Trichuris suis ova therapy for allergic rhinitis does not affect allergen-specific cytokine responses despite a parasite-specific cytokine response

Clinical and Experimental Allergy

Volumn 42, Issue 11, 2012, Pages 1582-1595

  Bourke, C D ^a,g   Mutapi, F ^a   Nausch, N ^a   Photiou, D M F ^a   Poulsen, L K ^d   Kristensen, B ^f   Arnved, J ^c   Ronborg S ^c   Roepstorff, A ^e   Thamsborg, S ^e   Kapel, C ^e   Melbye, M ^b   Bager, P ^b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b STATENS SERUM INSTITUT   (Denmark)

^c Pulmonology and Allergy Clinic of Copenhagen   (Denmark)

^d Rigshospitalet   (Denmark)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

^f Thermo Fisher Scientific   (United States)

^g UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Allergic rhinitis; Cytokine; Helminth; Immune response; Pollen allergen; Trichuris suis

Indexed keywords

ALLERGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; PARASITE ANTIGEN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ALLERGIC RHINITIS; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOMETRY; DOUBLE BLIND PROCEDURE; FEMALE; HUMAN; IMMUNE RESPONSE; MAJOR CLINICAL STUDY; MALE; NONHUMAN; OOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PLASMA; POLLEN; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; TRICHURIASIS; TRICHURIS SUIS;

ADULT; ALLERGENS; ANIMALS; ANTIGENS, HELMINTH; CYTOKINES; DESENSITIZATION, IMMUNOLOGIC; FEMALE; HUMANS; LEUKOCYTES, MONONUCLEAR; MALE; MIDDLE AGED; OVUM; PATIENT COMPLIANCE; POACEAE; POLLEN; RHINITIS, ALLERGIC, PERENNIAL; TRICHURIASIS; TRICHURIS; YOUNG ADULT;

EID: 84868104302     PISSN: 09547894     EISSN: 13652222     Source Type: Journal    
DOI: 10.1111/j.1365-2222.2012.04063.x     Document Type: Article

References (57)

