Allergy, Asthma & Respiratory Disease

The Korean Academy of Asthma, Allergy and Clinical Immunology (대한천식알레르기학회)
권호 표지
DOI QR코드

DOI QR Code

Allergic rhinitis and hygiene hypothesis

알레르기비염과 위생가설

  • Hye Mi Jee (Department of Pediatrics, CHA Bundang Medical Center, CHA University School of Medicine) ;
  • Minji Kim (Department of Pediatrics, Chungnam National University Sejong Hospital, Chungnam National University College of Medicine) ;
  • Hyun Hee Kim (Department of Pediatrics, College of Medicine, The Catholic University of Korea) ;
  • Hyo-Bin Kim (Department of Pediatrics, Inje University Sanggye Paik Hospital) ;
  • Yeong-Ho Rha (Department of Pediatrics, School of Medicine, Kyung Hee University) ;
  • Yang Park (Department of Pediatrics, Jangheung Integrative Medical Hospital, Wonkwang University School of Medicine) ;
  • Myongsoon Sung (Department of Pediatrics, Soonchunhyang University Gumi Hospital) ;
  • Youn Ho Shin (Department of Pediatrics, CHA Gangnam Medical Center, CHA University School of Medicine) ;
  • Hye Yung Yum (Department of Pediatrics, Seoul Medical Center) ;
  • Kyung Suk Lee (Department of Pediatrics, Hanyang University Guri Hospital, Hanyang University College of Medicine) ;
  • Yong Ju Lee (Department of Pediatrics, Yongin Severance Hospital, Yonsei University College of Medicine) ;
  • Yoon Hong Chun (Department of Pediatrics, College of Medicine, The Catholic University of Korea) ;
  • Bong Seok Choi (Department of Pediatrics, School of Medicine, Kyungpook National University) ;
  • Sun Hee Choi (Department of Pediatrics, School of Medicine, Kyung Hee University) ;
  • Yong Mean Park (Department of Pediatrics, Konkuk University Medical Center, Konkuk University School of Medicine) ;
  • Rhinitis Study Group in the Korean Academy of Pediatric Allergy and Respiratory Diseases (Korean Academy of Pediatric Allergy and Respiratory Diseases)
  • 지혜미 (차의과학대학교 의학전문대학원 분당차병원 소아청소년과) ;
  • 김민지 (충남대학교 의과대학 세종충남대학교병원 소아청소년과) ;
  • 김현희 (가톨릭대학교 의과대학 소아과학교실) ;
  • 김효빈 (인제대학교 상계백병원 소아청소년과) ;
  • 나영호 (경희대학교 의과대학 소아청소년과학교실) ;
  • 박양 (원광대학교 의과대학 장흥통합의료병원 소아청소년과) ;
  • 성명순 (순천향대학교 구미병원 소아청소년과) ;
  • 신윤호 (차의과학대학교 의학전문대학원 강남차병원 소아청소년과) ;
  • 염혜영 (서울의료원 소아청소년과) ;
  • 이경석 (한양대학교 의과대학 소아청소년과학교실) ;
  • 이용주 (연세대학교 의과대학 용인세브란스병원 소아청소년과) ;
  • 전윤홍 (가톨릭대학교 의과대학 소아과학교실) ;
  • 최봉석 (경북대학교 의과대학 소아과학교실) ;
  • 최선희 (경희대학교 의과대학 소아청소년과학교실) ;
  • 박용민 (건국대학교 의학전문대학원 소아과학교실) ;
  • 대한 소아알레르기 호흡기학회 비염연구회 (대한 소아알레르기 호흡기학회)
  • Received : 2023.08.03
  • Accepted : 2023.09.07
  • Published : 2024.01.30
Download PDF
⟨ Previous Next ⟩

Abstract

The hygiene hypothesis, first proposed in 1989, suggested that reduced exposure to infections in early life leads to allergic diseases by the defects in the establishment of immune tolerance. Although many studies provided evidence that some exposure conditions, including family size, antibiotics, probiotics, and viral or bacterial infections, are strongly related to the prevalence of allergic diseases, thereby supporting the hygiene hypothesis, some evidence does not provide acceptable results for the hygiene hypothesis. Further, most studies have focused on patients with asthma or atopic dermatitis, not allergic rhinitis. In this review, we summarize the recent studies for and against the 'hygiene hypothesis' and identify causal association with the prevalence of allergic rhinitis.

