Risk behaviors for sexually transmitted infections in noninjecting drug users: A cross-sectional study

Abstract

The objective of this study was to investigate risk behaviors for sexually transmitted infections (STIs) in noninjecting drug users (NIDUs), using STI diagnosis history as an indicator. A cross-sectional study was conducted in 323 NIDUs of two facilities for alcohol and/or drug dependence treatment in the Goiás State, Central Brazil. All participants were interviewed about risk behaviors and STI history. Multivariable analysis was performed in order to identify predictors of STIs. Adjusted prevalence ratio (APR) with confidence intervals of 95% was obtained using a Poisson regression model. Prevalence of self-reported STIs in the previous 12 months was 25.4% (95% confidence interval [95% CI]: 21.0–30.4%). A multivariable model verified that age (APR: 1.01; 95% CI: 1.00–1.01), sexual contact with partners diagnosed with STIs (APR: 1.27; 95% CI: 1.12–1.45) and injecting drug users (IDUs) (APR: 1.14; 95% CI: 1.14; 95% CI: 1.01–1.31), exchange sex for money and/or drugs (APR: 1.12; 95% CI: 1.02–1.21), and a history of sexual violence (APR: 1.04; 95% CI: 1.04–1.32) were predictors of STIs. Elevated rates of STI history and risk behaviors were observed in NIDUs, supporting the vulnerability of this group for these infections. Public policies and health outreach should be intensified in this population, principally regular STI testing of individuals in treatment for drug dependence and their sexual partners.

Keywords

South America sexually transmitted infections high-risk behavior sexual behavior noninjecting drug users

Introduction

Sexually transmitted infections (STIs) represent a significant problem in public health. It is estimated that approximately 499 million new cases of curable STIs such as Chlamydia, syphilis, gonorrhea, and trichomoniasis occur, per year, worldwide.¹ Furthermore, it is estimated that 536 million and 35.3 million people live with herpes simplex type-2 and human immunodeficiency virus (HIV), respectively.^1,2 These infections are more prevalent in key populations, such as adolescents and young adults, men who have sex with men, sex workers, and injection and noninjecting drug users (NIDUs).¹

NIDUs are individuals highly vulnerable to acquiring STIs.³ Studies show that this population present elevated rates of risk behaviors, such as multiple sexual partners, inconsistent condom use, exchange of sex for money and/or drugs, and sex with high-risk sexual partners (e.g. injecting drug users [IDUs]).^3–6 Also, unfavorable socioeconomic conditions such as low income and low level of education and difficulty accessing medical services have contributed to high rates of STIs among NIDUs.⁷

Investigations have shown elevated prevalence of STIs in these populations in diverse locations, such as the United States of America (USA) (16.0% HIV infection),⁸ Luxembourg (4.8% HIV infection and 46.7% hepatitis B virus [HBV] seropositivity),⁹ and Argentina (6.3% HIV, 9.0% HBV, and 4.2% syphilis).¹⁰ In 2012 a study conducted in noninstitutionalized crack users in 41 geographic regions of Brazil estimated a prevalence of HIV of 4.97% (95% confidence interval [95% CI]: 3.75–6.56%) and high rates of risk behaviors, especially inconsistent condom use and exchange of sex for money and/or drugs, demonstrating the vulnerability of these individuals to STIs.¹¹

In Brazil, the largest country of South America, data on sexual behavior for STIs among NIDUs have been limited to those living in large coastal towns and/or in more developed regions (Southeast region).^4,12,13 Thus, information on NIDUs living in small town from the interior of the country is still scarce, and they may be different from that of NIDUs from large cities, requiring more specific interventions. Therefore, the purpose of this study was to investigate risk behaviors for STIs among NIDUs from an inner city area in Central Brazil.

Methods

Between October 2014 and March 2015, a cross-sectional study was conducted among NIDUs in two facilities for alcohol and/or drug dependence treatment in the southwest region of Goiás, Central Brazil.^14,15 These institutions offer ambulatory and inpatient treatment to alcohol and illicit drug users by way of the Brazilian National Health Care system or private insurance plans.

