Chronic intestinal helminth infections are associated with immune hyporesponsiveness and induction of a regulatory network

Infection and Immunity

Volumn 78, Issue 7, 2010, Pages 3160-3167

  Figueiredo, Camila Alexandrina ^a   Barreto, Mauricio L ^a   Rodrigues, Laura C ^b   Cooper, Philip J ^c,d   Silva, Nívea Bispo ^a   Amorim, Leila D ^a   Alcantara Neves, Neuza Maria ^a  

^a FEDERAL UNIVERSITY OF BAHIA   (Brazil)

^b LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^c ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^d UNIVERSIDAD SAN FRANCISCO DE QUITO   (Ecuador)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G4; INTERLEUKIN 10; INTERLEUKIN 5;

ADOLESCENT; ARTICLE; ASCARIASIS; ASCARIS LUMBRICOIDES; BRAZIL; CHILD; CLINICAL TRIAL; CYTOKINE PRODUCTION; FECES ANALYSIS; GENE REPRESSION; HUMAN; IMMUNE RESPONSE; INTESTINE INFECTION; LEUKOCYTE; MAJOR CLINICAL STUDY; MIXED INFECTION; PRIORITY JOURNAL; SCHOOL CHILD; TRICHURIASIS; TRICHURIS;

ANIMALS; ANTIBODIES, HELMINTH; ASCARIASIS; ASCARIS LUMBRICOIDES; CHILD; CHILD, PRESCHOOL; FEMALE; HUMANS; IMMUNITY, HUMORAL; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-13; INTERLEUKIN-5; MALE; TRICHURIASIS; TRICHURIS;

EID: 77953941153     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01228-09     Document Type: Article

References (38)

