Factors associated with secretory IgA levels in colostrum and breastmilk
A Cohort Study
Abstract
Background Secretory IgA (sIgA) content of breastmilk in the first postpartum month is a reflection of the pregnant woman's immune response to environmental antigen exposure. The role of secretory IgA in breastmilk is to protect and support the development of the neonatal immune response in early life.
Objective To examine possible factors associated with sIgA levels in breastmilk and colostrum, including environmental exposure, food consumed, maternal history of atopy, and the appearance of allergic symptoms in infants. As a secondary objective, we determined the association between infant factors (IgE, exposure to cigarette smoke) and maternal factors (sIgA, maternal allergies) with infant allergies.
Methods This prospective cohort study of 80 postpartum mothers and their infants was conducted at Sultan Agung Islamic Hospital, Semarang. We collected maternal colostrum on the second or third postpartum day and mature milk between the 22nd to 25th postpartum day. Exposure factors to mothers and infants in the final trimester of pregnancy up to one month postpartum was recorded through a questionnaire and home visits. The infant’s IgE level was measured at 4 months of age.
Results Mean colostrum sIgA was 108.9 (SD 16.5) mg/dL (95%CI 97.9 to 121.1 mg/dL) and mean mature milk sIgA was 94.1 (SD 23.9) mg/dL (95%CI 89.1 to 99.2 mg/dL). Mean colostrum sIgA levels were higher in mothers exposed to cigarette smoke [119.1 (SD 1.7) vs. 92.9 (SD 1.5) mg/dL; P=0.026] and frequent infections [128.2 (SD 1.7) vs. 95.9 (SD 1.6) mg/dL; P=0.007] compared to that in unexposed mothers. Mean colostrum sIgA was also higher in mothers with atopic allergy than in those without (136.8 mg/dL vs. 99.3 mg/dL; p=0.017) and in mothers of infants with IgE levels >29 IU/ml than in mothers of infants with IgE levels <29 IU/mL (136.8 vs. 101.2 mg/mg/dL; P=0.045). Elevated colostrum sIgA (>136.8 mg/dL) was not associated with allergies in the infants (P=0.269).
Conclusions Maternal atopic allergy and frequent infections are associated with increased colostrum sIgA levels. Breastmilk sIgA levels are not associated with allergies in the infant. Maternal exposure to antigens may stimulate the production of specific breastmilk sIgA.
References
2. M’Rabet L, Vos AP, Boehm G, Garssen J. Breast-feeding and its role in early development of the immune system in infants: consequences for health later in life. J Nutr. 2008;138:1782-90. DOI: https://doi.org/10.1093/jn/138.9.1782S.
3. International Union Against Tuberculosis and Lung Disease, International Study of Asthma and Allergies in Children/ISAAC . The Global Asthma Report 2011. Paris:The International Union Against Tuberculosis and Lung Disease;2011. p.1-13. ISBN: 978-2-914365-83-3.
4. Health Research and Development Agency. Hasil Utama RISKESDAS 2018 [Internet]. Jakarta; Ministry of Health R.I. 2018; [cited 2021 Jan 8]. Available from: https://kesmas.kemkes.go.id/assets/upload/dir_519d41d8cd98f00/files/Hasil-riskesdas-2018_1274.pdf.
5. Abbas AK, Lichtman AH, Pillai S. Cellular and molecular immunology. 8th ed. Philadelphia: Elsevier Saunders; 2015.
6. Mantis NJ, Rol N, Corthésy B. Secretory IgA's complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunol. 2011;4:603-11. DOI: https://doi.org/10.1038/mi.2011.41.
7. Savilahti E, Siltanen M, Kajosaari M, Vaarala O, Saarinen KM. IgA antibodies, TGF-beta1 and -beta2, and soluble CD14 in the colostrum and development of atopy by age 4. Pediatr Res. 2005;58:1300-5. DOI: https://doi.org/10.3389/fimmu.2018.02222.
8. Pawankar R, Canonica GW, Holgate ST, Lockey RF, editors. World allergy organization white book on allergy [Internet]. Milwaukee: World Allergy Organization; 2013[cited 2016 Aug 2]. Available from: https:// https://www.worldallergy.org/UserFiles/file/WhiteBook2-2013-v8.pdf.
9. Tada J. Diagnostic standard for atopic dermatitis. JMAJ. 2002;45:460–5.
10. International Study of Asthma and Allergies in Childhood Phase II Modules [Internet]. Munster: The University of Auckland; c2012; [cited 2017 Aug 12]. Available from: http://isaac.auckland.ac.nz/phases/phasetwo/phasetwomodules.pdf.
