Multiple Sexual Partners as a Potential Independent Risk Factor for Cervical Cancer: a Meta-analysis of Epidemiological Studies

  • Liu, Zhi-Chang (School of Public Health, Guangdong Key Laboratory of Molecular Epidemiology) ;
  • Liu, Wei-Dong (School of Public Health, Guangdong Key Laboratory of Molecular Epidemiology) ;
  • Liu, Yan-Hui (College of Pharmacy, Guangdong Pharmaceutical University) ;
  • Ye, Xiao-Hua (School of Public Health, Guangdong Key Laboratory of Molecular Epidemiology) ;
  • Chen, Si-Dong (School of Public Health, Guangdong Key Laboratory of Molecular Epidemiology)
  • Published : 2015.05.18


It's known that having multiple sexual partners is one of the risk factors of human papillomavirus (HPV) infection which is a major cause of cervical cancer. However, it is not clear whether the number of sexual partners is an independent risk factor for cervical cancer. We identified relevant studies by searching the databases of MEDLINE, PubMed and ScienceDirect published in English from January 1980 to January 2014. We analyzed those studies by combining the study-specific odds ratios (ORs) using random-effects models. Forty-one studies were included in this meta-analysis. We observed that the number of sexual partners was associated with the occurrence of non-malignant cervical disease (OR=1.82, 95%CI 1.63-2.00) and invasive cervical carcinoma (OR=1.77, 95%CI 1.50-2.05). Subgroup analyses revealed that the association remained significant after controlling for HPV infection (OR=1.52, 95%CI 1.21-1.83 for non-malignant disease; OR=1.53, 95%CI 1.30-1.76 for invasive cervical carcinoma). We found that there was a non-linear relation of the number of sexual partners with both non-malignant cervical disease and invasive cervical carcinoma. The risk of both malignant and non-malignant disease is relatively stable in women with more than 4-7 sexual partners. Furthermore, the frequency-risk of disease remained significant after controlling for HPV infection.The study suggested that h aving multiple sexual partners, with or without HPV infection, is a potential risk factor of cervical cancer.


