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Dietary Diversity during Early Infancy Increases Microbial Diversity and Prevents Egg Allergy in High-Risk Infants

  • Bo Ra Lee (Department of Pediatrics, Uijeongbu Eulji Medical Center, Eulji University School of Medicine) ;
  • Hye-In Jung (Department of Pediatrics, Nowon Eulji Medical Center, Eulji University School of Medicine) ;
  • Su Kyung Kim (Department of Pediatrics, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Mijeong Kwon (Environmental Health Center for Atopic Diseases, Samsung Medical Center) ;
  • Hyunmi Kim (Environmental Health Center for Atopic Diseases, Samsung Medical Center) ;
  • Minyoung Jung (Department of Pediatrics, Kosin University Gospel Hospital, Kosin University School of Medicine) ;
  • Yechan Kyung (Department of Pediatrics, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine) ;
  • Byung Eui Kim (Environmental Health Center for Atopic Diseases, Samsung Medical Center) ;
  • Suk-Joo Choi (Department of Obstetrics and Gynecology, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Soo-Young Oh (Department of Obstetrics and Gynecology, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Sun-Young Baek (Center for Biomedical Statistics, Samsung Medical Center) ;
  • Seonwoo Kim (Center for Biomedical Statistics, Samsung Medical Center) ;
  • Jaewoong Bae (R&D Institute, BioEleven Co., Ltd.) ;
  • Kangmo Ahn (Department of Pediatrics, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Jihyun Kim (Department of Pediatrics, Samsung Medical Center, Sungkyunkwan University School of Medicine)
  • Received : 2021.09.17
  • Accepted : 2021.10.29
  • Published : 2022.04.30

Abstract

We aimed to investigate associations of dietary diversity (DD) with gut microbial diversity and the development of hen's egg allergy (HEA) in infants. We enrolled 68 infants in a high-risk group and 32 infants in a control group based on a family history of allergic diseases. All infants were followed from birth until 12 months of age. We collected infant feeding data, and DD was defined using 3 measures: the World Health Organization definition of minimum DD, food group diversity, and food allergen diversity. Gut microbiome profiles and expression of cytokines were evaluated by bacterial 16S rRNA sequencing and real-time reverse transcriptase-polymerase chain reaction. High DD scores at 3 and 4 months were associated with a lower risk of developing HEA in the high-risk group, but not in the control group. In the high-risk group, high DD scores at 3, 4, and 5 months of age were associated with an increase in Chao1 index at 6 months. We found that the gene expression of IL-4, IL-5, IL-6, and IL-8 were higher among infants who had lower DD scores compared to those who had higher DD scores in high-risk infants. Additionally, high-risk infants with a higher FAD score at 5 months of age showed a reduced gene expression of IL-13. Increasing DD within 6 months of life may increase gut microbial diversity, and thus reduce the development of HEA in infants with a family history of allergic diseases.

Keywords

Acknowledgement

This work was supported by Korea Environment Industry and Technology Institute (KEITI) through Environmental Health Action Program, funded by Korea Ministry of Environment (MOE) (2017001360006).

