Multiparameter Flow Cytometric Analysis of Colon Polyps

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1 Multiparameter Flow Cytometric Analysis of Colon Polyps BARBARA F. BANNER, M.D., MARY S. CHACHO, M.D., DAVID L. ROSEMAN, M.D., AND JOHN S. COON, M.D., PH.D. Sixty-eight colonic polyps of various histologic types were studied using retrospectiveflowcytometric (FCM) DNA analysis to determine the prevalence of aneuploid cell populations and whether they were associated with any particular histologic features. Overall, 13 of 68 polyps (19%) contained DNA-aneuploid cells, including 3 of 9 villous and 4 of 10 villoglandular polyps with histologic features of carcinoma in situ (OS), 4 of 11 villous and 1 of 18 villoglandular polyps without CIS, and 1 of 12 adenomatous polyps. Eight hyperplastic polyps were diploid. These results show (1) retrospective FCM analysis can detect DNA aneuploidy in polyps; (2) DNA aneuploidy may occur before histologic evidence of invasive carcinoma; and (3) this change is more frequent in types of polyps thought to have increased malignant potential (i.e., those with villous morphology and/or CIS). (Key words: Colon polyps; DNA aneuploidy; Flow cytometry) Am J Clin Pathol 1987; 87: COLON POLYPS have a definite but unpredictable potential to become malignant, 9 but detection of early malignant change is difficult by both histologic and clinical evaluation. Because DNA aneuploidy is typical of invasive colon carcinomas, 1 ' 10,12,18 it is reasonable to expect that it might also be present in polyps in the process of malignant transformation. The capacity of flow cytometry to detect parameters such as aneuploid DNA content, present in only a small fraction of the cells being analyzed, makes it an ideal technic for analyzing polyps. Furthermore, the recent development by Hedley and colleagues 6 of a method for performing FCM analysis on paraffinembedded tissue allows study of archival material. The aim of this study, then, was to analyze colon polyps of various types retrospectively to determine the prevalence of DNA aneuploidy and to determine whether DNA aneuploidy was related to histologic type and/or established features predictive of malignant potential in colon polyps. Case Material Materials and Methods Polypectomy specimens in the surgical pathology files of Rush-Presbyterian-St. Luke's Medical Center from Received April 1, 1986; received revised manuscript and accepted for publication July 17, Address reprint requests to Dr. Coon: Department of Pathology, Rush- Presbyterian-St. Luke's Medical Center, 1753 W. Congress Parkway, Chicago, Illinois Rush-Presbyterian-St. Luke's Medical Center, Chicago, Illinois, and Montefiore Hospital, Bronx, New York 1975 to 1980 were screened; and those with the entire polyp present and well preserved in the specimen, and available paraffin blocks were included in the study. A group of 68 polyps was thus obtained, including 8 hyperplastic, 12 adenomatous, 18 villoglandular, 11 villous, and 10 villoglandular and 9 villous polyps with carcinoma in situ (CIS) confined to the polyp. The polyps were classified with the use of standard histologic criteria." The villoglandular polyps, in particular, were defined by the presence of villous fronds in from 20% to 50% of the polyp. CIS was defined as disorganized, complex architecture with cytologically malignant cells within the epithelial compartment of the polyp, without invasion of stroma. The patients included 44 men and 24 women, age range Sixty-two were resected by endoscopic polypectomy, 6 by segmental colonic resection. Twenty-one polyps were submitted with other resected polyps; the remainder were solitary specimens. One polyp was associated with a synchronous separate colon carcinoma. Tissue Preparation Blocks for FCM analysis were prepared with the use of a modification of the method of Hedley and associates. 6 Thirty-micron sections cut from the formalin-fixed, paraffin-embedded tissue blocks were dewaxed, rehydrated, and mechanically minced with scissors. A conventional thin histologic section deep to the thick section for FCM analysis was stained and examined to verify the morphologic characteristics of the specimen. The tissue was digested with 0.5% (5 g/l) pepsin (Sigma, St. Louis, MO) in 0.9% (9 g/l) NaCI at ph 1.5 for 30 minutes at 37 C to produce a suspension of bare nuclei. The suspension was washed and filtered through a 41 nm nylon mesh to remove aggregates, and the concentration was adjusted to 2 X 10 5 nuclei/ml. The nuclei were incubated for 10 minutes with 0.1 mg/ml (0.1 g/l) Ribonuclease A (Sigma) then stained for DNA with propidium iodide (Sigma) at 0.13 mg/ml (0.13 g/l) for 15 minutes, according to the method of Vindelov and associates. FCM analysis was conducted within one hour of staining. For 313

