Revised August, 2009

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Program Accomplishments

Residual Tissue Repository (RTR) program accomplishments to date include publications based on tissue microarrays (TMAs) from breast, colorectal, and pancreatic tumors. From a subset of incident colorectal cancer cases recorded in the Hawaii registry for 1995 (n=286/603; 47%), Hernandez et al. observed that cytokeratins 20 and 7 were over-expressed in malignant versus histologically normal tissue. The TMA cases were similar to non-TMA cases with respect to age, gender, race/ethnicity, anatomic site and survival, but differed from all cases in the population with respect to stage and treatment.

In another reported study, Takikita et al. utilized RTR specimens from the Iowa, Hawaii, and Los Angeles county registries to create a population-based, pancreatic cancer TMA from 161/13,650 recorded cases (1.2%), with over-representation of African-American (12% vs. 9%) and Asian-Pacific Islander (40% vs. 14%) cases compared to the registry populations at large. Multiple core samples were obtained from malignant epithelial and benign normal tissues for each case. Candidate biomarkers were analyzed with respect to survival time from diagnosis to death, using multivariable Cox proportional hazard regression models. Tumor mucin expression (MUC1, MUC2 and MUC5AC) was found to be associated with shorter survival time, even after adjusting for gender, age, race, stage of disease, pancreatic origin versus metastatic site, and ever versus never surgical or radiation treatment. Histologic features and biomarker patterns differed by race, but the investigators acknowledged that the TMA did not include adequate case numbers from diverse population subgroups to provide robust inferences by race/ethnicity.

Single registries within the SEER RTR program have also developed valuable biospecimens resources. These biospecimens have been used in studies of lung, breast, and hematopoietic cancers. The RTR Committee intends to expand the contribution of this population-based biospecimen resource through collaborative cancer research. In keeping with this objective, current and proposed RTR projects are examining biospecimens from SEER cases with a variety of tumor types including primary central nervous system lymphoma, AIDS/HIV-associated cancers, Burkitt lymphoma, and breast, ovarian, colorectal, hepatocellular, and HPV-related cancers.

Selected Publications

Alemany L, Saunier M, Alvarado-Cabrero I, Quirós B, Salmeron J, Shin HR, Pirog EC, Guimerà N, Hernandez-Suarez G, Felix A, Clavero O, Lloveras B, Kasamatsu E, Goodman MT, Hernandez BY, Laco J, Tinoco L, Geraets DT, Lynch CF, Mandys V, Poljak M, Jach R, Verge J, Clavel C, Ndiaye C, Klaustermeier J, Cubilla A, Castellsagué X, Bravo IG, Pawlita M, Quint WG, Muñoz N, Bosch FX, de Sanjosé S; HPV VVAP Study Group. Human papillomavirus DNA prevalence and type distribution in anal carcinomas worldwide. International Journal of Cancer 2015 Jan 1;136(1):98-107.

Altekruse SA, Rosenfeld GE, Carrick DM, Pressman EJ, Schully SD, Mechanic LE, Cronin KA, Hernandez BY, Lynch CF, Cozen W, Khoury MJ, Penberthy LT. SEER cancer registry biospecimen research: yesterday and tomorrow. Cancer Epidemiology, Biomarkers & Prevention 2014 Dec;23(12):2681-7.

Altirriba J, García A, Sánchez B, Haba L, Altekruse S, Stratmann T, Bombí JA, Mezquita C, Gomis R, Mora C. The sole presence of cdk4 is not a solid criterion for discriminating between tumor and healthy pancreatic tissues. International Journal of Cancer 2012;(11):2743-2745.

Carrick DM, Mehaffey MG, Sachs MC, Altekruse S, Camalier C, Chauqui R, Cozen W, Das B, Hernandez BY, Lih CJ, Lynch CF, Makhlouf H, McGregor P, McShane LM, Phillips Rohan J, Walsh WD, Williams PM, Gillanders EM, Mechanic LE, Schully SD. Robustness of next generation sequencing on older formalin-fixed paraffin-embedded tissue. PLoS One 2015 Jul 29;10(7):e0127353.

