Syphilis infection among people who use and inject drugs in Cambodia: a cross-sectional study using the respondent-driven sampling method

Abstract

This cross-sectional study explored the prevalence and correlates of syphilis infection among people who use and inject drugs (PWUD/PWID) in Cambodia. Data were collected in 2017 from 1,677 PWUD/PWID living in the capital city of Phnom Penh and 11 other major provinces using the respondent-driven sampling method. The SD Bioline HIV/Syphilis Duo test was used to determine human immunodeficiency virus (HIV) and current or past syphilis infection. A multivariable logistic regression analysis was conducted to identify risk factors associated with current or past syphilis infection. The prevalence of current or past syphilis infection was 3.8% (95% confidence interval = 2.4–4.6). After adjustment, current or past syphilis infection remained positively associated with being female, living on the streets, having an average monthly income of US$100–299, having transactional sex in the past three months, and having been to a rehabilitation centre in the past 12 months. Current or past syphilis infection was negatively associated with having attained at least high school level of formal education. The findings indicate vulnerability to syphilis infection among PWUD/PWID in Cambodia, particularly among subpopulations who are more marginalized. Syphilis prevention and control programmes should be systematically integrated into HIV and sexually transmitted infection policy and services in the country.

Keywords

Sexually transmitted infection drug use HIV key population sexual behaviour Asia

Introduction

Syphilis is one of the four most common and curable sexually transmitted infections (STIs) and a cause of significant health burden globally.^1,2 Current incidence data suggest that 5.6 million people aged 15–49 years acquire syphilis annually.² Prevalence studies suggest that 0.5–1.1% of the global population have syphilis at any one time,^1,3 and on average, 11.1% have it over their lifetime.⁴ In recent years, syphilis has drawn significant international interest due to its impact on morbidity and mortality, particularly among women and children.⁵ Among neonates, congenital syphilis is a leading cause of prematurity, low birth weight, and stillbirths.^6,7 Consequently, the elimination of mother-to-child transmission of syphilis is a current global priority.⁵

The public health importance of syphilis is closely linked to the HIV epidemic. Identifying and treatment of people at risk of syphilis is, therefore, an important element of HIV combination prevention. The World Health Organization (WHO) recommends syphilis testing for sexually active members of HIV key populations at least once a year.^8,9 Despite the needs, data regarding the magnitude of syphilis among people who use and inject drugs (PWUD/PWID) are limited globally.⁸ Few studies suggest that PWUD/PWID in countries such as Afghanistan, Bangladesh, China, Iran, and the United States are frequently at risk of syphilis infection.^10–13 As part of a global response, expert consensus on the importance of syphilis among PWUD/PWID has recently been published.⁴

In Cambodia, although PWUD/PWID are a priority population in HIV programmes, prevention of syphilis among this population is not a current focus. PWUD/PWID are defined as persons who have used any types of illicit drugs, as specified in the Cambodian Law on Control of Drugs, in the past 12 months. In 2017, it was estimated that there were 26,500 PWUD/PWID across the country,¹⁴ and HIV prevalence among PWUD and PWID was 5.7% and 15.2%, respectively.^14,15 Syndromic management, an approach to identify and treat a syndrome caused by an STI, has been implemented with a focus on syphilis in other HIV key populations, including female entertainment workers, men who have sex with men, and transgender women.

The cornerstone of public health services to PWUD/PWID is community-based harm reduction programmes, through which PWUD/PWID are reached with HIV and syphilis testing, methadone maintenance therapy, education, and needle exchange programmes.¹⁶ However, targeted screening for syphilis in PWUD/PWID is not emphasized in the national harm reduction strategies and conceptual framework,¹⁷ despite the fact that risky sexual behaviours can feature alongside drug use to expose PWUD/PWID to HIV, syphilis, and other STIs. This gap may be related to the limited available data on the magnitude of syphilis infection in this population. This study was therefore conducted with a primary objective of generating relevant data regarding the prevalence and correlates of syphilis infection among PWUD/PWID in Cambodia, in order to inform future programmes and interventions.

