Differences in the risk of cervical cancer and human papillomavirus infection by education level

British Journal of Cancer

Volumn 101, Issue 5, 2009, Pages 865-870

  Franceschi, S ^a   Plummer, M ^a   Clifford, G ^a   De Sanjose, S ^b   Bosch, X ^b   Herrero, R ^c   Muoz N ^d   Vaccarella, S ^a  

^a INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^b HOSPITAL DURAN I REYNALS   (Spain)

^c Proyecto Epidemiologico Guanacaste   (Costa Rica)

^d Instituto Nacional de Cancerología   (Colombia)

Author keywords

Age at first pregnancy; Age at first sexual intercourse; Cervical cancer; Education; Human papillomavirus

Indexed keywords

ARTICLE; CANCER RISK; CANCER SCREENING; CONDOM; CORRELATIONAL STUDY; EDUCATIONAL STATUS; FEMALE; GROUPS BY AGE; HUMAN; MAJOR CLINICAL STUDY; MATERNAL AGE; ORAL CONTRACEPTION; PAPANICOLAOU TEST; PAPILLOMA; PARITY; POLYMERASE CHAIN REACTION; PREVALENCE; PRIMIPARA; PRIORITY JOURNAL; SEXUAL BEHAVIOR; SEXUAL INTERCOURSE; SEXUALITY; SMOKING; SOCIAL STATUS; UTERINE CERVIX CANCER; VIRUS DETECTION; WART VIRUS;

ADOLESCENT; ADULT; CASE-CONTROL STUDIES; EDUCATIONAL STATUS; FEMALE; HUMANS; ODDS RATIO; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; REGRESSION ANALYSIS; RISK FACTORS; UTERINE CERVICAL NEOPLASMS;

EID: 70249092483     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6605224     Document Type: Article

References (47)

