Background
Over the past two decades, Cambodia has been successful in its fight to slow the spread of HIV [
1]. HIV prevalence among the general population decreased from an estimated 1.6% in 1998 to 0.6% in 2015 [
2,
3]. The estimated number of new HIV cases per year also decreased from roughly 4400 in 2005 to 700 in 2015 [
2,
3]. Despite this success, as of 2015, an estimated 74,000 Cambodians were living with the virus [
4]; with about 27% of these individuals (~19,000) being unaware of their HIV-positive status [
2].
Early HIV diagnosis and initiation onto antiretroviral therapy (ART) may prevent ongoing spread of HIV. Knowledge of one’s HIV-positive status has been shown to be associated with increased condom use [
5]. ART initiation, when resulting in viral load suppression, can reduce the risk of HIV infection between 89% to 96% to uninfected sexual partners of an HIV positive individual [
6‐
10].
The Government of Cambodia has committed to ending the AIDS epidemic by 2020 [
3]. It means, by the year 2020, the annual number of new HIV infections must fall below 300 [
3]. To successfully reduce the number of new HIV infections, innovative approaches are needed to reach people living with HIV who are unaware of their HIV status and link them to early diagnosis and treatment. One such approach, the Risk Tracing Snowball Approach (RTSA) has been shown to be effective in detecting new HIV cases that would otherwise not have been found [
11‐
13]. RTSA is an adaptation of the Respondent Driven Sampling method, a form of sampling often used in bio-behavioural surveillance studies, in which study recruitment relies on peer-referrals [
14]. RTSA, which is also sometimes referred to as a “Peer-Driven Intervention,” has been successfully used to increase the rate of newly undiagnosed HIV infected individuals among high-risk heterosexuals in the US [
13]. It has also been found to be an effective approach to rapidly identify newly undiagnosed HIV individuals among people who use and inject drugs in Greece [
12] and among heterosexual couples in China [
11]. However, it has never been implemented in Cambodia context.
The main objective of this study was to evaluate the effectiveness of RTSA in increasing the rate of newly identified HIV cases among high-risk populations, including female entertainment workers (FEW), men who have sex with men (MSM), transgender (TG) women, people who inject drugs (PWID), people who use drugs (PWUD), and the general population who have social connections to key populations. The second objective was to evaluate the effectiveness of RTSA, as compared to the walk-in group, in increasing the number of HIV tests and early HIV case detection by comparing CD4 count between clients from the two groups.
Methods
Study settings
The RTSA was implemented between April 1 and September 30, 2016 at two clinics, Chhouk Sar I and Chhouk Sar II, in the capital city of Phnom Penh. The two clinics are operated by the Chhouk Sar Association, a non-governmental organization (NGO) established in 2010. These two clinics provide comprehensive HIV and sexual and reproductive health services, including HIV testing and counselling, ART, as well as sexually transmitted infection (STI) screening and treatment for key populations— FEW, MSM, TG women, PWID, and PWUD. These clinics also provide HIV testing services, but not ART, to the general population. Newly identified HIV positive individuals from the general population are referred to a governmental ART site.
Intervention
The RTSA was designed by the HIV/AIDS Flagship Project [
15,
16] to reach high-risk populations. We hypothesized that this intervention would increase the number of HIV tests and early HIV case detection. All clients who presented for HIV testing and counselling services at one of the two clinics were given the opportunity to serve as
“seeds” and recruit other high-risk individuals within their personal social and sexual networks to get tested for HIV. Seeds were supplied with five coupons for use in recruiting up to five individuals from their networks. If a recruited individual (or so-called
“recruit”) presented at either clinic with a valid coupon and screened as being “at risk” for HIV infection and completed HIV testing, the initial seed who recruited this individual would receive a financial incentive (2.5 USD). Recruits who received HIV testing and a risk assessment interview also received the same financial incentive (2.5 USD). Recruits were then offered the same opportunity as the initial seeds to recruit other high-risk peers within their social and sexual networks to get tested for HIV. This procedure was applied to all recruits, regardless of wave length, up until September 30, 2016.
Target populations and inclusion criteria
The goal of RTSA was to reach populations at higher risk of HIV infection, but less frequently tested for HIV. This intervention included all clients presenting for HIV testing at the two selected clinics who (1) were at least 18 years old, (2) had not been tested for HIV anywhere during the previous 3 months, and (3) provided verbal informed consent which included being finger printed. They can be a FEW, MSM, TG women, PWID, PWUD, and the general population who have social connections to those key populations.
Implementation procedures
The RTSA was built on the existing system in place at both Chhouk Sar clinics. All procedures for voluntary confidential counselling and testing (VCCT) were followed, except two more activities added to the RTSA. These two activities are described in Table
1.
