Impact of hookworm infection and deworming on anaemia in non-pregnant populations: a systematic review

Abstract

Objectives: To summarise age- and intensity-stratified associations between human hookworm infection and anaemia and to quantify the impact of treatment with the benzimidazoles, albendazole and mebendazole, on haemoglobin and anaemia in non-pregnant populations.

Methods: Electronic databases (MEDLINE, EMBASE, PubMed) were searched for relevant studies published between 1980 and 2009, regardless of language, and researchers contacted about potential data. Haemoglobin concentration (Hb) was compared between uninfected individuals and individuals harbouring hookworm infections of different intensities, expressed as standardised mean differences (SMD) and 95% confidence intervals (CI). Meta-analysis of randomised control trials (RCTs) investigated the impact of treatment on Hb and anaemia.

Results: Twenty-three cross-sectional studies, six pre- and post-intervention studies and 14 trials were included. Among cross-sectional studies, moderate- and heavy-intensity hookworm infections were associated with lower Hb in school-aged children, while all levels of infection intensity were associated with lower Hb in adults. Among RCTs using albendazole, impact of treatment corresponded to a 1.89 g/l increase (95%CI: 0.13-3.63) in mean Hb while mebendazole had no impact. There was a positive impact of 2.37 g/l (95%CI: 1.33-3.50) on mean Hb when albendazole was co-administered with praziquantel, but no apparent additional benefit of treatment with benzimidazoles combined with iron supplementation. The mean impact of treatment with benzimidazoles alone on moderate anaemia was small (relative risk (RR) 0.87) with a larger effect when combined with praziquantel (RR 0.61).

Conclusions: Anaemia is most strongly associated with moderate and heavy hookworm infection. The impact of anthelmintic treatment is greatest when albendazole is co-administered with praziquantel.

Figure 1

Forest plot of the difference in haemoglobin concentration (Hb) among school-aged children (a) uninfected with hookworm and children with a light (1–1999 eggs/gram) hookworm infection and (b) uninfected with hookworm and children with a heavy (4000+ eggs/gram) hookworm infection. Standardised mean difference less than zero indicates lower Hb levels in children harbouring infections compared to uninfected children. The area of the shaded box represents the contribution (or weight) assigned to the estimate of effect from each study (centre point). The diamond represents the overall pooled estimates of the effect of hookworm infection on Hb. Study ID refer to references in Table S1.

Figure 2

Forest plot of the difference in haemoglobin concentration (Hb) among non-pregnant adults (a) uninfected with hookworm and adults with a light (1–1999 eggs/gram) hookworm infection and (b) uninfected with hookworm and adults with a heavy (4000+ eggs/gram) hookworm infection. Standardised mean difference less than zero indicates lower Hb levels in adults harbouring infections compared to uninfected adults. The area of the shaded box represents the contribution (or weight) assigned to the estimate of effect from each study (centre point). The diamond represents the overall pooled estimates of the effect of hookworm infection on Hb. Study ID refer to references in Table S1.

Figure 3

Forest plot of the difference in the mean change in haemoglobin concentration (Hb) among individuals treated with an anthelmintic and individuals given a placebo in interventions studies (n= 10). Standardised mean difference greater than zero indicates a greater increase in Hb levels in the treated group (or a smaller decrease) compared to the control group. The area of the shaded box represents the contribution (or weight) assigned to the treatment effect estimated from each study (centre point). Diamonds represent pooled estimates among studies stratified by (a) benzimidazole type in those studies not administering praziquantel and (b) co-administration of praziquantel in the intervention arm. The lowest diamond represents the overall pooled estimates of the effect of any treatment on the mean change in Hb.