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

Tropical Medicine and International Health

Volumn 15, Issue 7, 2010, Pages 776-795

  Smith, Jennifer L ^a   Brooker, Simon ^a,b  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

Author keywords

Anaemia; Ancylostoma duodenale; Anthelmintic treatment; Haemoglobin; Hookworm; Necator americanus

Indexed keywords

ALBENDAZOLE; BENZIMIDAZOLE DERIVATIVE; HEMOGLOBIN; IRON; MEBENDAZOLE; PLACEBO; PRAZIQUANTEL;

AGE STRUCTURE; ANEMIA; ANTIBIOTICS; CONFIDENCE INTERVAL; DATABASE; DISEASE TREATMENT; FOOD SUPPLEMENTATION; HEMOGLOBIN; INFECTIVITY; META-ANALYSIS; PARASITE INFESTATION; PREGNANCY;

ANEMIA; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; DISEASE SEVERITY; HOOKWORM INFECTION; HUMAN; IRON THERAPY; META ANALYSIS; PREVALENCE; RANDOMIZED CONTROLLED TRIAL; REVIEW; SCHISTOSOMIASIS; SYSTEMATIC REVIEW; TREATMENT RESPONSE; VITAMIN SUPPLEMENTATION; WORM EXPULSION;

ADOLESCENT; ADULT; AGED; ALBENDAZOLE; ANEMIA; ANTHELMINTICS; CHILD; CHILD, PRESCHOOL; FEMALE; HEMOGLOBINS; HOOKWORM INFECTIONS; HUMANS; INFANT; MEBENDAZOLE; MIDDLE AGED; PRAZIQUANTEL; PREGNANCY; RESEARCH DESIGN;

EID: 77953193904     PISSN: 13602276     EISSN: 13653156     Source Type: Journal    
DOI: 10.1111/j.1365-3156.2010.02542.x     Document Type: Review

References (77)

