Serrated Adenomatous Polyposis in Humans

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1 GASTROENTEROLOGY 1996;110: Serrated Adenomatous Polyposis in Humans EMINA TORLAKOVIC and DALE C. SNOVER Department of Laboratory Medicine and Pathology, University of Minnesota Medical School, Minneapolis, Minnesota See editorial on page 950. polyposis of the colon who had colorectal carcinoma or adenomas have also been reported, raising questions in regard to the premalignant potential of these lesions. 2 9 Background & Aims: Hyperplastic polyposis clinically This report describes a morphological reevaluation of 6 resembles adenomatous polyposis and has not gener- patients with hyperplastic polyposis of the colon who ally been considered precancerous. However, since the also had adenocarcinoma of the colon (4 patients) or original description, a number of cases associated with numerous frankly adenomatous foci (2 patients) with speadenocarcinoma have been reported. The aim of this cial reference to the possible neoplastic nature of these study was to reevaluate patients previously diagnosed with hyperplastic polyposis. Methods: Pathological polyps. analysis of polyps in 6 patients with putative hyperplastic polyposis and 4 with associated carcinoma was Materials and Methods compared with classic isolated hyperplastic polyps, ad- Cases that fulfilled the following criteria were included enomas, and solitary serrated adenomas. Immunohis- in the study: (1) colons had to have numerous serrated polyps tochemical study for the detection of p53 protein, blood (i.e., polyps with a sawtooth crypt configuration originally groups antigens, including Lewis a and Lewis b, and pea- diagnosed as hyperplastic polyps), (2) extensive sampling of nut lectin binding was performed. Results: Polyps in our the polyps for histological evaluation had to be performed, and patients were much more similar to serrated adenomas (3) colons had to be resected (for full evaluation). than to hyperplastic polyps and were characterized by Five cases were obtained retrospectively from the consultalarge size, prominent architectural distortion, cytologi- tion files of one of the authors (D.C.S.), and one was obtained cally atypical nuclei, focal nuclear crowding and nuclear from a local hospital after subsequent recognition of the lesion. dispolarity, and rare upper zone mitotic figures. The Routinely formalin-fixed, paraffin-embedded tissue stained polyps in our patients and control serrated adenomas with H&E was available in all cases. Paraffin blocks with reprehad a decrease or absence of endocrine cells compared sentative tissue were available in 5 cases and were studied with with classic hyperplastic polyps and normal colon and Churukian Schenk silver stain and by avidin-biotin complex similar immunohistochemical reactivity for p53 and method for p53 protein (1:1 mixture of clone d07 from DAKO, Lewis a and Lewis b antigens. Conclusions: Our results Carpinteria, CA, and clone 1801 from Oncogene Science, Camindicate that the polyps in our patients are serrated bridge, MA; dilution, 1:2000). In 3 patients with lesions localadenomas. Serrated adenomatous polyposis has not ized in the left colon, an immunohistochemical detection by been described before and should be distinguished avidin-biotin method was performed for blood group subfrom true hyperplastic polyposis given a possible asso- stances including Lewis a and Lewis b (Signet, Dedham, MA; ciation with adenocarcinoma in the former group. dilution, 1:500) and peanut lectin binding (Vector Laboratories, Burlingame, CA; dilution, 1:2000). Control cases were obtained from the files of the Division yperplastic polyposis of the colon is a poorly de- entity which, on endoscopic and/or radiologi- and Pathology, University of Minnesota Hospital and Clinic, of Surgical Pathology, Department of Laboratory Medicine Hfined Minneapolis, Minnesota, and included the following: 15 examcal examination, resembles familial adenomatous polypoples of classic hyperplastic polyp (10 solitary and 5 associated sis. 1 However, the histology of the polyps in hyperplastic with adenoma, see below), 10 cases of classic adenomas (4 polyposis of the colon has been interpreted as that of tubular adenomas, 4 villous adenomas, and 2 tubulovillous hyperplastic polyps, and the condition has hence not been adenomas, selected such that 5 were single adenomas and 5 generally considered precancerous. The group of patients adenomas also had one separate synchronous hyperplastic with this condition have not had a family history of polyp), and 3 cases of solitary serrated adenoma. Controls were colonic disease. They may present with rectal bleeding, selected on the basis of previously described criteria for the perianal hematoma, tenesmus, mucous diarrhea, and abdominal pain. 1 Despite the perceived lack of association 1996 by the American Gastroenterological Association with carcinoma, a number of patients with hyperplastic /96/$3.00

