Case–Control Study of Cutaneous Human Papillomaviruses in Squamous Cell Carcinoma of the Skin

Cancer Epidemiology Biomarkers and Prevention - Tập 21 Số 8 - Trang 1303-1313 - 2012
Michelle R. Iannacone1,2,3, Tarik Gheit1,2,3, Tim Waterboer1,2,3, Anna R. Giuliano1,2,3, Jane L. Messina1, Neil A. Fenske1,3, Basil S. Cherpelis1,2,3, Vernon K. Sondak1,2,3, Richard G. Roetzheim1,2,3, Kristina M. Michael1,2,3, Massimo Tommasino1,2,3, Michael Pawlita1,2,3, Dana E. Rollison1,2,3
1Authors' Affiliations: 1Department of Cancer Epidemiology, 2Cutaneous Oncology Program, Moffitt Cancer Center; Departments of 3Pathology and Cell Biology, 4Dermatology & Cutaneous Surgery, and 5Family Medicine, University of South Florida College of Medicine, Tampa, Florida; 6International Agency for Research on Cancer, Lyon, France; and 7Infection and Cancer Program, German Cancer Research Center Deutsches Krebsforschungszentrum, DKFZ, Heidelberg, Germany
2Infection and Cancer Program, German Cancer Research Center, Deutsches Krebsforschungszentrum, DKFZ, Heidelberg, Germany
3International Agency for Research on Cancer, Lyon, France

Tóm tắt

Abstract Background: Cutaneous human papillomavirus (HPV) infection may be a risk factor for squamous cell carcinoma (SCC) of the skin. Methods: To investigate the association between cutaneous HPV and SCC, a case–control study was conducted, including 173 SCC cases from a university dermatology clinic and 300 controls that screened negative for skin cancer. Serum antibodies against cutaneous HPV types in genera alpha, beta, gamma, mu, and nu were measured. Tumor tissue from 159 SCC cases was tested for the presence of DNA for genus-beta HPV types. Using logistic regression ORs and 95% confidence intervals (CI) were estimated for the associations between SCC and cutaneous HPV infection, adjusting for age and sex. The Bonferroni method was used to account for multiple comparisons. Results: SCC was positively associated with seropositivity to any genus-beta HPV type (OR, 1.93; 95% CI, 1.23–3.02), particularly with types in species-1 (OR, 1.86; 95% CI, 1.22–2.85). Type-specific associations with SCC were observed for HPV 8 (OR, 1.80; 95% CI, 1.14–2.84), 17 (OR, 1.59; 95% CI, 1.02–2.49) and HPV 10 from genus-alpha (OR, 2.24; 95% CI, 1.04–4.85). None of the type-specific associations remained statistically significant after correction for multiple comparisons. When DNA-positive SCC cases were compared with controls, strong serologic associations were observed for HPVs 5 (OR, 3.48; 95% CI, 1.27–9.59), 17 (OR, 3.36; 95% CI, 1.29–8.72), and 24 (OR, 3.79; 95% CI, 1.24–11.5). Conclusion: Genus-beta HPV infections were associated with SCC in our study population. Impact: Identifying the role of cutaneous HPV infection in SCC may lead to improved characterization of high-risk individuals and the development of novel prevention strategies. Cancer Epidemiol Biomarkers Prev; 21(8); 1303–13. ©2012 AACR.

Từ khóa


Tài liệu tham khảo

Jemal, 2010, Cancer statistics, 2010, CA Cancer J Clin, 60, 277, 10.3322/caac.20073

Saladi, 2005, The causes of skin cancer: a comprehensive review, Drugs Today(Barc), 41, 37, 10.1358/dot.2005.41.1.875777

Andersson, 2008, Seroreactivity to cutaneous human papillomaviruses among patients with nonmelanoma skin cancer or benign skin lesions, Cancer Epidemiol Biomarkers Prev, 17, 189, 10.1158/1055-9965.EPI-07-0405

Casabonne, 2007, A prospective pilot study of antibodies against human papillomaviruses and cutaneous squamous cell carcinoma nested in the Oxford component of the European Prospective Investigation into Cancer and Nutrition, Int J Cancer, 121, 1862, 10.1002/ijc.22885

