for the sake of consistency, it would be better perhaps, to designate the latterly the term 'bulbus coli' rather than 'ampulla coli.'

Both the internal circular and the outer longitudinal muscle coats of the rectum are distinct; also the levator ani and external sphincter muscles are apparent. The circular layer of the muscularis of the rectum extends dow^n to the constriction between the swellings of the two zones, but displays no special thickening which characterizes this region in later stages. The outer longitudinal muscle coat is still faintly visible, but its fibers can be seen running beyond the region of the circular coat. They soon become lost in the mesenchyma. The levator ani is seen running an oblique course from above downward and toward the rectum. The external sphineter lies just below its inferior extremity and its fibers are not distinctly" marked off from those of the levator ani. Numerous nerve fibers and small blood vessels are seen in the substance of and between the muscle layers.

The epithelium is different in different regions. In the bulbus analis it is 0.036 to 0.045 mm. in thickness and has two to three layers of oval shaped nuclei. C'ell boundaries are not distinct. In the region of the anal opening the epithelium is of the same thickness, but the cells of the epithelium are polygonal in shape, and have distinct boundaries. Of the four to five layers of cells, the uppermost are somewhat flattened. In the region of and that adjoining the bulbus terminalis the epithelium is only 0.024 to 0.030 mm. At the lower extremity of the Inilbus terminalis is the transition between the two types of epithelia described above. The lumen is pervious throughout, a slight opening being present through the anal membrane.

As regards the degree of development of the rectum, the embryo just described pro))ably represents a retarded stage. This is made evident because in three other embryos of about the same age which were studied - 29 mm. (H.E.C. 914), 30 mm. (H. 108), 31 mm. (H. 57) - more advanced conditions were found.

The epithelial tube of the rectum of the embryo of 29 mm, is shown in figures 9 and 13. It will be observed that the three infoldings are well marked, though they are somewhat less developed than in the above-described 30 mm. stage. These infoldings extend themselves throughout the full extent of the bulbus analis and terminate below on the bulbus terminalis. Above they terminate (with the exception of the ventral one) at the upper limit of the swelling. The ventral infolding extends beyond the bulbus analis. It should also be noted that whereas before the bulbus terminalis was flattened dorso-ventrally, it is now flattened laterally. Moreover, a distinct swelling in this region can hardly be said to exist.

The outfoldings of the epithelial tube demand especial attention. It is to be noted that the outfolding forming the left border of the rectum, can be traced into the upper border of the flattened bulbus terminalis. The one on the right terminates on the right side of the bulbus terminalis, while the dorsal passes down directly into the dorsal wall of the same. These conditions suggest that the epithelial tube in its lower part has been twisted through an angle of 90"^ in a direction which, when looked at from above, is clockwise. Whether any such twisting does take place between the two last described stages is a rather difficult problem to determine. More will be said in regard to this below.

Although the bulbus terminalis shows again as a flattened slitlike canal in embryos of 30 mm. (H. 108) and 31 mm. (H. 57), slight A^ariations are met with in regard to the folds, particularly at the lower end of the zona columnaris. In the 30 mm. stage is found a small additional ventral out-folding arising from about the middle of the ventral infolding. At 31 mm. the left outfolding does not quite reach the upper border of the bulbus terminalis but ends on the side of it near the upper border.

In an embryo 37 mm. (H.E.C. 820) the epithelial tube of the rectum presents a number of long longitudinal folds (figs. 10 and 14). Examination of the model of this rectum shows distinctly that the three outfoldings described in earlier stages are still present, although their identity is somewhat obscured by the presence of additional secondary folds. As in the 29 mm. stage the out folding on the left side passes down onto the ventral border of the flattened bullus terniinalis, the right terminates on the right side of the bulbus terniinalis about half way between the dorsal and ventral borders, while the posterior outfolding forms the dorsal border. Both the right and posterior oiitfoldings are divided into secondary folds. Just abo\'e the bulbus analis five to six irregular folds are seen which undoubtedly represent the previllous folds of the ampulla recti. Regarding the outer layers of the rectum, but few changes have taken place. The outer longitudinal coat is more distinct than before and is pierced by numerous small groups of nerve fibers, particularly along its dorsal wall. The external sphincter muscle is seen as a distinct broad band of fibers entirely encircling the lower portion of the rectum. It lies just below the fibers of the levator ani.

As seen in figures 15 and 17, the epithelial tube of the pars analis recti in an embryo of 44.3 mm. (H.E.C, 1611) presents a more advanced condition with regard to folds. Although more secondary folds are present, the primary folds are distinguishable and present similar relations to those of the 37 mm. embryo. Both primary and secondary folds show distinctly in a series of cross sections of the rectum of a 58 mm. embryo. The primary folds are similar in position and relation to those of the former stage. The secondary folds are more numerous, the right primary fold being divided up into six secondary folds, the left into seven, and the dorsal into eight. New secondary folds are seen beginning in between those already present. They develop largely after the manner of villi in the small intestine, by first a thickening of the epithelium and then an invagination of the epithelium along the thickened ridge into the lumen.

A model of the pars analis recti at 65 mm. (H. 55) is shown in figures 16 and IS. With the exception of a few additional secondary folds, the same picture is i:)resented as before. The right primary is made up of five secondary folds, the left of seven, and the dorsal which is much the largest, is composed of about ten secondary folds. Comparison between figures 10, 15, and 16 and figures 14, 17, and 18 will show that the growth of the bulbus analis has taken place by an outward expansion alone, there being practically no lengthening of this portion of the rectum.

In embryos of 70 mm. and 88 mm. similar relations with regard to folds are seen. The number of secondary folds is only slightly greater than at 65 mm.

Longitudinal sections of the 88 mm. stage show several new points with regard to the epithelium and the outer coats. The transition from the simple columnar' epithelium of the ampulla to the stratified squamous epithelium of the skin is not effected by a continuously gradual transition but takes place in three clearly defined stages. The epithelium of the ampulla is simple columnar containing many goblet cells. For the most part the bulbus analis is lined with an epithelium of two to three layers of columnar cells, the basal of which are cuboidal and have deeply staining nuclei. The protoplasm of the cells is distinctly granular. For a short distance below the beginning of this epithelium are found a few scattered goblet cells similar to those in the epithelium above. The transition between this epithelium and that of the ampulla takes place rather gradually at the ano-rectal line. This line, however, does not correspond in position to the constriction between the bulbus analis and rectal ampulla, as will be shown later.

