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1 /STRU^NI RAD UDK Prognostic value of clinical, pathological and immunohistochemical markers in stage II colon cancer patients... Z. [tor 1, G.S. Frkovi} 2, M. Bra~ko 2, S. Rep{e 1 1 Department of Abdominal Surgery, University Medical Centre Ljubljana, Slovenia 2 Department of Pathology, Institute of Oncology, Ljubljana, Slovenia. Background/Aims: The purpose of our analysis was to determine the prognostic value of molecular markers for identifying high-risk TNM stage II colon cancer patients, the association with various clinical and pathological features, and possible relation to survival. Methods: In 191 colon cancer patients who underwent a potentially curative resection, clinical and pathological factors (age, tumour site, histological grade of malignancy, pt stage, presence of venous, lymphatic and perineural invasion) and tumour molecular markers were analysed. Molecular markers were assessed immunohistochemically in sections of paraffin-embedded tissues. Patients were followed for a median of 8.7 years. The 5-year survival rate was estimated using the the Kaplan-Meier statistical method. Results: From 1. Jan.1994 to 31.Dec.2000, 191 patients underwent radical resection for T3-4 N0M0 colorectal cancer without adjuvant chemotherapy. A significant decrease in survival was identified in older patients, patients with tumours pt4 and with perineural invasion. We found no significant differences in survival of patients with expression of MLH1, Cyclin D1 and reduced overexpression of E-cadherin. Conclusions: The results of our study indicate that the presence of perineural invasion, pt4 stage and the patient s age are significantly correlated with the expected survival in radically resected TNM stage II colon cancer patients, while immunohistochemical markers are not related to survival. Key words: Colon cancer, UICC stage II, tumour markers, prognosis. rezime INTRODUCTION The prognosis of colorectal carcinoma depends on the anatomic extent of the disease (TNM classification and revised UICC TNM classification), and onits amenability to radical (R0) resection (residual tumour (R) classification) 1. Patients who die from the disease most commonly succumb to the effects of secondary metastases in the liver. The prognosis of this cancer is influenced by a variety of factors present at the time of initial diagnosis. These include: age, gender duration of symptoms, presence of bowel obstruction, tumour location, need for blood transfusion and the quality of surgical intervention 2,3,7. Treatment of colorectal cancer is unsuccessful if the aggressive tumour phenotype is identified at surgery. The most important variable influencing long - term outcome is the AJCC/UICC TNM stage, with depth of invasion and infiltration of lymph nodes or distant organs (Table 1) 7. Stage D was not included in the original Dukes staging system, but has become commonly used to represent distant metastasis. Table 1: Comparison of the two most commonly used pathological staging systems for colorectal cancer 4. Postoperative adjuvant chemotherapy is indicated in patients with node-positive, Dukes stage C disease. Although up to 40% of patients with Dukes B colorectal cancer will develop recurrent disease during their lifetime, the role of adjuvant chemotherapy in this setting is still unclear 5. In patients with metastastatic recurrence further curative resection is rarely possible. Palliation by radiotherapy or surgery is feasible in a small proportion of remaining cases. Partial response rates to cytotoxic chemotherapy, ranging from 18% to 48%, have been reported for regimens based on 5-fluorouracil and folic acid 6 ; some of these studies established a survival benefit of chemotherapy 7. Identifying the categories of patients with high-risk colorectal cancer would greatly help us improve treatment strategies and outcome in patients with the node-negative disease 8.

