Volume 76, Issue 6
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645


Helminth infections are prevalent in malaria-endemic areas, yet the potential for helminths to alter malaria transmission has not been closely examined. We used the murine model of co-infection to assess the impact of helminth co-infection on malaria transmission. In four replicate experiments, mosquitoes exposed to co-infected mice five days post-malaria infection had a higher rate of infectivity (80.1%, n = 241) than those exposed to malaria only–infected mice (72.0%, n = 232, = 0.039). Intensity of malaria parasite transmission was also greater, with approximately two-fold more oocysts (geometric mean = 19.2 versus 10.5, = 0.004) and an increase in sporozoite burden observed in mosquitoes exposed to co-infected mice. Malaria parasite prevalence and anemia were similar between co-infected and malaria only–infected mice, which suggested that enhanced malaria parasite transmission was due to helminth-induced modulation of host responses.


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  1. Karunaweera ND, Carter R, Grau GE, Kwiatkowski D, del Giudice G, Mendis KN, 1992. Tumour necrosis factor-dependent parasite-killing effects during paroxysms in non-immune Plasmodium vivax malaria patients. Clin Exp Immunol 88 : 499–505. [Google Scholar]
  2. Naotunne TS, Karunaweera ND, Del Giudice G, Kularatne MU, Grau GE, Carter R, Mendis KN, 1991. Cytokines kill malaria parasites during infection crisis: extracellular complementary factors are essential. J Exp Med 173 : 523–529. [Google Scholar]
  3. Kaushal DC, Carter R, Rener J, Grotendorst CA, Miller LH, Howard RJ, 1983. Monoclonal antibodies against surface determinants on gametes of Plasmodium gallinaceum block transmission of malaria parasites to mosquitoes. J Immunol 131 : 2557–2562. [Google Scholar]
  4. Rener J, Graves PM, Carter R, Williams JL, Burkot TR, 1983. Target antigens of transmission-blocking immunity on gametes of Plasmodium falciparum. J Exp Med 158 : 976–981. [Google Scholar]
  5. Naotunne TD, Rathnayake KD, Jayasinghe A, Carter R, Mendis KN, 1990. Plasmodium cynomolgi: serum-mediated blocking and enhancement of infectivity to mosquitoes during infections in the natural host, Macaca sinica. Exp Parasitol 71 : 305–313. [Google Scholar]
  6. Peiris JS, Premawansa S, Ranawaka MB, Udagama PV, Munasinghe YD, Nanayakkara MV, Gamage CP, Carter R, David PH, Mendis KN, 1988. Monoclonal and polyclonal antibodies both block and enhance transmission of human Plasmodium vivax malaria. Am J Trop Med Hyg 39 : 26–32. [Google Scholar]
  7. Butcher GA, Sinden RE, Billker O, 1996. Plasmodium berghei: infectivity of mice to Anopheles stephensi mosquitoes. Exp Parasitol 84 : 371–379. [Google Scholar]
  8. de Silva NR, Brooker S, Hotez PJ, Montresor A, Engels D, Savioli L, 2003. Soil-transmitted helminth infections: updating the global picture. Trends Parasitol 19 : 547–551. [Google Scholar]
  9. Mwangi TW, Bethony JM, Brooker S, 2006. Malaria and helminth interactions in humans: an epidemiological viewpoint. Ann Trop Med Parasitol 100 : 551–570. [Google Scholar]
  10. Buck AA, Anderson RI, MacRae AA, 1978. Epidemiology of poly-parasitism. IV. combined effects on the state of health. Trop Med Parasitol 29 : 253–268. [Google Scholar]
  11. Nacher M, Singhasivanon P, Yimsamran S, Manibunyong W, Thanyavanich N, Wuthisen R, Looareesuwan S, 2002. Intestinal helminth infections are associated with increased incidence of Plasmodium falciparum malaria in Thailand. J Parasitol 88 : 55–58. [Google Scholar]
  12. Spiegel A, Tall A, Raphenon G, Trape JF, Druilhe P, 2003. Increased frequency of malaria attacks in subjects co-infected by intestinal worms and Plasmodium falciparum malaria. Trans R Soc Trop Med Hyg 97 : 198–199. [Google Scholar]
  13. Le Hesran JY, Akiana J, Ndiaye EH, Dia M, Senghor P, Konate L, 2004. Severe malaria attack is associated with high prevalence of Ascaris lumbricoides infection among children in rural Senegal. Trans R Soc Trop Med Hyg 98 : 397–399. [Google Scholar]
  14. Sokhna C, Le Hesran JY, Mbaye PA, Akiana J, Camara P, Diop M, Ly A, Druilhe P, 2004. Increase of malaria attacks among children presenting concomitant infection by Schistosoma mansoni in Senegal. Malar J 3 : 43. [Google Scholar]
