1921
Volume 92, Issue 3
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

The relationship between intestinal helminth infection and susceptibility to malaria remains unclear. We studied the relationship between these infections. Seven schools in Ilero, Nigeria referred all pupils with febrile illness to our study center for free malaria treatment during a 3-month study period. At the end, all pupils submitted a stool sample for microscopic investigation for helminth eggs. We used an unmatched case-control design to calculate the odds ratios for helminth infection in children with at least one attack of malaria (cases) and children with no malaria episodes during the study (controls). We recorded 115 malaria cases in 82 of 354 (23.2%), 16 of 736 (2.2%), and 17 of 348 (4.7%) children ages ≤ 5, 6–10, and 11–15 years old, respectively ( = 0.001). Helminth infection rate in cases was 21 of 115 (18.3%) compared with 456 of 1,327 (34.4%) in controls. Weighted odds ratio stratified by age group for helminth infection in cases versus controls was 0.50 (95% confidence interval = 0.2–0.84, < 0.01). and hookworm were the most common helminths detected, with prevalence rates of 14 (12.2%) and 6 (5.2%) among cases compared with 333 (25.1%) and 132 (10.0%) in controls, respectively ( = 0.001). The negative association between helminth infection and malaria may be of importance in the design of deworming programs.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.14-0548
2015-03-04
2017-09-20
Loading full text...

Full text loading...

/deliver/fulltext/14761645/92/3/578.html?itemId=/content/journals/10.4269/ajtmh.14-0548&mimeType=html&fmt=ahah