The epithelium of the bulbus terminalis, or zona intermedia as it will hereafter be called, is composed of five to ten layers of polygonal cells, and differs only from that of the skin of the nates in thickness. The transition between this and that of the zona columnaris is again rather gradual. It forms the linea sinuosa analis. The zona intermedia passes directly over into the zona cutanea, the line of division between the two, the ano-cutaneous line, not being developed at this stage. The muscularis mucosae in the region of the ampulla is distinct but its few fibers dwindle out in the region of the bulbus analis.

Practically the same relations are seen in an embryo of 99 mm. The portion of the circular muscle layer which develops into the internal sphincter shows a slight thickening.

In figure 25 is represented one-half of the rectum of a 110 nun. embryo viewed from the inside. The figure was drawn directly from a dissection with the aid of a magnifier. Rectal columns and sinuses of different sizes show themselves distinctly. At the lower ends of the rectal sinuses can be seen the beginnings of the anal valves. The ano-rectal line cannot be definitely located, but the sinuous anal line is marked by the position of the anal valves. In this specimen the bulbus analis does not seem to be present as a distinct swelling.

Johnson1914 fig01.jpg

Fig. 1 Longitudinal section through the rectum of a human embryo of 88 mm. X 40 diameters. Between the ano-rectal line and the sinuous line is the zona coluumaris lined with stratified columnar epithelium. Below the sinuous line is the zona intermedia. The ano-cutaneous line is not developed at this stage, ext. sph., external sphincter muscle;, intestinal gland; int.sph., internal splimcter muscle; l.ano-rec, ano-rectal line; I. sin., sinuous line; ler.ani., levator ani; m.m., muscularis mucosae; rtcs., rectal sinus; trans. vil., transitory villus of the ampulla recti.

Longitudinal series of sections of embryos of 134 and 140 mm. show the addition of numerous secondary folds. Owing, however, to the advantage which transverse sections give to their study, a description of these folds is reserved for the succeeding stage. The outer coats again deserve special attention. The fibers of the muscularis mucosae are now distinctly seen, and extend a short distance below the beginning of the zona columnaris. The circular muscle coat extends slightly below the inferior Imiit of the same zone and terminates abruptly by becoming slightly thickened. The longitudinal muscle fibers become fewer and fewer when followed down. Some of them extend into the connective tissue septae between the fibers of the external sphincter muscle. Above and to the outside of the external sphincter are seen the fibers of the levator ani.

In a series of transverse sections of the rectum of a well preserved embryo of 135 mm., the pars analis recti presents a condition which, although it contains more secondary folds, is nevertheless greatly similar to that of the above-described embryo of 65 mm. The three primary folds particularly occupj^ the same position and present the same relations. The bulbus analis again appears as a swelling as is shown in the graphic reconstruction presented in figiure 2, A. With respect to its diameter, it is relatively shorter than in the younger stages, although it is actually double the length of the swelling of the 65 mm. embryo. Some idea of its form may be -obtained from the cross sections shown in figure 2. In section 600 there are three main folds of the mucous membrane, one ventral and two lateral. A glance at the two following figures will suffice to show that these folds are continued downward on the swelling of the bulbus analis. In section 600 and above it the mucous membrane presents both glands and villi which are similar to those found in other parts of the large intestine. Intestinal glands are distinctly seen in the figure but the villi are in most places quite low. The epithelium lining this portion of the rectum is simple columnar, composed of cells with a clear ]irotoi)lasm, many of which are goblet cells. At the basal ends of the glands a thin zone of developing muscle fibers, the muscularis mucosae, (0.018 mm. in thickness) is apparent. The muscularis proper is well developed, both layers forming continuous rings around the epithelial tube (together 0.117 mm. thick).

Fig. - 2 A, Reconstruction of the lower part of the rectum of an embryo of 1.3") mm. X ). . Z>, E. F . Successive sections taken at the levels as shown in .1 . X lo. '. hair follicle; tjLitd., intestinal gland; s.col.cp., simple columnar epitheliimi; slr.i-Dl.ep., stratified columnar epithelium; str.sij.ep., stratifie<l scjuamous epithelium.

Between the two layers of the muscularis are seen numerous nerve fibres and few nerve cells enil^eclded in the connective tissue. Separated from the outer longitudinal muscle coat h^y a thin band of connective tissue is seen a third heavy layer of muscle fibers, . the levator ani. Already striations can be made out in these fibers. At the level of section ()()() the fibers of the levator ani are arranged circularly, but the ring is discontinuous both ventrally and dorsally.

In section 650 the villi and the intestinal glands have for the greater part disappeared, although several can be seen in the immediate region of those labelled in the figure. The epithelium lining these is the same as before. In the remainder of the tube the epithelium is stratified, composed of three to four layers of low columnar cells. The protoplasm of these cells is finely granular and stains more intensely than that of the cells in the glands. The transition between this epithelium and that of the ampulla recti is gradual and forms the ano-rectal line. Since section 650 passes through the bulbus analis. it becomes evident that the histologically-described ano-rectal line lies within this swelling and does not correspond in position to the constriction between the bulbus analis and the ampulla recti. Few goblet cells appear in the stratified epithelium below the ano-rectal line but these become fewer and fewer and finally disappear when followed downward. The remaining outward projections of the epithelium in the figure, namely those which are not glands, are secondary outfoldings.

In section 700 (fig. 2, D) glands, villi and intestinal epithelium with its goblet cells, have entirely disappeared. However the stratified columnar epithelium does not pre\'ail throughout for on the summits of the ventral and left primary infoldings, a stratified squamous epithelium has made its appearance. This gradually becomes thicker and more extensive as the anal canal is followed caudally. The transition between this and the stratified columnar epithelium (linea sinuosa analis) is, as pointed out by Herrmann, gradual.

