期刊论文详细信息
Allergy, Asthma & Clinical Immunology
The development of TH2 responses from infancy to 4 years of age and atopic sensitization in areas endemic for helminth infections
Yenny Djuardi3  Taniawati Supali1  Heri Wibowo1  Yvonne CM Kruize3  Serge A Versteeg2  Ronald van Ree2  Erliyani Sartono3  Maria Yazdanbakhsh3 
[1] Department of Parasitology, Faculty of Medicine, University of Indonesia, Salemba 6, Jakarta 10430, Indonesia
[2] Department of Experimental Immunology and Department of Otorhinolaryngology, Academic Medical Center, Amsterdam University, Amsterdam, The Netherlands
[3] Department of Parasitology, Leiden University Medical Center, Leiden, The Netherlands
关键词: Children;    Skin prick test;    Atopy;    Helminth;    IL-5;    IgE;    TH2;   
Others  :  792341
DOI  :  10.1186/1710-1492-9-13
 received in 2012-11-13, accepted in 2013-03-01,  发布年份 2013
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【 摘 要 】

Background

Helminth infections and allergies are associated with TH2 responses. Whereas the development of TH2 responses and allergic disorders in pediatric populations has been examined in affluent countries, no or little data exist from low income regions of the world.

The aim of this study is to examine factors influencing the development of TH2 responses of children born in areas endemic for helminth infections and to relate these factors to atopic sensitization at 4 years of age.

Methods

Data were collected from pregnant mothers on helminth infections, education and socioeconomic status (SES). Total IgE, IL-5 in response to mitogen, and helminth antigens were measured in children at 2, 5, 12, 24 and 48 months of age. Skin prick testing (SPT) and allergen-specific IgE were determined at 4 years of age.

Results

Strong TH2 responses were seen at 5 months of age and increased with time. Although maternal filarial infection was associated with helminth-antigen specific TH2 responses, it was low maternal education or SES but not helminth infection, which was associated with the development of high total IgE and PHA-induced IL-5. At 4 years of age when allergen reactivity was assessed by SPT, the high general TH2 responses did not translate into higher prevalence of SPT. The risk factor for SPT reactivity was low maternal education which decreased the risk of SPT positivity to allergens (adjusted OR, 0.32; 95% CI, 0.12 – 0.87) independently of maternal filarial infection which tended to reduce the child’s risk for being SPT positive (adjusted OR, 0.35; 95% CI, 0.07 – 1.70).

Conclusions

In areas endemic for helminths, potent TH2 responses were seen early in life, but did not translate into a higher SPT reactivity to allergens. Therefore, in many parts of the world TH2 responses in general and IgE in particular cannot be used for diagnosis of allergic diseases.

