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1 GASTROENTEROLOGY 2002;122: CASE REPORTS Molecular Evidence for the Same Clonal Origin of Both Components of an Adenosquamous Barrett Carcinoma BASTIAAN P. VAN REES,* REMIGIO W. ROUSE,* MIREILLE J. DE WIT,* CAREL J. M. VAN NOESEL,* GUIDO N. J. TYTGAT, J. JAN B. VAN LANSCHOT, and G. JOHAN A. OFFERHAUS* *Departments of Pathology, Gastroenterology, and Surgery, Academic Medical Center, Amsterdam, the Netherlands We describe an uncommon case of adenosquamous carcinoma arising in a Barrett esophagus in a 72-yearold white man who occasionally used alcohol, and was a nonsmoker for 34 years. Polymerase chain reaction based microsatellite analysis was performed on the adenocarcinoma component (AC) and squamous cell carcinoma component (SC) of the tumor. The metaplastic Barrett epithelium (BE), the AC and the SC all showed loss of the same allele at 4 markers on chromosome 9p. Furthermore, the AC and the SC both showed loss of the same allele at all informative markers tested on chromosomal arms 3p, 5q, 10q, 14q, and 18q. In addition, both the SC and AC component contained the same missense mutation in the p53 tumor-suppressor gene. The only observed difference was a shift at a marker on chromosome 16q in the AC, whereas no shift was found in the BE and the SC. These findings suggest that this biphasic tumor has a monoclonal origin. The divergence presumably occurred late in the tumorigenesis of this carcinoma. Cancer of the esophagus is almost always either a squamous cell carcinoma or an adenocarcinoma. Most adenocarcinomas arise in a Barrett esophagus, and Barrett carcinoma is currently the most rapidly increasing cancer in the Western world. 1 Adenosquamous carcinoma of the esophagus is an uncommon malignant tumor with biphasic histology of an adenocarcinoma and squamous cell carcinoma component simultaneously. Because these tumors have an admixture of diverse neoplastic cells, their origin and histogenesis has been uncertain. Adenosquamous carcinoma has been described in the Barrett mucosa bearing esophagus, 2 4 but glandular differentiation in conventional squamous cell carcinoma or tumors arising from the submucosal glands have also been described, and finally collision of an adenocarcinoma and a squamous cell carcinoma at the squamocolumnar junction would also be conceivable. 5 In this report, a case of adenosquamous carcinoma in Barrett esophagus is presented in which molecular analysis of the various neoplastic components provided convincing evidence that both the adenocarcinoma and squamous cell carcinoma component originated from the Barrett mucosa that surrounded the cancer. Case Report A 72-year-old white man presented with pyrosis and long-standing complaints of severe gastroesophageal reflux. He had no difficulty with food passage and had no weight loss. There was no history of smoking for the last 34 years and he occasionally used alcohol, on average 3 units per week. Physical examination was unremarkable, sedimentation rate was 6 mm/hour, and hemoglobin 9.4 mmol/l. At gastroscopy, Barrett mucosa over a length of 9 cm (29 to 38 cm from the incisors) and a hiatus hernia (38 to 41 cm from the incisors) were observed. In the Barrett mucosa a small, well-circumscribed exophytic fragile tumor was present over a length of 3 cm and 30% of the circumference. A computed tomography scan and endoscopic ultrasonography indicated that the tumor growth was limited to the esophageal wall, which was 8-mm thick. No metastases were detected. A transhiatal esophagectomy with partial gastrectomy was performed, followed by gastric tube reconstruction. Macroscopically, the resected specimen contained ulcerated Barrett mucosa in which a well-circumscribed exophytic-growing tumor with a diameter of 3 cm was seen. The tumor was located in the Barrett lined segment of the esophagus, 2.5 cm above the anatomic esophago- Abbreviations used in this paper: AC, adenocarcinoma component; AIF, allelic imbalance factor; BE, Barrett epithelium; LOH, loss of heterozygosity; NSE, normal squamous epithelium; PCR, polymerase chain reaction; SC, squamous cell carcinoma component by the American Gastroenterological Association /02/$35.00 doi: /gast