2 40 Z. Stor et al. ACI Vol. LV TABLE 1 COMPARISON OF THE TWO MOST COMMONLY USED PATHOLOGICAL STAGING SYSTEMS FOR COLORECTAL CANCER Dukes stage AJCC/UICC stage Tumour invading the submucosa or muscularis propria A I Tumour penetrating muscular coat of the bowel B II Evidence of tumour in regional lymph nodes regardless of clocal tumour invasion Distant mestastases, regardless of local tumour invasion or lymph node status C D III IV Evidence is accumulating that several prognostic molecular markers may be useful in defining individual patients risk after radical surgery and in selecting patients who might benefit most from adjuvant chemotherapy 9, 10. PATIENTS AND METHODS Patients Blocks of paraffin-embedded tissue were obtained from 191 patients with colon carcinoma who underwent resection at the Department of Abdominal Surgery, University Medical Centre Ljubljana, during the period 1 Jan Dec The patient group consisted of 106 (55.5%) men and 85 (44.6%) women, with a mean age of 67 years; range years. Among 191 colon tumours, 69 (36.1%) were located in the sigmoid colon, 39 (20.4%) in the ascending colon, 32 (16.7%) in the coecum, 15 (7.8%) in the hepatic flexure, 15 (7.8%) in the transverse colon, 13 (6.8%) in the descending colon and eight (4.2%) in the splenic flexure. The tumours were staged using the UICC TNM classification. There were 181 (94.8%) patients with T3NOM0 tumours and ten (5.2%) patients with T4N0M0 lesions. All patients were treated by surgery (Table 2). By the UICC R classification, all tumour resections are classified as radical and curative procedures (R0). None of the patients received preoperative radiotherapy or postoperative radiotherapy and chemotherapy. All of them were followed for a median of 8.7 years (3 13 years) according to our protocol for colorectal cancer patients. The follow-up was scheduled every three months during the first two years after surgery, and every six months thereafter. The follow-up schedule consisted of phy-sical examination, tumour markers determination (CEA, Ca 19-9), chest X-ray, abdominal ultrasonography, CT scanning and endoscopy. In patients with elevated tumour markers or clinically suspected metastatic disease, imaging examinations, including chest X-ray, ultrasonography, CT scan and colonoscopy, were performed when necessary. TABLE 2 TYPES OF RESECTION IN COLON CANCER PATIENTS Type of resection N(%) Right hemicolectomy 95 (49,8) Left hemicolectomy 19 (9,9) Segmental resection 3 (1,5) Sigmoid resection 66(34.6) Total and subtotal colectomy 8(4,2) Total 191 (100) IMMUNOHISTOCHEMICAL METHODS Tumour samples Colon cancer cases were retrieved retrospectively from the files of the Department of Pathology, Institute of Oncology. The specimens were formalin-fixed and paraffinembedded. For the validation study we selected 191 colon cancers received between 1994 and Tissue microarray technique A map of receiver block was prepared with coordinates for each sample to correctly identify the tumour. Under a microscope, areas of interest that were non-necrotic and rich in tumoral glands were marked out accurately with an indelible pen on the whole section of each donor block. The tissue microarrayer was used. Cores 2.0 mm in diameter were punched from the donor blocks and positioned in the recipient paraffin array blocks. The array blocks were incubated at 37 o C for 30 min. to improve adhesion between cores and paraffin of the recipient blocks. They were cut at room temperature with a standard microtome. Description of the array blocks of the study For the validation study two blocks of 124 cores were prepared: each colon cancer was punched six times.