【 授权许可】

   
2013 Djuardi et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Kurukulaaratchy RJ, Matthews S, Arshad SH: Defining childhood atopic phenotypes to investigate the association of atopic sensitization with allergic disease. Allergy 2005, 60:1280-1286.
  • [2]Pesonen M, Kallio MJ, Siimes MA, Elg P, Bjorksten F, Ranki A: Cord serum immunoglobulin E as a risk factor for allergic symptoms and sensitization in children and young adults. Pediatr Allergy Immunol 2009, 20:12-18.
  • [3]Perkin MR, Strachan DP, Hc W, Lack G, Golding J: The predictive value of early life total immunoglobulin E measurement in identifying atopic children in a population-based birth cohort study. Pediatr Allergy Immunol 2006, 17:118-124.
  • [4]Prescott SL, Macaubas C, Smallacombe T, Holt BJ, Sly PD, Holt PG: Development of allergen-specific T-cell memory in atopic and normal children. Lancet 1999, 353:196-200.
  • [5]Rothers J, Halonen M, Stern DA, Lohman IC, Mobley S, Spangenberg A: Adaptive cytokine production in early life differentially predicts total IgE levels and asthma through age 5 years. J Allergy Clin Immunol 2011, 128:397-402.
  • [6]Asher MI, Montefort S, Bjorksten B, Lai CK, Strachan DP, Weiland SK: Worldwide time trends in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and eczema in childhood: ISAAC phases One and three repeat multicountry cross-sectional surveys. Lancet 2006, 368:733-743.
  • [7]Yazdanbakhsh M, van den Biggelaar A, Maizels RM: Th2 Responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends Immunol 2001, 22:372-377.
  • [8]Feary J, Britton J, Leonardi-Bee J: Atopy and current intestinal parasite infection: a systematic review and meta-analysis. Allergy 2011, 66:569-578.
  • [9]van den Biggelaar AH, Lopuhaa C, van RR, van der Zee JS, Jans J, Hoek A: The prevalence of parasite infestation and house dust mite sensitization in gabonese schoolchildren. Int Arch Allergy Immunol 2001, 126:231-238.
  • [10]Flohr C, Quinnell RJ, Britton J: Do helminth parasites protect against atopy and allergic disease? Clin Exp Allergy 2009, 39:20-32.
  • [11]Hogewoning AA, Larbi IA, Addo HA, Amoah AS, Boakye D, Hartgers F: Allergic characteristics of urban schoolchildren with atopic eczema in ghana. J Eur Acad Dermatol Venereol 2010, 24:1406-1412.
  • [12]Weinmayr G, Weiland SK, Bjorksten B, Brunekreef B, Buchele G, Cookson WO: Atopic sensitization and the international variation of asthma symptom prevalence in children. Am J Respir Crit Care Med 2007, 176:565-574.
  • [13]Obeng BB, Hartgers F, Boakye D, Yazdanbakhsh M: Out of africa: what can be learned from the studies of allergic disorders in africa and africans? Curr Opin Allergy Clin Immunol 2008, 8:391-397.
  • [14]Djuardi Y, Wibowo H, Supali T, Ariawan I, Bredius RG, Yazdanbakhsh M: Determinants of the relationship between cytokine production in pregnant women and their infants. PLoS One 2009, 4:e7711.
  • [15]Yazdanbakhsh M, Paxton WA, Kruize YC, Sartono E, Kurniawan A, van het WA: T cell responsiveness correlates differentially with antibody isotype levels in clinical and asymptomatic filariasis. J Infect Dis 1993, 167:925-931.
  • [16]Eriksson M, Sartono E, Martins CL, Bale C, Garly ML, Whittle H: A comparison of ex vivo cytokine production in venous and capillary blood. Clin Exp Immunol 2007, 150:469-476.
  • [17]Grogan JL, Kremsner PG, Deelder AM, Yazdanbakhsh M: Elevated proliferation and interleukin-4 release from CD4+ cells after chemotherapy in human schistosoma haematobium infection. Eur J Immunol 1996, 26:1365-1370.
  • [18]van den Biggelaar AH, van RR, Rodrigues LC, Lell B, Deelder AM, Kremsner PG: Decreased atopy in children infected with schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 2000, 356:1723-1727.
  • [19]Havstad S, Wegienka G, Zoratti EM, Lynch SV, Boushey HA, Nicholas C: Effect of prenatal indoor pet exposure on the trajectory of total IgE levels in early childhood. J Allergy Clin Immunol 2011, 128:880-885.
  • [20]Reijmerink NE, Kerkhof M, Bottema RW, Gerritsen J, Stelma FF, Thijs C: Toll-like receptors and microbial exposure: gene-gene and gene-environment interaction in the development of atopy. Eur Respir J 2011, 38:833-840.
  • [21]Kjaer HF, Eller E, Andersen KE, Host A, Bindslev-Jensen C: The association between early sensitization patterns and subsequent allergic disease. The DARC birth cohort study. Pediatr Allergy Immunol 2009, 20:726-734.
  • [22]Arshad SH, Tariq SM, Matthews S, Hakim E: Sensitization to common allergens and its association with allergic disorders at age 4 years: a whole population birth cohort study. Pediatrics 2001, 108:E33.
  • [23]Kerkhof M, Wijga A, Smit HA, de Jongste JC, Aalberse RC, Brunekreef B: The effect of prenatal exposure on total IgE at birth and sensitization at twelve months and four years of age: the PIAMA study. Pediatr Allergy Immunol 2005, 16:10-18.
