GENERALIZED JUVENILE GASTROINTESTINAL POLYPOSIS
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1 GASTROENTEROLOGY Copyright 1970 by The Williams & Wilkins Co. Vol. 58, No.5 I ~ r t lin l tu.s.a. e d GENERALIZED JUVENILE GASTROINTESTINAL POLYPOSIS A hereditary syndrome CHARLES R. SACHATELLO, M.D., JOHN W. PICKREN, M.D., AND JAMES T. GRACE, JR., M.D. Department of Surgery and Pathology, Roswell Park Memorial Institute, Buffalo, New York Generalized juvenile gastrointestinal polyposis was recognized in 3 members of a kindred, This hereditary syndrome is characterized by the development of numerous juvenile polyps of the stomach, small intestine, colon, or rectum in various combinations, Juvenile type polyps may be present at birth or become manifest later as a developmental abnormality. These polyps may produce acute or chronic gastrointestinal blood loss and repeated bouts of intussusception. Operative treatment should be conservative to preserve maximal gastrointestinal function since juvenile polyps are hamartomas and not premalignant. Generalized juvenile gastrointestinal polyposis appears to be a hereditary syndrome quite distinct from juvenile polyposis coli, familial (adenomatous) polyposis of the colon, and Peutz-Jeghers syndrome. A classification of hereditary polypoid diseases of the gastrointestinal tract is proposed, using the microscopic characteristics of the polyps per se as the basis for delineating the several distinct syndromes. This report is based on a kindred in which 3 members of three generations developed generalized juvenile gastrointestinal polyposis involving the stomach, small intestine, and colon. A 4th member of this kindred has manifested only juvenile polyps of the colon to date (fig. 1). The belated recognition of the many unusual aspects of this kindred prompted a thorough review of their complicated medical history. Case Histories Case I. R.P.M.I. no (I1I-2), a 7-yearold boy, first was seen at Roswell Park Memorial Institute in October 1956 because of intermittent rectal bleeding of I-year dura- Received June 17, Accepted November 21, Address requests for reprints to: Dr. Charles R. Sachatello, Department of Surgery and Pathology, Roswell Park Memorial Institute, 666 Elm Street, Buffalo, New York tion. Several rectal polyps had been removed through a sigmoidoscope in February 1956, and diagnosed.as "severely inflamed adenomatous polyps." A barium enema with air contrast studies in February 1956 was normal. The boy's parents were in good health, but the paternal grandmother had a subtotal gastric resection in 1953 for a gastric tumor. Physical examination was normal except for the fact the child appeared to be of low normal intelligence for his age. No oral or circumoral pigmentation was noted. Sigmoidoscopy revealed numerous rectal polyps. Repeat barium enema and air contrast studies in October and November 1956 were suggestive, but not diagnostic, of colon polyposis. The patient was operated on in July 1958 and approximately 40 polyps were removed through multiple colotomies. These lesions were typical juvenile polyps. A subsequent barium enema 1 year later revealed recurrent colonic polyps and a total abdominal colectomy and ileorectal anastomosis was performed in August There were 13 polyps in the resected specimen. Although these were considered to be adenoma-
2 700 SACHA TELLO ET AL. Vol. 58, No.5-1'- JUVENILE GASTROINTESTINAL POLYPOSIS n ~ 21 m 0 Ill: o I 19 I!'iii o3 o 3 I 13!!J 4 SEPT.,68 No. AGE [ij POLYPOSIS - SMALL BOWEL 0 MALE - NORMAL!!J POLYPOSIS - COLON 0 FEMALE - NORMAL ~ NO FAMILY ~ POLYPOSIS - GASTRIC 00 DIED IN INFANCY FIG. 1. Pedigree of present kindred. FIG. 2. Polyp removed from colon of patient III-2 at age 9 (A) and from rectum (B) at age 10. Note the large cystic spaces filled with mucus and the inflammatory reaction in the stroma. X 40.