2 March 1996 SERRATED ADENOMATOUS POLYPOSIS 749 Table 1. Clinical and Gross Features of Cases Studied Polyps Synchronous versus Patient Sex/age (yr) No. Size (cm) Shape Distribution Present metachronous 1 M/53 Numerous S Left colon Yes Synchronous 2 M/43 Numerous S Diffuse Yes Synchronous 3 F/85 ú S ú P Diffuse Yes Synchronous 4 M/39 ú S ú P Left colon No 5 M/63 Numerous S, P Diffuse Yes Metachronous 6 M/57 Numerous S ú P Right colon No NOTE. Numerous indicates either more than 100 polyps and/or large areas of the thickened mucosa (carpet-like lesions). P, pedunculated; S, sessile. Cancer diagnosis of hyperplastic polyp, adenoma, and serrated ade- noma. 10,11 The following parameters were evaluated for each polyp: size, presence or absence of a stalk, nuclear atypia (as defined by nuclear enlargement, irregular nuclear membranes, chromatin clumping, conspicuous and/or multiple and irregular nucleoli, and hyperchromasia), shape of the nuclei (round vs. oval vs. elongated), crowding and pseudostratification of nuclei, the presence and distribution of mitotic figures in at least 10 crypts, the length and dilatation of the crypts, serration, the presence of branching and horizontally oriented crypts, the content of goblet cells (absolute content per crypt), and the number of endocrine cells (eosinophilic endocrine cells on H& E and argyrophilic cells on Churukian Shenk stained slides). The terms serrated, serration, and traditional adenomatous change were used as previously described. 10 Serrated and serration refer to a sawtooth crypt configuration due to luminal infoldings, and traditional adenomatous change refers to a polyp with closely spaced tubules (tubular adenoma) and/or villi (villous and tubulovillous adenoma) composed of incom- pletely differentiated columnar cells, usually with decreased mucin content and elongated and pseudostratified nuclei. The presence of mitotic figures in different compartments was designated as b for basal only and as d for diffuse distribution (including the middle and upper zones of the crypt). The content of endocrine cells was determined by counting endocrine cells in at least 10 crypts (every fourth crypt in the polyp was studied) and expressed as an average number per crypt. The distribution of the cytoplasmic reactivity with Churukian Shenk stain was also recorded. All parameters, except the presence and distribution of mitotic figures and content of endocrine cells, were scored on a semiquantitative scale from 0 to 3 as follows: 0, negative; 1/ (mild), focal, scattered, slight; 2/ (moderate), readily apparent; and 3/ (marked), predominant. In each polyp, focal find- ings were also scored separately. The type of the mucosa present at the margins of the 4 carcinomas was examined and designated as either transitional mucosa (nonpolypoid, nonneoplastic colonic or rectal mucosa that lies within a few centimeters of a colorectal adenocarcinoma that shows an increase in mucosal thickness and mild distortion of crypt architecture, increase in goblet cells in crypts, and increase in lamina propria vascularity), traditional adenoma, or serrated polyps. Results Patients The age of the patients; number, shape, average size, and distribution of the polyps; and presence of can- cer are summarized in Table 1. Pathology Macroscopically, the dominant feature of polyps in our patients was their large size (the largest was 4.5 cm with an average of at least 1.2 cm) (Figure 1A and 1B). Patients 1 and 2 had only sessile polyps, whereas the other 4 patients also had rare pedunculated polyps. All 10 control classic hyperplastic polyps were sessile and measured no more than 0.6 cm. Of 10 control adenomas, 3 were sessile and 7 were pedunculated. The largest adenoma measured 2.2 cm. Two of 3 control serrated adenomas were sessile, and 1 was pedunculated. The largest control serrated adenoma measured 2.5 