Helmintosis y eventos alérgicos
Helminth infections and allergic events
DOI:
https://doi.org/10.33936/qkrcs.v1i1.119Resumen
En las últimas tres décadas se ha reconocido un alarmante aumento en la frecuencia de las en- fermedades alérgicas, asociadas con cuadros de parasitismos, y este número sigue creciendo. Se realizó una revisión del tema, en cuanto a características clínicas, epidemiológicas y factores inmunológicos que identifican a esta asociación. El objetivo de esta revisión es exponer, algunos aspectos relevantes de estas patologías. Se destaca la importancia del papel modulador de las hel- mintiasis, en el desarrollo de las alergias; sin embargo, las evidencias de esta asociación no están claramente establecidas, por lo que existe todavía en la comunidad científica, la controversia y el debate, acerca de este tema y específicamente de los mecanismos que intervienen en la modula- ción de las alergias por los parásitos helmintos.
Palabras clave: Geohelmintosis, helmintiasis, alergia.
Abstract:
In the last three decades an alarming increase in the frequency of allergic diseases associated with symptoms of parasitism has been recognized, and this number continues to grow. A review of the topic was conducted regarding clinical, epidemiological and immunological factors that identify this association. The objective of this review is to present some important aspects of these pathologies. The importance of modulatory helminthiasis, in the development of allergies is highlighted; however, the evidence of this association is not clearly established, so there is still, in the scientific community, controversy and debate about this issue and specifically of the mechanisms involved in the modula- tion of allergies by helminth parasites.
Key words: Geohelmintosis, helminth infections, allergies.
Descargas
La descarga de datos todavía no está disponible.
Citas
1. Stoll N. This wormy world. J Parasitol. 1947; 85:392-396.
2. Hotez P, Remme J, Buss P, Alleyne G, Morel C, Breman J. Combating tropical infectious disea- ses: report of the disease control priorities in developing countries project. Clin Infect Dis. 2004;38:871-878.
3. Hotez PJ, Brindley PJ, Bethony JM. Helminth infections: the great neglected tropical diseases. JClin Invest. 2008; 118:1311-1321.
4. World Health Organization. Prevention and control of schistosomiasis and soil-transmitted hel- minthiasis: report of a WHO Expert Committee. Geneva: World Health Organization, 2002. WHO Technical Report Series No.912.
5. Crompton DWT. How much helminthiasis is there in the world? J Parasitol. 1999; 85:397-403.
6. McCarty TR, Turkeltaub JA, Hotez PJ. Global progress towards eliminating gastrointestinal hel-minth infections. Curr Opin Gastroenterol. 2014; 30:18-24.
7. Strunzl EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman M. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med. [serial on the Internet]. 2014 Mar, 11(3): [about 38 p.]. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3965411/pdf/pmed.1001620.pdf
8. Levecke B, Montresor A, Albonico M, Ame SM, Behnke JM,5 Bethony JM. Assessment of anthel- mintic efficacy of mebendazole in school children in six countries where soil-transmitted helminths are endemic. PLoS Negl Trop Dis. [serial on the Internet]. 2014 Oct 9; 8(10): [about 12 p.]. Available from:
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4191962/pdf/pntd.0003204.pdf
9. OPS. Datos clave de las enfermedades infecciosas desatendidas. Helmintiasis transmitidas por el suelo. Washington DC, 2014.
10. Bruschi F, Araujo MI, Harnett W, Pinelli E. Allergy and Parasites. J Parasitol Res. [serial on the Internet]. 2013 Feb 13, Vol. 2013:[about 2 p.]. Available from: https://www.ncbi.nlm.nih.gov/pmc/ articles/PMC3583124/pdf/JPR2013-502562.pdf
11. Taylor B, Wadsworth J, Wadsworth M, Peckham M. Changes in the reported prevalence of child- hood eczema since the 1939-45 war. Lancet. 1984; 2:1255-1257.
12. Ring J. Davos Declaration: allergy as a global problem. Allergy. 2012; 67:141-143.
13. Leonardi-Bee J, Pritchard D, Britton J. Asthma and current intestinal parasite infection. Am J Respir Crit Care Med. 2006; 174:514-523.
14. Rujeni N, Taylor D, Mutapi F. Human Schistosome Infection and Allergic Sensitisation. J Pa- rasitol Res. [serial on the Internet]. 2012 Jun, Vol. 2012:[about 18 p.]. Available from: https://www. hindawi.com/journals/jpr/2012/154743/
15. Johansson S, Bieber T, Dahl T. Revised nomenclature for allergy for global use: report of the Nomenclature Review Committee of the World Allergy Organization, October 2003. J Allergy Clin Immunol. 2004; 113:832-836.
