The Anorectal Myenteric Plexus: Its Relation to Hypoganglionosis of the Colon
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1 The Anorectal Myenteric Plexus: Its Relation to Hypoganglionosis of the Colon ARTHUR G. WEINBERG, M.D. The Children's Hospital of Akron and Case-Western Reserve University School of Medicine, Akron, Ohio ABSTRACT Weinberg, Arthur G.: The anorectal myenteric plexus: its relation to hypoganglionosis of the colon. Amer. J. Clin. Path. 54: , To define the anatomy of the distal anorectal myenteric plexus more clearly, specimens from this region obtained at autopsy from 25 patients ranging from premature infants to children six years of age were studied. A distal zone characterized by a paucity of ganglion cells and the presence of nonmyelinated nerve trunks was identified. This zone is similar in appearance to areas of hypoganglionosis occurring in association with various forms of Hirschsprung's disease. The extent of this zone is quite variable but tends to increase slightly with age. It may extend up to 2.5 cm. proximal to Hilton's line or 2 cm. proximal to the pectinate line. In performing a rectal biopsy for the diagnosis of Hirschsprung's disease care must be taken to remain proximal to this zone. Interpretation of the rectal biopsy should not rest solely upon the identification of ganglion cells but must include an evaluation of the entire morphology of the myenteric plexus. IN 1948 Whitehouse and Kernohan 14 published the first detailed observations concerning the absence of ganglion cells from the myenteric plexus in the distal narrowed colonic segment in Hirschsprung's disease (congenital agnnglionic megacolon). This abnormality is now recognized as forming the basic morphologic feature of this disease. Based upon this fact, biopsy of the rectum was introduced by Swenson 12 in 1955 as a means of evaluating plexus structure. It has since played and continues to play a definitive role in the diagnosis of Hirschsprung's disease. Several authors, including Swenson, 2 ' 3 > 1S have commented upon the normal occurrence of a sparsity of ganglion cells in the Received November 20, 1969; accepted tor publication January Supported in part, by the Kramer-All en Fund. Dr. Weinberg's present address is Children's Medical Center, Dallas, Texas immediate region of the internal sphincter, but until very recently little has been written concerning the exact extent of this anatomic variation. We have recently encountered a number of rectal biopsy specimens in which the numbers of ganglion cells in the myenteric plexuses appeared reduced. In addition, nerve trunks were present within the plexuses, producing a pattern of hypoganglionosis. This prompted us to examine more closely the normal microscopic anatomy of the distal myenteric plexus in the anorectum. Methods The rectum and anus including the perianal skin were removed intact at autopsy from each of 25 consecutive patients dying at the Children's Hospital of Akron from causes unrelated to the gastrointestinal tract. The specimens were divided into
2 638 WEINBERG AJ.C.H. Vol. 54 paraffin. Single sections 6 p in thickness were cut from each block, stained with hematoxylin and eosin, and mounted on glass slides. Utilizing a standard eyepiece micrometer the following measurements were recorded in millimeters: (A) distal margin of the internal sphincter (Hilton's line) to the squamocolumnar junction (pectinate line); (B) Hilton's line to the first identifiable ganglion cell; (C) Hilton's line to normal-appearing myenteric plexus. These parameters are defined in Figure 1. The number of nonmyelinated nerve trunks in the distal plexus was estimated and graded on a scale of 0 to +++, the latter representing cases in which these trunks appeared most prominent. Fin. I. Semidiagramniatic representation o the anorectal wall. A, 15, and C refer to the parameters measured (see Table 1). three groups. Group I included premature infants whose weights ranged from 670 to 2,000 Gm. and whose ages ranged from one day to three weeks. Group II included term infants ranging from one day to ten weeks in age, whose weights ranged from 2,500 to 4,000 Gm. Group III included older infants and children whose ages ranged from five months to six years and whose weights ranged from 5 to 20 kg. The specimens were opened longitudinally along the posterior wall, pinned to cardboard, and fixed in 10% formalin buffered with sodium acetate. After fixation, a single longitudinal strip of tissue from the posterior wall, including the internal sphincter and extending proximally for a distance of 6 cm., was excised, separated into three segments, and embedded in Results Table 1 summarizes the measurements obtained. Although the pectinate line serves as a prominent surgical landmark, Hilton's line was used as the basic microscopic reference point in this study because of its uniform circumferential plane and its constant relation to the internal sphincter. The pectinate line runs an undulating course relative to the rectal valves, makingits location in histologic section more dependent upon the exact plane of the histologic section than the location of Hilton's line. Despite this, the variation in measure- Table J. Summary of Measurements (Millimeters) Group I (10) Group II (8) Group III (7) Mean S.D Range Mean S.D Range Mean S.D Range