cm. Microscopically, low-power analysis of the polyps in our patients showed serrated, elongated, and greatly di- lated crypts with dilatation most prominent at the base of the crypts (Figure 2). In many areas, there were hori- zontally oriented crypts running just above the muscu- laris mucosae (Figure 3A), often with goblet cells at the base of the crypts (Figure 3B). The content of goblet cells varied from decreased to similar to that of normal mucosa or hyperplastic polyp and to focally increased (Figure 3A). The most dilated crypts had an increased content of goblet cells with mucus collecting in the crypts and on the surface of the mucosa. However, in many areas, there was slight or moderate depletion of the mucin content, which was most frequently found in areas with eosinophilic cytoplasm (Figure 4) or more traditional adenomatous change. These were randomly

3 750 TORLAKOVIC AND SNOVER GASTROENTEROLOGY Vol. 110, No. 3 it was difficult to precisely compare it with polyps in our patients due to more complex architecture. Dilatation of the crypts also varied greatly in different adenomas as well as in different areas of the same adenoma and had no predilection for more prominent dilatation towards the base of the crypts. Some horizontally oriented crypts were present. They were not limited to close proximity of the muscularis mucosae as in our patients, but rather the crypts had a random orientation and distribution. Branching of the crypts was prominent. Three control serrated adenomas by definition had serrated as well as elongated crypts. One case had random dilatation of the crypts as well as randomly distributed crypts with variable orientation, similar to more tradi- tional adenoma. Diminished mucin content was prominent and was accompanied by eosinophilic cytoplasm throughout the polyp. Branching of the crypts was prominent (Figure 5). Two control serrated adenomas had areas that were identical to those found in our patients in addition to the above-described features. Medium- and high-power analysis of our 6 cases showed mainly round and oval nuclei located basally in the cell with very focal nuclear elongation, crowding, and pseudostratification (Figure 6). Mitotic figures were found in the base and middle zones of the crypts with rare mitotic figures present in the upper zone and surface. Nuclear atypia, including nuclear enlargement, irregular nuclear membranes, chromatin clumping, hyperchromasia, and prominent single or multiple large nucleoli, was uniformly present. Fifteen control hyperplastic polyps had uniform round or focally, slightly elongated nuclei. No prominent elongation, crowding, and pseudostratification was found. Mitotic figures were limited to the basal zones of the crypts. In 6 of 10 polyps, there were also vesiculated distributed. Serration of the crypts was prominent and extended deeply into the crypts, some of which were serrated at the base (Figure 2). Branching of the crypts was absent or minimal. Fifteen control classic hyperplastic polyps were serrated with slightly to moderately elongated crypts that were only focally slightly dilated. No horizontally oriented crypts were present. The content of goblet cells was evaluated in the upper and middle zones of the crypts and was increased; however, no mucus accumulation was noted in the crypts or on the surface. Although serration of the crypts was prominent, in 6 polyps it was limited to the upper zone, in 2 it extended also into the middle zone, and in the remaining 2 it closely approached the base of the crypts. No definite branching was present. Ten control traditional adenomas showed no serration. Variable elongation of the crypts was present; however, Figure 1. Gross specimen from patient 3. (A) Note the presence of several sessile elevations of the mucosa with the appearance of thickened folds lighter in color than the surrounding mucosa (arrows). (B) Cut section through one of these sessile lesions (top section in figure with margins of the lesion marked by arrows) shows thickening of the mucosa in comparison with a section of noninvolved mucosa from the same specimen (bottom section in figure). Note that the increase in thickness is confined to the mucosa; the total wall thickness is essentially unchanged. Figure 2. A sessile serrated polyp from one of our patients with markedly dilated crypts more prominent at the base. Some crypts show serration at the base (arrow).

