Sexually transmitted infection prevalence and related risk factors among heterosexual male methamphetamine users in China

Abstract

Few studies have examined the association between methamphetamine (MA) abuse and sexually transmitted infection (STI) risk among heterosexual male MA users in China. A total of 288 heterosexual male MA users who met our inclusion criteria were recruited from nightclubs, KTVs, bars, bath centres and an STI clinic. STIs were screened among the participants, and the risk factors related to STIs were analysed by multivariate logistic regression in SPSS 11.0. Among the 288 heterosexual male MA users, 51 (17.7%) had syphilis, 36 (12.5%) had genital warts, 2 (0.7%) had genital herpes, 3 (1.0%) had HIV infection and 41 (14.2%) had urethritis. STIs were associated with the following variates: ‘MA has the function of anti-inebriation’ (OR = 2.522, 95%CI = 1.337–4.756), ‘I am addicted to MA’ (OR = 4.030, 95%CI = 2.194–7.401), ‘It occurred to me to abstain from MA’ (OR = 2.939, 95%CI = 1.246–6.934), ‘Years of MA abuse’ (OR = 2.622, 95%CI = 1.318–5.215), ‘Times of MA abuse per week’ (OR = 5.275, 95%CI = 1.988–14.002), ‘Number of persons using MA together’ (OR = 2.579, 95%CI = 1.246–5.340) and ‘Number of female sex workers as sex partners per MA abuse’ (OR = 4.004, 95%CI = 1.526–10.508). Our findings show that MA users belong to the high-risk group for STI in China. STIs, except for HIV, have spread widely among heterosexual male MA users. Thus, specific interventions must be conducted to prevent the spread of STIs in this population in China.

Keywords

Heterosexual male methamphetamines drug use risk factors sexually transmitted infection HIV

Introduction

Methamphetamine (MA) is a highly addictive stimulant that has received widespread popularity globally. MA abuse has gained public attention as a social problem since the 2000s in China. Despite such attention the population of MA users has been increasing at an alarming rate in the last ten years in China.^1,2 New types of stimulants, such as MA, methylamphetamine and ketamine, have taken the place of traditional drugs and became the most popular and hazardous drugs in the country.

The total number of drug users registered in China increased from 1.14 million in 2004 to 2.48 million in 2013, whereas the proportion of MA users increased from 9.5% to 34.2%. By 2013, the total number of MA users registered in China reached 0.85 million, with a yearly increase of 42.1%.^1,2 A survey conducted at a drug addiction treatment centre in China showed that 63% of 177 drug users were registered as MA users.³ Such explosion of MA abuse has had devastating consequences on individuals, families and society. Injury and crimes caused by MA abuse are frequently reported in mass media. Despite being a public health problem, MA abuse has not been a topic of serious concern for the government and academe in China.

Studies demonstrate that MA abuse is strongly associated with high-risk sexual behaviour, including increased number of sexual partners, decreased use of condoms, multi-partner sexual activities, engaging in sex with casual and anonymous partners and engaging in unprotected receptive and insertive anal sex with casual partners.^4–6 Many studies have focused on men who have sex with men (MSM) and indicate that MA abuse is related to the risk of contracting sexually transmitted infections (STIs), including HIV.^7–9 Studies have reported that the prevalence of syphilis is high among MA users, especially among female sex workers (FSWs) who use MA in China.^10,11

Most studies have focused on high-risk groups (such as MSM, FSWs) who used MA. However, most MA users are heterosexual males in China who may become high-risk groups after MA abuse. In addition, heterosexual male MA users may have higher risk of transmitting STIs to their families. However, the association between MA abuse and STI among heterosexual male MA users is poorly known. In this study, we sought to determine STI-related risk factors of heterosexual male MA users in China.