  15. Nacher M, Gay F, Singhasivanon P, Krudsood S, Treeprasertsuk S, Mazier D, Vouldoukis I, Looareesuwan S, 2000. Ascaris lumbricoides infection is associated with protection from cerebral malaria. Parasite Immunol 22 : 107–113. [Google Scholar]
  16. Nacher M, Singhasivanon P, Silachamroon U, Treeprasertsuk S, Vannaphan S, Traore B, Gay F, Looareesuwan S, 2001. Helminth infections are associated with protection from malaria-related acute renal failure and jaundice in Thailand. Am J Trop Med Hyg 65 : 834–836. [Google Scholar]
  17. Lyke KE, Dicko A, Dabo A, Sangare L, Kone A, Coulibaly D, Guindo A, Traore K, Daou M, Diarra I, Sztein MB, Plowe CV, Doumbo OK, 2005. Association of Schistosoma haematobium infection with protection against acute Plasmodium falciparum malaria in Malian children. Am J Trop Med Hyg 73 : 1124–1130. [Google Scholar]
  18. Briand V, Watier L, Hesran JY, Garcia A, Cot M, 2005. Coin-fection with Plasmodium falciparum and Schistosoma haematobium: protective effect of schistosomiasis on malaria in Senegalese children? Am J Trop Med Hyg 72 : 702–707. [Google Scholar]
  19. Brutus L, Watier L, Briand V, Hanitrasoamampionona V, Razanatsoarilala H, Cot M, 2006. Parasitic co-infections: Does As-caris lumbricoides protect against Plasmodium falciparum infection? Am J Trop Med Hyg 75 : 194–198. [Google Scholar]
  20. Lwin M, Last C, Targett GA, Doenhoff MJ, 1982. Infection of mice concurrently with Schistosoma mansoni and rodent malarias: contrasting effects of patent S. mansoni infections on Plasmodium chabaudi, P. yoelii and P. berghei. Ann Trop Med Parasitol 76 : 265–273. [Google Scholar]
  21. Christensen NØ, Furu P, Kurtzhals J, Odaibo A, 1988. Heterologous synergistic interactions in concurrent experimental infection in the mouse with Schistosoma mansoni, Echinostoma revolutum, Plasmodium yoelii, Babesia microti, and Trypanosoma brucei. Parasitol Res 74 : 544–551. [Google Scholar]
  22. Noland GS, Graczyk TK, Fried B, Fitzgerald EJ, Kumar N, 2005. Exacerbation of Plasmodium yoelii malaria in Echinostoma caproni infected mice and abatement through anthelmintic treatment. J Parasitol 91 : 944–948. [Google Scholar]
  23. Helmby H, Kullberg M, Troye-Blomberg M, 1998. Altered immune responses in mice with concomitant Schistosoma mansoni and Plasmodium chabaudi infections. Infect Immun 66 : 5167–5174. [Google Scholar]
  24. Yoshida A, Maruyama H, Kumagai T, Amano T, Kobayashi F, Zhang M, Himeno K, Ohta N, 2000. Schistosoma mansoni infection cancels the susceptibility to Plasmodium chabaudi through induction of type 1 immune responses in A/J mice. Int Immunol 12 : 1117–1125. [Google Scholar]
  25. Su Z, Segura M, Morgan K, Loredo-Osti JC, Stevenson MM, 2005. Impairment of protective immunity to blood-stage malaria by concurrent nematode infection. Infect Immun 73 : 3531–3539. [Google Scholar]
  26. Yan Y, Inuo G, Akao N, Tsukidate S, Fujita K, 1997. Down-regulation of murine susceptibility to cerebral malaria by inoculation with third-stage larvae of the filarial nematode Brugia pahangi. Parasitology 114 : 333–338. [Google Scholar]
  27. Graham AL, Lamb TJ, Read AF, Allen JE, 2005. Malaria-filaria coinfection in mice makes malarial disease more severe unless filarial infection achieves patency. J Infect Dis 191 : 410–421. [Google Scholar]
  28. Bastien P, Landau I, Baccam D, 1987. Inhibition of the infectivity of Plasmodium gametocytes by the serum of the parasite host. Perfecting an experimental model. Ann Parasitol Hum Comp 62 : 195–208. [Google Scholar]
  29. Nacher M, Singhasivanon P, Silachamroon U, Treeprasertsu S, Krudsood S, Gay F, Mazier D, Looareesuwan S, 2001. Association of helminth infections with increased gametocyte carriage during mild falciparum malaria in Thailand. Am J Trop Med Hyg 65 : 644–647. [Google Scholar]
  30. Mellor PS, Boorman J, 1980. Multiplication of bluetongue virus in Culicoides nubeculosus (Meigen) simultaneously infected with the virus and the microfilariae of Onchocerca cervicalis (Railliet & Henry). Ann Trop Med Parasitol 74 : 463–469. [Google Scholar]
  31. Paulson SL, Poirier SJ, Grimstad PR, Craig GB Jr, 1992. Vector competence of Aedes hendersoni (Diptera: Culicidae) for la crosse virus: Lack of impaired function in virus-infected salivary glands and enhanced virus transmission by sporozoite-infected mosquitoes. J Med Entomol 29 : 483–488. [Google Scholar]