4 March 1996 SERRATED ADENOMATOUS POLYPOSIS 751 Figure 5. Control solitary serrated adenoma. Serration, branching of the crypts, nuclear atypia, and moderately decreased mucin content are noted. Ten control adenomas had crowded oval or elongated nuclei. In rare, cystically dilated crypts, there was no nuclear crowding, and nuclei were round or oval. The nuclei were located basally in the cell in 7 polyps at least focally; however, for the most part, there was prominent pseudostratification. Mitotic figures were frequently found throughout the crypts, including the surface. Nuclear enlargement, irregular nuclear membranes, chromatin clumping, hyperchromasia, and prominent nucleoli were also prominent. One control serrated adenoma had nuclear features very similar to the above-described more traditional ade- noma. Two other cases, in areas that were on low power architecturally identical to polyps in our patients, also had nuclear features comparable with them (Figure 8). In our patients, the contents of endocrine cells assessed by analysis of H&E-stained sections showed complete Figure 3. (A) Horizontally oriented crypts are typically present just above muscularis mucosae. Overall mucin production is comparable with normal mucosa and/or hyperplastic polyp. (B) Numerous goblet cells are present at the base of this crypt (note the muscularis mucosae just visible in the lower right corner). Focal decreased mucin content and nuclear elongation, and crowding is present toward luminal aspect of this crypt. nuclei (mostly in the basal and middle zones) that contained small inconspicuous single nucleoli. However, there was no significant nuclear enlargement, no irregular nuclear membranes, and no hyperchromasia (Figure 7). Figure 4. Decreased mucin content is apparent in these irregularly shaped serrated crypts. The cytoplasm is eosinophilic in some segments of these crypts (arrows). Figure 6. Nuclear elongation, pseudostratification, and nuclear crowding in sessile serrated adenomas in our patients varied in extent; however, they were mainly focal and could be easily overlooked at low power.

5 752 TORLAKOVIC AND SNOVER GASTROENTEROLOGY Vol. 110, No. 3 The contents of endocrine cells assessed on Churukian Shenk-stained slides paralleled results obtained on H&E-stained slides. In polyps from our patients, typical endocrine cells with strong subnuclear staining were ab- sent, although rare cells that had centrally located nuclei showed diffuse weak cytoplasmic staining. Adjacent his- tologically normal mucosa and control hyperplastic polyps had strongly stained endocrine cells with a predomi- nately subnuclear staining pattern. Control adenomas and serrated adenomas showed both strongly and weakly stained cells. Serrated adenomas, in areas identical to polyps in our patients, had a few weakly stained cells and very rare strongly stained cells. Two patterns of p53 positivity were observed in our patients and control serrated adenomas: a focal positivity in proliferation zones and a single cell pattern (frequently the cells that lost polarity or were dysmorphic goblet cells). Tubular/tubulovillous adenomas had p53 positiv- ity in either diffuse or focal distribution (random cell groups throughout the adenoma). Two hyperplastic polyps diffusely overexpressed p53, whereas 13 others were negative, including in the proliferation zones. Serrated polyps in our patients coexpressed Lewis a and Lewis b antigens either diffusely (1 patient) or focally (2 patients). The coexpression of these antigens was also seen in 3 of 3 control serrated adenomas, 4 of 15 hyperplastic polyps, and 5 of 10 control tubular/tubulovillous adenomas. Apical and/or glycocalyx binding of peanut lectin was seen at least focally in serrated polyps in our patients, 3 of 3 control serrated adenoma, 3 of 15 hyperplastic polyps, and 2 of 10 control tubular/tubulovillous adenomas. The mucosal margins of all four carcinomas (patients absence or very rare eosinophilic endocrine cells in the polyps, whereas adjacent, histologically normal appearing mucosa had 1 7 eosinophilic endocrine cells per crypt (average, ú2.6; located mainly at the basal zone of the crypts). Nine control hyperplastic polyps had normal and 6 had increased eosinophilic endocrine cells (average, ú4.6 per crypt; mainly at the basal and middle zones, some at the surface). Control adenomas showed great variability in the contents of eosinophilic endocrine cells, which also varied in different areas of the same adenoma. Some crypts contained numerous endocrine cells, whereas others had none. Overall, in 10 control traditional adenomas, the contents of eosinophilic endocrine cells was decreased to an average of õ2.0 per crypt. Three serrated adenomas also showed variable contents of eosinophilic endocrine cells, which were also absent or very rare in areas that resembled those of polyps in our patients, and variable, with an average of per crypt, in more adenomatous but also serrated areas. Figure 7. Comparison of the (A) control hyperplastic polyp and (B) a sessile serrated polyp (patient 3). Although these areas have almost identical low-power appearance, the nuclei in the hyperplastic polyp are small and only occasional nuclei contain inconspicuous nucleoli. The nuclei in the sessile serrated polyp are larger and have prominent nucleoli. Figure 8. Comparison of the nuclear features in the least atypical areas in a control isolated serrated adenoma (right) and a sessile serrated polyp from one of our patients that was initially diagnosed as a hyperplastic polyp (left) (patient 3). Both polyps have large round nuclei with prominent nucleoli. Depletion of mucin content is more prominent in the control serrated adenoma, whereas both have irregular distribution of goblet cells.