Those included in the study were individuals aged 18 or over, with a medical diagnosis of mental and behavioral disorders due to psychoactive substance according to the 10th revision of the International Statistical Classification of Diseases and Related Health problems (ICD-10) (verified by means of medical records),¹⁶ and who used illicit drugs in the month prior to their admission to the institution. Individuals were excluded if they reported previous history of injecting drug use and were unable to provide informed consent due to sedation or mental confusion. In Brazil, the following drugs are considered illicit: marijuana, intranasal cocaine, crack, noninjection heroin, d-lysergic acid diethylamide (LSD), and inhalants (e.g. aerosol sprays – lança-perfume).^17,18

Initially, all participants were invited to participate in the study by health care professionals in the participating institutions. Having agreed to participate, and having signed the free and informed consent form, they were interviewed face to face using a structured questionnaire regarding sociodemographic characteristics, risk behaviors, and previous history of STIs. The questionnaire included variables associated with STIs already tested and validated in other studies in vulnerable populations.^4,19–32

Variables

The dependent variable investigated was the medical diagnosis of STIs within the past year, having been self-reported, obtained by asking the question: ‘Were you diagnosed with an STI/venereal disease in the past 12 months?’ This variable has previously been used as a marker for risk behavior in vulnerable groups including use of illicit drugs.^13,33,34

The following independent variables were also analyzed: gender (male versus female), age (years), marital status (single, married, or widowed/divorced/separated), age of starting drug use (years), time using drugs (years), lived on the street (yes or no), previous psychiatric hospitalization (yes or no), binge drinking (yes or no) in the past 30 days, sexual orientation (heterosexual versus homosexual/bisexual), anal sex (yes or no), sexual violence history (yes or no), exchange of sex for money and/or drugs (yes or no), sexual relations with IDUs (yes or no), sexual relations with partners diagnosed with STIs (yes or no), and inconsistent use of condoms with steady or occasional sexual partners (yes or no). Questions regarding sexual behavior were restricted to sexual activity within the past 12 months.

Binge drinking was characterized as the consumption of five alcoholic drinks on one occasion for men and four for women.³⁵ History of sexual violence was obtained by the following question: ‘Did someone physically force you to have sexual intercourse against your will in the last year?’³² Exchange of sex for money and/or drugs was defined as a behavior to obtain directly the drug or to obtain money to buy drugs,³⁶ obtained through the question: ‘Have you received money and/or drugs in exchange for sex in the last year?’ Sexual relations with IDUs were verified by the question: ‘Have you had sex with injecting drug users in the last year?’ Sexual relations with partners diagnosed with STIs were verified by the question: ‘Have you had sex with someone with a medical diagnosis of any STI/venereal disease (syphilis, gonorrhea, Chlamydia, etc.) in the past year?’ Inconsistent condom use was defined as irregular use (sometimes or never) in sexual relations (oral, vaginal, and/or anal) with steady or occasional sexual partners.⁴

Analysis statistics

Data were analyzed using STATA, version 14.0 (StataCorp., College Station, TX, USA). Initially, descriptive data analysis was performed, with calculation of means and standard deviations (SDs) for quantitative variables and simple frequencies for qualitative variables. Prevalence of reports of STIs was estimated with a 95% CI. To estimate the factors associated with reports of STIs, bivariate analysis was performed between the outcome variable and other variables investigated. Chi square test³⁷ or Student’s t-test was used to compare the differences between proportions of those reported a previous STI to those who did not. Following that, the variables with p < 0.10 were subjected to a Poisson regression model with a robust variance for obtaining the adjusted prevalence ratio (APR) and 95% CI,^38,39 and values with p < 0.05 were considered statistically significant.

Ethical aspects

This study was approved by the Committee on Ethics in Research at the Federal University of Goiás, protocol number 926.819/2014. The consent of all participants was obtained.

