1921
Volume 96, Issue 6
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract

More than 2 billion people are infected with parasites globally, and the majority have coinfections. Intestinal protozoa and helminths induce polarizing CD4 T-helper cell 1 (Th1) mediated cytokine responses within the host. Such immune polarization may inhibit the ability of the host to mount an adequate immune response for pathogen clearance to concurrent pathogens. The current study evaluated the plasma cytokine profile in and coinfected children compared with - and -only infected children. Fecal samples and blood samples were collected from asymptomatic 3-year-old children living in the district of Quininde, Ecuador. Stool samples that tested positive for -only, only, or and coinfections were confirmed by quantitative real-time polymerase chain reaction. Plasma samples from the study subjects were used to quantitate cytokines. A total of 39 patients were evaluated. Children with coinfection had a significant decrease in Th1 cytokine production, interleukin 2 (IL-2) ( < 0.05), IL-12 ( < 0.05), and tumor necrosis factor alpha ( < 0.05) compared with -only infected children. Coinfected children had an increase in IL-10/interferon gamma (IFN-γ) ratio compared with uninfected ( < 0.05) and alone ( < 0.05). The increased IL-10/IFN-γ ratio in the setting of decreased Th1 cytokine response indicates Th2 polarization in the coinfected group. Reduced Th1 cytokines in children coinfected with and may impair the host's ability to eradicate infection leading to chronic giardiasis.