Keywords

References

  1. Strachan DP. Hay fever, hygiene, and household size. BMJ 1989;299:1259-60.
  2. Braun-Fahrlander C, Riedler J, Herz U, Eder W, Waser M, Grize L, et al. Environmental exposure to endotoxin and its relation to asthma in schoolage children. N Engl J Med 2002;347:869-77.
  3. Strachan DP, Ait-Khaled N, Foliaki S, Mallol J, Odhiambo J, Pearce N, et al. Siblings, asthma, rhinoconjunctivitis and eczema: a worldwide perspective from the International Study of Asthma and Allergies in Childhood. Clin Exp Allergy 2015;45:126-36.
  4. Celedon JC, Wright RJ, Litonjua AA, Sredl D, Ryan L, Weiss ST, et al. Day care attendance in early life, maternal history of asthma, and asthma at the age of 6 years. Am J Respir Crit Care Med 2003;167:1239-43.
  5. Metsala J, Lundqvist A, Virta LJ, Kaila M, Gissler M, Virtanen SM. Prenatal and post-natal exposure to antibiotics and risk of asthma in childhood. Clin Exp Allergy 2015;45:137-45.
  6. Baraniuk JN. Pathogenesis of allergic rhinitis. J Allergy Clin Immunol 1997;99:S763-72.
  7. Lee SY, Kwon JW, Seo JH, Song YH, Kim BJ, Yu J, et al. Prevalence of atopy and allergic diseases in Korean children: associations with a farming environment and rural lifestyle. Int Arch Allergy Immunol 2012;158:168-74.
  8. Kim DS, Park MR, Yu JS, Lee HS, Lee JH, Suh J, et al. Prevalence and risk factors of asthma and allergic rhinitis in elementary school children in Jinan-Gun. Pediatr Allergy Respir Dis 2012;22:374-82.
  9. Seo JH, Kim HY, Jung YH, Kwon JW, Kim BJ, Kim HB, et al. The association between sibling and allergic rhinitis in adolescents. Allergy asthma Respir Dis 2013;1:67-72.
  10. Yang SI, Lee E, Jung YH, Kim HY, Seo JH, Kwon JW, et al. Effect of antibiotic use and mold exposure in infancy on allergic rhinitis in susceptible adolescents. Ann Allergy Asthma Immunol 2014;113:160-5.e1.
  11. Kim Y, Seo JH, Kwon JW, Yang SI, Cho HJ, Ha M, et al. The prevalence and risk factors of allergic rhinitis from a nationwide study of Korean elementary, middle, and high school students. Allergy asthma Respir Dis 2015;3:272-80.
  12. Bernsen RM, de Jongste JC, van der Wouden JC. Birth order and sibship size as independent risk factors for asthma, allergy, and eczema. Pediatr Allergy Immunol 2003;14:464-9.
  13. Westergaard T, Rostgaard K, Wohlfahrt J, Andersen PK, Aaby P, Melbye M. Sibship characteristics and risk of allergic rhinitis and asthma. Am J Epidemiol 2005;162:125-32.
  14. Azad MB, Coneys JG, Kozyrskyj AL, Field CJ, Ramsey CD, Becker AB, et al. Probiotic supplementation during pregnancy or infancy for the prevention of asthma and wheeze: systematic review and meta-analysis. BMJ 2013;347:f6471.
  15. Lee SL, Wong W, Lau YL. Increasing prevalence of allergic rhinitis but not asthma among children in Hong Kong from 1995 to 2001 (Phase 3 International Study of Asthma and Allergies in Childhood). Pediatr Allergy Immunol 2004;15:72-8.
  16. Lodrup Carlsen KC, Roll S, Carlsen KH, Mowinckel P, Wijga AH, Brunekreef B, et al. Does pet ownership in infancy lead to asthma or allergy at school age? Pooled analysis of individual participant data from 11 European birth cohorts. PLoS One 2012;7:e43214.
  17. Loo EXL, Liew TM, Yap GC, Wong LSY, Shek LP, Goh A, et al. Trajectories of early-onset rhinitis in the Singapore GUSTO mother-offspring cohort. Clin Exp Allergy 2021;51:419-29.
  18. Kalliomaki M, Salminen S, Arvilommi H, Kero P, Koskinen P, Isolauri E. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet 2001;357:1076-9.
  19. Isolauri E, Arvola T, Sutas Y, Moilanen E, Salminen S. Probiotics in the management of atopic eczema. Clin Exp Allergy 2000;30:1604-10.