Methods

Study design and settings

Data used for this study were collected from June to December 2017 as part of a large-scale cross-sectional survey conducted in the capital city of Phnom Penh and 11 other major provinces. These study sites were selected based on (1) a feasibility assessment conducted by the study team before finalizing the research protocol and data collection plan and (2) HIV-related data showing that these sites contained the 21 operational districts with high burdens of HIV and drug use.

Participant eligibility and recruitment

To be included in the study, an individual must: (1) be at least 18 years old; (2) have a valid study coupon; (3) have not participated in this survey earlier; (4) meet criteria according to the definition of PWUD and PWID; and (5) be able and willing to provide written informed consent to participate in the study.

The respondent-driven sampling (RDS) method was used to recruit participants and the Strengthening the Reporting of Observational Studies in Epidemiology for RDS studies statement was followed. The RDS was conducted in five steps. First, four eligible seeds were identified in each site, and informed consent was obtained from them. Second, each seed was given a personal identification number and enrolled as a participant. Third, each seed received three coupons and was asked to refer three additional PWUD/PWID. Each successful referral was rewarded with US$2, and each seed was expected to extend up to six ‘recruitment waves’. If the initial seeds did not recruit participants or if enrolment has been halted because all recruitment chains had ‘dried up’ (i.e. stopped recruiting), additional seeds would be selected based on the above criteria. Finally, recruited individuals were provided with the same opportunity as seeds to recruit other participants.

Sample size calculation

Sample size calculation was primarily based on estimated population size in the country (13,000 PWUD and 1,300 PWID)¹⁸ and the prevalence of HIV, the main objective of the main survey. The study null hypothesis was that the prevalence of HIV among PWUD and PWID would remain unchanged since the 2012 survey.¹⁸ We used the HIV prevalence of 3.5% for PWUD and 24.8% for PWID, a margin error of 1.5%, a confidence interval (CI) of 95%, a response rate of 90%, and a design effect of 1.5 to estimate the sample size. Given these parameters, the minimum sample size of PWUD and PWID required for the survey was 1,390 and 290, respectively. The sample recruitment was stratified by study sites to ensure that at least 15% of the estimated PWUD/PWID in each site would be recruited. Data collection was conducted in 21 locations (six locations in Phnom Penh and 15 locations in the remaining provinces). The number of the selected locations was determined based on the required sample size in each study site.

Data collection tool and procedures

Interviewers and field supervisors received a three-day training that covered research ethics, interview techniques, rehearsal of survey administration, and biological data collection. The study protocol and tools were developed collaboratively through consultative meetings with representatives of relevant national programmes, development partners, non-governmental organizations, community-based organizations, and PWUD/PWID communities. A structured questionnaire was developed using standardized and validated tools adapted from previous studies among HIV key populations in Cambodia.^19,20 It was initially developed in English, translated into Khmer, and then back-translated into English. A pilot testing of the protocol and tools was conducted with 20 PWUD/PWID in Phnom Penh, who were later excluded from the main study.

The survey questionnaire collected diverse information related to (1) socio-demographic characteristics (study site, age, gender, education, employment status, type of employment, income); (2) types of illicit drugs and drug use experiences in the past three months; (3) sexual risk behaviours with different types of partners in the past three months; and (4) access to HIV and harm reduction programmes in the past 12 months.

HIV and syphilis screening was performed using SD Bioline HIV/Syphilis Duo test (Standard Diagnostics, Inc. Yongin, Gyeonggi, South Korea), which uses immunochromatographic detection of antibodies to all isotypes (IgG, IgM, and IgA) specific to HIV-1/2 and/or Treponema pallidum. According to a prequalification performance evaluation conducted by WHO, the final sensitivity and specificity for HIV antibodies was 100% (95% CI 98.2–100%) and 99.5% (95% CI 97.2–100%), respectively, compared to the reference assays.²¹ For antibodies to T. pallidum, the final sensitivity and specificity was 87.0% (95% CI 81.5–91.3%) and 99.5% (95% CI 97.2–100%), respectively, compared to the reference assays.²¹ An HIV reactive result from the SD Bioline HIV/Syphilis Duo test was confirmed on-site using the HIV 1/2 STAT-PAK® Assay (Chembio, Medford, New York, United States). A positive T. pallidum test result indicated that a person had a current or past syphilis infection.

