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Despite tremendous advances in HIV care and increased funding for treatment, morbidity and mortality from HIV/AIDS in developing countries remains unacceptably high. A major contributing factor is that globally over 800 million people remain chronically undernourished and the HIV epidemic largely overlaps with populations already suffering from low diet quality and quantity. We present an updated review of the relationship between HIV, nutritional deficiencies and food insecurity, and consider efforts to interrupt this cycle at a programmatic level. As HIV infection progresses, it causes a catabolic state and increased susceptibility to infection which are compounded by lack of caloric and other nutrient intake, leading to progressive worsening of malnutrition. Despite calls from national and international organizations to integrate HIV and nutrition programs, data are lacking on how such programs can be effectively implemented in resource-poor settings, on the optimum content and duration of nutrition support and on ideal target recipients.
Morbidity and mortality related to HIV infection in the developing world remain unacceptably high, despite major advances in HIV therapy and increased international funding for care [1, 2]. People living with HIV infection (themselves or among family members) face not just sickness, but also impaired productivity, declining income, and increasingly difficult choices among essential but competing expenses, such as food versus healthcare or schooling versus rent . The physiological complications of HIV progression are compounded by the problems associated with poverty as it translates into insufficient consumption of a diet of adequate quality and quantity to bolster immune function and support medical therapy. Recently, several international agencies emphasized that targeted nutrition interventions should be systematically linked to antiretroviral interventions [4-11]. The World Bank has called for a scaling up of action on nutrition and AIDS through ‘action research’ and ‘learning by doing’ . A recent review of nutrition approaches within HIV programs in Africa concluded that current HIV/AIDS ‘[policies] have tended toward highly medicalized approaches’, and called for ‘a comprehensive approach to link health strategies with community-oriented food-based strategies’ . Despite this, few data exist to help guide the development of effective programs integrating both HIV and nutrition.
Food insecurity, defined as persistent lack of access to adequate food in needed quantity and quality, undernutrition (including deficiencies in micronutrients as well as macronutrients), and HIV/AIDS are overlapping and have additive effects . Over 800 million people worldwide are chronically undernourished and over 33 million are living with HIV infection [1, 2, 13]. Combating undernutrition and HIV/AIDS are two of the eight United Nations Millennium Development Goals to be achieved by 2015 – international targets which form a blueprint for galvanizing priorities for the world's poor. The complex interactions between HIV and nutrition seriously threaten the achievement of these goals.
Advances in the treatment of HIV infection in the last twenty years have resulted in combinations of antiretroviral therapy (ART) that can result in reduced HIV RNA, improved immunologic function and dramatic improvements in health, reductions in morbidity and prolonged life [14-17]. Increased funding has become available for HIV treatment in the developing world and the vast majority of such programs have demonstrated excellent clinical outcomes [18, 19]. Despite this, optimism is tempered by the fact that HIV infection remains a major cause of morbidity and mortality , at the same time as child malnutrition remains the main cause of child mortality across the developing world . The largest burden of HIV disease remains in low- and middle-income countries, where over 2 million deaths due to AIDS occurred in 2007 alone and just 31% of patients requiring ART have access to treatment . Early mortality while on ART is a common feature in many programs, with individuals presenting for care with very advanced disease and multiple co-morbid conditions [18, 21]. Co-morbidities such as tuberculosis, undernutrition, diarrheal disease and malaria are highly prevalent in these areas and all have negative interactions with HIV [22, 23].
Barriers to effective HIV care in the developing world are many, including a lack of trained healthcare professionals, lack of infrastructure and lack of resources devoted to health . The financial cost of care to individuals also has an important impact on HIV care in resource-constrained environments; paying for care has been associated both with worse outcomes and worse adherence to therapy [25-28]. Households, as well as governments, face competing choices for their expenditures: food (often accounting for as much as 75% of total household spending), healthcare and education are frequent competitors . In this context, the complex interaction of HIV, undernutrition and food insecurity can be a critical barrier to effective HIV care, and the development of evidence-based programmatic solutions to these issues becomes essential.