3 Br. 3 Prognostic value of clinical, pathological and 41 immunohistochemical markers in stage II colon ca patients TABLE 3 ANTIBODIES USE IN THE STUDY Antibody Clon Produced by Dilution Preparation HMLH1 G BD 1:10 MV, TRIS-EDTA, ph9, 98 o C, 45 Cyclin D1 SP4 TFS 1:50 MV, TRIS/EDTA, ph9, 98 o C, 45 E-cadherin HCH-38 Dako 1:10 MV, TRIS-EDTA, ph 9, 98 o C, 45 TFS: Thermo Fisher Scientific, MV" microware IMMUNOHISTOCHEMISTRY Immunohistochemical staining was performed using the EnVision ChemMate (DAKO Corporation, Carpinteria, CA, USA) method on sections of formalin-fixed paraffinembedded tissue samples. After antigen retrieval performed by 10 min microwave treatment in TRIS-EDTA at 110 C, and blocade of endogenous peroxidase activity with H2O2, the sections were incubated with antibody for 25 min. The reaction product was visualized using the ChemMate EnVision detection kit. (Table 3) STATISTICAL METHODS Survival rates are based on the data provided by the Cancer Registry of Slovenia. The 5-year survival rate was determined by the Kaplan-Meier method and defined by death of any cause (with or without tumour). Differences between survival curves were tested using the log rank test. A P value of was considered statistically significant. The multivariante Cox proportional hazards model was used to check for possible confounding statistically significant variables form univariante analysis. RESULTS The crude 5-year survival and the 10-year survival for all resected patients was 77.2% and 58.0%, respectively. The tumour-specific 5-year survival rate was 88.2%, and the tumour-specific 10-year survival was 80.0%. The results of univariante survival analysis for 191 patients with stage II colon cancer are listed on Table 4. Among the original nine clinicopathological variables three had statistically significant univariate associations with survival. There was no significant correlation between histological grade of malignancy and lower survival. There was a strong association, however, between age and decreased survival. The number of lymph nodes examined ranged from 2 to 66, with a median of Lymphatic invasion was found in 12 (6.3%) specimens of this series. Vascular invasion was present in six (3.1%) and perineural invasion in four (2.1%) specimens. Patients showing perineural invasion had a significantly poorer prognosis (0.0227) Cut-off indicates the percentage of cells with positive membranous staining. E-cadherin shows reduced overexpression. Positivity of Cyclin D1, Mhl1 and reduced overexpression of E-cadherin, were not correlated with reduced survival (Table 5). Table 4 shows lower survival rates for patients with neural invasion, T4 stage and strong association between decreased survival and age. DISCUSSION The results of the study indicate independent influence of some prognostic variables on survival of patients with stage II colon cancer. Clinical and pathological markers were found to be the major prognostic determinants. Close collaboration between surgeon and pathologist is essential to accurate clinicopathological staging. Clinicopathological stage defined in this way proved to be the dominant, independent variable affecting survival of patients with stage II colon cancer 11. The results of investigations into the association of tumour site and survival of colon cancer patients have varied. Some autors maintained that the site of the lesion does not influence survival 12, and others that cancer of the left colon is associated with poorer survival 13. The results of our study suggest that there is no significant influence of tumor site on long-term outcome. Histological grade has not been found to have a significant effect on survival. Despite this variability, histological grade has repeatedly been shown by multivariate analysis to be a stage-independent prognostic factor 14. Specifically, it has been demonstrated that high tumour grade is an adverse prognostic factor 14. The variables that we have used to define the direct spread of the tumour T3: tumour invades through the muscularis propria