The gland-like protuberances seen in the ventral fold of section 700 are merely the downward projections of the ends of folds, similar to those seen all around the tube. A model of some of these projections is shown in figure 21 . In section 700 the muscularis mucosae has ahnost disappeared but traces of it can be found in tlie form of a few scattered fibers lying (dose to the ei)ithelium, particularly at the bases of the folds.

Between sections 700 and 750 are found the lower limits of the secondary folds. These terminate as downward projections in the form of tubules. Those belonging to the left ventral outfolding are represented in figure 21. These tubular structures are lined with a cuboidal epithelium of two to three layers of cells and take on very much the appearance of glands. No evidence that the epithelium is a glandular one, however, was obtainable anywhere. Some of the tubules, about seven in number, turn outward and come in contact with the internal sphincter muscle. Two others pierce the internal sphincter and lie between it and the outer longitudinal layer of muscle, one of which is shown in the figure. It is this type of tubule which Herrmann describes under the term 'intramuscular sinus.

The lining epithelium of section 750 (fig. 2, E) is entirely stratifed squamous, composed of seven to ten layers of cells. It presents a few thickenings of the basal layer of cells which mark the beginning of the hair follicles. It would seem from this that this section was near the border line between the zona intermedia and the zona cutanea. The superficial one to three layers of squamous cells take the stain (orange G) more intensely and their nuclei are smaller and more deeply staining than those of the remaining layers, marking the beginning of a stratum corneum.

In the section 800 (hg. 2, F) the zona cutanea proper is reached. Here the epithelium is slightly thicker than above, but its chief characteristic is the i:)resence of numerous hair follicles. The irregularities of the epithelium are skin folds which extend radially from the anal opening. Testut ('95) refers to these under the term plis radies de I'anus" and Symington ('12) as the "anal skin folds. "

The longitudinal section of the rectum of an embryo of 1S7 mm. represented in figure 3 shows well the topographical relations of the various parts and structures of this region. The ampulla recti is lined with the simple columnar epithelium which for the most part is made up of large goblet cells. The villi are quite low but everywhere in evidence. In passing aborally into the pars analis recti the glands become further spread apart, the goblet cells become fewer and fewer and the epithelium gradually changes over into a stratified columnar type. Although the histological ano-rectal line is not so sharply marked in this section as in many others, nevertheless, it is clear that few goblet cells are present in the upper part of the zona columnaris.

Fig. 3 Longitudinal section through the pars analis recti. From a hunum embryo of 1S7 mm. ampulla, ampulla recti; circ.m., and long.m., circular and longitudinal layers of the muscularis; foll.pili, hair follicle;, intestinal gland; gl.intrm., intramuscular gland; gl.seb., sebaceous gland; l.ano-cut., anocutaneous line; l.ano-rec., ano-rectal line; l.sin., sinuous line; m.lev.ani., levator ani muscle; exl.sph., external sphincter muscle of the anus; int.spJi., internal sphincter muscle of the anus; irans.vil., transitory villus of the ampulla.

The bulbus analis presents numerous folds as in the former embryos but these are not seen in the figui'e, owing to the fact that the section passed directly through one of the large infoldings of the epithelium. Extending into the connective tissue subjacent to the epithelium are to be found here and there through out the series, long tubular projections of the epithelium. In some cases they extend only as far as the internal sphincter while in others they pierce this muscular layer. One of them is shown in figure 3, gl. iutrm. It extends in an outward and oral direction and divides into three or four branches, only one of which penetrates the muscularis. These glands are lined with a cuboidal epithelium of two to three layers of cells. The inner layer consists of cubical cells with distinct boundaries, a granular protoplasm and rounded nuclei. The outer cells are usually small, they have no distinct boundaries, and their nuclei are smaller and more deeply staining. For the most part the intramuscular tubules of this embryo project upward (orally) but not always, for few were seen extending outwards and downwards. The transition from the stratified columnar epithelium of the zona columnaris to the stratified squamous epithelium of the zona intermedia takes place gradually, forming the sinuous anal line.

The zona intermedia presents a thickened region of the epithelium. The stratified squamous epithelium is from ten to fourteen layers of cells thick in the upper part of this zone, but in the lower part it gradually becomes thinner. The basal two layers of cells are granular, and have large round and ovtxl nuclei. The middle layers of cells are vesicular and polygonal in shape. They are made up of a faintly staining, finely granular protoplasm, and contain small but deeply staining irregular nuclei. The top two or three layers of cells are flattened and in the lower part of the zone, appear cornified.

The ano-cutaneoiis line is marked by the beginning of the first hair follicles. Beyond this line is the zona cutanea. The hair follicles are accompanied by beginning sebaceous glands. Still further out are found the beginnings of a few scattered sweat glands which undoubtedly represent the “circum-anal glands" of Gay. A few dermal papillae are also present in this zone. The marked difference between this stage and the stages of 135 mm. and 140 mm. in regard to the disposition of hair follicles can only be explained as individual variations.

The muscularis mucosa (fig. 3) is distinctly seen in the region of the Lieberkuhn glands and a few fibers can be traced down into the zona columnaris. The thickening of the circular muscle coat to form the internal sphincter begins in the lower portion of the ampulla and extends down into the region of the zona intermedia a distance of 3.5 to 4.5 mm.

The external sphincter is placed below and to the outside of the internal sphincter and is again separated into numerous bundles of fibers by connective tissue septae. The fibers of the longitudinal muscle layer seem to terminate just before reaching the external sphincter b}' ending in the connective tissue septae. Above and to the outside of the external sphincter is the levator ani.

Fig. 20 Side view of reconstruction of the epithelium of the pars analis recti of an embryo of 240 mm. x6

A model of the pars analis recti of an embryo of 240 mm is represented in figures 19 and 20. The ampulla is shown above as cut off at a point where it has about reached its greatest width. It is separated from the bulbiis analis by a constricted zone which, as determined from the sections of this series, lies a little above the ano-rectal line. This portion of the rectum (ampulla) presents only intestinal glands, \'illi having entirely disappeared. Owing, however, to the difficulty met with in modeling the glands at the magnification used (24 diameters) no attempt has been made to represent them. All the folds of the pars analis recti have been modelled. The primary folds can be best seen in cross sections of this region but they are distinguishable in the model. The posterior, right, and left primary outfoldings are present as in the youngest stages, and the left, as seen in the figures, passes down onto the aiitcrioi' hordci' of the fhittciKHl zona intermedia. The posterior i-iinai'y fold passes into the posterior border of the same, while the right fold terminates on the side of the zona intermedia. The secondary folds are more numerous than in the above described stages. Of these there are about twelve on the left primary fold, twenty-two on the right, and about twenty-six on the left, about sixty in all.