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References

  1. Supali T, Verweij JJ, Wiria AE, Djuardi Y, Hamid F, Kaisar MMM, Wammes LJ, van Lieshout L, Luty AJF, Sartono E, Yazdanbakhsh M, , 2010. Polyparasitism and its impact on the immune system. Int J Parasitol 40: 11711176.[Crossref] [Google Scholar]
  2. Blackwell AD, Martin M, Kaplan H, Gurven M, . 2013. Antagonism between two intestinal parasites in humans: the importance of co-infection for infection risk and recovery dynamics. Proc Biol Sci 280: 20131671.[Crossref] [Google Scholar]
  3. Cox FE, , 2001. Concomitant infections, parasites and immune responses. Parasitology 122 (Suppl): S23S38. Available at: http://www.ncbi.nlm.nih.gov/pubmed/11442193. Accessed March 21, 2016.[Crossref] [Google Scholar]
  4. Lamberton PHL, Jourdan PM, , 2015. Human ascariasis: diagnostics update. Curr Trop Med Rep 2: 189200.[Crossref] [Google Scholar]
  5. Mejia R, Vicuña Y, Broncano N, Sandoval C, Vaca M, Chico M, Cooper PJ, Nutman TB, , 2013. A novel, multi-parallel, real-time polymerase chain reaction approach for eight gastrointestinal parasites provides improved diagnostic capabilities to resource-limited at-risk populations. Am J Trop Med Hyg 88: 10411047.[Crossref] [Google Scholar]
  6. Cimino RO, Jeun R, Juarez M, Cajal PS, Vargas P, Echazú A, Bryan PE, Nasser J, Krolewiecki A, Mejia R, , 2015. Identification of human intestinal parasites affecting an asymptomatic peri-urban Argentinian population using multi-parallel quantitative real-time polymerase chain reaction. Parasit Vectors 8: 380.[Crossref] [Google Scholar]
  7. Hagel I, Cabrera M, Puccio F, Santaella C, Buvat E, Infante B, Zabala M, Cordero R, Di Prisco MC, , 2011. Co-infection with Ascaris lumbricoides modulates protective immune responses against Giardia duodenalis in school Venezuelan rural children. Acta Trop 117: 189195.[Crossref] [Google Scholar]
  8. Sanchez AL, Mahoney DL, Gabrie JA, , 2015. Interleukin-10 and soil-transmitted helminth infections in Honduran children. BMC Res Notes 8: 55.[Crossref] [Google Scholar]
  9. Rafi W, Ribeiro-Rodrigues R, Ellner JJ, Salgame P, , 2012. Coinfection-helminthes and tuberculosis. Curr Opin HIV AIDS 7: 239244.[Crossref] [Google Scholar]
  10. Mouser EEIM, Pollakis G, Paxton WA, , 2012. Effects of helminths and Mycobacterium tuberculosis infection on HIV-1: a cellular immunological perspective. Curr Opin HIV AIDS 7: 260267.[Crossref] [Google Scholar]
  11. Nash TE, Herrington DA, Losonsky GA, Levine MM, , 1987. Experimental human infections with Giardia lamblia . J Infect Dis 156: 974984. Available at: http://www.ncbi.nlm.nih.gov/pubmed/3680997. Accessed March 21, 2016.[Crossref] [Google Scholar]
  12. Stark D, Barratt JLN, van Hal S, Marriott D, Harkness J, Ellis JT, , 2009. Clinical significance of enteric protozoa in the immunosuppressed human population. Clin Microbiol Rev 22: 634650.[Crossref] [Google Scholar]
  13. Lopez-Romero G, Quintero J, Astiazarán-García H, Velazquez C, , 2015. Host defences against Giardia lamblia . Parasite Immunol 37: 394406.[Crossref] [Google Scholar]
  14. Ferreira FS, Baptista-Fernandes T, Oliveira D, Rodrigues R, Neves E, Lima A, Garrido E, Afonso G, Zaky A, Telles de Freitas P, Atouguia J, Centeno-Lima S, , 2015. Giardia duodenalis and soil-transmitted helminths infections in children in São Tomé and Príncipe: do we think Giardia when addressing parasite control? J Trop Pediatr 61: 106112.[Crossref] [Google Scholar]
  15. Nash TE, Ohl CA, Thomas E, Subramanian G, Keiser P, Moore TA, , 2001. Treatment of patients with refractory giardiasis. Clin Infect Dis 33: 2228.[Crossref] [Google Scholar]
  16. Heyworth MF, , 2014. Immunological aspects of Giardia infections. Parasite 21: 55.[Crossref] [Google Scholar]
  17. Redpath SA, Fonseca NM, Perona-Wright G, , 2014. Protection and pathology during parasite infection: IL-10 strikes the balance. Parasite Immunol 36: 233252.[Crossref] [Google Scholar]
  18. Saghaug CS, Sørnes S, Peirasmaki D, Svärd S, Langeland N, Hanevik K, , 2016. Human memory CD4+ T cell immune responses against Giardia lamblia . Clin Vaccine Immunol 23: 1118.[Crossref] [Google Scholar]
  19. Cooper PJ, Chico ME, Sandoval C, Espinel I, Guevara A, Kennedy MW, Urban JF, Jr Griffin GE, Nutman TB, , 2000. Human infection with Ascaris lumbricoides is associated with a polarized cytokine response. J Infect Dis 182: 12071213.[Crossref] [Google Scholar]
  20. Ezenwa VO, Jolles AE, , 2011. From host immunity to pathogen invasion: the effects of helminth coinfection on the dynamics of microparasites. Integr Comp Biol 51: 540551.[Crossref] [Google Scholar]
  21. Curry AJ, Else KJ, Jones F, Bancroft A, Grencis RK, Dunne DW, , 1995. Evidence that cytokine-mediated immune interactions induced by Schistosoma mansoni alter disease outcome in mice concurrently infected with Trichuris muris . J Exp Med 181: 769774. Available at: http://www.ncbi.nlm.nih.gov/pubmed/7836929. Accessed March 21, 2016.[Crossref] [Google Scholar]
  22. Cooper PJ, Chico ME, Platts-Mills TA, Rodrigues LC, Strachan DP, Barreto ML, , 2015. Cohort profile: the Ecuador Life (ECUAVIDA) study in Esmeraldas Province, Ecuador. Int J Epidemiol 44: 15171527.[Crossref] [Google Scholar]
  23. Cooper PJ, Chico ME, Guadalupe I, Sandoval CA, Mitre E, Platts-Mills TAE, Barreto ML, Rodrigues LC, Strachan DP, Griffin GE, , 2011. Impact of early life exposures to geohelminth infections on the development of vaccine immunity, allergic sensitization, and allergic inflammatory diseases in children living in tropical Ecuador: the ECUAVIDA birth cohort study. BMC Infect Dis 11: 184.[Crossref] [Google Scholar]
  24. Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ, , 2006. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet (London, England) 367: 15211532.[Crossref] [Google Scholar]
  25. Griffiths EC, Pedersen AB, Fenton A, Petchey OL, , 2014. Analysis of a summary network of co-infection in humans reveals that parasites interact most via shared resources. Proc Biol Sci 281: 20132286.[Crossref] [Google Scholar]
  26. Figueiredo CA, Barreto ML, Rodrigues LC, Cooper PJ, Silva NB, Amorim LD, Alcantara-Neves NM, , 2010. Chronic intestinal helminth infections are associated with immune hyporesponsiveness and induction of a regulatory network. Infect Immun 78: 31603167.[Crossref] [Google Scholar]
  27. Dowd JB, Zajacova A, Aiello AE, , 2010. Predictors of inflammation in U.S. children aged 3–16 years. Am J Prev Med 39: 314320.[Crossref] [Google Scholar]
  28. Menzies SK, Rodriguez A, Chico M, Sandoval C, Broncano N, Guadalupe I, Cooper PJ, , 2014. Risk factors for soil-transmitted helminth infections during the first 3 years of life in the tropics; findings from a birth cohort. PLoS Negl Trop Dis 8: e2718.[Crossref] [Google Scholar]
  29. Turner JD, Jackson JA, Faulkner H, Behnke J, Else KJ, Kamgno J, Boussinesq M, Bradley JE, , 2008. Intensity of intestinal infection with multiple worm species is related to regulatory cytokine output and immune hyporesponsiveness. J Infect Dis 197: 12041212.[Crossref] [Google Scholar]
  30. Figueiredo CA, Amorim LD, Vaca M, Chico ME, Campos AC, Barreto ML, Cooper PJ, , 2016. Effects of poor hygiene on cytokine phenotypes in children in the tropics. World Allergy Organ J 9: 34.[Crossref] [Google Scholar]
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  • Received : 17 Jul 2016
  • Accepted : 18 Jan 2017

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