6 March 1996 SERRATED ADENOMATOUS POLYPOSIS 753 Table 2. Histological Findings: Comparison of Sessile Serrated Adenoma With Control Polyps and Normal Mucosa Normal Our Control Control Control serrated mucosa a patients hyperplastic polyp adenoma adenoma No. of cases Crypts Elongation 0 /// // ////// ////// Dilation 0 /// b 0// 0//// ///// Branching 0 0// 0 0//// 0/// Horizontal orientation 0 /// 0 0/// ///// Serration 0 /// /// 0 /// Goblet cells // ///// c /// 0/// ///// Eosinophilic cytoplasm 0 ///// 0 0 ////// Nuclei Atypia d 0 ///// 0// /// /// Elongation 0 0/// e 0// ////// 0//// Crowding 0 0// 0// /// 0//// Pseudostratification 0 0// 0// /// 0//// Mitotic figures b b/d e b d b/d Endocrine cells H&E // 0 ////// 0//// 0/// Churukian Shenk // 0// ////// 0//// 0// a Adjacent to polyps (7 cases had no adjacent normal appearing mucosa); 0, not present; /, rare, focal; //, readily apparent; ///, predominant. b At the base of the crypt (typically, the dilated bases of the crypts contain mature goblet cells). c Random distribution of mucin-depleted areas (accompanied with mitoses and interpreted as proliferation zones). d Nuclear atypia as defined by nuclear enlargement, irregular nuclear membranes, chromatin clumping, hyperchromasia, and large prominent nucleoli. e Minimal. b, basal; d, diffuse; slash separates different areas. 1, 2, 3, and 5) was transitional mucosa. In patient 2, the of 7 patients with colons showing an endoscopic or gross carcinoma was focally surrounded by a large serrated appearance of polyposis coli but in which the polyps had a polyp; however, the patient had numerous large serrated histological appearance interpreted as that of hyperplastic polyps in that area, so it was not clear whether the carcidrome polyps. 1 The specific polyps associated with this syn- noma originated in the polyp or merely extended into were not illustrated. None of the original cases of it. Williams et al. were associated with carcinoma or with Results of the histological study and Churukian a positive family history of polyposis. Reports of similar Schenk staining are summarized in Table 2. Reactivity cases by other investigators in small series or case reports for p53, blood group antigens, and peanut lectin binding included patients who had synchronous or metachronous are shown in Table 3. adenocarcinoma of the colon. 2 9 Of all reported cases, Discussion including the present series, 47% have been associated with adenocarcinoma. Review of the literature, including The term hyperplastic/metaplastic polyposis was the present cases, would indicate that association with introduced in 1980 by Williams et al. to describe a series carcinoma is possible and suggests that a review of the Table 3. Immunohistochemical Findings: Comparison of Sessile Serrated Adenoma With Control Polyps and Normal Mucosa Normal Our Control hyperplastic Control Hyperplastic polyps Control serrated mucosa a patients polyps adenomas associated with adenoma adenomas No (5) c Coexpression of Le a and Le b a/g peanut agglutinin Both b p a Normal appearing mucosa adjacent to polyps. b Both, coexpression of Lewis antigens and a/g binding of peanut agglutinin. c Five patients were studied only for p53. a/g peanut agglutinin, apical and/or glycocalyx reactivity for peanut agglutinin, focal only.