Table 1
Process of RTSA implementation
Step 1: Clients arrived at Chhouk Sar clinic, greeted by a receptionist, and asked about services needed. | Yes | |
Step 2: Clients presented for HIV testing were referred to the VCCT floor, where they received a queue number. | Yes | |
Step 3a: Clients met with a counsellor for HIV pre-testing counselling. | Yes | |
Step 3b: Clients who consented were registered, fingerprinted, and then interviewed using a tablet-based questionnaire. | | Yes |
Step 4: Clients were tested for HIV—Determine Test, Stat-Pak, and Uni-Gold [ 21]. | Yes | |
Step 5: Clients received HIV post-testing counselling. If HIV-positive, they were asked to immediately enroll into Pre-ART/ART treatment at the clinics if they self-identified as a key population. Those self-identified as the general population were referred to other Pre-ART/ART sites. | Yes | |
Step 6: Clients met with coupon manager if they agreed to be part of RTSA. Coupon manager explained to seeds/recruiters on how to use the coupons and the benefits for referring. | | Yes |
To receive the financial incentive associated with successful referrals, some seeds/recruiters presented at the clinics with the recruited individuals, while others called coupon managers to check whether their referral was a success.
It should be noted that the online fingerprint system, as mentioned in step 3b in Table
1, was an important tool to ensure that clients could not get tested for HIV more than once within a three-month period. A counsellor-administered, tablet-based questionnaire was built using the Qualtrics application. The application automatically generated the level of risk for HIV infection at the end of the interview. Clients could reject being registered into the fingerprint system or the interview. While they could still be tested for HIV, they were not part of the RTSA study.
Questionnaire development and measures
The “risk screening tool” questionnaire was initially developed by a technical working group led by the National Centre for HIV/AIDS Dermatology and STD (NCHADS) and included key stakeholders in Cambodia. It was developed to screen for HIV risk behaviors of key populations. This study used this risk screening tool to identify individuals at risk for HIV infection.
The main outcome of interest in this study was the rate of newly identified HIV positive cases. In addition, there were three other exploratory secondary outcomes, including the absolute number of HIV tests conducted, the absolute number of newly-identified HIV positive cases, and CD4 count for those individuals tested HIV positive.
The risk assessment tool included questions used to determine key populations (FEW, MSM, TG women, PWUD, PWID) categorization, sexual behaviors with different types of sexual partners since last HIV test, or lifetime number of sexual partners if not previously been tested for HIV. Information was also collected on the history of STI symptoms, illicit drug use, hormone injection for TG women, and pregnancy and abortion for women.
Data analyses
The rate of newly identified HIV positive cases was calculated by dividing the total number of newly identified HIV positive individuals by the total number of individuals tested for HIV during the implementation period. Chi-square test, or Fisher’s exact test when a cell count was smaller than five, were used to describe and compare characteristics between the walk-in group and the RTSA group. Factors associated with the rate of newly identified HIV positive cases were explored separately among the walk-in group and RTSA group. Bivariate and multivariable logistic regression analyses were conducted. All variables associated with HIV infection at a level of p < 0.25 in bivariate analyses were included in the multivariable models. STATA Version 14.1 for Windows (Stata Corp, TX, USA) was used to conduct the data analyses.
Ethical consideration
This study was approved by the National Ethics Committee for Health Research (No.085 NECHR) of Ministry of Health in Cambodia and the FHI 360’s Protection of Human Subjects Committee (No. 590334 PHSC). All participants provided a verbal informed consent, ensuring that they understood about the voluntary and confidential participation in the study.
Discussion
This study found that the rate of newly identified HIV positive cases generated by RTSA was significantly lower compared to the rate in the traditional walk-in approach. However, we found that the absolute number of HIV cases detected during RTSA implementation (RTSA and walk-in approach combined) was much higher than that in the six-month period prior to the RTSA implementation and the six-month period after the RTSA implementation ended. This finding indicates that a combination of RTSA and a traditional walk-in approach may increase new case detection among high-risk populations, especially key populations.
The lower rate of newly identified HIV positive cases among the RTSA clients than that in the walk-in clients is not surprising. Individuals who walked in to get tested are more likely to do so because of their self-perception of their risky behaviors, or because they felt sick. It is also plausible that when more individuals are tested, the HIV rate will naturally go down.