1. Adams EJ, Stephenson LS, Latham MC Kinoti SN (1994) 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 124, 1199-1206.
2. Albonico M, Stoltzfus RJ, Savioli L et al. (1998) Epidemiological evidence for a differential effect of hookworm species, Ancylostoma duodenale or Necator americanus, on iron status of children. International Journal of Epidemiology 27, 530-537.
3. Anderson RM May RM (1985) Helminth infections of humans: mathematical models, population dynamics, and control. Advances in Parasitology 24, 1-101.
4. Anderson RM Schad GA (1985) Hookworm burdens and faecal egg counts: an analysis of the biological basis of variation. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 812-825.
5. Awasthi S Bundy DAP (2007) Intestinal nematode infection and anaemia in developing countries. British Medical Journal 334, 1065-1066.
6. Awasthi S, Pande VK Fletcher RH (2000) Effectiveness and cost-effectiveness of albendazole in improving nutritional status of pre-school children in urban slums. Indian Pediatrics 37, 19-29.
7. Beasley M, Tomkins AM, Hall A et al. (1999) The impact of population level deworming on the haemoglobin levels of schoolchildren in Tanga, Tanzania. Tropical Medicine and International Health 4, 744-750.
8. Beaver PC (1951) Hemoglobin determination in hookworm disease case-finding. American Journal of Tropical Medicine 21, 90-97.
9. Bennett A Guyatt H (2000) Reducing intestinal nematode infection: efficacy of albendazole and mebendazole. Parasitology Today 16, 71-74.
10. Bhargava A, Jukes M, Lambo J et al. (2003) Anthelmintic treatment improves the hemoglobin and serum ferritin concentrations of Tanzanian schoolchildren. Food and Nutrition Bulletin 24, 332-342.
11. Bradley M, Chandiwana SK Bundy DAP (1993) The epidemiology and control of hookworm infection in the Burma Valley area of Zimbabwe. Transactions of the Royal Society of Tropical Medicine & Hygiene 87, 145-147.
12. Brito LL, Barreto ML, Silva Rde C, et al. (2006) 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 75, 939-944.
13. Brooker S, Bethony J, Hotez PJ et al. (2004) Human hookworm infection in the 21st century. Advances in Parasitology 58, 197-288. (Pubitemid 39643145)
14. Brooker S, Peshu N, Warn PA, et al. (1999) 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 93, 240-246.
15. Brooker S, Jardim-Botelho A, Quinnell RJ et al. (2007a) 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 101, 146-154.
16. Brooker S, Akhwale W, Pullan R et al. (2007b) 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 77, 88-98.
17. Brooker S, Hotez PJ Bundy DAP (2008) Hookworm-related anaemia among pregnant women: a systematic review. PLoS Neglected Tropical Diseases 2, e291.
18. Bundy DAP, Shaeffer S, Jukes M et al. (2006) School based health and nutrition programs. In : Disease Control Priorities for Developing Countries (eds JG Breman, AR Measham, G Alleyne et al.) Oxford University Press
19. Bundy DAP, Kremer M, Bleakley H, Jukes MCH Miguel E (2009) Deworming and Development: Asking the Right Questions, Asking the Questions Right. PLoS Neglected Tropical Diseases 3, e362.
20. Carr HP (1926) Observations upon hookworm disease in Mexico. American Journal of Hygiene 6, 42-61.
21. Casey GJ, Phuc TQ, Macgregor L et al. (2009) 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 24, 261.
22. Chernin E (1954) 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 3, 338-347.
23. Crompton DWT Stephenson LS (1990) Hookworm infection, nutritional status and productivity. In : Hookworm Disease, Current Status and New Directions (eds GA Schad KS Warren) Taylor and Francis
24. Crompton DWT Whitehead RR (1993) Hookworm infections and human iron metabolism. Parasitology 107, S137-S145.
25. De Clercq D, Sacko M, Behnke J, Gilbert F, Dorny P Vercruysse J (1997) Failure of mebendazole in treatment of human hookworm infections in the southern region of Mali. American Journal of Tropical Medicine and Hygiene 57, 25-30.
26. Dossa RA, Ategbo EA, de Koning FL, van Raaij JM Hautvast JG (2001) Impact of iron supplementation and deworming on growth performance in preschool Beninese children. European Journal of Clinical Nutrition 55, 223-228.
27. Ezeamama AE, McGarvey ST, Acosta LP et al. (2008) The synergistic effect of concomitant schistosomiasis, hookworm, and trichuris infections on children's anemia burden. PLoS Neglected Tropical Diseases 2, e245.
28. Fleming AF (2000) Iron deficiency. In : Hunter's Tropical Medicine, 8th edn (ed GT Strickland) W.B. Saunders
29. Friedman JF, Kanzaria HK McGarvey ST (2005) Human schistosomiasis and anemia: the relationship and potential mechanisms. Trends in Parasitology 21, 386-392.
