Skip to main content
Top
Published in: Infectious Agents and Cancer 1/2011

Open Access 01-12-2011 | Research article

Distribution of HPV genotypes in cervical intraepithelial lesions and cervical cancer in Tanzanian women

Authors: Adriana C Vidal, Susan K Murphy, Brenda Y Hernandez, Brandi Vasquez, John A Bartlett, Olola Oneko, Pendo Mlay, Joseph Obure, Francine Overcash, Jennifer S Smith, Mike van der Kolk, Cathrine Hoyo

Published in: Infectious Agents and Cancer | Issue 1/2011

Login to get access

Abstract

Background

Infection with human papillomavirus (HPV) is associated with uterine cervical intraepithelial neoplasia (CIN) and invasive cancers (ICC). Approximately 80% of ICC cases are diagnosed in under-developed countries. Vaccine development relies on knowledge of HPV genotypes characteristic of LSIL, HSIL and cancer; however, these genotypes remain poorly characterized in many African countries. To contribute to the characterization of HPV genotypes in Northeastern Tanzania, we recruited 215 women from the Reproductive Health Clinic at Kilimanjaro Christian Medical Centre. Cervical scrapes and biopsies were obtained for cytology and HPV DNA detection.

Results

79 out of 215 (36.7%) enrolled participants tested positive for HPV DNA, with a large proportion being multiple infections (74%). The prevalence of HPV infection increased with lesion grade (14% in controls, 67% in CIN1 cases and 88% in CIN2-3). Among ICC cases, 89% had detectable HPV. Overall, 31 HPV genotypes were detected; the three most common HPV genotypes among ICC were HPV16, 35 and 45. In addition to these genotypes, co-infection with HPV18, 31, 33, 52, 58, 68 and 82 was found in 91% of ICC. Among women with CIN2-3, HPV53, 58 and 84/83 were the most common. HPV35, 45, 53/58/59 were the most common among CIN1 cases.

