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HIV-associated anemia in children: a systematic review from a global perspective

Calis, Job CJa; van Hensbroek, Michaël Boelea,b; de Haan, Rob Jc; Moons, Peterd; Brabin, Bernard Ja,b; Bates, Imeldab

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doi: 10.1097/QAD.0b013e3282fa759f
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Early in the HIV-pandemic anemia appeared to be the most common hematological complication in HIV-infected adults [1] and a positive association had been reported between the prevalence of anemia and the severity of clinical disease [2]. Subsequently, anemia was repeatedly identified as a strong, independent and reversible predictor of mortality in large studies in western settings [3–5].

The highest prevalence of both HIV and anemia occurs in tropical countries where over 60% of cases of both conditions occur in women and children [6,7]. However, current knowledge on HIV-related anemia is predominantly based on studies in western men. This knowledge may not be applicable to children, especially for those living in resource-poor settings, as the epidemiology and management of HIV infection and anemia, and etiological factors differ between these two settings [6,7]. In children, it may present with weakness, fatigue, tachypnea and congestive cardiac failure and is associated with poor mental, motor, social–emotional, and neurophysiologic functioning [8]. In combination with HIV infection, anemia may have an enhanced effect on the quality of life [8].

The pathogenesis of anemia in HIV-infected adults, although multifactorial, relates primarily to a reduced production of erythrocytes [9–12]. This reduction is influenced by several etiological factors including infection and neoplasms, drugs such as zidovudine (ZDV), a direct effect of HIV on erythropoiesis, a blunted response to erythropoietin and nutritional deficiencies [9–12]. Compared with adults there is very little information available about the association between HIV infection and anemia in children. This situation is not likely to improve because in western countries, which generate most of the research on this topic, pediatric HIV infection is declining [7].

The aim of this study is to systematically review the prevalence and incidence of anemia in HIV-infected compared with uninfected children in both western and tropical settings. We use the results of the review to discuss anemia pathogenesis, etiology and interventions in these children at a time of rapidly increasing global availability of highly active antiretroviral therapy (HAART).


Search strategy

The following databases were searched for primary studies reporting on anemia and hemoglobin (Hb)/hematocrit levels in HIV-infected children: PubMed (1950–September 2006), Embase (1980–2006), African Index Medicus (1960–2006), and African Journals Online (1998–2006). The search strategy included French or English terms: anemia or anaemia or anémie, HIV or AIDS or VIH or SIDA and child or children or infant or infants or enfant or enfants and was performed on text words or all fields, as applicable to the individual databases. Finally, reference lists of pertinent articles and reviews were scanned for relevant articles. No language restriction was used and the articles were translated as necessary.

Selection criteria

All studies that met the following criteria were included: presented data either on prevalence or incidence or mean Hb/hematocrit levels or all in HIV-infected children (<18 years) or provided sufficient information to calculate these numbers; and had a well defined definition for anemia. If a study presented both Hb and hematocrit data for a single population, the former was used. The following studies were excluded: case reports and reviews; those assessing restricted or possibly biased populations such as intervention trials with prophylactic or therapeutic regimens against Pneumocystis carinii pneumonia (PCP) or HIV; studies on children with a specific (secondary) infection only; and duplicated studies. For the sections on pathogenesis and etiology in the Discussion, we used all articles on anemia in HIV-infected children. Data were extracted by the first author, and when there were doubts about whether studies should be included in the analysis these were resolved by discussion between the authors.

Definitions and subgroup analysis

AIDS was defined as the presence of Centers for Disease Control (CDC) stage C or in the older classification system as having P2 disease other than P2A [13]. Studies were grouped by origin of study population: tropical settings (Africa, Central and South America, Asia with the exemption of the former Soviet Union, China and Mongolia) or western settings (Europe and North America) and the cut-off used to define anemia. Hb cut-offs closest to 11 g/dl (range 10.0–12.0) were used to define mild anemia, 9 g/dl (range 8.0–9.9) for moderate anemia, 7 g/dl (range 6.0–7.9) for marked anemia, and 5 g/dl (<5.9) for severe anemia. If studies used hematocrit values to define anemia, these values were divided by three to provide an approximate equivalent Hb level [6]. Both HIV-unexposed and children who were HIV-uninfected, but transiently expressed maternal antibody against HIV (seroreverted children), were accepted as control groups in the meta-analysis and combined if appropriate. Studies that did not recruit a control group of uninfected children are reported in the tables but were not included in the meta-analysis.