2 314 BANNER ET AL. AJ.C.P. March 1987 Table 1. DNA Analysis of Polyps in Relation to Histologic Type Type Hyperplastic Adenomatous Villoglandular Villoglandular (with CIS) Villous Villous (with CIS) Total Number Diploid Nondiploid (19%) DNA Ind< , 1.37, 1.43, , 1.16, 1.22, , 1.37, 1.66 FCM analysis, nuclei were adjusted to a concentration of 5 X 10 5 /ml in trisodium citrate buffer. Flow Cytometry The relative DNA content (red fluorescence) of 10 5 nuclei was analyzed in a Coulter Epics V (Hialeah, FL) flow cytometer equipped with a Coherent (Worcester, MA) argon ion laser operating at 200 mw at 488 nm. All tumor samples contained diploid inflammatory and stromal cells that served as an internal diploid standard as previously described. 6 The high voltage of the photomultiplier tube was adjusted so that the G0G1 peak of the diploid cells was located in channel 50 of a total of 256 channels. Nondiploid populations were defined by the presence of a discrete G0G1 population differing from the diploid peak by at least 10%. The DNA index for nondiploid populations was calculated as the quotient of the channel of the nondiploid peak divided by the channel of the diploid peak. We developed a gating routine to reduce contamination of tumor cell DNA histograms by nuclear aggregates and inflammatory cells, which may be a large component of some polyps. Four measurements for each of 10 5 nuclei stained with propidium iodide were collected in a list mode file for subsequent analysis: integral red fluorescence, peak red fluorescence, forward light scatter (related to nuclear size), and 90 degree light scatter (related to nuclear size and structure). Inflammatory cell nuclei were excluded by correlated measurement of the scatter parameters, while doublet discrimination was achieved by gating on peak versus integral red fluorescence. The boundaries of the inflammatory cell "window" were set by analysis of nuclei derived from normal, paraffinembedded lymphoid tissue. Results All specimens produced interpretable histograms, defined as having at least one G1G0 peak with a coefficient of variation of less than 10%. Overall, DNA aneuploid cells were detected in 13 of 68 polyps (19%), as shown in Table 1. With the exception of 1 adenomatous polyp, all of the aneuploid cell populations occurred in polyps with villous features (P < 0.001); 5 of 28 villoglandular polyps (18%) and 7 of 20 villous polyps (37%) contained DNAaneuploid cell populations. Aneuploidy was associated with histologic atypia, being present in 7 of 19 (37%) polyps with CIS. No hyperplastic polyps contained aneuploid cells. Comparison of gated versus ungated DNA histograms showed enhanced detection of aneuploid peaks with significant reduction of contamination with inflammatory cells and aggregates (Fig. IA). Within each histologic category, there were no detectable morphologic differences between polyps with and without an aneuploid stem line. In more detail, the group of polyps with histologically identifiable CIS contained a large proportion with aneuploid cell populations (7 of 19 polyps, 37%), as compared with the group without CIS (6 of 49 polyps, 12%). However, when polyps with villous features with and without CIS were compared for the frequency of aneuploid cells, there was no statistically significant association of aneuploidy with CIS (0.10 < P < 0.25). An example of an aneuploid DNA histogram from a villous adenoma with CIS is shown in Figure I A. The foci of CIS were characterized by complex architecture with secondary gland formation, papillary tufting of the epithelium, aberrant distribution of goblets, and occasionally necrosis (Fig. IB). These areas were usually multifocal and sharply demarcated from the surrounding benign polyp, which was classified as villoglandular in ten cases and villous in nine. The aneuploid and diploid