7 754 TORLAKOVIC AND SNOVER GASTROENTEROLOGY Vol. 110, No. 3 hyperplastic nature of the polyps as well as natural sions as neoplastic are the results of Churukian Shenk history and the risk of developing carcinoma are in order. staining. The polyps in our series showed few or no Our study addressed pathological findings in 6 patients endocrine cells in contrast to classical hyperplastic polyps with numerous serrated polyps. that always contained these cells, frequently in greater Careful pathological analysis of the lesions in our pamas numbers than normal mucosa. Classic and serrated adenotients indicates that although they have a superficial apbers contained fields with decreased and increased num- pearance of hyperplastic polyp, including a sessile growth of endocrine cells within a single adenoma, which pattern, serrated crypts, and frequently basally located is a well-recognized pattern in adenomas. 17,18 In serrated nuclei, they also have many features that are not found adenoma, clusters of endocrine cells were present mainly in classic hyperplastic polyps. Most of the histological in areas similar to classic adenoma. Weak diffuse cyto- features are those of serrated adenoma, a term proposed plasmic staining, as seen occasionally in polyps from our by Longacre and Fenoglio-Preiser in an analysis of lesions patients, is not unusual in the neoplastic colon. 19 showing features originally interpreted as mixed hyperdistinction The immunohistochemical studies were less helpful in plastic-adenomatous polyps. 10,12 Although mixed hywith of serrated adenoma from hyperplastic polyp perplastic-adenomatous polyps composed of discrete areas results similar to those in previous studies of neoplastic and hyperplastic polyp together in the same Polyps in our patients and control serrated adenomas lesion exist, serrated adenomas are true adenomas that showed the same pattern of positivity for p53; a weak are serrated but may show a spectrum of morphological positivity in proliferation zones and strong positivity in features, some more similar to hyperplastic polyps and scattered single cells. Two of 10 hyperplastic polyps some more similar to adenoma. 10,12 16 In our series, serpolyps showed diffuse overexpression of p53. These hyperplastic rated adenomas showed the whole spectrum of morphowith were the same two that showed discordant results logical features described by Longacre and Fenogliomorphology peanut lectin, Lewis a, and Lewis b. However, their Preiser. 10 The morphological features of most serrated was that of a classic hyperplastic polyp. The adenomas in our patients, when viewed in a morphologipression biological significance of these findings is not clear. Coex- cal spectrum described by Longacre and Fenoglio-Preiser, of Lewis a and Lewis b as well as apical/glycocalyx belong to those that somewhat resemble hyperplastic binding of peanut lectin were seen in serrated polyps in polyps. These investigators also indicate that such polyps our patients, which was in accordance with previous stud- may be misinterpreted as hyperplastic polyps. 10 Al- ies of dysplastic and carcinomatous colonic mucosa though all our patients had true serrated adenomatous We have studied large numbers of polyps in our patients, polyposis, only 5 of 95 patients included in the study but the number of cases was too small for any definitive by Longacre and Fenoglio-Preiser had more than one conclusions regarding immunohistochemical pattern of lesion (the greatest number in any patient was 7). 