Cerhan JR, Natkunam Y, Morton LM, Maurer MJ, Asmann Y, Habermann TM, Vasef MA, Cozen W, Lynch CF, Allmer C, Slager SL, Lossos IS, Chanock SJ, Rothman N, Hartge P, Dogan A, Wang SS. LIM domain only 2 protein expression, LMO2 germline genetic variation, and overall survival in diffuse large B-cell lymphoma in the pre-rituximab era. Leukemia and Lymphoma 2012 Jun;53(6):1105-1112.

Chang CM, Schroeder JC, Huang WY, Dunphy CH, Baric RS, Olshan AF, Dorsey KC, Dent GA, Cerhan JR, Lynch CF, Rothman N, Cantor KP, Blair A. Non-Hodgkin Lymphoma (NHL) subtypes defined by common translocations: Utility of fluorescence in situ hybridization (FISH) in a case-control study. Leukemia Research 2010;34(2):190-195.

Chang CM, Schroeder JC, Olshan AF, Dunphy CH, Huang WY, Baric RS, Conway K, Cerhan JR, Lynch CF, Rothman N, Cantor KP, Blair A. A case-control study of tobacco use and other non-occupational risk factors for lymphoma subtypes defined by t(14;18) translocations and bcl-2 expression. Cancer Causes and Control 2010;21(7):1147-1154.

Chang CM, Wang SS, Dave BJ, Jain S, Vasef MA, Weisenburger DD, Cozen W, Davis S, Severson RK, Lynch CF, Rothman N, Cerhan JR, Hartge P, Morton LM. Risk factors for non-Hodgkin lymphoma subtypes defined by histology and t(14;18) in a population-based case-control study. International Journal of Cancer 2011; 129(4):938-947.

Chaturvedi AK, Engels EA, Pfeiffer RM, Hernandez BY, Xiao W, Kim E, Jiang B, Goodman MT, Siburg-Saber M, Cozen W, Liu L, Lynch CF, Wentzensen N, Jordan RC, Altekruse S, Anderson WF, Rosenberg PS, Gillison ML. Human papillomavirus and rising oropharyngeal cancer incidence in the United States. Journal of Clinical Oncology 2011;(32):4294-4301.

Cubilla AL, Lloveras B, Alemany L, Alejo M, Vidal A, Kasamatsu E, Clavero O, Alvarado-Cabrero I, Lynch C, Velasco-Alonso J, Ferrera A, Chaux A, Klaustermeier J, Quint W, de Sanjose S, Munoz N, Bosch FX. Basaloid squamous cell carcinoma of the penis with papillary features: a clinicopathology study of 12 cases. American Journal of Surgical Pathology 2012 Jun;36(6):869-875.

de Sanjosé S, Alemany L, Ordi J, Tous S, Alejo M, Bigby SM, Joura EA, Maldonado P, Laco J, Bravo IG, Vidal A, Guimerà N, Cross P, Wain GV, Petry KU, Mariani L, Bergeron C, Mandys V, Sica AR, Félix A, Usubutun A, Seoud M, Hernández-Suárez G, Nowakowski AM, Wilson G, Dalstein V, Hampl M, Kasamatsu ES, Lombardi LE, Tinoco L, Alvarado-Cabrero I, Perrotta M, Bhatla N, Agorastos T, Lynch CF, Goodman MT, Shin HR, Viarheichyk H, Jach R, Cruz MO, Velasco J, Molina C, Bornstein J, Ferrera A, Domingo EJ, Chou CY, Banjo AF, Castellsagué X, Pawlita M, Lloveras B, Quint WG, Muñoz N, Bosch FX; HPV VVAP study group. Worldwide human papillomavirus genotype attribution in over 2000 worldwide cases of intraepithelial and invasive lesions of the vulva. European Journal of Cancer 2013 Nov;49(16):3450-3461.

Esser AK, Miller MR, Huang Q, Meier MM, Beltran-Valero de Bernabe D, Stipp CS, Campbell KP, Lynch CF, Smith BJ, Cohen MB, Henry MD. Loss of LARGE2 disrupts functional glycosylation of α-dystroglycan in prostate cancer. Journal of Biological Chemistry 2013 Jan 25;288(4):2132-42.

Gargano JW, Wilkinson EJ, Unger ER, Steinau M, Watson M, Huang Y, Copeland G, Cozen W, Goodman MT, Hopenhayn C, Lynch CF, Hernandez BY, Peters ES, Saber MS, Lyu CW, Sands LA, Saraiya M. Prevalence of human papillomavirus types in invasive vulvar cancers and vulvar intraepithelial neoplasia 3 in the United States before vaccine introduction. Journal of Lower Genital Tract Disease 2012 Oct;16(4):471-479.