Feltkamp, 2003, Seroreactivity to epidermodysplasia verruciformis-related human papillomavirus types is associated with nonmelanoma skin cancer, Cancer Res, 63, 2695

Karagas, 2006, Human papillomavirus infection and incidence of squamous cell and basal cell carcinomas of the skin, J Natl Cancer Inst, 98, 389, 10.1093/jnci/djj092

Karagas, 2010, Genus beta human papillomaviruses and incidence of basal cell and squamous cell carcinomas of skin: population based case-control study, BMJ, 341, c2986, 10.1136/bmj.c2986

Struijk, 2006, Markers of cutaneous human papillomavirus infection in individuals with tumor-free skin, actinic keratoses, and squamous cell carcinoma, Cancer Epidemiol Biomarkers Prev, 15, 529, 10.1158/1055-9965.EPI-05-0747

Bernard, 2010, Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments, Virology, 401, 70, 10.1016/j.virol.2010.02.002

Forslund, 2003, A broad spectrum of human papillomavirus types is present in the skin of Australian patients with non-melanoma skin cancers and solar keratosis, Br J Dermatol, 149, 64, 10.1046/j.1365-2133.2003.05376.x

Waterboer, 2008, Serological association of beta and gamma human papillomaviruses with squamous cell carcinoma of the skin, Br J Dermatol, 159, 457, 10.1111/j.1365-2133.2008.08621.x

Forslund, 2007, Cutaneous human papillomaviruses found in sun-exposed skin: Beta-papillomavirus species 2 predominates in squamous cell carcinoma, J Infect Dis, 196, 876, 10.1086/521031

Harwood, 2000, Human papillomavirus infection and non-melanoma skin cancer in immunosuppressed and immunocompetent individuals, J Med Virol, 61, 289, 10.1002/1096-9071(200007)61:3<289::AID-JMV2>3.0.CO;2-Z

Pfister, 2003, High prevalence of epidermodysplasia verruciformis-associated human papillomavirus DNA in actinic keratoses of the immunocompetent population, Arch Dermatol Res, 295, 273, 10.1007/s00403-003-0435-2

Stockfleth, 2004, Human papillomaviruses in transplant-associated skin cancers, Dermatol Surg, 30, 604

Termorshuizen, 2004, Sunlight exposure and (sero)prevalence of epidermodysplasia verruciformis-associated human papillomavirus, J Invest Dermatol, 122, 1456, 10.1111/j.0022-202X.2004.22617.x

Rollison, 2012, Case-control study of Merkel cell polyomavirus infection and cutaneous squamous cell carcinoma, Cancer Epidemiol Biomarkers Prev, 21, 74, 10.1158/1055-9965.EPI-11-0764

Sehr, 2002, HPV antibody detection by ELISA with capsid protein L1 fused to glutathione S-transferase, J Virol Methods, 106, 61, 10.1016/S0166-0934(02)00134-9

Sehr, 2001, A generic capture ELISA for recombinant proteins fused to glutathione S-transferase: validation for HPV serology, J Immunol Methods, 253, 153, 10.1016/S0022-1759(01)00376-3

Waterboer, 2005, Multiplex human papillomavirus serology based on in situ-purified glutathione s-transferase fusion proteins, Clin Chem, 51, 1845, 10.1373/clinchem.2005.052381

Waterboer, 2006, Suppression of non-specific binding in serological Luminex assays, J Immunol Methods, 309, 200, 10.1016/j.jim.2005.11.008

Michael, 2008, Seroprevalence of 34 human papillomavirus types in the German general population, PLoS Pathog, 4, e1000091, 10.1371/journal.ppat.1000091

Gheit, 2007, Development of a sensitive and specific multiplex PCR method combined with DNA microarray primer extension to detect Betapapillomavirus types, J Clin Microbiol, 45, 2537, 10.1128/JCM.00747-07

Gheit, 2006, Development of a sensitive and specific assay combining multiplex PCR and DNA microarray primer extension to detect high-risk mucosal human papillomavirus types, J Clin Microbiol, 44, 2025, 10.1128/JCM.02305-05