10 Based reactivity for the above antigens. on morphological analysis of numerous and large serrated The illustrations of cases previously reported as hyperplastic adenomas in our patients that encompassed the whole polyposis or giant hyperplastic polyps associated spectrum of possible appearances of serrated adenomas with adenocarcinoma have in most cases inadequate photographic described previously, 10 we have found the following criteria documentation of the polyps to enable comdescribed to be helpful in the distinction of hyperplastic polyp plete comparison with our patients. A striking similarity like serrated adenoma from hyperplastic polyp: (1) dilatation to our polyps is found in cases reported by Heng et al. of the crypts that is most prominent in the base; and Cooper et al. 6,9 The case reported by Sumner et al. (2) presence of horizontally oriented crypts; (3) large areas is included in our study (patient 5). 2 without endocrine cells on H&E- or Cherukian Shenk- All of these features together lead to the conclusion stained sections; (4) nuclear atypia, including basally that the term hyperplastic polyposis is a misnomer at located oval or round nuclei that are enlarged, hyperchro- least for our cases and some cases previously described matic, and have prominent nucleoli; (5) focal mucus over- in the literature. We suggest that serrated adenomatous production (resembling mucinous cystadenomas of the polyposis be considered in the differential diagnosis of appendix); (6) proliferation zone frequently moved from hyperplastic polyposis as described by Williams et al., 1 the base of the crypt to a middle or upper portion of the especially because the latter showed no association with crypt with the presence of the numerous goblet cells in the development of adenocarcinoma. 1 The natural history the base of the crypts (which parallels the distribution and a risk of developing carcinoma in patients with serof mitotic figures); and (7) frequent (focal or diffuse) rated adenomatous polyposis need to be further exameosinophilia of the cytoplasm. ined. Supporting the histological interpretation of our le- In summary, our study is the first to describe true

8 March 1996 SERRATED ADENOMATOUS POLYPOSIS 755 polyposis with serrated adenomas. It also confirms that 15. Franzin G, Novelli P. Adenocarcinoma occurring in a hyperplastic (metaplastic) polyp of the colon. Endoscopy 1982;14: serrated adenomas have variable histological appearances, 16. Franzin G, Zamboni G, Scarpa A, Dina R, Iannucci A, Novelli P. including those adenomas that resemble hyperplastic pol- Hyperplastic (metaplastic) polyps of the colon: a histologic and yps; this was the basis for the initial interpretation of histochemical study. Am J Surg Pathol 1984;8: Kaye GI, Fenoglio CM, Pascal RR, Lane N. Comparative electron these polyps as hyperplastic polyps and the polyposis as microscopic features of normal, hyperplastic, and adenomatous hyperplastic polyposis. The above-listed criteria, which human colonic epithelium. Gastroenterology 1973;64:926 are helpful in distinguishing serrated adenomas from hy perplastic polyps, are a combination of previously deof the intestines. Washington, DC: Armed Forces Institute of 18. Fenoglio-Preiser CM, Pascal RR, Perzin KH. Adenomas. Tumors scribed features by Longacre and Fenoglio-Preiser 10 and Pathology, 1988: features derived from this study. The importance of these 19. Smith DM, Haggitt RC. The prevalence and prognostic signifi- criteria is not only for the accurate identification of ser- cance of argyrophil cells in colorectal carcinomas. Am J Surg Pathol 1984;8: rated adenomatous polyposis but also for the accurate 20. Yuan M, Itzkowitz SH, Palekar A, Shamsuddin AM, Phelps PC, identification of solitary serrated adenomas. Trump BF, Kim YS. Distribution of blood group antigens A, B, H, Lewis a, and Lewis b, in human normal, fetal, and malignant colonic References tissue. Cancer Res 1985;45: Cooper HS, Marshall C, Ruggerio F, Steplewski Z. Hyperplastic 1. Williams GT, Arthur JF, Bussey HJR, Morson BC. Metaplastic polyps of the colon and rectum: an immunohistochemical study polyps and polyposis of the colorectum. Histopathology with monoclonal