Gaudet MM, Press MF, Haile RW, Lynch CF, Glaser SL, Schildkraut J, Gammon MD, Thompson W, Bernstein JL. Risk factors by molecular types of breast cancer across a population-based study of women 56 years or younger. Breast Cancer Research and Treatment 2011;130(2):587-597.

Goodman MT, Saraiya M, Thompson TD, Steinau M, Hernandez BY, Lynch CF, Lyu CW, Wilkinson EJ, Tucker T, Copeland G, Peters ES, Altekruse S, Unger ER, and the HPV Typing of Cancers Workgroup. Human Papillomavirus Genotype and Oropharynx Cancer Survival in the United States. European J Cancer 2015 Sep.

Graham RP, Vierkant RA, Tillmans LS, Wang AH, Laird PW, Weisenberger DJ, Lynch CF, French AJ, Slager SL, Raissian Y, Garcia JJ, Kerr SE, Eun Lee H, Thibodeau SN, Cerhan JR, Limburg PJ, Smyrk TC. Tumor budding and colorectal carcinoma; confirmation of prognostic significance and histologic cutoff in a population-based cohort. American Journal of Surgical Pathology 2015 Jul 21.

Hernandez BY, Goodman MT, Lynch CF, Cozen W, Unger ER, Steinau M, Thompson T, Saber MS, Altekruse SF, Lyu C, Saraiya M, The HPV Typing of Cancer Workgroup. Human papillomavirus prevalence in invasive laryngeal cancers in the United States. PLoS One 2014 Dec 29;9(12):e115931.

Hernandez BY, Goodman MT, Unger ER, Steinau M, Powers A, Lynch CF, Cozen W, Saber MS, Peters ES, Wilkinson EJ, Copeland G, Hopenhayn C, Huang Y, Watson M, Altekruse SF, Lyu C, Saraiya M, The HPV Typing of Cancer Workgroup. Human papillomavirus genotype prevalence in invasive penile cancers from a registry-based United States population. Frontiers in Oncology 2014 Feb 5;4:9.

Hopenhayn C, Christian A, Christian WJ, Watson M, Unger ER, Lynch CF, Peters ES, Wilkinson EJ, Huang Y, Copeland G, Cozen W, Saber MS, Goodman MT, Hernandez BY, Steinau M, Lyu C, Tucker TT, Saraiya M. Prevalence of human papillomavirus types in invasive cervical cancers from 7 U.S. cancer registries before vaccine introduction. Journal of Lower Genital Tract Disease 2014 Apr;18(2):182-9.

Jia J, Bosley AD, Thompson A, Hoskins JW, Cheuk A, Collins I, Parikh H, Xiao Z, Ylaya K, Dzyadyk M, Cozen W, Hernandez BY, Lynch CF, Loncarek J, Altekruse SF, Zhang L, Westlake CJ, Factor VM, Thorgeirsson S, Bamlet WR, Hewitt SM, Peterson GM, Andresson T, Amundadottir LT. CLPTM1L promotes growth and enhances aneuploidy in pancreatic cancer cells. Cancer Research 2014 May 15;74(10):2785-95.

Lal G, Hashimi S, Smith BJ, Lynch CF, Zhang L, Robinson RA, Weigel RJ. Extracellular matrix 1 (ECM1) expression is a novel prognostic marker for poor long-term survival in breast cancer: a hospital-based cohort study in Iowa. Annals of Surgical Oncology 2009;16(8):2280-2287.

Limburg PJ, Limsui D, Vierkant RA, Tillmans L, Wang AH, Lynch CF, Anderson KE, French AJ, Haile RW, Harnack LJ, Potter JD, Slager SL, Smyrk TC, Thibodeau SN, Cerhan JR. Postmenopausal hormone therapy and colorectal cancer risk in relation to somatic KRAS mutation status among older women. Cancer Epidemiology, Biomarkers and Prevention 2012;(4):681-684.