Statistical analyses

The prevalence of current or past syphilis infection was calculated by dividing the total number of participants with a positive T. pallidum test result by the total number of participants tested. We used weighting compensation techniques to account for the complex survey design and estimated the national-level prevalence (with standard error values) for each of the measures. Chi square test (or Fisher’s exact test for an expected cell value of <5) was used to compare characteristics and behavioural variables of participants who had a positive T. pallidum test result to those of the participants who did not. Age, level of education, and income were transformed into categorical variables. A weighted multivariable logistic regression model was constructed to identify independent factors associated with current or past syphilis infection. Variables with a significance level of p < 0.25 in the bivariate analyses were simultaneously included in the model. Age, gender, level of education, and income were included in the model regardless of the significance level. Backward stepwise selection method was used to eliminate variables with the highest p-value one by one from the model. We obtained an adjusted odds ratio (AOR) for each comparison and presented it with a CI and p-value. Stata (StataCorp LP, version 14.1) was used for the data analyses.

Ethical statement

The National Ethics Committee for Health Research (NECHR) of the Ministry of Health, Cambodia (No. 420 NECHR) approved this study. We protected the confidentiality and privacy of the participants by removing personal identifiers from the study documents and conducting the data collection in private places. We informed the participants about the nature of the study, and the risks and benefits they may expect from their participation in the study. We obtained written informed consent from each participant. Each participant received a gift in kind worth approximately US$5 to compensate for their time.

Results

Socio-demographic characteristics

After excluding 62 participants who did not meet the eligibility criteria and nine with missing T. pallidum test results, this study included 1,677 participants (1,367 PWUD/310 PWID). The mean age of the participants was 28.7 years (SD = 7.9). The prevalence of current or past syphilis infection in the total study population was 3.8%. The prevalence was 3.4% in PWUD compared to 5.2% in PWID. As shown in Table 1, the majority of the participants (88.6%) lived in urban communities, and 37.2% were female. The majority of the participants (77.1%) were younger than 35 years old, and almost half (46.0%) were never married. More than half (53.5%) had only primary education or lower, and 10.2% lived on the streets. About one-third (35.6%) were farmer or labourer, and 77.3% reported an average monthly income in the past six months of <US$200. Compared to the prevalence in their respective reference group, the prevalence of current or past syphilis infection was significantly higher among participants who were living in urban communities, female, widowed/divorced/separated, less educated, living on the streets, and entertainment workers.

Table 1.

Characteristics of people who use and inject drugs who tested positive for Treponema pallidum.

Socio-demographic characteristics	Total (n = 1677)	Tested positive for Treponema pallidum (n = 63, 3.8%)
Socio-demographic characteristics	n (%)	n (%)	p-Value¹
Living in an urban community	1485 (88.6)	61 (4.1)	0.03
Female gender	624 (37.2)	37 (5.9)	<0.001
Age group (years)			0.66
18–24	578 (34.5)	19 (3.3)
25–34	713 (42.6)	27 (3.8)
≥35	383 (22.9)	17 (4.4)
Current marital status			0.003
Never married	769 (46.0)	26 (3.4)
Married	624 (37.3)	16 (2.6)
Widowed/divorced	278 (16.6)	20 (7.2)
Level of formal education attained			<0.001
Primary (0–6 years)	896 (53.5)	49 (5.5)
Secondary (7–9 years)	462 (27.6)	8 (1.7)
Higher (≥10 years)	316 (18.9)	4 (1.3)
Living situation			0.02
On the streets (homeless)	171 (10.2)	12 (7.0)
With parents or relatives	781 (46.7)	19 (2.4)
In own dwelling	382 (22.8)	14 (3.7)
With friends/colleagues	172 (10.3)	8 (4.7)
Other (orphanage, pagoda)	167 (10.0)	10 (6.0)
Main occupation			0.001
Unemployed	197 (11.7)	9 (4.6)
Hair dresser/beautician	82 (4.9)	0 (0.0)
Office worker	79 (4.7)	1 (1.3)
Labourer/farmer	597 (35.6)	18 (2.7)
Self-employed	212 (12.6)	4 (1.9)
Entertainment worker²	244 (14.5)	14 (7.5)
Student	41 (2.4)	1 (2.5)
Other	163 (9.7)	7 (6.7)
Average monthly income in the past six months (US$)			0.08
<100	605 (36.2)	28 (4.6)
100–199	687 (41.1)	21 (3.1)
200–299	240 (14.4)	5 (2.1)
≥300	140 (8.4)	9 (6.4)

