Many mental, neurological, and substance use (MNS) disorders are more prevalent among people living with HIV infection (PLWH) than among non–HIV-infected persons, adding to disability and poor quality of life.1 Several MNS disorders also directly or indirectly increase the risk of HIV treatment failure, and some also increase the risk of HIV acquisition2,3 (Fig. 1). A focus on MNS is thus fundamental to addressing both the risk of contracting HIV and health outcomes for PLWH. This article will focus on 3 conditions considered to be high-priority MNS disorders by the World Health Organization (WHO)4: depression, alcohol use disorder (AUD), and neurocognitive disorders.
There is evidence that in low- and middle-income countries (LMICs), all 3 are more prevalent among PLWH than among the general population1,5 and that in these countries, the disorders predict worse HIV clinical outcomes for PLWH2,6 (Fig. 1). In this article, we review the evidence for the relationship of each of these interlinked conditions to HIV infection, antiretroviral therapy (ART) adherence, and HIV progression in LMICs, and we outline research priorities, making recommendations for interventions using an integrated approach that prevents and treats these conditions in resource-poor settings. Where data are lacking from LMICs, we will draw evidence from high-income countries (HICs).
Because of space constraints, this article will not review HIV MNS comorbidities such as epilepsy, stroke (discussed in this issue's article on cardiovascular and pulmonary diseases by Bloomfield et al7), peripheral neuropathy, psychotic disorders, anxiety disorders, and illicit drugs.
We used a combination of systematic reviews of MNS disorders in PLWH conducted globally since 2005 and epidemiologic studies in LMICs since 1995. We constructed search terms to ensure that we captured studies measuring our 3 conditions of particular interest: depression, alcohol use, and neurocognitive disorder/dementia/neurocognitive impairment. We used LMIC regional names, exploding them when the database allowed and adding developing countries and low-income countries. We searched MEDLINE, EMBASE, PsycINFO, and Global Health databases. We also included literature cited in publications, when relevant.
Depression is the most common psychiatric disorder found among PLWH in LMICs.1,8–10 It adversely impacts the lives and functionality of PLWH and their families6,11,12 but remains mainly undiagnosed because few HIV care settings carry out routine screening.
Depression is defined by diagnostic (Fifth Edition of the Diagnostic and Statistical Manual of Mental Disorders [DSM-V]; International Classification of Diseases, Tenth Edition) or screening criteria based on the number and severity of symptoms and behaviors, including sadness, loss of interest, lack of pleasure, poor sleep, concentration, and appetite, and impaired social and work roles. Screening tools for depression validated in LMICs in the general population are mostly those developed in HICs, such as the Hopkins Symptoms Checklist (HSCL-25) and the Patient Health Questionnaire (PHQ-9).13–18 Challenges of diagnosing depressive disorder in PLWH in LMICs include the overlap in symptoms with HIV infection (eg, fatigue, memory loss, and weight loss)19 and how to take into account locally meaningful symptoms of depression. For instance, in Zimbabwe, Tanzania, Rwanda, South Africa, and Zambia, “thinking too much” is an important symptom of depression19–22 but does not appear in tools such as PHQ-9,23–26 although it is now recognized in DSM-V.27 Somatic symptoms, which are common and can be metaphors for distress, such as having a “heavy heart” (in Zimbabwe), are often attributed to social problems.21,25,28 Cross-cultural methods have been used in a small number of settings, whereby local informants are consulted and indigenous idioms of distress are used to develop screening tools.19,24 However, in the absence of culturally specific tools, international tools are acceptable if they are translated, back translated, and adapted to ensure the meaning stays close to the original and that the questions are understandable. If they are validated, the methods used should take into account local concepts of mental disorder.18,19,25 In Uganda, a visual depression screening tool showed good psychometric properties among PLWH with low literacy.29
Relationship Between Depression and HIV Infection