polyps with CIS could not be distinguished by histologic features during blind examination. The ten villoglandular polyps with CIS came from five men andfivewomen from 45 to 84 years of age. One was removed by a segmental resection; the others were removed endoscopically. The four aneuploid polyps in this group ranged in size from 1.2 to 3.4 cm in diameter; the six diploid polyps were cm. There was no significant difference in polyp size when the aneuploid and diploid groups were compared by a two-tailed F-test and by a one-tailed Mest of the means. The nine villous adenomas with CIS came from five men and four women, ages years. One was removed by segmental resection. The three aneuploid polyps in this group were 1.0, 1.5, and 9.5 (aggregate) cm in diameter; the diploid polyps were cm. The size difference between these two groups was significant according to analysis by a two-tailed F-test and a one-tailed Mest of the means. The 11 villous adenomas came from seven males and four females, ages years. In three cases the polyps were removed by resection, and these ranged in size from 1.8 to 4.0 cm in diameter. The four polyps containing aneuploid cells ranged in size from 0.5 to 2.5 cm; the diploid polyps were cm.

3 Vol. 87 No. 3 FLOW CYTOMETRY OF COLON POLYPS 315 V,'-' %. : ' ; ' * r < &. - %* 1 'I /i i, H :-». JZ T ^ 192 RED FLUORESCENCE IDNA) FIG. 1. Villous adenoma with carcinoma in situ and aneuploid DNA histogram. A (upper, left). DNA histogram showing scattergram with gating windows drawn around areas expected to contain primarily inflammatory cells (/) and tumor cells (T) (upper, left); total histogram containing both diploid and aneploid peaks (upper, right); diploid histogram from inflammatory cell area (lower, left); and histogram from tumor cell area showing isolated aneuploid population (lower, right). B (upper, right). Light microscopic section showing a focus of carcinoma in situ (arrow) among the simpler, benign glands of the polyp. Hematoxylin and eosin (XI40). FlG. 2. Villoglandular polyp with diploid DNA histogram. A (lower, right). DNA histogram showing total population (above) and population gated to enhance tumor cell component (below). Both histograms are diploid. B (lower, left). Light microscopic section showing the mixed tubular and villous elements of the polyp. Hematoxylin and eosin (XI40). The 18 villoglandular polyps came from ten men and eight women, from 50 to 77 years of age. All were removed endoscopically, and eight were submitted along with one or more other polyps. An example of 1 of the 17 diploid polyps is shown in Figures 1A and B. The one polyp with DNA aneuploidy (DNA index 1.18) was from a 69-year- old man. It was 1.0 cm in diameter and was one of six villoglandular polyps that displayed histologic features of cell atypia, characterized by foci of hypercellularity with irregular stratification of nuclei and occasional secondary gland formation. However, scattered foci like this were present in the diploid polyps as well, and this polyp was

4 316 BANNER ET AL. AJ.C.P. March 1987 FIG. 3. Adenomatous polyp with aneuploid DNA histogram. A (upper, left). DNA histogram showing total population (above) and population gated to enhance tumor cell component (below). The aneuploid peak is prominent in the gated histogram. B (upper, right). Light microscopic section showing the tubular architecture and bland epithelium of the polyp. Hematoxylin and eosin (X140). FIG. 4. High-power microscopic sections of the aneuploid polyp in Figure \A (A, center, left), the diploid polyp in Figure 2B (B, lower, left), and the aneuploid polyp in Figure 3C(C, lower, right), demonstrating the similarity of their epithelia. Hematoxylin and eosin (X875). We were unable to predict which polyps were aneuploid on the basis of histologic examination. not distinct from the others. Indeed, aneuploidy could not be predicted on the basis of histologic examination during blind examination of the villoglandular and villous polyps. The 12 adenomatous polyps came from ten men and two women from 46 to 77 years of age. All were removed endoscopically and five were submitted along with other excised polyps, indicating multiplicity. The one polyp that contained DNA-aneuploid cells (DNA index 1.27) was 0.7 cm in diameter, from a 46-year-old man who had a villoglandular polyp removed as well. The histogram and histologic characterisitics are shown in Figures 3A and B. Histologically, the polyp did not display any unusual features. It was composed of simple tubular structures with regular, evenly distributed gland lumina lined by a single layer of epithelial cells, many glands were hypercellular with no goblet formation, but the cell nuclei were small and basally situated. The eight hyperplastic polyps came