Conclusions

In women with no evidence of cytological abnormalities, the most prevalent genotypes were HPV58 with HPV16, 35, 52, 66 and 73 occurring equally. Although numerical constraints limit inference, findings that 91% of ICC harbor only a small number of HPV genotypes suggests that prevention efforts including vaccine development or adjuvant screening should focus on these genotypes.
Literature
1.
go back to reference Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM: Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 2008, 127: 2893-2917.CrossRef Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM: Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 2008, 127: 2893-2917.CrossRef
2.
go back to reference Bosch FX, Lorincz A, Munoz N, Meijer CJL, Shah KV: The causal relationship between human papillomavirus and cervical cancer. J Clin Pathol. 2002, 55: 244-265. 10.1136/jcp.55.4.244.PubMedPubMedCentralCrossRef Bosch FX, Lorincz A, Munoz N, Meijer CJL, Shah KV: The causal relationship between human papillomavirus and cervical cancer. J Clin Pathol. 2002, 55: 244-265. 10.1136/jcp.55.4.244.PubMedPubMedCentralCrossRef
3.
go back to reference Jung WW, Chun T, Sul D, Hwang KW, Kang HS, Lee DJ, Han IK: Strategies Against Human Papillomavirus Infection and Cervical Cancer. J Microbiol. 2004, 42: 255-266.PubMed Jung WW, Chun T, Sul D, Hwang KW, Kang HS, Lee DJ, Han IK: Strategies Against Human Papillomavirus Infection and Cervical Cancer. J Microbiol. 2004, 42: 255-266.PubMed
4.
go back to reference Tjalma WAA, Arbyn M, Paavonen J, Van Waes TR, Bogers JJ: Prophylactic human papillomavirus vaccines: the beginning of the end of cervical cancer. Int J Gynecol Cancer. 2004, 14: 751-761. 10.1111/j.1048-891X.2004.014505.x.PubMedCrossRef Tjalma WAA, Arbyn M, Paavonen J, Van Waes TR, Bogers JJ: Prophylactic human papillomavirus vaccines: the beginning of the end of cervical cancer. Int J Gynecol Cancer. 2004, 14: 751-761. 10.1111/j.1048-891X.2004.014505.x.PubMedCrossRef
5.
go back to reference Baseman JG, Koutsky LA: The epidemiology of human papillomavirus infections. Review. J Clin Virol. 2005, 32 (Suppl): S16-S24.PubMedCrossRef Baseman JG, Koutsky LA: The epidemiology of human papillomavirus infections. Review. J Clin Virol. 2005, 32 (Suppl): S16-S24.PubMedCrossRef
6.
go back to reference JM M, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snidjers PJ, Peto J, Meijer CJL, Munoz N: Human papilomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol. 1999, 189: 12-19. 10.1002/(SICI)1096-9896(199909)189:1<12::AID-PATH431>3.0.CO;2-F.CrossRef JM M, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snidjers PJ, Peto J, Meijer CJL, Munoz N: Human papilomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol. 1999, 189: 12-19. 10.1002/(SICI)1096-9896(199909)189:1<12::AID-PATH431>3.0.CO;2-F.CrossRef
7.
go back to reference Sigurdsson K, Taddeo FJ, Benediktsdottir KR, Olafsdottir K, Sigvaldason H, Oddsson K, Rafnar T: HPV genotypes in CIN 2-3 lesions and cervical cancer: a population-based study. Int J Cancer. 2007, 121: 2682-2687. 10.1002/ijc.23034.PubMedCrossRef Sigurdsson K, Taddeo FJ, Benediktsdottir KR, Olafsdottir K, Sigvaldason H, Oddsson K, Rafnar T: HPV genotypes in CIN 2-3 lesions and cervical cancer: a population-based study. Int J Cancer. 2007, 121: 2682-2687. 10.1002/ijc.23034.PubMedCrossRef
8.
go back to reference Coutlee F, Ratnam S, Ramanakumar AV, Insinga RP, Bentley J, Escott N, Ghatage P, Koushik A, Ferenczy A, Franco EL: Distribution of human papillomavirus genotypes in cervical intraepithelial neoplasia and invasive cervical cancer in Canada. J Med Virol. 2011, 83: 1034-1041. 10.1002/jmv.22081.PubMedCrossRef Coutlee F, Ratnam S, Ramanakumar AV, Insinga RP, Bentley J, Escott N, Ghatage P, Koushik A, Ferenczy A, Franco EL: Distribution of human papillomavirus genotypes in cervical intraepithelial neoplasia and invasive cervical cancer in Canada. J Med Virol. 2011, 83: 1034-1041. 10.1002/jmv.22081.PubMedCrossRef
