From host immunity to pathogen invasion: The effects of helminth coinfection on the dynamics of microparasites

Integrative and Comparative Biology

Volumn 51, Issue 4, 2011, Pages 540-551

  Ezenwa, Vanessa O ^a   Jolles, Anna E ^b  

^a UNIVERSITY OF GEORGIA   (United States)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ANIMAL DISEASE; BACTERIAL INFECTION; BIOLOGICAL MODEL; BUFFALO; CONFERENCE PAPER; DISEASE TRANSMISSION; HELMINTH; HELMINTHIASIS; HOST PARASITE INTERACTION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; MICROBIOLOGY; MIXED INFECTION; MYCOBACTERIUM BOVIS; NEMATODE; NEMATODIASIS; PARASITOLOGY; PHYSIOLOGY; TUBERCULOSIS;

ANIMALS; BACTERIAL INFECTIONS; BUFFALOES; COINFECTION; HELMINTHIASIS; HELMINTHS; HOST-PARASITE INTERACTIONS; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; MODELS, BIOLOGICAL; MYCOBACTERIUM BOVIS; NEMATODA; NEMATODE INFECTIONS; TUBERCULOSIS;

SYNCERUS CAFFER; VERMES;

EID: 80053259523     PISSN: 15407063     EISSN: 15577023     Source Type: Journal    
DOI: 10.1093/icb/icr058     Document Type: Conference Paper

References (71)

