Mechanism of Obstruction in Carcinoid Tumors of the Small Intestine
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1 Mechanism of Obstruction in Carcinoid Tumors of the Small Intestine JOHN E. MCNEAL, M.D. Herrick Hospital, 2001 Dwight Way, Berkeley, California ABSTRACT McNeal, John E.: Mechanism of obstruction in carcinoid tumors of the small intestine. Amer. J. Clin. Path. 56: , Six carcinoid tumors of the small intestine were studied histologically. In three cases, a very small tumor had caused obstruction by a kinking process which was intrinsic within the bowel wall and was apparently produced by lateral submucosal tumor growth with traction on an underlying adherent muscularis. Hypertrophy of the muscularis and serosal fibrosis were contributory factors and possibly were related to tumor hormone production. The phenomenon was thought to depend on the interaction of several unusual features of the carcinoid tumor and so may be specific for this type of neoplasm. The tumor was concealed by the kink in these cases so that its presence was not suspected at surgery. Unless this gross appearance is recognized at surgery, the opportunity for definitive therapy with wide mesenteric resection may be missed. CHRONIC, PROGRESSIVE BOWEL OBSTRUCTION is a common clinical feature of carcinoid tumor of the small intestine. In at least half of symptomatic patients, obstructive symptoms are the presenting complaint and the main indication for surgery. 2 " 7 Paradoxically, the obstructing lesion in the resected bowel segment is typically very small often 1 cm. in diameter and rarely larger than 2 cm. 4 The mechanism by which such a small neoplasm might produce obstruction has not been thoroughly investigated, even though the frequency of this complication suggests that it might result from some process intrinsic to the natural history of this disease. Descriptions in previous literature tend to support the view that no unique intrinsic mechanism exists, but rather that Received August 10, 1970; revised manuscript received October 12, 1970; accepted for publication October 29, obstruction results from a variety of nonspecific processes which might complicate the course of any malignant tumor. The process most frequently described is kinking of the bowel wall secondary to tumor infiltrating the mesentery and causing mesenteric fibrosis with retraction. 3 ' 4 - Less often reported is luminal constriction secondary to fibrosis accompanying the spread of tumor within the intestinal wall. 1 ' s - 4> In other cases, serosal fibrosis caused by the tumor has produced adhesions to other loops of intestine or the abdominal wall with secondary kinking of the affected area. 2 ' 5 There are occasional reports of obstruction due to intussusception 1 > 4 > 6 " 8 or resulting from intestinal infarction produced by metastatic tumor compressing mesenteric vessels. 2 These explanations constitute a heterogeneous group. The only common elements are the dependence of some mechanisms on
2 October 1971 OBSTRUCTING CARCINOID TUMORS 453 tumor growth beyond the bowel wall and the relation of others to the well known tendency of carcinoid tumors to induce fibroplasia. 1 ' 2 ' 7 Despite this diversity, a note of underlying unity is struck in many accounts by frequent repetition of the terms "kinking," "buckling," or "puckering" in reference to the obstructed focus. 1 " 0 ' 0 The present investigation describes what may well be a single basic mechanism underlying the apparently diverse phenomena described in most of the previous cases. The process involved is probably specific for carcinoid tumor and is related only in small part to the induction of fibrosis by the tumor or to the extension of tumor beyond the bowel wall. Material and Methods Three clinically obstructing small intestinal carcinoid tumors removed at surgery were noted to have unusual features in common and were subjected to detailed gross and microscopic evaluation by routine procedures. During this period, three incidental carcinoids were found in the small intestine at autopsy, and their characteristics were compared to the three surgical cases. Detailed clinical data were available for only one surgical case. The report of this case follows. Report of a Case A 68-year-old Negro woman was hospitalized with severe, progressive, epigastric pain for 72 hr. associated with nausea and vomiting. The pain was intermittent, with radiation into the right upper quadrant. She reported previous attacks which had been less severe. Physical examination was essentially normal except for abdominal findings. The abdomen was obese and moderately distended, with epigastric and right upper quadrant tenderness. Bowel sounds were hypoactive. There were no abdominal masses. Roentgenographic examination of the abdomen showed dilated loops of small bowel with fluid levels consistent with small bowel obstruction. On conservative management, the patient's symptoms and abdominal distention gradually subsided. She was discharged asymptomatic but was readmitted with a recurrence of identical symptoms 5 weeks later. During the interval, the patient had daily episodes of intermittent abdominal pain of relatively mild degree. Physical findings and roentgenograms of the abdomen were identical to those of the previous admission. An exploratory laparotomy on the fourth hospital day showed a single area of sharp kinking of the small intestine not associated with any demonstrable intestinal tumor and presumed to be due to a localized area of intestinal adhesions. No adhesions were present elsewhere in the peritoneal cavity. Immediately proximal to the kink, the bowel showed dilatation and thickening of the wall consistent with acute and chronic obstruction. In the mesentery beneath the point of kinking, and not attached to the bowel wall, was a firm, nodular tumor mass measuring 5 cm. in greatest dimension. The mesentery was not retracted or otherwise abnormal. The retroperitoneal tissues around the aorta showed multiple, enlarged, confluent lymph nodes. Because of the characteristic gross appearance of the area of intestinal kinking, the diagnosis of intestinal carcinoid was suspected from the above description given by the surgeon at the time of surgery. This diagnosis was supported by the appearance of the lesion on cut section and was confirmed by frozen section of a mesenteric node. Following resection of the point of obstruction and underlying mesenteric nodes, the patient had an uneventful postoperative course. She remains clinically well 1 year after surgery and has normal urinary 5-hydroxyindoleacetic acid levels despite the fact that periaortic lymph node metastases were not removed and small metastatic nodules were visible in the liver.