Methods

Participant recruitment

The study was conducted in Chengyang District, Qingdao, Shandong Province, China. A total of 288 participants were recruited from nightclubs, KTVs (a kind of entertainment venues with many private rooms equipped with top grade audio equipment where customers can sing and dance by themselves), bars, bath centres and STI clinic, accounting for 58 (20.1%), 79 (27.4%), 89 (30.9%), 35 (12.5%) and 27 (9.4%), respectively. The following inclusion criteria were used: (1) self-identified heterosexual, (2) use of MA as a major addictive drug, (3) use of MA by any means apart from injection and (4) use of MA at least once in the one month prior to screening. Any person who satisfied all of the criteria was recruited for an interview and examination at an STI clinic in the community hospital the following day. The research protocol was approved by the Ethics Committee of Shandong Provincial Hospital for Skin Diseases, and all the participants provided verbal informed consent prior to participation. Verbal informed consent was easily acceptable to participants at entertainment venues. Those who agreed to participate signed their names on paper with a statement of willing participation. The consent procedure was approved by the ethics committee.

Data collection

All the surveys and examinations were conducted at an STI clinic in the community hospital by an STI doctor and a nurse. An interviewer-administered questionnaire was used to obtain data. The following characteristics of MA users were examined: demographics, perception of MA, perception of STIs, MA abuse behaviour and high-risk sexual behaviour related to MA abuse. Each topic area was covered by several variables, and each variable was given in the form of a question that had been tested in a pilot investigation.

STI screening

STIs, including syphilis, HIV infection, genital warts and genital herpes, were diagnosed according to diagnostic criteria for STIs published by the Ministry of Health of the People’s Republic of China. Syphilis was screened for using the rapid plasma reagin test (RPR, Shanghai Rong Sheng Biostix Inc., Shanghai, China) and Treponema pallidum particle agglutination test (Shanghai Rong Sheng Biostix Inc., Shanghai, China). HIV screening was conducted using enzyme-linked immunosorbent assays (ELISA) (InTec Products, Xiamen, China). If the result of ELISA was positive, the blood sample was sent to the Qingdao Municipal Center for Disease Control and Prevention for confirmation by Western blot (HIV Blot 2.2 WBTM, Genelabs Diagnostics, Singapore). Genital warts and genital herpes were screened for clinically. The diagnosis of urethritis (both gonococcal and nongonococcal) was determined by referring suspected patients to municipal hospitals for further testing. Free treatment of STI diagnosed during screening procedure was provided on site except for HIV infection, which was referred to local centre for disease prevention and control.

Statistical analysis

All data were analysed using SPSS 11.0 (Chicago, IL). The prevalence of each STI among heterosexual male MA users was determined. STI prevalence was defined as the dependent variable, and the factors including demographics, perception of MA, perception of STIs, MA abuse behaviour and high-risk sexual behaviour related to MA abuse were defined as independent variables. Perception of STIs was measured by seven questions (Have you ever heard of syphilis? Do you know the transmission routes of syphilis? Do you know the transmission routes of HIV? Can HIV be transmitted by eating together? Do you know the risk of multiple sex partners? Can HIV infection be identified by appearance? Can STD/AIDS be prevented by using condoms?). Each correct response was awarded one point, so the participants could earn up to seven points. We first conducted bivariate analyses to compare the dependent and independent variates among heterosexual male MA users. Multivariate logistic regressions (Backward: LR) were performed to identify the factors associated with STI prevalence. OR and 95% confidence intervals are reported.

Results

Demographic information of the participants

The average age of 288 participants was 34.2 ± 1.0 (16–67) years. Of those, 203 (70.5%) were married or living with a permanent partner, 85 (29.5%) were single or divorced. A total of 262 (91.0%) were ethnic Han and 26 (9.0%) were Korean or of other ethnicities, 72 (25.0%) had high school or higher education and 216 (75.0%) had middle school or lower education, 249 (86.5%) were local permanent residents and 39 (13.5%) were from other cities in Shandong province or from other provinces, 225 (78.2%) were employed and 63 (21.9%) were unemployed.

Prevalence of STIs among heterosexual male MA users

Of the 288 heterosexual male MA users, 51 (17.7%) had syphilis, 36 (12.5%) had genital warts, two (0.7%) had genital herpes, three (1.0%) had HIV infection, 41 (14.2%) had urethritis, 115 (39.9%) had at least one kind of STI and 18 (6.3%) had at least two kinds of STIs.