Results

During the study period, 380 users were invited to participate, 25 refused, 20 were found in an apparent state of sedation and/or agitation before the interview, and 22 had injected illicit drugs during their lifetime, according to self-reports. Thus, the study included 323 NIDUs with an average age of 32.4 years (SD ± 11.3 years). The majority of participants were male (83.0%) and single (72.2%). Individuals reported crack use (75.9%), intranasal cocaine powder (47.2%), cannabis (51.5%), inhalants (26.5%), LSD (13.0%), ecstasy (12.7%), and noninjecting heroin (3.7%). The average age for beginning drug use and time using drugs was 16.9 years (SD ± 6.4 years) and 12.4 years (SD ± 8.7 years), respectively.

The prevalence of STIs history was 25.4% (95% CI: 21.0–30.4%). Of the individuals who reported some STIs (n = 82), 58.5% reported gonorrhea, 12.2% human papillomavirus/condyloma acuminatum, 9.8% reported syphilis, 6.1% herpes, 6.1% HIV infection, 3.7% chancroid, and 3.6% other STIs. Of the individuals diagnosed with some STIs, 98.7% reported having received medical treatment.

According to Table 1, bivariate analysis demonstrated that the rate of infections increased with increasing age and with time of drug use (p < 0.01). Additionally, prevalence of STIs was higher among individuals who reported practicing anal sex, exchange sex for money and/or drugs for sex, sexual relations with IDUs and/or with sexual relations with partners diagnosed with STIs, users who reported sexual violence (p < 0.05). These variables and binge drinking (p = 0.078), rehospitalization (p = 0.056), and inconsistent use of condoms with occasional partners (p = 0.059) were included in a Poisson regression model.

Table 1.

Bivariate analysis of factors associated with self report of sexually transmitted infections in noninjecting drug users, Central Brazil, 2014–2015.

Variables	Totala (N = 323)		STIs				p
Variables	n	%	Yes	%	No	%	p
Quantitative
Age (years; mean; SD)	32.4 (11.3)		37.6 (10.7)		30.6 (10.1)		<0.001
Age of starting drug use (years; Mean; SD)	16.9 (6.4)		17.9 (7.5)		16.6 (6.0)		0.163
Time using drugs (years; Mean; SD)	12.4 (8.7)		16.2 (9.5)		11.1 (8.0)		<0.001
Number of sexual partners (Mean; SD)	6.3 (13.9)		7.4 (10.7)		5.9 (14.9)		0.502
QualitativeGender
Male	268	83.0	71	26.4	197	73.5	0.314
Female	55	17.0	11	20.0	44	80.0
Marital status
Single	233	72.1	57	24.5	176	75.5	0.473
Married	51	15.8	12	23.5	39	76.5
Widowed/divorced/separated	39	12.1	13	33.3	26	66.7
Lived on the streetsb
No	265	82.0	63	23.8	202	76.2	0.154
Yes	58	18.0	19	32.8	39	67.2
Previous psychiatric hospitalization
No	239	74.0	54	22.6	185	77.4	0.052
Yes	84	26.0	28	33.3	56	66.7
Binge drinking
No	37	11.5	5	13.5	32	86.5	0.078
Yes	286	88.5	77	26.9	209	73.1
Anal sexb
No	124	38.4	19	15.3	105	84.7	0.001
Yes	199	61.6	63	31.7	136	68.3
Sexual orientation
Heterosexual	286	88.5	69	24.1	217	75.9	0.148
Homosexual or bisexual	37	11.5	13	35.1	24	64.9
Inconsistent condom use with steady partnerb
No	15	7.9	3	20.0	12	80.0	1.000
Yes	174	92.1	40	23.0	134	77.0
Inconsistent condom use with casual partnerb
No	77	36.0	16	20.8	61	79.2	0.059
Yes	137	64.0	46	66.4	46	33.6
Used a condom in their last sexual encounter
No	138	42.7	39	21.0	109	79.0	0.119
Yes	185	57.3	53	28.6	132	79.0
Sexual relations with IDUsb
No	299	92.6	71	23.7	228	76.3	0.017
Yes	24	7.4	11	45.8	13	54.2
Exchange of sex for money and/or drugsb
No	200	62.7	41	20.5	159	79.5	0.014
Yes	119	37.3	39	32.8	80	67.2
Sexual relations with partners diagnosed with STIsb
No	287	90.8	61	21.3	226	78.7	<0.001
Yes	29	9.2	21	72.2	8	27.4
Sexual violenceb
No	284	88.2	66	23.2	218	76.8	<0.001
Yes	38	11.8	16	42.1	22	57.9

IDU: injecting drug users; SD: standard deviation; STIs: sexually transmitted infections.