3 454 McNKAL A.J.C.P. Vol. 56 Detailed clinical information was not available lor the two earlier surgical cases. The presenting complaint in each, however, was intestinal obstruction. In each, no neoplasm was identified at surgery, either in bowel or mesenteric nodes, and postoperative diagnosis was obstruction due to adhesions. Only in the third case, presented above, was frozen section requested on the suspicion of mesenteric lymphoma. Pathologic Findings In the three surgical cases, the gross specimens were almost identical in appearance. There was no evidence of intestinal neoplasm on inspection and palpation from the serosal surface before opening the bowel. The region of the tumor showed only an abrupt kinking of the small intestine with a sudden change in the direction of its long axis. A deep crease marked the focus of kinking, and the apposed serosal surfaces were adherent in an area of poorly defined granular opacity consistent with inflammatory fibrosis. In all three specimens, the area of the crease was halfway between the mesenteric and antimesenteric borders. The crease indicated the exact location of the tumor but at the same time prevented its gross recognition. Palpation at this point, immediately overlying the tumor, revealed only a diffuse thickening consistent with what might result from serosal fibrosis plus folding of the intestine on itself. There was no discrete tumor mass. Cut section through the center of the crease in the long axis of the intestine showed preservation of the normal layers of the bowel wall (Fig. 1). The muscularis was somewhat hypertrophied, and the submucosal and subserosal tissues were diffusely thickened by white to pale yellow tissue. This represented tumor and scirrhous reaction but did not form a discrete nodule. The bowel lumen was markedly narrowed by kinking and intrusion of the folded thickened area of intestinal wall. In the case reported here there was a mass of nodes replaced by metastatic tumor in the mesentery but not in continuity with the primary lesion. One of the other cases had several small mesenteric nodes which contained tumor, but grossly appeared normal. The status of nodes on the third case is not known, except that no nodes were found within 1 cm. of the serosal surface. The three autopsy tumors were all discrete mucosal nodules and were pale yellow on cut section. Microscopically, they had well demarcated margins, consistent with a primarily expansile growth. All three invaded a short distance into the inner coat of the muscularis by microscopic examination but presented a sharp border in its superficial portion. The bulk of the tumor in each case lay in the submucosa. Here it formed a flat, button-like mass, reflecting a predominance of lateral spread over increase in thickness. No scirrhous reaction was seen in any case. In one of the incidental tumors, there were additional features which appeared to represent an early phase of the kinking process seen in the surgical cases. In this tumor there was unusual distortion of the muscularis, particularly the inner, transverse layer (Fig. 2). The inner layer showed moderate hypertrophy diffusely beneath the entire deep margin of the tumor. In addition, the muscle bundles at the deep lateral margins of the tumor were stretched and retracted laterally. Muscle bundles toward the midportion of the tumor showed progressively less lateral traction, producing a pattern of fanning out of the ordinarily perpendicular bundles away from the center of the specimen. The appearance suggested that the tumor had become fixed to the muscle when its lateral dimension was about 30% smaller, and continued lateral growth had pulled the muscle along with the neoplasm. The deeper longitudinal muscle layer was also hypertrophied,
4 October 1971 OBSTRUCTING CARCINOID TUMORS 455 FIG. I. Sites of kinking in three obstructing carcinoid minors of the small intestine. The specimen at lower right is from the patient reported clinically. Cross specimens, x 1.7. diffuse hypertrophy of the inner muscle layer sharply limited to the area of tumor penetration (Fig. 1). Lateral traction as a primary process could not be assessed be- cause the entire contour of the bowel con- formed to that which would be produced by such traction. The deep muscle layer showed more diffuse hypertrophy in these cases and was much more extensively in- vaded by tumor, which penetrated it to grow diffusely in the siibserosal tissues. The siibserosal growth of tumor was second in but only in a sharply defined area at the center of the specimen, producing a triangular mass of thickened fibers. A few microscopic nests of tumor penetrated the deep muscle in the thickened area, whereas elsewhere it was confined to the superficial third of the inner layer. Beneath the central area, the serosa was slightly dimpled but showed no fibrosis, inflammation, or other pathologic change. Comparison of this case with the three surgical cases showed that they also had