¹Chi square (or Fisher’s exact test when a cell count was smaller than 5) was used.

²Entertainment workers refer to women working in entertainment establishments such as karaoke bars, beer gardens, and massage parlours.

Characteristics of drug use

Table 2 shows that the majority of the participants (81.5%) were currently using non-injecting drugs, and 78.9% reported using drugs in the past three months. Methamphetamine was the most commonly used in the past three months, reported by 91.3% of the participants. About one in five participants (18.5%) reported injecting drugs in the past 12 months; of whom, 27.8% reported having injected drugs in the past three months. The prevalence of current or past syphilis infection was significantly higher among participants who reported using drugs in the past three months, having been to a rehabilitation centre in the past 12 months, and having been arrested by police or other law enforcement officers in the past 12 months than among participants who did not.

Table 2.

Characteristics of drug use among people who use and inject drugs who tested positive for Treponema pallidum.

Drug use characteristics	Total (n = 1677)	Tested positive for Treponema pallidum (n = 63, 3.8%)
Drug use characteristics	n (%)	n (%)	p-Value¹
Used drugs in the past three months	1324 (78.9)	57 (4.3)	0.03
Type of drugs commonly used in the past three months
Methamphetamine (yaba, ice)	1222 (91.3)	54 (4.4)	0.57
Heroin	184 (13.8)	3 (3.8)	0.47
Ecstasy	70 (5.2)	3 (4.3)	0.99
Inhalants	53 (4.0)	1 (1.9)	0.72
Cannabis	40 (3.0)	1 (2.5)	0.48
Having injected drugs in the past three months	162 (27.8)	9 (7.4)	0.15
Been to a rehabilitation centre in the past 12 months	266 (15.9)	20 (7.5)	<0.001
Been arrested by police or other law enforcement officers in the past 12 months	324 (19.3)	19 (5.9)	0.03
Been imprisoned in the past 12 months	188 (11.2)	10 (5.3)	0.23

¹Chi square test (or Fisher’s exact test when a cell count was smaller than 5) was used for categorical variables and Mann–Whitney U test for continuous variables.

Sexual behaviours

As shown in Table 3, only 24.9% of the total of 1,557 sexually active participants reported always using condoms with any type of partners, and 40.1% reported having sexual intercourse when a partner was intoxicated with drugs or alcohol in the past three months. More than one-third (35.8%) reported having sexual intercourse in exchange for money or gifts, of whom, 39.1% reported always using condoms with commercial partners in the past three months. Only 23.0% of the total participants perceived that they were at higher sexual risk compared to the general population. The prevalence of current or past syphilis infection was significantly higher among participants who reported having sexual intercourse when a partner was intoxicated with drugs or alcohol and having sexual intercourse in exchange for money or gifts in the past three months than among participants who did not.

Table 3.

Sexual behaviours and perceived HIV risk among people who use and inject drugs who tested positive for Treponema pallidum.

Sexual behaviours in the past three months	Total (n = 1677)	Tested positive for Treponema pallidum (n = 63, 3.8%)
Sexual behaviours in the past three months	n (%)	n (%)	p-Value¹
Had sexual intercourse	1557 (92.8)	62 (4.0)	0.08
Always used condoms with any type of partners	288 (24.9)	16 (5.6)	0.14
Had sex when partner was intoxicated	462 (40.1)	26 (5.5)	0.03
Always used condoms with non-commercial partners	128 (23.0)	5 (3.9)	0.45
Had sex in exchange for money or gifts	416 (35.8)	28 (6.7)	0.001
Always used condoms with commercial partners	162 (39.1)	11 (6.8)	0.94
Perceived sexual risk compared to the general population			0.69
Higher	385 (23.0)	13 (3.4)
About the same	544 (42.5)	20 (3.7)
Lower	256 (15.3)	13 (5.1)
Don’t know	487 (29.1)	17 (3.5)

¹Chi square test was used for categorical variables and Mann–Whitney U test for continuous variables.