1. Yazdanbakhsh M, Kremsner PG, van Ree R. Allergy, parasites, and the hygiene hypothesis. Science 2002; 296:490-4.
2. Wilson MS, Maizels RM. Regulation of allergy and autoimmunity in helminth infection. Clin Rev Allergy Immunol 2004; 26:35-50.
3. Figueiredo CA, Barreto ML, Rodrigues LC et al. Chronic intestinal helminth infections are associated with immune hyporesponsiveness and induction of a regulatory network. Infect Immun 2010; 78:3160-7.
4. Smits HH, Everts B, Hartgers FC, Yazdanbakhsh M. Chronic helminth infections protect against allergic diseases by active regulatory processes. Curr Allergy Asthma Rep 2010; 10:3-12.
5. Cooper PJ, Chico ME, Rodrigues LC et al. Reduced risk of atopy among school-age children infected with geohelminth parasites in a rural area of the tropics. J Allergy Clin Immunol 2003; 111:995-1000.
6. Feary J, Britton J, Leonardi-Bee J. Atopy and current intestinal parasite infection: a systematic review and meta-analysis. Allergy 2011; 66:569-78.
7. van den Biggelaar AH, van Ree R, Rodrigues LC et al. Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 2000; 356:1723-7.
8. Mutapi F, Imai N, Nausch N et al. Schistosome infection intensity is inversely related to auto-reactive antibody levels. PLoS One 2011; 6:e19149.
9. van den Biggelaar AHJ, Rodrigues LC, van Ree R et al. Long-term treatment of intestinal helminths increases mite skin-test reactivity in Gabonese schoolchildren. J Infect Dis 2004; 189:892-900.
10. Maizels RM. Infections and allergy - helminths, hygiene and host immune regulation. Curr Opin Immunol 2005; 17:656-61.
11. Erb KJ. Can helminths or helminth-derived products be used in humans to prevent or treat allergic diseases? Trends Immunol 2009; 30:75-82.
12. Croese J, O'Neil J, Masson J et al. A proof of concept study establishing Necator americanus in Crohn's patients and reservoir donors. Gut 2006; 55:136-7.
13. Summers RW, Elliott DE, Urban JF, Thompson R, Weinstock JV. Trichuris suis therapy in Crohn's disease. Gut 2005; 54:87-90.
14. Summers RW, Elliott DE, Urban JF, Thompson RA, Weinstock JV. Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 2005; 128:825-32.
15. Bager P, Arnved J, Ronborg S et al. Trichuris suis ova therapy for allergic rhinitis: a randomized, double-blind, placebo-controlled clinical trial. J Allergy Clin Immunol 2010; 125:123-30.
16. Feary JR, Venn AJ, Mortimer K et al. Experimental hookworm infection: a randomized placebo-controlled trial in asthma. Clin Exp Allergy 2010; 40:299-306.
17. Fallon PG, Amu S, Saunders SP, Kronenberg M, Mangan NE, Atzberger A. Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model. J Allergy Clin Immunol 2010; 125:1114-24.
18. Araujo MI, Cardoso LS, Oliveira SC et al. Schistosoma mansoni antigens modulate the allergic response in a murine model of ovalbumin-induced airway inflammation. Clin Exp Immunol 2010; 160:266-74.
19. Hartmann S, Schnoeller C, Dahten A et al. Gastrointestinal nematode infection interferes with experimental allergic airway inflammation but not atopic dermatitis. Clin Exp Allergy 2009; 39:1585-96.
20. Oliveira SC, Pacifico LGG, Marinho FAV et al. Schistosoma mansoni antigens modulate experimental allergic asthma in a murine model: a major role for CD4(+) CD25(+) Foxp3(+) T cells independent of interleukin-10. Infect Immun 2009; 77:98-107.
21. Schnoeller C, Rausch S, Pillai S et al. Helminth immunomodulator reduces allergic and inflammatory responses by induction of IL-10-producing macrophages. J Immunol 2008; 180:4265-72.
22. Trujillo-Vargas CM, Werner-Klein M, Wohlleben G et al. Helminth-derived products inhibit the development of allergic responses in mice. Am J Respir Crit Care Med 2007; 175:336-44.
23. Wilson MS, Taylor MD, Balic A, Finney CAM, Lamb JR, Maizels RM. Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J Exp Med 2005; 202:1199-212.
24. Fleming J, Lee J, Luzzio C, Carrithers M, Field A, Fabry Z. A phase-1 trial of probiotic helminth ova in relapsing remitting rultiple sclerosis (RRMS). Neurology 2009; 72:A358-A58.
25. Fleming J, Isaak A, Lee J et al. Probiotic helminth administration in relapsing-remitting multiple sclerosis: a phase 1 study. Mult Scler J 2011; 17:743-54.
26. Summers RW, Elliott DE, Weinstock JV. Reply. Gastroenterology 2005;129: 769-69.
27. Faulkner H, Turner J, Kamgno J, Pion SD, Boussinesq M, Bradley JE. Age- and infection intensity-dependent cytokine and antibody production in human trichuriasis: The importance of IgE. J Infect Dis 2002; 185:665-72.
28. Jackson JA, Turner JD, Rentoul L et al. Cytokine response profiles predict species-specific infection patterns in human GI nematodes. Int J Parasitol 2004; 34:1237-44.
29. Benson M, Strannegard IL, Wennergren G, Strannegard O. Cytokines in nasal fluids from school children with seasonal allergic rhinitis. Pediatr Allergy Immunol 1997; 8:143-9.
30. Scavuzzo MC, Rocchi V, Fattori B et al. Cytokine secretion in nasal mucus of normal subjects and patients with allergic rhinitis. Biomed Pharmacother 2003; 57:366-71.
