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

Abstract

Summary 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.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 77

1. 1.

   Adams EJ, Stephenson LS, Latham MC, Kinoti SN. Physical activity and growth of Kenyan school children with hookworm, Trichuris trichiura and Ascaris lumbricoides infections are improved after treatment with albendazole. Journal of Nutrition. 1994;124:1199-1206.

   Not in our library10.1093/jn/124.8.1199

2. 2.

   Albonico M, Stoltzfus RJ, Savioli L, et al. Epidemiological evidence for a differential effect of hookworm species, Ancylostoma duodenale or Necator americanus, on iron status of children. International Journal of Epidemiology. 1998;27:530-537.

   Not in our library10.1093/ije/27.3.530

3. 3.

   Anderson RM, May RM. Helminth infections of humans: mathematical models, population dynamics, and control. Advances in Parasitology. 1985;24:1-101.

   Not in our library10.1016/s0065-308x(08)60561-8

4. 4.

   Anderson RM, Schad GA. Hookworm burdens and faecal egg counts: an analysis of the biological basis of variation. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1985;79:812-825.

   Not in our library10.1016/0035-9203(85)90128-2

5. 5.

   Awasthi S, Bundy DAP. Intestinal nematode infection and anaemia in developing countries. British Medical Journal. 2007;334:1065-1066.

   Not in our library10.1136/bmj.39211.572905.80

6. 6.

   Awasthi S, Pande VK, Fletcher RH. Effectiveness and cost-effectiveness of albendazole in improving nutritional status of pre-school children in urban slums. Indian Pediatrics. 2000;37:19-29.

   Not in our library

7. 7.

   Beasley M, Tomkins AM, Hall A, et al. The impact of population level deworming on the haemoglobin levels of schoolchildren in Tanga, Tanzania. Tropical Medicine and International Health. 1999;4:744-750.

   Not in our library10.1046/j.1365-3156.1999.00486.x

8. 8.

   Beaver PC. Hemoglobin determination in hookworm disease case-finding. American Journal of Tropical Medicine. 1951;21:90-97.

   Not in our library10.4269/ajtmh.1951.s1-31.90

9. 9.

   Bennett A, Guyatt H. Reducing intestinal nematode infection: efficacy of albendazole and mebendazole. Parasitology Today. 2000;16:71-74.

   Not in our library10.1016/s0169-4758(99)01544-6

10. 10.

    Bhargava A, Jukes M, Lambo J, et al. Anthelmintic treatment improves the hemoglobin and serum ferritin concentrations of Tanzanian schoolchildren. Food and Nutrition Bulletin. 2003;24:332-342.

    Not in our library10.1177/156482650302400403

11. 11.

    Bradley M, Chandiwana SK, Bundy DAP. The epidemiology and control of hookworm infection in the Burma Valley area of Zimbabwe. Transactions of the Royal Society of Tropical Medicine & Hygiene. 1993;87:145-147.

    Not in our library10.1016/0035-9203(93)90463-z

12. 12.

    Brito LL, Barreto ML, Silva Rde C, et al. Moderate- and low-intensity co-infections by intestinal helminths and Schistosoma mansoni, dietary iron intake, and anemia in Brazilian children. American Journal of Tropical Medicine & Hygiene. 2006;75:939-944.

    Not in our library

13. 13.

    Brooker S, Bethony J, Hotez PJ, et al. Human hookworm infection in the 21st century. Advances in Parasitology. 2004;58:197-288.

    Not in our library10.1016/s0065-308x(04)58004-1

14. 14.

    Brooker S, Peshu N, Warn PA, et al. The epidemiology of hookworm infection and its contribution to anaemia among pre-school children on the Kenyan coast. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1999;93:240-246.

    Not in our library10.1016/s0035-9203(99)90007-x

15. 15.

    Brooker S, Jardim-Botelho A, Quinnell RJ, et al. Age-related changes in hookworm infection, anaemia and iron deficiency in an area of high Necator americanus hookworm transmission in south-eastern Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene. 2007a;101:146-154.

    Not in our library10.1016/j.trstmh.2006.05.012

16. 16.

    Brooker S, Akhwale W, Pullan R, et al. Epidemiology of plasmodium-helminth co-infection in Africa: populations at risk, potential impact on anemia, and prospects for combining control. American Journal of Tropical Medicine & Hygiene. 2007b;77:88-98.

    Not in our library

17. 17.
    Hookworm-Related Anaemia among Pregnant Women: A Systematic Review · 2008

    No notice
18. 18.

    Bundy DAP, Shaeffer S, Jukes M, Breman JG, Measham AR, Alleyne G, et al. School based health and nutrition programs. Disease Control Priorities for Developing Countries. 2006;1091-1108.

    Not in our library

19. 19.

    Bundy DAP, Kremer M, Bleakley H, Jukes MCH, Miguel E. Deworming and Development: Asking the Right Questions, Asking the Questions Right. PLoS Neglected Tropical Diseases. 2009;3:e362.

    Not in our library10.1371/journal.pntd.0000362

20. 20.

    Carr HP. Observations upon hookworm disease in Mexico. American Journal of Hygiene. 1926;6:42-61.

    Not in our library

21. 21.

    Casey GJ, Phuc TQ, Macgregor L, et al. A free weekly iron-folic acid supplementation and regular deworming program is associated with improved hemoglobin and iron status indicators in Vietnamese women. BMC Journal Public Health. 2009;24:261.

    Not in our library10.1186/1471-2458-9-261

22. 22.