HIV infection and STI symptoms

Table 4 shows that 7.5% of PWUD/PWID in this study tested positive for HIV; of whom, 63.2% were aware that they had HIV before the survey. About one-third (32.5%) reported having at least one STI symptom in the past 12 months; of whom, 20.4% did not seek treatment for their most recent symptom. The prevalence of current or past syphilis infection was significantly higher among participants who reported knowing their HIV-positive status before the survey, having cuts or sores around the genital area in the past 12 months, having abnormal urethral discharge in the past 12 months, and seeking treatment for the most recent symptom than among their respective reference groups.

Table 4.

HIV and STI symptoms among people who use and inject drugs who tested positive for Treponema pallidum.

HIV and STI symptoms	Total (n = 1677)	Tested positive for Treponema pallidum(n = 63, 3.8%)
HIV and STI symptoms	n (%)	n (%)	p-Value¹
Tested positive for HIV	125 (7.5)	8 (6.4)	0.11
Aware of HIV-positive status prior to the survey	79 (63.2)	7 (8.9)	0.005
Had an STI symptom	540 (32.5)	25 (4.6)	0.22
Cuts or sores around genital area	95 (17.1)	9 (9.5)	0.01
Swelling around genital area	94 (14.9)	3 (3.2)	0.78
Abnormal urethral discharge	430 (77.3)	15 (3.5)	0.03
Symptoms around the anus	35 (6.3)	2 (5.7)	0.67
Symptoms in the mouth or throat	57 (10.3)	1 (1.8)	0.50
Sought treatment for the most recent symptom	430 (79.6)	24 (6.0)	0.004

HIV: human immunodeficiency virus; STI: sexually transmitted infection.

¹Chi square or Fisher’s exact test was used as appropriate.

Factors associated with syphilis infection

Table 5 shows factors associated with current or past syphilis infection in a multivariable logistic regression model. After adjusting for other covariates, the odds of having current or past syphilis infection remained significantly higher among participants who were female (AOR = 2.97, 95% CI = 1.26–7.01), living on the streets (AOR = 3.44, 95% CI = 1.27–9.32), having an average monthly income in the past six months of US$100 to 199 (AOR = 2.25, 95% CI = 1.05–4.82) and US$200 to 299 (AOR = 2.12, 95% CI = 1.04–6.06), having transactional sex in the past three months (AOR = 2.40, 95% CI = 1.25–4.61), and having been to a rehabilitation centre in the past 12 months (AOR = 2.54, 95% CI = 1.01–6.57) relative to their respective reference group. The odds of having current or past syphilis infection remained lower among participants who had attained at least high school level of formal education relative to participants who had attained only primary or lower level of formal education (AOR = 0.28, 95% CI = 0.08–0.98).

Table 5.

Factors associated with current and past syphilis among people who use and inject drugs in a multivariable logistic regression model (n = 1677).

Variables in the final model¹	AOR (95% CI)	p-Value
Gender
Male	Reference
Female	2.97 (1.26–7.01)	0.01
Level of formal education attained
Primary (0–6 years)	Reference
Secondary school (7–9 years)	0.48 (0.21–1.07)	0.07
High school or higher (≥10 years)	0.28 (0.08–0.99)	0.04
Current living situation
With family/relatives	Reference
On the streets (homeless)	3.44 (1.27–9.32)	0.02
In own dwelling	2.79 (0.96–8.14)	0.06
With friends/colleagues	2.17 (0.69–6.77)	0.18
Other (orphanage, pagoda)	3.06 (1.03–9.99)	0.05
Average monthly income in the past six months (US$)
<100	Reference
100–199	2.25 (1.05–4.82)	0.03
200–299	2.12 (1.04–6.06)	0.04
≥300	0.78 (0.30–2.05)	0.61
Had sex in exchange for money or gifts in the past three months
No	Reference
Yes	2.40 (1.25–4.61)	0.009
Been to a rehabilitation centre in the past 12 months
No	Reference
Yes	2.54 (1.01–6.37)	0.04

AOR: adjusted odds ratio; CI: confidence interval.