3 May 1970 JUVENILE GASTROINTESTINAL POLYPOSIS 701 tous in nature, reexamination of the specimens clearly showed a histological abnormality consistent with juvenile polyps (fig. 2). The patient was noted to be severely anemic at age 12 in October Sigmoidoscopy, barium enema, upper gastrointestinal series, and small bowel X-rays were normal. He was treated with orally administered iron and his hemoglobin returned to normal. Two years later, at age 14, a small bowel series demonstrated numerous polyps. The patient was reoperated on and nine polyps were removed from the small intestine through multiple enterotomies. Examination in April 1969 revealed a well developed 220-lb, 19-year-old youth who was moderately retarded mentally. Roentgenographic studies of the stomach, small intestine, and colon in addition to sigmoidoscopy disclosed no abnormal findings. Case II. R.P.M.I. no (I-I), a 63-yearold woman, first was seen at Roswell Park Memorial Institute in February 1957 because of recurrent anemia. She had had a subtotal gastric resection 3 years previously for a polypoid filling defect in the antrum. The resected specimen contained numerous polyps. The initial physical examination in February 1957 revealed a thin, pale woman with multiple subcutaneous lipoma and a left seventh nerve palsy. The lipomas were noticed only after the patient lost weight over a I-year period before admission, while the facial nerve palsy developed following an ear infection as a' child. Laboratory data revealed a hemoglobin level of 5.0 g and a normal Schilling test. The serum albumin was 2.76 g per 100 ml and the hemoglobin, 2.38 g per 100 ml. An upper gastrointestinal roentgenographic study was consistent with gastric polyposis and the barium enema study was normal. The patient had a total gastrectomy and esophagojejunostomy in March The resected specimen revealed extensive polyposis (fig. 3). There was no evidence of jejunal ulceration. Although these polyps were called adenomatous, they were found to be typical juvenile polyps on subsequent reexamination. The patient gained 20 lb in the first 6 months following her total gastrectomy. She developed severe anemia in early 1958 and presented with a hemoglobin of 3.8 g. An upper gastrointestinal series demonstrated a normally functioning esophagojejunostomy. Sigmoidoscopy FIG. 3. Patient 1-1. Residual stomach resected in There is no normal gastric mucosa. Normal jejunum from the previous gastrojejunostomy can be seen in the lower center of the specimen.
4 702 SACHA TELLO ET AL. Vol. 58, No. 5 FIG. 4. Patient II-I. The stomach has been opened along the greater curvature and the pylorus is at the right of the photograph. Note that the juvenile polyps in the fundus are larger and more pendunculated than those in the antrum. revealed a single small polyp at 8 cm, while numerous polyps were noted on a barium enema study. A second operation was performed in June 1958 and six colonic polyps were removed through separate colotomies. These lesions were juvenile polyps. The patient had no further difficulty for 1 year but again was noted to be anemic. She received 30 to 40 U of blood over the next 3 years because of persistent anemia and chronic gastrointestinal blood loss. Repeated sigmoidoscopic examinations were normal, but barium enema studies suggested recurrent colonic polyps in November In February 1963, at age 69, a total abdominal colectomy and ileoproctostomy were performed. The resected colon revealed extensive polyposis which were typical juvenile polyps on reexamination. Examination in March 1969 revealed a thin, pale female with numerous small subcutaneous lipomata. No oral or circumoral pigmentation was noted. No osteomas were demonstrable on bone survey films. Laboratory data showed a hemoglobin of 10.0 g, and white blood count of 4100 per mm", normal differential and platelets. An upper gastrointestinal series, small bowel examination, and barium enema did not show any polyps in the remaining small bowel or rectum. Case III. R.P.M.I. no (II-I), a 33-yearold male, was examined at Roswell Park in May 1960 because of anemia. Initial physical examination and laboratory data were normal. A partially obstructing lesion in the transverse colon and numerous smaller polyps were noted on barium enema. Sigmoidoscopy and upper gastrointestinal series were normal. A total abdominal colectomy and ileoproctostomy was performed in May The resected specimen revealed a single polypoid lesion 4 X 4 cm, in the transverse colon and one other l-cm polyp. The larger lesion had produced intermittent colocolic intussusception.