Extending outward from this region are to be seen the intramuscular glands. These are more highly developed in the lower portions than abo\e. Some few which did not lend themselves easily to modelling are not shown in the figures. The intramuscular glands extend out from the stratified columnar epithelium of the zona columnaris. Some of them are solid cords of cells throughout, others have distinct lumens, while still others have lumens only in certain portions. Those with lumens are lined by an epithelium of two to three layers of cells, the uppermost of which are in many places columnar and suggestive of secretory cells.

The zona intermedia, owing to distention caused by the presence of meconium in this region, is not so flattened as in the preceding stages. The larger folds of the zona columnaris are prolonged down onto this region and give it an irregular appearance. Several of these folds are directly continuous with the skin folds of the zona cutanea. The zona intermedia is lined with a stratified squamous epithelium of from six to fifteen layers of cells, the uppermost of which show distinct cornification. The epithelium is thickest between the infoldings (0.07 mm.) and thinnest on their tops (0.32 mm). AMth the exception of one sebaceous gland (without a hair shaft) which is present high up on the right side of the zona intermedia, no other glands or follicles are present in this region. A considerable distance further down hair follicles and sebaceous glands appear and mark the beginning of the zona cutanea. The zona cutanea is lined with a stratified squamous epithelium of 0.03 to 0.30 mm. thick and is composed of five to ten layers of cells. It is distinctly cornified and shows numerous papillae, hair follicles, and sebaceous glantls.

In another embryo of about the same age, (length 245 mm.) a few noteworthy differences were observed. The ampulla and pars analis were both distended with meconium. The series of sections includes the whole of the zona cutanea, the zona intermedia, but only a portion of the zona columnaris. This latter, while its lumen is relatively large, shows distinct folds of its mucous membrane quite similar to those of the other stages described.

Fig. 4 Portion of a cross section of the pars analis recti of a human embryo of 24o mm. X 30. Between .r and x' is a rectal sinus, lined with a stratified columnar epithelium. It belongs to the zona columnaris. The remainder of the surface epithelium is stratified squamous, and belongs to the zona intermedia. circ.m., and long.m.. circular and longitudinal layers of the muscularis; ^fLr/i^rw., intramuscular gland ; ni.ler.atiiAcvaior ani muscle; rcc.cul.. rectal column; x and x', sinuous line.

The epithelium lining the tube of the uppermost section of the series is for the most part stratified columnar, although it is stratified squamous on the tops of the larger infoldings and again in few of the outfoldings between them. Unlike in the preceding stages the six distinct intramuscular glands found in this series arise from the upper portion of the stratified squamous epithelium, that is, from the zona intermedia. All are distinctly tubular and have distinct lumens throughout. For a short distance they are lined with a stratified squamous epithelium but this soon passes over into a stratified columnar which in the branches becomes cuboidal. In all these glands evidences of a secretory epithelium are apparent. One gland, of which a model is shown in figure 23, extends more than half way through the longitudinal muscle coat, giving off at various levels several branches. The primary duct of the gland courses in an outward and downward direction until it reaches the internal sphincter muscle. It then assumes a horizontal direction and in the substance of the internal sphincter, presents a flattened ampulla-like dilation. From this ampulla branches arise which extend on through the internal sphincter and terminate in the connective tissue between the muscle layers. The gland labelled B in the same figure represents a simple tubular type which extends only to the internal sphincter but does not pierce it. Another simple gland is shown in figure 22. It has a somewhat ampullated ending at the outer border of the internal sphincter. Several small knob-like protuberances mark what seem to be acini. They are lined with a cuboidal epithelium which is distinctly of a secretory character.

The zona intermedia is lined with a thick stratified squamous epithelium which is cornified. This is thrown into a few large folds which are directly continuous with the larger folds of the zona columnaris above and with the anal skin folds below. The zona cutanea presents no special features.

The external sphincter muscle is of interest in that it gives off vertical columns of striated muscle which extend up into some of the larger folds for varying distances. Likewise small bundles of smooth muscle fibers pass horizontally or obliquely toward the epithelium and also turn upward into the large mucosal folds. Both types of muscle fibers can be traced up into the zona columnaris, where they terminate. No evidence of such fibers are apparent in this region of the previously-described embryos.

The rectum at birth has been studied from five different specimens. Of these series 10.8 and 10.23 were cut sagittally, series 10.20, 10.21, and 10.22 were cut in cross sections.

The form of the rectum is best seen in the latter two series. Neither of these present any notable differences in form from that of the 240 mm. embryo described above. As shown in a model of series 10.22 (not figured) the primary and secondary folds correspond very closely with those shown in figures 10 and 20. The lumen and size of the tube, however, is somewhat smaller, owing undoubtedly to less distention. Series 10.20 presents what appears to be a flattened and distorted condition of the whole pars analis recti. However, as the preservation of this specimen is poor, a description of it will be omitted.

The form of series 10.21 is shown in figure 5. In 5 is represented a section through the lower portion of the ampulla showing true intestinal glands and no villi. In C is seen a section through the zona columnaris. The three primary and numerous secondary folds are quite distinct. Section D is through the upper part of the zona intermedia. Several intramuscular glands, which arise from the zona columnaris higher up, are seen just outside the epithelial tube. In E is shown a section taken through the lower portion of the zona intermedia. The sharp irregular folds have given way to larger and more rounded ones. The three primary folds terminate in this zone in a manner as described for the preceding stages. Section F shows numerous sebaceous glands and hair follicles, and is therefore through the zona cutanea.