¹Age, gender, marital status, education level, and variables associated with HIV infection in the bivariate analyses at a level of p < 0.25 were simultaneously included in the model.

Discussion

The prevalence of current or past syphilis among PWUD/PWID in this study was 3.8%. The prevalence was lower in PWUD (3.4%) than in PWID (5.2%). The prevalence among PWUD/PWID reported in other studies ranges widely from a low level of 0.6% in Iran¹¹ and 1.9% in Nigeria,²² moderate level of 3.0% in Pakistan,²³ and high level of 12.6% in China,¹³ 16.0% in Brazil,²⁴ and up to 20.0% in Russia.²⁵ Rarely, studies have reported prevalence of over 20.0%, for example in Bangladesh.²⁶ These studies reported the prevalence of ever having syphilis based only on rapid plasma reagin (RPR) test^11,24 or presumed active infection confirmed by T. pallidum haemagglutination assay^22,23,26 or detection of T. pallidum antibodies.^13,25 Additionally, these studies employed varying definitions of PWUD/PWID and the substances they used – all of which may affect comparability. Despite this heterogeneity, these studies together support the conclusion that PWUD/PWID are often at high risk of syphilis, highlighted in a recent expert consensus paper.⁴

Our study found that several sociodemographic, behavioural, and structural factors are associated with current or past syphilis. These included female gender, lower education, being involved in transactional sex, having been taken to a rehabilitation centre, and living on the streets. Our finding that involvement in transactional sex predicted syphilis infection is similar to other studies that report an association between syphilis and engagement in sex work among PWUD/PWID.^10,13,23 This finding is particularly important given that engagement in sex work is a common avenue for PWUD/PWID to obtain money for drugs.²³ Not surprisingly, being female is strongly associated with syphilis sero-prevalence among PWUD/PWID in multiple studies,^12,24,27,28 as well as our own.

Regarding the association between syphilis infection and education, our results are in line with findings from two studies in Afghanistan¹⁰ and Brazil.²⁴ Although income was associated with syphilis infection in our study, the directionality of this association was U-shaped as very low or very high income seemed to be protective, a finding that requires further research. We also found that homelessness increased the risk of syphilis infection. The relationship between unmarried status or living with family is generally inconsistent across the literature, with some suggesting that married status could either increase¹² or decrease²⁷ the risk of infection. Finally, there is some evidence that mandatory detention adversely affects sexual behaviours such as condom use,¹⁷ which may explain the observed relationship between syphilis infection and history of rehabilitation. In general terms, poor outcomes associated with rehabilitation or detention suggest a need for more supportive environments to improve the sexual and general well-being of PWUD/PWID.

This study has some limitations. First, although this survey included a large sample of PWUD/PWID, participants were recruited only from the capital city and 11 provinces where most PWUD/PWID were to be found. Therefore, the generalizability of the study findings to the national level should be made with caution. Second, although RDS is an effective method to rapidly recruit hidden populations, network size can affect an individual’s probability of being recruited, and subsequently affects the estimated prevalence.²⁹ The third limitation concerns the use of a T. pallidum test to measure syphilis infection. The test usually remains positive for life, even after successful treatment, and cannot distinguish between current and past syphilis infection. Fourth, the associations found in our study are not causative, and indeed some studies report no such associations among male PWUD/PWID.²⁸ Finally, PWUD/PWID are a heterogeneous group – our sample included persons who were consuming different substances including methamphetamine, ecstasy, heroin, and cannabis, and through various modes including via injection, snorting, and inhalation. These variations have an impact on the results. For instance, a recent systematic review found that stimulant users are more likely to have multiple sexual partners and acquire HIV and other STIs.³⁰ We, therefore, must emphasize here that risk factors for acquisition of STIs are differentially situated based on the substances used by individuals and their mode of use.³⁰