Data from HICs show that depression is more common among PLWH than in the general population, with an estimated prevalence of 5%–20%.30 However, the magnitude of the association of depression with HIV is difficult to estimate because of variability in diagnostic criteria and measures, lack of appropriate controls, and confounding factors.31 Most studies of depression among PLWH in LMICs consisted of small clinical samples with varying methods of measurement and wide variation in reported prevalence.32 For example, some studies report more than twice the prevalence of depression in PLWH compared with matched non–HIV-infected persons,33–36 and some report a depression prevalence in PLWH of more than 30%.6,20,35,37,38 Two large studies39,40 using internationally accepted diagnostic criteria found a prevalence of major depression of 7%–8% in PLWH. These discrepancies may be due to methodological issues such as sampling and difference in HIV clinical stages. Also, depression symptoms, such as self-criticism, may be part of common reactions to an HIV diagnosis, co-existing severe life events,35 or co-existing cognitive impairment and associated posttraumatic stress disorder symptoms rather than to a depressive disorder.41–44 More than 80% of Zambians recently commenced on ART were found to have anxiety and depression symptoms severe enough to warrant additional intervention or support, and a higher burden of this psychiatric morbidity was associated with early mortality.45
Although the direct effects of HIV on depression are not well understood, studies from HICs have postulated a biological mechanism for depression in HIV infection. For example, HIV virus penetration or HIV-induced exposure to proinflammatory cytokines of the brain's basal ganglia and hippocampal regions can cause depression symptoms such as insomnia, poor concentration, and psychomotor slowing.46–48 These symptoms also overlap with HIV-associated neurocognitive disorders (HAND), prompting some to question whether depression and HAND could be part of the same disease spectrum.49
Depression and ART Adherence
A meta-analysis of 95 independent studies from HICs showed a consistent association between depression and ART nonadherence (P < 0.0001; 95% confidence interval: 0.14–0.25),50 as did 2 systematic reviews in LMICs.2,6 One of the systematic reviews showed that 5 of 6 prospective studies and 3 of 4 cross-sectional studies using multivariate analysis had adjusted odds ratios of 1.13–3.13 for association of depression and 1.75–3.36 for nonadherence to ART.2 Poor adherence to ART at least partially explains the association between depression and increased risk of HIV disease progression.50,51 Immunological effects of depression and stress may also hasten disease progression,52 and risky behavior may confound the association between depression and HIV mortality.53 Corollary effects of suicidal ideation and negative thinking, such as forgetfulness and poor concentration, or deficits in problem-solving that come about through a depressed mood, may contribute to poor adherence.53
Interventions to Address Depression in PLWH
A systematic review of interventions for the treatment of depression in PLWH revealed that psychological and psychotropic interventions were effective, whereas social interventions alone were ineffective.54 In HICs, treatment of depression can also lead to improvements in HIV-related outcomes, especially when they are integrated with adherence interventions that make use of motivational and problem-solving approaches.55,56 The poor availability of antidepressants in most LMICs makes the use of psychotropic interventions a challenge.57,58 Clinical trials of psychological therapies among PLWH in Asia have demonstrated improved depression outcomes.59–62 Psychological therapies require the availability of skilled health professionals, who are not readily accessible in LMICs. However, task shifting approaches in both HIV and non-HIV populations show that lower-level cadres can deliver adapted forms of psychological interventions, which can be escalated to more intense psychotherapy or antidepressants for those who do not recover.63–67 Two studies from sub-Saharan Africa using simple structured approaches based on problem-solving therapy and other cognitive behavioral techniques provided preliminary evidence for the effectiveness of psychological interventions for depression in PLWH.68,69 Expanded provision of antidepressants in Africa, especially low-cost serotonin-reuptake inhibitors such as Fluoxetine, which have fewer side effects than tricyclic antidepressants, needs to be studied to assess their effectiveness.58
One research priority is the development and validation of screening tools for depression that are integrated with screening tools for cognitive impairment and alcohol abuse, particularly for use in primary health care in LMICs. Another key priority is randomized controlled trials (RCTs) of the effectiveness and cost-effectiveness of interventions for depression (Table 2) in HIV care programs in LMICs,70 especially those that can be delivered by lower-level cadres through stepped care or task shifting models.71 Evidence from HICs suggests that problem-solving approaches to ART adherence should be integrated with depression interventions.56
We focused on alcohol use because it is the most abused substance in sub-Saharan Africa, where 70% of PLWH reside globally, making this the substance use problem of greatest public health importance in the HIV population. However, we acknowledge that substance abuse varies by country and that a limitation of this review is that it does not address the occurrence of other important kinds of substance use among HIV-infected individuals.