1. Anh PT, Hieu NT, Herrero R, Vaccarella S, Smith JS, Thuy NT, Nga NH, Duc NB, Ashley R, Snijders PJ, Meijer CJ, Munoz N, Parkin DM, Franceschi S (2003) Human papillomavirus infection among women in South and North Vietnam. Int J Cancer 104: 213-220 (Pubitemid 36249797)
2. Banura C, Franceschi S, van Doorn LJ, Arslan A, Wabwire-Mangen F, Mbidde EK, Quint W, Weiderpass E (2008) Infection with human papillomavirus and HIV among young women in Kampala, Uganda. J Infect Dis 197: 555-562 (Pubitemid 351321533)
3. Bardin A, Vaccarella S, Clifford GM, Lissowska J, Rekosz M, Bobkiewicz P, Kupryjanczyk J, Krynicki R, Jonska-Gmyrek J, Danska-Bidzinska A, Snijders PJ, Meijer CJ, Zatonski W, Franceschi S (2008) Human papillomavirus infection in women with and without cervical cancer in Warsaw, Poland. Eur J Cancer 44: 557-564
4. Bayo S, Bosch FX, de Sanjose S, Munoz N, Combita AL, Coursaget P, Diaz M, Dolo A, van den Brule AJ, Meijer CJ (2002) Risk factors of invasive cervical cancer in Mali. Int J Epidemiol 31: 202-209
5. Chaouki N, Bosch FX, Munoz N, Meijer CJ, El Gueddari B, El Ghazi A, Deacon J, Castellsague X, Walboomers JM (1998) The viral origin of cervical cancer in Rabat, Morocco. Int J Cancer 75: 546-554
6. Chichareon S, Herrero R, Munoz N, Bosch FX, Jacobs MV, Deacon J, Santamaria M, Chongsuvivatwong V, Meijer CJ, Walboomers JM (1998) Risk factors for cervical cancer in Thailand: a case-control study. J Natl Cancer Inst 90: 50-57 (Pubitemid 28078081)
7. Dai M, Bao YP, Li N, Clifford GM, Vaccarella S, Snijders PJF, Huang RD, Sun LX, Meijer CJLM, Qiao YL, Franceschi S (2006) Human papilloma-virus infection in Shanxi Province, People?s Republic of China: a population-based study. Br J Cancer 95: 96-101 (Pubitemid 43980561)
8. de Sanjose S, Almirall R, Lloveras B, Font R, Diaz M, Munoz N, Catala I, Meijer CJ, Snijders PJ, Herrero R, Bosch FX (2003) Cervical human papillomavirus infection in the female population in Barcelona, Spain. Sex Transm Dis 30: 788-793
9. de Sanjose S, Bosch FX, Munoz N, Shah K (1997) Social differences in sexual behaviour and cervical cancer. IARC Sci Publ 138: 309-317
10. Deacon JM, Evans CD, Yule R, Desai M, Binns W, Taylor C, Peto J (2000) Sexual behaviour and smoking as determinants of cervical HPV infection and of CIN3 among those infected: a case-control study nested within the Manchester cohort. Br J Cancer 83: 1565-1572
11. Dondog B, Clifford GM, Vaccarella S, Waterboer T, Unurjargal D, Avirmed D, Enkhtuya S, Kommoss F, Wentzensen N, Snijders PJ, Meijer CJ, Franceschi S, Pawlita M (2008) Human papillomavirus infection in Ulaanbaatar, Mongolia: a population-based study. Cancer Epidemiol Biomarkers Prev 17: 1731-1738
12. Eluf-Neto J, Booth M, Munoz N, Bosch FX, Meijer CJ, Walboomers JM (1994) Human papillomavirus and invasive cervical cancer in Brazil. Br J Cancer 69: 114-119
13. Ferreccio C, Prado RB, Luzoro AV, Ampuero SL, Snijders PJ, Meijer CJ, Vaccarella S, Jara AT, Puschel KI, Robles SC, Herrero R, Franceschi S, Ojeda JM (2004) Population-based prevalence and age distribution of human papillomavirus among women in Santiago, Chile. Cancer Epidemiol Biomarkers Prev 13: 2271-2276 (Pubitemid 40054329)
14. Franceschi S, Herrero R, Clifford GM, Snijders PJ, Arslan A, Anh PT, Bosch FX, Ferreccio C, Hieu NT, Lazcano-Ponce E, Matos E, Molano M, Qiao YL, Rajkumar R, Ronco G, de Sanjose S, Shin HR, Sukvirach S, Thomas JO, Meijer CJ, Munoz N, the IARC HPV Prevalence Surveys Study Group (2006) Variations in the age-specific curves of human papillomavirus prevalence in women worldwide. Int J Cancer 119: 2677-2684
15. Franceschi S, Rajkumar T, Vaccarella S, Gajalakshmi V, Sharmila A, Snijders PJ, Munoz N, Meijer CJ, Herrero R (2003) Human papilloma-virus and risk factors for cervical cancer in Chennai, India: a case-control study. Int J Cancer 107: 127-133