1. Abu-Raddad LJ, Patnaik P, Kublin JG. 2006. Dual infection with HIV and malaria fuels the spread of both diseases in sub-Saharan Africa. Science 314:1603-6. (Pubitemid 44907155)
2. Bradley JE, Jackson JA. 2008. Measuring immune system variation to help understand host-pathogen community dynamics. Parasitol 135:807-23. (Pubitemid 351913468)
3. Brady MJ, O'Neill SM, Dalton JP, Mills KHG. 1999. Fasciola hepatica suppresses a protective Th1 response against Bordetella pertussis. Infect Immunol 67:5372-8. (Pubitemid 29455315)
4. Briand V, Watier L, Le Hesran JY, Garcia A, Cot M. 2005. Coinfection with Plasmodium falciparum and Schistosoma haematobium: protective effect of schistosomiasis on malaria in Senegalese children. Am J Trop Med Hyg 72:702-7. (Pubitemid 41278787)
5. Brown M, Kizza M, Watera C, Quigley MA, Rowland S, Hughes P, Whitworth JAG, Elliott AM. 2004. Helminth infection is not associated with faster progression of HIV disease in coinfected adults in Uganda. J Infect Dis 190:1869-79. (Pubitemid 39487834)
6. Brown M, Mawa PA, Kaleebu P, Elliott AM. 2006a. Helminths and HIV infection: epidemiological observations on immunological hypotheses. Paras Immunol 28:613-23. (Pubitemid 44581387)
7. Brown M, Miiro G, Nkurunziza P, Watera C, Quigley MA, Dunne DW, Whitworth JAG, Elliott AM. 2006b. Schistosoma mansoni, nematode infections, and progression to active tuberculosis among HIV-1 infected Ugandans. Am J Trop Med Hyg 74:819-25. (Pubitemid 46774403)
8. Bruce MC, Donnelly CA, Alpers MP, Galinski MR, Barnwell JW, Walliker D, Day KP. 2000. Cross-species interactions between malaria parasites in humans. Science 287:845-8. (Pubitemid 30084325)
9. Cattadori IM, Albert R, Boag B. 2007. Variation in host susceptibility and infectiousness generated by co-infection: the myxoma-Trichostrongylus retortaeformis case in wild rabbits. J R Soc Interface 4:831-40. (Pubitemid 47523489)
10. Chandra RK. 1996. Nutrition, immunity and infection: From basic knowledge of dietary manipulation of immune responses to practical application of ameliorating suffering and improving survival. PNAS 93:14304-7. (Pubitemid 26418958)
11. Chen CC, Louie S, McCormick B, Walker WA, Shi HN. 2005. Concurrent infection with an intestinal helminth parasite impairs host resistance to enteric Citrobacter rodentium and enhances Citrobacter-induced colitis in mice. Infect Immun 73:5468-81. (Pubitemid 41192981)
12. Co TR, Hirsch CS, Toossi Z, Dietze R, Ribeiro-Rodrigues R. 2007. Intestinal helminth coinfection has a negative impact on both anti-Mycobacterium tuberculosis immunity and clinical response to tuberculosis therapy. Clin Exp Immunol 147:45-52. (Pubitemid 44915554)
13. Diniz LM, Magalhaes EFL, Pereira FEL, Dietze R, Ribeiro-Rodrigues R. 2010. Presence of intestinal helminths decreases T helper type 1 responses in tuberculoid leprosy patients and may increase the risk for multi-bacillary leprosy. Clin Exp Immunol 161:142-50.
14. Edwards MJ, Buchatska O, Ashton M, Montoya M, Bickle QD, Borrow P. 2005. Reciprocal immunomodulation in a Schistosome and hepatotropic virus coinfection model. J Immunol 175:6275-85. (Pubitemid 41598866)
15. Elias D, Akuffo H, Thors C, Pawlowski A, Britton S. 2005. Low dose chronic Schistosoma mansoni infection increases susceptibility to Mycobacterium bovis BCG infection in mice. Clin Exp Immunol 139:398-404. (Pubitemid 40333250)
16. Elliott AM, Mawa PA, Joseph S, Namujju PB, Kizza M, Nakiyingi JS, Watera C, Dunne DW, Whitworth JAG. 2003. Associations between helminth infection and CD4 T cell count, viral load and cytokine responses in HIV-1 infected Ugandan adults. Trans R Soc Trop Med Hyg 97:103-8. (Pubitemid 36874058)
17. Else KJ, Finkelman FD. 1998. Intestinal nematode parasites, cytokines and effector mechanisms. Int J Parasitol 28:1145-58. (Pubitemid 28386909)
18. Eraud C, Trouve C, Dano S, Chastel O, Faivre B. 2008. Competition for resources modulates cell-mediated immunity and stress hormone level in nested collared doves (Streptopelia decaocto). Gen Comp End 155: 542-51. (Pubitemid 351200509)
19. Erb KJ, Trujillo C, Fugate M, Moll H. 2002. Infection with the helminth Nippostrongylus brasiliensis does not interfere with efficient elimination of Mycobacterium bovis BCG from the lungs of mice. Clin Diagn Lab Immunol 9:727-30. (Pubitemid 34538242)
20. Ezenwa VO, Etienne RS, Luikart G, Beja-Pereira A, Jolles AE. 2010. Hidden consequences of living in a wormy world: nematode-induced immune suppression facilitates tuberculosis invasion in African Buffalo. Am Nat 176:613-24.