9.
go back to reference Clifford GM, Smith JS, Aguado T, Franceschi S: Comparison of HPV type distribution in high-grade cervical lesions and cervical intraepithelial neoplasia grade 3. Cancer Epidemiol Biomarkers Prev. 2003, 19: 1675-1681. Clifford GM, Smith JS, Aguado T, Franceschi S: Comparison of HPV type distribution in high-grade cervical lesions and cervical intraepithelial neoplasia grade 3. Cancer Epidemiol Biomarkers Prev. 2003, 19: 1675-1681.
10.
go back to reference Insinga RP, Liaw KL, Johnson LG, Madeleine MM: A systematic review of the prevalence and attribution of human papillomavirus types among cervical, vaginal, and vulvar precancers and cancers in the Unites States. Cancer Epidemiol Biomarkers Prev. 2008, 17: 1611-11622. 10.1158/1055-9965.EPI-07-2922.PubMedPubMedCentralCrossRef Insinga RP, Liaw KL, Johnson LG, Madeleine MM: A systematic review of the prevalence and attribution of human papillomavirus types among cervical, vaginal, and vulvar precancers and cancers in the Unites States. Cancer Epidemiol Biomarkers Prev. 2008, 17: 1611-11622. 10.1158/1055-9965.EPI-07-2922.PubMedPubMedCentralCrossRef
11.
go back to reference Munoz N, Bosch FX, Castellsague X, Diaz M, de-SanJose S, Hammouda D, Shah KV, Meijer CJL: Against which human papillomavirus types shall we vaccinate and screen? The international perspective. Int J Cancer. 2004, 111: 278-285. 10.1002/ijc.20244.PubMedCrossRef Munoz N, Bosch FX, Castellsague X, Diaz M, de-SanJose S, Hammouda D, Shah KV, Meijer CJL: Against which human papillomavirus types shall we vaccinate and screen? The international perspective. Int J Cancer. 2004, 111: 278-285. 10.1002/ijc.20244.PubMedCrossRef
12.
go back to reference Clifford GM, Smith JS, Plummer M, Munoz N, Franceschi S: Human papillomavirus types in invasive cervical cancer worldwide: a meta-analysis. Br J Cancer. 2003, 88: 63-73. 10.1038/sj.bjc.6600688.PubMedPubMedCentralCrossRef Clifford GM, Smith JS, Plummer M, Munoz N, Franceschi S: Human papillomavirus types in invasive cervical cancer worldwide: a meta-analysis. Br J Cancer. 2003, 88: 63-73. 10.1038/sj.bjc.6600688.PubMedPubMedCentralCrossRef
13.
go back to reference Cuzick J, Arbyn M, Sankaranarayanan R, Tsu V, Ronco G, Mayrand MH, Dillner J, Meijer CJLM: Overview of human papillomavirus-based and other novel options for cervical cancer screening in developed and developing countries. Vaccine. 2008, 265: K29-K41.CrossRef Cuzick J, Arbyn M, Sankaranarayanan R, Tsu V, Ronco G, Mayrand MH, Dillner J, Meijer CJLM: Overview of human papillomavirus-based and other novel options for cervical cancer screening in developed and developing countries. Vaccine. 2008, 265: K29-K41.CrossRef
14.
go back to reference Castellsague X, Menendez C, Loscertales MP, Kornegay JR, dos Santos F, Gomez-Olive FX, Lloveras B, Abarca N, Vaz N, Barreto A, Bosch FX, Alonso P: Human papillomavirus genotypes in rural Mozambique. Lancet. 2001, 358: 1429-1430. 10.1016/S0140-6736(01)06523-0.PubMedCrossRef Castellsague X, Menendez C, Loscertales MP, Kornegay JR, dos Santos F, Gomez-Olive FX, Lloveras B, Abarca N, Vaz N, Barreto A, Bosch FX, Alonso P: Human papillomavirus genotypes in rural Mozambique. Lancet. 2001, 358: 1429-1430. 10.1016/S0140-6736(01)06523-0.PubMedCrossRef
15.