Statistical analysis

Data on prevalence, incidence and mean Hb/hematocrit were summarized using descriptive statistics. The effects of the different anemia cut-offs on prevalence were depicted using exponential curves based on weighted data. In both the prevalence and incidence studies, the risk of anemia in HIV-infected children was assessed by meta-analyses on studies that included a control group. Effect sizes of binary data were expressed in (pooled) relative risks (RR) or odds ratios (OR) estimates, when appropriate. Continuous data (mean Hb/hematocrit values) were pooled using standardized mean difference (SMD). Additionally, planned sensitivity analyses exploring the consistency of the findings across western and tropical settings were performed. In the case study, results were heterogeneously distributed (χ2 analysis: P < 0.20) and random-effects models (e.g. random odds ratio) were used. Fixed-effects models were used if no heterogeneity could be shown. Statistical uncertainty was expressed in 95% confidence intervals (CIs). Publication bias was visually assessed using funnel plots. All analyses were performed in Review Manager 4.2.7 (The Cochrane Collaboration) and SPSS 12.0 (SPSS Inc., Chicago, Illinois, USA).


Selection of articles

The combined search retrieved 1027 hits. Eight hundred and two articles remained after exclusion of duplicate citations and of these, 226 concerned anemia in HIV-infected children. For the meta-analysis, articles were excluded if they were case reports or reviews (74), did not present anemia incidence or prevalence data (29), presented data on children enrolled in trials using PCP, prevention of mother to child transmission (PMTCT) or antiretroviral therapy (ART) (34), focused on children that had a specific coinfection (nine), or described the same study twice (six). A final set of 36 articles, 14 longitudinal and 22 cross-sectional studies remained. Fourteen studies were performed in a western setting and 22 in a tropical setting.

For the prevalence section, 15 of these 36 studies were used, as 11 did not provide extractable data [14–24] and 10 did not define anemia [25–34]. The incidence section consisted of seven studies, as four studies did not provide extractable data [23,35–37] and three did not define anemia [30,31,34]. The section on mean Hb was written using 12 articles; the remaining 24 did not provide extractable data [14–21,23,25–30,32–34,38–43].

The meta-analysis represents data on 903 HIV-infected and 3441 HIV-uninfected children who were enrolled in controlled studies. Hb and anemia data from an additional 1170 HIV-infected children recruited in uncontrolled studies are also presented. Not all studies provided data on sex, age or both. For those controlled studies that did provide data the overall age range was 0.0–18 years and the overall male: female ratio was 1.00: 1.13.

Prevalence of anemia in HIV-infected children

Fifteen studies were included in the analysis of anemia prevalence in HIV-infected children (Table 1) [35–39,42,44–52]. Seven studies included controls of non-HIV-infected children.

Table 1
Table 1:
Prevalence of anemia in HIV-infected children by use of a control group of HIV-uninfected children and location.

The overall prevalence of mild or moderate anemia in HIV-infected children varied between 22–94 and 3–82%, respectively. One study presented data on marked and none on severe anemia. All studies with a control group except one [44] reported a significantly higher prevalence of anemia in HIV-infected than in uninfected children (Fig. 1a) [44,46]. The pooled random-effect OR for mild anemia in HIV-infected children was 4.5 (95% CI 2.5–8.3; Fig. 1a), and for moderate anemia it was 4.5 (95% CI 2.0–10.3; Fig. 1b). Studies that included a control group were further analyzed using a weighted curve (Fig. 2a). The nonoverlapping 95% CIs indicate that anemia was significantly more prevalent in HIV-infected children.