16. Nguyen T, Casale TB. Immune modulation for treatment of allergic disease. Immunol Rev. 2011; 242:258-271.
17. Jutel M, Akdis CA. T-cell subset regulation in atopy. Curr Allergy Asthma Rep. 2011; 11:139-145.
18. Paul WE, Zhu J. How are T(H)2-type immune responses initiated and amplified. Nat Rev Immu- nol. 2010; 10:225-235.
19. Jex AR, Liu S, Li B. Ascaris suum draft genome. Nature. 2011; 479:529-533.
20. Allen JE, Maizels RM. Diversity and dialogue in immunity to helminths. Nat Rev Immunol. 2011; 11:375-388.
21. Fallon PG, Mangan NE. Suppression of TH2-type allergic reactions by helminth infection. Nat Rev Immunol. 2007; 7:220-230.
22. Akdis M, Verhagen J, Taylor A. Immune responses in healthy and allergic individuals are characterized by a fine balance between allergen-specific T regulatory 1 and T helper 2 cells. J Exp Med. 2004; 199:1567-1575.
23. García-Hernández MH. Regulatory T cells in children with intestinal parasite infection. Parasite Immunol 2009; 31:597-603.
24. Hagan P, Blumenthal UJ, Dunn D, Simpson AJG, Wilkins HA. Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature. 1991; 349:243-245.
25. Joseph S. Increases in human T helper 2 cytokine responses to Schistosoma mansoni worm and worm-tegument antigens are induced by treatment with praziquantel. J Infect. Dis 2004; 190:835- 842.
26. Manoury B, Gregory WF, Maizels RM, Watts C. Bm-CPI-2, a cystatin homolog secreted by the filarial parasite Brugia malayi, inhibits class II MHC-restricted antigen processing. Curr Biol. 2001; 11:447-451.
27. Sartono E, Kruize YCM, Kurniawan-Atmadja A, Maizels RM, Yazdanbakhsh M. Depression of antigen-specific interleukin-5 and interferon-γ responses in human lymphatic filariasis as a function of clinical status and age. J Infect Dis. 1997; 175:1276-1280.
28. Matisz CE, McDougall JJ, Sharkey KA, McKay D. Helminth parasites and the modulation of joint inflammation. J Parasitol Res. [serial on the Internet]. 2011 Feb, Vol. 2011:[about 8 p.]. Available from: https://www.hindawi.com/journals/jpr/2011 /942616/
29. Hagel I, Cabrera M, Buvat E. Antibody responses and resistance against Ascaris lumbricoides infection among Venezuelan rural children: the influence of ethnicity. J Trop Pediatr. 2008; 54:354-356.
30. Turner JD, Faulkner H, Kamgno J. Allergen-specific IgE and IgG4 are markers of resistance and susceptibility in a human intestinal nematode infection. Microbes Infect. 2005; 7:990-996.
31. McSharry C, Xia Y, Holland CV, Kennedy MW. Natural immunity to Ascaris lumbricoides asso- ciated with immunoglobulin E antibody to ABA-1 allergen and inflammation indicators in children. Infect Immun. 1999; 67:484-489.
32. Jackson JA, Turner JD, Rentoul L. T helper cell type 2 responsiveness predicts future susceptibility to gastrointestinal nematodes in humans. J Infect. Dis 2004; 190:1804-1811.
33. Moro K, Yamada T, Tanabe M. Innate production of T(H)2 cytokines by adipose tissue-associa- ted c-Kit(+)Sca-1(+) lymphoid cells. Nature. 2010; 463:540-544.
34. Neill DR,Wong SH, Bellosi A. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature. 2010; 464:1367-1370.
35. Saenz SA, Siracusa MC, Perrigoue JG. IL25 elicits a multipotent progenitor cell population that promotes T(H)2 cytokine responses. Nature. 2010; 464:1362-1366.
36. Nicolaou N, Siddique N, Custovic A. Allergic disease in urban and rural populations: increasing prevalence with increasing urbanization. Allergy. 2005; 60:1357-1360.
37. Cooper PJ. Interactions between helminth parasites and allergy. Curr Opin Allergy Clin Immunol. 2009; 9:29-37.
38. Acevedo N, Caraballo L. IgE cross-reactivity between Ascaris lumbricoides and mite allergens: possible influences on allergic sensitization and asthma. Parasite Immunol. 2011; 33:309-321.
39. Spillmann RK. Pulmonary ascariasis in tropical communities. Am J Trop Med Hyg. 1975; 24:791800.
40. Joubert JR, de Klerk HC, Malan C. Ascaris lumbricoides and allergic asthma: a new perspective. S Afr Med J. 1979; 56:599-602.
41. Joubert JR, van Schalkwyk DJ, Turner KJ. Ascaris lumbricoides and the human immunoge- nic response: enhanced IgE-mediated reactivity to common inhaled allergens. S Afr Med J. 1980; 57:409-412.
42. Patterson R, Harris KE, Pruzansky JJ. Induction of IgE-mediated cutaneous, cellular, and airway reactivity in rhesus monkeys by Ascaris suum infection. J Lab Clin Med. 1983; 101:864-872.
43. Patterson R, Harris KE. IgE-mediated rhesus monkey asthma: natural history and individual animal variation. Int Arch Allergy Immunol. 1992; 97:154-159.
