Missed opportunities for HIV testing in newly-HIV-diagnosed patients, a cross sectional study

In the past decade in developed countries, highly active antiretroviral therapies have dramatically decreased HIV infection morbidity and mortality [1‐3]. When HIV care is initiated early, patient’s life expectancy becomes closer to that of the general population [4, 5]. More recently, compelling evidence has demonstrated benefits of early treatment of HIV-infected patients for the global population by reducing HIV transmissions [6, 7]. Consequently in some countries like US or France, treatment guidelines have moved toward initiating earlier HIV therapy, i.e. at CD4 cell counts <500/mm³[8‐10]. However, most patients are diagnosed long after the optimal moment of treatment initiation. Recent studies estimated that approximately 30% of people living with HIV in Europe are unaware of their infection [11]. Other studies, mostly from western Europe, estimated that 24-39% of HIV-infected patients presented for care at an advance stage of the disease (with AIDS and/or CD4 cell count <200/mm³) [12‐19]. Late diagnosis compromises benefits of antiretroviral therapies.

In most European countries, risk-factor-based HIV testing strategy alone shows limits to detect HIV-infected people because 1) people do not consider themselves at risk and 2) healthcare providers fail in risk assessment [20‐24]. In line with the US CDC recommendations [25, 26], in 2008 the UK guidelines stated that HIV screening should be considered in general practice and for all general medical admissions in regions where HIV prevalence exceeds two per 1,000 [27]. In 2009, new French guidelines recommended one-time routine voluntary HIV screening to be implemented population-wide in France [28, 29]. However, these recommendations are not applied because of feasibility and budget impact issues [30‐32].

Few studies have evaluated patient consultations during the possibly-HIV-infected period [22, 33‐36], and the bulk of them were carried out in the US or the UK. To assess the situation in France, the objectives of the present study conducted in newly diagnosed HIV-infected patients were to describe: 1) in all patients, frequenting of healthcare settings prior to HIV diagnosis during the period in which they were likely to be HIV-infected; and 2) in at-risk populations (MSM) and patients with possibly HIV-related conditions, opportunities for testing proposal and consequently earlier HIV diagnosis.

During the study period, 2,009 newly diagnosed HIV-infected patients sought care in the 69 participating centers throughout France. Overall, 659 (33%) were excluded because they did not fulfill inclusion criteria: 288 had been living in France for <1 year, 95 had had the initial HIV-positive test performed abroad, 148 sought care ≥6 months after HIV diagnosis, 18 were aged ≤18 years, and 110 were excluded for other reasons (mainly because they did not speak French). The study was not proposed to 227 patients mainly because of time pressure and lack of availability of care providers, and 115 more patients refused to participate in the study. Finally, 1,008 patients (50%) were enrolled. The overall 2,009 patients who sought care in study centers were not different from newly diagnosed HIV-infected patients in France during the same period [42] in terms of sex, age, clinical or immunological characteristics at HIV diagnosis (Table 1). However, the 1,008 patients enrolled in the study were more frequently men, older, born in France, diagnosed during acute HIV infection when compared with patients not enrolled.

This study, which included more than one thousand newly HIV-diagnosed patients in France, demonstrated that 99% of the patients had had at least one medical encounter during the 3-year period prior to HIV diagnosis, and 89% had seen a general practitioner at least once a year during that period. Moreover, results revealed the high proportion of missed opportunities for HIV testing among MSM and those seeking care for possibly HIV-related conditions. Seventy nine percent of overall MSM who visited a healthcare provider did not receive an HIV test proposal. Likewise, HIV testing was not proposed by the healthcare provider to 82% of patients who sought care for possible HIV-related conditions upon first contact.

This study had some strengths and limitations. We enrolled 1,008 newly-HIV-diagnosed patients, who accounted for 16% of new HIV diagnoses in France during the same period [19]. Enrolled patients were not representative of overall newly HIV diagnosed patients because of eligibility criteria. In order to study missed opportunities possibly occurring in France, patients diagnosed overseas or living in France for <1 year were excluded; hence, migrants were underrepresented (27% vs. 47% recorded in 2009 French surveillance data [42]) and MSM were overrepresented (53% vs. 38% recorded in 2009 French surveillance data [42]). Migrants were more likely women, young and being diagnosed for HIV at chronic or advanced stage of HIV infection [42] that explains difference in enrolled and non-enrolled patients. However, characteristics of overall patients were close to those of French surveillance data, and our study sample may be representative of patients who acquired HIV in France.

We evaluated the patient course through the healthcare system in the years prior to HIV diagnosis. That may be subject to recall bias, leading to an underestimation of the number of missed opportunities. To limit this bias, patients diagnosed >6 months previously were excluded, and the period during which retrospective data were collected was restricted to three years. Another limitation may be the misperception of being tested. On one hand, some patients may be tested without knowing the test was performed, without the consent process, leading to overestimate missed opportunities proportion. On another hand, some patients may think having been tested for HIV because a blood analysis was performed during an inpatient stay for example, which may this time, underestimate missed opportunities proportion.

In MSM or patients presenting with possibly HIV-related conditions, we determined whether an HIV test was proposed upon first contact with the healthcare setting. This may underestimate the HIV test proposal rate, since HIV infection may be brought up at the second or a later visit. First, the effect of this bias was reduced by accounting only for visits that had occurred >3 months before HIV diagnosis, ensuring these events did not lead to HIV diagnosis. Next, a high proportion of patients with missed opportunities for HIV testing did not undergo any other HIV test prior to the test that diagnosed the HIV infection.