go back to reference De Vuyst H, Steyaert S, Van Renterghem L, Claeys P, Muchiri L, Sitati S, Vansteelandt S, Quint W, Kleter B, Van Marck E, Temmerman M: Distribution of human papillomavirus in a family planning population in Nairobi, Kenya. Sex Transm Dis. 2003, 30: 137-142. 10.1097/00007435-200302000-00009.PubMedCrossRef De Vuyst H, Steyaert S, Van Renterghem L, Claeys P, Muchiri L, Sitati S, Vansteelandt S, Quint W, Kleter B, Van Marck E, Temmerman M: Distribution of human papillomavirus in a family planning population in Nairobi, Kenya. Sex Transm Dis. 2003, 30: 137-142. 10.1097/00007435-200302000-00009.PubMedCrossRef
16.
go back to reference Wall SR, Scherf CF, Morrison L, Hart KW, West B, Ekpo G, Fiander AN, Man S, Gelder CM, G. Walraven G, Borysiewicz LK: Cervical human papilloma virus infection and squamous intraepithelial lesions in rural Gambia, West-Africa: viral sequence analysis and epidemiology. Br J Cancer. 2005, 93: 1068-1076. 10.1038/sj.bjc.6602736.PubMedPubMedCentralCrossRef Wall SR, Scherf CF, Morrison L, Hart KW, West B, Ekpo G, Fiander AN, Man S, Gelder CM, G. Walraven G, Borysiewicz LK: Cervical human papilloma virus infection and squamous intraepithelial lesions in rural Gambia, West-Africa: viral sequence analysis and epidemiology. Br J Cancer. 2005, 93: 1068-1076. 10.1038/sj.bjc.6602736.PubMedPubMedCentralCrossRef
17.
go back to reference Mayaud P, Weiss HA, Lacey CJN, Gill DK, Mabey DCW: Genital human papillomavirus genotypes in Northwestern Tanzania. J Clin Microbiol. 2003, 41: 4451-4453. 10.1128/JCM.41.9.4451-4453.2003.PubMedPubMedCentralCrossRef Mayaud P, Weiss HA, Lacey CJN, Gill DK, Mabey DCW: Genital human papillomavirus genotypes in Northwestern Tanzania. J Clin Microbiol. 2003, 41: 4451-4453. 10.1128/JCM.41.9.4451-4453.2003.PubMedPubMedCentralCrossRef
18.
go back to reference Didelot-Rousseau MN, Nagot N, Costes-Martineau V, Valles X, Ouedraogo A, Konate I, Weiss HA, Van de Perre P, Mayaud P, Segondy M: Human papillomavirus genotype distribution and cervical squamous intraepithelial lesions among high-risk women with and without HIV-I infection in Burkina Faso. Br J Cancer. 2006, 95: 355-362. 10.1038/sj.bjc.6603252.PubMedPubMedCentralCrossRef Didelot-Rousseau MN, Nagot N, Costes-Martineau V, Valles X, Ouedraogo A, Konate I, Weiss HA, Van de Perre P, Mayaud P, Segondy M: Human papillomavirus genotype distribution and cervical squamous intraepithelial lesions among high-risk women with and without HIV-I infection in Burkina Faso. Br J Cancer. 2006, 95: 355-362. 10.1038/sj.bjc.6603252.PubMedPubMedCentralCrossRef
19.
go back to reference Apgar BS, Zoschnick L, Wright TC: The 2001 Bethesda system terminology. Am Fam Physician. 1998, 68: 10- Apgar BS, Zoschnick L, Wright TC: The 2001 Bethesda system terminology. Am Fam Physician. 1998, 68: 10-
20.
go back to reference Gravitt PE, Kamath AM, Gaffikin L, Chirenje ZM, Womack S, Shah KV: Human papillomavirus genotype prevalence in high-grade squamous intraepithelial lesions and colposcopically normal women from Zimbabwe. Int J Cancer. 2002, 100: 729-732. 10.1002/ijc.10538.PubMedCrossRef Gravitt PE, Kamath AM, Gaffikin L, Chirenje ZM, Womack S, Shah KV: Human papillomavirus genotype prevalence in high-grade squamous intraepithelial lesions and colposcopically normal women from Zimbabwe. Int J Cancer. 2002, 100: 729-732. 10.1002/ijc.10538.PubMedCrossRef
21.
go back to reference Mayhood MK, Afwamba IA, Odhiambo CO, Ndanu E, Thielman NM, Morrissey AB, Shao JF, Wells Pence B, Crump JA: Validation, performance under field conditions, and cost-effectiveness of Capiullus HIV-1/HIV-2 and Determine HIV1/2 rapid human immunodeficiency virus antibody assays using sequencial and parallel testing algorithms in Tanzania. J Clin Microbiol. 2008, 46: 3946-3951. 10.1128/JCM.01045-08.PubMedPubMedCentralCrossRef Mayhood MK, Afwamba IA, Odhiambo CO, Ndanu E, Thielman NM, Morrissey AB, Shao JF, Wells Pence B, Crump JA: Validation, performance under field conditions, and cost-effectiveness of Capiullus HIV-1/HIV-2 and Determine HIV1/2 rapid human immunodeficiency virus antibody assays using sequencial and parallel testing algorithms in Tanzania. J Clin Microbiol. 2008, 46: 3946-3951. 10.1128/JCM.01045-08.PubMedPubMedCentralCrossRef