44. Tsuji M, Hayashi T, Yamamoto S, Sakata Y, Toshida T. IgE-type antibodies to Ascaris antigens in man. Int Arch Allergy Appl Immunol. 1977; 55:78-81.
45. Palmer LJ, Celedon JC, Weiss ST, Wang B, Fang Z, Xu X. Ascaris lumbricoides infection is associated with increased risk of childhood asthma and atopy in rural China. Am J Respir Crit Care Med. 2002; 165:1489-1493.
46. Takeuchi H, Zaman K, Takahashi J. High titre of anti-Ascaris immunoglobulin E associated with bronchial asthma symptoms in 5-year-old rural Bangladeshi children. Clin Exp Allergy. 2008; 38:276-282.
47. Hunninghake GM, Soto-Quiros ME, Avila L. Sensitization to Ascaris lumbricoides and severity of childhood asthma in Costa Rica. J Allergy Clin Immunol 2007; 119:654-661.
48. Hagel I, Cabrera M, Hurtado MA. Infection by Ascaris lumbricoides and bronchial hyper reactivi- ty: an outstanding association in Venezuelan school children from ndemic areas. Acta Trop. 2007; 103:231-241.
49. Obihara CC, Beyers N, Gie RP. Respiratory atopic disease, Ascaris immunoglobulin E and tuberculin testing in urban South African children. Clin Exp Allergy. 2006; 36:640-648.
50. Dold S, Heinrich J, Wichmann HE, Wjst M. Ascaris-specific IgE and allergic sensitization in a cohort of school children in the former East Germany. J Allergy Clin Immunol. 1998; 102:414-420.
51. Alcantara-Neves NM, Badaro SJ, dos Santos MC, Pontes-de-Carvalho L, Barreto ML. The pre- sence of serum anti-Ascaris lumbricoides IgE antibodies and of Trichuris trichiura infection are risk factors for wheezing and/or atopy in preschool-aged Brazilian children. Respir Res. [serial on the Internet]. 2010 Aug; 11(114): [about 9 p.]. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2939601/pdf/1465-9921-11-114.pdf
52. Pinelli E, Willers SM, Hoek D. Prevalence of antibodies against Ascaris suum and its association with allergic manifestations in 4-year-old children in The Netherlands: the PIAMA birth cohort study. Eur J Clin Microbiol Infect Dis. 2009; 28:1327-1334.
53. Scrivener S, Yemaneberhan H, Zebenigus M. Independent effects of intestinal parasite infection and domestic allergen exposure on risk of wheeze in Ethiopia: a nested case-control study. Lancet. 2001; 358:1493-1499.
54. Flohr C, Tuyen LN, Lewis S. Poor sanitation and helminth infection protect against skin sensitization in Vietnamese children: a cross-sectional study. J Allergy Clin Immunol. 2006; 118:1305-1311.
55. Schafer T, Meyer T, Ring J, Wichmann HE, Heinrich J. Worm infestation and the negative asso- ciation with eczema (atopic/nonatopic) and allergic sensitization. Allergy. 2005; 60:1014-1020.
56. Selassie FG, Stevens RH, Cullinan P. Total and specific IgE (house dust mite and intestinal helminths) in asthmatics and controls from Gondar, Ethiopia. Clin Exp Allergy. 2000; 30:356-358.
57. Van Riet E, Hartgers FC, Yazdanbakhsh M. Chronic helminth infections induce immunomodula- tion: consequences and mechanisms. Immunobiology. 2007; 212:475-490.
58. Araujo CA, Perini A, Martins MA, Macedo MS, Macedo-Soares MF. PAS-1, a protein from Asca- ris suum, modulates allergic inflammation via IL-10 and IFN-gamma, but not IL-12. Cytokine. 2008; 44:335-341.
59. Tsuji N, Miyoshi T, Islam MK. Recombinant Ascaris 16-kilodalton protein-induced protec- tion against Ascaris suum larval migration after intranasal vaccination in pigs. J Infect Dis. 2004; 190:1812-1820.
60. Tsuji N, Suzuki K, Kasuga-Aoki H. Intranasal immunization with recombinant Ascaris suum
14-kilodalton antigen coupled with cholera toxin B subunit induces protective immunity to A. suuminfection in mice. Infect Immun. 2001; 69:7285-7292.
61. Tsuji N, Kasuga-Aoki H, Isobe T, Arakawa T, Matsumoto Y. Cloning and characterization of a highly immunoreactive 37 kDa antigen with multi-immunoglobulin domains from the swine roundworm Ascaris suum. Int J Parasitol 2002. 32:1739-1746.
62. Islam MK, Miyoshi T, Yokomizo Y, Tsuji N. Molecular cloning and partial characterization of anematode-specific 24 kDa protein from Ascaris suum. Parasitol. 2005; 130:131-139.
63. Van Riet E,Wuhrer M,Wahyuni S. Antibody responses to Ascaris-derived proteins and glycoli- pids: the role of phosphorylcholine. Parasite Immunol. 2006; 28:363-371.