Multiple sexual partners;cervical cancer;meta-analysis;HPV infection


  1. (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, 1108-24.
  2. (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, 1060-9.
  3. Begg CB, Mazumdar M (1994). Operating characteristics of a rank correlation test for publication bias. BIOMETRICS, 50, 1088-101.
  4. Bosch FX, Munoz N, de Sanjose S, et al (1992). Risk factors for cervical cancer in Colombia and Spain. INT J CANCER, 52, 750-8.
  5. Boyd JT, Doll R (1964). A study of the aetiology of carcinoma of the cervix uteri. Br J Cancer, 13, 419-34.
  6. Brisson J, Morin C, Fortier M, et al (1994). Risk factors for cervical intraepithelial neoplasia: differences between lowand high-grade lesions. AM J EPIDEMIOL, 140, 700-10.
  7. Brisson J, Roy M, Fortier M, et al (1988). Condyloma and intraepithelial neoplasia of the uterine cervix: a case-control study. AM J EPIDEMIOL, 128, 337-42.
  8. Buckley JD, Harris RW, Doll R, et al (1981). Case-control study of the husbands of women with dysplasia or carcinoma of the cervix uteri. LANCET, 2, 1010-5.
  9. Castellsague X, Diaz M, de Sanjose S, et al (2006). Worldwide human papillomavirus etiology of cervical adenocarcinoma and its cofactors: implications for screening and prevention. J Natl Cancer Inst, 98, 303-15.
  10. Coker AL, Rosenberg AJ, McCann MF, et al (1992). Active and passive cigarette smoke exposure and cervical intraepithelial neoplasia. Cancer Epidemiol Biomarkers Prev, 1, 349-56.
  11. Egger M, Davey SG, Schneider M, et al (1997). Bias in meta-analysis detected by a simple, graphical test. BMJ, 315, 629-34.
  12. Hernandez-Hernandez DM, Ornelas-Bernal L, Guido-Jimenez M, et al (2003). Association between high-risk human papillomavirus DNA load and precursor lesions of cervical cancer in Mexican women. GYNECOL ONCOL, 90, 310-7.
  13. Herrero R, Brinton LA, Reeves WC, et al (1990). Sexual behavior, venereal diseases, hygiene practices, and invasive cervical cancer in a high-risk population. CANCER-AM CANCER SOC, 65, 380-6.
  14. Herrington CS (1999). Do HPV-negative cervical carcinomas exist?--revisited. J PATHOL, 189, 1-3.<1::AID-PATH432>3.0.CO;2-P
  15. Higgins JP, Thompson SG (2002). Quantifying heterogeneity in a meta-analysis. STAT MED, 21, 1539-58.
  16. Higgins JP, Thompson SG, Deeks JJ, et al (2003). Measuring inconsistency in meta-analyses. BMJ, 327, 557-60.
  17. Kanjanavirojkul N, Pairojkul C, Yuenyao P, et al (2006). Risk factors and histological outcome of abnormal cervix with human papilloma infection in northeastern Thai-women. Asian Pac J Cancer Prev, 7, 567-70.
  18. Kim J, Kim BK, Lee CH, et al (2012). Human papillomavirus genotypes and cofactors causing cervical intraepithelial neoplasia and cervical cancer in Korean women. INT J GYNECOL CANCER, 22, 1570-6.
  19. Kjaer SK (1998). Risk factors for cervical neoplasia in Denmark. APMIS Suppl, 80, 1-41.
  20. Kjaer SK, van den Brule AJ, Bock JE, et al (1996). Human papillomavirus--the most significant risk determinant of cervical intraepithelial neoplasia. INT J CANCER, 65, 601-6.<601::AID-IJC8>3.0.CO;2-6
  21. Kjellberg L, Hallmans G, Ahren AM, et al (2000). Smoking, diet, pregnancy and oral contraceptive use as risk factors for cervical intra-epithelial neoplasia in relation to human papillomavirus infection. Br J Cancer, 82, 1332-8.
  22. Malamba SS, Wagner HU, Maude G, et al (1994). Risk factors for HIV-1 infection in adults in a rural Ugandan community: a case-control study. AIDS, 8, 253-7.
  23. McDougall JA, Madeleine MM, Daling JR, et al (2007). Racial and ethnic disparities in cervical cancer incidence rates in the United States, 1992-2003. Cancer Causes Control, 18, 1175-86.
  24. Millikan RC (1994). Epidemiologic evidence showing that human papillomavirus infection causes most cervical intraepithelial neoplasia. J Natl Cancer Inst, 86, 392-3.
  25. Moher D, Liberati A, Tetzlaff J, et al (2010). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. INT J SURG, 8, 336-41.
  26. Olsen AO, Dillner J, Gjoen K, et al (1996). A population-based case-control study of human papillomavirus-type-16 seropositivity and incident high-grade dysplasia of the uterine cervix. INT J CANCER, 68, 415-9.<415::AID-IJC2>3.0.CO;2-3
  27. Orsini N, Li R, Wolk A, et al (2012). Meta-analysis for linear and nonlinear dose-response relations: examples, an evaluation of approximations, and software. AM J EPIDEMIOL, 175, 66-73.
  28. Parazzini F, La Vecchia C, Negri E, et al (1988). Risk factors for adenocarcinoma of the cervix: a case-control study. Br J Cancer, 57, 201-4.
  29. Parazzini F, La Vecchia C, Negri E, et al (1992). Risk factors for cervical intraepithelial neoplasia. CANCER-AM CANCER SOC, 69, 2276-82.
  30. Rostad B, Schei B, Da CF (2003). Risk factors for cervical cancer in Mozambican women. Int J Gynaecol Obstet, 80, 63-5.
  31. Schroder KE, Carey MP, Vanable PA (2003). Methodological challenges in research on sexual risk behavior: II. Accuracy of self-reports. Ann Behav Med, 26, 104-23.
  32. Sitas F, Pacella-Norman R, Carrara H, et al (2000). The spectrum of HIV-1 related cancers in South Africa. INT J CANCER, 88, 489-92.<489::AID-IJC25>3.0.CO;2-Q
  33. Thomas DB, Qin Q, Kuypers J, et al (2001). Human papillomaviruses and cervical cancer in Bangkok. II. Risk factors for in situ and invasive squamous cell cervical carcinomas. AM J EPIDEMIOL, 153, 732-9.
  34. Vaccarella S, Franceschi S, Herrero R, et al (2006). Sexual behavior, condom use, and human papillomavirus: pooled analysis of the IARC human papillomavirus prevalence surveys. Cancer Epidemiol Biomarkers Prev, 15, 326-33.
  35. Velema JP, Ferrera A, Figueroa M, et al (2002). Burning wood in the kitchen increases the risk of cervical neoplasia in HPV-infected women in Honduras. INT J CANCER, 97, 536-41.
  36. Walboomers JM, Jacobs MV, Manos MM, et al (1999). Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J PATHOL, 189, 12-9.<12::AID-PATH431>3.0.CO;2-F
  37. Wang PD, Lin RS (1996). Risk factors for cervical intraepithelial neoplasia in Taiwan. GYNECOL ONCOL, 62, 10-8.
  38. Ye X, Fu J, Yang Y, et al (2013). Dose-risk and duration-risk relationships between aspirin and colorectal cancer: a meta-analysis of published cohort studies. PLOS ONE, 8, e57578.
  39. Yoo KY, Kang D, Koo HW, et al (1997). Risk factors associated with uterine cervical cancer in Korea: a case-control study with special reference to sexual behavior. J EPIDEMIOL, 7, 117-23.
  40. Zunzunegui MV, King MC, Coria CF, et al (1986). Male influences on cervical cancer risk. AM J EPIDEMIOL, 123, 302-7.

Cited by

  1. Arsenic Exposure and Haematological Derangement in Cervical Cancer Cases in India vol.16, pp.15, 2015,
  2. The evolution of links between cancer and sexuality: a critical review of the literature vol.10, pp.2, 2016,
  3. Prevalence, Genotype Distribution and Risk Factors for Cervical Human Papillomavirus Infection in the Grand Tunis Region, Tunisia vol.11, pp.6, 2016,