Skip to main content
×
×
Home

Assortative mixing as a source of bias in epidemiological studies of sexually transmitted infections: the case of smoking and human papillomavirus

  • P. LEMIEUX-MELLOUKI (a1) (a2), M. DROLET (a1) (a2), J. BRISSON (a1) (a2), E. L. FRANCO (a3), M.-C. BOILY (a4), I. BAUSSANO (a5) and M. BRISSON (a1) (a2) (a4)...
Summary

For studies examining risk factors of sexually transmitted infections (STIs), confounding can stem from characteristics of partners of study subjects, and persist after adjustment for the subjects’ individual-level characteristics. Two conditions that can result in confounding by the subjects’ partners are: (C1) partner choice is assortative by the risk factor examined and, (C2) sexual activity is associated with the risk factor. The objective of this paper is to illustrate the potential impact of the assortativity bias in studies examining STI risk factors, using smoking and human papillomavirus (HPV) as an example. We developed an HPV transmission-dynamic mathematical model in which we nested a cross-sectional study assessing the smoking–HPV association. In our base case, we assumed (1) no effect of smoking on HPV, and (2) conditions C1–C2 hold for smoking (based on empirical data). The assortativity bias caused an overestimation of the odds ratio (OR) in the simulated study after perfect adjustment for the subjects’ individual-level characteristics (adjusted OR 1·51 instead of 1·00). The bias was amplified by a lower basic reproductive number (R 0), greater mixing assortativity and stronger association of smoking with sexual activity. Adjustment for characteristics of partners is needed to mitigate assortativity bias.

Copyright
Corresponding author
* Author for correspondence: Dr M. Brisson, Centre de recherche du CHU de Québec, Axe Santé des populations et pratiques optimales en santé, 1050 Chemin Sainte-Foy, Québec, Canada, G1S 4L8. (Email: Marc.Brisson@crchudequebec.ulaval.ca)
References
Hide All
1. Adimora, AA, Schoenbach, VJ. Social context, sexual networks, and racial disparities in rates of sexually transmitted infections. Journal of Infectious Diseases 2005; 191 (Suppl. 1): S115122.
2. Fine, P, Eames, K, Heymann, DL. ‘Herd immunity’: a rough guide. Clinical Infectious Diseases 2011; 52: 911916.
3. Schlecht, NF, et al. Repeatability of sexual history in longitudinal studies on HPV infection and cervical neoplasia: determinants of reporting error at follow-up interviews. Journal of Epidemiology and Biostatistics 2001; 6: 393407.
4. Furber, AS, et al. Is smoking tobacco an independent risk factor for HIV infection and progression to AIDS? A systemic review. Sexually Transmitted Infections 2007; 83: 4146.
5. Doherty, IA, et al. Determinants and consequences of sexual networks as they affect the spread of sexually transmitted infections. Journal of Infectious Diseases 2005; 191 (Suppl. 1): S4254.
6. Agrawal, A, et al. Assortative mating for cigarette smoking and for alcohol consumption in female Australian twins and their spouses. Behavior Genetics 2006; 36: 553566.
7. Laumann, EO, Youm, Y. Racial/ethnic group differences in the prevalence of sexually transmitted diseases in the United States: a network explanation. Sexually Transmitted Diseases 1999; 26: 250261.
8. Clark, AE, Etile, F. Don't give up on me baby: spousal correlation in smoking behaviour. Journal of Health Economics 2006; 25: 958978.
9. Vaccarella, S, et al. Smoking and human papillomavirus infection: pooled analysis of the International Agency for Research on Cancer HPV Prevalence Surveys. International Journal of Epidemiology 2008; 37: 536546.
10. Cavazos-Rehg, PA, et al. Number of sexual partners and associations with initiation and intensity of substance use. AIDS and Behavior 2011; 15: 869874.
11. Boily, MC, Anderson, RM. Human immunodeficiency virus transmission and the role of other sexually transmitted diseasesx. Measures of association and study design. Sexually Transmitted Diseases 1996; 23: 312332.
12. Desai, KN, et al. Simulation studies of phase III clinical trials to test the efficacy of a candidate HIV-1 vaccine. Epidemiology and Infection 1999; 123: 6588.
13. White, MT, et al. Heterogeneity in malaria exposure and vaccine response: implications for the interpretation of vaccine efficacy trials. Malaria Journal 2010; 9: 82.
14. Vickerman, P, Foss, A, Watts, C. Using modeling to explore the degree to which a microbicide's sexually transmitted infection efficacy may contribute to the HIV effectiveness measured in phase 3 microbicide trials. Journal of Acquired Immune Deficiency Syndromes 2008; 48: 460467.
15. Koopman, JS, et al. Assessing risk factors for transmission of infection. American Journal of Epidemiology 1991; 133: 11991209.
16. Wolf, R, Freedman, D. Cigarette smoking, sexually transmitted diseases, and HIV/AIDS. International Journal of Dermatology 2000; 39: 19.
17. Gillison, ML, et al. Prevalence of oral HPV infection in the United States, 2009–2010. Journal of the American Medical Association 2012; 307: 693703.
18. Beachler, DC, et al. Risk factors for oral HPV infection among a high prevalence population of HIV-positive and at-risk HIV-negative adults. Cancer Epidemiology, Biomarkers & Prevention 2012; 21: 122133.
19. Sellors, JW, et al. Prevalence and predictors of human papillomavirus infection in women in Ontario, Canada. Survey of HPV in Ontario Women (SHOW) Group. Canadian Medical Association Journal 2000; 163: 503508.
20. Granath, F, et al. Estimation of a preference matrix for women's choice of male sexual partner according to rate of partner change, using partner notification data. Mathematical Biosciences 1991; 107: 341348.
21. Aral, SO, et al. Sexual mixing patterns in the spread of gonococcal and chlamydial infections. American Journal of Public Health 1999; 89: 825833.
22. Van de Velde, N, et al. Population-level impact of the bivalent, quadrivalent, and nonavalent human papillomavirus vaccines: a model-based analysis. Journal of the National Cancer Institute 2012; 104: 17121723.
23. Johnson, HC, Elfstrom, KM, Edmunds, WJ. Inference of type-specific HPV transmissibility, progression and clearance rates: a mathematical modelling approach. PLoS ONE 2012; 7: e49614.
24. Bogaards, JA, et al. Model-based estimation of viral transmissibility and infection-induced resistance from the age-dependent prevalence of infection for 14 high-risk types of human papillomavirus. American Journal of Epidemiology 2010; 171: 817825.
25. Drolet, M, et al. The psychosocial impact of an abnormal cervical smear result. Psychooncology 2012; 21: 10711081.
26. Manhart, LE, et al. Influence of study population on the identification of risk factors for sexually transmitted diseases using a case-control design: the example of gonorrhea. American Journal of Epidemiology 2004; 160: 393402.
27. Liljeros, F, Edling, CR, Nunes Amaral, LA. Sexual networks: implications for the transmission of sexually transmitted infections. Microbes and Infection 2003; 5: 189196.
28. Ley, C, et al. Determinants of genital human papillomavirus infection in young women. Journal of the National Cancer Institute 1991; 83: 9971003.
29. Kjaer, SK, et al. Determinants for genital human papillomavirus (HPV) infection in 1000 randomly chosen young Danish women with normal Pap smear: are there different risk profiles for oncogenic and nononcogenic HPV types? Cancer Epidemiology, Biomarkers and Prevention 1997; 6: 799805.
30. Burk, RD, et al. Sexual behavior and partner characteristics are the predominant risk factors for genital human papillomavirus infection in young women. Journal of Infectious Diseases 1996; 174: 679689.
31. Franco, EL, Spence, AR. Commentary: Smoking and human papillomavirus infection: the pursuit of credibility for an epidemiologic association. International Journal of Epidemiology 2008; 37: 547548.
32. Wheeler, CM, et al. A population-based study of human papillomavirus genotype prevalence in the United States: baseline measures prior to mass human papillomavirus vaccination. International Journal of Cancer 2013; 132: 198207.
33. Chinsembu, K. Sexually transmitted infections in adolescents. Open Infectious Diseases Journal 2009; 3: 107117.
34. Johnson, AM, et al. Sexual behaviour in Britain: partnerships, practices, and HIV risk behaviours. Lancet 2001; 358: 18351842.
35. Chandra, A, et al. Sexual behavior, sexual attraction, and sexual identity in the United States: data from the 2006–2008 National Survey of Family Growth. National Health Statistics Report 20111–36.
36. Hiscock, R, et al. Socioeconomic status and smoking: a review. Annals of the New York Academy of Sciences 2012; 1248: 107123.
37. Laumann, EO GJ, Michael, RT, Michaels, S. The Social Organization of Sexuality. Chicago: The University of Chicago Press, 1994.
38. Cohen, MS, et al. Prevention of HIV-1 infection with early antiretroviral therapy. New England Journal of Medicine 2011; 365: 493505.
39. Zhang, YJ, et al. HIV transmission and related risk factors among serodiscordant couples in Liuzhou, China. Journal of Medical Virology 2015; 87: 553556.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Epidemiology & Infection
  • ISSN: 0950-2688
  • EISSN: 1469-4409
  • URL: /core/journals/epidemiology-and-infection
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Type Description Title
WORD
Supplementary materials

Lemieux-Mellouki supplementary material S1
Lemieux-Mellouki supplementary material

 Word (39 KB)
39 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 3
Total number of PDF views: 67 *
Loading metrics...

Abstract views

Total abstract views: 465 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 20th August 2018. This data will be updated every 24 hours.