Undernutrition and HIV status have negative feedback loops, with severe impacts on the resilience of individuals, households, and communities. Such interactions manifest at the level of the HIV-infected individual as well as at the level of affected households in terms of clinical, nutritional, quality of life and economic outcomes.
At the individual level, a lack of access to appropriate foods and the direct effect of HIV on impaired metabolic functions in absorption, storage and utilization of nutrients, can translate into compromised immunity, nutrient deficiencies and increased vulnerability to infectious diseases [29, 30]. Lack of sufficient food intake and/or malabsorption lead to weight loss, which further exacerbates the catabolic nature of HIV infection [31, 32]. Weight loss is itself a significant, independent risk factor for AIDS-related mortality and HIV-associated wasting often persists even with use of ART [33, 34].
HIV infection reduces the efficiency of nutrient absorption and utilization partly due to frequent diarrhea from compromised immunity [35-37]. Malabsorption of fats and carbohydrates is common, the former adversely affecting the absorption and utilization of fat-soluble vitamins, compromising immunity and worsening nutrient deficiencies . Infections and nutritional deficiencies cause an increase in pro-oxidants, resulting in oxidative stress, which may indirectly accelerate HIV replication . Metabolic changes, including changes in insulin and glucagon, result from both reduced food intake and the immune response to infection and may lead to muscle wasting . HIV infection increases resting energy expenditure as a function of HIV load, people living with HIV have higher protein requirements than their non-infected counterparts [35, 37-40] and HIV-infected children suffering from weight loss have energy requirements 50-100% above normal . ART itself increases resting energy expenditure, independently of viral load, further contributing to HIV-associated weight loss [33, 39]. As HIV progresses, it can cause a catabolic state which is compounded by lack of caloric intake, increasing the severity of pre-existing undernutrition [30, 32, 41]. In children, advanced HIV infection often presents with clinical features that are indistinguishable from severe undernutrition . These facts further highlight the particular need to ensure adequate caloric and multivitamin intake in adults and children with HIV infection.
Of critical importance is the growing recognition that individuals on ART face serious drug side-effects, resulting in lack of adherence, when faced with a lack of food in the household [43-45]. Undernutrition increases the probability of developing hepatic toxicity to nevirapine . Food facilitates the absorption and effectiveness of drugs, and increased appetite is an intended and desirable effect of drug therapy - needed to reverse loss of body mass and promote recuperation and enhanced immune functions [47, 48]. At the household level, a lack of food can lead to the adoption of risky coping strategies, such as sale of assets, redirection of (wage) labor, or exchange of sex for money or food, all of which increase exposure to HIV and increase economic vulnerability [49-51]. Reduced food intake in the HIV-affected household can also result from loss of income and food production capacity in the family due to labor loss, psychosocial factors, or medication side-effects (such as dizziness and nausea) [36, 37, 52]. ART is difficult to take on an empty stomach, travel to a health facility may become impossible due to weakness and lethargy; time in the fields or at work cannot be spared for medical visits; migration in search of work impacts continuity of care [53, 54]. In other cases, assets are sold to pay for medical care or children are removed from school due to lack of funds or need for additional labor, leading families into worsening cycles of poverty [55, 56]. A lack of access to food drives families into social crisis, migration and displacement that subsequently puts them at increased risk of HIV infection and its consequences [53, 57]. High HIV prevalence rural communities may face aggregate reductions in local food supply and increased labor costs . The result of these interactions is a series of ripple effects extending far beyond the infected individual to the household and societal levels . The overall loss of productivity contributes significantly to hunger and poverty for families and communities. The total economic loss from HIV/AIDS worldwide is estimated at US $25 billion per year and rising .
In other words, HIV/AIDS substantially complicates the already multi-dimensional problem of global undernutrition and undernutrition in turn complicates the global fight against the HIV epidemic [36, 55].