The relations of the different zones is well shown in sagittal series 10.8. The zona columnaris, like in the preceding stages, is lined with a stratified columnar epithelium. The sinuous anal line is distinctly marked by a sharp transition from the stratified columnar epithelium to the stratified squamous epithelium. The epithelium of the zona intermedia is much thicker than that of the zona columnaris and shows only a slight amount of cornification. This, however, increases when followed downward so that at the ano-cutaneous line the stratum corneum is as thick as that of the zona cutanea. The description of the zona cutanee lisse" of Robin and Cadiat is in agreement with what is found in the zona intermedia at birth. It is a smooth zone, contains no hair follicles, sebaceous or sweat glands and only a few dermal papillae.

Fig. 5 A, reconstruction of the lower part of the rectum of a full term fetusX 4. 5, C, D, E, F. Succepsive sections of the rectum taken at the levels as shown in A. X 8. foll.pili., hair follicle;, intestinal gland; gl.inirm.', intramuscular gland; gl.seh., sebaceous gland; s.col.ep., simple columnar epithelium; str.col.ep., stratified columnar epithelium; sir.sq.ep., stratified squamous epithelium.


These latter are found only in the lower part of the zone. The ano-cutaneous line is arbitrarily placed at the point where the hair follicles and sebaceous glands begin to appear. A short distance beyond this point are found numerous sweat glands, which represent the circumanal glands of Gay.

Intramuscular glands were found in series 10.20, 10.21 and 10.22. In all three series they arise from the bottoms of the outfoldings of the zona columnaris. In structure they are similar to those seen at 240 mm. Although evidences of secretory cells are rare in these glands at birth, few were seen in different places.

No intramuscular glands were found in series 10.8 and 10.23 but as these series only contained a few sections each, it is not improbable that the glands were present in the specimens but that none happened to be cut through in these sections.

No marked differences were observed in the outer coats of the rectum. In 10.22 distinct but small bundles of striated muscle fibers were seen extending up from the external sphincter muscle into the folds of the zona columnaris. In some instances these fibers are closely grouped together; in others, they are more widely separated. About six groups in all were present, containing from ten to twenty-five fibers each. In none of the other series were similar fibers found.

In all the rectums at birth the muscularis mucosae is distinct in the region of the ampulla but cannot be distinctly traced down as muscle columns in the large mucosal folds. As in the preceding stages, a few fibers of this muscle layer can be traced below the ano-rectal line into the zona columnaris. These lie quite close to the epithelium and in the lower part of the zona columnaris become lost in the connective tissue.

Plicae transversales recti

The development of the plicae transversales recti has been described by Baur ('60). The few observations given below are essentially in accordance with those of Baur. Apparently these folds develop in a manner quite similar to the plicae circulares of the small intestine and the plicae semilunares of the large intestine, that is, by a gradual infolding of the mucous membrane.

In an embryo of 70 mm. a careful macroscopic examination of the rectal wall showed no evidence of transverse folds. At 99 mm., however, two small folds are perceptible in the lower portion of the ampulla. At 140 mm. the transverse folds, which are quite distinct, are arranged somewhat obliquely around the wall of the ampulla recti. Three such folds are present, placed at distances of 10 to 13 mm., 15 to 18 mm., and 20 to 22 mm. above the anal opening.

In an embryo of 187 mm. two small folds are present on the right side at distances of 20 mm. and 25 mm. above the anus, while a third larger fold is present on the left side, 30 mm. above the anal opening.

Out of four fetuses at birth the plicae transversales are present in three. In the first case the lowest fold is on the left side 30 mm. above the anal opening. Above this fold are two others both on the right side at distances 40 mm. and 50 mm. above the anus. As seen in figure 24, these folds extend around onto the left side for a short distance. In the second fetus at birth, only two folds are present, the lower being on the left side, while the upper is on the right. These lie at distances of 35 mm. and 45 mm. above the anus respectively. The third fetus likewise has two folds, but the lower is on the right side and the higher on the left, at distances of 30 mm. and 40 mm. above the anus. In the fourth fetus the plicae are entirely absent. The ampulla, however, is very much distended with meconium, which probably in part accounted for their absence.

These observations are not entirely in accordance with those of Otis ('87) who found that when two folds were present the lowest was on the right side and the upper on the left, while when three folds were present, the lowest was on the left side.

With regard to the direction of the folds it may be said that in practically no case did the folds run directly transverse to the long axis of the rectum. Usually they were placed somewhat obliquely. However, in no instance did they have a distinct spiral arrangement around the wall of the rectum, after the manner described by Vance.

The relation of the developing rectum to the vertebral column

Along with the development and descent of the various structures and organs of the pelvis, there take place corresponding changes in the position of the rectum. These changes are particularly noticable in case of the pars analis recti which, in its early stages, lies at a higher level and is relatively greater in its extent than in the later stages. Whereas in the adult the first portion of the rectum begins at the level of the third sacral vertebra (by definition) and lies along the concavity of the remainder of the sacrum and coccyx, in very early stages this portion of the rectum is found above the third sacral vertebra. Likewise the pars analis recti which in the adult is an inch or more in front of and below the tip of the coccyx, early is found occupying a position extending from the third sacral vertebra to the tip of the coccyx. The determination of such relations has only been made possible through the existence of the bulbus analis, which as has been shown, is present as a swelling throughout stages up to birth, and which forms in a large part the zona columnaris.

In an embryo of 16 mm. (H. 133) the spindle-shaped bulbus analis lies along the concavity of the sacrum. Its upper limit lies on a level with the third or fourth sacral vertebra. The anus is found in the neighborhood of the second or third coccygeal vertebra. Such levels, however, can only be approximately determined. This is because the epithelial tube of the rectum does not lie directly against the bodies of the vertebra, and because of the great curvature of the body in this region. The long axis of the embryo in this region, therefore, is a much curved line.

In figure 6, A are seen the relations which exist in an embryo of 28.8 mm. (H.E.C. 1598). The upper portion of the bulbus analis a^aiii lies at about the level of the third or fourth sacral vertebra, while the anal opening lies at about the same level as the tip of the coccyx.

In embryos of 31 mm. (H. 57) and 35 mm. (H. 51) the bulbus analis reaches only as high as the fifth sacral vertebra, while the anal opening presents the same relations as in the preceding stage.