  20. Rosenfeldt V, Benfeldt E, Nielsen SD, Michaelsen KF, Jeppesen DL, Valerius NH, et al. Effect of probiotic Lactobacillus strains in children with atopic dermatitis. J Allergy Clin Immunol 2003;111:389-95.
  21. Lee J, Seto D, Bielory L. Meta-analysis of clinical trials of probiotics for prevention and treatment of pediatric atopic dermatitis. J Allergy Clin Immunol 2008;121:116-21.e11.
  22. Kim JY, Kwon JH, Ahn SH, Lee SI, Han YS, Choi YO, et al. Effect of probiotic mix (Bifidobacterium bifidum, Bifidobacterium lactis, Lactobacillus acidophilus) in the primary prevention of eczema: a double-blind, randomized, placebo-controlled trial. Pediatr Allergy Immunol 2010;21(2 Pt 2):e386-93.
  23. Lee SY, Lee JY, Jang SO, Kang MJ, Song YH, Kim BJ, et al. The immuologic effects of Lactobacillus rhamnosus (Lcr35) supplements in adult patients with atopic dermatitis. Korean J Asthma Allergy Clin Immunol 2008;28:128-33.
  24. Kong DY, Yang HJ, Pyun BY. The effects on treatment of atopic dermatitis with oral Lactobacillus casei supplements in Korean children. Pediatr Allergy Respir Dis 2007;17:27-37.
  25. Ahn SH, Lee HY, Song YE, Park SY, Lim DH, Kim JH, et al. The social and environmental risk factors of allergic rhinitis in children. Pediatr Allergy Respir Dis 2012;22:100-9.
  26. Ivory K, Chambers SJ, Pin C, Prieto E, Arques JL, Nicoletti C. Oral delivery of Lactobacillus casei Shirota modifies allergen-induced immune responses in allergic rhinitis. Clin Exp Allergy 2008;38:1282-9.
  27. Ivory K, Wilson AM, Sankaran P, Westwood M, McCarville J, Brockwell C, et al. Oral delivery of a probiotic induced changes at the nasal mucosa of seasonal allergic rhinitis subjects after local allergen challenge: a randomised clinical trial. PLoS One 2013;8:e78650.
  28. Du X, Wang L, Wu S, Yuan L, Tang S, Xiang Y, et al. Efficacy of probiotic supplementary therapy for asthma, allergic rhinitis, and wheeze: a meta-analysis of randomized controlled trials. Allergy Asthma Proc 2019;40:250-60.
  29. Wickens K, Barthow C, Mitchell EA, Kang J, van Zyl N, Purdie G, et al. Effects of Lactobacillus rhamnosus HN001 in early life on the cumulative prevalence of allergic disease to 11 years. Pediatr Allergy Immunol 2018;29:808-14.
  30. Peldan P, Kukkonen AK, Savilahti E, Kuitunen M. Perinatal probiotics decreased eczema up to 10 years of age, but at 5-10 years, allergic rhinoconjunctivitis was increased. Clin Exp Allergy 2017;47:975-9.
  31. Helin T, Haahtela S, Haahtela T. No effect of oral treatment with an intestinal bacterial strain, Lactobacillus rhamnosus (ATCC 53103), on birchpollen allergy: a placebo-controlled double-blind study. Allergy 2002;57:243-6.
  32. Koyama T, Kirjavainen PV, Fisher C, Anukam K, Summers K, Hekmat S, et al. Development and pilot evaluation of a novel probiotic mixture for the management of seasonal allergic rhinitis. Can J Microbiol 2010;56:730-8.
  33. Ouwehand AC, Nermes M, Collado MC, Rautonen N, Salminen S, Isolauri E. Specific probiotics alleviate allergic rhinitis during the birch pollen season. World J Gastroenterol 2009;15:3261-8.
  34. Wassenberg J, Nutten S, Audran R, Barbier N, Aubert V, Moulin J, et al. Effect of Lactobacillus paracasei ST11 on a nasal provocation test with grass pollen in allergic rhinitis. Clin Exp Allergy 2011;41:565-73.
  35. Kim DH, Han K, Kim SW. Effects of antibiotics on the development of asthma and other allergic diseases in children and adolescents. Allergy Asthma Immunol Res 2018;10:457-65.
  36. Seo JH, Kim HY, Jung YH, Lee E, Yang SI, Yu HS, et al. Interactions between innate immunity genes and early-life risk factors in allergic rhinitis. Allergy Asthma Immunol Res 2015;7:241-8.