5 456 McNEAL A.J.C.P. Vol. 56 mass only to the submucosal volume. The least growth was in the inner muscle layer, which therefore preserved its intact appearance on gross examination. A prominent scirrhous reaction was associated only with the subserosal tumor, although minimal degrees were seen in the submucosal and deep muscle layers. As a result of this fibrosis, the serosal surfaces were adherent and focally obliterated. In contrast to the rather bulky mass of submucosal tumor in the incidental autopsy case, all three surgical cases showed a narrower strip with less protrusion of the overlying mucosa into the lumen. Comment In three surgical cases of carcinoid tumor of the small intestine and one autopsy case, kinking of the bowel wall has been produced by an apparently unique process. In contrast to many earlier descriptions of kinking with intestinal obstruction, all of the events involved in these cases appear to be limited to the bowel wall and to the immediate vicinity of the primary tumor. This, therefore, is an entirely intrinsic process within the intestinal wall, unrelated to the status of the nodes, mesentery, or other loops of bowel. In fact, all four tumors arose at a point midway between mesenteric and antimesenteric borders, so that direct mesenteric extension was not possible. The process itself remains obscure, but a similar phenomenon does not appear to have been reported with other neoplasms, if all of its features are kept in mind. This suggests that it may be a unique and intrinsic feature of the natural history of carcinoid tumors. Utilizing the observations from these cases, a reasonable hypothesis can be constructed to explain the kinking process. The hypothesis depends in part on the relationship between invasive and expansile growth in carcinoid tumors as deduced from observations in the present six cases. Small intestinal carcinoids in their early stages appear to grow more by expansion than by invasion and tend to expand mainly in the lateral direction, following the tissue plane of the submucosa. At a more advanced stage, a minimal invasive tendency is expressed in the slight penetration and fixation to the inner muscle, but with preservation of an expansile border. Further lateral growth after fixation exerts traction on the muscle. This tendency will be maximized by the slow orderly growth pattern of these neoplasms. Relative absence of tissue destruction, necrosis, or host reaction tends to preserve established anatomic relationships and lines of differential stress. The continued spread of tumor against its relatively unyielding deep attachment will now cause the central portion of the tumor to bulge upward, simultaneously retracting the central portion of the bowel wall to produce a dimpling of the serosa. The lateral traction, expressed differentially at the tumor margins, will tend to pull the margins downward and together. This bowing of the tumor's further growth configuration should be augmented by the fact that the point of lateral traction is not an inert substance but actively contracting muscle. The consistent presence of local muscle hypertrophy suggests that the presence of the tumor does in fact stimulate considerable muscle contraction. Local muscle contraction oriented about one point would by itself tend to produce the type of deformity observed. In this connection it can be postulated that the effect of the tumor to cause contraction may well be mediated by high local concentrations of serotonin or bradykinin produced by the tumor. This possibility is reinforced by the observation in one autopsy case that diffuse hypertrophy of the inner muscle corresponded to diffuse tumor attachment, whereas the deeper muscle showed hypertrophy only in the most central area where it was invaded by tumor.