Fig. 1
Fig. 1:
Risks of mild anemia (Hb < 10.0–12.0) and moderate anemia (Hb < 8.0–9.9) at mean hemoglobin and hematocrit levels. Random effect models of the risk of mild (a) and moderate anemia (b) using prevalence data and mean hemoglobin/hematocrit levels (c) per location. Original data are given in Tables 1 (prevalence) and 3 (mean hemoglobin). (c) Two studies could not be displayed as the data were incomplete [44,46]. CI, confidence interval; Hb, hemoglobin; Ht, hematocrit; OR, odds ratio; SMD, standardized mean difference.
Fig. 2
Fig. 2:
Prevalence of anemia in HIV-infected and uninfected children. (a) Prevalence of anemia in HIV-infected and uninfected children (only studies that simultaneously included both groups, n = 7). Curves display weighted exponential trendlines (thick lines) and 95% confidence intervals (thin lines) for HIV-infected (R 2 = 0.83) and HIV-uninfected children (R 2 = 0.84). For the analyses, data for 12 cut-offs were used reflecting 700 HIV-infected and 2387 uninfected children. (b) Prevalence of anemia in HIV-infected children in tropical vs. western (Europe and North America) settings. Curves display weighted exponential trendlines (thick lines) and 95% confidence intervals (thin lines) for HIV-infected children in tropical (R 2 = 0.77) and western settings (R 2 = 0.63). The analyses included 15 studies presenting data for 23 cut-offs in 1085 HIV-infected children.

The prevalence of mild and moderate anemia in western settings ranged between 22–94 and 11–82%, respectively. In tropical settings, the equivalent ranges were 50–91% for mild anemia and 3–38% for moderate anemia. In the latter setting, pooled ORs for mild and moderate anemia were 3.6 (95% CI 2.8–4.7) and 3.0 (95% CI 2.3–3.8), respectively. To compare the prevalence of anemia in HIV-infected children living in western or tropical settings, the prevalences were plotted against the different cut-offs used (Fig. 2b). The 95% CIs for this comparison widely overlapped and did not suggest a significant effect of location on the prevalence of anemia in HIV-infected children.

Incidence of anemia in HIV-infected children

Seven longitudinal studies reported anemia incidence including two studies with a control group of HIV-uninfected children (Table 2) [16,19–22,24,53]. Of these seven studies, five reported a mean or a median duration of follow-up and ranged from 0.6 to 2.3 years.

Table 2
Table 2:
Incidence of anemia in HIV-infected children in longitudinal analyses by use of a control group of HIV-uninfected children and location.

The incidence of mild and moderate anemia in HIV-infected children varied between 0.41–0.44 and 0.07–0.37 per person-year of follow-up, respectively. No study reported data for marked anemia and only one for severe anemia. The two studies with control groups showed that anemia was more frequent in HIV-infected children (Table 2). Although both studies presented RRs with 95% significance, the pooled random effect RR for mild anemia was 1.35 (95% CI 0.85–2.27, data not graphically presented).

In western settings, mild and moderate anemia was reported in 74–87 and 16–37% of HIV-infected children studied. In tropical settings these numbers ranged between 73–100 and 29–58%. Too little data were available in these subgroups to compare per person-year incidence rates.

Mean hemoglobin and hematocrit levels

Three studies presented longitudinal data (Fig. 3) [23,36,54] and 12 studies presented cross-sectional data on mean/median Hb or hematocrit levels in HIV-infected children (Table 3) [31,32,36,37,44–51].

Fig. 3
Fig. 3:
Mean hemoglobin levels of cohorts of HIV-infected and uninfected infants in Zimbabwe [54] (upper left), Kenya [23] (upper right), and Italy [36] (bottom left). The curves in the bottom right graph compare the mean hemoglobin levels in HIV-infected children in these settings. Hb, hemoglobin.
Table 3
Table 3:
Mean hemoglobin and hematocrit levels in HIV-infected children by use of a control group of HIV-uninfected children and location.

In the cross-sectional studies, mean Hb levels for HIV-infected children ranged from 8.0 to 13.0 g/dl. All seven studies with a control group reported lower values in HIV-infected children. In two studies, these differences were not significant, one of these had a very small sample size (n = 14) and the other showed borderline significance (P = 0.07). Five studies that reported means and standard deviations could be included in the meta-analysis. The pooled SMD was −0.78 (95% CI −0.47 to −1.10), equivalent to −1.1 g/dl Hb (Fig. 1c).

In western studies, mean Hb levels for HIV-infected children varied between 9.8 and 13.0 g/dl (one with a mean hematocrit value of 27.5%). In tropical areas, mean values ranged from 8.0 to 10.4 g/dl (one with a mean hematocrit value of 28.9%). In both settings, the pooled SMD indicated a significantly decreased Hb level in HIV-infected children (Fig. 1c).