Targeted food and nutrition assistance to individuals with HIV infection (and their family) has the potential to improve nutrition [10, 61] and may decrease susceptibility to HIV infection [36, 49, 61, 62]. Targeted food rations, for example, may allow infected individuals to improve adherence to therapy, while preserving assets by not having to sell possessions to purchase food . In the US, nutrition interventions to prevent weight loss and wasting in HIV patients have often focused on counseling and nutrient supplements, rather than food rations, to increase energy and protein intake [47, 63]. Many have been shown to be very successful [47, 64]. Interventions that seek to enhance mothers' nutrition knowledge and behaviors have been recognized for decades as valuable for child nutrition [65, 66]. Although techniques and message content vary widely across programs, communicating specific nutrition information is consistently associated with positive outcomes . Targeted food interventions may also enable increased labor supply and the productivity of that labor, the benefits of which might include increased home production of food as well as increased wage earning, both of which contribute to household food security. In other words, food and other nutrition assistance programs have the potential to improve the course of HIV disease in developing country settings, where undernutrition and food insecurity are major coexisting factors.
While agreement is growing that nutrition support is beneficial, the optimal form of such support remains unknown and largely unstudied . A recent training manual developed in Ethiopia asserts that food-based approaches to increasing vitamin and mineral intake and optimizing immune function are ‘the most preferred strategy’, and that foods should include local vegetables and fortified staple products [69, 70]. However, there is no international consensus on a ‘universal HIV food ration’, making it difficult to determine programmatically what any food basket should contain [70, 71]. It is increasingly argued that more attention is needed on the importance of complementary community outreach in tandem with food - that is, seeking to empower care-givers or individuals by imparting tailored knowledge about causes and solutions to these conditions.
A growing focus of attention in food support has recently been on the use of ready-to-use-therapeutic foods (RUTFs), particularly on spreads that are semi-solid variants of F100 therapeutic milk – a milk formulation used for the treatment of severe childhood malnutrition. The most widely used spread is a mixture of milk powder, sugar, vegetable oil, peanuts, vitamins, and minerals – an energy dense product that resists bacterial contamination and requires no cooking [72, 73]. Providing an RUTF for HIV-infected individuals, as well as food aid rations to affected family members, appears to have potential for nutritional gains across the household. The RUTF adds a nutrient dense supplement that can be targeted to the HIV-infected individual, with other foods in the basket serving to buffer other family members from consumption inadequacy. Significant impacts on morbidity and nutrition outcomes have been shown by the use of fortified blended foods as well as RUTF among refugees in Algeria [74, 75], Nepal , Bangladesh , and Zambia . In Angola, anemia prevalence in children decreased from 48% to 24% in a period of 12 months, while vitamin A deficiency in adolescents was reduced from 47% to 20% . RUTFs are also increasingly used in HIV programs [80, 81].
Despite current understanding of the complex interactions between HIV infection, food intake and low income, the quantitative clinical benefits of food assistance to individuals with HIV infection, the appropriate enrollment criteria for targeted food programs, appropriate duration of food assistance, and the effects of such programs on household members remain largely undocumented [82-84]. A recent Cochrane Systematic Review reported that, based on the current evidence, no conclusions could be drawn regarding the impact of macronutrient supplementation on morbidity and mortality of people living with HIV . A pilot study of food ration supplementation in Zambia suggested that food assistance is associated with better adherence to ART, however did not observe a significant impact on weight gain or CD4 count. This may be attributable in part to a small sample size; the authors call for a large, randomized study to demonstrate clinical outcomes of food supplementation . Prevention of any unintended adverse effects of food assistance is also important. Although data are lacking on the incidence of refeeding syndrome among those with severe HIV wasting, these individuals may be at risk for potentially fatal shifts in fluid and electrolyte balance during rapid refeeding [87, 88]. In addition to the direct health benefits of food assistance on the individual, attention must also be paid to the effects of the interventions on households – on labor productivity and other measures of broader household welfare. Understanding these effects will be critical to effective sustainable food program development [68, 89].
The detailed discussion of interventions other than assistance in the form of food rations is beyond the scope of this review; however, the role of such potentially complementary interventions – agricultural interventions, socioeconomic assistance, accompaniment, education and training [59, 90-92]– are of the utmost importance and need critical consideration in an effort to improve the livelihoods of people living with HIV and food insecurity.