  32. Turell MJ, Mather TN, Spielman A, Bailey CL, 1987. Increased dissemination of dengue 2 virus in Aedes aegypti associated with concurrent ingestion of microfilariae of Brugia malayi. Am J Trop Med Hyg 37 : 197–201. [Google Scholar]
  33. Vaughan JA, Turell MJ, 1996. Dual host infections: enhanced infectivity of eastern equine encephalitis virus to Aedes mosquitoes mediated by Brugia microfilariae. Am J Trop Med Hyg 54 : 105–109. [Google Scholar]
  34. Vaughan JA, Turell MJ, 1996. Facilitation of rift valley fever virus transmission by Plasmodium berghei sporozoites in Anopheles stephensi mosquitoes. Am J Trop Med Hyg 55 : 407–409. [Google Scholar]
  35. Vaughan JA, Trpis M, Turell MJ, 1999. Brugia malayi microfilariae (Nematoda: Filaridae) enhance the infectivity of Venezuelan equine encephalitis virus to Aedes mosquitoes (Diptera: Culicidae). J Med Entomol 36 : 758–763. [Google Scholar]
  36. Zytoon EM, el Belbasi HI, Matsumura T, 1993. Mechanism of increased dissemination of Chikungunya virus in Aedes albopictus mosquitoes concurrently ingesting microfilariae of Dirofilaria immitis. Am J Trop Med Hyg 49 : 201–207. [Google Scholar]
  37. Burkot TR, Molineaux L, Graves PM, Paru R, Battistutta D, Dagoro H, Barnes A, Wirtz RA, Garner P, 1990. The prevalence of naturally acquired multiple infections of Wuchereria bancrofti and human malarias in anophelines. Parasitology 100 : 369–375. [Google Scholar]
  38. Munderloh UG, Kurtti TJ, 1987. The infectivity and purification of cultured Plasmodium berghei ookinetes. J Parasitol 73 : 919–923. [Google Scholar]
  39. Ponnudurai T, Lensen AH, Van Gemert GJ, Bensink MP, Bolmer M, Meuwissen JH, 1989. Infectivity of cultured Plasmodium falciparum gametocytes to mosquitoes. Parasitology 98 : 165–173. [Google Scholar]
  40. Haji H, Smith T, Charlwood JD, Meuwissen JH, 1996. Absence of relationships between selected human factors and natural infectivity of Plasmodium falciparum to mosquitoes in an area of high transmission. Parasitology 113 : 425–431. [Google Scholar]
  41. Sinden RE, Butcher GA, Billker O, Fleck SL, 1996. Regulation of infectivity of Plasmodium to the mosquito vector. Adv Parasitol 38 : 53–117. [Google Scholar]
  42. Gautret P, Gantier JC, Baccam D, Miltgen F, Saulai M, Chabaud AG, Landau I, 1996. The gametocytes of Plasmodium vinckei petteri, their morphological stages, periodicity and infectivity. Int J Parasitol 26 : 1095–1101. [Google Scholar]
  43. Gautret P, Miltgen F, Chabaud AG, Landau I, 1996. Synchronized Plasmodium yoelii yoelii: pattern of gametocyte production, sequestration and infectivity. Parassitologia 38 : 575–577. [Google Scholar]
  44. Gautret P, Miltgen F, Gantier JC, Chabaud AG, Landau I, 1996. Enhanced gametocyte formation by Plasmodium chabaudi in immature erythrocytes: pattern of production, sequestration, and infectivity to mosquitoes. J Parasitol 82 : 900–906. [Google Scholar]
  45. Wargo AR, Randle N, Chan BH, Thompson J, Read AF, Babiker HA, 2006. Plasmodium chabaudi: reverse transcription PCR for the detection and quantification of transmission stage malaria parasites. Exp Parasitol 112 : 13–20. [Google Scholar]
  46. Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A, Xiao S, 2004. Hookworm infection. N Engl J Med 351 : 799–807. [Google Scholar]
  47. Friedman JF, Kanzaria HK, McGarvey ST, 2005. Human schistosomiasis and anemia: The relationship and potential mechanisms. Trends Parasitol 21 : 386–392. [Google Scholar]
  48. Price R, Nosten F, Simpson JA, Luxemburger C, Phaipun L, ter Kuile F, van Vugt M, Chongsuphajaisiddhi T, White NJ, 1999. Risk factors for gametocyte carriage in uncomplicated falciparum malaria. Am J Trop Med Hyg 60 : 1019–1023. [Google Scholar]
  49. Wisnewski N, Fried B, Halton DW, 1986. Growth and feeding of Echinostoma revolutum on the chick chorioallantois and in the domestic chick. J Parasitol 72 : 684–689. [Google Scholar]
  50. Taylor PJ, Hurd H, 2001. The influence of host haematocrit on the blood feeding success of Anopheles stephensi: implications for enhanced malaria transmission. Parasitology 122 : 491–496. [Google Scholar]
  51. Murray J, Murray A, Murray M, Murray C, 1978. The biological suppression of malaria: an ecological and nutritional interrelationship of a host and two parasites. Am J Clin Nutr 31 : 1363–1366. [Google Scholar]

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  • Received : 16 Nov 2006
  • Accepted : 13 Feb 2007

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