2 March 2002 CLONALITY OF ADENOSQUAMOUS BARRETT CARCINOMA 785 Figure 1. (A ) Macroscopy of the resected specimen: the tumor is indicated by an arrow. SM, preexistent squamous cell mucosa of the esophagus; BE, Barrett esophagus; GM, gastric mucosa. A small patch of squamous cell mucosa adjacent to the tumor is indicated by an asterisk. (B) Microscopy of the adenosquamous carcinoma; white arrows indicate the squamous cell carcinoma component, black arrows point to the adenocarcinoma component (H&E). (C ) Microscopy of a representative part of the adenocarcinoma component that was microdissected and used for the p53 mutation analysis and microsatellite analyses (H&E). (D) Positive staining for the cytokeratin marker Cam 5.2 in the adenocarcinoma component. (E ) Microscopy of a representative part of the squamous cell carcinoma component that was microdissected and used for the p53 mutation analysis and microsatellite analyses (H&E). (F ) The squamous cell carcinoma component is negative for Cam 5.2. gastric junction, and extended to the squamocolumnar junction of a patch of squamous cell mucosa adjacent to the tumor (Figure 1A). Paraffin-embedded tissue blocks were routinely sampled from which H&E-stained section slides were prepared for microscopy. The microscopy of the esophagus showed Barrett mucosa of the distinctive type, and invasive adenocarcinoma, focally intermingled with squamous cell carcinoma (Figure 1B). Both components were confined to the submucosa. The esophagus and stomach resection margins were unremarkable. One lymph node contained a metastasis with adenocarcinoma differentiation. Materials and Methods Immunohistochemistry Immunohistochemistry for cytokeratin (clone Cam 5.2; Becton Dickinson, San Jose, CA) and p53 (clone DO-7; Dako, Glostrup, Denmark) was performed using standard methods.
3 786 VAN REES ET AL. GASTROENTEROLOGY Vol. 122, No. 3 Table 1. Results of the Microsatellite Marker Analysis and p53 Sequence Analysis Marker Microsatellite analysis Chromosomal arm BE AC BAT26 2p No shift No shift No shift D3S1478 3p R LL LL D5S346 5q R LS LS D5S107 5q R LS LS D9S162 9p LL LL LL D9S171 9p LL LL LL D9S259 9p LL LL LL D9S925 9p LL LL LL D10S q R LS LS D14S68 14q R LL LL D16S q No shift Shift No shift D18S64 18q R LS LS LN p53 sequence analysis (codon 163) NSE BE AC TAC TAC TAC TAC 3 AAC TAC 3 AAC (Wt Tyr) (Wt) (Wt) (Tyr 3 Asn) (Tyr 3 Asn) BE, Barrett epithelium; AC, adenocarcinoma component; SC, squamous cell component; LN, lymph node; NSE, normal squamous epithelium; R, retention (no LOH); LL, LOH of the larger allele; LS, LOH of the smaller allele; Wt, wild-type. Microsatellite Analysis Formalin-fixed, paraffin-embedded tissue was available from normal lymphocytes, normal squamous cell epithelium (NSE), metaplastic Barrett epithelium (BE), invasive adenocarcinoma (AC), and squamous cell carcinoma (SC). Enrichment for metaplastic and tumor cells was achieved by careful microdissection. Microdissection for the AC and SC component was performed on areas of the tumor in which each individual component was present separately (Figure 1C F) to avoid contamination of 1 component with the other. DNA was isolated using a standard proteinase-k digestion. Loss of heterozygosity (LOH) analysis was performed using 18 polymorphic microsatellite markers and an Alu repeat located within the p53 gene. Polymerase chain reaction (PCR) amplification was performed in a 20 L reaction volume containing 40 ng of each primer of which 1 primer was labeled with a fluorescent marker, 0.2 mmol/l dntps, 1.5 mmol/l MgCl 2, and 1.0 units of Platinum Taq DNA polymerase (Gibco BRL/Life Technologies Inc., Rockville, MD) in the buffer supplied by the manufacturer. Cycling was performed in a PTC-100 cycler (MJ Research Inc., Waltham, MA) during 40 cycles at an annealing temperature of 55 C and the PCR) products were analyzed using an automated ABI-377 sequencer and Genescan 2.1 software (Applied Biosystems, Foster City, CA). For the 12 informative markers (Table 1), LOH was determined by calculating the ratio of the peak heights of the smaller and larger allele for