In an embryo of 50 mm. (H. 115, fig. 6, B) the bulbus analis is relatively much shorter. Its upper limit now lies on a level with the second or third coccygeal vertebra, while the anal opening is found on about the same level as the tip of the coccyx. At 140 mm. the curvature of the sacrum and coccyx is less than before, and the bulbus analis lies entirely below the tip of the coccyx. At birth practically the adult relations are met with (fig. 24).

Fig. () Sagittal section through the anal regions of human embryos. A, 28.8 mm., (H.E.C. 1598) and B, 50 mm. (H. 115). X 6. all., allantois; anip.r., ampulla recti; bul.a., bulbus analis; bul.l., bulbus terminalis; C.I to IV, coccygeal vertebrae; ex.sph., external sphincter muscle; Icv.a., levator ani muscle; per.c, peritoneal cavity; S.I. to V., sacral vertebrae; sym.p., symphysis pubis;^., zona intermedia.

The limit between the entoderm and ectoderm

Retterer ('90) in a study of the early stages of embryos of the sheep, pig, and rabbit, concluded that the mucous membrane of the anal region is derived directly from the ectoderm and the underlying connective tissue. Herrmann ('80) likewise believed that the whole of the pars analis recti is derived from the ectoderm, the line of separation between the ectoderm and entoderm being represented by the ano-rectal Une. His reason for maintaining this view was because of the change in the character of the epithelium at this point. The few isolated intestinal glands Cglandes erratiques') and goblet cells he regards as fragments of entodermic epithelium which have descended into the ectoderm of the anal region.

After the breaking down of the anal membrane, there is no apparent line of demarcation between the entoderm and the ectoderm. However, when the cloacal or anal membranes are present, the junction of the two germ layers is definitely marked. This junction lies just below the bulbus terminalis. Since both the bulbus analis and the bulbus terminalis lie above the anal membrane they are composed of entoderm and it is evident, therefore, that the derivatives of these, the zona columnaris and the zona intermedia of the pars analis recti, are of entodermal origin. The exact line of demarcation in the adult cannot be definitely located, but it is undoubtedly somewhere in the neighborhood of the linea ano-cutanea.

Discussion and Summary

A study of a few young stages of the human embryo confirmed the results of Keibel and Pohlman in that the cloaca in the human embryo is never open to the outside, and that division of the cloaca into urogenital sinus and rectum takes place in embryos of about 16 mm in length. After separation has taken place, the posterior portion of the cloacal membrane persists as the anal membrane and occludes the rectum at its lower extremity. It is present for some little time and exists in the form of a few irregular cells similar to those of the wall of the anus. This was last observed in an embryo of 22.8 mm. An exception to this is found in the 16 mm embryo, in which the anal canal is already open to the outside. Keibel ('08), however, shows that ordinarily the anus is closed in embryos as old as 26 mm., while Broman ('11) states that its lumen becomes patent in embryos of about 33 mm.

In embryos of 7 and 10 mm. the rectal tube presents a spindleshaped swelling. It is apparent as a swelling throughout stages up to birth, although its form changes greatly At first it is elongated. It increases in size proportionally up to the 37 mm. stage. Little or no increase in length occurs throughout stages 42, 44.3 and 65 mm., although the increase in its cross diameter is considerable. From this stage on there is an increase in the length of the swelling, but the direction of greatest growth is transversely. Whereas in the earlier stages its length is several times its diameter, at birth the diameter slightly exceeds its length.

In embryos of 13.6 and 16 mm. there appears below the abovedescribed spindle-shaped swelling a second swelling. This is much shorter, and not so well marked as the upper. It exists as a swelling only for a short period of embryonic life. In an embryo of 29 mm. the swelling has largely disappeared, while in embryos of 30 mm. and over it is represented as a narrow slitlike cavity.

Keibel and Lewis have described these swellings of the rectal tube in corresponding stages of development. The upper of the two swellings, which I have termed the 'bulbus analis,' occupies a position in the embryo which corresponds quite closely to that occupied by the ampulla recti of the adult. However, as has been shown, it does not form the adult rectal ampulla. The walls of the embryonic swelling become invaginated and form numerous longitudinal .folds and ridges. The study of these folds throughout successive stages of development show that they are the rectal columns. As these are found principally within the zona columnaris of the pars analis recti, it follows that the spindle-shaped swelling of the embryo becomes in large part the zona columnaris of the adult. The upper portion of the bulbus analis, however, lies above the ano-rectal line, and from the standpoint of histology, belongs to the ampulla recti. The lower swelling, which I have termed the 'bulbus terminalis,' develops from the dorsal portion of the cloaca which Tourneux has called the 'vestibule anal.' It is limited above by the constriction between it and the bulbus analis, and below by the anal membrane. It forms the lower portion of the pars analis recti, namely the zona intermedia. It cannot be definitely said, however, in regard to either of the two swellings that their boundaries correspond absolutely to the boundaries of the two above-named zones.

The first evidence of the development of folds in the bulbus analis was found in an embryo of 22.8 mm. At 30 mm, three distinct folds are present, the outfoldings of the epithelium occupying positions posteriorly, and on the right and left sides. These three primary folds are present throughout stages up to birth. Whether they are present in post-natal rectums has not been determined. They extend throughout the whole length of the bulbus analis. Below they terminate by ending on the zona intermedia. This, in stages up to about 30 mm., is flattened ventro-dorsally. The right and left primary folds become directly continuous with the right and left borders of the bulbus terminalis respectively. In stages of 31 mm. and over, the bulbus terminalis or zona intermedia is flattened laterally. This band-like portion of the rectum, therefore, either undergoes a rapid change in its form or in its position. Just what happens at this stage was not clearly brought out by the embryos examined. From the position occupied by the left fold, in the later stages, a twisting to the right through an angle of 90 degrees seems to have taken place. However, from the arrangement of the other two primary folds and the tissues in the immediate neighborhood of epithelial tube, it is not probable that any such twisting has gone on.

In all the later stages of development the constancy with which the primary folds are found is very striking. Moreover, these folds terminate at their lower extremites in a similar manner .in almost all stages examined. The outfolding on the left side passes up onto the ventral border of the laterally flattened zona intermedia; the posterior fold extends directly into the dorsal border of the same ; while the right fold extends as far as the zona intermedia and terminates on its right side, about half way between its ventral and dorsal borders.