Efficient targeting of food assistance is critical for management of scarce resources, but few data exist to guide programs on which individuals or households to target in locations where there is both high food insecurity and high prevalence of HIV infection. Often programs are targeted to individuals on ART, but it is also highly plausible that food assistance would benefit those not yet requiring ART, potentially preventing progression of HIV disease and delaying the need for ART. It is not clear how food or other nutrition support (supplements or nutrition education) are shared within families. Households are not unitary decision-making bodies; foods are shared and allocated differently within different types of households depending on demographic composition, who within the household is sick or has died, social standing, socioeconomic status and other factors . Understanding the differing bases for sharing food is critical to improving the targeting of ‘therapeutic’ foods versus foods intended for general household consumption [70, 94, 95].
Quantity of calories is important, but so is quality in terms of the nutrient components and mixes within food baskets. There is growing scientific consensus that food ‘sufficiency’ is a critical component of the treatment of both malnutrition and malnutrition-mediated disease outcomes, and that sufficiency requires close attention to diet quality, not merely quantity or adequacy. However the optimal composition of food support for HIV-infected individuals has not been established and has rarely been studied in resource-poor settings. Furthermore, food rations require resources, but few data exist on the cost-effectiveness of nutrition interventions in the context of HIV care in developing countries [96-98]. This may differ substantially from that of more general studies of the returns to nutrition interventions [47, 99]. By further linking clinical and nutritional effects of food interventions to determinants of household welfare, one could extend understanding of the benefits of both to HIV-infected individuals and their household members.
There is considerable debate and uncertainty over the nutritional and health impacts of ‘generic food rations’, which are used for many programmatic purposes around the world. Their role in preventing starvation in emergencies, or buffering household level consumption among the very poor, is clearly important, but not only do those programs have different objectives than food assistance programs for chronic disease such as HIV, the nutritional impact of so called ‘standard’ rations has been questioned [100, 101]. For example, in Haiti, recent research demonstrated that one of the common ‘nutritionally-enhanced’ components of World Food Programme (WFP) rations - a micronutrient fortified corn-soy blend - had little or no impact on childhood anemia unless further fortified with a form of powdered micronutrient mix added to the food at the time of serving . Thus, WFP and other food assistance agencies have argued strongly of a need for more insight into appropriate food formulations and nutrition packages that may achieve measurable nutrition and health outcomes in the context of HIV programs [89, 103].
In addition to direct health benefits on individuals and their households, economists have long proposed the possibility that increased caloric intake and improved nutritional status may lead to higher wages and labor productivity (i.e., the ‘efficiency wage hypothesis’) . Strong empirical support for this hypothesis has been established in countries as diverse as Sierra Leone  and India . As the labor force in high HIV prevalence countries becomes depleted by disease, with potentially devastating economic consequences , understanding and measuring the productivity cost of HIV and how food supplementation may affect it is also critical in designing public health responses.
HIV infection is a global public health emergency and is most prevalent in areas of the world where undernutrition is also a serious concern. The concept of enhancing access to food among undernourished people, regardless of HIV status, is longstanding; however critical questions remain on the most effective ways to incorporate nutrition effectively into HIV programs. The differentiation between food and nutrition must be emphasized, as must the concept that quantity of food is not synonymous with nutritional value. This has been less of a focus due to the urgency of the situation and the reflex to get whatever food is available to those who are hungry in emergencies. The negative interactive effects of undernutrition, inadequate food consumption and HIV infection demand special focused efforts to ensure that effective, cross-sectoral solutions are devised and implemented.
This work was supported in part by National Institute of Allergy and Infectious Disease (K23 AI063998 to LCI; K24 AI062476 to KAF) and by the Harvard Center for AIDS Research (P30 AI060354-02S1).
Potential conflicts of interest: L.C.I., K.A.C, S.B., K.A.F., P.W., and J.C.: no conflicts.