References

  1. Natsume O, Kabashima S, Nakazato J, Yamamoto-Hanada K, Narita M, Kondo M, Saito M, Kishino A, Takimoto T, Inoue E, et al. Two-step egg introduction for prevention of egg allergy in high-risk infants with eczema (PETIT): a randomised, double-blind, placebo-controlled trial. Lancet 2017;389:276-286.
  2. Sicherer SH, Sampson HA. Food allergy: a review and update on epidemiology, pathogenesis, diagnosis, prevention, and management. J Allergy Clin Immunol 2018;141:41-58.
  3. Park M, Kim D, Ahn K, Kim J, Han Y. Prevalence of immediate-type food allergy in early childhood in Seoul. Allergy Asthma Immunol Res 2014;6:131-136.
  4. Du Toit G, Roberts G, Sayre PH, Bahnson HT, Radulovic S, Santos AF, Brough HA, Phippard D, Basting M, Feeney M, et al. Randomized trial of peanut consumption in infants at risk for peanut allergy. N Engl J Med 2015;372:803-813.
  5. Caffarelli C, Di Mauro D, Mastrorilli C, Bottau P, Cipriani F, Ricci G. Solid food introduction and the development of food allergies. Nutrients 2018;10:1790.
  6. Togias A, Cooper SF, Acebal ML, Assa'ad A, Baker JR Jr, Beck LA, Block J, Byrd-Bredbenner C, Chan ES, Eichenfield LF, et al. Addendum guidelines for the prevention of peanut allergy in the United States: report of the National Institute of Allergy and Infectious Diseases-sponsored expert panel. J Allergy Clin Immunol 2017;139:29-44.
  7. Roduit C, Frei R, Depner M, Schaub B, Loss G, Genuneit J, Pfefferle P, Hyvarinen A, Karvonen AM, Riedler J, et al. Increased food diversity in the first year of life is inversely associated with allergic diseases. J Allergy Clin Immunol 2014;133:1056-1064.
  8. Venter C, Maslin K, Holloway JW, Silveira LJ, Fleischer DM, Dean T, Arshad SH. Different measures of diet diversity during infancy and the association with childhood food allergy in a UK birth cohort study. J Allergy Clin Immunol Pract 2020;8:2017-2026.
  9. Kulkarni DH, Gustafsson JK, Knoop KA, McDonald KG, Bidani SS, Davis JE, Floyd AN, Hogan SP, Hsieh CS, Newberry RD. Goblet cell associated antigen passages support the induction and maintenance of oral tolerance. Mucosal Immunol 2020;13:271-282.
  10. Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly-Y M, Glickman JN, Garrett WS. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013;341:569-573.
  11. Stefka AT, Feehley T, Tripathi P, Qiu J, McCoy K, Mazmanian SK, Tjota MY, Seo GY, Cao S, Theriault BR, et al. Commensal bacteria protect against food allergen sensitization. Proc Natl Acad Sci U S A 2014;111:13145-13150.
  12. Wei-Liang Tan J, Valerio C, Barnes EH, Turner PJ, Van Asperen PA, Kakakios AM, Campbell DE; Beating Egg Allergy Trial (BEAT) Study Group. A randomized trial of egg introduction from 4 months of age in infants at risk for egg allergy. J Allergy Clin Immunol 2017;139:1621-1628.e8.
  13. Perkin MR, Logan K, Tseng A, Raji B, Ayis S, Peacock J, Brough H, Marrs T, Radulovic S, Craven J, et al. Randomized trial of introduction of allergenic foods in breast-fed infants. N Engl J Med 2016;374:1733-1743.
  14. Venter C, Greenhawt M, Meyer RW, Agostoni C, Reese I, du Toit G, Feeney M, Maslin K, Nwaru BI, Roduit C, et al. EAACI position paper on diet diversity in pregnancy, infancy and childhood: novel concepts and implications for studies in allergy and asthma. Allergy 2020;75:497-523.
  15. On HR, Lee SE, Kim SE, Hong WJ, Kim HJ, Nomura T, Suzuki S, Shimizu H, Kim SC. Filaggrin mutation in Korean patients with atopic dermatitis. Yonsei Med J 2017;58:395-400.
  16. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010;7:335-336.
  17. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 2006;72:5069-5072.
  18. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017;67:1613-1617.
  19. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010;26:2460-2461.
  20. Segata N, Huttenhower C. Toward an efficient method of identifying core genes for evolutionary and functional microbial phylogenies. PLoS One 2011;6:e24704.
  21. Sampson HA, O'Mahony L, Burks AW, Plaut M, Lack G, Akdis CA. Mechanisms of food allergy. J Allergy Clin Immunol 2018;141:11-19.
  22. Lopes JP, Sicherer S. Food allergy: epidemiology, pathogenesis, diagnosis, prevention, and treatment. Curr Opin Immunol 2020;66:57-64.
  23. Derrien M, Veiga P. Rethinking diet to aid human-microbe symbiosis. Trends Microbiol 2017;25:100-112.
  24. Derrien M, Alvarez AS, de Vos WM. The gut microbiota in the first decade of life. Trends Microbiol 2019;27:997-1010.
  25. Marrs T, Jo JH, Perkin MR, Rivett DW, Witney AA, Bruce KD, Logan K, Craven J, Radulovic S, Versteeg SA, et al. Gut microbiota development during infancy: Impact of introducing allergenic foods. J Allergy Clin Immunol 2021;147:613-621.e9.
  26. Fleischer DM, Chan ES, Venter C, Spergel JM, Abrams EM, Stukus D, Groetch M, Shaker M, Greenhawt M. A consensus approach to the primary prevention of food allergy through nutrition: guidance from the American Academy of Allergy, Asthma, and Immunology; American College of Allergy, Asthma, and Immunology; and the Canadian Society for Allergy and Clinical Immunology. J Allergy Clin Immunol Pract 2021;9:22-43.e4.
  27. Perkin MR, Logan K, Bahnson HT, Marrs T, Radulovic S, Craven J, Flohr C, Mills EN, Versteeg SA, van Ree R, et al. Efficacy of the Enquiring About Tolerance (EAT) study among infants at high risk of developing food allergy. J Allergy Clin Immunol 2019;144:1606-1614.e2.