Risk factors related to STIs among heterosexual male MA users

In the bivariate analysis, ‘education’ in demographic factors made a significant difference in STI prevalence (χ²= 4.637, p = 0.031); six variates in perception of MA including ‘MA has the function of anti-inebriation’ (χ²= 9.848, p = 0.002), ‘MA can relieve pain’ (χ²= 10.369, p = 0.001), ‘MA is addictive’ (χ²= 41.39, p < 0.001), ‘I am addicted to MA’ (χ²= 45.313, p < 0.001), ‘It occurred to me to abstain from MA’ (χ²= 7.8, p = 0.005) and ‘I want to have a try to abstain from MA’ (χ²= 14.72, p < 0.001) were associated with having STI. Four variates in MA abuse behaviour and four variates in high-risk sexual behaviour that were related to MA abuse were associated with having STI. Participants who had more ‘years of MA abuse’ (χ²= 22.503, p < 0.001), more ‘times of MA abuse per week’ (χ²= 28.56, p < 0.001), more ‘number of persons using MA together’ (χ²= 10.56, p = 0.001) and who ‘always use MA with heterosexual partners’ (χ²= 5.635, p = 0.018) were more likely to have STI. By contrast, participants who ‘had sex with multiple partners during MA abuse’ (χ²= 6.176, p = 0.013), ‘exchanged sex partners during MA abuse’ (χ²= 19.109, p < 0.001), had more ‘number of FSWs as sex partners per MA abuse’ (χ²= 33.979, p < 0.001) and never used a condom in sex with FSWs (χ²= 4.382, p < 0.05) were more likely to have STI (Table 1).

Table 1.

Bivariate analysis on risk factors related to STI among 288 heterosexual male MA users.

Variable	Proportion infected by STI (n/N, %)	χ²	p value
1. Demographic information
Age
<30 years old	42/104 (40.4)	0.014	0.906
≥30 years old	73/184 (39.7)
Marital status
Married or living with permanent partner	82/203 (40.4)	0.062	0.804
Single or divorced	33/85 (38.8)
Ethnicity
Han	106/262 (40.5)	0.337	0.562
Korean or others	9/26 (34.6)
Education
High school or above	21/72 (29.2)	4.637	0.031
Middle school or below	94/216 (43.5)
Residency
Permanent residents	99/249 (39.8)	0.023	0.881
Mobile population	16/39 (41.0)
Employment
Employed	93/225 (41.3)	0.844	0.358
Unemployed	22/63 (34.9)
2. Perceptions of MA
MA use is as common as smoking
Yes	111/277 (40.1)		1
No	4/11 (36.4)
MA can enhance sexuality
Yes	113/280 (40.4)	0.765	0.382
No	2/8 (25.0)
MA has the function of anti-inebriation
Yes	86/184 (46.7)	9.848	0.002
No	29/104 (27.9)
MA can relieve pain
Yes	64/127 (50.4)	10.369	0.001
No	51/161 (31.7)
MA is addictive
Yes	81/136 (59.6)	41.390	<0.001
No	34/152 (22.4)
I am addicted to MA
Yes	81/133 (60.9)	45.313	<0.001
No	34/155 (21.9)
It occurred to me to abstain from MA
Yes	24/40 (60.0)	7.8	0.005
No	91/248 (36.7)
I want to have a try to abstain from MA
Yes	27/40 (67.5)	14.72	<0.001
No	88/248 (35.5)
3. Perceptions of STIs/HIV
Score < 4	69/165 (41.8)	0.574	0.449
Score ≥ 4	46/123 (37.4)
4. MA use behaviours
Kinds of drug used
Using MA only, n(%)	111/273 (40.7)	1.161	0.281
Using MA and others, n(%)	4/15 (26.7)
Onset age of MA use
<30 years old	53/129 (41.1)	0.13	0.719
≥30 years old	62/159 (39.0)
Years of MA use
<4 years	64/205 (31.2)	22.503	<0.001
≥4 years	51/83 (61.4)
Times of MA use per week
<3 times	82/245 (33.5)	28.56	<0.001
≥3 times	33/43 (76.7)
Number of persons using MA together
<5 persons	46/149 (30.9)	10.56	0.001
≥5 persons	69/139 (49.6)
Always using MA with heterosexual partners
Yes	98/225 (43.6)	5.635	0.018
No	17/63 (27.0)
5. High-risk sexual behaviours related to MA use
Had sex with multiple partners during MA use
Yes	115/279 (41.2)	6.176	0.013
No	0/9 (0)
Exchanged sex partners during MA use
Yes	100/210 (47.6)	19.109	<0.001
No	15/78 (19.2)
Had sex with FSWs during MA use
Yes	113/277 (40.8)		0.209
No	2/11 (18.2)
Number of FSWs as sex partners per MA use
<2	79/233 (33.9)	28.821	<0.001
≥2	34/44 (77.3)
Condom use in sex with FSWs
Always or usually	20/77 (26.0)	4.382	<0.05
Never	93/200 (46.5)