5 Vol. 87 No. 3 FLOW CYTOMETRY OF COLON POLYPS 317 from seven men and one woman, ages years. All of the polyps were removed endoscopically, were less than 1.0 cm, and were diploid. Discussion Several preneoplastic states of the colon with propensity for eventual development of colon carcinoma have been recognized. These include polyposis syndromes, 9 solitary polyps with villous architecture and histologic atypia, 9 and inflammatory bowel disease. 13 There are currently no reliable indicators as to which patients' conditions will progress to overt cancer or when in a given patient's course this will occur. In the case of polyps, size greater than 2.0 cm and presence of dysplasia regardless of histologic type were associated with increased risk for development of malignancy in Morson and Dawson's studies of thousands of polyps. 9 Aneuploid DNA content has been reported in colon carcinomas with frequencies from 40% 18 to 75%.' Thus, it is reasonable to expect polyps with malignant foci and perhaps even those in the process of malignant transformation to contain aneuploid cell populations. Because FCM conveniently analyzes many thousands of cells individually, it can detect aneuploid cell populations that constitute only a small fraction of the cells being analyzed. The novel gating procedure that we used for exclusion of inflammatory cells significantly increased the sensitivity of the technic for detection of DNA aneuploidy. Thus, this technic should be ideal for detecting malignant cell populations in lesions such as polyps, where aneuploid cells may be exceedingly sparse and the histologic and clinical appearance is benign. The recent development by Hedley and associates 6 of a method for preparing bare nucleus suspensions for FCM analysis from paraffin blocks now permits FCM analysis and histologic evaluation on the same section of tissue. The ability of FCM to detect malignant tumors at a time when they are undetectable by any other means has already been demonstrated in the urinary bladder. 2 Also, the efficacy of FCM analysis in detecting minute cell populations in paraffin-embedded biopsy-size samples has been well established for bladder biopsies. 3 The presence of DNA aneuploid cell populations in 19% of the polyps in our study is of note because no invasive carcinomas were included. The incidence of aneuploidy in premalignant lesions of the colon is not established, although abnormalities have been detected in a number of cytogenetic, 3 ' 7 ' 8 microspectrophotometric 12 and FCM studies Lubs and Clark 7 found abnormal numbers and architecture of chromosomes in karyotypes prepared from cell suspensions of fresh tissue from colonic adenomas and carcinomas. One adenomatous polyp had a normal karyotype. Enterline and Arvan 4 found abnormal ploidy and abnormal individual chromosomes in karyotypes of adenocarcinomas, adenomas, and adenomas with atypia, but not in inflammatory lesions of the colon. Similarly, Mark and co-workers found pseudodiploidy and hyperdiploidy in karyotypes of polyps from a patient with Gardner's syndrome. Stich and colleagues 14 studied the DNA content of mitotic cells from eight colonic polyps and ten carcinomas by microspectrophotometry of Feulgen-stained nuclei. Two of eight polyps contained mitotic cells with more than 4 N DNA content, indicating DNA aneuploidy. The carcinomas all contained aneuploid cell populations. Two other FCM studies of ploidy in colon polyps agree that aneuploid cells are present in polyps, although not with the same frequency as in established carcinomas. Weiss and colleagues 17 performed cell cycle analysis and DNA distribution by FCM analysis of fresh tissue from 64 colon polyps, including 41 tubular adenomas and 23 tubulovillous adenomas with varying degrees of dysplasia. Comparable to our study, aneuploid stem lines were found in about 20% of the polyps, associated