AUD is defined by diagnostic (DSM-V; International Classification of Diseases, Tenth Edition) or screening criteria that include the pattern of drinking (quantity, frequency, binge drinking) and the consequences of use (eg, harmful drinking or dependence). A commonly used screening test in both HICs and LMICs is the Alcohol Use Disorders Identification Test (AUDIT),72 a 10-item test that categorizes high-scoring patients as hazardous, harmful, or alcohol-dependent drinkers. Alcohol use is the leading risk factor for mortality and disability-adjusted life years in several LMIC regions, including southern Africa, Eastern Europe, and Andean Latin America.73 The prevalence of AUD varies geographically, and many of the LMICs with the heaviest alcohol use burdens also have high HIV prevalence or rapidly emerging HIV epidemics, such as in Eastern Europe, where prevalence of AUD is estimated at 16%. In southern Africa, the region with the highest HIV prevalence globally, more than one third of adults are estimated to be engaged in heavy episodic drinking (defined as drinking at least 60 g of pure alcohol on at least 1 occasion in the past week).73
Relationship Between Alcohol Use and HIV Infection
There is strong and consistent evidence that alcohol use is associated with HIV incidence and prevalence in LMICs. A recent meta-analysis of studies in sub-Saharan Africa identified 35 studies with a summary odds ratio of 1.61 (95% confidence interval: 1.44 to 1.80).74 The association held among both high-risk groups and the general population and was stronger among heavier drinkers. There are several possible mechanisms for this association: the biological plausibility that heavy alcohol use increases susceptibility to and severity of HIV infection through effects on innate and adaptive immune system aspects, the central nervous system (CNS), the liver, and other organ systems; the direct effect of alcohol consumption on cognitive capacity and its disinhibiting effect on behavior, which can affect consistent condom use or the ability to negotiate safe sex; the co-occurrence of alcohol use and risky sexual behavior among individuals with risk-taking personality characteristics75; and the dual character of places that sell alcohol, which are also sometimes meeting spots for potential sex partners (Fig. 1).