into the subserosa; T4: tumuor directly invades other organs or structures were shown to carry prognostic information. Previous univariate 15 and multivariate analyses 16 have confirmed the prognostic importance of direct spread of node positive tumours. In our series intramural spread (pt stage) was a significant indicator of survival in univariante analysis (p= ). It has been shown that 12 to 15 lymph nodes predict for regional node negativity 14. The number of uninvolved lymph nodes in the resected specimen is another factor predicting tumour recurrence. According to Chaplin et al. examination of six or fewer nodes is related to poor prognosis 25. There seem to be two explanations for this observation:

4 42 Z. Stor et al. ACI Vol. LV TABLE 4 CLINICAL CHARACTERISTICS OF 191 PATIENTS WITH STAGE II COLON CANCER Categories Patient No (%) Univeriante analysis (p) Age < (62.8) >65 71 (37.2) Gender male 106 (55,5) female 85 (44,5) Tumour site right colon 159 (83.2) left colon 32 (16.8) pt stage T3 181 (94,8) T4 10 (5,2) No of lymph hodes examined >12 50 (26.2) < (73,8) Histological grade low grade 172 (90.1) high grade 19 (9,9) Lymphatic invasion absent 169 (88.5) present 12(6.3) Vascular invasion absent 173 (91,1) present 6 (3.1( Perineural invasion absent 174 (91,1) present 4 (2,1) a) the lack of sufficient nodes may signify inadequate resection and may be associated with a higher recurrence and lower survival rate, because of down-staging during the pathologic examination, and b) variability of the host-specific response to the tumour. The lymphocytic infiltrate has been demonstrated to be related significantly to the paracortical hyperplasia in regional lymph nodes in Dukes stage B colorectal carcinoma, which is assocciated with a better prognosis 26.Therefore, if fewer than 12 nodes are found, regional negativity is not reliable. It may be argued that a large lymph node harvest (median 17.3) would influence the significance of regional negativity. The presence of fewer than 12 isolated nodes has not been shown in univariate analysis to be associated with a significant decrease in survival (p=0.5096). We have identified vascular invasion in 3.1% of patients in our series. The results of univariante analysis did not comfirm the reported significant independent effect of the presence of venous invasion on prognosis in colon cancer patients treated by resection.talbot et al. have reported poorer survival in patients with the presence of venous invasion in node-positive tumours 17. In several studies, both lymphatic and perineural invasion have been shown by multivariate analysis to be indicators of poor prognosis 11,18. In our present study, univariate analysis showed that perineural invasion was associated with a significantly decreased survival (p=0.0227). Multivariate analysis suggests that gender is a powerful independant prognostic variable. Significant differences in survival rates between men and women have been reported by US Centers for Disease Control 19. The observed gender differences are not in keeping with the findings of a prospective study of 11,000 patients with colorectal cancer that demonstrated higher survival rates in women than in men 20. In the present study, which included only UICC TNM stage II ( T3-4 N0M0) colon cancer patients, imunohistochemical markers Cyclin D1, Mhl1 and E-cadherin revealed no significance in multivariate survival analysis. E-cadherin is a member of cadherin family of calciumdependent adhesion molecules that function as mediators of cell adhesion. It is a transmembrane protein with a large extracellular domain and a small cytoplasmic component, which interacts with cytoplasmic proteins, particulary -catenin. Loss of E-cadherin is associated with increased cell invasiveness 9. Normal membranous E-cadherin expression is essential for establishing cell polarity and maintaining epithelial integrity and cellular differentiation 21. Reduced E-cadherin expression has been found to correlate with an increased rate of local recurrence and metastatic spread in