^aNumber of valid responses.

^bIn the last 12 months.

The results of the Poisson regression analysis are presented in Table 2. The final model was adjusted for age, time using drugs, binge drinking, anal sex, inconsistent condom use with occasional partners, sexual relations with IDUs, exchange of sex for money and/or drugs, sexual relations with partners diagnosed with STIs, and sexual violence history. According to the model, each year of life the prevalence of STIs increased by 1% (APR: 1.01; p = 0.003). The following risk factors were associated with STIs: sexual contact with partners diagnosed with STIs (APR: 1.27; p<0.001) and with IDUs (APR: 1.14; p = 0.039), exchange of sex for money and/or drugs (APR: 1.12; p = 0.002), and sexual violence history (APR: 1.24; p = 0.007).

Table 2.

Factors associated with self report of sexually transmitted infections in noninjecting drug users, Central Brazil, 2014–2015.

Variables	Adjusted PR (95% CI)a	pb
Age (years)	1.01 (1.00–1.01)	0.003
Sexual contact with IDUs	1.14 (1.01–1.31)	0.039
Sexual violence	1.04 (1.04–1.32)	0.007
Sexual contact with partners diagnosed with STIs	1.27 (1.12–1.45)	<0.001
Exchange of sex for money and/or drugs	1.12 (1.04–1.21)	0.002

CI: confidence interval; IDUs: injecting drug users; PR: prevalence ratio; STIs: sexually transmitted infections.

^aAdjusted for age, time using drugs, binge drinking, anal sex, inconsistent condom use with casual partners, sexual contact with IDUs, exchange of sex for money and/or drugs, sexual contact with STI carriers and sexual violence.

^bWald Chi-Square Test.

Discussion

This study investigated risk behaviors for STIs in NIDUs in treatment for chemical dependency in Central Brazil, using as an indicator a reported history of STIs in the last 12 months. Multiple factors were verified that support the vulnerability of these individuals to these infections, such as exchange of sex for money and/or drugs, sexual relations with partners diagnosed with STIs and IDUs, and sexual violence history.

Use of illicit drugs increased with the rate of sexual activity, diminishing the perception of risk and capacity for negotiating the use of a condom,^40–42 leading individuals to adopt high-risk behaviors, which in turn are responsible for a large part of the global burden of STIs in NIDUs. In this study the prevalence of reporting STIs was 25.3%. This rate was similar to that estimated globally for individuals in treatment for drug use dependence in Brazil (28.4%),⁴³ NIDUs from the Southwest Region (22.1%),⁴ and institutionalized crack users in Midwestern Region (26.2%).¹³

In the study, STIs history was independently associated with age, which is supported by other investigations conducted in illicit drug users.^13,43 Prevalence increased with age, suggesting a cumulative risk of STIs acquisition and multiple chances for exposure to these infections throughout life.^13,43,44

The results found in the study suggest an elevated risk of dissemination of STIs in social and sexual networks of investigated NIDUs. Association between STIs and sexual relations with sexual relations with partners diagnosed with STIs and IDUs was observed. In the USA, Khan et al.,⁴⁵ found an increased prevalence of sexual relations with partners diagnosed with STIs, within the last year in crack/noninjecting cocaine users when compared with other participants who did not use those drugs. In Goiânia (Central Brazil), Guimarães et al.¹³ also found association between a STI history and sexual contact with persons living with HIV/AIDS among institutionalized crack users. In Argentina, Rossi et al.¹⁰ found an increased risk of HBV and hepatitis C virus infection in individuals with a history of sexual contact with IDUs.