1. Agresti, A. 2007. Introduction to categorical data analysis, 2nd ed. Wiley-Interscience, New Jersey, NJ.
2. Akdis, M. 2008. T cell tolerance to inhaled allergens: mechanisms and therapeutic approaches. Expert Opin. Biol. Ther. 8:769-777.
3. Araujo, M. I., B. Hoppe, M. Medeiros, Jr., L. Alcântara, M. C. Almeida, A. Schriefer, R. R. Oliveira, R. Kruschewsky, J. P. Figueiredo, A. A. Cruz, and E. M. Carvalho. 2004. Impaired T helper 2 response to aeroallergen in helminth infected patients with asthma. J. Infect. Dis. 190:1797-1803.
4. Reference deleted.
5. Barreto, M. L., B. Genser, A. Strina, M. G. Teixeira, A. M. Assis, R. F. Rego, C. A. Teles, M. S. Prado, S. M. Matos, D. N. Santos, L. A. dos Santos, and S. Cairncross. 2007. Effect of city-wide sanitation programme on reduction in rate of childhood diarrhea in northeast Brazil: assessment by two cohort studies. Lancet 370:1622-1628.
6. Barreto, M. L., S. S. Cunha, N. Alcântara-Neves, L. P. Carvalho, A. A. Cruz, R. T. Stein, B. Genser, P. J. Cooper, and L. C. Rodrigues. 2006. Risk factors and immunological pathways for asthma and other allergic diseases in children: background and methodology of a longitudinal study in a large urban center in northeastern Brazil (Salvador-SCAALA study). BMC Pulm. Med. 6:15.
7. Burkhart, C., G. Y. Liu, S. M. Anderton, B. Metzler, and D. C. Wraith. 1999. Peptide-induced T cell regulation of experimental autoimmune encephalomyelitis: a role for IL-10. Int. Immunol. 11:1625-1634.
8. Cooper, P. J., A. L. Moncayo, I. Guadalupe, S. Benitez, M. Vaca, M. Chico, and G. E. Griffin. 2008. Repeated treatments with albendazole enhance Th2 responses to Ascaris lumbricoides, but not to aeroallergens, in children from rural communities in the Tropics. J. Infect. Dis. 198:1237-1242.
9. Cooper, P. J., I. Espinel, W. Paredes, R. H. Guderian, and T. B. Nutman. 1998. Impaired tetanus-specific cellular and humoral responses following tetanus vaccination in human onchocerciasis: a possible role of interleukin-10. J. Infect. Dis. 178:1133-1138.
10. Cooper, P. J. 2009. Interactions between helminth parasites and allergy. Curr. Opin. Allergy Clin. Immunol. 9:29-37.
11. Eastoe, E. F., C. J. Halsal, J. E. Heffernan, and H. Hun. 2006. A statistical comparison of survival and replacement analyses for the use of censored data in a contaminant air database: a case study from the Canadian Arctic. Atmos. Environ. 40:6528-6540.
12. Eriksson, M., E. Sartono, C. L. Martins, C. Balé, M. L. Garly, H. Whittle, et al. 2007. A comparison of ex vivo cytokine production in venous and capillary blood. Clin. Exp. Immunol. 150:469-476.
13. Figueiredo, C. A., N. M. Alcântara-Neves, R. Veiga, L. D. Amorim, V. Dattoli, L. R. Mendonça, S. Junqueira, B. Genser, M. Santos, L. C. de Carvalho, P. J. Cooper, L. Rodrigues, and M. L. Barreto. 2009. Spontaneous cytokine production in children according to biological characteristics and environmental exposures. Environ. Health Perspect. 117:845-849.
14. Reference deleted.
15. Helsel, D. R. 2005. More than obvious: better methods for interpreting nondetect data. Environ. Sci. Technol. 39:419-423.
16. Helsel, D. R. 2005. Nondetects and data analysis: statistics for censored environmental data, 1st ed. Wiley-Interscience, New Jersey, NJ.
17. Hoffman, W. A., J. A. Pons, and J. L. Janer. 1934. The sedimentation-concentration method in schistosomiasis mansoni. Puerto Rico J. Public Health 9:281-298.
18. Katz, N., A. Chaves, and J. Pellegrino. 1972. A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Rev. Inst. Med. Trop. Sao Paulo 14:397-400.
19. Lee, L., and D. Helsel. 2007. Statistical analysis of water-quality data containing multiple detection limits. II. S-language software for nonparametric distribution modeling and hypothesis testing. Comput. Geosci. 33:696-704.
20. Lowry, O. H., N. J. Rosenbrough, A. L. Faar, and R. J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
21. Maizels, R. M., and M. Yazdanbakhsh. 2003. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat. Rev. Immunol. 3:733-744.
22. Matricardi, P. M., and S. Bonini. 2000. High microbial turnover rate preventing atopy: a solution to inconsistencies impinging on the hygiene hypothesis? Clin. Exp. Allergy 30:1506-1510.
23. Mingomataj, E. Ç., F. Xhixha, and E. Gjata. 2006. Helminths can protect themselves against rejection inhibiting hostile respiratory allergy symptoms. Allergy 61:400-406.
24. Reference deleted.
25. Nookala, S., S. Srinivasan, P. Kaliraj, R. B. Narayanan, and T. B. Nutman. 2004. Impairment of tetanus-specific cellular and humoral responses following tetanus vaccination in human lymphatic filariasis. Infect. Immun. 72:2598-2604.
26. + T cells independent of interleukin-10. Infect. Immun. 77:98-107.
27. Pearce, E. J., C. M. Kane, J. Sun, J. J. Taylor, A. S. McKee, and L. Cervi. 2004. Th2 response polarization during infection with the helminth parasite Schistosoma mansoni. Immunol. Rev. 201:117-126.
28. Ponte, E. V., F. Lima, M. I. Araújo, R. R. Oliveira, L. S. Cardoso, and A. A. Cruz. 2006. Skin test reactivity and Der p-induced interleukin 10 production in patients with asthma or rhinitis infected with Ascaris. Ann. Allergy Asthma Immunol. 96:713-718.
29. Rodrigues, L. C., P. J. Newcombe, S. S. Cunha, N. M. Alcantara-Neves, B. Genser, A. A. Cruz, S. M. Simoes, R. Fiaccone, L. Amorim, P. J. Cooper, M. L. Barreto, and Social Change, Asthma and Allergy in Latin America. 2008. Early infection with Trichuris trichiura and allergen skin test reactivity in later childhood. Clin. Exp. Allergy 38:1769-1777.
30. Sabin, E. A., M. I. Araujo, E. M. Carvalho, and E. J. Pearce. 1996. Impairment of tetanus toxoid-specific Th1-like immune responses in humans infected with Schistosoma mansoni. J. Infect. Dis. 173:269-272.
31. Smits, H. H., and M. Yazdanbakhsh. 2007. Chronic helminth infections modulate allergen-specific immune responses: protection against development of allergic disorders? Ann. Med. 39:428-439.
32. Strachan, D. P. 1989. Hay fever, hygiene, and household size. Br. Med. J. 299:1259.
33. Strina, A., S. Cairncross, M. L. Barreto, C. Larrea, and M. S. Prado. 2003. Childhood diarrhea and observed hygiene behavior in Salvador, Brazil. Am. J. Epidemiol. 157:1032-1038.
34. Therneau, T., and P. Grambsch. 2000. Modeling survival data: extending the Cox model, 1st ed. Springer Verlag, New York, NY.
35. Turner, J. D., J. A. Jackson, H. Faulkner, J. Behnke, K. J. Else, J. Kamgno, M. Boussinesq, and J. E. Bradley. 2008. Intensity of intestinal infection with multiple worm species is related to regulatory cytokine output and immune hyporesponsiveness. J. Infect. Dis. 197:1204-1212.
36. Wilson, M. S., M. D. Taylor, A. Balic, C. A. M. Finney, J. R. Lamb, and R. M. Maizels. 2005. Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J. Exp. Med. 202:1199-1212.
37. Yazdanbakhsh, M., P. G. Kremsner, and R. Ree. 2002. Allergy, parasites, and the hygiene hypothesis. Science 296:490-494.
38. Zaccone, P., Z. Fehervari, J. M. Phillips, D. W. Dunne, and A. Cooke. 2006. Parasitic worms and inflammatory diseases. Parasite Immunol. 28:515-523.