16. Gelman A, Jakulin A, Pittau MG, Su YS (2008) A weakly informative default prior distribution for logistic and other regression models. Ann Appl Stat 2: 1360-1383
17. Hammouda D, Munoz N, Herrero R, Arslan A, Bouhadef A, Oublil M, Djedeat B, Fontaniere B, Snijders P, Meijer C, Franceschi S (2005) Cervical carcinoma in Algiers, Algeria: human papillomavirus and lifestyle risk factors. Int J Cancer 113: 483-489
18. Hibbitts S, Jones J, Powell N, Dallimore N, McRea J, Beer H, Tristram A, Fielder H, Fiander AN (2008) Human papillomavirus prevalence in women attending routine cervical screening in South Wales, UK: a cross-sectional study. Br J Cancer 99: 1929-1933
19. Hildesheim A, Gravitt P, Schiffman MH, Kurman RJ, Barnes W, Jones S, Tchabo JG, Brinton LA, Copeland C, Epp J (1993) Determinants of genital human papillomavirus infection in low-income women in Washington, D.C. Sex Transm Dis 20: 279-285 (Pubitemid 23286958)
20. International Collaboration of Epidemiological Studies of Cervical Cancer (2006) Cervical carcinoma and reproductive factors: collaborative reanalysis of individual data on 16,563 women with cervical carcinoma and 33,542 women without cervical carcinoma from 25 epidemiological studies. Int J Cancer 119: 1108-1124
21. International Collaboration of Epidemiological Studies of Cervical Cancer (2009) Cervical carcinoma and sexual behavior: collaborative reanalysis of individual data on 15,461 women with cervical carcinoma and 29,164 women without cervical carcinoma from 21 epidemiological studies. Cancer Epidemiol Biomarkers Prev 18: 1060-1069
22. Jacobs MV, Roda Husman AM, van den Brule AJ, Snijders PJ, Meijer CJ, Walboomers JM (1995) Group-specific differentiation between high-and low-risk human papillomavirus genotypes by general primer-mediated PCR and two cocktails of oligonucleotide probes. J Clin Microbiol 33: 901-905
23. Jacobs MV, Walboomers JM, Snijders PJ, Voorhorst FJ, Verheijen RH, Fransen-Daalmeijer N, Meijer CJ (2000) Distribution of 37 mucosotropic HPV types in women with cytologically normal cervical smears: the age-related patterns for high-risk and low-risk types. Int J Cancer 87: 221-227
24. Jones EG, MacDonald I, Breslow L (1958) A study of epidemiologic factors in carcinoma of the uterine cervix. Am J Obstet Gynecol 76: 1-10
25. Keita N, Clifford GM, Koulibaly M, Douno K, Kabba I, Haba M, Sylla BS, van Kemenade FJ, Snijders PJ, Meijer CJ, Franceschi S (2009) HPV infection in women with and without cervical cancer in Conakry, Guinea. Br J Cancer 101(1): 202-208.
26. Khan MJ, Partridge EE, Wang SS, Schiffman M (2005) Socioeconomic status and the risk of cervical intraepithelial neoplasia grade 3 among oncogenic human papillomavirus DNA-positive women with equivocal or mildly abnormal cytology. Cancer 104: 61-70 (Pubitemid 40847753)
27. Konno R, Shin HR, Kim YT, Song YS, Sasagawa T, Inoue M, Park JS (2008) Human papillomavirus infection and cervical cancer prevention in Japan and Korea. Vaccine 26(Suppl 12): M30-M42
28. Lazcano-Ponce E, Herrero R, Munoz N, Cruz A, Shah KV, Alonso P, Hernandez P, Salmeron J, Hernandez M (2001) Epidemiology of HPV infection among Mexican women with normal cervical cytology. Int J Cancer 91: 412-420
29. Li LK, Dai M, Clifford GM, Yao WQ, Arslan A, Li N, Shi JF, Snijders PJ, Meijer CJ, Qiao YL, Franceschi S (2006) Human papillomavirus infection in Shenyang City, People?s Republic of China: a population-based study. Br J Cancer 95: 1593-1597 (Pubitemid 44863366)
30. Louie KS, de Sanjose S, Diaz M, Castellsague X, Herrero R, Meijer CJ, Shah K, Franceschi S, Munoz N, Bosch FX (2009) Early age at first sexual intercourse and early pregnancy are risk factors for cervical cancer in developing countries. Br J Cancer 100: 1191-1197
31. Matos E, Loria D, Amestoy G, Herrera L, Prince MA, Moreno J, Krunfly C, van den Brule AJ, Meijer CJ, Munoz N, Herrero R, Proyecto Concordia Collaborative Group (2003) Prevalence of human papillomavirus infection among women in Concordia, Argentina: a population-based study. Sex Transm Dis 30: 593-599