This study found an elevated prevalence of exchange of sex for money and/or drugs in investigated individuals (37.3%), this being a variable associated with STIs history. This high rate is consistent with other investigations conducted among NIDUs.^7,13 The craving, defined as an uncontrollable urge to use drugs, removes or diminishes the perception of risk of users, leading them to behaviors such as using sex to obtain drugs and/or money.⁴¹ Furthermore, with the objective of earning more, NIDUs that practice sex work could submit to unprotected sex, increasing the potential of risk to acquire STIs.³ In Latin America and the Caribbean, cocaine and crack users represent a population that is particularly affected by the HIV epidemic, through higher rates of involvement in the commercial sex trade to sustain their drug habits.⁴¹

Sexual violence history was associated with reporting STIs. Sexual violence is associated with epidemics of HIV around the world, especially in women.⁴⁶ Also individuals with a sexual violence history demonstrate patterns of increased alcohol consumption and high rates of risk behaviors (e.g. inconsistent use of condoms and anal sex), which in turn increase the chances of unsafe sexual practices.^46,47

An elevated prevalence of binge drinking (88.5%) among study participants was found. Although there was no observed statistical association between this variable and reporting of STIs, alcohol consumption has a direct impact on increasing the global burden of these infections in several key populations, including users of illicit drugs.⁴⁸ The use of these substances promotes a reduction in cognitive capacity, reducing risk perception and inhibitions, and can lead an individual to engage in multiple sexual risk behaviors, especially sex work and inconsistent use of condoms.⁴⁹

The results of the study should be considered in the context of its limitations. The nature of cross-sectional studies does not permit the establishment of causal relationships between a history of STIs and the other investigated variables. The study considered only individuals in treatment and as a result could not be used to generalize all NIDUs in other locations of Brazil. Behavioral data and STI data were self-reported, susceptible to memory and response bias. Also many STIs are asymptomatic, which can cause underestimation of results.

Public policy and health-related actions should be intensified for this population, including health education, counseling on safe sex, as well as regular STI testing of individuals in treatment for substance-related disorders and their sexual partners. In addition, future research should be conducted in NIDUs in Brazil in all geographic regions, investigating the prevalence and potential determinants in this population, in order to verify the real dimension of STIs in this population. Future studies may improve current research by assessing longitudinally risk factors for STIs in NIDUs.

Conclusion

In conclusion, elevated rates of history of STIs and risk behaviors were observed in NIDUs confirming the vulnerability of this group to infections transmitted by sexual contact. These individuals are at risk of acquiring an STI principally through their social and sexual networks (partners diagnosed with STIs and IDUs) and by engagement in sex work.

Footnotes

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by Fundação de Amparo à Pesquisa do Estado de Goiás (Brazil), process no. 201200661660420.

References

World Health Organization. Sexually Transmitted Infections (STIs): the importance of a renewed commitment to STI prevention and control in achieving global sexual and reproductive health, http://apps.who.int/iris/bitstream/10665/82207/1/WHO_RHR_13.02_eng.pdf (2013, accessed 27 October 2017).

Joint United Nations Programme on HIV/AIDS. Global report: UNAIDS report on the global AIDS epidemic 2013, http://www.unaids.org/sites/default/files/media_asset/UNAIDS_Global_Report_2013_en_1.pdf (2015, accessed 27 October 2017).

Strathdee

Stockman

Epidemiology of HIV among injecting and non-injecting drug users: current trends and implications for interventions. Curr HIV/AIDS Rep 2010; 7: 99–106.

Diehl

Vieira

Rassool

et al . Sexual risk behaviors in non-injecting substance-dependent Brazilian patients. Adicciones 2014; 26: 208–220.

Jarlais

McKnight

Arasteh

et al . A perfect storm: crack cocaine, HSV-2, and HIV among non-injecting drug users in New York City. Subst Use Misuse 2014; 49: 783–792.

Mackesy-Amiti

Boodram

Williams

et al . Sexual risk behavior associated with transition to injection among young non-injecting heroin users. AIDS Behav 2013; 17: 2459–2466.

Nunes

Andrade

Galvão-Castro

et al . Assessing risk behaviors and prevalence of sexually transmitted and blood-borne infections among female crack cocaine users in Salvador–Bahia, Brazil. Braz J Infect Dis 2007; 11: 561–566.