30. Friis H, Mwaniki D, Omondi B et al. (2003) Effects on haemoglobin of multi-micronutrient supplementation and multi-helminth chemotherapy: a randomized, controlled trial in Kenyan school children. European Journal of Clinical Nutrition 57, 573-579.
31. Gilgen DD, Mascie-Taylor CG Rosetta LL (2001) Intestinal helminth infections, anaemia and labour productivity of female tea pluckers in Bangladesh. Tropical Medicine and International Health 6, 449-457.
32. Gilles HM Williams EJW (1964) Hookworm infection and anaemia. an epidemiological, clinical, and laboratory study. Quarterly Journal of Medicine 33, 482-486.
33. Gulani A, Nagpal J, Osmond C Sachdev HPS (2007) Effect of administration of intestinal anthelmintic drugs on haemoglobin: systematic review of randomised controlled trials. British Medical Journal 334, 1095-1097.
34. Guyatt HL, Brooker S, Kihamia CM, Hall A Bundy DAP (2001) Evaluation of efficacy of school-based anthelmintic treatments against anaemia in children in the United Republic of Tanzania. Bulletin of the World Health Organization 79, 695-703.
35. Hall A (2007) Micronutrient supplements for children after deworming. Lancet Infectious Diseases 7, 297-302.
36. Higgins JPT Green S (eds 2009) Cochrane Handbook for Systematic Reviews of Interventions Version 5.0.2 [updated September 2009]. The Cochrane Collaboration. Available from http://www.cochrane-handbook.org.
37. Horton J (2003) Global anthelmintic chemotherapy programs: learning from history. Trends in Parasitology 19, 405-409.
38. Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A Xiao S (2004) Hookworm infection. New England Journal of Medicine 351, 799-807.
39. Keiser J Utzinger J (2008) Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. Journal of the American Medical Association 299, 1937-1948.
40. King CH, Dickman K Tisch DJ (2005) Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365, 1561-1569.
41. Koukounari A, Fenwick A, Whawell S et al. (2006) Morbidity indicators of Schistosoma mansoni: relationship between infection and anemia in Ugandan schoolchildren before and after praziquantel and albendazole chemotherapy. American Journal of Tropical Medicine & Hygiene 75, 278-286.
42. Koukounari A, Gabrielli AF, Toure S et al. (2007) Schistosoma haematobium infection and morbidity before and after large-scale administration of praziquantel in Burkina Faso. Journal of Infectious Diseases 196, 659-669.
43. Kurtzhals JA, Addae MM, Akanmori BD et al. (1999) Anaemia caused by asymptomatic Plasmodium falciparum infection in semi-immune African schoolchildren. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, 623-627.
44. Kurz KM, Stephenson LS, Latham MC Kinoti SN (1986) The effectiveness of metrifonate in reducing hookworm infection in Kenyan school children. American Journal of Tropical Medicine and Hygiene 35, 571-574.
45. Latham MC, Stephenson LS, Hall A, Wolgemuth JC, Elliott TC Crompton DW (1982) A comparative study of the nutritional status, parasitic infections and health of male roadworkers in four areas of Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 734-740.
46. Layrisse M Roche M (1964) The relationship between anemia and hookworm infection. Results of surveys of rural Venezuelan population. American Journal of Hygiene 79, 279-301.
47. Le Huong T, Brouwer ID, Nguyen KC, Burema J Kok FJ (2007) The effect of iron fortification and de-worming on anaemia and iron status of Vietnamese schoolchildren. British Journal of Nutrition 97, 955-962.
48. Lwambo NJS, Bundy DAP Medley GFH (1992) A new approach to morbidity risk assessment in hookworm endemic communities. Epidemiology and Infection 108, 469-481.
49. Martinez-Torres C, Ojeda A, Roche M Layrisse M (1967) Hookworm infection and intestinal blood loss. Transactions of the Royal Society of Tropical Medicine and Hygiene 61, 373-383.
50. Menendez C, Fleming AF Alonso PL (2000) Malaria-related anaemia. Parasitology Today 16, 469-476.
51. Miller TA (1979) Hookworm infection in man. Advances in Parasitology 17, 315-384.
52. Murray CJ, Lopez AD, Black R et al. (2007) Global Burden of Disease 2005: call for collaborators. Lancet 370, 109-110.
53. Nga TT, Winichagoon P, Dijkhuizen MA et al. (2009) Multi-micronutrient- fortified biscuits decreased prevalence of anemia and improved micronutrient status and effectiveness of deworming in rural Vietnamese school children. Journal of Nutrition 139, 1013-1021.
54. Olds GR, King C, Hewlett J et al. (1999) Double-blind placebo-controlled study of concurrent administration of albendazole and praziquantel in schoolchildren with schistosomiasis and geohelminths. Journal of Infectious Diseases 179, 996-1003.
55. Olsen A, Magnussen P, Ouma JH, Andreassen J Friis H (1998) The contribution of hookworm and other parasitic infections to haemoglobin and iron status among children and adults in western Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 643-649.