64. Perrigoue JG, Marshall FA, Artis D. On the hunt for helminths: innate immune cells in the recog- nition and response to helminth parasites. Cell Microbiol. 2008; 10:1757-1764.
65. Da Silva CA, Pochard P, Lee CG, Elias JA. Chitin particles are multifaceted immune adjuvants. Am J Respir Crit Care Med. 2010; 182:1482-1491.
66. Acevedo N, Sanchez J, Erler A. IgE cross-reactivity between Ascaris and domestic mite aller- gens: the role of tropomyosin and the nematode polyprotein ABA-1. Allergy. 2009; 64:1635-1643.
67. Acevedo NEA, Briza P, Puccio F, Ferreira F, Caraballo L. Allergenicity of Ascaris lumbricoides tropomyosin and IgE sensitization among asthmatic patients in a tropical environment. Int Arch of Allergy Immunol. 2011; 154:195-206.
68. Lopez N, de Barros-Mazon S, Vilela MM, Condino Neto A, Ribeiro JD. Are immunoglobulin E levels associated with early wheezing? A prospective study in Brazilian infants. Eur Respir J. 2002; 20:640-645.
69. Endara P, Vaca M, Chico ME. Long-term periodic anthelmintic treatments are associated with increased allergen skin reactivity. Clin Exp Allergy. 2010; 40:1669-1677.
70. Strachan DP. Hay fever, hygiene, and household size. BMJ. 1989; 299:1259-1260.
71. Mc Sorley HJ, Maizels RM. Helminth Infections and Host Immune Regulation. Clin Microbiol Rev. 2012; 25:585-608.
72. Flohr C, Nagel G, Weinmayr G. Tuberculosis, bacillus Calmette-Guerin vaccination, and allergic disease: findings from the International Study of Asthma and Allergies in Childhood Phase Two. Pe- diatr Allergy Immunol. 2012; 23:324-331.
73. Sharma SK, Banga A. Prevalence and risk factors for wheezing in children from rural areas of north India. Allergy Asthma Proc. 2007; 28:647-653.
74. Chatkin MN, Menezes AM, Victora CG, Barros FC. High prevalence of asthma in preschool chil- dren in Southern Brazil: a population-based study. Pediatr Pulmonol. 2003; 35:296-301.
75. Pitrez PM, Stein RT. Asthma in Latin America: the dawn of a new epidemic. Curr Opin Allergy Clin Immunol. 2008; 8:378-383.
76. Pearce N, Ait-Khaled N, Beasley R. Worldwide trends in the prevalence of asthma symptoms: phase III of the International Study of Asthma and Allergies in Childhood (ISAAC). Thorax. 2007; 62:758-766.
77. Sole D, Melo KC, Camelo-Nunes IC. Changes in the prevalence of asthma and allergic diseases among Brazilian schoolchildren (13-14 years old): comparison between ISAAC Phases One and Three. J Trop Pediatr. 2007; 53:13-21.
78. Kuschnir FC, Alves da Cunha AJ. Environmental and socio-demographic factors associated to asthma in adolescents in Rio de Janeiro, Brazil. Pediatr Allergy Immunol. 2007; 18:142-148.
79. Garcia E, Aristizabal G, Vasquez C, Rodriguez-Martinez CE, Sarmiento OL, Satizabal CL. Pre- valence of and factors associated with current asthma symptoms in school children aged 6-7 and 13-14 yrs. old in Bogota, Colombia. Pediatr Allergy Immunol. 2008; 19:307-314.
80. Cooper PJ, Chico ME, Rodrigues LC. 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.
81. Lynch NR, Lopez RI, Di Prisco-Fuenmayor MC. Allergic reactivity and socio-economic level in a tropical environment. Clin Allergy. 1987; 17:199-207.
82. Holt PG. Parasites, atopy, and the hygiene hypothesis: resolution of a paradox? Lancet. 2000; 356:1699-1701.
83. Van Dellen RG, Thompson Jr JH. Absence of intestinal parasites in asthma. N Engl J Med. 1971; 285:146-148.
84. Gerrard JW, Geddes CA, Reggin PL, Gerrard CD, Horne S. Serum IgE levels in white and metis communities in Saskatchewan. Ann Allergy. 1976; 37:91-100.
85. Yazdanbakhsh M, Kremsner PG, van Ree R. Allergy, parasites, and the hygiene hypothesis. Science. 2002; 296:490-494.
86. McKay DM. The therapeutic helminth? Trends Parasitol. 2008; 24:1-6.
87. Weinstock JV. The worm returns. Nature. 2012; 491:183-185.
88. Fleming JO, Weinstock JV. Clinical trials of helminth therapy in autoimmune diseases: rationale and findings. Parasite Immunol. 2015; 6:277-292.