Relationship to ART Adherence
In the ART era, the primary predictor of HIV-related mortality, morbidity, and treatment failure is nonadherence to ART.76 Systematic reviews have shown that alcohol use is strongly associated with poor adherence to ART,77,78 with alcohol users being around 50%–60% less likely to adhere to ART than nonusers. For example, a recent study from South Africa found that good adherence was reported by 65% of nondrinkers but only 39.7% of drinkers (P < 0.001).79 Adherence was lower still among hazardous or harmful drinkers (30.3%). The evidence for a causal effect of AUD on ART adherence is strengthened by dose–response and temporal relationships.79–82
The mechanisms by which alcohol consumption reduces ART adherence are similar to those that increase the risk of HIV acquisition, that is, cognitive factors (due to acute intoxication), personality factors (eg, risk taking), structural factors (eg, chaotic environment), and misconceptions about toxic interactions of alcohol use and ART.83 These factors can contribute to poor adherence when alcohol users taking medications off-schedule or missing doses, not renewing prescriptions, or having decreased access to ART.78,84
Interventions to Address Alcohol Use Among PLWH
The primary evidence-based interventions to reduce AUD are structural interventions (eg, comprehensive policy measures to regulate the availability of alcohol and reduce demand through taxation and pricing mechanisms) and individual psychotherapeutic interventions (eg, screening and brief interventions by trained primary health care professionals). There have been few RCTs assessing the effects of psychotherapeutic interventions on alcohol use and ART adherence in HIV-infected alcohol users. One trial found a significant intervention effect on ART adherence and HIV virological and immunological outcomes at the 3-month follow-up, but not at 6 months,82 and a second trial found no significant intervention effects on adherence or virological endpoints.83,85 The difference may have been attributable to key variations between these trials, including the behavior change model used, the intensity and duration of the intervention, the type of counselor, the control condition, and the duration of follow-up. Another RCT found that a motivational enhancement intervention had a significant effect on HIV viral load at 6 months86 among PLWH aged 16–25 years, including a borderline significant reduction in alcohol use. Three other studies have evaluated the effect of motivational interview-based counseling on alcohol use among PLWH with AUD,87–90 but they did not measure ART adherence at HIV-related endpoints. Each of these studies found a large and significant intervention effect on alcohol use (Table 1). Further research is needed to refine and evaluate interventions to improve adherence among alcohol users in LMICs.
Further qualitative studies should be conducted to understand the role of alcohol in HIV acquisition through event-level data (eg, an in-depth examination of alcohol use and sexual activity occurring on particular occasions). Pilot studies are needed that would adapt alcohol-reduction interventions to suit HIV-infected populations in LMICs, followed by RCTs to evaluate the impact of such interventions on ART adherence and disease progression.
HIV-Associated Neurocognitive Disorder (HAND)
HAND is a general term that includes a number of disorders that are complications of HIV infection. The definition is based on the consensus opinion of experts in the field, and patients are diagnosed using a battery of neuropsychological tests.91 The term HAND includes asymptomatic neurocognitive impairment, mild neurocognitive disorder, and HIV-associated dementia.91
HIV-associated dementia is the severe form of HAND. Prevalence in HICs has declined after the introduction of ART.92 HIV-associated dementia is characterized by subcortical dementia, which involves motor and cognitive slowing, with a neuropathology consistent with HIV encephalitis.49 Prognosis is poor and survival is usually less than a year.93
Asymptomatic neurocognitive impairment and mild neurocognitive disorders are the most common manifestations of HAND in the era of ART in HICs.92 This phenotype is characterized by cortical symptoms such as memory loss and seems to be distinct from HIV-associated dementia; however, our understanding of this phenotype is still evolving.49,94 Unlike HIV-associated dementia, milder cognitive disorders are not associated with higher HIV viral load and lower CD4+ T-lymphocyte count, but they are associated with previous cardiovascular disease.92,95 A longitudinal study with a follow-up period of 3 years showed that symptoms were nonprogressive, but the very long-term prognosis is unclear.96 Postulated mechanisms for mild cognitive disorders include direct ART toxicity, chronic immune activation, or immune reconstitution syndrome.97,98 In addition to ART toxicity, the direct and indirect effects of HIV also play a role in cognitive disorders.49