22.
go back to reference Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, Benbrahim-Tallaa L, Guha N, Freeman C, Galichet L, Cogliano V: WHO International agency for research on cancer monograph working group: a review of human carcinogenesis - Part B: biological agents. Lancet Oncol. 2009, 10: 321-322. 10.1016/S1470-2045(09)70096-8.PubMedCrossRef Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, Benbrahim-Tallaa L, Guha N, Freeman C, Galichet L, Cogliano V: WHO International agency for research on cancer monograph working group: a review of human carcinogenesis - Part B: biological agents. Lancet Oncol. 2009, 10: 321-322. 10.1016/S1470-2045(09)70096-8.PubMedCrossRef
23.
go back to reference Smith JS, Lindsay L, Hoots B, Keys J, Franceschi S, Winer R, Clifford GM: Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update. Int J Cancer. 2007, 121: 621-632. 10.1002/ijc.22527.PubMedCrossRef Smith JS, Lindsay L, Hoots B, Keys J, Franceschi S, Winer R, Clifford GM: Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update. Int J Cancer. 2007, 121: 621-632. 10.1002/ijc.22527.PubMedCrossRef
24.
go back to reference Ter Meulen J, Eberhardt HC, Luande J, Mgaya HN, Chang-Claude J, Mtiro H, Minha M, Kashaija P, Yu X, Meinhardt G, Gissman L, Pawlita M: Human papillomavirus (HPV) infection, HIV-1 infection and cervical cancer in Tanzania, East Africa. Int J Cancer. 1992, 51: 515-521. 10.1002/ijc.2910510403.PubMedCrossRef Ter Meulen J, Eberhardt HC, Luande J, Mgaya HN, Chang-Claude J, Mtiro H, Minha M, Kashaija P, Yu X, Meinhardt G, Gissman L, Pawlita M: Human papillomavirus (HPV) infection, HIV-1 infection and cervical cancer in Tanzania, East Africa. Int J Cancer. 1992, 51: 515-521. 10.1002/ijc.2910510403.PubMedCrossRef
25.
go back to reference Chabaud M, Le Cann P, Mayelo V, Leboulleux D, Diallo AS, Enogat N, Afoutou JM, Anthonioz P, Coll-Seck AM, Coursaget P: Detection by PCR of human papillomavirus genotypes in cervical lesions of Senegalese women. J Med Virol. 1996, 49: 259-263. 10.1002/(SICI)1096-9071(199608)49:4<259::AID-JMV1>3.0.CO;2-2.PubMedCrossRef Chabaud M, Le Cann P, Mayelo V, Leboulleux D, Diallo AS, Enogat N, Afoutou JM, Anthonioz P, Coll-Seck AM, Coursaget P: Detection by PCR of human papillomavirus genotypes in cervical lesions of Senegalese women. J Med Virol. 1996, 49: 259-263. 10.1002/(SICI)1096-9071(199608)49:4<259::AID-JMV1>3.0.CO;2-2.PubMedCrossRef
26.
go back to reference La Ruche G, You B, Mensah-Ado I, Bergeron C, Montcho C, Ramon R, Toure-Coulibaly K, Welffens-Ekre C, Dabis F, Orth G: Human papillomavirus and human immunodeficiency virus infections: relation with cervical dysplasia - neoplasia in African women. Int J Cancer. 1998, 76: 480-486. 10.1002/(SICI)1097-0215(19980518)76:4<480::AID-IJC6>3.0.CO;2-N.PubMedCrossRef La Ruche G, You B, Mensah-Ado I, Bergeron C, Montcho C, Ramon R, Toure-Coulibaly K, Welffens-Ekre C, Dabis F, Orth G: Human papillomavirus and human immunodeficiency virus infections: relation with cervical dysplasia - neoplasia in African women. Int J Cancer. 1998, 76: 480-486. 10.1002/(SICI)1097-0215(19980518)76:4<480::AID-IJC6>3.0.CO;2-N.PubMedCrossRef
27.
go back to reference Bayo S, Bosch FX, de Sanjose S, Munoz N, Combita AL, Coursaget P, Diaz M, Dolo A, van den Brule AJ, Meijer CJL: Risk factors of invasive cervical cancer in Mali. Int J Epidemiol. 2002, 31: 202-209. 10.1093/ije/31.1.202.PubMedCrossRef Bayo S, Bosch FX, de Sanjose S, Munoz N, Combita AL, Coursaget P, Diaz M, Dolo A, van den Brule AJ, Meijer CJL: Risk factors of invasive cervical cancer in Mali. Int J Epidemiol. 2002, 31: 202-209. 10.1093/ije/31.1.202.PubMedCrossRef