antibodies against blood groups antigens (Si- 1980;4: alosyl-le a,le b,le x,le y, A, B, H). Lab Invest 1987;57: Sumner HW, Wasserman NF, McClain CJ. Giant hyperplastic pol- 22. Cordon-Cardo C, Lloyd KO, Sakamoto J, McGroarty ME, Old LJ, yposis of the colon. Dig Dis Sci 1981;26: Melamed MR. Immunohistologic expression of blood-group anti- 3. Bengoechea O, Martinez-Penuela JM, Larrinaga B, Valerdi J, gens in normal human gastrointestinal tract and colonic carci- Borda F. Hyperplastic polyposis of the colorectum and adenocar- noma. Int J Cancer 1986;37: cinoma in a 24 year-old-man. Am J Surg Pathol 1987;11: Blaszczyk M, Pak KY, Herlyn M, Sears HF, Steplewski Z. Charac terization of Lewis antigens in normal colon and gastrointestinal 4. McCann BG. A case of metaplastic polyposis of the colon associated adenocarcinoma. Proc Natl Acad Sci USA 1985;82: with focal adenomatous change and metachronous adeno- 24. Cooper HS, Reuter VE. Peanut lectin-binding sites in polyps of carcinomas. Histopathology 1988;13: the colon and rectum: adenomas, hyperplastic polyps, and ade- 5. Kusunoki M, Fujita S, Sakanoue Y, Shoji Y, Yanagi H, Yamamura nomas with in situ carcinoma. Lab Invest 1983;49: T, Utsunomiya J. Disappearance of hyperplastic polyposis after 25. Jass JR. Relation between metaplastic polyps and carcinoma of resection of rectal cancer: report of two cases. Dis Colon Rectum the colorectum. Lancet 1983;1: ;34: Jass JR, Filipe MI, Abbas S, Falcon CAJ, Wilson Y, Lovell D. A 6. Heng Teoh H, Delahunt B, Isbister WH. Dysplastic and malignant morphologic and histochemical study of metaplastic polyps of areas in hyperplastic polyps of the large intestine. Pathology the colorectum. Cancer 1984;53: ;21: Cooper HS, Reuter VE. Peanut lectin-binding sites in polyps of 7. Spjut HJ, Estrada RG. The significance of epithelial polyps of the the colon and rectum. Lab Invest 1983;49: large bowel. Pathol Annu 1977;12: Boland CR, Montgomery CK, Kim YS. A cancer-associated mucin 8. Cooke SAR. Polyposis coli: the clinical spectrum in adults. S Afr alteration in benign colonic polyps. Gastroenterology 1982; Med J 1978;53: : Cooper HS, Patchefsky AS, Marks G. Adenomatous and carcinonohistochemical 29. Hamana T, Kawai K, Serizawa A, Tsutsumi Y, Watanabe K. Immumatous changes within hyperplastic colonic epithelium. Dis demonstration of p53 protein in colorectal ade- Colon Rectum 1979;22: nomas and adenocarcinoma. Reliable application of the heat- 10. Longacre TA, Fenoglio-Preiser CM. Mixed hyperplastic adenomabedded induced antigen retrieval method to formalin-fixed, paraffin-emtous polyps/serrated adenomas: a distinct form of colorectal material. Pathol Int 1994;44: neoplasia. Am J Surg Pathol 1990;14: Wobler R, Owen D. Differential expression of p53 protein in co- 11. Fenoglio CM, Kaye GI, Pascal RR, Lane N. Defining the precursor lonic adenomas containing invasive carcinoma, in-situ carcinoma tissue of ordinary large bowel carcinoma: Implications for cancer and pseudoinvasion (abstr). San Francisco: US and Canadian prevention. Pathol Annu 1977;12: Academy of Pathology, March 12 18, Urbanski SJ, Marcon N, Kossakowska AE, Bruce WR. Mixed hyperplastic adenomatous polyps: an underdiagnosed entity. Am J Received February 14, Accepted October 6, Surg Pathol 1984;8: Address requests for reprints to: Dale C. Snover, M.D., Department 13. Goldman H, Ming SC, Hickok DF. Nature and significance of hy- of Pathology, Fairview Southdale Hospital, 6401 France Avenue perplastic polyps of the human colon. Arch Pathol 1970;89:349 South, Edina, Minnesota Fax: (612) Presented in part at the 83rd annual meeting of the United States 14. Estrada RG, Spjut HJ. Hyperplastic polyps of the large bowel. Am and Canadian Academy of Pathology in San Francisco, California, J Surg Pathol 1980;4: March 12 18, 1994.

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