In an embryo of 37 mm. secondary folds begin to appear on the bulbus analis. These are longitudinal folds similar to, but smaller than, the primary folds. They develop rapidly and soon obscure the primary folds. At 54 nun. the secondary folds are quite numerous. Most of them are formed in an embryo of 135 mm., but an embryo of 240 mm. shows some increase in their numbers. Apparently none are formed after this stage.

The significance of these longitudinal folds of the bulbus analis cannot be questioned. The infoldings of the mucosa form the columnae rectales (columns of Morgagni). When viewed from the inside (fig. 25) the primary folds are not distinguishable and only the larger columns are apparent. Numerous small secondary folds lie at the bottom of the outfoldings or sinuses. The number of such vertical folds or columns is large, there being as many as 60 in a 240 mm. embryo. The smaller of these folds, so far as general structure is concerned, do not dift'er from the larger columns and should, therefore, be considered as the equivalents of the usually-described rectal column.

The rectal sinuses (sinus rectales) of the adult, as they are usually described, are found at the lower extremities of the intercolumnar clefts. An examination of models shows that such pockets are present as the lower portions of the outfoldings, which in places extend down below the general level of the mouth or opening of the cleft.

The anal valves are found at the lower limits of the folds. In the embryo these do not have so much the appearance of the aortic valves as is usually figured for the adult, but are narrower and thicker. It seems reasonable to the author that distention must play an important part, in the further formation of the valves and sinuses. The great variation in number, size, and and shape in the same and in difTerent individuals, and the extent to which the pars analis later becomes distended, would seem to be evidence in support of this view.

The histology of the rectum throughout the different periods of development may next be briefly reviewed and summarized. The first part of the rectum including the ampulla is similar in its development to the colon as has been previously described (Johnson '13).

In the earlier stages of development the pars analis recti is lined by an epithelium composed of two to three layers of low columnar cells. This epithelium is similar to that found in other parts of the digestive tube in its early stages. Differentiation was first noted in an embryo of 55 mm. But few changes take place from this time until birth. The following description, although taken largely from an embryo of 240 mm., will hold good for any of the later stages.

The pars analis recti is the region in which takes place the transition between the mucosa of the digestive tube and the skin. This transition does not take place gradually but in three separate steps, thus forming three distinct superimposed zones, the zona columnaris, the zona intermedia, and the zona cutanea. The last of these zones, however, does not belong to the pars analis, properly speaking, but to the outer skin.

The zona columnaris is the region of the rectal columns, but these, however, are not always confined to this zone alone. They may extend up into the first part of the rectum for a short distance, and they may also be continuous with the anal skin folds which extend inward and upward from below. The zona columnaris is lined by a stratified columnar epithelium of from two to three layers of cells. The transition from the simple columnar to the stratified columnar epithelium takes place rather gradually. It forms the linea ano-rectale. In the upper part of the zone are to be found usually a few intestinal glands and goblet cells.

In the lower part of the zona columnaris, arising from the rectal sinuses, are found tubular gland-like structures. These may be of a simple tubular form lying completely within the submucosa, or they may be branched tubules which pierce the underlying muscle layers. The latter type are known as the intramuscular glands. There are seldom more than six or eight of these in any one rectum. The main ducts of the glands extend outward, and usually downwards, and penetrate the internal sphincter muscle. Here an ampulla-like swelling is usually met with. Extending beyond this ampulla are several tubular branches which continue through the internal sphincter and end blindly in the intramuscular connective tissue. Occasionally a tubule is seen piercing the longitudinal muscle layer. Around the terminations of the tubules which sometimes take on the appearance of acini, is to be found a small amount of lymphoid tissue. The epithelium lining the glands is made up of several layers of polygonal cells in the main ducts, but in the ampullae and branches it is composed of one to two layers of cuboidal cells. It is claimed that evidences of secretory cells are wanting in the adult, but in the fetus and at birth they are present.

This summary, Braun tabulates the epithelia of the zona columnaris as follows :

(a) Einfaches Cylinderepithel findet sich in dem proximalen Teil der Columnen ; in dem proximalen Teil der Sinus ; in alien Lieberkühnschen Drüsen; am unteren, blinden Ende der rohrenformigen Anhange der Ausbuchtungen der Sinus. (Simple cylindrical epithelium is found in the proximal part of the column; in the proximal part of the sinus; in all the Lieberkühn's glands; At the lower, blind end of the tube-shaped appendages of the bulges of the sinus.)

(b) Geschichtetes Cylinderepithel findet sich in dem distalen Abschnitte der Sinus; auf den die Sinus begrenzenden Flachen der Columnen; in den sekundaren Ausbuchtungen der Sinus; in den Ausführungsgangen der rohrenformigen Anhange der Ausbuchtungen. (Layered cylindrical epithelium is found in the distal portion of the sinus; on the sinusoid surfaces of the columns; in the secondary bulges of the sinus; in the embodiments of the tubular appendages of the bulges.)

(c) Geschichtetes Plattenepithel (polyedrisches Epithel) findet sich auf der Hohe der Columnen in ihrem distalen Abschnitt. (Layered squamous epithelium (polyhedral epithelium) is found on the top of the column in its distal portion.)

The results of my own work regarding the epithelium of the zona columnaris are in accordance with the above tabulation, but I must also add that:

(d) Stratified cuboidal epithelium is found in the larger ducts of the intramuscular glands.

(e) Simple cuboidal epithelium is found in the branches of the intramuscular glands.

The zone intermedia is lined by a stratified squamous epithelium. This is composed of several layers of polygonal cells forming a thicker layer than the epidermis of the skin. Dermal papillae are present, but hairs and sweat glands are absent. In the lower part of this zone may be found a few isolated sebaceous glands without hairs, and a slight amount of cornification of the epithelium. The transition between the epithelium of this zone and that of the zona columnaris is rather abrupt. It lies at the level of the anal valves, but in between the valves it extends upward on the summits of the rectal columns. It thus forms a zigzag line, which is known as the linea sinuosa analis (ano-cutaneous line of Herrmann). At its lower limit the zona intermedia gradually goes over into the skin. The transition here forms the true linea ano-cutanea, but it is not well marked. It has been defined as the place where the first hair follicles appear. The skin in the immediate neighborhood of the anus is known as the zona cutanea. Sweat glands, the circum-anal glands of Gay, are found only in this zone.