  37. Bremner SA, Carey IM, DeWilde S, Richards N, Maier WC, Hilton SR, et al. Early-life exposure to antibacterials and the subsequent development of hayfever in childhood in the UK: case-control studies using the General Practice Research Database and the Doctors' Independent Network. Clin Exp Allergy 2003;33:1518-25.
  38. Alm B, Goksor E, Pettersson R, Mollborg P, Erdes L, Loid P, et al. Antibiotics in the first week of life is a risk factor for allergic rhinitis at school age. Pediatr Allergy Immunol 2014;25:468-72.
  39. Alm B, Goksor E, Thengilsdottir H, Pettersson R, Mollborg P, Norvenius G, et al. Early protective and risk factors for allergic rhinitis at age 4(1/2) yr. Pediatr Allergy Immunol 2011;22:398-404.
  40. Thelin A, Hoglund S. Change of occupation and retirement among Swedish farmers and farm workers in relation to those in other occupations. A study of "elimination" from farming during the period 1970-1988. Soc Sci Med 1994;38:147-51.
  41. Ege MJ, Mayer M, Normand AC, Genuneit J, Cookson WO, Braun-Fahrlander C, et al. Exposure to environmental microorganisms and childhood asthma. N Engl J Med 2011;364:701-9.
  42. Lee YJ, Jee HM, Kim BJ, Kim HB, Yu J, Lee SY, et al. Prevalence of allergic diseases in children according to mode of delivery. Pediatr Allergy Respir Dis 2011;21:197-206.
  43. Gungor D, Nadaud P, LaPergola CC, Dreibelbis C, Wong YP, Terry N, et al. Infant milk-feeding practices and food allergies, allergic rhinitis, atopic dermatitis, and asthma throughout the life span: a systematic review. Am J Clin Nutr 2019;109(Suppl_7):772S-799S.
  44. Codispoti CD, Levin L, LeMasters GK, Ryan P, Reponen T, Villareal M, et al. Breast-feeding, aeroallergen sensitization, and environmental exposures during infancy are determinants of childhood allergic rhinitis. J Allergy Clin Immunol 2010;125:1054-60.e1.
  45. Rautava S, Luoto R, Salminen S, Isolauri E. Microbial contact during pregnancy, intestinal colonization and human disease. Nat Rev Gastroenterol Hepatol 2012;9:565-76.
  46. Kim J, Kim K. Association of antimicrobial household exposure with development of allergic rhinitis in Korea. Pediatr Allergy Immunol 2019;30:569-71.
  47. Matheson MC, Walters EH, Simpson JA, Wharton CL, Ponsonby AL, Johns DP, et al. Relevance of the hygiene hypothesis to early vs. late onset allergic rhinitis. Clin Exp Allergy 2009;39:370-8.
  48. Matricardi PM, Rosmini F, Ferrigno L, Nisini R, Rapicetta M, Chionne P, et al. Cross sectional retrospective study of prevalence of atopy among Italian military students with antibodies against hepatitis A virus. BMJ 1997;314:999-1003.
  49. Manuel AM, Kuljit S, Gopalakrishnan G, Suresh KG, Balraj P. The role of worm infestation in allergic rhinitis. Trop Biomed 2012;29:360-5.
  50. Matricardi PM, Rosmini F, Riondino S, Fortini M, Ferrigno L, Rapicetta M, et al. Exposure to foodborne and orofecal microbes versus airborne viruses in relation to atopy and allergic asthma: epidemiological study. BMJ 2000;320:412-7.
  51. Akiner U, Yener HM, Gozen ED, Kuzu SB, Canakcioglu S. Helicobacter pylori in allergic and non-allergic rhinitis does play a protective or causative role? Eur Arch Otorhinolaryngol 2020;277:141-5.
  52. 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;102:414-20.
  53. Flohr C, Quinnell RJ, Britton J. Do helminth parasites protect against atopy and allergic disease? Clin Exp Allergy 2009;39:20-32.
  54. Lin CT, Gopala K, Manuel AM. The impact of pulmonary tuberculosis treatment on the prevalence of allergic rhinitis. Ear Nose Throat J 2013;92:358-99.
  55. Dayal AK, Sinha V. Trend of allergic rhinitis post COVID-19 pandemic: a retrospective observational study. Indian J Otolaryngol Head Neck Surg 2022;74:50-2.