32. Molano M, Posso H, Weiderpass E, van den Brule AJ, Ronderos M, Franceschi S, Meijer CJ, Arslan A, Munoz N, the HPV Study Group (2002) Prevalence and determinants of HPV infection among Colombian women with normal cytology. Br J Cancer 87: 324-333
33. Munoz N, Bosch FX, de Sanjose S, Tafur L, Izarzugaza I, Gili M, Viladiu P, Navarro C, Martos C, Ascunce N (1992) The causal link between human papillomavirus and invasive cervical cancer: a population-based case-control study in Colombia and Spain. Int J Cancer 52: 743-749
34. Munoz N, Franceschi S, Bosetti C, Moreno V, Herrero R, Smith JS, Shah KV, Meijer CJ, Bosch FX, for the IARC Multicentric Cervical Cancer Study Group (2002) Role of parity and human papillomavirus in cervical cancer: the IARC multicentric case-control study. Lancet 359: 1093-1101
35. Murillo R, Almonte M, Pereira A, Ferrer E, Gamboa OA, Jeronimo J, Lazcano-Ponce E (2008) Cervical cancer screening programs in Latin America and the Caribbean. Vaccine 26(Suppl 11): L37-L48
36. Ngelangel C, Munoz N, Bosch FX, Limson GM, Festin MR, Deacon J, Jacobs MV, Santamaria M, Meijer CJ, Walboomers JM (1998) Causes of cervical cancer in the Philippines: a case-control study. J Natl Cancer Inst 90: 43-49 (Pubitemid 28078080)
37. Parikh S, Brennan P, Boffetta P (2003) Meta-analysis of social inequality and the risk of cervical cancer. Int J Cancer 105: 687-691
38. Plummer M (2004) Improved estimates of floating absolute risk. Stat Med 23: 93-104
39. Rolon PA, Smith JS, Munoz N, Klug SJ, Herrero R, Bosch X, Llamosas F, Meijer CJ, Walboomers JM (2000) Human papillomavirus infection and invasive cervical cancer in Paraguay. Int J Cancer 85: 486-491
40. Santos C, Munoz N, Klug S, Almonte M, Guerrero I, Alvarez M, Velarde C, Galdos O, Castillo M, Walboomers J, Meijer C, Caceres E (2001) HPV types and cofactors causing cervical cancer in Peru. Br J Cancer 85: 966-971
41. Schiffman M, Castle PE, Jeronimo J, Rodriguez AC, Wacholder S (2007) Human papillomavirus and cervical cancer. Lancet 370: 890-907
42. Shapiro S, Carrara H, Allan BR, Hoffman M, Rosenberg L, Kelly JP, Cooper DD, Williamson AL (2003) Hypothesis: the act of taking a Papanicolaou smear reduces the prevalence of human papillomavirus infection: a potential impact on the risk of cervical cancer. Cancer Causes Control 14: 953-957
43. Shin HR, Lee DH, Herrero R, Smith JS, Vaccarella S, Hong SH, Jung KY, Kim HH, Park UD, Cha HS, Park S, Touze A, Munoz N, Snijders PJ, Meijer CJ, Coursaget P, Franceschi S (2003) Prevalence of human papillomavirus infection in women in Busan, South Korea. Int J Cancer 103: 413-421 (Pubitemid 36076436)
44. Sukvirach S, Smith JS, Tunsakul S, Munoz N, Kesararat V, Opasatian O, Chichareon S, Kaenploy V, Ashley R, Meijer CJ, Snijders PJ, Coursaget P, Franceschi S, Herrero R (2003) Population-based human papillomavirus prevalence in Lampang and Songkla, Thailand. J Infect Dis 187: 1246-1256
45. Thomas JO, Herrero R, Omigbodun AA, Ojemakinde K, Ajayi IO, Fawole A, Oladepo O, Smith JS, Arslan A, Munoz N, Snijders PJ, Meijer CJ, Franceschi S (2004) Prevalence of papillomavirus infection in women in Ibadan, Nigeria: a population-based study. Br J Cancer 90: 638-645 (Pubitemid 38297204)
46. van den Brule AJ, Pol R, Fransen-Daalmeijer N, Schouls LM, Meijer CJ, Snijders PJ (2002) GP5+/6+ PCR followed by reverse line blot analysis enables rapid and high-throughput identification of human papilloma-virus genotypes. J Clin Microbiol 40: 779-787
47. Wu RF, Dai M, Qiao YL, Clifford GM, Liu ZH, Arslan A, Li N, Shi JF, Snijders PJ, Meijer CJ, Franceschi S (2007) Human papillomavirus infection in women in Shenzhen City, People?s Republic of China, a population typical of recent Chinese urbanisation. Int J Cancer 121: 1306-1311