with dysplasia. Van den Ingh and associates" studied bare nucleus suspensions of cells scraped fresh from the surface of 55 colon polyps larger than 0.5 cm, 16 colon carcinomas, and 9 control specimens. Aneuploid cell populations were detected in 56% of the carcinomas, 27% of the polyps (but not the hyperplastic polyps), and in one inflammatory polyp. Presence of aneuploidy was related to polyp size, and the DNA index of aneuploid polyps was higher (but not significantly higher) for those of tubulovillous than adenomatous type. In three studies, then, of preparations of fresh tissue 17 and of cells scraped from the surface 15 and our study of paraffin-embedded sections of polyps, the incidence of DNA aneuploidy in colonic polyps is in the range of 20%. Our findings agree with the others in the association of DNA aneuploidy with polyps with villous features 15 and with polyps containing histologic atypia The association of aneuploidy with size was not as clear in our study as it was in that of Van den Ingh and co-workers. 15 In our villoglandular group there was no difference in size between aneuploid and diploid polyps in both a two-tailed F-test and a one-tailed Mest of the means. In the villous groups, however, there was a significant size difference, and this was because of one 9.5- cm polyp in the aneuploid group. In the study of Van den Ingh and associates, the group of polyps larger than 2.0 cm consisted predominantly of those with villous features. There has long been controversy over the definition of "carcinoma in situ" in a polyp. Specifically, the problem has been how to regard the foci in which the epithelium exhibits architectural complexity and irregularity, often with cytologic atypia, beyond that present in the remainder of the polyp but without evidence of invasion of lamina propria stroma or the muscularis mucosa. One view is to call this "atypia," 4 ' 5 because there is evidence that this lesion is not an established tumor capable of metastasis. 5 Another view, supported by the FCM data, is to call these lesions CIS to delineate a group of polyps that

6 318 BANNER ET AL. AJ.C.P. March 1987 may contain a cell population with malignant DNA indices that might have a greater propensity than other polyps to have an invasive malignancy develop. The fact that aneuploidy was common in this category in our study lends support to this concept. Eventually, quantitative DNA analysis of polyps may enable us to refine these histologic definitions. Of special interest is our group of six polyps (one adenomatous, one villoglandular, and four villous) in which aneuploid populations were detected by FCM, but there were no foci of CIS as defined by current histologic criteria. Their presence suggests that potentially malignant cells may exist without microscopically identifiable structural change in a polyp. On retrospective blind review of the villoglandular and villous polyps without CIS, we noted atypical cells with an increased nucleo cytoplasmic ratio and pleomorphic vesicular nuclei with prominent eosinophilic nucleoli within otherwise benign-appearing glandular structures of the polyps in seven villoglandular and six villous polyps. These cells were found equally in both aneuploid and diploid polyps, however, so we were unable to identify the aneuploid cells by light microscopic examination. The high-power light microscopic pictures (Fig. 4) of the three polyps taken randomly illustrate the histologic similarities among them. Thus, the presence of aneuploid cells in polyps has been established, but not their significance. It seems that aneuploid cell populations are associated with histologic features that are well-documented predictors of carcinomatous change in polyps. However, even this association does not tell us whether the cells are simply altered but incapable of further growth, or if they represent incipient carcinomas that would eventually proliferate and metastasize if left unattended. Is the aneuploid cell population localized or scattered throughout the polyps? Does it dictate the proliferative rate and eventual size of the polyp? Is aneuploidy a reversible state in polyps? Is this an isolated event, or do certain patients have multiple aneuploid cell populations in their polyps and even in nonneoplastic colonic glands? These questions may