56. Pawlowski ZS, Scahd GA Stott GJ (1991) Hookworm Infection and Anaemia. Approaches to Prevention and Control. World Health Organization
57. Perroncito E (1880) Helminthological observations upon the endemic disease developed among the labourers in the Tunnel of Mount St Gothard. Queckett Journal of Microscopy Club 6, 141-148.
58. Quinnell RJ, Slater AFG, Tighe P et al. (1993) Reinfection with hookworm after chemotherapy in Papua New Guinea. Parasitology 106, 379-385.
59. Reynoldson JA, Behnke JM, Pallant LJ et al. (1997) Failure of pyrantel in treatment of human hookworm infection (Ancylostoma duodenale). in the Kimberely region of North West Australia. Acta Tropica 68, 301-312.
60. Rohner F, Zimmermann MB, Amon RJ et al. (2010) In a randomized controlled trial of iron fortification, anthelmintic treatment, and intermittent preventive treatment of malaria for anemia control in Ivorian children, only anthelmintic treatment shows modest benefit. Journal of Nutrition 140, 634-641.
61. Schad GA Banwell JG (1984) Hookworms. In : Tropical and Geographical Medicine (eds KS Warren AAF Mahmoud) McGraw-Hill Book Company
62. Schad GA Anderson RM (1985) Predisposition to hookworm infection in humans. Science 228, 1537-1540.
63. Sharman A (2000) Anemia Testing in Population-Based Surveys: General Information and Guidelines for Country Monitors and Program Managers. ORC Macro, Calverton, Maryland USA.
64. Stephenson LS, Latham MC Kurz KM (1985) Relationships of Schistosoma haematobium, hookworm and malarial infections and metrifonate treatment to hemoglobin level in Kenyan school children. American Journal of Tropical Medicine and Hygiene 34, 519-528.
65. Stephenson LS, Latham MC, Kinoti SN, Kurz KM Brigham H (1990) Improvements in physical fitness of Kenyan schoolboys infected with hookworm, Trichuris trichiura and Ascaris lumbricoides following a single dose of albendazole. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 277-282.
66. Stephenson LS, Latham MC, Adams EJ, Kinoti SN Pertet A (1993) Physical fitness, growth and appetite of Kenyan school boys with hookworm, Trichuris trichiura and Ascaris lumbricoides infections are improved four months after a single dose of albendazole. Journal of Nutrition 123, 1036-1046.
67. Stoltzfus RJ, Albonico M, Chwaya HM et al. (1996) Hemoquant determination of hookworm-related blood loss and its role in iron deficiency in African children. American Journal of Tropical Medicine and Hygiene 55, 399-404.
68. Stoltzfus RJ, Dreyfuss ML, Chwaya HM Albonico M (1997) Hookworm control as a strategy to prevent iron deficiency. Nutrition Reviews 55, 223-232.
69. Stoltzfus RJ, Albonico M, Chwaya HM, Tielsch JM, Schulze KJ Savioli L (1998) Effects of the Zanzibar school-based deworming program on iron status of children. American Journal of Clinical Nutrition 68, 179-186.
70. Stoltzfus RJ, Chwaya HM, Montresor A, Albonico M, Savioli L Tielsch JM (2000) Malaria, hookworms and recent fever are related to anemia and iron status indicators in 0- to 5-y old Zanzibari children and these relationships change with age. Journal of Nutrition 130, 1724-1733.
71. Stoltzfus RJ, Chway HM, Montresor A et al. (2004) Low dose daily iron supplementation improves iron status and appetite but not anemia, whereas quarterly anthelminthic treatment improves growth, appetite and anemia in Zanzibari preschool children. Journal of Nutrition 134, 348-356.
72. Taylor M, Jinabhai CC, Couper I, Kleinschmidt I Jogessar VB (2001) The effect of different anthelmintic treatment regimens combined with iron supplementation on the nutritional status of schoolchildren in KwaZulu-Natal, South Africa: a randomized controlled trial. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 211-216.
73. Taylor-Robinson D, Jones AP Garner P (2007) Deworming drugs for treating soil-transmitted intestinal worms in children: effects on growth and school performance. Cochrane Database of Systematic Reviews. Issue 4. Art. No. CD000371. DOI: 10.1002/14651858.CD000371.pub3.
74. Tohon ZB, Mainassara HB, Garba A et al. (2008) Controlling schistosomiasis: significant decrease of anaemia prevalence one year after a single dose of praziquantel in nigerian schoolchildren. PLoS Neglected Tropical Diseases 2, e241.
75. WHO (2002) Prevention and Control of Schistosomiasis and Soil-Transmitted Helminthiasis: Report of a WHO Expert Committee. World Health Organization
76. WHO (2008) Worldwide Prevalence of Anaemia 1993-2005: WHO Global Database on Anaemia. World Health Organization
77. Zimmermann MB (2008) Methods to assess iron and iodine status. British Journal of Nutrition 99, S2-S9.