5 May 1970 JUVENILE GASTROINTESTINAL POL YPOSIS 703 The patient was noted to be severely anemic 4 years later in March Interim barium studies and sigmoidoscopy had been normal. A repeat upper gastrointestinal series revealed gastric polyposis. A 12-hr collection of gastric juice revealed 12 meq of free acid. A total gastrectomy with esophagoduodenostomy was performed in August The resected specimen revealed extensive gastric polyposis (fig. 4). In July 1968 the patient was noted to be a well developed, relatively well nourished male who had minimal gastrointestinal symptoms. His weight was 156 Ib, 50 Ib less than his weight prior to his total gastrectomy. Barium studies noted a normally functioning esophagoduodenostomy with relatively slow small bowel transit time. No filling defects were noted in the small bowel. Barium enema and sigmoidoscopy were normal. Case IV. R.P.M.I. no (III-4), a 13- year-old boy, was first examined at age 4 in Sigmoidoscopy and barium enema examination were normal. These studies were repeated yearly and were normal until age 12. The barium enema in July 1967 was suggestive of multiple polyps of the colon. Sigmoidoscopy was normal. Patients II-2, III-I, and III-3 were all examined and found to have normal sigmoidoscopy and barium enema studies. None were anemic. Patient II-3 is 52 years old and in good health. She has not been examined. She has 3 children and 2 grandchildren, all of whom are in good health. The grandmother (1-1), who was born in Poland, has no specific medical information about her parents or siblings, but all were long lived and none had any abdominal operations. Results Summary of Family History Three members of this kindred have had a total of 10 major abdominal operations in addition to an uncountable number of sigmoidoscopic fulgurations of rectal polyps. The presenting and recurrent symptom in each patient was anemia or rectal bleeding. A 4th member of the kindred has had two barium enema examinations suggestive of colon polyps. The grandmother has numerous subcutaneous lipomas on her arms, which became manifest only after a 20- to 30-lb weight loss. Their significance as a true pathological entity is debatable. No member of the family has oral or circumoral pigmentation. None have any osteomas or bony irregularities demonstrated by bone survey films. The propositus (III-2, fig. 1) is moderately retarded mentally, but the other family members are of normal intelligence. Each family member studied had complete blood counts and numerous blood chemistry studies. All studies were normal with the exception of the low hemoglobin. The serum albumin was decreased in patient I-Ion several occasions while the patient was anemic. The peripheral leukocyte karyotype was normal in patients I-I and II-I. Pathology The gross appearance of the resected stomachs in the grandmother (I-I) and the father (II-I) was similar (figs. 3 and 4). The polypoid lesions were larger and more pedunculated in (I-I). The colon removed from the propositus (III-2) contained 13 juvenile polyps. Approximately 40 polyps had been removed 1 year earlier from this colon through multiple colotomies. The resected colon from the grandmother (I-I) had innumerable polyps from 0.2 to 2 cm in diameter. The colon resected from the father (II-I) of the propositus contained only two juvenile polyps. The largest one was 4 X 5 cm with a short pedicle. The microscopic appearance of the gastric, intestinal, and colonic polyps was similar (figs. 2 and 5). The typical juvenile polyp consists of an epithelial component surrounded by abundant connective tissue stroma which often displays a primitive mesenchymal appearance. 1 The surface of the polyp is covered by a single layer of columnar epithelial cells often containing mucus within their cytoplasm and on their surfaces (fig. 2A). This layer is often absent on juvenile polyps removed from the rectum (fig. 2B) owing to infection or ulceration. The epithelial element is arranged in tubules associated with an apparent over production (or possible retention) of mucus. These cystic spaces may contain abundant nuclear debris and polymorphonuclear leukocytes. Epithelial cells compressed or destroyed by excessive mu-