3 October 1970 THE ANORECTAL MYENTERIC PLEXUS 639. ":. - < <, >< \. t '»' i j, ' * * V ".' * *vrc<* =*", -**-«# C^?. *.. t*:&*. **!*** «' *e Fic. 2 (upper). Normal myenteric plexus. Arrows denote ganglia. Hematoxylin and eosin. X 100. FIG. 3 (lower). Hypoganglionic area in anorectal myenteric plexus. Sparse ganglion cells are indicated by arrow. Hematoxylin and eosin. X 100. ments within patient groups and the overlap in measurements between patient groups was considerable. As would be expected, the measurements tended to increase as the size of the patient increased. However, considerable overlap existed between groups of patients that differed markedly in stature. The width of the pecten, the area between Hilton's line and the pectinate line, was wider in some premature infants than in certain young children. The same overlap held for other measurements. The extent of overlap was greatest between Groups II and III. Although the mean measurements in Group III were slightly greater than those of Group II, there was no significant difference between these two groups. These data demonstrate the existence of a zone ranging from 1.5 to 23.0 mm. in extent proximal to Hilton's line within which the structure of the myenteric plexus
4 640 WEINBERG A.J.CP. Vol. 54 is atypical. Even in premature infants this zone may extend proximally for distances up to 14.5 mm. Within the proximal third of this zone there is a paucity of ganglion cells, which are irregularly distributed (Figs. 2 and 3). Nonmyelinated nerve trunks may be associated with these ganglion cells. Such nerve trunks are not normally found within more proximal areas of the myenteric plexus. In the distal twothirds of this zone ganglion cells were entirely absent. Nonmyelinated nerve trunks were more prominent in this region (Fig. 4). The numbers of nerve trunks identified tended to increase with increasing maturity of the patient. They were most prominent in Group III and least prominent in Group I. Discussion Although recent studies have suggested the use of physiologic parameters for the diagnosis of Hirschsprung's disease, 0 '" the rectal biopsy remains the definitive test in the diagnosis of this disorder. Interpretation of the biopsy specimen rests upon the shoulders of the surgical pathologist, who is frequently unfamiliar with the microscopic anatomy of this region. Duhamel 4 has alluded to the structural variation which may be present in the most distal aspect of the myenteric plexus. Bodian 3 has noted the absence of ganglion cells in the distal 3 to 15 mm. of the myenteric plexus in 11 control patients. Hofmann and Orestano 8 have documented the existence of a hypoganglionic zone in the region of the internal anal sphincter, but they provide no definitive measurements as to the extent of this zone. More recently, Aldridge and Campbell 1 have studied the anatomy of the anorectal myenteric plexus in greater detail. They define a hypoganglionic zone extending up to 1.4 cm. proximal to the pectinate line, within which ganglion cells cannot be identified in longitudinal sections. Proximal to this is an additional zone which may be as much as 1.5 cm. wide within which ganglion cells are present but are sparse. Nonmyelinated nerve trunks may be present within these areas. These authors conclude that the absence of ganglion cells in biopsies obtained within these distal zone does not permit the diagnosis of Hirschsprung's disease, but the presence of ganglion cells in biopsies obtained within these zones excludes this diagnosis. Our observations regarding the anatomy of this region are essentially in agreement with the data of Aldridge and Campbell. However, we would include under the term "hypoganglionic" the entire zone from the distal margin of the internal anal sphincter to the appearance of a fully developed myenteric plexus having a full complement of ganglion cells and lacking nonmyelinated nerve trunks. A histologic pattern of sparse ganglion cells and prominent nonmyelinated nerve trunks (i.e., hypoganglionosis) identical to that observed normally in the distal myenteric plexus may be seen in certain pathologic conditions. This pattern is observed in the transitional zone of classic colonic aganglionosis between the aganglionic and normal segments of bowel. 6 This hypoganglionic zone is usually of limited extent. A similarly altered myenteric plexus may occupy longer segments of the gastrointestinal tract in association with distal aganglionosis. 7 ' 10 This finding is much less common, and may represent an exaggeration of the usual transitional zone. We have observed an immature infant boy weighing 1.5 kg. with Hirschsprung's Disease in whom the distal aganglionic segment measured only 2.5 cm. in length, but in whom a hypoganglionic segment of bowel extended proximally for an additional distance of 6 cm. (Fig. 5). Finally, hypoganglionosis unassociated with a distal aganglionic segment has been described by Bentley 2 and Ehrenpreis and associates. 6