Limsui D, Vierkant RA, Tillmans LS, Wang AH, Weisenberger DJ, Laird PW, Lynch CF, Anderson KE, French AJ, Haile RW, Harnack LJ, Potter JD, Slager SL, Smyrk TC, Thibodeau SN, Cerhan JR, Limburg PJ. Cigarette smoking and colorectal cancer risk by molecularly-defined subtypes. J Natl Cancer Inst 2010;21;102(14):1012-1022.

Limsui D, Vierkant RA, Tillmans LS, Wang AH, Weisenberger DJ, Laird PW, Lynch CF, Anderson KE, French AJ, Haile RW, Harnack LJ, Potter JD, Slager SL, Smyrk TC, Thibodeau SN, Cerhan JR, Limburg PJ. Postmenopausal hormone therapy and colorectal cancer risk by molecularly defined subtypes among older women. Gut 2012 Sep;61(9):1299-1305.

Matsuno RK, Sherman ME, Visvanathan K, Goodman MT, Hernandez BY, Lynch CF, Ioffe OB, Horio D, Platz C, Altekruse SF, Pfeiffer RM, Anderson WF. Agreement for tumor grade of ovarian carcinoma: analysis of archival tissues from the surveillance, epidemiology and end results residual tissue repository. Cancer Causes and Control 2013 Apr;24(4):749-57.

Mbulaiteye SM, Pullarkat ST, Nathwani BN, Weiss LM, Rao N, Emmanuel B, Lynch CF, Hernandez B, Neppalli V, Hawes D, Cockburn MG, Kim A, Williams M, Altekruse S, Bhatia K, Goodman MT, Cozen W. Epstein-Barr virus patterns in U.S. Burkitt lymphoma tumors from the SEER residual tissue repository during 1979-2009. APMIS 2014 Jan;122(1):5-15.

Morton LM, Cerhan JR, Hartge P, Vasef MA, Neppalli VT, Natkunam Y, Dogan A, Dave BJ, Jain S, Levy R, Lossos IS, Cozen W, Davis S, Schenk MJ, Maurer MJ, Lynch CF, Rothman N, Chatterjee N, Yu K, Staudt LM, Weisenburger DD, Wang SS. Immunostaining to identify molecular subtypes of diffuse large B-cell lymphoma in a population-based study in the pre-rituximab era. International Journal of Molecular Epidemiology and Genetics 2011 Aug 30;2(3):245-252.

Muniz VP, Askeland RW, Zhang X, Reed SM, Tompkins VS, Hagen J, McDowell BD, Button A, Smith BJ, Weydert JA, Mezhir JJ, Quelle DE. RABL6A promotes oxaliplatin resistance in tumor cells and is a new marker of survival for resected pancreatic ductal adenocarcinoma patients. Genes Cancer 2013 Jul;4(7-8):273-84.

O’Leary BR, Fath MA, Bellizzi AM, Hrabe JE, Button AM, Allen BG, Case AJ, Altekruse S, Wagner B, Buettner GR, Lynch CF, Hernandez BY, Cozen W, Beardsley RA, Keene J, Henry MD, Domann FE, Spitz DR, Mezhir JJ. Loss of SOD3 (EcSOD) expression promotes an aggressive phenotype in human pancreatic ductal adenocarcinoma. Clinical Cancer Research 2015 Apr 1;21(7):1741-1751.

Razzak AA, Oxentenko AS, Vierkant RA, Tillmans LS, Wang AH, Weisenberger DJ, Laird PW, Lynch CF, Anderson KE, French AJ, Haile RW, Harnack LJ, Potter JD, Slager SL, Smyrk TC, Thibodeau SN, Cerhan JR, Limburg PJ. Associations between intake of folate and related micronutrients and molecularly defined colorectal cancer risks in the Iowa Women’s Health Study. Nutrition and Cancer 2012 Oct;64(7):899-910.

Razzak AA, Oxentenko AS, Vierkant RA, Tillmans LS, Wang AH, Weisenberger DJ, Laird PW, Lynch CF, Anderson KE, French AJ, Haile RW, Harnack LJ, Slager SL, Smyrk TC, Thibodeau SN, Cerhan JR, Limburg PJ. Alcohol intake and colorectal cancer risk by molecularly defined subtypes in a prospective study of older women. Cancer Prevention Research 2011;(12):2035-2043.