28.
go back to reference Kay P, Soeters R, Nevin J, Denny L, Dehaeck CMC, Williamson AL: High prevalence of HPV16 in South African women with cancer of the cervix and cervical intraepithelial neoplasia. J Med Virol. 2003, 71: 265-273. 10.1002/jmv.10479.PubMedCrossRef Kay P, Soeters R, Nevin J, Denny L, Dehaeck CMC, Williamson AL: High prevalence of HPV16 in South African women with cancer of the cervix and cervical intraepithelial neoplasia. J Med Virol. 2003, 71: 265-273. 10.1002/jmv.10479.PubMedCrossRef
29.
go back to reference Koushik A, Ghosh A, Duarte-Franco E, Forest P, Voyer H, Matlashewski G, Coutlee F, Franco EL: The p53 codon 72 polymorphism and risk of high-grade cervical intraepithelial neoplasia. Cancer Detect Prev. 2005, 29: 307-316. 10.1016/j.cdp.2005.06.007.PubMedCrossRef Koushik A, Ghosh A, Duarte-Franco E, Forest P, Voyer H, Matlashewski G, Coutlee F, Franco EL: The p53 codon 72 polymorphism and risk of high-grade cervical intraepithelial neoplasia. Cancer Detect Prev. 2005, 29: 307-316. 10.1016/j.cdp.2005.06.007.PubMedCrossRef
30.
go back to reference Castle PE, Schiffman M, Wheeler CM, Wentzensen N, Gravitt PE: Human papillomavirus genotypes in cervical intraepithelial neoplasia grade 3. Cancer Epidemiol Biomarkers Prev. 2010, 19: 1675-1681. 10.1158/1055-9965.EPI-10-0251.PubMedPubMedCentralCrossRef Castle PE, Schiffman M, Wheeler CM, Wentzensen N, Gravitt PE: Human papillomavirus genotypes in cervical intraepithelial neoplasia grade 3. Cancer Epidemiol Biomarkers Prev. 2010, 19: 1675-1681. 10.1158/1055-9965.EPI-10-0251.PubMedPubMedCentralCrossRef
31.
go back to reference de San Jose S, Diaz M, Castellsague X, Clifford G, Bruni L, Munoz N, Bosch FX: Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: a meta-analysis. Lancet Infect Dis. 2007, 7: 453-459. 10.1016/S1473-3099(07)70158-5.CrossRef de San Jose S, Diaz M, Castellsague X, Clifford G, Bruni L, Munoz N, Bosch FX: Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: a meta-analysis. Lancet Infect Dis. 2007, 7: 453-459. 10.1016/S1473-3099(07)70158-5.CrossRef
32.
go back to reference Gravitt PE, Kamath AM, Gaffikin L, Chirenje ZM, Womack S, Shah KV: Human papillomavirus genotype prevalence in high-grade squamous intraepithelial lesions and colposcopically normal women from Zimbabwe. Int J Cancer. 2002, 100: 729-732. 10.1002/ijc.10538.PubMedCrossRef Gravitt PE, Kamath AM, Gaffikin L, Chirenje ZM, Womack S, Shah KV: Human papillomavirus genotype prevalence in high-grade squamous intraepithelial lesions and colposcopically normal women from Zimbabwe. Int J Cancer. 2002, 100: 729-732. 10.1002/ijc.10538.PubMedCrossRef
33.
go back to reference Adam E, Kaufman RH, Berkova Z, Icenogle J, Reeves WC: Is human papillomavirus testing an effective triage method for detection of high-grade (grade 2 or 3) cervical intraepithelial neoplasia?. Am J Obstet Gynecol. 1998, 178: 1235-1244. 10.1016/S0002-9378(98)70328-X.PubMedCrossRef Adam E, Kaufman RH, Berkova Z, Icenogle J, Reeves WC: Is human papillomavirus testing an effective triage method for detection of high-grade (grade 2 or 3) cervical intraepithelial neoplasia?. Am J Obstet Gynecol. 1998, 178: 1235-1244. 10.1016/S0002-9378(98)70328-X.PubMedCrossRef
34.
go back to reference Ho GYF, Kadish AS, Burk RD, Basu J, Palan PR, Mikhail M, Romney SL: HPV 16 and cigarette smoking as risk factors for high-grade cervical intra-epithelial neoplasia. Int J Cancer. 1998, 78: 281-285. 10.1002/(SICI)1097-0215(19981029)78:3<281::AID-IJC3>3.0.CO;2-R.PubMedCrossRef Ho GYF, Kadish AS, Burk RD, Basu J, Palan PR, Mikhail M, Romney SL: HPV 16 and cigarette smoking as risk factors for high-grade cervical intra-epithelial neoplasia. Int J Cancer. 1998, 78: 281-285. 10.1002/(SICI)1097-0215(19981029)78:3<281::AID-IJC3>3.0.CO;2-R.PubMedCrossRef