be difficult to study in most patients, where polyps are treated by total excision. For the same reason, the clinical role for FCM analysis of polyps will be difficult to establish. Careful prospective collection of follow-up data on such patients may address the issue of whether patients with aneuploid polyps are at greater risk for subsequent development of carcinoma elsewhere in the colon. In thefive-yearfollow-up of our retrospective group, two patients with aneuploid polyps died of unrelated causes, one had a subsequent polypectomy, and the rest had no further follow-up. We conclude (1) retrospective FCM analysis can detect DNA aneuploidy in polyps; (2) DNA aneuploidy may occur in the absence of histologic evidence of carcinoma; and (3) this change is more frequent in types of polyps thought to have increased malignant potential (i.e., those with villous morphology and/or CIS). Whether DNA analysis of colon polyps will have practical implications for patient management is unknown at present. Resolution of this question will require study of additional polyps with careful clinical correlation. Acknowledgments. The authors thank Donald Anderson for technical assistance and Christine Spano for typing the manuscript. References 1. Banner BF, Tomas-de la Vega JE, Roseman DL, Coon JS: Should flow cytometric DNA analysis precede definitive surgery for colon carcinoma? Ann Surg 1985; 202: Collste LG, Darzynkiewicz Z, Traganos F, et al: Flow cytometry in bladder cancer detection and evaluation using acridine orange metachromatic nucleic acid staining of irrigation cytology specimens. J Urol 1980; 123: Coon JS, Schwartz D, Summers JL, Miller AW, Weinstein RS: Flow cytometry of deparaffinized nuclei in urinary bladder carcinoma. Comparison with cytogenetic analysis. Cancer 1986; 57: Enterline HT, Arvan DA: Chromosome constitution of adenoma and adenocarcinoma of the colon. Cancer 1967; 20: Fenoglio CM, Pascal RR: Colorectral adenomas and cancer. Pathologic relationships. Cancer 1982; 50: Hedley DW, Friedlander ML, Taylor IW, Rugg CA, Musgrove EA: Method for analysis of cellular DNA content of paraffin-embedded pathological material using flow cytometry. J Histochem Cytochem 1983;31: Lubs HA, Clark R: The chromosome complement of human solid tumors, I. Gastrointestinal tumors and technic. N Engl J Med 1963;268: Mark J, Mitelman F, Dencker H, Norryd C, Tranberg KG: The specificity of the chromosomal abnormalities in human colonic polyps. A cytogenetic study of multiple polyps in a case of Gardner's syndrome. Acta Pathol Microbiol Immunol Scand A 1973; 81: Morson BC, Dawson IMP: Gastrointestinal pathology, second edition. Oxford, Blackwell Scientific Publications, 1979, pp 635, 636, Petersen SE, Lorentzen M, Bichel P: A mosaic subpopulation structure of human colorectal carcinomas demonstrated by flow cytometry. Acta Pathol Microbiol Immunol Scand A 1981; 274(suppl): Robbins SI, Cotran RS, Kumar V: Pathologic basis of disease, third edition. Philadelphia, WB Saunders, 1984, p Rognum TO, Thorud E, Elgjo K, et al: DNA flow cytometry (FCM) in carcinomas of the large bowel compared with the two functional cell markers secretory component (SC) and carcinoembryonic antigen (CEC), the histological tumour grade and the clinical stage. A preliminary communication. Acta Pathol Microbiol Immunol Scand [A] 1981; 274(suppl): Sleisenger MH, Fordtran JS: Gastrointestinal disease. Pathophysiology diagnosis management, third edition. Philadelphia, WB Saunders, 1983; pp Stich HF, Florian SF, Emson HE: The DNA content of tumor cells. I. Polyps and adenocarcinoma of the large intestine of man. Journal of the National Cancer Institute 1960; 24: Van den Ingh HF, Griffioen G, Cornelisse CJ: Flow cytometric detection of aneuploidy in colorectal adenomas. Cancer Res 1985; 45: Vindelov LL, Christensen IJ, Nissen NI: A detergent-trypsin method for the preparation of nuclei for flow cytometric DNA analysis. Cytometry 1983; 3: Weiss H, Wildner GP, Jacabasch KH, Heinz U, Schaelicke W: Characterization of human adenomatous polyps of the colorectal bowel by means of DNA distribution patterns. Oncology 1985; 42: Wolley RC, Schreiber K, Koss LG, Karas M, Sherman A: DNA distribution in human colon carcinoma, and its relationship to clinical behaviour. 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