Introducing rapid oral–fluid HIV testing among high risk populations in Shandong, China: feasibility and challenges

It is estimated that by the end of 2011, the number of people living with HIV in China was about 780,000 [1]. The National HIV/AIDs report showed that, men who have sex with men (MSM) and female sex workers FSW recorded a 5% and 6% (median) estimated prevalence respectively in 2009 which far exceeds the general populations’ prevalence of 0.05% [2, 3]. Hence, MSM and FSW are categorized as ‘populations at highest risk’ of infection for HIV in China. Report at the end of October 2012 showed that cumulatively, the number of reported HIV/AIDS cases was 492, 191, with 383,285 people living with HIV/AIDS [4]. This means that over half of people living with HIV/AIDS do not know that they are infected. Studies showed that about 33.2% of MSM and 42% of FSW have never been tested [3, 5] and 86.1% of infected MSM are unaware of their infection status [5‐7]. Thus, testing rate among both MSM and FSW is low and this means that over half of people living with HIV/AIDS do not know that they are infected [5‐9].

Voluntary counseling and testing (VCT) has been an important tool employed by WHO and other health organizations worldwide to identify new cases and implement treatment as prevention strategies [10]. The imperative of scaling up HIV testing in China was recognized as an important strategy for identifying unknown positives and preventing onward transmission of HIV [11, 12]. Free HIV testing has been made available, and expanded from 365 counties in 15 provinces in 2002 to over 2300 counties, with 3037 sites, in all provinces by 2006 [1, 4, 11]. However, the biological, social, economic, political, and ethical concerns surrounding HIV surveillance, access to care and prevention still remains complex [1, 2, 13].

Currently, enzyme-linked immunosorbent assay (ELISA) combined with western-blot and rapid blood testing are the major HIV antibody testing methods employed in HIV testing in most countries including China [14‐16]. Though ELISA is the ‘gold-standard’ HIV testing method for screening, which is recognized traditionally, it is not without disadvantages [17‐19]. For example, it cannot be used in point-of care since it requires ELISA equipment and professional staff for its use, waiting time for results has been reported to be too long and expensive hence discouraging users [20]. Also, the use of needles and sharp objects with their associated pains to obtain the needed blood sample deter many people from using it. For FSW and MSM, providing an alternative testing method eliminates the issue of facing professionals in front of whom they might have to answer questions on their number of sexual partners and their sexual orientation which most of them find uncomfortable [2, 3, 5‐9]. Notwithstanding there is an urgent need for acceptable and feasible testing methods among MSM, FSW and VCT clients in order to scale up HIV testing.

Rapid oral fluid based testing method has already been approved and is in use in most HIV testing institutes worldwide [7, 21‐25]. The testing kits and testing method have further been found to be accurate, much safer and easier to use and therefore recommended for adoption and use in the developing countries due to its simplicity, versatility and, feasibility that enables easier implementation and use even in rural areas and private health institutions [22, 23]. Also, incorporation of oral HIV tests could form part of a multi-pronged prevention strategy in transforming the trajectory of the HIV epidemic in China and possibly the world at large [24, 25]. A study conducted in Seattle indicated that clients are more likely to accept HIV testing using this method instead of standard blood testing because it is less intrusive and painless [26].

Although four testing kits have been approved as of the end of 2011; [27] “ Sidaizhiyu Oral Fluid HIV ½ Antibody Diagnostic Kit” (Wondfo Biomedical Co., Ltd, 2011), “Union Oral Mucosal Transudate HIV-1/2 Antibody Detection Kit “(Chengdu Union Bio-technology Ltd., 2011), “Aware HIV-1/2 OMT” (Beijing Marrbio Ltd, 2008) and “HIV 1/2 antibody Dot ELISA rapid test” (Beijing Wantai Biological Pharmacy Enterprise Co., Ltd., 2011 ), [28] rapid oral testing is however not been widely used and no data exist to assess the uptake of oral testing and how accurate these kits are in real world settings in China. Hence this studies to ascertain the feasibility of up scaling its usage in China.

There were 371 MSM, 405 FSW and 361 VCT clients with participation rates of 98.9%, 99.3% and 98.1% respectively.