the normal DNA and for the DNA from the different neoplastic components. Subsequently, the allelic imbalance SC SC factor (AIF) was calculated for each neoplastic component by dividing its allelic ratio by the ratio from the normal DNA. 6 LOH of the larger allele was defined as an AIF of 1.7 or more and LOH of the smaller allele was defined as an AIF of 0.59 or less. All PCR reactions were repeated at least once to ensure reproducibility. p53 Mutation Analysis Full-length complementary DNA (cdna) was derived from snap-frozen material of the AC component using standard methods. This was subjected to sequence analysis as described by Rozemuller et al. 7 using an ABI 3100 automated sequencer (Applied Biosystems, Foster City, CA) and the software provided by the manufacturer. Subsequently, the DNA of normal lymphocytes, NSE, BE, AC, and SC was analyzed by direct sequencing for the presence of the same missense mutation that was found in the cdna of the AC component. Results Adenosquamous carcinoma of the esophagus is a very rare tumor with an obscure histogenesis. We describe a case of adenosquamous carcinoma in Barrett esophagus in a patient who occasionally used alcohol, but was a nonsmoker. In this case, we used a molecular-genetic approach to characterize and to understand the histogenesis of this adenosquamous carcinoma arising in Barrett mucosa. Table 1 summarizes the results of the LOH and p53 sequence analysis for BE, AC, and SC. The LOH on chromosomal arm 9p clearly indicates that this is an early event in the tumorigenesis because in addition to the LOH at 4 markers (D9S162, D9S171, D9S259, and D9S925) in the AC and the SC, loss of the same alleles was also found in the BE (Figure 2A). LOH at this locus as an early event in metaplastic Barrett mucosa has also been described by other investigators. 8 Besides the LOH on chromosome 9p, the AC and the SC both show LOH with loss of the same alleles at all informative markers tested on chromosomal arms 3p, 5q, 10q, 14q, and 18q (Table 1, Figure 2A). This indicates the evolution of a clonal population with an accumulation of molecular-genetic alterations. 9 In addition to the LOH analysis, sequence analysis of the p53 tumor-suppressor gene revealed the same missense mutation in the AC and SC component (Figure 2B D, Table 1). It is extremely unlikely that 2 different tumors share the loss of the same alleles at so many different loci and harbor the exact same point mutation. The molecular studies in this case show the potential power of this approach to follow the clonal evolution of tumors with markers that identify LOH. A collision tumor or a mucoepidermoid tumor arising from a sub-
4 March 2002 CLONALITY OF ADENOSQUAMOUS BARRETT CARCINOMA 787 Figure 2. (A ) Representative examples of the microsatellite marker analysis. The results of markers at loci on chromosomal arms 9p (D9S259), 16q (D16S2624), and 3p (D3S1478) are shown for normal lymphocytes (N), Barrett epithelium (BE), adenocarcinoma (AC), and squamous cell carcinoma (SC) component. The alleles are highlighted by arrows and the AIF is indicated in red, where applicable. There is LOH of the larger allele at marker D9S259 in BE, AC, and SC. At marker D16S2624 there is a shift only in the AC component (red arrowhead). There is LOH of the larger allele at marker D3S1478 both in the AC and in the SC component. (B and C ) Positive staining for p53 in both the (B) AC component and (C ) the SC component. (D) Sequencing of the p53 gene revealed the same T3 A missense mutation in codon 163 in both the AC and the SC component (black arrowheads). Figure 3. Schematic representation of the postulated tumor progression pathway in this case of adenosquamous carcinoma. LOH at chromosomal arm 9p has occurred as an early event because it was found already in Barrett epithelium and is shared by both the SC and the AC component. LOH at chromosomal arms 3p, 5q, 10q, 14q, and 18q and the p53 point mutation occurred before the divergence because these events are observed in both components. A shift at marker D16S2624 is found only in the AC-component, and therefore must have occurred as a late event, after the divergence.