Samadder NJ, Vierkant RA, Tillmans LS, Wang AH, Lynch CF, Anderson KE, French AJ, Haile RW, Harnack LJ, Potter JD, Slager SL, Smyrk TC, Thibodeau SN, Cerhan JR, Limburg PJ. Cigarette smoking and colorectal cancer risk by KRAS mutation status among older women. American Journal of Gastroenterology 2012 May;107(5):782-789.

Samadder NJ, Vierkant RA, Tillmans LS, Wang AH, Weisenberger DJ, Laird PW, Lynch CF, Anderson KE, French AJ, Haile RW, Potter JD, Slager SL, Smyrk TC, Thibodeau SN, Cerhan JR, Limburg PJ. Associations between colorectal cancer molecular markers and pathways with clinicopathologic features in older women. Gastroenterology 2013 Aug;145(2):348-356.

Saraiya M, Unger ER, Thompson TD, Lynch CF, Hernandez BY, Lyu CW, Steinau M, Watson M, Wilkinson EJ, Hopenhayn C, Copeland G, Cozen W, Peters ES, Huang Y, Saber MS, Goodman MT; HPV Typing of Cancer Workgroup. Use of HPV types in cancers: Implications for current HPV and 9-valent vaccines. Journal of the National Cancer Institute 2015 Apr 29;107(6).

Sinno AK, Saraiya M, Thompson TD, Hernandez BY, Goodman MT, Steinau M, Lynch CF, Cozen W, Saber MS, Peters ES, Wilkinson EJ, Copeland G, Hopenhayn C, Watson M, Lyu C, Unger ER. Human papillomavirus genotype prevalence in invasive vaginal cancers from a registry-based population. Obstetrics & Gynecology 2014 Apr;123(4):817-821.

Steinau M, Saraiya M, Goodman MT, Peters ES, Watson M, Cleveland JL, Lynch CF, Wilkinson EJ, Hernandez BY, Copeland G, Saber MS, Hopenhayn C, Huang Y, Cozen W, Lyu C, Unger ER; HPV Typing of Cancers Workgroup. Human papillomavirus prevalence in oropharyngeal cancers before vaccine introduction, United States. Emerging Infectious Diseases 2014 May;20(5):822-8.

Steinau M, Unger ER, Hernandez BY, Goodman MT, Copeland G, Hopenhayn C, Cozen W, Saber MS, Huang Y, Peters ES, Lynch CF, Wilkinson EJ, Rajeevan MS, Lyu C, Saraiya M. Human papillomavirus prevalence in invasive anal cancers in the United States before vaccine introduction. Journal of Lower Genital Tract Disease 2013 Oct;17(4):397-403.

Sy MS, Altekruse SF, Li C, Lynch CF, Goodman MT, Hernandez BY, Huang X, Saber MS, Hewitt SM, Xin W. Association of prion protein expression with pancreatic adenocarcinoma survival in the SEER Residual Tissue Repository. Cancer Biomarkers 2012;10:251–258.

Takikita M, Altekruse S, Lynch CF, Goodman MT, Hernandez BY, Green M, Cozen W, Cockburn M, Saber MS, Topor M, Zeruto C, Abedi-Ardekani B, Reichman ME, Hewitt SM. Associations between selected biomarkers and prognosis in a population-based pancreatic cancer tissue microarray. Cancer Research 2009; 69(7):2950-2955.

Tillmans LS, Vierkant RA, Wang AH, Samadder NJ, Lynch CF, Anderson KE, French AJ, Haile RW, Harnack LJ, Potter JD, Slager SL, Smyrk TC, Thibodeau SN, Cerhan JR, Limburg PJ. Associations between cigarette smoking, hormone therapy and folate intake with incident colorectal cancer by TP53 protein expression level in a population-based cohort of older women. Cancer Epidemiology, Biomarkers & Prevention 2014 Feb;23(2):350-5.

Tillmans LS, Vierkant RA, Wang AH, Samadder NJ, Lynch CF, Anderson KE, French AJ, Haile RW, Harnack LJ, Potter JD, Slager SL, Smyrk TC, Thibodeau SN, Cerhan JR, Limburg PJ. Associations between environmental exposures and incident colorectal cancer by ESR2 protein expression level in a population-based cohort of older women. Cancer Epidemiology, Biomarkers, and Prevention 2015 Apr;24(4):713-719. 2015.