The three longitudinal studies reported mean Hb levels in infants living in Zimbabwe [54], Kenya [23] and Italy [36] (Fig. 3). The mean Hb levels from birth to 1 month of age were not different between HIV-infected and uninfected children in all the studies. From 6 to 12 weeks, the mean Hb levels of HIV-infected infants were significantly lower than those of uninfected infants and this difference increased slowly during infancy. In HIV-infected Italian, but not in African infants, the Hb levels did recover from the physiological nadir at 6 weeks, but then decreased slowly over time. Seroreverting infants had similar Hb curves to infants born to mothers not infected with HIV (Kenya and Zimbabwe only).


In this first review on children, we assessed if anemia was more common in HIV-infected children compared with uninfected children in both western and tropical settings. Mild anemia (Hb < 11 g/dl) appeared to be a common complication of HIV in children in both settings and occurred in 73–100% of cases. A difference in mean Hb between infected and uninfected children was present from the age of 6 to 12 weeks with lower Hb levels in HIV-infected children.

Prevalence rates for mild and moderate anemia were higher, and the mean Hb and hematocrit levels lower, in HIV-infected compared with uninfected children. These differences were identified in both tropical and western settings. This, combined with the overlapping anemia prevalence for HIV-infected children living in tropical compared with western settings (Fig. 2b), indicates that mild anemia can be highly prevalent in all HIV-infected children irrespective of the region.

Only two incidence studies included a control group and these showed that mild anemia was more common in HIV-infected children, but the combined difference did not reach significance. The only controlled study from a tropical setting was performed in Brazil. No controlled data were available for Africa where the greatest burden of HIV lies. Two uncontrolled studies from Africa reported that anemia occurred in almost all children with HIV infection [24,53], which stresses the magnitude of the anemia problem.

A limitation of this review was that the number of studies in the meta-analysis was small and heterogeneous. We partly addressed the heterogeneity by performing subgroup analyses by setting. Publication bias, commonly seen in diagnostic studies, could have affected our results but the funnel plots were not suggestive of bias (not displayed). Most studies that were published after 2000 needed to be excluded as they were clinical trials of antiretroviral drug regimens. These studies commonly excluded anemic children at enrollment. Despite this selection, anemia was still commonly reported [55–62] suggesting that even after the introduction of HAART, anemia continues to be an important, and largely neglected, complication of pediatric HIV.

Studies mainly from tropical [41,48,53] and to a lesser extent from western settings [36,47] have reported that severity of the anemia was related to disease progression. We were unable to calculate incidence rates of (mild) anemia according to disease progression as only two studies reported these data. Little comparative data on the prevalence and incidence of more severe anemia in HIV-infected children was reported. One case–control study from Kenya reported HIV prevalence in children with and without severe anemia (Hb < 5 g/dl) and found no difference (7.6 vs. 9.6%, respectively) [63]. This study did not control for confounding factors and contrasts to other studies that have shown an association between HIV and severe anemia in adults [64] and children with malaria [65]. More data on severe anemia are needed as these conditions occur frequently in children in tropical countries and are associated with a high morbidity and mortality [66].

Disease progression

As in adults [3–5], higher anemia prevalences were reported in children with more advanced disease [41,48,51]. Anemia (Hb < 8 or <9 g/dl) was identified as an independent risk factor for disease progression and death in four of the five longitudinal studies in children [16,22,36,53,67]. The CDC and WHO criteria currently include anemia (Hb < 8 g/dl) as an indicator of moderate disease on the basis of the data from an Italian study [13,22,68]. Only recently this marker of disease progression was shown to be of similar importance in children living in a tropical area [69]. Since the determination of Hb is relatively robust and cheap, compared with other tests used to monitor HIV disease, Hb may prove to be a useful tool to guide decisions on when to start or alter antiretroviral treatment [70]. This would be of additional use of HIV-infected children living in areas where CD4 cell counts and viral load determinations are not available.

Morphology and pathogenesis

Whether reversal of anemia in children increases life expectancy, as has been shown, for adults is unclear [4,5]. Although anemia reversal appears to be an attractive option to reduce morbidity and mortality in HIV-infected children, it requires an understanding of the pathogenesis and etiology of HIV-associated anemia in children. The current pathological data on children suggest that, as in adults, insufficient production of erythrocytes is the most important pathogenetic mechanism for anemia, as blood loss [14,38,47,52,71–73] and hemolysis [21,41,47,73,74] are not prominent features in HIV-infected children with anemia. In addition, these studies suggest that a positive Coombs, or direct antiglobulin test, is merely a reflection of hyperglobulinemia than actual hemolysis [21,41,47,73,74].