epithelial-type cancers at various sites, such as prostate, bladder, breast, lung, stomach, colon and rectum 22. Immunohistochemistry for hmlh1 expression may represent a practical test for identifying DNA mismatch repair-deficient tumours, and has been used in retrospective prognostic analysis in colorectal cancer 23. This phenomenon is known as microsatellite instability (MSI) and is due to the silencing of the mismatch repair genes, MLH1 and MLH2 24. Cyclin D1 (CCND1) is a protein that plays a key role in cell cycle control, particulary in the transition from G1 to S phase, which is regulated by cyclin-dependent kinases 27. The overexpression of the CCND1 gene occurs in more than one-third of all colorectal cancers 28. The strongest evidence to date has linked the CCND1 A870G poly-

5 Br. 3 Prognostic value of clinical, pathological and 43 immunohistochemical markers in stage II colon ca patients TABLE 5 THE RESULTS OF MOLECULAR MARKER ASSAYS (CYCLIN D1, E-c adherin AND hmhll) FOR ALL PATIENTS Marker % possitive cases cut-off Univariate analysis (p) Cyclin D1 18, E-cadherin* 43.5 >95 0./3029 Mhll 35.6 > Positivity of Cyclin D1, Mhll and reduced overexpression of E-cadherin, were not correlated with reduced survival morphism with an increased risk of colorectal cancer and adenomas 29,30,31. CONCLUSIONS The results of our study indicate that the presence of perineural invasion, pt4 stage and the patient s age are significantly correlated with the expected survival in radically resected TNM stage II colon cancer patients, while immunohistochemical markers are not related to survival. SUMMARY PROGNOSTI^KI ZNA^AJ KLINI^KIH, PATOLO[KIH I IMUNOHISTOHEMIJSKIH MARKERA KOD II STADI- JUMA KOLOREKTALNOG KARCINOMA. Cilj: Cilj ove analize je da se odredi prognosti~ki zna~aj molekulskih markera u identifikaciji visokorizi~nih pacijenata II stadijuma karcinoma kolona TNM, ocenjivanjem odredjenih klini~kih i patolo{kih parametara i u odnosu na pre ivljavanje. Metode: Kod 191 pacijenta obolelog od karcinoma kolona koji su podvrgnuti potencijalno kurativnoj resekciji, analizirani su klini~ki i patolo{ki parametri (godine, lokalizacija tumora, histolo{ki gradus maligniteta, pt stadijum, venska, limfati~na i perineuralna invazija) i tumorski molekulski markeri. Molekulski markeri su mereni imunohistohemijski u presecima parafinskih preparata tkiva. Srednje vrema pra}enja pacijenata iznosilo je 8.7 godina. Petogodi{nje pre ivljavanje odredjivano je Kaplan-Meier statisti~kom metodom. Rezultati: Od 1. januara do 31. decembra 2000., 191 pacijent je podvrgnut radikalnoj resekciji zbog T3-4 N0M0 kolorektalnog karcinoma bez adjuvantne hemioterapije. Zna~ajno ni e pre ivljavanje zabele eno je kod starijih pacijenata, pacijenata sa T4 stadijumom i kod postojanja perineuralne invazije. Nismo nali zna~ajnu razliku u pre ivljavanju sa ekspresijom MLH1, CyclidinD1 i smanjenom ekspresijom E-cadherina. Zaklju~ak: Rezultati na{e studije pokazuju da prisustvo perineuralne invazije, pt4 stadijum i starost pacijenta imaju zna~ajnu korelaciju sa o~ekivanim pre ivljavanjem kod radikalno operisanih pacijenata II stadijuma kolorektalnog karcinoma po TNM-u, dok imunohistohemijski markeri nisu pokazali povezanost sa pre ivljavanjem. Klju~ne re~i: karcinom kolona, tumorski markeri, prognoza REFERENCES 1. UICC TNM Atlas. 4 th ed. Hermanek P, Hutter RVP, Sobin LH, Wagner G, Wittekind C. Berlin: Springer, McArdle CS and Hole D. Impact of variability among surgeons on postoperative morbidity and mortality and ultimate survival. Br Med J 1991; 302: Hermanek P, Wiebelt H, Staimner D and Riedl S. Prognostic factors of rectum carcinoma-experience of German multicentre study SGCRC. German Study Group Colo-Rectal Carcinoma. Tumori 1995; 81: McLeod HL and Murray GI. Tumour markers of prognosis in colorectal cancer. Br J Cancer 1999; 79: McDonald JS. Adjuvant therapy of colorectal cancer. CA Cancer J Clin 1999; 49: Doroshow JH, Multhauf P, Leong L et al. Prospective randomised comparison of fluorouracil versus fluorouracil and high-dose continuous infusion levcovorin