89. Summers RW. Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease. Am J Gastroenterol. 2003; 98:2034-2041.
90. Bager P, Arnved J, Rønborg S, Wohlfahrt J, Poulsen LK, Westergaard T. Trichuris suis ova the- rapy for allergic rhinitis: a randomized, double-blind, placebo-controlled clinical trial. J Allergy Clin Immunol. 2010; 125:123-130.
91. Feary J, Venn A, Brown A, Hooi D, Falcone FH, Mortimer K. Safety of hookworm infection in indi- viduals with measurable airway responsiveness: a randomized placebo-controlled feasibility study. Clin Exp Allergy. 2009; 39:1060-1088.
92. Feary JR, Venn AJ, Mortimer K, Brown AP, Hooi D, Falcone FH. Experimental hookworm infection: a randomized placebo-controlled trial in asthma. Clin Exp Allergy. 2010; 40:299-306.
93. Helmby H. Helminths and our immune system: friend or foe? Parasitol Int. 2009; 58:121-127.
2. Hotez P, Remme J, Buss P, Alleyne G, Morel C, Breman J. Combating tropical infectious disea- ses: report of the disease control priorities in developing countries project. Clin Infect Dis. 2004;38:871-878.
3. Hotez PJ, Brindley PJ, Bethony JM. Helminth infections: the great neglected tropical diseases. JClin Invest. 2008; 118:1311-1321.
4. World Health Organization. Prevention and control of schistosomiasis and soil-transmitted hel- minthiasis: report of a WHO Expert Committee. Geneva: World Health Organization, 2002. WHO Technical Report Series No.912.
5. Crompton DWT. How much helminthiasis is there in the world? J Parasitol. 1999; 85:397-403.
6. McCarty TR, Turkeltaub JA, Hotez PJ. Global progress towards eliminating gastrointestinal hel-minth infections. Curr Opin Gastroenterol. 2014; 30:18-24.
7. Strunzl EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman M. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med. [serial on the Internet]. 2014 Mar, 11(3): [about 38 p.]. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3965411/pdf/pmed.1001620.pdf
8. Levecke B, Montresor A, Albonico M, Ame SM, Behnke JM,5 Bethony JM. Assessment of anthel- mintic efficacy of mebendazole in school children in six countries where soil-transmitted helminths are endemic. PLoS Negl Trop Dis. [serial on the Internet]. 2014 Oct 9; 8(10): [about 12 p.]. Available from:
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4191962/pdf/pntd.0003204.pdf
9. OPS. Datos clave de las enfermedades infecciosas desatendidas. Helmintiasis transmitidas por el suelo. Washington DC, 2014.
10. Bruschi F, Araujo MI, Harnett W, Pinelli E. Allergy and Parasites. J Parasitol Res. [serial on the Internet]. 2013 Feb 13, Vol. 2013:[about 2 p.]. Available from: https://www.ncbi.nlm.nih.gov/pmc/ articles/PMC3583124/pdf/JPR2013-502562.pdf
11. Taylor B, Wadsworth J, Wadsworth M, Peckham M. Changes in the reported prevalence of child- hood eczema since the 1939-45 war. Lancet. 1984; 2:1255-1257.
12. Ring J. Davos Declaration: allergy as a global problem. Allergy. 2012; 67:141-143.
13. Leonardi-Bee J, Pritchard D, Britton J. Asthma and current intestinal parasite infection. Am J Respir Crit Care Med. 2006; 174:514-523.
14. Rujeni N, Taylor D, Mutapi F. Human Schistosome Infection and Allergic Sensitisation. J Pa- rasitol Res. [serial on the Internet]. 2012 Jun, Vol. 2012:[about 18 p.]. Available from: https://www. hindawi.com/journals/jpr/2012/154743/
15. Johansson S, Bieber T, Dahl T. Revised nomenclature for allergy for global use: report of the Nomenclature Review Committee of the World Allergy Organization, October 2003. J Allergy Clin Immunol. 2004; 113:832-836.
16. Nguyen T, Casale TB. Immune modulation for treatment of allergic disease. Immunol Rev. 2011; 242:258-271.
17. Jutel M, Akdis CA. T-cell subset regulation in atopy. Curr Allergy Asthma Rep. 2011; 11:139-145.
18. Paul WE, Zhu J. How are T(H)2-type immune responses initiated and amplified. Nat Rev Immu- nol. 2010; 10:225-235.
19. Jex AR, Liu S, Li B. Ascaris suum draft genome. Nature. 2011; 479:529-533.
20. Allen JE, Maizels RM. Diversity and dialogue in immunity to helminths. Nat Rev Immunol. 2011; 11:375-388.
21. Fallon PG, Mangan NE. Suppression of TH2-type allergic reactions by helminth infection. Nat Rev Immunol. 2007; 7:220-230.
22. Akdis M, Verhagen J, Taylor A. Immune responses in healthy and allergic individuals are characterized by a fine balance between allergen-specific T regulatory 1 and T helper 2 cells. J Exp Med. 2004; 199:1567-1575.
23. García-Hernández MH. Regulatory T cells in children with intestinal parasite infection. Parasite Immunol 2009; 31:597-603.