In eight studies reporting peripheral blood findings in HIV-infected children microcytic and hypochromic abnormalities appeared to be common with prevalences ranging from 12 to 100% and from 20 to 100%, respectively [28,38,47,48,52,53,71,73]. Though microcytic and hypochromic abnormalities appeared to be prevalent in HIV-infected children and might even increase during disease progression [48], the only study that compared peripheral blood findings in HIV-infected and uninfected children concluded that mean cell volume (MCV) and mean cell Hb (MCH) curves were comparable during the first 2 years of life [36]. In addition, no difference in the pooled prevalence of the cellular appearance was noticed between tropical and western settings (data not displayed). Pancytopenia was found in 11–20% of HIV-infected anemic children [47,71,73], which further suggests that the bone marrow might be restricted in these children. One study reported that pancytopenia was associated with ultimately fatal opportunistic infections [47].

Bone marrow examinations have rarely been carried out in HIV-infected children and most data come from retrospective analyses of hospital records that did not include a control group [38,47,71–73]. No specific morphological findings have been identified [72], but bone marrow abnormalities, especially dyserythropoiesis, were generally noted to be more common in the later stages of HIV disease [47]. As in HIV-infected adults [9,75], hypocellularity is uncommon in children with HIV infection [38,47,71–73]. Data on more accessible markers of bone marrow function that could be used to study erythropoiesis in HIV-infected children, such as reticulocyte counts, have not been reported.


The etiology of this reduction in (effective) erythropoiesis is diverse and includes the direct effect of HIV on erythropoiesis, HIV-associated infections and neoplasms, medications, and micronutrient deficiencies.

In-vitro data suggested that HIV itself may diminish erythropoiesis through apoptosis of erythroid precursors or infection of auxiliary cells, by altering cytokine and erythropoietin responses [12]. Children may be more vulnerable to these mechanisms because they differ from adults in their hematopoiesis [76], increased cytokine responses [26], or viral loads [77]. Erythropoietin [45,54] has been used to improve erythropoiesis in HIV-infected children in small studies and appeared to be successful [78], well tolerated [79–81] and cost-effective in western settings [82]. Costs and the need for regular subcutaneous injections make the use of erythropoietin challenging in tropical settings. More information is needed about the cost-effectiveness, feasibility and usefulness of erythropoietin compared with blood transfusions in HIV-infected children in developing countries.

HIV-associated conditions, predominantly infection's and, to a lesser extent, neoplastic diseases are the largest group of factors associated with anemia [83]. Mycobacterial infections, such as Mycobacterium tuberculosis and especially Mycobacterium avium-intracellulare, were found to be common in HIV-infected children worldwide and were often associated with severe anemia and pancytopenia [53,64,74,75,84–87]. Other bacterial infections associated with anemia included nontyphoid salmonella, bacteraemias, which were mainly found in African children [88,89]. Viral causes of anemia included hepatitis C [90], cytomegalovirus (CMV) [72], Epstein–Barr virus and parvovirus B19 [9]. Although persistent parvovirus B19 infections have been identified as a cause of severe anemia in HIV-infected adults [10], this was not confirmed in the only study performed in HIV-infected children [91]. Penicillium marneffei is a fungal infection, mainly found in South-East Asia and China, and in HIV-infected children, commonly presented with severe anemia [92,93]. Other fungi were rarely associated with anemia [73] with the exception of Histoplasma capsulatum[94]. Although Pneumocystis jiroveci (previously carinii) was commonly found in HIV-infected African infants, hematological data on this coinfection is lacking. The incidence of opportunistic infections may be different in HIV-infected children living in tropical or western settings. M. avium and CMV are more common in western settings, whereas tuberculosis and malaria more often affect those living in tropical settings, PCP appears to occur equally in both settings [95]. It is less clear whether the children living in tropical settings are affected earlier during HIV disease with specific opportunistic infections than their western counterparts.

