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Micronutrients and Human Immunodeficiency Virus Type 1 Disease Progression among Adults and Children

  1. Fawzi Wafaie
  1. Departments of Nutrition and Epidemiology, Harvard School of Public Health, Boston, Massachusetts
  1. Reprints or correspondence: Dr. Wafaie Fawzi, Dept. of Nutrition, Harvard School of Public Health, 665 Huntington Ave., Boston MA 02115 (mina{at}hsph.harvard.edu).
 
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Abstract

The results of randomized trials among men and nonpregnant women have confirmed the potential benefits of vitamins B, C, and E supplements on the immune status of human immunodeficiency virus (HIV)–infected individuals. Larger trials are needed to ascertain whether these benefits are sustained and to examine the effect of supplementation on clinical outcomes. Among pregnant women, vitamin A supplements increase the risk of mother-to-child transmission. Supplementation with vitamins B, C, and E during prenatal and breastfeeding periods should be encouraged, in light of the protective effects on adverse pregnancy and child outcomes. In children aged >6 months, vitamin A supplements are beneficial for reducing morbidity and mortality in developing countries, including among HIV-infected children. There are no data on the relationships of other micronutrients and child health. For adults and children, more research is warranted on the role of selenium, zinc, and other trace elements on various measures of health among HIV-infected individuals.

As of the end of 2001, ∼40 million people were living with HIV/AIDS [1]. New infections totaled 5 million in 2001; of these, 1.8 million were in women, and 800,000 were in children. Of the 3 million HIV-related deaths during the same year, about one-fifth occurred in children aged <15 years. The most heavily affected geographical region is sub-Saharan Africa, which is home to ∼70% (∼28.1 million) of the world's total number of persons with HIV/AIDS. Furthermore, by the end of 1999, sub-Saharan Africa accounted for 92% of all children orphaned by AIDS. South/Southeast Asia is home to ∼6.1 million persons with HIV/AIDS and is at risk of substantial increases in HIV infection rates, because the epidemic is reaching heavily populated areas that have previously been little affected. Considerable increases in HIV infection rates have recently been observed in Eastern Europe and Central Asia, where the spread of the disease is driven mainly by injection drug use.

Micronutrient malnutrition is prevalent in many developing countries and may contribute to a weakening of immune status and, thus, a worsening of clinical condition among HIV-infected individuals. In the present review, the potential roles of micronutrients in slowing HIV-1 disease progression are examined. Studies of varying designs and using different measures of clinical or immunological or virological status were done in a number of geographical locations, to examine the importance of vitamins, selenium, and zinc. Less research has been conducted to assess the role of iron status; however, limited published data provide contradictory evidence and are reviewed separately [2]. In the present review, findings from studies among adults will be reviewed first, followed by those among children.

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Micronutrients and Disease Progression Among Adults

According to the results of cross-sectional studies, low biochemical indices of individual vitamins were more prevalent among HIV-infected persons than among HIV-negative persons [3–5]. Blood selenium levels and glutathione peroxidase activity were lower in HIV-infected individuals, compared with uninfected individuals [6, 7]. These cross-sectional studies were limited by the difficulty in determining the temporal relationship between infection and nutritional deficiency. Prospective observational studies and randomized trials have addressed this limitation. Findings from these studies are summarized in table 1.

Table 1
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Table 1

Relationships between micronutrient status and HIV-1 disease progression among adults and children.

In longitudinal studies, nutritional status was assessed either by using a biochemical marker of the nutrient or by measurement of the dietary intake of that nutrient using food-frequency questionnaires. In data from asymptomatic HIV-positive individuals, higher intakes of individual micronutrients (including vitamins B and C) and multivitamins were related to better outcomes in terms of CD4 cell counts, clinical progression to AIDS, and mortality [8–10]. Low serum levels of vitamin B12 and E were also prospectively associated with HIV disease progression [11–13].

In a prospective observational study among US adults, low plasma levels of vitamin A were associated with significantly higher risks of death over the duration of follow-up [14]. Results from 2 other prospective studies, however, raised concerns about the potential adverse effects of vitamin A in HIV infection. In a study among HIV-1–negative Kenyan men, lower plasma vitamin A levels were associated with a decreased risk of HIV-1 seroconversion [15]. In another prospective study among HIV-infected men in the United States, a U-shaped relationship was observed between dietary vitamin A intake and the risks of progression to AIDS [10] and mortality [11], which suggests that men with higher or lower levels of intake were at higher risk than men who consumed moderate amounts of vitamin A. It was suggested that vitamin A supplements may increase the risk of transmission of HIV-1 by enhancing the differentiation of myeloid and lymphoid cells, which is associated with an increased expression of CCR5 receptors that increase the susceptibility to HIV-1 infection [15].