FSW: female sex worker; MA: methamphetamine; STI: sexually transmitted infection.

The results of the multivariate LR analysis showed that variates including ‘MA has the function of anti-inebriation’ (OR = 2.522, 95%CI = 1.337–4.756), ‘I am addicted to MA’ (OR = 4.030, 95%CI = 2.194–7.401), ‘It occurred to me to abstain from MA’ (OR = 2.939, 95%CI = 1.246–6.934), ‘Years of MA abuse’ (OR = 2.622, 95%CI = 1.318–5.215), ‘Times of MA abuse per week’ (OR = 5.275, 95%CI = 1.988–14.002), ‘Number of persons using MA together’ (OR = 2.579, 95%CI = 1.246–5.340) and ‘Number of FSWs as sex partners per MA abuse’ (OR = 4.004, 95%CI = 1.526–10.508) were associated with having STI (Table 2).

Table 2.

Multivariate analysis on risk factors related to STI among 288 heterosexual male MA users.

Variable	OR	95%CI
MA has the function of anti-inebriation (No = 0, Yes = 1)	2.522	1.337–4.756
I am addicted to MA (No = 0, Yes = 1)	4.030	2.194–7.401
It occurred to me to abstain from MA (No = 0, Yes = 1)	2.939	1.246–6.934
Years of MA use (<4 years = 0, ≥4 years = 1)	2.622	1.318–5.215
Times of MA use per week (<3 times = 0, ≥3 times = 1)	5.275	1.988–14.002
Number of persons using MA together (<5 persons = 0, ≥5 persons = 1)	2.579	1.246–5.340
Number of FSWs as sex partners per MA use (<2 = 0,2 and above = 1)	4.004	1.526–10.508

CI: confidence interval; FSW: female sex worker; MA: methamphetamine; OR: odds ratio; STI: sexually transmitted infection.

Discussion

The findings of the current study indicate high prevalence of STIs among heterosexual male MA users. The results show that the prevalence of syphilis in this population was as high as 17.7%, which was significantly higher than that reported among MSM, FSWs and intravenous drug users (IDUs). A prospective cohort study in China showed that the incidence of syphilis among MSM was 11.1 per 100 person-years.¹² A meta-analysis study in China indicated that the pooled prevalence of syphilis infection in MSM was 11.2%.¹³ A study based on national surveillance data from 2010 to 2012 in China revealed that the prevalence of syphilis among FSWs was 6.9 to 7.2%.¹⁴ MSM, FSWs and IDUs rather than heterosexual men are traditionally considered high-risk groups for STI/HIV.¹⁵ MA use can increase the risk of STI among MSM and FSWs, as well as among heterosexual men. Heterosexual men may become a high-risk group after MA abuse. MA users have not been considered as one of the high-risk groups for STI/HIV in China until recently. Liao et al.¹¹ reported that the prevalence of syphilis among MA users in Shandong Province was 8.3%, which indicated an increasing trend in this population. Our findings indicate that MA users constitute one of the major high-risk groups for STI in China. Significant efforts should be implemented to prevent STI epidemics in this population.