6 704 SACHATELLO ET AL. Vol. 58, No.5 FIG. 5 Gastric polyps removed from patient II-I at age 42 (A) and from his mother, I-I, at age 63 (B). There is striking similarity in these lesions compared with the polyps in figure 2, A and B X 40. cus may give rise to a pattern that can be falsely interpreted as colloid carcinoma (fig. 2B). Discussion There are several case reports of patients with adenomatous polyposis and familial (multiple) polyposis in whom both the clinical course and microscopic pathology are suggestive of generalized juvenile gastrointestinal polyposis. Ravitch reported a 10-month-old male who presented with anemia and who was found to have numerous polyps on barium enema examination. 2 The infant required continued transfusions because of chronic gastrointestinal blood loss and died 1 day after a resection of an ileoileal intussusception at 18 months of age. Innumerable polypoid tumors from the cardia of the stomach to the anus were noted at autopsy. Although no microscopic description is given in this report, the photomicrographs of the specimen and polyps are consistent with gener- alized juvenile gastrointestinal polyposis. LeFevre and Jacques reported a similar case in a 4-month-old male who presented with bloody stools and severe anemia. J The infant died 1 month later owing to ileoileal intussusception. Numerous polyps in the jejunum, ileum, and colon were noted at autopsy. Recent reviews of available sections by Dr. B. E. Favara (personal communication) and the authors show juvenile polyps. Pollack and Swinton reported a patient whose family history, clinical course, and pathology are similar to 2 of the cases in this present report. 4 Their patient (a male) had a staged colectomy and ileosigmoidostomy at age 19 in Polyposis of the small intestine was noted at age 35 in Numerous gastric polyps were noted at age 39 and a subtotal gastrectomy was performed. The patient experienced repeated bouts of upper gastrointestinal hemorrhage over the next decade leading to a total gastrectomy at age 49 in 1964.
7 May 1970 JUVENILE GASTROINTESTINAL POLYPOSIS 705 The patient died postoperatively. The patient's daughter had a total colectomy and ileorectal anastamosis at age 13 in She has since developed occasional rectal polyps (N. W. Swinton, personal communication). Morson has reviewed the microscopic slides in the father and considers these typical juvenile polyps. Additionally, Morson noted that he has studied 2 other cases with juvenile polyposis of the stomach, small and large bowel and 3 cases in which the juvenile polyps were confined to the small intestine and colon (personal communication). There are a number of additional reports in which the clinical course and gross pathology are compatible with either gastrointestinal juvenile polyposis or Peutz-Jeghers syndrome but which lack detailed microscopic pathology. 59 It is of interest that there were no cases of generalized juvenile polyposis noted in several large series of patients with juvenile polyps.lo-14 One patient who was considered to have generalized juvenile polyposis has since been diagnosed as having Peutz-Jeghers polyposisl 2 (also J. T. Prior, personal communication). In both the present kindred and in the Boston kindred, juvenile gastrointestinal polyposis appeared to be transmitted as a dominant genotype with variable, age dependent expressivity. Likewise, in each of these kindreds, both the symptoms and disease appeared earlier in each successive generation. Although the existence of anticipation as a true biological phenomenon is debatable,15 the progressively earlier onset of this disease in each generation of the present kindred is most impressive. The recognition of gastrointestinal juvenile polyposis as an hereditary syndrome distinct from Peutz-Jeghers syndrome, familial polyposis (adenomatous) of the colon, juvenile polyposis coli, and Gardner's syndrome permits more specific criteria for