21. Eziefula AC, Brown M. 2008. Intestinal nematodes: disease burden, deworming and the potential importance of co-infection. Curr Opin Infect Dis 21:516-22.
22. Fenton A. 2008. Worms and germs: the population dynamic consequences of microparasite-macroparasite co-infection. Parasitology 135:1545-60.
23. Frantz FG, Silva Rosada R, Turato WM, Peres CM, Coelho-Castelo AAM, Ramos SG, Aronoff DM, Silva CL, Faccioli LH. 2007. The immune response to toxocariasis does not modify susceptibility to Mycobacterium tuberculosis infection in BALB/c mice. Am J Trop Med Hyg 77:691-8. (Pubitemid 351844294)
24. Furze RC, Hussell T, Selkirk ME. 2006. Amelioration of influenza-induced pathology in mice by coinfection with Trichinella spiralis. Infect Immun 74:1924-32. (Pubitemid 43346830)
25. Gallagher M, et al. 2005. The effects of maternal helminth and malaria infections on mother-to-child HIV transmission. AIDS 19:1849-55. (Pubitemid 41546604)
26. Gibson LR, Li B, Remold SK. 2010. Treating cofactors can reverse the expansion of a primary disease epidemic. BMC Infect Dis 10:248.
27. Graham AL. 2008. Ecological rules governing helminth-microparasite coinfection. Proc Natl Acad Sci 105: 566-70. (Pubitemid 351171748)
28. Graham AL, Cattadori IM, Lloyd-Smith JO, Ferrari MJ, Bjornstad ON. 2007. Transmission consequences of coinfection: Cytokines writ large? Trends Parasitol 23:284-91. (Pubitemid 46771350)
29. 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 191:410-21. (Pubitemid 40139767)
30. Hartgers FC, Yazdanbakhsh M. 2006. Co-infection of helminths and malaria: modulation of the immune responses to malaria. Paras Immunol 28:497-506. (Pubitemid 44370855)
31. Hawley DM, Altizer SM. 2011. Disease ecology meets ecological immunology: understanding the links between organ-ismal immunity and infection dynamics in natural populations. Funct Ecol 25:48-60.
32. Hosseinipour MC, Napravnik S, Joaki G, Gama S, Mbeye N, Banda B, Martinson F, Hoffman I, Cohen MS. 2007. HIV and parasitic infection and the effect of treatment among adult outpatients in Malawi. J Infect Dis 195:1278-82. (Pubitemid 46649612)
33. Hotez PJ. 2009. Mass drug administration and integrated control for the world's high-prevalenceneglected tropical diseases. Clin Pharmacol Therapeut 85:659-64.
34. Jolles AE, Ezenwa VO, Etienne RS, Turner WC, Olff H. 2008. Interactions between macroparasites and microparasites drive infection patterns in free-ranging African buffalo. Ecology 89:2239-50.
35. Kamal SM, El Sayed Khalifa K. 2006. Immune modulation by helminthic infections: worms and viral infections. Paras Immunol 28:483-96. (Pubitemid 44370854)
36. Karp CL, Auwaerter PG. 2007. Coinfection with HIV and tropical infectious diseases. II.helminthic, fungal, bacterial, and viral pathogens. Clin Infect Dis 45:1214-20. (Pubitemid 47580324)
37. Keesing F, et al. 2010. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647-52.
38. Lamb TJ, Graham AL, Le Goff L, Allen JE. 2005. Co-infected C57BL/6 mice mount appropriately polarized and compartmentalized cytokine responses to Litomosoides sigmodontis and Leishmania major but disease progression is altered. Paras Immunol 27:317-24. (Pubitemid 41360826)
39. Legesse M, Erko B, Balcha F. 2004. Increased parasitaemia and delayed parasite clearance in Schistosoma mansoni and Plasmodium berghei coinfected mice. Acta Trop 91:161-6. (Pubitemid 38952717)
40. Lloyd-Smith JO, Poss M, Grenfell BT. 2008. HIV-1/parasite co-infection and the emergence ofnew parasite strains. Parasitology 135:795-806. (Pubitemid 351913466)
41. Lloyd-Smith JO, Schreiber SJ, Kopp PE, Getz WM. 2005. Superspreading and the effect of individual variation on disease emergence. Nature 438:355-9. (Pubitemid 41643951)
42. Long KZ, Nanthakumar N. 2004. Energetic and nutritional regulation of the adaptive immune response and tradeoffs in ecological immunology. Am J Human Biol 16:499-507. (Pubitemid 39199844)
43. Lyke KE, et al. 2005. Association of Schistosoma haematobium infection with protection against acute Plasmodium falcip-arum malaria in Malian children. Am J Trop Med Hyg 73:1124-30. (Pubitemid 43038266)
44. Maizels RM, Balic A, Gomez-Escobar N, Nair MD, Taylor M, Allen JE. 2004. Helminth parasites-masters of regulation. Immunol Rev 201:89-116.
45. Martin LB, Navara KJ, Weil ZM, Nelson RJ. 2007. Immunological memory is compromised by food restriction in deer mice Peromyscus maniculatus. Am J Physiol-Reg Integr Comp Physiol 292:R316-20. (Pubitemid 46089843)