Jarlais

Arasteh

McKnight

et al . Gender and age patterns in HSV-2 and HIV infection among non-injecting drug users in New York City. Sex Transm Dis 2010; 37: 637–643.

Removille

Origer

Couffignal

et al . A hepatitis A, B, C and HIV prevalence and risk factor study in ever injecting and non-injecting drug users in Luxembourg associated with HAV and HBV immunisations. BMC Public Health 2011; 11: 351.

10.

Rossi

Radulich

Muzzio

et al . Multiple infections and associated risk factors among non-injecting cocaine users in Argentina. Cad Saúde Pública 2008; 24: 965–974.

11.

Bastos

Bertoni

Pesquisa Nacional sobre o uso de crack: quem são os usuários de crack e/ou similares do Brasil? quantos são nas capitais brasileiras? Rio de Janeiro: ICICT/Fiocruz, 2014.

12.

Bertoni

Burnett

Cruz

et al . Exploring sex differences in drug use, health and service use characteristics among young urban crack users in Brazil. Int J Equity Health 2014; 13: 70.

13.

Guimarães

Silva

LNd

França

DDdS

et al . Risk behaviors for sexually transmitted diseases among crack users. Rev Lat Am Enfermagem 2015; 23: 628–634.

14.

Guimarães

Rodovalho

Fernandes

et al . Transactional sex among noninjecting illicit drug users: implications for HIV transmission. Sci World J 2016; 2016: 4690628.

15.

Guimarães

Lucchese

Felipe

RLd

et al . Inconsistent use of condoms in non-injecting illicit drug users. Braz J Infect Dis 2015; 20: 220–221.

16.

World Health Organization. ICD-10, international statistical classification of diseases and related health problems. 10th ed. Geneva: WHO, 2010.

17.

Gigliotti

Ribeiro

Aguilera

et al . Paradigms of public policies for licit and illicit drugs in Brazil. Subst Abus 2014; 35: 292–297.

18.

Abdalla

Madruga

Ribeiro

et al . Prevalence of cocaine use in Brazil: data from the II Brazilian national alcohol and drugs survey (BNADS). Addict Behav 2014; 39: 297–301.

19.

Deiss

Lozada

Burgos

et al . HIV prevalence and sexual risk behaviour among non-injection drug users in Tijuana, Mexico. Glob Public Health 2012; 7: 175–183.

20.

Ropelewski

Hulbert

Latimer

WW.

Factors related to past HIV testing among South African non-injection drug users. AIDS Care 2011; 23: 1519–1526.

21.

White

Rudolph

Jones

et al . Social and individual risk determinants of HIV testing practices among noninjection drug users at high risk for HIV/AIDS. AIDS Care 2013; 25: 230–238.

22.

Melo

APS

Machado

Guimarães

MDC.

HIV testing in psychiatric patients in Brazil. J Acquir Immune Defic Syndr 2011; 57: S157–S163.

23.

Agha

Factors associated with HIV testing and condom use in Mozambique: implications for programs. Reprod Health 2012; 9: 20.

24.

Saw

Yasuoka

Saw

et al . What are the factors associated with HIV testing among male injecting and non-injecting drug users in Lashio, Myanmar. BMJ Open 2013; 3: e002747.

25.

Park

Papworth

Billon

et al . Correlates of prior HIV testing among men who have sex with men in Cameroon: a cross-sectional analysis. BMC Public Health 2014; 14: 1220.

26.

Saw

Poudel

Kham

NPE

et al . Assessment of HIV testing among young methamphetamine users in Muse, Northern Shan State, Myanmar. BMC Public Health 2014; 14: 735.

27.

Ding

Zhu

et al . Sexual risk behaviors among club drug users in Shanghai, China: prevalence and correlates. AIDS Behav 2013; 17: 2439–2449.

28.

Straub

Arrington-Sanders

Harris

et al . Correlates of HIV testing history among urban youth recruited through venue-based testing in 15 US cities. Sex Transm Dis 2011; 38: 691–696.

29.

