Missed opportunities for HIV testing in patients newly diagnosed with HIV in Morocco

Late diagnosis of HIV infection, and therefore late access to antiretroviral treatment, leads to significant HIV-related morbidity and mortality, as well as an increase in onward HIV transmissions [1, 2]. In Morocco in 2011, of the estimated 29,000 people living with HIV, only 20% were aware of their HIV status. More than half of diagnoses were at the AIDS stage [3].

However, at this time, national guidelines recommended HIV testing for people who seek care with clinical signs suggestive of an underlying HIV infection and/or for people from key populations [4]. In 2011, although there was a low HIV prevalence in the general population (0.1%), people who inject drugs (PWIDs), men who have sex with men (MSM) and female sex workers (FSWs) were disproportionally affected by HIV with a prevalence of 11.4, 5.1 and 1.9%, respectively [5]. Considered together, these data highlighted insufficient access to HIV testing and failure of HIV strategies to reach those most at risk of HIV acquisition.

In other countries like France and Ivory Coast [6‐9], a large proportion of people who were unaware of their HIV infection had contacts with the healthcare system during the period of probable HIV infection. During these contacts, an HIV test was rarely offered by the healthcare provider even if the patients reported HIV indicators. Several diseases or clinical symptoms have been highlighted as HIV indicators since the undiagnosed HIV prevalence among the patients who suffer from them was > 0.1%, thus justifying routine HIV testing [10‐12]. Identifying these missed opportunities to offer a test and quantifying the missed opportunities could guide policy makers in extending HIV testing guidelines. The aim of this study was to assess the missed opportunities for HIV testing in patients newly diagnosed with HIV who accessed care in Morocco.

In Morocco, this multicenter study revealed that a high proportion of people newly diagnosed with HIV could have been tested earlier due to the presence of HIV-related high-risk behavioral and/or clinical conditions. First, nearly two out of three patients attended healthcare facilities during the period of probable HIV infection. Many of those with HIV indicators who sought care received no HIV test offer. For instance, 83% of MSM did not address their sexual behavior with the healthcare provider during this visit. Among the remaining MSM who had an opportunity for HIV testing, only one out of three was offered a test. In the same way, 69% of people who sought care for HIV-related clinical conditions were not offered an HIV test. Healthcare providers missed many opportunities to discover that their patients were living with HIV.

To our knowledge, this study is the first to describe the medical history of people infected with HIV before their HIV diagnosis in Morocco. In identifying all contacts with care, there was no computerized medical file common to the different health facilities. Therefore, medical information had to be collected retrospectively from the patients themselves, so the study may have suffered from recall bias leading to underestimation of the number of missed opportunities. To limit this bias, patients diagnosed with HIV more than 6 months before were excluded and the data collection period was restricted to 3 years prior to HIV diagnosis. Participants were asked about all clinical conditions of interest in our study, and a list of care facilities was drawn up to help them remember.

By directly interviewing patients, we investigated the overall patient trajectory through the healthcare system. Unlike some studies conducted in large urban hospitals in the United States and based on medical chart reviews [13, 16], we were able to detect HIV indicators whatever the access to care or the healthcare facility. This is all the more essential in a country where people often have access to care outside the hospital, mainly through private doctors or pharmacists.

Our study was based on a physician-administered questionnaire to help patients retrace their medical history, which consequently may have been subject to a social desirability bias concerning at-risk behaviors and sensitive issues that might be under-reported. Only 8% of participants (n = 51) reported being MSM, whereas it was estimated that nearly 15% of new HIV infections in Morocco occurred among MSM in 2010 [17]. Homosexuality was stigmatized in Morocco at this time and this may have had a negative impact on global health, HIV prevention, and retention in HIV care [18, 19]. Moreover, the National Strategic Plan against AIDS 2012–2016 [13] aimed to reduce discrimination and stigma, especially against MSM within healthcare settings [20].

Comparing our results with those of other studies was quite difficult because assessment of missed opportunities differed according to time-windows for retrospective detection of HIV testing opportunities, study designs and the populations considered [6‐9, 21, 22]. One study in France in 2010 [6] and one in Ivory Coast in 2014 [7] revealed 82 and 77% of missed opportunities for HIV testing in people who sought care for an HIV-related clinical condition, respectively; this proportion is even higher in Morocco (88%).

These people with a missed opportunity had low CD4 counts at diagnosis (median: 97 cells/mm³, see Table S1) suggesting they were probably already infected with HIV at the time of the contact. As in other studies on the topic [6, 9, 23], whatever the clinical indicator, the proportion of HIV testing offered was very low. All people who sought care for herpes zoster or community-acquired pneumonia had a missed opportunity for HIV testing. Physicians’ knowledge of HIV clinical indicators should be strengthened.

Behavioral indicators were rarely addressed with the healthcare provider. On the one hand, patients may not have mentioned their behavior – multiple sex partners, condomless sex with casual partners or MSM – for fear of stigma or discrimination, or because they did not consider themselves to be at risk [24]. On the other hand, the physician did not ask about at-risk behaviors and offer a test. Studies that assessed the barriers to physicians offering HIV testing have highlighted difficulties in addressing sexuality with patients [25‐28]. Our study showed that people who had been tested once in their lifetime were less likely to have a missed opportunity for testing compared to those who had never been tested before. This may be explained by the counseling associated with testing, which provided a better understanding of HIV transmission routes, and perception of risk-taking. Another key population very affected by HIV in Morocco is FSWs. No information was collected on sex work, but some women, who represented 11% of the study population, had a median of 40 partners (IQR: 20–100) and also reported more sexually transmitted infections and more behavioral indicators than others, but as many missed opportunities as others (data not shown). They were also more likely to have been tested for HIV during their lifetime.

In 2012, the Moroccan Ministry of Health implemented a new policy which aimed to strengthen HIV counseling and testing through a higher number of voluntary testing centers and the implementation of a mobile testing strategy [29]. Access to HIV testing has increased significantly with the introduction of community-based testing through rapid tests [30]. Of the estimated 20,000 people living with HIV in 2017, 70% were aware of their HIV status (versus 22% in 2010) [31]. This good result illustrates the need for sustained community-based HIV testing by lay providers to reach MSM and FSWs, who are still the populations most vulnerable to HIV infection [32, 33], and people in rural areas. To further strengthen and extend HIV testing services and overcome barriers to HIV testing, testing could be proposed in pharmacies to reach a large population given that pharmacists were consulted by 31% of our study population. The future implementation of self-testing in Morocco could also help to reach high-risk population groups, especially in a context of homosexuality and HIV stigmatization [34]. In addition, to curb the epidemic, the HIV testing strategies should be completed with strategies like treatment as prevention (TasP) or pre-exposure prophylaxis (PrEP) to prevent onwards transmission.

In Morocco, among people who were unaware of their HIV infection and sought care, many opportunities for HIV testing, based on at-risk behaviors or clinical indicators, were missed. This highlights the need to improve the recognition of HIV clinical indicators by physicians, further expand community-based HIV testing by lay providers, and implement self-testing to increase accessibility and privacy.