24. Hagan P, Blumenthal UJ, Dunn D, Simpson AJG, Wilkins HA. Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature. 1991; 349:243-245.
25. Joseph S. Increases in human T helper 2 cytokine responses to Schistosoma mansoni worm and worm-tegument antigens are induced by treatment with praziquantel. J Infect. Dis 2004; 190:835- 842.
26. Manoury B, Gregory WF, Maizels RM, Watts C. Bm-CPI-2, a cystatin homolog secreted by the filarial parasite Brugia malayi, inhibits class II MHC-restricted antigen processing. Curr Biol. 2001; 11:447-451.
27. Sartono E, Kruize YCM, Kurniawan-Atmadja A, Maizels RM, Yazdanbakhsh M. Depression of antigen-specific interleukin-5 and interferon-γ responses in human lymphatic filariasis as a function of clinical status and age. J Infect Dis. 1997; 175:1276-1280.
28. Matisz CE, McDougall JJ, Sharkey KA, McKay D. Helminth parasites and the modulation of joint inflammation. J Parasitol Res. [serial on the Internet]. 2011 Feb, Vol. 2011:[about 8 p.]. Available from: https://www.hindawi.com/journals/jpr/2011 /942616/
29. Hagel I, Cabrera M, Buvat E. Antibody responses and resistance against Ascaris lumbricoides infection among Venezuelan rural children: the influence of ethnicity. J Trop Pediatr. 2008; 54:354-356.
30. Turner JD, Faulkner H, Kamgno J. Allergen-specific IgE and IgG4 are markers of resistance and susceptibility in a human intestinal nematode infection. Microbes Infect. 2005; 7:990-996.
31. McSharry C, Xia Y, Holland CV, Kennedy MW. Natural immunity to Ascaris lumbricoides asso- ciated with immunoglobulin E antibody to ABA-1 allergen and inflammation indicators in children. Infect Immun. 1999; 67:484-489.
32. Jackson JA, Turner JD, Rentoul L. T helper cell type 2 responsiveness predicts future susceptibility to gastrointestinal nematodes in humans. J Infect. Dis 2004; 190:1804-1811.
33. Moro K, Yamada T, Tanabe M. Innate production of T(H)2 cytokines by adipose tissue-associa- ted c-Kit(+)Sca-1(+) lymphoid cells. Nature. 2010; 463:540-544.
34. Neill DR,Wong SH, Bellosi A. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature. 2010; 464:1367-1370.
35. Saenz SA, Siracusa MC, Perrigoue JG. IL25 elicits a multipotent progenitor cell population that promotes T(H)2 cytokine responses. Nature. 2010; 464:1362-1366.
36. Nicolaou N, Siddique N, Custovic A. Allergic disease in urban and rural populations: increasing prevalence with increasing urbanization. Allergy. 2005; 60:1357-1360.
37. Cooper PJ. Interactions between helminth parasites and allergy. Curr Opin Allergy Clin Immunol. 2009; 9:29-37.
38. Acevedo N, Caraballo L. IgE cross-reactivity between Ascaris lumbricoides and mite allergens: possible influences on allergic sensitization and asthma. Parasite Immunol. 2011; 33:309-321.
39. Spillmann RK. Pulmonary ascariasis in tropical communities. Am J Trop Med Hyg. 1975; 24:791800.
40. Joubert JR, de Klerk HC, Malan C. Ascaris lumbricoides and allergic asthma: a new perspective. S Afr Med J. 1979; 56:599-602.
41. Joubert JR, van Schalkwyk DJ, Turner KJ. Ascaris lumbricoides and the human immunoge- nic response: enhanced IgE-mediated reactivity to common inhaled allergens. S Afr Med J. 1980; 57:409-412.
42. Patterson R, Harris KE, Pruzansky JJ. Induction of IgE-mediated cutaneous, cellular, and airway reactivity in rhesus monkeys by Ascaris suum infection. J Lab Clin Med. 1983; 101:864-872.
43. Patterson R, Harris KE. IgE-mediated rhesus monkey asthma: natural history and individual animal variation. Int Arch Allergy Immunol. 1992; 97:154-159.
44. Tsuji M, Hayashi T, Yamamoto S, Sakata Y, Toshida T. IgE-type antibodies to Ascaris antigens in man. Int Arch Allergy Appl Immunol. 1977; 55:78-81.
45. Palmer LJ, Celedon JC, Weiss ST, Wang B, Fang Z, Xu X. Ascaris lumbricoides infection is associated with increased risk of childhood asthma and atopy in rural China. Am J Respir Crit Care Med. 2002; 165:1489-1493.
46. Takeuchi H, Zaman K, Takahashi J. High titre of anti-Ascaris immunoglobulin E associated with bronchial asthma symptoms in 5-year-old rural Bangladeshi children. Clin Exp Allergy. 2008; 38:276-282.