    Chernin E. Problems in tropical public health among workers at a jute mill near Calcutta. IV. Hemoglobin values and their relation to the intensity of hookworm infections in the labor force. American Journal of Tropical Medicine & Hygiene. 1954;3:338-347.

    Not in our library10.4269/ajtmh.1954.3.338

23. 23.

    Crompton DWT, Stephenson LS, Schad GA, Warren KS. Hookworm infection, nutritional status and productivity. Hookworm Disease, Current Status and New Directions. 1990;231-265.

    Not in our library

24. 24.

    Crompton DWT, Whitehead RR. Hookworm infections and human iron metabolism. Parasitology. 1993;107:S137-S145.

    Not in our library10.1017/s0031182000075569

25. 25.

    De Clercq D, Sacko M, Behnke J, Gilbert F, Dorny P, Vercruysse J. Failure of mebendazole in treatment of human hookworm infections in the southern region of Mali. American Journal of Tropical Medicine and Hygiene. 1997;57:25-30.

    Not in our library10.4269/ajtmh.1997.57.25

26. 26.

    Dossa RA, Ategbo EA, de Koning FL, van Raaij JM, Hautvast JG. Impact of iron supplementation and deworming on growth performance in preschool Beninese children. European Journal of Clinical Nutrition. 2001;55:223-228.

    Not in our library10.1038/sj.ejcn.1601126

27. 27.
    The synergistic effect of concomitant schistosomiasis, hookworm, and trichuris infections on children's anemia burden. · 2008

    Not checked
28. 28.

    Fleming AF, Strickland GT. Iron deficiency. Hunter’s Tropical Medicine. 2000;32-60.

    Not in our library

29. 29.

    Friedman JF, Kanzaria HK, McGarvey ST. Human schistosomiasis and anemia: the relationship and potential mechanisms. Trends in Parasitology. 2005;21:386-392.

    Not in our library10.1016/j.pt.2005.06.006

30. 30.

    Friis H, Mwaniki D, Omondi B, et al. Effects on haemoglobin of multi-micronutrient supplementation and multi-helminth chemotherapy: a randomized, controlled trial in Kenyan school children. European Journal of Clinical Nutrition. 2003;57:573-579.

    Not in our library10.1038/sj.ejcn.1601568

31. 31.

    Gilgen DD, Mascie-Taylor CG, Rosetta LL. Intestinal helminth infections, anaemia and labour productivity of female tea pluckers in Bangladesh. Tropical Medicine and International Health. 2001;6:449-457.

    Not in our library10.1046/j.1365-3156.2001.00729.x

32. 32.

    Gilles HM, Williams EJW. Hookworm infection and anaemia. an epidemiological, clinical, and laboratory study. Quarterly Journal of Medicine. 1964;33:482-486.

    Not in our library

33. 33.

    Gulani A, Nagpal J, Osmond C, Sachdev HPS. Effect of administration of intestinal anthelmintic drugs on haemoglobin: systematic review of randomised controlled trials. British Medical Journal. 2007;334:1095-1097.

    Not in our library10.1136/bmj.39150.510475.ae

34. 34.

    Guyatt HL, Brooker S, Kihamia CM, Hall A, Bundy DAP. Evaluation of efficacy of school-based anthelmintic treatments against anaemia in children in the United Republic of Tanzania. Bulletin of the World Health Organization. 2001;79:695-703.

    Not in our library

35. 35.

    Hall A. Micronutrient supplements for children after deworming. Lancet Infectious Diseases. 2007;7:297-302.

    Not in our library10.1016/s1473-3099(07)70084-1

36. 36.

    Higgins JPT, Green S. Cochrane Handbook for Systematic Reviews of Interventions Version 5.0.2. 2009.

    Not in our library

37. 37.

    Horton J. Global anthelmintic chemotherapy programs: learning from history. Trends in Parasitology. 2003;19:405-409.

    Not in our library10.1016/s1471-4922(03)00171-5

38. 38.

    Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A, Xiao S. Hookworm infection. New England Journal of Medicine. 2004;351:799-807.

    Not in our library10.1056/nejmra032492

39. 39.

    Keiser J, Utzinger J. Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. Journal of the American Medical Association. 2008;299:1937-1948.

    Not in our library10.1001/jama.299.16.1937

40. 40.

    King CH, Dickman K, Tisch DJ. Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet. 2005;365:1561-1569.

    Not in our library10.1016/s0140-6736(05)66457-4

Cited by papers we hold 8

• Prevalence, years lived with disability, and trends in anaemia burden by severity and cause, 1990–2021: findings from the Global Burden of Disease Study 2021 · 2023
  Corrected
• Neurodevelopmental performance among pre-schoolers treated for severe anaemia at Lira Regional Referral Hospital, Uganda. · 2020
  Not checked
• Anemia prevalence and etiology among women, men, and children in Ethiopia: a study protocol for a national population-based survey · 2019
  Not checked
• The Global Economic and Health Burden of Human Hookworm Infection · 2016
  No notice
• The Global Burden of Disease Study 2010: Interpretation and Implications for the Neglected Tropical Diseases · 2014
  No notice
• Global numbers of infection and disease burden of soil transmitted helminth infections in 2010 · 2014
  No notice
• Global, regional, and national trends in haemoglobin concentration and prevalence of total and severe anaemia in children and pregnant and non-pregnant women for 1995–2011: a systematic analysis of population-representative data · 2013
  No notice
• Low Efficacy of Single-Dose Albendazole and Mebendazole against Hookworm and Effect on Concomitant Helminth Infection in Lao PDR · 2012
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.