The muscularis mucosae in the first part of the rectum is similar to that of the colon. It is said to extend downward in the form of muscle columns into the rectal columns. In the embryos I have examined nothing in the way of distinct muscle columns were to be found. The muscularis mucosae extends into the zona columnaris as a thin sheet of fibers lying quite close to the epithelium. The fibers forming this sheet soon disappear, however. In two stages, 240 mm. and at birth, small bundles of voluntary striated muscle fibers are present in the larger rectal columns. These are composed of a number of fibers which arise from the external sphincter muscle turned obliquely toward the submucosa and then upward into the columns. A few fibers of the internal sphincter join some of these columns in the 240 mm. embryo.

The submucosa, while at first composed of mesenchyma, later becomes fibrous. It contains numerous nerve fibers and blood ves.sels, and Pacinian corpuscles as described by Pilliet ('92).

The muscularis of the rectum is the downward continuation of that of the colon. Both layers form, however, continuous sheaths around the rectum. The circular was first seen in an embryo of 16 mm., while the longitudinal appeared at 17 mm. The circular layer presents, in the region of the pars analis recti, a thickening, the sphincter ani internus. This does not become apparent until relatively late embryonic life (99 mm. embryo). The longitudinal muscle coat terminates below, after the manner described by Beraud ('58) and Roux ('81), by a spreading out of its fibers. These end in small connective tissue fibers, which, continuing downward, spread out fan-shaped, and as septae, divide up the muscle bundles of the external sphincter.

The external sphincter appears quite early. It was first definitely made out in an embryo of 22.8 mm. According to Otis ('05) the external sphincter arises from the mesenchyma within the anal papillae (slight elevations on the outside of the anus). He detects the anlagen of the fibers of this muscle in an embryo of 12.5 mm.

Attention should be made regarding the extent and relations of the various muscles to the different parts of the pars analis recti. In the early stages, both the circular and longitudinal layers of the muscularis terminate at the constriction between the bulbus analis and the bulbus terminalis. In the later embryonic stages the circular muscle extends well into the region of the zona intermedia, while the longitudinal layer extending not quite so far down, terminates just above the external sphincter muscle. The external sphincter muscle surrounds the middle part of the zona intermedia.

The development of the plicae transversales recti may be summarized in few words. They apparently develop after the manner of the folds of the large and small intestines, that is, by a gradual infolding of the mucous membrane. They were first seen in an embryo of 99 mm. From this stage on they become more pronounced. Gradually they spread further and further apart with the growth of the rectum as a whole.

A study of the developmental topography of the pars analis recti shows that it forms a relatively much greater portion of the digestive tube in the embryo than in the adult. Its growth in length, therefore, is proportionally less than its growth in diameter. With this relative shortening, the pars analis recti gradually descends in the pelvis. Whereas in the early stages the whole of the pars analis recti lies between the third sacral vertebra and the tip of the coccyx, at birth it lies completely below the tip of the coccyx.

In the early stages of the embryo the meeting point of the entoderm and the ectoderm lies at the lower end of the bulbus terminalis at the anal membrane. Since it has been shown that the bulbus terminalis develops into the zona intermedia, it follows that at birth and in the adult the limit between the two germ layers must lie somewhere near the lower boundary of this zone, that is, near the ano-cutaneous line.


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Plate 1

7 to 10 Wax reconstructions of the opitheliiim of the pars analis recti.

Fig. 7 Human embryo of 22.8 mm. H. E.G., 871. X 3G. 6. rt. , bulbus analis; fl.fcL anal ectoderm; a.m., position of anal membrane; !>.(., bulbus terminalis.

Fig. 8 Human embryo of 30 mm. H.E.C., 913. X 36.

Fig. 9 Human embryo of 29 mm. H.E.C., 914. X 3(3.

Fig. 10 Human embryo of 37 nun. II. E.G., 820. X 36.

Plate 2

Fig. 11 to 14 Side views of the same. Abbreviations as in figure

Plate 3

15 and I6 Wax reconstructions of the epithelium of the pars analis recti.

Fig. 15 Human embryo of 44.3 mm. H.E.C. 1611 . X 36.

Fig. 16 Human embryo of 65 nun. H. 55. X 36.

Plate 4

Fig. 17 and 18 Side views of the same.

Plate 5

Fig. 19 Reconstruction of the epithelium of the pars analis recti of an embryo of 240 mm. X 6.

Plate 6

Johnson1914 plate06.jpg

Fig. 20 Side view of reconstruction of the epithelium of the pars analis recti of an embryo of 240 mm. X6

Plate 7

Johnson1914 plate07.jpg

Fig. 21 Lower portion of the primary fold of a human embryo of 135 mm. X 72. gl.intrm., intramuscular gland; sc.f., secondary fold; tub., tubules; x, marks the point where the gland penetrates the internal sphincter muscle.

Fig. 22 Intramuscular gland. Human embryo of 245 mm. X 72. a., acinouslike ending; ep.w., epithelial wall.

Fig. 23 Branched intramuscular gland. Human embryo of 245 mm. X 72. a., acinous-like termination; amp., ampulla of gland; br., branch; ep.w., epithelial wall.

Fig. 24 Sagittal section through the pelvis at birth. X 1. b.w., body wall; bid., bladder; C.I., 1st coccygeal vertebra; ext.sph., external sphincter muscle; La., levator ani muscle;, plica transversalis recti; rec.a., rectal ampulla; S.I., 1st sacral vertebra; sym.p., symphysis pubis; z.col., zona columnaris;, zona intermedia.

Fig. 25 Sagittal section through the lower part of the rectum. X 6. a.v., anal valve; r.c, rectal column; rec.a., rectal ampulla; sin., rectal sinus; z.col., zona columnaris;, zona intermedia.

Cite this page: Hill, M.A. 2017 Embryology Paper - The development of the rectum in the human embryo. Retrieved December 18, 2017, from

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