Uptake of provider-initiated HIV and syphilis testing among Heterosexual STD Clinic attendees in Southern China: Results from a Cross-sectional Study

Background Provider-initiated HIV and syphilis testing and counseling (PITC) services are important components of HIV and syphilis prevention programs. However, PITC guidelines have neither been formalized nor widely implemented in China. Limited studies conducted to identify the barriers to offering PITC services from sexually transmitted diseases (STD) clinic attendees’ perspective. We conducted a cross-sectional survey on heterosexual STD clinic attendees to evaluate this in China. Methods A cross-sectional survey was conducted in 2016 in Southern China. Participants completed a validated questionnaire including social-demographic information, reasons for not conducting HIV and syphilis testing, and HIV and STD infection history. In this study, we limited the participants as individuals who self-identified as heterosexual. Results A total of 1943 participants were recruited in this study. Among those participants, 60.6% (1177/1943) and 74.3% (1443/1943) conducted HIV testing and syphilis testing during the study, respectively. Of whom, 2.2% (26/1177) and 21.5% (310/1443) are found to be HIV-positive and syphilis-positive, respectively. The most common barrier to HIV and syphilis testing is a lack of awareness of HIV and syphilis infection. Condom use in the last sexual act, having paid sex during the last 6 months, and receiving HIV and STD related knowledge were positively associated with uptake of both HIV and syphilis testing. Conclusions This study highlights the need and importance of promoting provider-initiated HIV and syphilis testing and counseling services in China. Future studies on exploring innovative methods to improve the knowledge and awareness of HIV and syphilis infection among STD clinic attendees is warranted.


Introduction
Sexually transmitted human immunodeficiency virus (HIV) infections have become a public health concern globally. An estimated 85% of HIV infections are transmitted through heterosexual intercourse worldwide [1]. In China, heterosexual transmission has been reported to account for 69.9% of HIV infections [2]. Integration of HIV services into routine STD clinical care has been proven useful for expanding HIV testing and treatment among populations at risk for both infections in many low-3 and middle-income countries [3][4][5].
In 2014, considering the high burden of HIV-syphilis co-infection and syphilis epidemic, the Chinese centers for disease control and prevention issued provider-initiated HIV/syphilis testing and counseling (PITC) guideline to increase provider HIV/syphilis testing in China [6]. However, promoting physicians providing HIV and syphilis testing actively to all patients presenting for STD medical care is no small task due to the high workload of clinicians in China [7]. To address this challenge, several studies suggested strategies of pay-for-performance, strengthened training and propaganda among physicians to encourage provider HIV/syphilis testing [6,8]. Although a good increase of HIV/syphilis testing rate among STD clinic attendees was observed with applying of these strategies, the rates of HIV testing [6](56.7%) and syphilis testing [6](68.6%) were still much lower than the target of 90% of people with HIV and syphilis to know their status by the year 2020[9, 10]. To date, limited studies conducted to analyze the factors associated with uptake of HIV/syphilis testing from STD clinic attendee's perspective in the context of PITC program [11][12][13].
In light of the high proportions (99.1%) of heterosexual population among STD clinic attendees [13], this study was conducted among heterosexual STD clinic attendees to analyze determinants of syphilis and HIV test uptake from patients' perspective in China to inform a better model for PITC implementation.

Participants and procedures
We conducted a cross-sectional study among heterosexual STD clinic attendees in seven public STD clinics in two cities in southern China from July 2016 to December 2016. The types of public STD clinics included three clinics in the general hospital, two clinics in the maternal-child health center and two clinics in the local STD prevention center. For participants who visited the seven STD clinics, physicians would actively recommend them to conduct HIV and syphilis testing during the consultation process. Participants meeting with the following inclusion criteria were asked to fill out a questionnaire with the help of a trained research assistant: self-identified heterosexual, engaged in vaginal or anal sex with an opposite-sex partner in the past 12 months, at least 18 years of age, and willing to provide written informed consent. After completing the questionnaire, for participants who were willing to uptake HIV and syphilis testing, approximately 10 ml of blood would be drawn by a trained nurse for HIV and syphilis testing.

Social-demographic and behavioral variables
Socio-demographic information included: age, gender, marital status, education, and monthly income.
Behavioral variables included condom use in the last sexual act, frequency of condom use in the last 6 months, and commercial sex behavior in the last 6 months.