A key finding that may impact the scale up of rapid oral HIV testing was that the test kit recorded lower sensitivity (77.5%) than stated by the manufactures, which may reduce credibility of this test and consequently, acceptability by populations at risk for HIV. A number of factors that may explain our observed low sensitivity include the small sample size and the many errors made by participants during the testing phase rendering most of the test results invalid. This could have also decreased the sensitivity of the test kit and thereby slightly lowering the positive predictive value (PPV) from the manufacturers stated value of 99% PPV. The comparison between consultant testing and client self-test recorded a low sensitivity of for self-testers. This observation could be due to errors committed by the clients during the testing process leading to the indeterminate results, invalid tests and missing data. The issue of indeterminate results and invalid tests which lowers the sensitivity of the test is a real life problem. Hence client with such results are encouraged to retest and also seek assistance from consultants. Also, the sensitivity of self-test may vary cross population, depending on the populations’ educational level and their ability to learn quickly [27].

Similar studies on the use of HIV rapid oral fluid test for self-testing have been conducted in the U.S. and some parts of Africa [17‐24]. Most of those studies concluded from their obtained results that, the idea of using saliva testing as an alternative testing method nationally was highly feasible if only the populations’ knowledge of how to use the test kit and its limitations is raised through education before implementation [19‐26]. The US studies was conducted using a rapid saliva test kit known as “OraQuick test (OraSure technologies)” that recorded a sensitivity of 97.4% and specificity of 99% [26, 29], though their observed sensitivity of 97.4% was somewhat greater than our observed sensitivity of 77.5%, the general conclusions we both derived from the studies are similar. Additionally, the use of rapid oral fluid testing as a testing or screening method for HIV antibodies was found to be safe and highly effective, thus highly feasible in a number of countries [19‐25, 30]. Findings from the descriptive analysis of our study suggests that, individuals from populations at risk for HIV determine what HIV test they will take based on accurate results, needs for privacy, and the cost of testing. To address the concern about accuracy, a validity and consistency analysis was conducted on the test results. Our analysis recorded a consistency rate of 0.970 with a kappa value of 0.551, indicating an excellent consistency. This consistency rate implies that the test results from the saliva test kit were both consistent with the results from the blood test and equally credible and accurate as other testing methods like blood tests.

Further analysis to assess feasibility depended on participants’ ability to operate the test kit and read results correctly. Observations made during the testing process showed that about half of all participants found the directions to be too complicated, which accounted for most of the errors observed during the process. For example, 40 (17.47%) did not want to watch or read the introduction book and reported that it was too complicated and with specialized language that they did not understand. These individuals had to go through the testing process with the assistance of medical professionals, 1(0.45%) touched the test area of test paper with the hand while running the test, 1(0.45%) tore off the middle membrane of test paper, and 4 (1.82%) could not find or take out the test paper. All these errors impacted the sensitivity and accuracy rate of the test kit itself. These errors could be eliminated through educational workshops and media education on the credibility and accuracy of the test kit, and through the development of simpler operational steps on how to operate the test kit and interpret results. Videos that walk testers through the steps in testing could be useful as well.

When questioned on testing venue preferences, 519 (52.7%) subjects wanted to be tested at the CDC office that currently provides HIV testing services to the public and 277 (24.5%) preferred to be tested in the hospital. HIV home testing was preferred by 353 (57.3%) participants because it was convenient, and 360 (58.4%) participants wanted home testing for privacy reasons. Another study among Chinese MSM also found that MSM prefer to test at a VCT clinic opened by a local CDC rather than a hospital [6]. Thus, many participants were willing to accept the use of the rapid oral fluid HIV testing, which suggests high feasibility in the population. However, we did find that the thought of results not being credible and testing method not being nationally recognised as participants put it explains why many participants are hesitant to pick this method as their HIV testing method of choice.

This study has a few limitations. Some of the subjects refused to answer questions required for the descriptive analysis leading to missing data which may or may not have affected the overall study results. This was attributed to reasons like them not knowing the answer to the question or did not really understand the question. Also, could be that they were uncomfortable with how personal the question was. A total of 6 missing data points representing 3% was recorded. Another limitation was limited budget constraint which affected the total number of people we could sample and test.

The findings from this study indicate that the introduction of rapid oral fluid HIV testing (saliva testing) as an additional testing or screening method in these cities is highly feasible. However, challenges still exist, for example, the level of knowledge on rapid oral fluid testing is low among the high risk population groups; operational errors influence the accuracy and sensitivity of the test. Hence, there is a need for mass education before the implementation of this new method. One option for mass education may be an easy-to-understand video that can be shared online to increase awareness and accuracy. Finally, additional research should be conducted to understand feasibility in other parts of the country.