There were no data suggesting that parasites commonly associated with anemia, such as schistosomiasis or hookworm, occurred more frequently in HIV-infected children. Other parasites including leishmaniasis have been associated with both anemia and pediatric HIV infections [96]. The most well recognized cause of anemia in tropical settings, falciparum malaria, was not found more frequently [23,97,98], or with higher parasite densities in HIV-infected than in uninfected children [65,97–99]. However, children with HIV and malaria were found to be more anemic, and to have more severe anemia (Hb < 5 g/dl), than children with either infection alone [23,65]. Whether this is simply the additional effect of two risk factors for anemia or the result of a biological interaction, such as increased viral loads [100], or the introduction of other coinfections such as nontyphoid salmonella [89], remains unclear and requires further evaluation.

Several drugs given during the course of HIV disease could cause anemia in children including antiretrovirals [101,102] (especially ZDV [103–106]), other antiviral agents [90,107]; antibiotics [108], tuberculostatic [84]; and cytostatic agents [109]. HAART was reported to increase Hb levels in adults, despite the hematotoxic effects of some individual agents [3], and this may also apply to children [110]. Prophylactic regimens against P. jiroveci pneumonia commonly include antifolate agents. Several combinations that were tested in children, however, were not associated with anemia [111–113]. The current WHO-recommended regimen of cotrimoxazole was proven to be protective against malaria in adults [114,115]. The effect of this regimen on malaria incidence and immunity in these children requires further studies, as the evidence is limited [116] and conflicting [117].

The micronutrient deficiencies that have been associated with HIV infection and could lead to anemia are iron, folate, vitamin B12, vitamin A and zinc. Although iron deficiency appeared to be common in HIV-infected children in studies that assessed bone marrow [47,71,72] and peripheral markers [20,28,38,39,41,42,47,48,50,52–54,71–73], studies with a control group suggested that iron deficiency may not have been more common in HIV-infected than in uninfected children [20,42,54]. Bone marrow iron status was found to be unrelated to anemia in these children [47]. Definitive evidence on the contribution of iron deficiency to the anemia of HIV-infected children and the effects and possible harm of iron supplementation [118–120] was lacking as intervention trials have not been undertaken in children or adults infected with HIV. Such information is urgently needed [95] as presumptive supplementation is recommended for most children living in tropical countries [121].

Folate and vitamin B12 deficiency were not common in pediatric HIV infection [14,48,71,72,122–124] and the hematopoietic effect of supplementation with these hematinics has not been assessed in HIV-infected children. Deficiencies of vitamin A and zinc appeared to occur more frequently in HIV-infected children than those without infection [125–128] and zinc supplementation increased mean Hb in a placebo-controlled trial in South African children with HIV infection [129]. Data on the effect of antenatal vitamin A supplementation on Hb levels in HIV-infected newborns [37,130] and on vitamin A supplementation in older HIV-infected children are limited and conflicting [131,132] and need further research.


Worldwide anemia occurred in 73–100% of HIV-infected children studied. Prevalence of mild and moderate anemia is higher in HIV-infected children compared with those without HIV infection in both tropical and western settings. There are very limited data on severe anemia, a common diagnosis in tropical areas, which is associated with high morbidity and mortality. The role of HIV in the development of severe anemia should be a focus for future research.

As in adults, an association between anemia and disease progression was reported in children regardless of geographical location. The use of Hb to predict and monitor disease progression and the effect of anemia reduction for reversing disease progression in children infected with HIV in resource-poor settings are neglected and important areas for research.

HAART is rapidly becoming available worldwide and has altered HIV from a rapidly fatal to a chronic disease. Therefore, the importance of and the possibilities for prevention of anemia are increasing. Failure of erythropoiesis was the most important mechanism for anemia in HIV-infected children and adults. The conditions leading to failing erythropoiesis were diverse and complex and included secondary infections. HAART (especially without ZDV) and the prevention or treatment of secondary infections appeared to be the most effective therapies for anemia reduction. Erythropoietin can improve anemia in children with HIV infection but has not been evaluated in developing countries. Micronutrient supplementation may be helpful in individual children with HIV infection but data to support mass supplementation are lacking. The potential benefits or risks of iron supplementation in HIV-infected children require evaluation.


Supported by independent grants of the Nutricia Research Foundation and the Ter Meulen Fund, Royal Netherlands Academy of Arts and Sciences.

There are no conflicts of interest.


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