In this study, we found that STI among MA users is significantly associated with the severity of MA abuse (e.g. years and frequency of MA abuse, addiction). Those who had more ‘Years of MA abuse’, who had more ‘Times of MA abuse per week’, who recognized that they are addicted to MA and those to whom it occurred that they should abstain from MA were at higher risk of contracting STI. Our study also found that STI risk among MA users was associated with having multiple sex partners (‘Number of persons using MA together’, ‘Number of FSWs as sex partners per MA abuse’), but showed no association with any demographic factors. This indicates that high-risk sexual behaviour rather than sexual orientation and gender is the key factor that is both independently associated with MA abuse and high STI prevalence among MA users. Other studies have reported that both male and female MA users engage in high-risk behaviour that could increase their risk for STI.^16,17 Therefore, it appears that any MA user using MA for unsafe sex is at risk of STI. We can assume that the mechanism increasing the risk of STI among MA users is similar to those affecting other populations such as MSM and FSWs.

The characteristics of MA may lead to susceptibility of MA users to STI by sexual transmission. On the one hand, MA can affect a host’s innate and adaptive immunity, thus increasing the chance of acquisition of diverse pathogens.¹⁸ For example, MA modulates gene expression patterns in monocyte-derived mature dendritic cells and may increase susceptibility to HIV.¹⁹ MA can enhance Cryptococcus neoformans pulmonary infection and dissemination to the brain.²⁰ MA abuse is related to tuberculosis epidemics and outbreaks as well.²¹ On the other hand, MA can intensify emotions, increase energy, elevate self-esteem and heighten sexuality, thus reducing inhibitions and impairing judgement.²² Studies on MSM indicate that MA abuse is related to increased sexual activity without regard for the consequences associated with unprotected sexual intercourse as well as increasing STI prevalence in this population.^23,24 Molitor et al.⁶ reported that MA abuse among MSM is associated with low rates of condom use, high rates of unprotected anal sex, prolonged sexual activity and having multiple or casual partners. In our previous study, we found that high-risk sexual behaviour related to MA abuse among heterosexual MA users was very common, including having sex with multiple partners and exchanging sex partners.²⁵

The major route of HIV transmission has changed from intravenous drug injection to sexual transmission in China. The proportion of reported HIV infections transmitted by intravenous drug injection in China decreased from 34.1% in 2006 to 6% in 2014, whereas the proportion of sexually-transmitted HIV infections increased from 33.1% in 2006 to 92.2% in 2014.²⁶ STI is strongly associated with the HIV epidemic. High prevalence of STI is a strong predictor of HIV among MA users. An important finding in our study is that HIV has not spread widely among heterosexual male MA users. Therefore, there is a chance to conduct specific interventions to prevent the spread of HIV in this population in China.

This study has several limitations. First, the research subjects were not randomly recruited because of difficulties in identifying or reaching the population of interest. Some participants were recruited from STI clinics, which may overestimate the STI burden among this population. Hence generalization of these results should be done very cautiously. Second, our study focused on heterosexual male MA users and no comparisons were made to females because very few heterosexual female MA users could be recruited. Third, some cases in this study were screened clinically (e.g. only symptomatic urethritis were referred to as suspected cases), which may underestimate the prevalence of STI among heterosexual male MA users since most STIs are asymptomatic. Considering these limitations, several issues need to be addressed in further studies. First, comparing the prevalence of STI and risk factors among different high-risk groups of MA users (e.g. MSM and FSWs who use MA; MA users in different age groups or venues) is necessary for designing specific interventions. Second, we suggest conducting interventions in different high-risk groups of MA users considering different ages, gender and venues (e.g. nightclubs, KTVs, bars, bath centres, STI clinics and detention centres) and comparing the effectiveness of such interventions. Third, we suggest comparing the difference in clinical manifestations and treatment effectiveness of STI between MA users and non-MA users.

In summary, our results indicate that MA users belong to the high-risk group for STI in China. STIs apart from HIV have spread widely among heterosexual male MA users. Thus, specific interventions must be carried out to prevent the spread of STI/HIV in this population in China.

Footnotes

Acknowledgements

The authors thank for the technical supports from the Chinese Foundation for Prevention of STD and AIDS. The publication’s contents are solely the responsibility of the authors and do not necessarily represent the official view of the Chinese Foundation for Prevention of STD and AIDS.

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 received no financial support for the research, authorship, and/or publication of this article.

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