Waterboer, 2009, Antibody responses to 26 skin human papillomavirus types in the Netherlands, Italy and Australia, J Gen Virol, 90, 1986, 10.1099/vir.0.010637-0

Plasmeijer, 2011, The Association between Cutaneous Squamous Cell Carcinoma and Betapapillomavirus Seropositivity: a Cohort Study, Cancer Epidemiol Biomarkers Prev, 20, 1171, 10.1158/1055-9965.EPI-11-0110

Bouwes, 2010, Multicenter study of the association between betapapillomavirus infection and cutaneous squamous cell carcinoma, Cancer Res, 70, 9777, 10.1158/0008-5472.CAN-10-0352

Kremsdorf, 1983, Human papillomaviruses associated with epidermodysplasia verruciformis. II. Molecular cloning and biochemical characterization of human papillomavirus 3a, 8, 10, and 12 genomes, J Virol, 48, 340, 10.1128/jvi.48.2.340-351.1983

Boxman, 2001, Transduction of the E6 and E7 genes of epidermodysplasia-verruciformis-associated human papillomaviruses alters human keratinocyte growth and differentiation in organotypic cultures, J Invest Dermatol, 117, 1397, 10.1046/j.0022-202x.2001.01602.x

Tomlins, 2010, Cutaneous HPV5 E6 causes increased expression of Osteoprotegerin and Interleukin 6 which contribute to evasion of UV-induced apoptosis, Carcinogenesis, 31, 2155, 10.1093/carcin/bgq200

Dong, 2008, Loss of p53 or p73 in human papillomavirus type 38 E6 and E7 transgenic mice partially restores the UV-activated cell cycle checkpoints, Oncogene, 27, 2923, 10.1038/sj.onc.1210944

Dong, 2005, Skin hyperproliferation and susceptibility to chemical carcinogenesis in transgenic mice expressing E6 and E7 of human papillomavirus type 38, J Virol, 79, 14899, 10.1128/JVI.79.23.14899-14908.2005

Jackson, 2000, Role of Bak in UV-induced apoptosis in skin cancer and abrogation by HPV E6 proteins, Genes Dev, 14, 3065, 10.1101/gad.182100

Jackson, 2000, E6 proteins from diverse cutaneous HPV types inhibit apoptosis in response to UV damage, Oncogene, 19, 592, 10.1038/sj.onc.1203339

Simmonds, 2008, Identification of the regions of the HPV 5 E6 protein involved in Bak degradation and inhibition of apoptosis, Int J Cancer, 123, 2260, 10.1002/ijc.23815

Viarisio, 2011, E6 and E7 from beta HPV38 cooperate with ultraviolet light in the development of actinic keratosis-like lesions and squamous cell carcinoma in mice, PLoS Pathog, 7, e1002125, 10.1371/journal.ppat.1002125

Hall, 2006, Re: Human papillomavirus infection and incidence of squamous cell and basal cell carcinomas of the skin, J Natl Cancer Inst, 98, 1425, 10.1093/jnci/djj379

Iannacone, 2012, Sunlight exposure and cutaneous human papillomavirus seroreactivity in basal cell and squamous cell carcinomas of the skin, J Infect Dis, 10.1093/infdis/jis374

Caldeira, 2003, The E6 and E7 proteins of the cutaneous human papillomavirus type 38 display transforming properties, J Virol, 77, 2195, 10.1128/JVI.77.3.2195-2206.2003

Iannacone, Risk factors for cutaneous human papillomavirus seroreactivity among patients undergoing skin cancer screening in Florida, J Infect Dis, 201, 760, 10.1086/650466

Rollison, 2008, Measures of cutaneous human papillomavirus infection in normal tissues as biomarkers of HPV in corresponding nonmelanoma skin cancers, Int J Cancer, 123, 2337, 10.1002/ijc.23795

Thông tin
Thông tin xuất bản

Cancer Epidemiology Biomarkers and Prevention

Tập 21 Số 8

1303-1313

Thông tin tác giả