References

  1. Greenwood BM, Fidock DA, Kyle DE, Kappe SH, Alonso PL, Collins FH, Duffy PE, , 2008. Malaria: progress, perils, and prospects for eradication. J Clin Invest 118: 12661276.[Crossref]
  2. World Health Organization, 2012. Report on Malaria. Geneva: World Health Organization.
  3. Chan MS, , 1997. The global burden of intestinal nematode infections – fifty years on. Parasitol Today 13: 438443.[Crossref]
  4. World Health Organization, 2006. WHO Geographical Distribution and Useful Facts and Stats. Geneva: World Health Organization.
  5. Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, Abraham J, Adair T, Aggarwal R, Ahn SY, Alvarado M, Anderson HR, Anderson LM, Andrews KG, Atkinson C, Baddour LM, Barker-Collo S, Bartels DH, Bell ML, Benjamin EJ, Bennett D, Bhalla K, Bikbov B, Bin Abdulhak A, Birbeck G, Blyth F, Bolliger I, Boufous S, Bucello C, Burch M, Burney P, Carapetis J, Chen H, Chou D, Chugh SS, Coffeng LE, Colan SD, Colquhoun S, Col-son KE, Condon J, Connor MD, Cooper LT, Corriere M, Cortinovis M, deVaccaro KC, Couser W, Cowie BC, Criqui MH, Cross M, Dabhadkar KC, Dahodwala N, De Leo D, Degenhardt L, Delossantos A, Denenberg J, Des Jar-lais DC, Dharmaratne SD, Dorsey ER, Driscoll T, Duber H, Ebel B, Erwin PJ, Espindola P, Ezzati M, Feigin V, Flaxman AD, Forouzanfar MH, Fowkes FG, Franklin R, Fransen M, Freeman MK, Gabriel SE, Gakidou E, Gaspari F, Gillum RF, Gonzalez-Medina D, Halasa YA, Haring D, Harrison JE, Havmoeller R, Hay RJ, Hoen B, Hotez PJ, Hoy D, Jacobsen KH, James SL, Jasrasaria R, Jayaraman S, Johns N, Karthikeyan G, Kassebaum N, Keren A, Khoo JP, Knowlton LM, Kobusingye O, Koranteng A, Krishnamurthi R, Lipnick M, Lipshultz SE, Ohno SL, Mabweijano J, MacIntyre MF, Mallinger L, March L, Marks GB, Marks R, Matsumori A, Matzopoulos R, Mayosi BM, McAnulty JH, McDermott MM, McGrath J, Mensah GA, Merriman TR, Michaud C, Miller M, Miller TR, Mock C, Mocumbi AO, Mokdad AA, Moran A, Mulholland K, Nair MN, Naldi L, Narayan KM, Nasseri K, Norman P, O'Donnell M, Omer SB, Ortblad K, Osborne R, Ozgediz D, Pahari B, Pandian JD, Rivero AP, Padilla RP, Perez-Ruiz F, Perico N, Phillips D, Pierce K, Pope CA, 3rd Porrini E, Pourmalek F, Raju M, Ranganathan D, Rehm JT, Rein DB, Remuzzi G, Rivara FP, Roberts T, De Leon FR, Rosenfeld LC, Rushton L, Sacco RL, Salomon JA, Sampson U, Sanman E, Schwebel DC, Segui-Gomez M, Shepard DS, Singh D, Singleton J, Sliwa K, Smith E, Steer A, Taylor JA, Thomas B, Tleyjeh IM, Towbin JA, Truelsen T, Undurraga EA, Venketasubramanian N, Vijayakumar L, Vos T, Wagner GR, Wang M, Wang W, Watt K, Weinstock MA, Weintraub R, Wilkinson JD, Woolf AD, Wulf S, Yeh PH, Yip P, Zabetian A, Zheng ZJ, Lopez AD, Murray CJ, AlMazroa MA, Memish ZA, , 2012. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380: 20952128.[Crossref]
  6. World Health Organization, 2002. Malaria, Filariasis, and Other Parasitic Diseases. Geneva: World Health Organization.
  7. Brooker S, Akhwale W, Pullan RL, Estambale B, Clarke SE, Snow RW, Hotez PJ, , 2007. Epidemiology of Plasmodium-helminth co-infection in Africa: populations at risk, potential impact on anemia, and prospects for combining control. Am J Trop Med Hyg 77: 8898.
  8. Mwangi TW, Bethony J, Brooker S, , 2006. Malaria and helminth interactions in humans: an epidemiological viewpoint. Ann Trop Med Parasitol 100: 551570.[Crossref]
  9. Nacher M, , 2011. Interactions between worms and malaria: good worms or bad worms? Malar J 10: 16.[Crossref]
  10. Anonymous, 2014. Ilero Town in Nigeria. Available at: http://www.fallingrain.com/world/NI/00/Ilero.html. Accessed August 21, 2014.
  11. Adebiyi AO, Asuzu MC, , 2009. Condom use amongst out of school youths in a local government area in Nigeria. Afr Health Sci 9: 9297.
  12. Baird JK, , 1998. Age-dependent characteristics of protection versus susceptibility to Plasmodium falciparum . Ann Trop Med Parasitol 92: 367390.[Crossref]
  13. Pinkevych M, Petravic J, Chelimo K, Kazura JW, Moormann AM, Davenport MP, , 2012. The dynamics of naturally acquired immunity to Plasmodium falciparum infection. PLOS Comput Biol 8: e1002729.[Crossref]