47. Hunninghake GM, Soto-Quiros ME, Avila L. Sensitization to Ascaris lumbricoides and severity of childhood asthma in Costa Rica. J Allergy Clin Immunol 2007; 119:654-661.
48. Hagel I, Cabrera M, Hurtado MA. Infection by Ascaris lumbricoides and bronchial hyper reactivi- ty: an outstanding association in Venezuelan school children from ndemic areas. Acta Trop. 2007; 103:231-241.
49. Obihara CC, Beyers N, Gie RP. Respiratory atopic disease, Ascaris immunoglobulin E and tuberculin testing in urban South African children. Clin Exp Allergy. 2006; 36:640-648.
50. Dold S, Heinrich J, Wichmann HE, Wjst M. Ascaris-specific IgE and allergic sensitization in a cohort of school children in the former East Germany. J Allergy Clin Immunol. 1998; 102:414-420.
51. Alcantara-Neves NM, Badaro SJ, dos Santos MC, Pontes-de-Carvalho L, Barreto ML. The pre- sence of serum anti-Ascaris lumbricoides IgE antibodies and of Trichuris trichiura infection are risk factors for wheezing and/or atopy in preschool-aged Brazilian children. Respir Res. [serial on the Internet]. 2010 Aug; 11(114): [about 9 p.]. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2939601/pdf/1465-9921-11-114.pdf
52. Pinelli E, Willers SM, Hoek D. Prevalence of antibodies against Ascaris suum and its association with allergic manifestations in 4-year-old children in The Netherlands: the PIAMA birth cohort study. Eur J Clin Microbiol Infect Dis. 2009; 28:1327-1334.
53. Scrivener S, Yemaneberhan H, Zebenigus M. Independent effects of intestinal parasite infection and domestic allergen exposure on risk of wheeze in Ethiopia: a nested case-control study. Lancet. 2001; 358:1493-1499.
54. Flohr C, Tuyen LN, Lewis S. Poor sanitation and helminth infection protect against skin sensitization in Vietnamese children: a cross-sectional study. J Allergy Clin Immunol. 2006; 118:1305-1311.
55. Schafer T, Meyer T, Ring J, Wichmann HE, Heinrich J. Worm infestation and the negative asso- ciation with eczema (atopic/nonatopic) and allergic sensitization. Allergy. 2005; 60:1014-1020.
56. Selassie FG, Stevens RH, Cullinan P. Total and specific IgE (house dust mite and intestinal helminths) in asthmatics and controls from Gondar, Ethiopia. Clin Exp Allergy. 2000; 30:356-358.
57. Van Riet E, Hartgers FC, Yazdanbakhsh M. Chronic helminth infections induce immunomodula- tion: consequences and mechanisms. Immunobiology. 2007; 212:475-490.
58. Araujo CA, Perini A, Martins MA, Macedo MS, Macedo-Soares MF. PAS-1, a protein from Asca- ris suum, modulates allergic inflammation via IL-10 and IFN-gamma, but not IL-12. Cytokine. 2008; 44:335-341.
59. Tsuji N, Miyoshi T, Islam MK. Recombinant Ascaris 16-kilodalton protein-induced protec- tion against Ascaris suum larval migration after intranasal vaccination in pigs. J Infect Dis. 2004; 190:1812-1820.
60. Tsuji N, Suzuki K, Kasuga-Aoki H. Intranasal immunization with recombinant Ascaris suum
14-kilodalton antigen coupled with cholera toxin B subunit induces protective immunity to A. suuminfection in mice. Infect Immun. 2001; 69:7285-7292.
61. Tsuji N, Kasuga-Aoki H, Isobe T, Arakawa T, Matsumoto Y. Cloning and characterization of a highly immunoreactive 37 kDa antigen with multi-immunoglobulin domains from the swine roundworm Ascaris suum. Int J Parasitol 2002. 32:1739-1746.
62. Islam MK, Miyoshi T, Yokomizo Y, Tsuji N. Molecular cloning and partial characterization of anematode-specific 24 kDa protein from Ascaris suum. Parasitol. 2005; 130:131-139.
63. Van Riet E,Wuhrer M,Wahyuni S. Antibody responses to Ascaris-derived proteins and glycoli- pids: the role of phosphorylcholine. Parasite Immunol. 2006; 28:363-371.
64. Perrigoue JG, Marshall FA, Artis D. On the hunt for helminths: innate immune cells in the recog- nition and response to helminth parasites. Cell Microbiol. 2008; 10:1757-1764.
65. Da Silva CA, Pochard P, Lee CG, Elias JA. Chitin particles are multifaceted immune adjuvants. Am J Respir Crit Care Med. 2010; 182:1482-1491.
66. Acevedo N, Sanchez J, Erler A. IgE cross-reactivity between Ascaris and domestic mite aller- gens: the role of tropomyosin and the nematode polyprotein ABA-1. Allergy. 2009; 64:1635-1643.
67. Acevedo NEA, Briza P, Puccio F, Ferreira F, Caraballo L. Allergenicity of Ascaris lumbricoides tropomyosin and IgE sensitization among asthmatic patients in a tropical environment. Int Arch of Allergy Immunol. 2011; 154:195-206.
