• 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 4.

    Lamberton PHL, Jourdan PM, 2015. Human ascariasis: diagnostics update. Curr Trop Med Rep 2: 189200.

  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 8.

    Sanchez AL, Mahoney DL, Gabrie JA, 2015. Interleukin-10 and soil-transmitted helminth infections in Honduran children. BMC Res Notes 8: 55.

  • 9.

    Rafi W, Ribeiro-Rodrigues R, Ellner JJ, Salgame P, 2012. Coinfection-helminthes and tuberculosis. Curr Opin HIV AIDS 7: 239244.

  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 13.

    Lopez-Romero G, Quintero J, Astiazarán-García H, Velazquez C, 2015. Host defences against Giardia lamblia. Parasite Immunol 37: 394406.

  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

  • 16.

    Heyworth MF, 2014. Immunological aspects of Giardia infections. Parasite 21: 55.

  • 17.

    Redpath SA, Fonseca NM, Perona-Wright G, 2014. Protection and pathology during parasite infection: IL-10 strikes the balance. Parasite Immunol 36: 233252.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
 
 
 

 

 
 
 

 

 

 

 

 

 

Comparison of Cytokine Responses in Ecuadorian Children Infected with Giardia, Ascaris, or Both Parasites

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  • 1 National School of Tropical Medicine, Baylor College of Medicine, Houston, Texas.
  • | 2 Fundación Ecuatoriana para la Investigación en Salud, Quito, Ecuador.
  • | 3 Facultad de Ciencias Medicas, de la Salud y la Vida, Universidad Internacional del Ecuador, Quito, Ecuador.
  • | 4 Institute of Infection and Immunity, St. George's University of London, London, United Kingdom.

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 Ascaris and Giardia coinfected children compared with Giardia- and Ascaris-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 Giardia lamblia-only, Ascaris lumbricoides-only, or G. lamblia and A. lumbricoides 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) (P < 0.05), IL-12 (P < 0.05), and tumor necrosis factor alpha (P < 0.05) compared with Giardia-only infected children. Coinfected children had an increase in IL-10/interferon gamma (IFN-γ) ratio compared with uninfected (P < 0.05) and Ascaris alone (P < 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 Ascaris and Giardia may impair the host's ability to eradicate Giardia infection leading to chronic giardiasis.

Author Notes

* Address correspondence to Rojelio Mejia, Texas Children's Hospital, Feigin Building, Suite 0550.10, Houston, TX 77030. E-mail: rmejia@bcm.edu

Authors' addresses: Jill Weatherhead, Department of Pediatrics, Baylor College of Medicine, Houston, TX, E-mail: weatherh@bcm.edu. Andrea Arévalo Cortés, Carlos Sandoval, Maritza Vaca, Martha Chico, Sophia Loor, and Philip J. Cooper, Facultad de Ciencias Medicas, Universidad International del Ecuador, Quito, Ecuador, E-mails: aarevalocortes@gmail.com, sandoval_acarlos@hotmail.com, marimar_ecq@yahoo.com, marthachico6@yahoo.es, sofy_loor@hotmail.es, and pcooper@sgul.ac.uk. Rojelio Mejia, National School of Tropical Medicine, Baylor College of Medicine, Houston, TX, E-mail: rojelio.mejia@bcm.edu.

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