classifying individual cases as belonging to one or another of these syndromes. Peutz-Jeghers Syndrome Peutz-Jeghers syndrome is characterized by the association of pigmentation of the lips or buccal mucosa and gastrointestinal polyps.lo The polyps in the Peutz-Jeghers syndrome may have the same distribution as the polyps in generalized juvenile polyposis but have different microscopic characteristics. The typical Peutz-Jegher polyp contains muscularis mucosa and the epithelial element is related to the smooth muscle in the same manner as it is in the normal mucous membrane. I The Peutz Jeghers polyps have been considered hamartomas of the muscularis mucosa while the juvenile polyp has been regarded as due to a connective tissue abnormality. I, It is becoming increasingly apparent however, that a small percentage of Peutz-Jegher's polyps may be locally aggressive, implant in abdominal wounds, or metastasize. IS 21 Additionally, approximately 5% of females with Peutz-Jegher's syndrome have been found to have ovarian neoplasms usually of the theca cellgranulosa type. 20 Familial Adenomatous Polyposis of the Colon Familial adenomatous polyposis of the colon is a hereditary disease characterized by the appearance of numerous adenomatous polyps of the colon usually between the ages of 10 and , 23 The great majority of untreated patients will develop an associated adenocarcinoma of the large bowel between the ages of 15 and 50. True adenomatous polyps have been documented in only a few patients with familial adenomatous polyposis of the colon before 10 years of age. Extensive gastrointestinal polyposis (adenomatous type) associated with familial adenomatous polyposis appears to be quite rare, although isolated adenomatous polyps or neoplasms of the duodenum have been recognized in patients with familial adenomatous polyposis. 24,25 A number of patients with familial polyposis of the colon have extensive lymphoid hyperplasia in the terminal ileum. The resulting mucosal excresences may be misinterpreted as representing adenomatous polyps2o (also C. R. Sachatello, unpublished data).
8 706 SACHATELLO ET AL. Vol. 58, No.5 Juvenile Polyposis Coli Juvenile polyposis coli is characterized by the development of numerous juvenile polyps of the colon. This syndrome has been recognized only recently as being distinct from familial adenomatous polyposis of the colon by the St. Mark's group."7,:.!8 None of the original 11 patients had polyps in either the stomach or small intestine, although several had other congenital abnormalities. There was a strong family history of bowel cancer in 4 of the cases, but none of the patients with juvenile polyposis coli developed colorectal cancer. Smilow et al. subsequently reported 3 cases of juvenile polyposis coli in three generations of one family. :.!9 The oldest patient in this family had an adenocarcinoma of the colon resected at age 60, but the juvenile polyps were not recognized until 18 months postoperatively. Gardner's Syndrome Gardner described two large kindreds with familial adenomatous polyposis of the colon, epidermoid cysts, osteomas, desmoid tumors, and a variety of dental abnormalities in J o ell Smith first used the eponym in 1958 in reporting patients who had familial polyposis of the colon and desmoid tumors.3:.! Eight years later Jones and Cornell were able to review more than 80 patients with this syndrome. o3 McKusik suggested that classic familial polyposis and Gardner's syndrome were distinct entities. 34 McConnell further subdivided patients with familial adenomatous polyps of the colon into a number of "distinct entities" associated with (a) tumors of the nervous system, (b) sebaceous cysts, (c) gastric polyps, or (d) duodenal polyps.35 ' A decade after first using the term Gardner's syndrome, Smith noted that the continued elaboration of new syndromes based on a combination of extracolonic lesions was inconsistent with clinical experience. He further suggested that Gardner's syndrome may not represent a distinct entity and that the term familial polyposis be retained. 