68. Lopez N, de Barros-Mazon S, Vilela MM, Condino Neto A, Ribeiro JD. Are immunoglobulin E levels associated with early wheezing? A prospective study in Brazilian infants. Eur Respir J. 2002; 20:640-645.
69. Endara P, Vaca M, Chico ME. Long-term periodic anthelmintic treatments are associated with increased allergen skin reactivity. Clin Exp Allergy. 2010; 40:1669-1677.
70. Strachan DP. Hay fever, hygiene, and household size. BMJ. 1989; 299:1259-1260.
71. Mc Sorley HJ, Maizels RM. Helminth Infections and Host Immune Regulation. Clin Microbiol Rev. 2012; 25:585-608.
72. Flohr C, Nagel G, Weinmayr G. Tuberculosis, bacillus Calmette-Guerin vaccination, and allergic disease: findings from the International Study of Asthma and Allergies in Childhood Phase Two. Pe- diatr Allergy Immunol. 2012; 23:324-331.
73. Sharma SK, Banga A. Prevalence and risk factors for wheezing in children from rural areas of north India. Allergy Asthma Proc. 2007; 28:647-653.
74. Chatkin MN, Menezes AM, Victora CG, Barros FC. High prevalence of asthma in preschool chil- dren in Southern Brazil: a population-based study. Pediatr Pulmonol. 2003; 35:296-301.
75. Pitrez PM, Stein RT. Asthma in Latin America: the dawn of a new epidemic. Curr Opin Allergy Clin Immunol. 2008; 8:378-383.
76. Pearce N, Ait-Khaled N, Beasley R. Worldwide trends in the prevalence of asthma symptoms: phase III of the International Study of Asthma and Allergies in Childhood (ISAAC). Thorax. 2007; 62:758-766.
77. Sole D, Melo KC, Camelo-Nunes IC. Changes in the prevalence of asthma and allergic diseases among Brazilian schoolchildren (13-14 years old): comparison between ISAAC Phases One and Three. J Trop Pediatr. 2007; 53:13-21.
78. Kuschnir FC, Alves da Cunha AJ. Environmental and socio-demographic factors associated to asthma in adolescents in Rio de Janeiro, Brazil. Pediatr Allergy Immunol. 2007; 18:142-148.
79. Garcia E, Aristizabal G, Vasquez C, Rodriguez-Martinez CE, Sarmiento OL, Satizabal CL. Pre- valence of and factors associated with current asthma symptoms in school children aged 6-7 and 13-14 yrs. old in Bogota, Colombia. Pediatr Allergy Immunol. 2008; 19:307-314.
80. Cooper PJ, Chico ME, Rodrigues LC. 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.
81. Lynch NR, Lopez RI, Di Prisco-Fuenmayor MC. Allergic reactivity and socio-economic level in a tropical environment. Clin Allergy. 1987; 17:199-207.
82. Holt PG. Parasites, atopy, and the hygiene hypothesis: resolution of a paradox? Lancet. 2000; 356:1699-1701.
83. Van Dellen RG, Thompson Jr JH. Absence of intestinal parasites in asthma. N Engl J Med. 1971; 285:146-148.
84. Gerrard JW, Geddes CA, Reggin PL, Gerrard CD, Horne S. Serum IgE levels in white and metis communities in Saskatchewan. Ann Allergy. 1976; 37:91-100.
85. Yazdanbakhsh M, Kremsner PG, van Ree R. Allergy, parasites, and the hygiene hypothesis. Science. 2002; 296:490-494.
86. McKay DM. The therapeutic helminth? Trends Parasitol. 2008; 24:1-6.
87. Weinstock JV. The worm returns. Nature. 2012; 491:183-185.
88. Fleming JO, Weinstock JV. Clinical trials of helminth therapy in autoimmune diseases: rationale and findings. Parasite Immunol. 2015; 6:277-292.
89. Summers RW. Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease. Am J Gastroenterol. 2003; 98:2034-2041.
90. Bager P, Arnved J, Rønborg S, Wohlfahrt J, Poulsen LK, Westergaard T. Trichuris suis ova the- rapy for allergic rhinitis: a randomized, double-blind, placebo-controlled clinical trial. J Allergy Clin Immunol. 2010; 125:123-130.
91. Feary J, Venn A, Brown A, Hooi D, Falcone FH, Mortimer K. Safety of hookworm infection in indi- viduals with measurable airway responsiveness: a randomized placebo-controlled feasibility study. Clin Exp Allergy. 2009; 39:1060-1088.
92. Feary JR, Venn AJ, Mortimer K, Brown AP, Hooi D, Falcone FH. Experimental hookworm infection: a randomized placebo-controlled trial in asthma. Clin Exp Allergy. 2010; 40:299-306.
93. Helmby H. Helminths and our immune system: friend or foe? Parasitol Int. 2009; 58:121-127.