  14. Brutus L, Watier L, Hanitrasoamampionona V, Razanatsoarilala H, Cot M, , 2007. Confirmation of the protective effect of Ascaris lumbricoides on Plasmodium falciparum infection: results of a randomized trial in Madagascar. Am J Trop Med Hyg 77: 10911095.
  15. Kiggundu VL, O'Meara WP, Musoke R, Nalugoda FK, Kigozi G, Baghendaghe E, Lutalo T, Achienge MK, Reynolds SJ, Makumbi F, Serwadda D, Gray RH, Wools-Kaloustian KK, , 2013. High prevalence of malaria parasitemia and anemia among hospitalized children in Rakai, Uganda. PLoS ONE 8: 16.[Crossref]
  16. Kinung'hi SM, Magnussen P, Kaatano GM, Kishamawe C, Vennervald BJ, , 2014. Malaria and helminth co-infections in school and preschool children: a cross-sectional study in Magu District, north-western Tanzania. PLoS ONE 9: e86510.[Crossref]
  17. Specht S, Hoerauf A, , 2007. Does helminth elimination promote or prevent malaria? Lancet 369: 446447.[Crossref]
  18. Strunz E, , 2011. Expanding the Deworming Program in Nigeria. Available at: http://www.childrenwithoutworms.org/. Accessed November 6, 2014.
  19. Midzi N, Mtapuri-Zinyowera S, Sangweme D, Paul NH, Makware G, Mapingure MP, Brouwer KC, Mudzori J, Hlerema G, Chadukura V, Mutapi F, Kumar N, Mduluza T, , 2011. Efficacy of integrated school based de-worming and prompt malaria treatment on helminthes-Plasmodium falciparum co-infections: a 33 months follow up study. BMC Int Health Hum Rights 11: 9.[Crossref]
  20. Mwinzi PNM, Montgomery SP, Owaga CO, Mwanje M, Muok EM, Ayisi JG, Laserson KF, Muchiri EM, Secor WE, Karanja DMS, , 2012. Integrated community-directed intervention for schistosomiasis and soil transmitted helminthes in western Kenya – a pilot study. Parasit Vectors 5: 110.[Crossref]
  21. Stewart GR, Boussinesq M, Coulson T, Elson L, Nutman T, Bradley JE, , 1999. Onchocerciasis modulates the immune response to mycobacterial antigens. Clin Exp Immunol 117: 517523.[Crossref]
  22. Sabin EA, Araujo MI, Carvalho EM, Pearce EJ, , 1996. Impairment of tetanus toxoid-specific Th1-likeimmune responses in humans infected with Schistosoma mansoni . J Infect Dis 173: 269272.[Crossref]
  23. Cooper PJ, Chico ME, Losonsky G, Sandoval C, Espinel I, Sridhara R, Aguilar M, Guevara A, Guderian RH, Levine MM, Griffin GE, Nutman TB, , 2000. Albendazole treatmentof children with ascariasis enhances the vibriocidal antibody response to the live attenuated oral cholera vaccine CVD 103-HgR. J Infect Dis 182: 11991206.[Crossref]
  24. Da'Dara AA, Lautsch N, Dudek T, Novitsky V, Lee TH, Essex M, Harn DA, , 2006. Helminth infection suppresses T-cell immune response to HIV-DNA-based vaccine in mice. Vaccine 24: 52115219.[Crossref]
  25. Cruz-Chan JV, Rosado-Vallado M, Dumonteil E, , 2010. Malaria vaccine efficacy: overcoming the helminth hurdle. Expert Rev Vaccines 9: 707711.[Crossref]
  26. Noland GS, Chowdhury DR, Urban JF, Jr Zavala F, Kumar N, , 2010. Helminth infection impairs the immunogenicity of a Plasmodium falciparum DNA vaccine, but not irradiated sporozoites, in mice. Vaccine 28: 29172923.[Crossref]
  27. Su Z, Segura M, Stevenson MM, , 2006. Reduced protective efficacy of a blood-stage malaria vaccine by concurrent nematode infection. Infect Immun 74: 21382144.[Crossref]
  28. Elias D, Wolday D, Akuffo H, Petros B, Bronner U, Britton S, , 2001. Effect of deworming on human T cell responses to mycobacterial antigens in helminth-exposed individuals before and after bacilli Calmette-Guerin (BCG) vaccination. Clin Exp Immunol 123: 219225.[Crossref]
  29. Ghosh K, Wu W, Antoine AD, Bottazzi ME, Valenzuela JG, Hotez PJ, Mendez S, , 2006. The impact of concurrent and treated Ancylostoma ceylanicum hookworm infections on the immunogenicity of a recombinant hookworm vaccine in hamsters. J Infect Dis 193: 155162.[Crossref]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.14-0548
Loading
/content/journals/10.4269/ajtmh.14-0548
Loading

Data & Media loading...

  • Received : 30 Aug 2014
  • Accepted : 11 Nov 2014

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error