Conclusions

In the midst of a paucity of data on syphilis among PWUD/PWID in Cambodia, this study identifies several socio-demographic, behavioural, and structural factors associated with current or past syphilis infection. The results suggest that PWUD/PWID should be accorded with higher consideration in regard to surveillance and service provision related to syphilis. While our study provides useful initial data, there remains a need for more research regarding precisely how syphilis screening and treatment can be implemented, for instance, through self-testing, mobile methods, and more. We suggest that: (1) policy strengthening of harm reduction policy to incorporate syndromic screening, (2) education and promotion of condoms, (3) training and monitoring of harm reduction staff on STI screening, and (4) strengthening of availability of point-of-care testing would all be critical starting points. Our study used dual tests for HIV and syphilis, and this could be an important addition to syndromic management nationally. Given our findings, regular screening and surveillance of syphilis among PWUD/PWID are needed for sustainable HIV and syphilis control in Cambodia.

Footnotes

Acknowledgements

The National Integrated Biological and Behavioral Survey among People Who Use and Inject Drugs 2017 was conducted under the leadership of National Center for HIV/AIDS, Dermatology and STD and National Authority for Combatting Drugs. We thank data collection teams, community-based organizations, local authorities, and all participants for their substantial contribution.

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: The National Integrated Biological and Behavioural Survey among People Who Use and Inject Drugs 2017 was funded by The Global Fund to Fight AIDS, Tuberculosis and Malaria in Cambodia.

ORCID iD

Siyan Yi

References

World Health Organization. Global prevalence and incidence of selected curable sexually transmitted infections: overview and estimates. Geneva: World Health Organization, 2001.

Newman

Rowley

Vander Hoorn

, et al. Global estimates of the prevalence and incidence of four curable sexually transmitted infections in 2012 based on systematic review and global reporting. PLoS One 2015; 10: e0143304.

Smolak

Rowley

Nagelkerke

, et al. Trends and predictors of syphilis prevalence in the general population: global pooled analyses of 1103 prevalence measures including 136 million syphilis tests. Clin Infect Dis 2018; 66: 1184–1191.

Coffin

Newberry

Hagan

, et al. Syphilis in drug users in low and middle income countries. Int J Drug Policy 2010; 21: 20–27.

John-Stewart

Peeling

Levin

, et al. Prevention of mother-to-child transmission of HIV and syphilis. In: Holmes

Bertozzi

Bloom

, et al. (eds) Major infectious diseases. Washington, DC: International Bank for Reconstruction and Development/World Bank, 2017.

Korenromp

Rowley

Alonso

, et al. Global burden of maternal and congenital syphilis and associated adverse birth outcomes – estimates for 2016 and progress since 2012. PLoS One 2019; 14: e0211720.

Institute of Medicine Committee on Improving Birth Outcomes. In: Bale

Stoll

Lucas

, et al. (eds) Improving birth outcomes: meeting the challenge in the developing world. Washington, DC: National Academies Press – National Academy of Sciences, 2003.

Ong

Smith

, et al. Expanding syphilis testing: a scoping review of syphilis testing interventions among key populations. Expert Rev Anti-Infect Ther 2018; 16: 423–432.

World Health Organization. Strategies and laboratory methods for strengthening surveillance of sexually transmitted infection 2012. Geneva: World Health Organization, 2012.

10.

Todd

Nasir

Raza Stanekzai

, et al. Prevalence and correlates of syphilis and condom use among male injection drug users in four Afghan cities. Sex Transm Dis. 2010; 37: 719–725.

11.

Jahanbakhsh

Bagheri Amiri

Sedaghat

, et al. Prevalence of HAV Ab, HEV (IgG), HSV2 IgG, and syphilis among sheltered homeless adults in Tehran, 2012. Int J Health Policy Manag 2017; 7: 225–230.

12.

Ruan

Liang

Zhu

, et al. Gender and ethnic disparities of HIV and syphilis seroconversions in a 4-year cohort of injection drug users. Southeast Asian J Trop Med Public Health 2013; 44: 842–853.