Among trace elements, the relationship of selenium and zinc levels to outcomes were examined. Low serum selenium levels were associated with significantly higher risks of mortality and the occurrence of AIDS-defining opportunistic infections [16, 17]. The reported relationships of zinc and HIV-related outcomes were not consistent across studies. In the San Francisco Men's Health Study, the dietary intake of zinc was positively related to CD4 cell count but not to progression to AIDS [8]. In the Multi-Centered AIDS Cohort Study, dietary zinc intake was associated with an apparent increase in the rate of progression [10] and mortality [11]; in contrast, patients who progressed to AIDS in the same study population had significantly lower serum zinc levels than nonprogressors and HIV-negative subjects [18]. In another prospective study, a normalization of zinc levels over the period between clinic visits was associated with higher CD4 cell counts among men [12].

Observational studies are not without limitations. In several of them, the results were adjusted for potential confounding by baseline signs and symptoms and immunological surrogates such as CD4 cell counts. However, residual confounding is still a possible explanation for the findings [19]. All of the studies were done among prevalent cohorts of HIV-seropositive persons; hence, the duration of infection was not known and was therefore not adjusted for in the analyses. The biochemical studies were limited by the fact that low serum vitamin A, zinc, or selenium levels among individuals with infection do not necessarily indicate the poor status of these nutrients, because low levels may be part of the response to infection.

A few randomized, placebo-controlled trials have examined the role of nutritional supplements. More details of the design and results of these trials will be provided, given that they are least confounded and provide the best opportunity to understand the role of micronutrients. Daily β-carotene supplements of 180 mg provided for 1 month resulted in a small but statistically significant increase in the total WBC count and percentage change in CD4 count in one trial [20]. Another trial, however, found no beneficial effect [21]. Those authors suggested that the fact the all of the individuals in the latter trial had received 5000 IU of vitamin A may have reduced the chances of detecting any beneficial effect of the supplements.

The effects of micronutrients on markers of disease progression among adults were examined in a randomized, double-blinded, placebo-controlled trial in Tanzania [22]. Pregnant women (n = 1078) were randomized to receive vitamin A and/or multivitamins (including vitamins B, C, and E), using a 2 × 2 factorial design. Daily doses in multiples of the recommended dietary allowance were provided. Taking multivitamins resulted in a significant increase in the CD4+ and CD8+ cell counts that was sustained for at least 10 months of treatment. Hemoglobin levels at the time of delivery (after ∼4 months in the trial) were also significantly increased. In the same study, vitamin A alone did not significantly affect any of these outcomes. In another trial, in Canada, daily megadoses of vitamins C and E provided for 3 months resulted in a clinically important reduction in virus load that was of borderline statistical significance [23]. The relevance of the findings of the latter 2 trials in terms of clinical progression of HIV disease has yet to be determined.

In a randomized placebo-controlled study from Zambia, the effects of 2 weeks of oral daily supplements of multiple micronutrients (vitamins A, C, and E, selenium, and zinc) were examined among HIV-infected patients with persistent diarrhea [24]. All patients were also given albendazole. Micronutrients did not reduce the duration of diarrhea or the mortality rate during the first month and had no effect on CD4 cell counts or hematological parameters.

Finally, 3 randomized, placebo-controlled studies in the United States [25, 26] and South Africa [27] examined the effect of vitamin A supplements on virus load. A single large dose of 200,000 IU of vitamin A was not associated with a change in HIV-1 virus load in the 2 studies in the Unites States. In the South African trial, there was no effect on virus load of daily doses of vitamin A and β-carotene supplements that were provided to pregnant women between 28 and 32 weeks of gestation and delivery. The effect of vitamin A supplements given over longer periods than in these trials has not been examined.

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Micronutrients and Disease Progression Among Children

Cross-sectional studies among children have similarly indicated that biochemical micronutrient deficiencies are more prevalent among infected children than among uninfected children [28–30]. In an observational study, low baseline levels of plasma selenium were also found to be associated with a statistically significant 6-fold higher risk of mortality in a cohort of HIV-infected children in Miami [31]. As was mentioned earlier, these study designs have limitations such that one cannot exclude the possibility of alternative explanations to the findings in favor of a protective role of micronutrients.

Other than vitamin A, no randomized trials have examined the efficacy of micronutrient supplementation in children born to HIV-infected mothers. Intervention trials with high-dose vitamin A supplementation showed impressive reductions in child mortality among children who were presumably not infected with HIV. The results of a meta-analysis showed that substantial reductions (estimated at 23%) in the mortality rate in children aged >6 months could be accomplished with vitamin A supplementation [32]. Vitamin A supplements also resulted in improvements in health outcomes among children hospitalized with measles and other common infections of childhood [33]. Three trials examined the efficacy of vitamin A in the context of HIV infection among children. In a study among children in Tanzania, periodic supplementation with vitamin A resulted in a large and significant reduction in mortality and morbidity among HIV-infected children [34, 35]. In a placebo-controlled trial in South Africa among children born to HIV-positive women, vitamin A supplements resulted in an ∼50% reduction in diarrheal morbidity among HIV-infected children [36]. Finally, compared with placebo, vitamin A administered to HIV-infected children in South Africa before influenza vaccination did not enhance the vaccine serological response but was associated with a dampening in the increase in virus load associated with the vaccination [37].