The prevalence of HAND in LMICs varies, ranging from 6% to 64% in children and adults99–106 (Table 1). Not all of the individuals in these studies were on ART, which could partially account for the variation. Other factors that may also explain the differing prevalence rates are people's HIV subtypes, which may contribute to more severe forms of HAND, as seen in some subtypes found in Uganda107,108; the increasing burden of comorbidities related to cognition such as stroke109; demographic, educational, and cultural differences; or differing approaches to measurement of impairment. Because treatment of HIV infection is often delayed in LMICs, the added burden of opportunistic infections mimicking HAND (eg, cryptococcal infection, tuberculosis, meningitis, or neurosyphilis) is also a possibility. Notably, in HICs, the norm is screening non-HIV populations with cognitive impairment for infections like syphilis.110 However, in LMICs, screening is neither routine for non-HIV populations nor for individuals with HAND, which could mean that the burden of HAND is overestimated and that treatable conditions are being neglected.111
Neuropsychological tests are pivotal to the definition of HAND but have several restrictions. First, the diagnosis by neuropsychological tests does not account for disease mechanism. Importantly, it does not differentiate between progressive disease directly associated with HIV infection and nonprogressive disease owing to HIV-associated insult to the brain.49 Including the latter cases could overestimate the milder forms of HAND. Second, neuropsychological tests should have at least the following neurocognitive domains: verbal/language, attention/working memory, abstraction/executive function, learning/recall, speed of information processing, and motor skills. However, the choice of domains used varies between the different tests.112–115 Third, normative data for healthy age- and sex-matched community controls, crucial for the interpretation of neuropsychological tests, are limited in LMICs. Furthermore, these neuropsychological tests should be validated for the target population's culture and language and administered and interpreted by appropriately trained professionals; this is not always the case in LMICs.49,116 Each neuropsychological test varies in length, and weighing the need for lengthy and more sensitive tests versus shorter and more conveniently administered tests is challenging. Currently, there is no consensus on the best approach.112 Although the development of standardized tools is important, linking these tools to biomarkers of HAND would make them dynamic and more specific. Biomarkers for HAND are currently in the process of being identified, and those related to monocyte activation (eg, CD14) have shown promising results.49 Depression and AUD overlap with cognitive impairment (Fig. 1); integrating a screening tool that encompasses both disorders may be an efficient way forward.110 This approach could reduce the time spent screening for these noncommunicable diseases separately in busy and overstretched ART clinics.
Despite the availability of numerous, albeit limited, neuropsychological tools, routine screening in ART clinics in LMICs is still not the norm. This could have important implications for people who have HIV–dementia but are not eligible to start ART based on their CD4+ T-lymphocyte cell count. HIV–dementia is an AIDS-defining illness and justifies starting ART.
Relationship to ART
Overall, ART has been beneficial for HAND in both HICs and LMICs. Eleven of 15 studies in a systematic review in 11 HICs and 4 LMICs showed improvement in neurocognitive status after treatment.111 The studies that showed no association were usually statistically underpowered and sometimes lacked appropriately matched normative data. Although ART may improve cognitive function in those with severe impairment, it does not seem to fully eradicate the milder forms of HAND.33,99,111,117,118
A multinational study evaluated the outcome of neurocognitive impairment and the degree of CNS penetration for 3 ART regimes (including WHO-recommended first-line treatments) in a large randomized trial.119 The study found no differences in the degree of CNS penetration of WHO-recommended ART regimens.119 Minocycline, a neuroprotective agent, was explored as an adjunct to ART in managing HAND in LMICs.120 Although this trial was unsuccessful, this should not discourage future trials from exploring the role of adjunctive neuroprotective/anti-inflammatory agents in reducing the burden of HAND.49
Relationship to ART Adherence
A prospective cohort study in Zambia showed that 495 PLWH who had recently commenced ART had cognitive impairment and poorer ART adherence.45 In HICs, mild neurocognitive impairment was associated with poorer quality of life, unemployment, worse medication adherence, lower driving ability, and reduced survival.121 Furthermore, HAND may also be associated with adverse HIV outcomes, including HIV resistance and poor ART adherence due to prospective memory impairment.122 Alcohol misuse may coexist in patients with HAND, which could also impact on adherence. However, the extent to which these factors play a role in HIV acquisition and disease progression in LMICs has yet to be completely understood.