13.

Huang

, et al. Infection status and risk factors of HIV, HBV, HCV, and syphilis among drug users in Guangdong, China – a cross-sectional study. BMC Public Health 2010; 10: 657.

14.

Mun

Tuot

Kao

, et al. National integrated biological and behavioral survey and population size estimation among people who use and inject drugs in Cambodia. Phomn Penh: National Center for HIV/AIDS, Dermatology and STD; 2017.

15.

Tuot

Mburu

Mun

, et al. Prevalence and correlates of HIV infection among people who use drugs in Cambodia: a cross-sectional survey using respondent driven sampling method. BMC Infect Dis 2019; 19: 515.

16.

National Center for HIV/AIDS, Dermatology and STD. Conceptual framework on virtual elimination of new HIV infections in Cambodia by 2020, Cambodia 3.0. Phnom Penh: National Center for HIV/AIDS, Dermatology and STD, 2012.

17.

Mburu

Ngin

Tuot

, et al. Patterns of HIV testing, drug use, and sexual behaviors in people who use drugs: findings from a community-based outreach program in Phnom Penh, Cambodia. Addict Sci Clin Pract 2017; 12: 27.

18.

Sopheab

Chhea

Tuot

, et al. HIV prevalence, related risk behaviors, and correlates of HIV infection among people who use drugs in Cambodia. BMC Infect Dis 2018; 18: 562.

19.

Chhim

Ngin

Chhoun

, et al. HIV prevalence and factors associated with HIV infection among transgender women in Cambodia: results from a national Integrated Biological and Behavioral Survey. BMJ Open. 2017; 7: e015390

20.

Tuot

Chhoun

, et al. Prevalence and correlates of psychological distress among drug users in Phnom Penh, Cambodia. Int J Drug Policy 2016; 36: 25–32.

21.

World Health Organization. WHO prequalification of in vitro diagnostics programmes public report. Product: SD bioline HIV/syphilis duo. Number PQDx 0179-012-00. Geneva: World Health Organization, 2015.

22.

Tun

Adebajo

, et al. Population-based prevalence of hepatitis B and C virus, HIV, syphilis, gonorrhoea and chlamydia in male injection drug users in Lagos, Nigeria. Int J STD AIDS 2013; 24: 619–625.

23.

Platt

Vickerman

Collumbien

, et al. Prevalence of HIV, HCV and sexually transmitted infections among injecting drug users in Rawalpindi and Abbottabad, Pakistan: evidence for an emerging injection-related HIV epidemic. Sex Transm Infect 2009; 85: ii17–ii22.

24.

Baptista

Dourado

Brignol

, et al. Factors associated with syphilis seroreactivity among polydrug users in Northeast Brazil: a cross-sectional study using Respondent Driven Sampling. Int J Drug Policy 2017; 39: 37–42.

25.

Rhodes

Platt

Maximova

, et al. Prevalence of HIV, hepatitis C and syphilis among injecting drug users in Russia: a multi-city study. Addiction 2006; 101: 252–266.

26.

Azim

Bogaerts

Yirrell

, et al. Injecting drug users in Bangladesh: prevalence of syphilis, hepatitis, HIV and HIV subtypes. AIDS 2002; 16: 121–123.

27.

Zou

Ling

Zhang

Trends and risk factors for HIV, HCV and syphilis seroconversion among drug users in a methadone maintenance treatment programme in China: a 7-year retrospective cohort study. BMJ Open 2015; 5: e008162.

28.

Scherbaum

Baune

Mikolajczyk

, et al. Prevalence and risk factors of syphilis infection among drug addicts. BMC Infect Dis 2005; 5: 33.

29.

Frost

Brouwer

Firestone Cruz

, et al. Respondent-driven sampling of injection drug users in two U.S.-Mexico border cities: recruitment dynamics and impact on estimates of HIV and syphilis prevalence. J Urban Health 2006; 83: i83–i 97.

30.

Tavitian-Exley

Vickerman

Bastos

, et al. Influence of different drugs on HIV risk in people who inject: systematic review and meta-analysis. Addiction 2015; 110: 572–584.