46. May RM, Gupta S, McLean AR. 2001. Infectious disease dynamics: what characterizes a successful invader? Phil Trans R Soc B 356:901-10. (Pubitemid 32614665)
47. Miller CMD, Smith NC, Ikin RJ, Boulter NR, Dalton JP, Donnelly S. 2009. Immunological interactions between 2 common pathogens, Th1-inducing protozoan Toxoplasma gondii and the Th2-inducing helminth Fasciola hepatica. PloS One 4:e5692.
48. Modjarrad K, Zulu I, Redden DT, Njobvu L, Lane HC, Bentwich Z, Vermund SH. 2005. Treatment of intestinal helminths does not reduce plasma concentrations of HIV-1 RNA in coinfected Zambian adults. J Infect Dis 192:1277-83. (Pubitemid 41368430)
49. Moreau E, Chauvin A. 2010. Immunity against helminths: Interactions with the host and the intercurrent infections. J Biomed Biotech 2010:42893.
50. Mosmann TR, Sad S. 1996. The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol Today 17:138-46. (Pubitemid 26074503)
51. Neto LMS, de Vasconcellos Carvalhaes de Oliveira R, Totino PR, Sant'Anna FM, Coelho VD, Rolla VC, Zanini GM. 2010. Enteroparasitosis prevalence and parasitism influence in clinical outcomes of tuberculosis patients with or without HIV co-infection in a reference hospital in Rio de Janeiro (2000-2006). Braz J Infect Dis 13:427-32.
52. Nmorsi O, Isaac C, Ukwandu NCD. 2009. Schistosoma hae-matobium and Plasmodium falciparum co-infection with protection against Plasmodium falciparum malaria in Nigerian children. As Pac J Trop Med 2:16-20.
53. Pedersen AB, Babayan RK. 2011. Wild immunology. Mol Ecol 20:872-80.
54. Pedersen AB, Fenton A. 2007. Emphasizing the ecology in parasite community ecology. Trends Ecol Evol 22:133-9. (Pubitemid 46273826)
55. Petney TN, Andrews RH. 1998. Multiparasite communities in animals and humans: Frequency, structure and pathogenic significance. Int J Parasitol 28:377-93. (Pubitemid 28156768)
56. Rodriguez-Sosa M, Rivera-Montoya I, Espinoza A, Romero-Grijalva M, Lopez-Flores R, Gonzales J, Terrazas LI. 2006. Acute cysticercosis favours rapid and more severe lesions caused by Leishmania major and Leishmania mexicana infection, a role for alternatively activated macrophages. Cell Immunol 242:61-71. (Pubitemid 46496968)
57. Sangweme DT, Midzi N, Zinyowera-Mutapuri S, Mduluza T, Diener-West M, Kumar N. 2010. Impact of Schistosome infection on Plasmodium falciparum malariometric indices and immune correlates in school age children in Burma Valley, Zimbabwe. PloS Negl Trop Dis 4:e882.
58. Sangweme DT, Shiff C, Kumar N. 2009. Plasmodium yoelii: Adverse outcomes of non-lethal P. yoelii malaria during co-infection with Schistosoma mansoni in BALB/c mouse model. Exp Parasitol 122:254-9.
59. Secor WE. 2006. Interactions between schistosomiasis and infection with HIV-1. Paras Immunol 28:597-603. (Pubitemid 44581385)
60. 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. Malaria J 3:43.
61. Specht S, Fernandez Ruiz D, Dubben B, Deininger S, Hoerauf A. 2010. Filaria-induced IL-10 suppresses murine cerebral malaria. Microb Infect 12:635-42.
62. Supali T, et al. 2010. Polyparasitism and its impact on the immune system. Int J Parasitol 40:1171-6.
63. Telfer S, Lambin X, Birtles R, Beldomenico P, Burthe S, Paterson S, Begon M. 2010. Species interactions in a parasite community drive infection risk in a wildlife population. Science 330:243-6.
64. Tompkins DM, Dunn AM, Smith MJ, Telfer S. 2011. Wildlife diseases: from individuals to ecosystems. J Animal Ecol 80:19-38.
65. van Riet E, Hartgers FC, Yazdanbakhsh M. 2007. Chronic helminth infections induce immunomodulation: Consequences and mechanisms. Immunobiology 212:475-90. (Pubitemid 46825248)
66. Waknine-Grinberg JH, Gold D, Ohayon A, Flescher E, Heyfets A, Doenhoff MJ, Schramm G, Haas H, Golenser J. 2010. Schistosoma mansoni infection reduces the incidence of murine cerebral malaria. Malaria J 9:5.
67. Walson JL, et al. 2008. Albendazole treatment of HIV-1 and helminth co-infection: a randomized, double-blind, placebo-controlled trial. AIDS 22:1601-9.
68. Wearing HJ, Rohani P. 2006. Ecological and immunological determinants of dengue epidemics. Proc Natl Acad Sci USA 103:11802-7. (Pubitemid 44182531)
69. Wolday D, Mayaan S, Mariam ZG, Berhe N, Seboxa T, Britton S, Galai N, Landay A, Bentwich Z. 2002. Treatment of intestinal worms is associated with decreased HIV plasma viral load. JAIDS 31:56-62.
70. Wolfe ND, Dunavan CP, Diamond J. 2007. Origins of major human infectious diseases. Nature 447:279-83. (Pubitemid 46788835)
71. Yoshida A, Maruyama H, Kumagai T, Amano T, Kobayashi F, Zhang MX, 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 12:1117-25. (Pubitemid 30616218)