The poor micronutrient status of HIV-infected mothers is expected to have an adverse effect on fetal and child health and survival. The risk of mother-to-child transmission of the virus may also be affected, because the mother's micronutrient status may affect various maternal or fetal and child risk factors for transmission, including stage of HIV disease; integrity of the epithelial lining of the placenta, lower genital tract, or breast; prematurity and low birth weight; and the integrity of the systemic and gastrointestinal mucosal immune systems in the fetus and child [38]. In observational data from Malawi [39] and Rwanda [40], higher serum retinol levels in HIV-infected pregnant women were associated with a reduced risk of vertical transmission. Two studies in the United States have provided conflicting results: a low serum vitamin A level was associated with a higher risk of vertical transmission in one study [41] but not in another study [42].

Three randomized controlled trials on the role of micronutrients in the mother-to-child transmission of HIV have been recently completed. In a trial in Malawi, HIV-positive pregnant women were randomized to receive either 10,000 IU of micronutrients or placebo during the prenatal period. The supplements had no effect on transmission at 6 weeks or 12 months or on the risks of prematurity but resulted in an improvement in birth weight [43]. In South Africa, pregnant women who received either preformed vitamin A or β-carotene versus placebo during the prenatal period had a significant reduction in the rate of premature birth, but no effect was noted on birth weight; the supplements had no effect on the risk of HIV infection in infants by age 3 months [44]. In both trials, vitamin A or placebo regimens were given during the antenatal period only. In Tanzania, pregnant women were randomized, using a 2 × 2 factorial design, to receive daily vitamin A and/or multivitamins (excluding vitamin A). These supplements were provided daily during the antenatal and breastfeeding periods in multiples of the recommended dietary allowance. Multivitamin supplements (including vitamins B, C, and E), but not vitamin A alone, significantly reduced the risks of fetal loss, low birth weight, and prematurity [22]. Receiving vitamin A resulted in a significant increase of 38% in the risk of vertical transmission [45]. Daily supplements of vitamins B, C, and E had no effect on the risk of vertical transmission of HIV in utero or during the intrapartum and early breastfeeding periods (up to age 6 weeks) [46]. However, multivitamins provided a modest but not statistically significant reduction in the overall risks of HIV infection through breastfeeding, mortality by age 24 months, and the combined risks of infection and mortality among children. Children born to women taking multivitamins who had relatively poorer nutritional or immunological conditions at baseline had a significant reduction in the risks of these end points. Maternal multivitamin supplementation also reduced child mortality among HIV-uninfected children [45].

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Conclusions

In summary, HIV-1 infection is having a devastating impact on many developing countries. A lot of evidence supports the hypotheses that poor nutritional status may be associated with poor outcomes in HIV-infected patients and that improving nutritional status can lead to an improvement in these outcomes. Previous studies were limited by their cross-sectional design, which does not allow for the ascertainment of the temporal relationship between nutritional status and disease outcome, and by the potential of residual confounding as an explanation for the findings. The results of a number of trials among adults confirmed the potential benefits of vitamins B, C, and E supplements on immune status among HIV-infected individuals. Larger trials are needed to examine the efficacy of micronutrient supplements on clinical outcomes and to ascertain whether these benefits are sustained beyond the first few weeks of the trial.

With respect to maternal supplementation, little evidence exists to support the use of vitamin A supplements in HIV-positive pregnant women. The possibility that maternal supplements of vitamin A increase the risk of transmission of HIV requires further investigation. Multivitamin supplementation of HIV-positive women during the prenatal period is increasingly being practiced, given the reported benefits on fetal outcomes. The provision of vitamins B, C, and E to lactating women ought to be encouraged in light of the protective effects of these vitamins against transmission through breastfeeding and mortality among immunologically and nutritionally compromised women. It may be difficult to target such an intervention only to women who are in these categories, because the added burden of screening for these characteristics will not be practical.

In children, there is evidence to indicate that vitamin A supplements are beneficial for reducing morbidity and mortality in developing countries, including among HIV-infected children. There are no data on the relationships of other micronutrients and child health among HIV-infected children. For adults and children, more research is warranted on the role of selenium, zinc, and other trace elements on various measures of health among HIV-infected individuals.

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Footnotes

  • Financial support: National Institute of Child Health and Human Development (R01 HD32257); National Institute of Allergy and Infectious Diseases (U01 AI45441); Fogarty International Center (D43 TW00004).

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  1. Clin Infect Dis. (2003) 37 (Supplement 2): S112-S116. doi: 10.1086/375882
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