35.
go back to reference McLehose RF, Harpster A, Lanier AP, Schiff MA, Koehler K, Murphy N, Becker TM: Risk factors for cervical intraepithelial neoplasm in Alaska Native women: a pilot study. Alaska Med. 1999, 41: 76-85. McLehose RF, Harpster A, Lanier AP, Schiff MA, Koehler K, Murphy N, Becker TM: Risk factors for cervical intraepithelial neoplasm in Alaska Native women: a pilot study. Alaska Med. 1999, 41: 76-85.
36.
go back to reference Liaw KL, Hidelsheim A, Burk RD, Gravitt P, Wacholder S, Manos MM, Scott DR, Scherman ME, Kurman RJ, Glass AG, Anderson SM, Schiffman MA: A prospective study of human papillomavirus (HPV) type 16 DNA detection by polymerase chain reaction and its association with acquisition and persistence of other HPV types. J Infect Dis. 2001, 183: 8-15. 10.1086/317638.PubMedCrossRef Liaw KL, Hidelsheim A, Burk RD, Gravitt P, Wacholder S, Manos MM, Scott DR, Scherman ME, Kurman RJ, Glass AG, Anderson SM, Schiffman MA: A prospective study of human papillomavirus (HPV) type 16 DNA detection by polymerase chain reaction and its association with acquisition and persistence of other HPV types. J Infect Dis. 2001, 183: 8-15. 10.1086/317638.PubMedCrossRef
37.
go back to reference Bosch XF, de Sanjose S: Human papillomavirus and cervical cancer- burden and assessment of causality. J Natl Cancer Inst Monogr. 2003, 31: 3-13.PubMedCrossRef Bosch XF, de Sanjose S: Human papillomavirus and cervical cancer- burden and assessment of causality. J Natl Cancer Inst Monogr. 2003, 31: 3-13.PubMedCrossRef
38.
go back to reference Bontkes HJ, deGruijl TD, Walboomers JM, Schiller JT, Dillner J, Helmerhorst TJ, Vereheijen RH, Schper RJ, Meijer CJL: Immune responses against human papillomavirus (HPV) type 16 virus-like particles in a cohort study of women with cervical intraepithelial neoplasia. II. Systemic but not local IgA responses correlate with clearance of HPV-16. J Gen Virol. 1999, 80: 409-417.PubMedCrossRef Bontkes HJ, deGruijl TD, Walboomers JM, Schiller JT, Dillner J, Helmerhorst TJ, Vereheijen RH, Schper RJ, Meijer CJL: Immune responses against human papillomavirus (HPV) type 16 virus-like particles in a cohort study of women with cervical intraepithelial neoplasia. II. Systemic but not local IgA responses correlate with clearance of HPV-16. J Gen Virol. 1999, 80: 409-417.PubMedCrossRef
39.
go back to reference Louie KS, de Sanjose S, Mayaud P: Epidemiology and prevention of human papillomavirus and cervical cancer in sub-Saharan Africa: a comprehensive review. Tropical Medicine and International Health. 2009, 14: 1287-1302. 10.1111/j.1365-3156.2009.02372.x.PubMedCrossRef Louie KS, de Sanjose S, Mayaud P: Epidemiology and prevention of human papillomavirus and cervical cancer in sub-Saharan Africa: a comprehensive review. Tropical Medicine and International Health. 2009, 14: 1287-1302. 10.1111/j.1365-3156.2009.02372.x.PubMedCrossRef
Metadata
Title
Distribution of HPV genotypes in cervical intraepithelial lesions and cervical cancer in Tanzanian women
Authors
Adriana C Vidal
Susan K Murphy
Brenda Y Hernandez
Brandi Vasquez
John A Bartlett
Olola Oneko
Pendo Mlay
Joseph Obure
Francine Overcash
Jennifer S Smith
Mike van der Kolk
Cathrine Hoyo
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Infectious Agents and Cancer / Issue 1/2011
Electronic ISSN: 1750-9378
DOI
https://doi.org/10.1186/1750-9378-6-20

Other articles of this Issue 1/2011

Infectious Agents and Cancer 1/2011 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine