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Risk Prediction Score for HIV Infection: Development and Internal Validation with Cross-Sectional Data from Men Who Have Sex with Men in China

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Abstract

Receptive anal intercourse, multiple partners, condomless sex, sexually transmitted infections (STIs), and drug/alcohol addiction are familiar factors that correlate with increased human immunodeficiency virus (HIV) risk among men who have sex with men (MSM). To improve estimation to HIV acquisition, we created a composite score using questions from routine survey of 3588 MSM in Beijing, China. The HIV prevalence was 13.4%. A risk scoring tool using penalized maximum likelihood multivariable logistic regression modeling was developed, deploying backward step-down variable selection to obtain a reduced-form model. The full penalized model included 19 sexual predictors, while the reduced-form model had 12 predictors. Both models calibrated well; bootstrap-corrected c-indices were 0.70 (full model) and 0.71 (reduced-form model). Non-Beijing residence, short-term living in Beijing, illegal drug use, multiple male sexual partners, receptive anal sex, inconsistent condom use, alcohol consumption before sex, and syphilis infection were the strongest predictors of HIV infection. Discriminating higher-risk MSM for targeted HIV prevention programming using a validated risk score could improve the efficiency of resource deployment for educational and risk reduction programs. A valid risk score can also identify higher risk persons into prevention and vaccine clinical trials, which would improve trial cost-efficiency.

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References

  1. Wu Z, Xu J, Liu E, Mao Y, Xiao Y, Sun X, et al. HIV and syphilis prevalence among men who have sex with men: a cross-sectional survey of 61 cities in China. Clin Infect Dis. 2013;57(2):298–309.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Chow EP, Lau JT, Zhuang X, Zhang X, Wang Y, Zhang L. HIV prevalence trends, risky behaviours, and governmental and community responses to the epidemic among men who have sex with men in China. Biomed Res Int. 2014;2014:607261.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Chow EP, Wilson DP, Zhang J, Jing J, Zhang L. Human immunodeficiency virus prevalence is increasing among men who have sex with men in China: findings from a review and meta-analysis. Sex Transm Dis. 2011;38(9):845–57.

    Article  PubMed  Google Scholar 

  4. Ma X, Zhang Q, He X, Sun W, Yue H, Chen S, et al. Trends in prevalence of HIV, syphilis, hepatitis C, hepatitis B, and sexual risk behavior among men who have sex with men. Results of 3 consecutive respondent-driven sampling surveys in Beijing, 2004 through 2006. J Acquir Immune Defic Syndr. 2007;45(5):581–7.

    Article  PubMed  Google Scholar 

  5. Ruan Y, Jia Y, Zhang X, Liang H, Li Q, Yang Y, et al. Incidence of HIV-1, syphilis, hepatitis B, and hepatitis C virus infections and predictors associated with retention in a 12-month follow-up study among men who have sex with men in Beijing, China. J Acquir Immune Defic Syndr. 2009;52(5):604–10.

    Article  PubMed  Google Scholar 

  6. Li S, Zhou Z, Jiang S, Liu Y, Li D, Zhang Z, et al. Incidence and risk factors of HIV and syphilis seroconversion among men who have sex with men in Beijing. Zhonghua Yu Fang Yi Xue Za Zhi. 2011;45(2):118–22 [Chinese].

    PubMed  Google Scholar 

  7. Fan S, Lu H, Ma X, Sun Y, He X, Li C, et al. Behavioral and serologic survey of men who have sex with men in Beijing, China: implication for HIV intervention. AIDS Patient Care STDS. 2012;26(3):148–55.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Li D, Li S, Liu Y, Gao Y, Yu M, Yang X, et al. HIV incidence among men who have sex with men in Beijing: a prospective cohort study. BMJ Open. 2012;2(6):e001829. https://doi.org/10.1136/bmjopen-2012-001829.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Li D, Gao Y, Yu M, Yang X, Li S, Xu J, et al. Study on the incidence of HIV and associated risk factors through a prospective cohort among men who have sex with men in Beijing, China. Zhonghua Liu Xing Bing Xue Za Zhi. 2012;33(7):663–6 [Chinese].

    PubMed  Google Scholar 

  10. Hao C, Yan H, Yang H, Huan X, Guan W, Xu X, et al. The incidence of syphilis, HIV and HCV and associated factors in a cohort of men who have sex with men in Nanjing, China. Sex Transm Infect. 2011;87(3):199–201.

    Article  PubMed  Google Scholar 

  11. Lau JT, Lin C, Hao C, Wu X, Gu J. Public health challenges of the emerging HIV epidemic among men who have sex with men in China. Public Health. 2011;125(5):260–5.

    Article  PubMed  CAS  Google Scholar 

  12. Lu H, Han Y, He X, Sun Y, Li G, Li X, et al. Alcohol use and HIV risk taking among Chinese MSM in Beijing. Drug Alcohol Depend. 2013;133(2):317–23.

    Article  PubMed  Google Scholar 

  13. Li D, Yang X, Zhang Z, Qi X, Ruan Y, Jia Y, et al. Nitrite inhalants use and HIV infection among men who have sex with men in China. Biomed Res Int. 2014;2014:365261.

    PubMed  PubMed Central  Google Scholar 

  14. Liu Y, Qian HZ, Ruan Y, Yin L, Ma J, Dahiya K, et al. Alcohol use among Chinese men who have sex with men: an epidemiological survey and meta-analysis. Biomed Res Int. 2014;2014:414381.

    PubMed  PubMed Central  Google Scholar 

  15. WHO. UNAIDS. Guidance on provider-initiated HIV testing and counselling in health facilities. Geneva: WHO Press; 2007.

    Google Scholar 

  16. WHO. UNODC. Guidance on testing and counselling for HIV in settings attended by people who inject drugs: improving access to treatment, care and prevention. Geneva: WHO Press; 2009.

    Google Scholar 

  17. World Health Organization, UNAIDS. Guidance on provider-initiated HIV testing and counselling in health facilities. Switzerland. (http://www.who.int/hiv/pub/guidelines/9789241595568_en.pdf) 2007.

  18. Wei C, Ruan S, Zhao J, Yang H, Zhu Y, Raymond HF. Which Chinese men who have sex with men miss out on HIV testing? Sex Transm Infect. 2011;87(3):225–8.

    Article  PubMed  Google Scholar 

  19. Zou H, Hu N, Xin Q, Beck J. HIV testing among men who have sex with men in China: a systematic review and meta-analysis. AIDS Behav. 2012;16(7):1717–28.

    Article  PubMed  Google Scholar 

  20. Wu Z, Sun X, Sullivan SG, Detels R. Public health. HIV testing in China. Science. 2006;312(5779):1475–6.

    Article  PubMed  CAS  Google Scholar 

  21. Fan W, Yin L, Qian HZ, Li D, Shao Y, Vermund SH, et al. HIV risk perception among HIV negative or status-unknown men who have sex with men in China. Biomed Res Int. 2014;2014:232451.

    PubMed  PubMed Central  Google Scholar 

  22. Li X, Lu H, Raymond HF, Sun Y, Jia Y, He X, et al. Untested and undiagnosed: barriers to HIV testing among men who have sex with men, Beijing, China. Sex Transm Infect. 2012;88(3):187–93.

    Article  PubMed  Google Scholar 

  23. Lau JT, Li D, Wang Z, Lai CH. Repeated HIV voluntary counseling and testing increased risk behaviors among men who have sex with men in China: a prospective cohort study. AIDS Behav. 2015;19(11):1966–77.

    Article  PubMed  Google Scholar 

  24. Lu H, Liu Y, Dahiya K, Qian HZ, Fan W, Zhang L, et al. Effectiveness of HIV risk reduction interventions among men who have sex with men in China: a systematic review and meta-analysis. PLoS ONE. 2013;8(8):e72747.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Liao W, Lau JT, Tsui HY, Gu J, Wang Z. Relationship between sexual compulsivity and sexual risk behaviors among Chinese sexually active males. Arch Sex Behav. 2015;44(3):791–8.

    Article  PubMed  CAS  Google Scholar 

  26. Schneider JA, Zhou AN, Laumann EO. A new HIV prevention network approach: sociometric peer change agent selection. Soc Sci Med. 2015;125:192–202.

    Article  PubMed  Google Scholar 

  27. McGinn TG, Guyatt GH, Wyer PC, Naylor CD, Stiell IG, Richardson WS. Users’ guides to the medical literature: XXII: how to use articles about clinical decision rules. Evidence-Based Medicine Working Group. JAMA. 2000;284(1):79–84.

    Article  PubMed  CAS  Google Scholar 

  28. Shapiro SE. Guidelines for developing and testing clinical decision rules. West J Nurs Res. 2006;28(2):244–53.

    Article  PubMed  Google Scholar 

  29. Chaudhury R, Jones HE, Wechsberg W, O’Grady KE, Tuten M, Chisolm MS. Addiction severity index composite scores as predictors for sexual-risk behaviors and drug-use behaviors in drug-using pregnant patients. Am J Drug Alcohol Abuse. 2010;36(1):25–30.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Kahle EM, Hughes JP, Lingappa JR, John-Stewart G, Celum C, Nakku-Joloba E, et al. An empiric risk scoring tool for identifying high-risk heterosexual HIV-1-serodiscordant couples for targeted HIV-1 prevention. J Acquir Immune Defic Syndr. 2013;62(3):339–47.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Powers KA, Miller WC, Pilcher CD, Mapanje C, Martinson FE, Fiscus SA, et al. Improved detection of acute HIV-1 infection in sub-Saharan Africa: development of a risk score algorithm. Aids. 2007;21(16):2237–42.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Menza TW, Hughes JP, Celum CL, Golden MR. Prediction of HIV acquisition among men who have sex with men. Sex Transm Dis. 2009;36(9):547–55.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Smith DK, Pals SL, Herbst JH, Shinde S, Carey JW. Development of a clinical screening index predictive of incident HIV infection among men who have sex with men in the United States. J Acquir Immune Defic Syndr. 2012;60(4):421–7.

    Article  PubMed  Google Scholar 

  34. Wahome E, Fegan G, Okuku HS, Mugo P, Price MA, Mwashigadi G, et al. Evaluation of an empiric risk screening score to identify acute and early HIV-1 infection among MSM in Coastal Kenya. AIDS. 2013;27(13):2163–6.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Hoenigl M, Weibel N, Mehta SR, Anderson CM, Jenks J, Green N, et al. Development and validation of the San Diego Early Test Score to predict acute and early HIV infection risk in men who have sex with men. Clin Infect Dis. 2015;61(3):468–75.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Haukoos JS, Lyons MS, Lindsell CJ, Hopkins E, Bender B, Rothman RE, et al. Derivation and validation of the Denver Human Immunodeficiency Virus (HIV) risk score for targeted HIV screening. Am J Epidemiol. 2012;175(8):838–46.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Hsieh YH, Haukoos JS, Rothman RE. Validation of an abbreviated version of the Denver HIV risk score for prediction of HIV infection in an urban ED. Am J Emerg Med. 2014;32(7):775–9.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Centers for Disease Control and Prevention. (CDC). Interim guidance: preexposure prophylaxis for the prevention of HIV infection in men who have sex with men. MMWR Morb Mortal Wkly Rep. 2011;60(3):65–8.

    Google Scholar 

  39. Buchbinder SP, Glidden DV, Liu AY, McMahan V, Guanira JV, Mayer KH, et al. HIV pre-exposure prophylaxis in men who have sex with men and transgender women: a secondary analysis of a phase 3 randomised controlled efficacy trial. Lancet Infect Dis. 2014;14(6):468–75.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Harrell FE Jr. Regression modeling strategies: with applications to linear models, logistic regression, and survival analysis. Berlin: Springer; 2001.

    Book  Google Scholar 

  41. Liu Y, Ruan Y, Strauss SM, Yin L, Liu H, Amico KR, et al. Alcohol misuse, risky sexual behaviors, and HIV or syphilis infections among Chinese men who have sex with men. Drug Alcohol Depend. 2016;168:239–46.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Liu Y, Vermund SH, Ruan Y, Liu H, Zhang C, Yin L, et al. HIV testing and sexual risks among migrant men who have sex with men: findings from a large cross-sectional study in Beijing, China. AIDS Care. 2017. https://doi.org/10.1080/09540121.2017.1381331.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Arnold DH, Gebretsadik T, Moons KG, Harrell FE, Hartert TV. Development and internal validation of a pediatric acute asthma prediction rule for hospitalization. J Allergy Clin Immunol Pract. 2015;3(2):228–35.

    Article  PubMed  Google Scholar 

  44. R Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Core Team. http://www.r-project.org/. Accessed 9 Mar 2015.

  45. Harrell FE, Jr. The rms Package for R: regression modeling strategies. Nashville, USA. http://biostat.mc.vanderbilt.edu/wiki/Main/Rrms2015. Accessed 15 Feb 2015.

  46. Harrell FE Jr, Lee KL, Mark DB. Multivariable prognostic models: issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors. Stat Med. 1996;15(4):361–87.

    Article  PubMed  Google Scholar 

  47. Steyerberg EW, Eijkemans MJ, Habbema JD. Stepwise selection in small data sets: a simulation study of bias in logistic regression analysis. J Clin Epidemiol. 1999;52(10):935–42.

    Article  PubMed  CAS  Google Scholar 

  48. Steyerberg EW, Eijkemans MJ, Harrell FE Jr, Habbema JD. Prognostic modeling with logistic regression analysis: in search of a sensible strategy in small data sets. Med Decis Making. 2001;21(1):45–56.

    Article  PubMed  CAS  Google Scholar 

  49. Justice AC, Covinsky KE, Berlin JA. Assessing the generalizability of prognostic information. Ann Intern Med. 1999;130(6):515–24.

    Article  PubMed  CAS  Google Scholar 

  50. Steyerberg EW. Clinical prediction models: a practical approach to development, validation, and updating. New York: Springer; 2009.

    Book  Google Scholar 

  51. Wu X, Hong F, Lan L, Zhang C, Feng T, Yang Y. Poor awareness of syphilis prevention and treatment knowledge among six different populations in south China. BMC Public Health. 2016;16:287.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Ruan S, Yang H, Zhu Y, Wang M, Ma Y, Zhao J, et al. Rising HIV prevalence among married and unmarried among men who have sex with men: Jinan, China. AIDS Behav. 2009;13(4):671–6.

    Article  PubMed  Google Scholar 

  53. Scott H, Vittinghoff E, Irving R, Liu A, Fields SD, Magnus M, et al. Sex pro: a personalized HIV risk assessment tool for men who have sex with men. In: Conference on Retroviruses and Opportunistic Infections (CROI); Seattle, Washington. 2015.

  54. WHO. Consolidated guidelines on the use of antiretroviral drugs for treating and preventing HIV infection: recommendations for a public health approach. Kuala Lumpur, Malaysia. June 2013.

  55. Liao M, Kang D, Tao X, Bouey JH, Aliyu MH, Qian Y, et al. Alcohol use, stigmatizing/discriminatory attitudes, and HIV high-risk sexual behaviors among men who have sex with men in China. Biomed Res Int. 2014;2014:143738.

    PubMed  PubMed Central  Google Scholar 

  56. Wasson JH, Sox HC, Neff RK, Goldman L. Clinical prediction rules. Applications and methodological standards. N Engl J Med. 1985;313(13):793–9.

    Article  PubMed  CAS  Google Scholar 

  57. Laupacis A, Sekar N, Stiell IG. Clinical prediction rules. A review and suggested modifications of methodological standards. JAMA. 1997;277(6):488–94.

    Article  PubMed  CAS  Google Scholar 

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Funding

This work was sponsored by the Grants from U.S. National Institutes of Health/National Institute of Allergy and Infectious Diseases (R01AI09462, R34AI091446, and P30AI110527).

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Author notes

  1. Lu Yin, Yuejuan Zhao and Meridith Blevins Peratikos These authors contribute equally to this work.

Authors and Affiliations

  1. Medical Research & Biometrics Center, National Center for Cardiovascular Diseases, Beijing, China

    Lu Yin

  2. Vanderbilt Institute for Global Health, Vanderbilt University Medical Center, Nashville, TN, USA

    Lu Yin, Sten H. Vermund & Han-Zhu Qian

  3. Beijing Municipal Center for Disease Control and Prevention & Centers for Preventive Medical Research, Beijing, China

    Yuejuan Zhao, Ruolei Xin & Li Zhang

  4. Departments of Biostatistics, Vanderbilt University Medical Center, Nashville, TN, USA

    Meridith Blevins Peratikos

  5. Chaoyang District Center for Disease Control and Prevention, Beijing, China

    Liang Song

  6. Xicheng District Center for Disease Control and Prevention, Beijing, China

    Xiangjun Zhang

  7. State Key Laboratory of Infectious Disease Prevention and Control, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, Chinese Center for Disease Control and Prevention, Beijing, China

    Zheya Sun, Yunan Xu, Yifei Hu, Yuhua Ruan & Yiming Shao

  8. Department of Epidemiology, College of Public Health and Health Professions, University of Florida, Gainesville, FL, USA

    Yunan Xu

  9. Department of Child, Adolescent Health and Maternal Health, School of Public Health, Capital Medical University, Beijing, China

    Yifei Hu

  10. School of Public Health, Sun Yat-sen University, Guangzhou, China

    Chun Hao

  11. Yale School of Public Health, Yale University, New Haven, CT, USA

    Sten H. Vermund & Han-Zhu Qian

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  1. Lu Yin
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Correspondence to Sten H. Vermund.

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All co-authors have no conflict of interest.

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This article does not contain any studies with animals performed by any of the authors. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

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Yin, L., Zhao, Y., Peratikos, M.B. et al. Risk Prediction Score for HIV Infection: Development and Internal Validation with Cross-Sectional Data from Men Who Have Sex with Men in China. AIDS Behav 22, 2267–2276 (2018). https://doi.org/10.1007/s10461-018-2129-y

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