6 October J9?J OBSTRUCTING CARCINOID TUMORS 457 Fin. 2. Carcinoid tumor obtained at autopsy showing fixation to muscle, lateral traction, hyper trophy of muscularis and early kinking without fibrosis. Trichrome stain. X 10. The progression of this deformity would eventually cause enough kinking to favor frequent contact of adjacent serosal surfaces during peristaltic action. Later, when the tumor reaches the serosa, fibrosis is stimulated. The current observations suggest that fibrosis is mainly a characteristic of the serosal and subserosal reaction to the tumor rather than an intrinsic characteristic expressed by the neoplasm regardless of location. Now the two roughened surfaces will tend to adhere on contact and become cemented together. This would appear to be the last stage in the process, however. The pathogenesis of the initial deformity is entirely related to an interaction between tumor and muscularis before the serosa is invaded. However, the serosal adhesion might well be the determining factor in the final precipitation of obstruction. Before this stage it seems possible that forceful peristaltic waves could produce partial, intermittent reduction of the deformity, allowing the passage of intestinal contents. Cementing of the serosal surfaces would abolish this flexibility and introduce a rigid barrier into the intestinal lumen. In all of the present cases, the location of tumor midway between mesenteric and antimesenteric borders would be optimal for producing contact of adjacent serosal surfaces. Whether the full expression of this syndrome would be altered with other tumor sites remains an unanswered question. This hypothesis appears to fit all the facts noted in this study. Furthermore, it relates the process of obstruction not to a single fortuitous circumstance but to an interaction of a number of unusual features which are characteristic of the carcinoid tumor. Consequently, it gives logical support to the idea that this mechanism for producing intestinal obstruction is unique to this neoplasm. The slow rate and orderly pattern of tumor development, interrelationship of expansile and invasive growth, hormone production, and fibrogenic serosal reaction probably all play a part. Careful rereading of previous descriptions suggests that this mechanism may have been involved in most previously reported cases, perhaps even in those which were ascribed
7 458 McNEAL A.J.C.P. Vol. 56 to intussusception. The emphasis in most reports was placed on the obvious serosal fibrosis and mesenteric tumor without proper consideration of the possible significance of an intrinsic process in the bowel wall. Photographs in two earlier papers show that a gross appearance identical to that presented here was involved in at least some earlier cases. 1 ' 4 The relationship between production of fibrosis and involvement of the serosa suggests an interesting parallel to another unique phenomenon associated with these neoplasms. This is the endocardial fibrosis which is sometimes a part of the carcinoid syndrome. In both endocardium and peritoneum, fibrosis is limited to the immediate vicinity of a nonepithelial surface. In at least the cardiac location, there is an implication of humoral effects because the neoplasm is at a distance from the fibrogenic lesion. Notably, however, such extensive fibrosis is not common in the primary mucosal or submucosal tumor or in deep tissue metastases, where humoral substances must also be highly concentrated. This suggests that fibrosis may be the product of an interaction between tumor hormones and specialized types of internal surface linings. The immediate practical value of the findings of this study relates to the appearance of these lesions at surgery. The presence of an intestinal neoplasm went unrecognized at surgery in all three clinical cases. The neoplasm was completely hidden by the kinking process, and even on cut section the presence of tumor was not immediately apparent. In at least one case, there were not even enlarged nodes to signal the presence of any further abnormality. Because recommended treatment for these lesions includes wide mesenteric resection, 5 ' 7 and because most obstructing tumors probably have positive mesenteric nodes, 4 definitive therapy depends upon operative recognition. Many of these lesions will not be identified at surgery, however, unless surgeons and pathologists are aware of the potential significance of an isolated focus of apparent intestinal adhesions. References 1. Dockerty MB: Carcinoid tumors. Calif Med 99: , Dockerty MB, Ashburn FS: Carcinoid tumors (so-called) of the ileum: Report of 13 cases in which there was metastasis. Arch Surg 47: , Miller ER, Herrmann WW: Argentaffin tumors of the small bowel: A roentgen sign of malignant change. Radiology 39: , Moertel CG, Sauer WG, Dockerty MB, et al.: Life history of the carcinoid tumor of the small intestine. Cancer 14: , Pearson CM, Fitzgerald PJ: Carcinoid tumors: A re-emphasis of their malignant nature. Cancer 2:1,004-1,026, Postlethwait RW: Gastrointestinal carcinoid tumors: A review. Postgrad Med 40: , Sanders RJ, Axtell HK: Carcinoids of the gastrointestinal tract. Surg Gynec Obstet 119: , Speirs RE, Williams ER: Carcinoids of the small bowel. Amer J Surg 110: , Stewart WH, Bartlett RM, Bishop HM, et al.: Carcinoid tumors presenting with acute abdominal signs. Ann Surg 154: , 1961
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