Even though the rate of newly identified HIV positive cases for the RTSA group was lower than the rate obtained from the clinics’ routine data (walk-in group), this rate should still be considered acceptable for four reasons. First, the combination of the routine walk-in testing and RTSA during RTSA implementation boosted the absolute number of HIV new case detection from 32 in the six-month period prior to the RTSA implementation to 52 cases in the six-month period of RTSA implementation. Second, CD4 count in RTSA group was higher than that in the walk-in group. This may infer that RTSA leads to earlier detection of people living with HIV. Third, the rate of newly identified HIV positive cases in RTSA group was much higher than the rate of newly identified HIV positive cases reported nationwide in programs using an outreach HIV testing approach among key populations—FEW, MSM, TG women, and PWID-- which has never reached more than 1.0% since the program implementation was started in 2013 [
15,
16]. Fourth, the rate of newly identified HIV positive cases in RTSA group is comparable to the national HIV prevalence in each key population: FEW (3.8% vs. 4.6%), MSM (1.7% vs. 2.3%), TG women (2.2% vs. 5.9%), and PWUD (1.7% vs. 4.1%), except PWID (0% vs. 25%) [
17‐
20].
Other than being in a high-risk group (TG women, MSM) and experiencing tested for HIV, our study did not find any factors associated with the rate of newly identified HIV positive cases in either groups—walk-in and RTSA. The non-significant differences may be explained by the following reasons. First, as with any other self-reporting measures, risky behaviors may have been underreported due to social desirability. This was also observed among the walk-in group by counsellors. Thus, levels of risks may have been misclassified. In contrast, the RTSA group may have over-reported their risks to make their recruiters eligible for financial incentives. It should be reminded that all recruited individuals can get HIV testing and receive 2.5 USD transportation compensation regardless their risk status and HIV testing result. However, seeds or recruiters can only get the incentive when their recruits were screened at risk for HIV infection. Second, our questionnaire has never been validated. We may not have asked the right questions to identify risks. And third, the small sample size may have contributed to the non-statistically significant associations. Regardless what might be the reasons, using a risk-screening tool to identify risky clients may have low validity, especially when it confounded by the use of monetary incentives. Excluding those who reported low risk to HIV infection may also have influenced our ability to further elucidate risk factors.
Theoretically, people are more likely to refer those who are similar to them [
14]. This theory is not necessarily true considering HIV testing results in this study. HIV negative clients may be happier after getting the test result and might be willing to refer their peers. In contrast, positive clients were more likely to stop the recruitment after they learned about their HIV-positive status. As shown in the network graph, most of the positive clients did not recruit anyone else to join the study. This nature has blocked the power of network referral. If HIV-positive clients could recruit more people, they may recruit their sexual partners and their peers who had similar risks. However, newly detected HIV-positive individuals need some time to stabilize their emotional condition first, or they will never recruit other people because they do not want others to suspect or learn about their HIV status.
The strength of this study is the use of well-managed patients tracking system in Chhouk Sar clinics where the study was conducted. The online fingerprint system can track HIV test interval of individual clients. Clients could not be tested multiple times at one or another Chhouk Sar clinic within 3 months. However, our study also has several limitations. First, we could only trace clients in our system. We could not manage if they were tested elsewhere. Second, the self-reported risky behaviors may not be reliable due to the use of monetary incentives. However, identifying sexual risky behaviors was not the main objective of the study. Rather, it was the rate of newly identified HIV positive cases that detected by three-test algorithm —Determine Test, Stat-Pak, and Uni-Gold [
21]. Third, the identification of newly detected cases was based on counsellors’ skills. In this sense, we cannot deny the possibility of inclusion of formerly detected HIV clients in the newly identified HIV positive group. However, because all newly identified HIV-positive clients were closely followed-up until they got enrolled in the treatment, only minor discrepancies were likely to happen. Lastly, our study ended up with inconclusive result whether the RTSA is cost-effective because the study design did not allow further investigation on this important aspect. To address this shortcoming, cost-effectiveness modelling should be conducted. This kind of study will be able to assess the number of people who will be prevented from HIV infection resulting from early detection by RTSA, and unit cost to invest to keep a person uninfected with HIV per year – known as Disability-Adjusted Life Year (DALY) [
22].
Acknowledgements
This study was conducted in a collaboration between the consortium partners of the HIV/AIDS Flagship Project including KHANA, FHI360, and PSI/PSK, and Chhouk Sar Association under the leadership of the National Center for HIV/AIDS, Dermatology and STD (NCHADS). We thank Dr. Laurent Ferradini and Amy Weissman, FHI 360 technical experts, who initiated the project. Also, we thank all Chhouk Sar’s staff and participants in the study who fully supported during the study design and data collection. Disclaimer: Content of this paper is the responsibility of the authors and does not reflect the view of USAID or our respective institutions.