calcium for the treatment of advanced mesurable colorectal cancer in patients previously unexposed to chemotherapy. J Clin Oncol 1990; 8: Poon MA, O Connell MJ, Moertel CG, et al. Biochemical modulation of fluorouracil: evidenced of significant improvement in survival and quality of life in patients with advanced colorectal carcinoma. J Clin Oncol 1989; 7: O Connell MJ, Schaid DJ, Ganju V et al. Current status of adjuvant therapy of colorectal cancer: can molecular markers play a role in predicting prognosis? Cancer 1992; 70 (Suppl): McLeod HL, Murray GI. Tumor markers of prognosis in colorectal cancer. Br J Cancer 1999; 79: Graziano F, Cascinu S. Prognostic molecular markers for planning adjuvant chemotherapy trials in Dukes B colorectal cancer patients: how much evidence is enough? Ann of Oncol 2003; 14: Chapuis PH,Dent OF, Fisher R, Newland RC, Pheils MT, Smyth E and Colquhoun K. A multivariate analysis of clinical and pathological variable in prognosis after resection of large bowel cancer. Br J Surg 1985; 72:

6 44 Z. Stor et al. ACI Vol. LV 12. Fielding LP, Phillips RKS, Fry JS, Hittinger R. Prediction of outcome after curative resection for large bowel cancer. Lancet 1986; 2: Halvorsen TB, Seim E. Tumour site: a prognostic factor in colorectal cancer. A multivariante analysis. Scan J Gastroenterol 1987;22: Compton CC. Pathology report in colon cancer: what is prognostically important? Dig Dis 1999;17: Phillips RK, Hittinger R, Blesovsky L, Fry JS, Fielding LP. Large bowel cancer: surgical pathology and its relationship to survival. Br J Surg 1984; 71: Jass JR, Love SB. Prognostic value of direct spread in Dukes C cases of rectal cancer. Dis Colon Rectum 1989; 32: Talbot IC, Ritchie S, Leighton MH, Hughes AO, Bussey HJR, Morson BC. The clinical significance of invasion of veins by rectal cancer. Br J. Surg 1980;67: Knudsen JB, Nilsson T, Sprechler M, Johansen A, Christensen N. Venous and nerve invasion as prognostic factors in postoperative survival of patients with resectable cancer of rectum. Dis Colon Rectum 1983; 26: Centers for Disease Control. Mortality patterns- United States, MMWR Morb Mortal Wkly Rep 1992; 41: Godwin JD II, Brown CC. Some prognostic factors in survival of patients with cancer of the colon and rectum. Journal of Chronic Disease 1975; 28: Takeichi M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science 1991; 251: Van Aken E, De Wever O, Correia de Rocha AS, Mareel M. Defective E-cadherin /catenin compexes in human cancer. Virchows Arch 2001; 439: Marcus VA, Madlenski L, Gryfe R et al. Immunohistochemistry for hmlh 1 and Hmlh2: a practical test for DNA mismatch repair deficient tumours. Am J Surg Pathol 1999; 23: Ionov Y, Peinado MA, Malkhosyan Set al. Ubiqutous somatic mutation in simple repeated sequences reveal a new mechanism for colonic tumorogenesis. Nature 1993; 363: Chaplin S, Cerottini JP, Bosman FT, et al. For patients with Dukes B (TNM stage II) colorectal carcinoma, examination of six or fewer lymph nodes is related to poor prognosis. Cancer 1998; 83: Pihl E, Malahy MA, Khankhanian N, et al. Immunomorphological features of prognostic significance in Dukes stage B colorectal carcinoma. Cancer Res 1977; 37: Sherr CJ. Cancer cell cycles. Science 1996; 274: Arber N, Hibshoosh H, Moss SF, Sutter T, Zhang Y, Begg M, Wang S, Weinstein IB, Holt PR. Increased expression of cyclin D1 is an early event in multistage colorectal carcinogenesis. Gastroenterology 1996; 110: Kong S, Wei Q, Amos CL, Lynch PM, Levin B, Zong J, Fraiser ML. Cyclin D1 polymorphisem and increased risk of colorectal cancer at young age. J Natl Cancer Inst. 2001; 93: Bala S, Peltomaki P. Cyclin D1 as a genetic modifier in hereditary nonpolyposis colorectal cancer. Cancer Res 2001; 61: Porter TR, Richards FM, Houlston RS, Evans DG, Jankowski JA, Mcdonald F, Norbury G, Payne SJ, Fisher SA, Tomlinson I, Maher er. Contribution of cyclin D1(CCND1) and E-cadherin(CDH19 polymorphisms to familial and sporadic colorectal cancer. Oncogen 2002; 21:

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