Cruz

Bertoni

Bastos

et al . Comparing key characteristics of young adult crack users in and out-of-treatment in Rio de Janeiro, Brazil. Subst Abuse Treat Prev Policy 2014; 9: 2.

30.

Calsyn

Cousins

Hatch-Maillette

et al . Sex under the influence of drugs or alcohol: common for men in substance abuse treatment and associated with high risk sexual behavior. Am J Addict 2010; 19: 119–127.

31.

Dunn

Laranjeira

RR.

HIV-risk behaviour among non-heroin using cocaine injectors and non-injectors in São Paulo, Brazil. AIDS Care 2000; 12: 471–481.

32.

Barros

Schraiber

França-Junior

Association between intimate partner violence against women and HIV infection. Rev Saúde Pública 2011; 45: 365–372.

33.

Teles

Matos

MAd

Caetano

KAA

et al . Comportamentos de risco para doenças sexualmente transmissíveis em caminhoneiros no Brasil. Rev Panam Salud Publica 2008; 24: 25–29.

34.

Guimarães

Lucchese

Felipe

RLd

et al . Factors associated with the report of sexually transmitted infections in drug users, Central Brazil: a cross-sectional study. Sex Transm Infect 2015; 91: 79.

35.

Dawson DA. Defining risk drinking. Alcohol Res Health 2011; 34: 144–156.

36.

Baral

Beyrer

Muessig

et al . Burden of HIV among female sex workers in low-income and middle-income countries: a systematic review and meta-analysis. Lancet Infect Dis 2012; 12: 538–549.

37.

McHugh

ML.

The Chi-square test of independence. Biochem Med 2013; 23: 143–149.

38.

Coutinho

LMS

Scazufca

Menezes

PR.

Methods for estimating prevalence ratios in crosssectional studies. Rev Saúde Pública 2008; 42: 1–6.

39.

Barros

Hirakata

VN.

Alternatives for logistic regression in cross-sectional studies: an empirical comparison of models that directly estimate the prevalence ratio. BMC Med Res Methodol 2003; 3: 21.

40.

El-Bassel

Shaw

Dasgupta

et al . Drug use as a driver of HIV risks: re-emerging and emerging issues. Curr Opin HIV AIDS 2014; 9: 150–155.

41.

García

Bayer

Cárcamo

The changing face of HIV in Latin America and the Caribbean. Curr HIV/AIDS Rep 2014; 11: 146–157.

42.

Strathdee

West

Reed

et al . Substance use and HIV among female sex workers and female prisoners: risk environments and implications for prevention, treatment, and policies. J Acquir Immune Defic Syndr 2015; 69: S110–S117.

43.

Dutra

Campos

Guimarães

MD.

Sexually transmitted diseases among psychiatric patients in Brazil. Braz

J Infect Dis 2014; 18: 13–20.

44.

Camoni

Regine

Salfa

et al . Continued high prevalence of HIV, HBV and HCV among injecting and noninjecting drug users in Italy. Ann Ist Super Sanita 2010; 46: 59–65.

45.

Khan

Berger

Hemberg

et al . Non-injection and injection drug use and STI/HIV risk in the United States: the degree to which sexual risk behaviors versus sex with an STI-infected partner account for infection transmission among drug users. AIDS Behav 2013; 17: 1183–1194.

46.

Campbell

Lucea

Stockman

et al . Forced sex and HIV risk in violent relationships. Am J Reprod Immunol 2013; 69: 41–44.

47.

Pitpitan

Kalichman

Eaton

et al . Gender-based violence and HIV sexual risk behavior: alcohol use and mental health problems as mediators among women in drinking venues, Cape Town. Soc Sci Med 2012; 75: 1417–1425.

48.

Kalichman

Simbayi

Kaufman

et al . Alcohol use and sexual risks for HIV/AIDS in sub-Saharan Africa: systematic review of empirical findings. Prev Sci 2007; 8: 141–151.

49.

Vagenas

Lama

Ludford

et al . A systematic review of alcohol use and sexual risk-taking in Latin America. Rev Panam Salud Publica 2013; 34: 267–274.