11. Morelli S, Mandal M, Goldsmith LT, Kashani BN, Ponzio NM. The maternal immune system during pregnancy and its influence on fetal development. Res Rep Biol. 2015;6:171-89. DOI: https://doi.org/10.2147/RRB.S80652.
12. Rowe JH, Ertelt JM, Xin L, Way SS. Pregnancy imprints regulatory memory that sustains anergy to fetal antigen. Nature. 2012; 490:102–6. DOI: https://doi.org/10.1038/nature11462.
13. Boonpiyathad T, Sozener ZC, Akdis M, Akdis C. The role of Treg cell subsets in allergic disease. Asian Pac J Allergy Immunol. 2020;38:139-49. DOI: https://doi.org/10.12932/AP-030220-0754.
14. Tomicic S, Johansson G, Voor T, Bjorksten B, Bottcher MF, Jenmalm MC. Breastmilk cytokine and IgA composition differ in Estonian and Swedish mothers-relationship to microbial pressure and infant allergy. Pediatr Res. 2010;68:330-4. DOI: https://doi.org/10.1203/PDR.0b013e3181ee049d.
15. Fox A, Marino J, Amanat F, Krammer F, Holbrook JH, Pazner SZ, et al. Evidence of a significant secretory-IgA-dominant SARS-CoV-2 immune response in human milk following recovery from COVID-19. medRxiv. 2020. 05.04.20089995. DOI: https://doi.org/10.1101/2020.05.04.20089995.
16. Ismail IH, Licciardi PV, Oppedisano F, Boyle RJ, Tang ML. Relationship between breastmilk sCD14, TGF-?1 and total IgA in the first month and development of eczema during infancy. Pediatr Allergy Immunol. 2013;24:352-60.
17. Subandi ST, Ratih NK, Soka S , Suwanto A. Effect of tempeh supplementation on the profiles of human intestinal immune system and gut microbiota. Microbiol Indones. 2017;11:12-7.
18. Mei C, Yang W, Wei X, Wu K, Huang D. The unique microbiome and innate immunity during pregnancy. Front Immunol. 2019;10:2886. DOI: https://doi.org/10.3389/fimmu.2019.02886.
19. Plunkett C, Nagler CR. The influenced of the microbiome on allergic sensitization to food. J Immunol. 2017;198:581-9. DOI: https://doi.org/10.4049/jimmunol.1601266.
20. Hagh LG, Zakavi F, Ansarifar S, Ghasemzadeh O, Solgi G. Association of dental caries and salivary sIgA with tobacco smoking. Aust Dent J. 2013;58:219-23. DOI: https://doi.org/10.1111/adj.12059.
21. Suzuki N, Nakanishi K, Yoneda M, Hirofuji T, Hanioka T. Relationship between salivary stress biomarker levels and cigarette smoking in healthy young adults: an exploratory analysis. Tob Induc Dis. 2016;14:20. DOI: https://doi.org/10.1186/s12971-016-0085-8.
22. Bauer RN, Diaz-Sanchez D, Jaspers I. Effects of air pollutants on innate immunity: the role of Toll-like receptors and nucleotide-binding oligomerization domain-like receptors. J Allergy Clin Immunol. 2012;129:14–26. DOI: https://doi.org/10.1016/j.jaci.2011.11.004.
23. Lee AJ, Thalayasingam M, Lee BW. Food allergy in Asia: how does it compare. Asia Pac Allergy. 2013;3:3-14. DOI: https://doi.org/10.5415/apallergy.2013.3.1.3.
24. Safri M, Putra AR. Early allergy symptoms in infants aged 0-6 months on breastmilk substitutes. Paediatr Indonesia. 2015;55:18-22. DOI: https://doi.org/10.14238/pi55.1.2015.13-7.
25. Priyantini S, Suprihati, Widyastiti NS, Soemantri . The low umbilical cord zinc levels lead to atopic allergic infants: a cohort study during 0-4 months of age. Bangladesh J Med Sci. 2019;19:114-21. DOI: https://doi.org/10.3329/bjms.v19i1.43883.
26. Siregar B, Irsa L, Supriatmo, Loebis S, Evalina R. Skin prick test reactivity in atopic children and their number of siblings. Paediatr Indones. 2015;55:189-93. DOI: https://doi.org/10.14238/pi55.4.2015.189-93.
27. Corthésy B. Roundtrip ticket for secretory IgA: role in mucosal homeostasis. J Immunol. 2007;178:27-32. DOI: https://doi.org/10.4049/immunol.178.1.27.
Copyright (c) 2023 Sri Priyantini Mulyani, Suprihati Winarto
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
Authors who publish with this journal agree to the following terms:
Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
Accepted 2023-03-02
Published 2023-03-02