5 788 VAN REES ET AL. GASTROENTEROLOGY Vol. 122, No. 3 mucosal esophageal gland could be ruled out. Given the many molecular-genetic similarities between the 2 components, the divergence in differentiation presumably occurred as a late event in tumorigenesis (Figure 3). Discussion The molecular alterations associated with adenocarcinoma and squamous cell carcinoma of the esophagus have been addressed in many recent studies and some of these studies have compared the molecular make-up of adenocarcinoma and squamous cell carcinoma. Our findings are in agreement with these studies; i.e., loss of the loci on chromosomal arms 3p, 5q, 9p, and 18q, as well as mutation of the p53 tumor-suppressor gene are frequently seen in both tumor types. 10,11 Surprisingly, adenocarcinoma and squamous cell carcinoma of the esophagus have many molecular alterations in common and there is little evidence for a specific distinction between these 2 tumors at the molecular-genetic level. In this study, the only observed difference between the 2 components was a shift at a marker on chromosomal arm 16q (Figure 2A). It is reasonable to question whether this observed difference between the moleculargenetic make-up of the 2 components can account for the phenotypic divergence. Thus, it remains unclear at the genetic level why in this particular patient an adenosquamous carcinoma developed in a Barrett mucosa, but perhaps epigenetic factors may explain the difference. Squamous cell carcinomas in the esophagus of patients with Barrett mucosa have been reported. 12 These are explained by the pathogenetic relationship of the 2 conditions that share many risk factors and carcinogens. Some of these carcinogens may push the neoplastic cells in different lineage directions, but the molecular basis of such phenomenon is still completely obscure. For practical purposes it is important to realize that patients with Barrett esophagus carry a risk not only for Barrett carcinoma but also for carcinomas at other sites of the upper aerodigestive tract. 6 References 1. Pera M, Cameron AJ, Trastek VF, Carpenter HA, Zinsmeister AR. Increasing incidence of adenocarcinoma of the esophagus and esophagogastric junction. Gastroenterology 1993;104: Smith RR, Hamilton SR, Boitnott JK, Rogers EL. The spectrum of carcinoma arising in Barrett s esophagus. A clinicopathologic study of 26 patients. Am J Surg Pathol 1984;8: Pascal RR, Clearfield HR. Mucoepidermoid (adenosquamous) carcinoma arising in Barrett s esophagus. Dig Dis Sci 1987;32: Ter RB, Govil YK, Leite L, Infantolino A, Ghabra M, Galan A, Katz PO. Adenosquamous carcinoma in Barrett s esophagus presenting as pseudoachalasia. Am J Gastroenterol 1999;94: Whitehead R, ed. Gastrointestinal and oesophageal pathology. London, England: Churchill Livingstone, 1989: van Rees BP, Cleton-Jansen AM, Cense HA, Polak MM, Clement MJ, Drillenburg P, van Lanschot JJ, Offerhaus GJ. Molecular evidence of field cancerization in a patient with 7 tumors of the aerodigestive tract. Hum Pathol 2000;31: Rozemuller EH, Kropveld A, Kreyveld E, Leppers FG, Scheidel KC, Slootweg PJ, Tilanus MG. Sensitive detection of p53 mutation: analysis by direct sequencing and multisequence analysis. Cancer Detect Prev 2001;25: Galipeau PC, Prevo LJ, Sanchez CA, Longton GM, Reid BJ. Clonal expansion and loss of heterozygosity at chromosomes 9p and 17p in premalignant esophageal (Barrett s) tissue. J Natl Cancer Inst 1999;91: Barrett MT, Sanchez CA, Prevo LJ, Wong DJ, Galipeau PC, Paulson TG, Rabinovitch PS, Reid BJ. Evolution of neoplastic cell lineages in Barrett oesophagus. Nat Genet 1999;22: Montesano R, Hollstein M, Hainaut P. Genetic alterations in esophageal cancer and their relevance to etiology and pathogenesis: a review. Int J Cancer 1996;69: Wijnhoven BP, Tilanus HW, Dinjens WN. Molecular biology of Barrett s adenocarcinoma. Ann Surg 2001;233: Rosengard AM, Hamilton SR. Squamous carcinoma of the esophagus in patients with Barrett esophagus. Mod Pathol 1989;2: 2 7. Received June 7, Accepted November 15, Address requests for reprints to: G. Johan A. Offerhaus, M. D., Department of Pathology, Academic Medical Center, Meibergdreef 9, 1105 AZ, Amsterdam, the Netherlands. g.j.offerhaus@ amc.uva.nl; fax: (31) The authors thank Eric Caspers for excellent technical assistance.
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