5 October 1970 THE ANORECTAL MYENTERIC PLEXUS 641 -V" Y,.<,/t. - *! $ > " 1.,* T '!*! </» /^>- j ws,.* ijf e V * *" FIG. 4 (upper). Most distal aspect of anorectal myenteric plexus. Note prominent nonmyelinated nerve trunks, absence of ganglion cells, and increased fibrous tissue which extends between smooth muscle bundles. Hematoxylin and eosin. x 100. Fie. 5 (lower). Hypoganglionosis of colon. Note isolated ganglion cells (A) and small nonmyelinated nerve trunk (B). Additional sparse ganglion cells and larger nerve trunks were present in adjacent sections. Hematoxylin and eosin. X 100. In Bentley's group of five patients ultrashort hypoganglionic segments were found "just proximal to the internal anal sphincter" in the absence of true aganglionosis. He does not define the exact proximal extent of this abnormality. Ehrenpreis does not define the extent of the lesion in his patient. As hypoganglionosis rather than or in addition to aganglionosis may occur in certain pathologic states, the simple identification of ganglion cells in the biopsy specimen should not be taken to exclude an anatomically based abnormality of the myenteric plexus, which may be reflected in significant alteration of physiologic func-
6 642 WEINBERG AJ.C.P. Vol. 54 tion. The relative number of ganglion cells present should be taken into consideration, as should the presence of prominent nonmyelinated nerve trunks. For this the pathologist must have available an adequate specimen which includes all layers of the bowel. The recommendation of a specimen at least 2 cm. in length, as defined by Swenson, 13 seems appropriate. Duhamel 4 has suggested a specimen extending proximally for a distance of 5 cm. from the anal verge. In view of the anatomy of the anorectal myenteric plexus as defined by this study and the work of others, this biopsy must be obtained at least 2.5 cm. proximal to the termination of the internal sphincter or 2 cm. proximal to the anal verge, and should extend proximally from this point for a distance of at least 2 cm. The biopsy should extend the full thickness of the rectal wall, to permit a complete evaluation of myenteric plexus structure, as in our experience sparse ganglion cells may be present in the submucosal plexus overlying an area in which the myenteric plexus is morphologically abnormal. Because of the existence of a normally occurring zone of hypoganghonosis in the anorectal myenteric plexus, a diagnosis of an abnormal myenteric plexus as manifested by hypoganghonosis should not be made unless the pathologist can be assured by the surgeon that the specimen was obtained at least 2.5 cm. proximal to the termination of the internal anal sphincter. Acknowledgment. Dr. Robert P. Bolande provided valuable advice in the development of this study. References 1. AMiidgc, R. T., and Campbell, P. E.: Ganglion cell distribution in the normal rectum and anal canal. A basis for the diagnosis of Hirschsprung's disease by anorectal biopsy. J. Pediat. Surg. 3: , Bentley, J. F.: Some new observations on megacolon in infancy and childhood with special reference to the management of megasigmoid and megarectum. Dis. Colon Rectum 7: , Bodian, M., Stephens, F. D., and Ward, B. C. H.: Hirschsprung's disease and idiopathic megacolon. Lancet 1: 6-11, Duhamel, B.: Histologic investigations into "diopathic megacolon." In Seminar on pseudo- Hirschsprung's disease and related disorders. Arch. Dis. Child. 41: , Ehrenpreis, T., Norberg, K. A., and Wirsen, C: Sympathetic innervation of the colon in Hirschsprung's disease: A histochemical study. J. Pediat. Surg. 3: 43-49, Gherardi, G. J.: Pathology of the ganglionicaganglionic junction in congenital megacolon. Arch. Path. 69: , Hermann, R. E., Izant, R. J., Jr., and Bolande, R. P.: Aganglionosis of the intestine in siblings. Surgery 53: , Hofmann, S., and Orestano, F.: Histology of the myenteric plexus in relation to rectal biopsy in congenital megacolon. J. Pediat. Surg. 2: , Lawson, J. O. N., and Nixon, H. H.: Anal canal pressures in the diagnosis of Hirschsprung's disease. J. Pediat. Surg. 2: , Pages, R., and Duhamel, B.: Intrinsic nonpropulsive colon. In Seminar on pseudo- Hirschsprung's disease and related disorders. Arch. Dis. Child. 41: , Schnaufer, L., Talbert, J. L Haller, J. A., Reid, N. C. R. W., Tobon F., and Schuster, M. M.: Differential sphincteric studies in the diagnosis of anorectal disorders of childhood. J. Pediat. Surg. 2: , Swenson, O., Fisher, J. H., and MacMahon, H. E.: Rectal biopsy as an aid in diagnosis of Hirschsprung's disease. New Eng. J. Med. 253: , Swenson, O., Fisher, J. H., Gherardi, G. J.: Rectal biopsy in the diagnosis of Hirschsprung's disease. Experience with one hundred biopsies. Surgery 45: , Whitehouse, F. R., and Kernohan, J. W.: Myenteric plexus in congenital megacolon. Arch. Intern. Med. 82: , 1948.
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