36 There is no evidence to suggest that the presence or absence of osteomas or epidermoid cyst influence the underlying colon pathology. Patients with extracolonic manifestations of familial polyposis of the colon are just as likely to develop. colorectal carcinoma as those patients without these manifestations. Additionally, full expression of extracolonic manifestations have been observed in patients who had no evidence or family history of colorectal pathology. 36 Desmoid tumors influence the underlying colon pathology in an indirect manner only. The fibrous tissue reaction may be so extensive or aggressive as to preclude colon resection, relief of intestinal obstruction, or construction of an ileostomy3:.!. '17, '18 (also C. R Sachatello, unpublished data). The present authors have studied approximately 10 patients with familial polyposis of the colon and an equal number of normal siblings. We have not found a consistent association between the presence or absence of polyposis and the extracolon manifestations. Use of any classification other than familial polyposis of the colon would result in our classifying blood relatives as representing three or four different subsyndromes. We would suggest that familial polyposis of the colon (adenomatous type) be considered the major syndrome, recognizing that the frequency of related abnormalities not only is extremely high, but also is related directly to the completeness of the evaluation.38. :19 Definitive classification ultimately will be based on elucidation of fundamental biochemical abnormalities. Chromosome studies of the skin, colon, polyps, and peripheral leukocytes in patients with familial polyposis with or without extracolonic manifestations have been normal":.!' 28, :13, 40 (also C. R. Sachatello, unpublished data). Our proposed clinical classification of hereditary polypoid diseases of the gastrointestinal tract is presented in table 1. This basis for this grouping is the microscopic characteristics of the polypoid lesions, the prime determinant of the necessity, and type of treatment indicated,
9 May 1970 JUVENILE GASTROINTESTINAL POLYPOSIS 707 TABLE 1. Hereditary polypoid diseases of gastrointestinal tract Disease Pathology Location Extraabdominal man i- festations (variable) Malignant potential Familial polyposis Adenomatous Colon (90- Osteomas, epidermoid At least 85-95% of colon polyps 100%) cysts, fibrous tumors of patients will (Gardner's Duodenum (desmoids), dental develop a colo- Syndrome) (1-2%) abnormalities, cuta- rectal adenocarneous pigmentation cinoma (rare), osseous abnormalities Peutz-J eghers Hamartomas Stomach, Buccal pigmentation Carcinoma (1-2%) syndrome of muscularis small bowel, Ovarian tumors mucosa colon (5%) Generalized gas- Juvenile Stomach, Very low trointestinal ju- polyps small bowel, venile polyposis colon Juvenile Juvenile Colon polyposis coli polyps Very low It does not seem meaningful to us to further subdivide patients with familial polyposis of the colon because of associated extracolonic malignancies of the central nervous system or thyroid It has been suggested that the presence of discrete polyps of the! colon may be a separate hereditary syndrome. 4 '1 REFERENCES 1. Morson, B. C Some peculiarities in the histology of intestinal polyps. Dis. Colon Rectum 5: Ravitch, M. M Polypoid adenomatosis of the entire gastrointestinal tract. Ann. Surg. 128: LeFevre, H. W., and T. F. Jacques Multiple polyposis in an infant of four months. Amer. J. Surg. 81: Pollack, J. L., and N. W. Swinton Congenital polyposis of the colon with extension to the small intestine and stomach. Lahey Clin. Found. Bull. 9: Bratrud, T futestinal polyposis with report of a case with three intussusceptions. Surg. Gynec. Obstet. 19: Glass, F. A Multiple polyposis of gastrointestinal tract. J. Oklahoma Med. Assn. 23: Welch, G., and G. McHardy Adenomatous polyposis of the whole gastrointestinal tract. Gastroenterology 13: Jensen, M. N Multiple polyposis of small and large intestine with multiple intussusceptions. Surgery 29: Boley, S. J., W. M. P. McKinnon, and V. F. Marzulli The management of familial gastrointestinal polyposis involving stomach and colon. Surgery 50: Helwig, E. B Adenomas of the large intestine in children. Amer. J. Dis. Child. 