31. Benzel F, Erdur H, Kohler S et al. Immune monitoring of Trichuris suis egg therapy in multiple sclerosis patients. J Helminthol 2011; 23: 1-9.
32. Cooper PJ, Chico ME, Sandoval C et al. Human infection with Ascaris lumbricoides is associated with a polarized cytokine response. J Infect Dis 2000; 182:1207-13.
33. Bradding P, Feather IH, Wilson S et al. Immunolocalization of cytokines in the nasal mucosa of normal and perennial rhinitic subjects - the mast cell as a source of IL-4, IL-5, and IL-6 in human allergic mucosal inflammation. J Immunol 1993; 151:3853-65.
34. Wachholz PA, Nouri-Aria KT, Wilson DR et al. Grass pollen immunotherapy for hayfever is associated with increases in local nasal but not peripheral Th1:Th2 cytokine ratios. Immunology 2002; 105:56-62.
35. Taylor A, Verhagen J, Blaser K, Akdis M, Akdis CA. Mechanisms of immune suppression by interleukin-10 and transforming growth factor-beta: the role of T regulatory cells. Immunology 2006; 117:433-42.
36. Bager P, Kapel C, Roepstorff A et al. Symptoms after ingestion of pig whipworm Trichuris suis eggs in a randomized placebo-controlled double-blind clinical trial. PLoS One 2011; 6:e22346.
37. Abe M, Harpel JG, Metz CN, Nunes I, Loskutoff DJ, Rifkin DB. An assay for transforming growth factor-beta using cells transfected with a plasminogen-activator inhibitor-1 promoter luciferase construct. Anal Biochem 1994; 216:276-84.
38. Grainger JR, Smith KA, Hewitson JP et al. Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-β pathway. J Exp Med 2010; 207:2331-41.
39. Sokal RR, Rohlf FJ. Chapter 13.12: non-parametric methids in lieu of two-way analysis of variance. Biometry: Third Edition: New York: W.H.Freeman & Co Ltd, 1995:609-84.
40. Diaz A, Allen JE. Mapping immune response profiles: the emerging scenario from helminth immunology. Eur J Immunol 2007; 37:3319-26.
41. McCune B, Grace JB. Analysis of Ecological Communities. Gleneden Beach, Oregon, USA: MJM Software Design, 2002.
42. Charleston B, Bankowski BM, Gubbins S et al. Relationship between clinical signs and transmission of an infectious disease and the implications for control. Science 2011; 332:726-9.
43. Groer MW, Beckstead JW. Multidimensional scaling of multiplex data: human milk cytokines. Biol Res Nurs 2011; 13:289-96.
44. Wilson MS, Cheever AW, White SD, Thompson RW, Wynn TA. IL-10 blocks the development of resistance to re-infection with Schistosoma mansoni. PLoS Pathog 2011; 7:e1002171.
45. Movérare R, Elfman L, Björnsson E, Stålenheim G. Cytokine production by peripheral blood mononuclear cells following birch-pollen immunotherapy. Immunol Lett 2000; 73:51-6.
46. Turner JD, Faulkner H, Kamgno J et al. Th2 cytokines are associated with reduced worm burdens in a human intestinal helminth infection. J Infect Dis 2003; 188:1768-75.
47. Imai N, Rujeni N, Nausch N et al. Exposure, infection, systemic cytokine levels and antibody responses in young children concurrently exposed to schistosomiasis and malaria. Parasitology 2011; 138:1519-33.
48. Mutapi F, Milner T, Reilly L et al. Circulating cytokine levels and antibody responses to human Schistosoma haematobium: IL-5 and IL-10 levels depend upon age and infection status. Parasite Immunol 2010; 32:710-21.
49. Steenhard NR, Kringel H, Roepstorff A, Thamsborg SM, Jungersen G. Parasite-specific IL-4 responses in Ascaris suum and Trichuris suis-infected pigs evaluated by ELISPOT. Parasite Immunol 2007; 29:535-8.
50. Jepsen KF, Nielsen L, Olsen OT, Bendtzen K, Poulsen LK. Seasonal variations in T-lymphocyte response to grass pollen allergens from pollen-allergic patients and healthy controls. Exp Clin Immunogenet 1998; 15:144-53.
51. Jones KP, Morris RHK, Rolf S, Davies BH. Seasonal variation in interleukin 4 in patients with hayfever. Cytokine 2000; 12:543-5.
52. Klimek L, Dormann D, Jarman ER, Cromwell O, Riechelmann H, Reske-Kunz AB. Short-term preseasonal birch pollen allergoid immunotherapy influences symptoms, specific nasal provocation and cytokine levels in nasal secretions, but not peripheral T-cell responses, in patients with allergic rhinitis. Clin Exp Allergy 1999; 29:1326-35.
53. Saito H, Howie K, Wattie J et al. Allergen-induced murine upper airway inflammation: local and systemic changes in murine experimental allergic rhinitis. Immunology 2001; 104:226-34.
54. Pinelli E, Brandes S, Dormans J, Gremmer E, van Loveren H. Infection with the roundworm Toxocara canis leads to exacerbation of experimental allergic airway inflammation. Clin Exp Allergy 2008; 38:649-58.
55. Demirturk N, Kozan E, Demirdall T et al. Effect of parasitosis on allergic sensitization in rats sensitized with ovalbumin: Interaction between parasitosis and allergic sensitization. Adv Ther 2007; 24:1305-13.
56. Michels C, Goyal P, Nieuwenhuizen N, Brombacher F. Infection with Syphacia obvelata (Pinworm) induces protective Th2 immune responses and influences ovalbumin-induced allergic reactions. Infect Immun 2006; 74:5926-32.
57. Summers RW, Elliott DE, Weinstock JV. Trichuris suis might be effective in treating allergic rhinitis. J Allergy Clin Immunol 2010; 125:766-7.