  • [24]Asarnoj A, Ostblom E, Kull I, Lilja G, Pershagen G, Hedlin G: Sensitization to inhalant allergens between 4 and 8 years of age is a dynamic process: results from the BAMSE birth cohort. Clin Exp Allergy 2008, 38:1507-1513.
  • [25]Johansson SG, Mellbin T, Vahlquist B: Immunoglobulin levels in ethiopian preschool children with special reference to high concentrations of immunoglobulin E (IgND). Lancet 1968, 1:1118-1121.
  • [26]Matricardi PM, Bockelbrink A, Gruber C, Keil T, Hamelmann E, Wahn U: Longitudinal trends of total and allergen-specific IgE throughout childhood. Allergy 2009, 64:1093-1098.
  • [27]Grundbacher FJ, Massie FS: Levels of immunoglobulin G, M, a, and E at various ages in allergic and nonallergic black and white individuals. J Allergy Clin Immunol 1985, 75:651-658.
  • [28]Levin ME, Le Souef PN, Motala C: Total IgE in urban black South African teenagers: the influence of atopy and helminth infection. Pediatr Allergy Immunol 2008, 19:449-454.
  • [29]Wahyuni S, Sartono E, Supali T, van der Zee JS, Mangali A, van RR: Clustering of allergic outcomes within families and households in areas endemic for helminth infections. Int Arch Allergy Immunol 2005, 136:356-364.
  • [30]Curtale F, Pezzotti P, Sharbini AL, Al MH, Ingrosso P, Saad YS: Knowledge, perceptions and behaviour of mothers toward intestinal helminths in upper Egypt: implications for control. Health Policy Plan 1998, 13:423-432.
  • [31]Ostan I, Kilimcioglu AA, Girginkardesler N, Ozyurt BC, Limoncu ME, Ok UZ: Health inequities: lower socio-economic conditions and higher incidences of intestinal parasites. BMC Publ Health 2007, 7:342. BioMed Central Full Text
  • [32]Quihui L, Valencia ME, Crompton DW, Phillips S, Hagan P, Morales G: Role of the employment status and education of mothers in the prevalence of intestinal parasitic infections in mexican rural schoolchildren. BMC Publ Health 2006, 6:225. BioMed Central Full Text
  • [33]Seiskari T, Kondrashova A, Viskari H, Kaila M, Haapala AM, Aittoniemi J: Allergic sensitization and microbial load–a comparison between finland and russian karelia. Clin Exp Immunol 2007, 148:47-52.
  • [34]Amberbir A, Medhin G, Erku W, Alem A, Simms R, Robinson K: Effects of helicobacter pylori, geohelminth infection and selected commensal bacteria on the risk of allergic disease and sensitization in 3-year-old ethiopian children. Clin Exp Allergy 2011, 41:1422-1430.
  • [35]Martino D, Prescott S: Epigenetics and prenatal influences on asthma and allergic airways disease. Chest 2011, 139:640-647.
  • [36]Szepfalusi Z, Pichler J, Elsasser S, van DK, Ebner C, Bernaschek G: Transplacental priming of the human immune system with environmental allergens can occur early in gestation. J Allergy Clin Immunol 2000, 106:530-536.
  • [37]Metenou S, Suguitan AL Jr, Long C, Leke RG, Taylor DW: Fetal immune responses to plasmodium falciparum antigens in a malaria-endemic region of cameroon. J Immunol 2007, 178:2770-2777.
  • [38]Bal MS, Mandal NN, DAS MK, Kar SK, Sarangi SS, Beuria MK: Transplacental transfer of filarial antigens from wuchereria bancrofti-infected mothers to their offspring. Parasitology 2010, 137:669-673.
  • [39]Eloi-Santos SM, Novato-Silva E, Maselli VM, Gazzinelli G, Colley DG, Correa-Oliveira R: Idiotypic sensitization in utero of children born to mothers with schistosomiasis or Chagas’ disease. J Clin Invest 1989, 84:1028-1031.
  • [40]Pit DS, Polderman AM, Schulz-Key H, Soboslay PT: Prenatal immune priming with helminth infections: parasite-specific cellular reactivity and Th1 and Th2 cytokine responses in neonates. Allergy 2000, 55:732-739.
  • [41]King CL, Malhotra I, Mungai P, Wamachi A, Kioko J, Ouma JH: B cell sensitization to helminthic infection develops in utero in humans. J Immunol 1998, 160:3578-3584.
  • [42]Supali T, Djuardi Y, Wibowo H, van RR, Yazdanbakhsh M, Sartono E: Relationship between different species of helminths and atopy: a study in a population living in helminth-endemic area in sulawesi, indonesia. Int Arch Allergy Immunol 2010, 153:388-394.
  • [43]Alcantara-Neves NM, Badaro SJ, dos Santos MC, Pontes-de-Carvalho L, Barreto ML: The presence 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 2010, 11:114. BioMed Central Full Text
  • [44]Medeiros M Jr, Almeida MC, Figueiredo JP, Atta AM, Mendes CM, Araujo MI: Low frequency of positive skin tests in asthmatic patients infected with schistosoma mansoni exposed to high levels of mite allergens. Pediatr Allergy Immunol 2004, 15:142-147.
  • [45]Santiago HC, Bennuru S, Boyd A, Eberhard M, Nutman TB: Structural and immunologic cross-reactivity among filarial and mite tropomyosin: implications for the hygiene hypothesis. J Allergy Clin Immunol 2011, 127:479-486.
  • [46]Mpairwe H, Webb EL, Muhangi L, Ndibazza J, Akishule D, Nampijja M: Anthelminthic treatment during pregnancy is associated with increased risk of infantile eczema: randomised-controlled trial results. Pediatr Allergy Immunol 2011, 22:305-312.
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