Of high priority is the development and validation of a standardized neuropsychological test that is resource appropriate, culturally tailored, and includes biomarkers of HAND to improve specificity (Table 2). Well-powered studies with appropriate normative data that examine the effect of ART in a well-characterized cohort (with brain imaging, exclusion of opportunistic infections, and autopsy confirmation of underlying pathologies) are needed in LMICs. Ideally, longitudinal studies should have a follow-up beyond the longest observation period of 3 years to determine the long-term prognosis of HAND in the ART era. In the meantime, screening for HAND needs to be instituted in clinics in LMICs, especially for patients not otherwise qualifying for ART.
Research Platforms and Training Opportunities
Existing research and care platforms could be harnessed to conduct MNS studies. New scientific collaborations could be established, for instance, with Demographic Surveillance Systems, such as those in the INDEPTH Network (www.indepth-network.org), and HIV research centers in LMICs, such as those supported by the UK Medical Research Council, the Wellcome Trust, and the US National Institutes of Health. Opportunities exist for incorporating MNS research into existing HIV research platforms. For example, researchers could use the IeDEA network, AIDS clinical trials group sites, the WHO STEPS surveys, and the African Partnership for Chronic Diseases. Challenges in implementing such research may include the lack of awareness among many HIV researchers, funders, and policymakers of the importance of mental health in addressing HIV/AIDS.
Strengthening research capacity in many LMICs that have exceedingly low numbers of specialists in neurology and psychiatry, a situation exacerbated by the ongoing brain drain, will be important. New initiatives are supporting capacity building in mental health research, particularly the research hubs in Africa, Asia, and Latin America funded by the US National Institute of Mental Health (www.fic.nih.gov/programs/Pages/medical-education), consortia funded through the UK Department for International Development (www.prime.uct.ac.za), and Grand Challenges Canada (www.grandchallenges.ca), which funds projects and rising investigators in global mental health. The US President's Emergency Plan for AIDS Relief/National Institutes of Health–funded Medical Education Partnerships Initiative (MEPI)123 is another potential platform on which to build research capacity in HIV mental health and neurology in Africa. Existing initiatives such as Fogarty International Center fellowships (http://www.fic.nih.gov/programs/pages/scholars-fellows.aspx) and Wellcome Trust international training fellowships (www.liverpoolwttc.org.uk) also fund research and training of investigators in global mental health and neurology. At an institutional level, mentorship schemes are needed to pair clinical academics in psychiatry and neurology with centers requesting support. Examples of specific training priorities include grant writing, qualitative methods, formative research, cross-cultural methods in psychiatry, clinical trials training, database management, and biostatistics.
CONCLUSION AND RECOMMENDATIONS
Addressing the burden of MNS conditions among PLWH in LMICs will contribute significantly to health, social, and economic outcomes as ART is scaled up. We focused this review on the 3 key MNS conditions most prevalent in HIV populations in LMICs, based on the current literature. Epilepsy, stroke, peripheral neuropathy, psychotic disorders, anxiety disorders (including post-traumatic stress disorder), and illicit drug use are other MNS conditions that we did not discuss in this review, but that are important areas for future research in LMICs.
Depression, AUD, and HAND contribute to poor HIV outcomes and are interlinked. Research is needed that improves our understanding of the underlying mechanism of these overlapping conditions. One research priority is to determine an integrated screening approach for depression, AUD, and neurocognitive disorders that can be used by nonspecialists in LMICs. Such a tool should ideally achieve a balance between time, skill needed to administer it, and the validity of the test. Another research priority is testing depression and AUD interventions that also target behavior change, as these could have an impact on ART adherence, accessing health care, and the improvement of mental symptoms. RCTs of such interventions, preceded by culturally informed formative work, are urgently needed.
Limited access to psychiatrists and neurologists in LMICs has been a long-standing issue; mentorship and fellowship schemes at an individual and institutional level do exist, but they need to be further supported. In the short-term, task shifting in the care of MNS disorders in HICs and LMICs has been successful and should be integrated into routine HIV care in LMICs.
The authors would like to thank Jessica Healy for her help with the literature search and Dr. Sam Nightingale for helpful discussions on the HAND section.
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