Only a few asymptomatic people belonging to a high-risk group other than MSM, i.e. sub-Saharan African migrants or heterosexuals with risky sexual behavior, were enrolled in the study and therefore we could not determine missed opportunities for them.

Our results are cause for concern and are in agreement with those reported in the medical literature that overall estimated high proportions of missed opportunities for HIV testing. However, a comparison of our results with other studies on the topic is difficult. Our study is unique in that it investigated the overall patient trajectory though the healthcare system; thus, it evaluated HIV testing strategies based on risk factors and symptoms such as applied currently. Most other studies [22, 33‐35, 43] were conducted in the US at single large urban medical centers with designs based on retrospective medical chart reviews; opportunities for testing that might occur in other facilities could not be collected [22, 34, 35], thereby underestimating missed opportunities for HIV testing in those studies compared to ours. The population enrolled in other studies was also different from ours in that they focused on specific subgroups; for example, late presenters [33], patients attending STI clinics [36] or immigrants [44]. Moreover, they used different definitions of a missed opportunity. Some authors defined a missed opportunity for testing in newly HIV-diagnosed patients as any medical appointment in the years prior to HIV diagnosis [44]. Others added to this definition the notification of HIV-related risks and/or clinical events (with events varying from one study to another [22, 34, 36]). Very few authors coupled the presence of HIV-related risks and/or clinical events with the absence of a test proposal by the care provider, which is the definition that we used [35]. As a result, the proportions of missed opportunities for HIV testing in the medical literature range from 20 to 80%.

Our study illustrates the failure to identify persons at high risk of being HIV-positive. In the past three years, >80% of the 191 asymptomatic MSM had seen a healthcare provider. However, only 48% of them informed the provider, either spontaneously or upon questioning, that they belonged to a risk group. Indeed, patients may be wary of the healthcare setting, fearing moral judgment of their behavior, leading to unwillingness to disclose sexual practices to care providers [45]. They may also not consider themselves at risk of HIV infection. This is the main reason why people do not test for HIV, according to a recent systematic literature review summarizing barriers to HIV testing in Europe [21]. In addition, healthcare providers themselves may be ill at ease when dealing with sexuality and behavior risk assessment [46, 47].

Even in patients identified as being at high risk of HIV infection, our study illustrates the failure to propose an HIV test: only one test proposed out of two MSM identified. Barriers to HIV testing on the part of the healthcare provider include a lack of training in HIV testing and a lack of self-confidence when proposing it [21]. The consent process and counseling requirements have been reported to be burdensome, particularly for general practitioners [20].

Thus, these findings suggest that risk-factor-based HIV testing is insufficient because its application is insufficient. In this situation, routine HIV testing may be attractive because it does not need risk assessment and follows an opt-out process. However, in US as in France where it is recommended, it is not widely applied because of implementation difficulties, and high costs [30‐32, 48]. Haukoos et al.[49] have recently proposed a score to identify people at risk of being HIV-infected based on eight demographical and behavioral items. Although this score require a minimum of risk assessment and may need validation for French population, it is a starting point to re-think routine HIV testing, and highlight specific populations at risk for HIV to be tested such as men. Routine screening can also be restricted to high prevalence geographical areas.

In patients with STIs, a test was only proposed to one out of two patients although a STI diagnosis is an indication for an HIV test [24, 28]. In patients with other HIV-related conditions who sought care, frequencies of missed opportunities were even higher, as high as 98% for those with recurrent bacterial infections. We found that patients who did not receive a test proposal had been diagnosed with significantly lower CD4 cell counts than patients who were proposed a test. This confirms that patients without a test proposal were probably HIV-infected when they consulted and thus had had a loss of chance of being diagnosed and entering into care. It is crucial to bring to healthcare providers this kind of evidence regarding HIV testing for them to improve their knowledge about HIV-related conditions and thus to increase the proportion of patients tested for HIV. An European study has been currently conducted to assess the prevalence of undiagnosed HIV infection in patients with some particular HIV indicator diseases (e.g. mononucleosis-like illness or malignant lymphoma); results show HIV prevalence above 1% in patients with these HIV indicator diseases [50]. This is another argument to convince healthcare providers of the importance of testing proposal for patients with HIV indicator diseases.

This study illustrates that the rate of missed opportunities for HIV testing remains unacceptable and highlights the low efficiency of risk-factor- and symptom-based HIV testing as it is currently applied. We must therefore reinforce and implement new HIV screening strategies. Testing initiated by the healthcare provider should be promoted. Because risk-factor based testing is not sufficient, routine screening should be considered in particular in high prevalence geographical areas and/or specific populations. In our study, most persons had contact with healthcare facilities and particularly general practitioners who should play an important role in future HIV testing strategies. But we must train physicians to better recognize HIV-related conditions and develop tools such as behavioral and clinical instruments to better identify those at high risk of HIV infection in whom HIV testing should be regularly performed. HIV testing has become a major tool and the basis of the new prevention strategies such as the Test and Treat strategy; it should be promoted urgently.

The study received approval from two French data protection authorities (CCTIRS, Comité Consultatif sur le Traitement de l’Information en matière de Recherche dans le domaine de la Santé, and CNIL, Commission Nationale de l’Informatique et des Libertés) and did not requite formal ethical approval according to French regulations. All patients signed an informed consent form before taking part to the study.