HIV and syphilis testing and related medical services variables
HIV and syphilis testing and related medical services included acceptance and uptake of HIV and syphilis testing during this visiting, reasons for not conducting HIV and syphilis testing at this time, HIV and STD infection history, education on HIV and STDs related knowledge in the past 12 months.

Laboratory testing
The Enzyme-linked Immunoassay (ELISA) test (Lizhu Biotech Inc, Zhuhai, China) was used for HIV screening and Western blot assay test (HIV Blot 2.2 WB, Wantai Biotech Inc, Beijing, China) was used for HIV test confirmation. The rapid plasma regains (RPR) test (Lizhu Biotech Inc, Zhuhai, China) and Treponema pallidum particle agglutination (TPPA, Rongsheng Biotech Inc, Shanghai, China) were used for syphilis screening and confirmation, respectively.

Statistical analysis
All data were double-entered with logic checks using EpiData3.0. Descriptive analysis was performed to describe socio-demographics, sexual behaviors, and HIV/syphilis testing. Univariate and multivariable logistic regressions were conducted to explore factors associated with uptake of HIV and syphilis testing as well as HIV and syphilis infection. In the multivariable model, we adjusted for age (continuous), gender, marital status, educational attainment, and monthly income. All data were analyzed using SAS 9.4 (SAS Int. Cary, NC, USA).

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A total of 1943 participants were recruited in this study. Of those participants, the majority were male
Around half of the individuals (56.9%, 1105/1943) were tested for HIV and syphilis at the same time, and 0.54% (6/1105) was co-infected with both HIV and syphilis (Table1 and Table2).

Factors associated with HIV and syphilis testing uptake
After adjusted for age, gender, ethnic, education level, marital status and monthly income, multivariable logistic regression analysis indicated that condom use in the last sexual encounter

Factors associated with HIV and syphilis infection
After adjusted for age, gender, ethnicity, education level, marital status and monthly income, multivariable logistic regression analysis indicated that participants who had paid sex during the last 6 months (aOR=2.00, 95%CI: 1.24 -3.12) were more likely to be infected with HIV. (Table 4).

Discussion
PITC was a key component of HIV and syphilis prevention programs [14]. Although many PITC successful pilots have been implemented in China, PITC guidelines have neither been formalized nor widely implemented. This study extended the existing literature by focusing on heterosexual STD clinic attendees and analyzing barriers to acceptance of provider-initiated HIV and syphilis testing service from patients' perspective. Data suggest that many barriers still exist preventing patients from accepting PITC services in China. Findings from this study provide insights for the future implementation of PITC services among STD clinic attendees in China.
We found a low acceptance of provider-initiated HIV and syphilis testing services among heterosexual STD clinic attendees in China. This rate is much lower than previously reported in Zambia [15], Botswana [16] and South Africa [17]. Whereas other studies showed that social stigma against HIV and STD [18], fear of testing [19] and Our study showed a high proportion of both HIV and syphilis prevalence among individuals who conducted HIV and syphilis testing. This prevalence is higher than previously reported in other studies in China [13], South Africa[22], Vietnam[23]. Additionally, our results found that engaging in commercial sex and the lack of condom use in the last sexual act were common among those testers, which is similar to previous studies in China [13] and England [24]. This indicates that heterosexual STI clinic attendees bear a high burden of HIV and syphilis infection, warranting the necessity of improving PITC implementation among this population.
Our data indicated that, amongst individuals who refused to test, a majority reported having never been tested for HIV and syphilis in the past year. However, commercial sex in the past 6 months and low rates of condoms use is particularly common among the non-testers in this study. This finding is consistent with previous other studies [12,[25][26][27]. Therefore, there may be many HIV and syphilis infected patients who remained undetected and untreated among this population.
This study has several limitations. First, all the data were collected through self-report, which may be prone to information bias. Second, the participants were not randomly selected in this study. This may limit the external validity of our findings. Third, this study was cross-sectional, so relations should be interpreted as associations that might or might not be casual. Finally, this study could not account for many factors that likely influence the frequency of testing-policy environment, clinic factors, and local norms.

Conclusion
In conclusion, provider-initiated HIV and syphilis testing is an effective strategy to reach high-risk individuals of contracting HIV and syphilis. However, this service is not well promoted among STD