72: Turell, R., and A. L. Maynard Adenomas of the rectum and colon in juvenile patients. J. A. M. A. 161: Mauro, J., and J. T. Prior Gastrointestinal polypoid lesions in childhood. Cancer 10: Knox, W. G., R. E. Miller, C. F. Begg, and H. A. Zintel Juvenile polyps of the colon. Surgery 48: Roth, S. I., and E. B. Helwig Juvenile polyps of the colon and rectum. Cancer 16: McKusick, V. A Heritable disorders of connective tissue, Ed. 3. C. V. Mosby Company, St. Louis. 16. Jeghers, H., V. A. McKusick, and K. H. Katz Generalized intestinal polyposis and melanin spots of the oral mucosa, lips and digits. New Eng. J. Med. 241: ; Weller, R. 0., and I. McColl Electron microscopic appearances of juvenile and Peutz Jeghers polyps. Gut 7: Hom, R. C., Jr., W. A. Payne, and G. Fine The Peutz-Jeghers syndrome. Arch. Path. (Chicago) 76:
10 708 SACHATELLO ET AL. Vol. 58, No Reid, J. D Duodenal carcinoma in the Peutz-Jeghers syndrome. Cancer 18: Humphries, A. L., M. H. Shepard, and H. J. Peters Peutz-Jeghers syndrome with colonic adenocarcinoma and ovarian tumors. J. A. M. A. 197: Mackman, S., G. Perna, and F. Gossett Peutz-Jeghers syndrome with metastases to an abdominal incision. Arch. Surg. (Chicago) 98: Veale, A. M. O Intestinal polyposis, eugenics laboratory, memoirs. Cambridge University Press, Cambridge, England. 23. Lockhart-Mummery, J. P Intestinal polyposis.?roc. Roy. Soc. Med. 60: Capps, W. F., M. I. Lewis, and D. A. Gazzaniga Carcinoma of the colon, ampulla of vater and urinary bladder associated with familial multiple polyposis. Dis. Colon Rectum 11: Yonemoto, R H., J. B. Slayback, R L. Bryon, Jr., and R B. Rosen Familial polyposis of the entire gastrointestinal tract. Arch. Surg. (Chicago) 99: Thomford, N. R, and N. J. Greenberger Lymphoid polyps of the ileum associated with Gardner's syndrome. Arch. Surg. (Chicago) 96: McColl, 1., R. J. R. Bussey, A. M. O. Veale, and B. C. Morson Juvenile polyposis coli.?roc. Roy. Soc. Med. 57: Veale, A. M. 0., 1. McColl, H. J. R Bussey, and B. C. Morson Juvenile polyposis coli. J. Med. Genet. 3: Smilow, P. C., C. A. Pyror, Jr., and N. W. Swinton Juvenile polyposis coli. Dis. Colon Rectum 9: Gardner, E. J., and R C. Richards Multiple cutaneous and subcutaneous lesions occurring simultaneously with hereditary polyposis and osteomatosis. Amer. J. Hum. Genet. 5: Gardner, E. J Follow-up study of a family group exhibiting dominant inheritance for a syndrome including intestinal polyps, osteomas, fibromas, and epidermal cysts. Amer. J. Hum. Genet. 14: Smith, W. G Multiple polyposis, Gardner's syndrome and desmoid tumors. Dis. Colon Rectum 1: Jones, E., and W. Cornell Gardner's syndrome. Arch. Surg. (Chicago) 92: McKusick, V. A Genetic factors in intestinal polyposis. J. A. M. A. 182: McConnell, R B The genetics of gastrointestinal disorders. Oxford University Press, London. 36. Smith, W. G Familial multiple polyposis. Dis. Colon Rectum 11: Simpson, RD., E. G. Harrison, Jr., and C. W. Mayo Mesenteric fibromatosis in familial polyposis of the colon. Cancer 17: Watne, A. L., J. G. Johnson, and C. H. Chang The challenge of Gardner's syndrome. CA 19: Chang, C. R., E. D. Piatt, K. E. Thomas, and A. L. Watne Bone abnormalities in Gardner's syndrome. Amer. J. Roentgen. 103: McConnell, T. S., and L. Parsons, Jr Chromosome evaluation in familial polyposis of the colon. Rocky Mountain Med. J. 65: Turcot, J., J. P. Despres, and F. St. Pierre Malignant tumors of the central nervous sys tem associated with familial polyposis of the colon. Dis. Colon Rectum 2: Carniel, M. R, J. E. Mule, L. L. Alexander, and D. L. Benninghoff Association of thy roid carcinoma with Gardner's syndrome in siblings. New Eng. J. Med. 278: Woolf, C. M., R C. Richards, and E. J. Gardner Occasional discrete polyps of the colon and rectum showing an inherited tendency in a kindred. Cancer 8:
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