Infant Gut Microbiota and the Hygiene Hypothesis of Allergic Disease: Impact of Household Pets and Siblings on Microbiota Composition and Diversity

Overview

Journal Allergy Asthma Clin Immunol

Specialty Allergy & Immunology

Date 2013 Apr 24

PMID 23607879

Citations 120

Authors

Meghan B Azad

Theodore Konya

Heather Maughan

David S Guttman

Catherine J Field

Malcolm R Sears

Allan B Becker

James A Scott

Anita L Kozyrskyj

Affiliations

Soon will be listed here.

Abstract

Background: Multiple studies have demonstrated that early-life exposure to pets or siblings affords protection against allergic disease; these associations are commonly attributed to the "hygiene hypothesis". Recently, low diversity of the infant gut microbiota has also been linked to allergic disease. In this study, we characterize the infant gut microbiota in relation to pets and siblings.

Methods: The study population comprised a small sub-sample of 24 healthy, full term infants from the Canadian Healthy Infant Longitudinal Development (CHILD) birth cohort. Mothers reported on household pets and siblings. Fecal samples were collected at 4 months of age, and microbiota composition was characterized by high-throughput signature gene sequencing.

Results: Microbiota richness and diversity tended to be increased in infants living with pets, whereas these measures were decreased in infants with older siblings. Infants living with pets exhibited under-representation of Bifidobacteriaceae and over-representation of Peptostreptococcaceae; infants with older siblings exhibited under-representation of Peptostreptococcaceae.

Conclusions: This study provides new evidence that exposure to pets and siblings may influence the early development of the gut microbiota, with potential implications for allergic disease. These two traditionally protective "hygiene hypothesis" factors appear to differentially impact gut microbiota composition and diversity, calling into question the clinical significance of these measures. Further research is required to confirm and expand these findings.

Citing Articles

The Etiology of IgE-Mediated Food Allergy: Potential Therapeutics and Challenges.

Carnazza M, Werner R, Tiwari R, Geliebter J, Li X, Yang N Int J Mol Sci. 2025; 26(4).

PMID: 40004029 PMC: 11855496. DOI: 10.3390/ijms26041563.

Rurality and relative poverty drive acquisition of a stable and diverse gut microbiome in early childhood in a non-industrialized setting.

Seco-Hidalgo V, Witney A, Chico M, Vaca M, Arevalo A, Schuyler A Sci Rep. 2025; 15(1):5601.

PMID: 39955323 PMC: 11830098. DOI: 10.1038/s41598-025-89224-5.

Early age of dog exposure is negatively associated with atopic dermatitis: A comprehensive analysis.

Gu X, Wang X, Li B, Wang Y, Zhu W, Su J Pediatr Res. 2025; .

PMID: 39837990 DOI: 10.1038/s41390-025-03864-x.

Comparative Analysis of Gut Microbiota in Humans Living with and Without Companion Animals.

Do K, Park J, Kim N, Ryu D, Kim M, Ahn H Life (Basel). 2025; 14(12.

PMID: 39768329 PMC: 11678384. DOI: 10.3390/life14121621.

Rurality and relative poverty drive acquisition of a stable and diverse gut microbiome in early childhood in a non-industrialized setting.

Seco-Hidalgo V, Witney A, Chico M, Vaca M, Arevalo A, Schuyler A Res Sq. 2024; .

PMID: 39678332 PMC: 11643292. DOI: 10.21203/rs.3.rs-5361957/v1.

References

Thum C, Cookson A, Otter D, McNabb W, Hodgkinson A, Dyer J . Can nutritional modulation of maternal intestinal microbiota influence the development of the infant gastrointestinal tract?. J Nutr. 2012; 142(11):1921-8. DOI: 10.3945/jn.112.166231. View

Kalliomaki M, Kirjavainen P, Eerola E, Kero P, Salminen S, Isolauri E . Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J Allergy Clin Immunol. 2001; 107(1):129-34. DOI: 10.1067/mai.2001.111237. View

Adlerberth I, Strachan D, Matricardi P, Ahrne S, Orfei L, Aberg N . Gut microbiota and development of atopic eczema in 3 European birth cohorts. J Allergy Clin Immunol. 2007; 120(2):343-50. DOI: 10.1016/j.jaci.2007.05.018. View

Damborg P, Nielsen S, Guardabassi L . Escherichia coli shedding patterns in humans and dogs: insights into within-household transmission of phylotypes associated with urinary tract infections. Epidemiol Infect. 2009; 137(10):1457-64. DOI: 10.1017/S095026880900226X. View

Flores G, Bates S, Knights D, Lauber C, Stombaugh J, Knight R . Microbial biogeography of public restroom surfaces. PLoS One. 2011; 6(11):e28132. PMC: 3223236. DOI: 10.1371/journal.pone.0028132. View

Bezirtzoglou E, Tsiotsias A, Welling G . Microbiota profile in feces of breast- and formula-fed newborns by using fluorescence in situ hybridization (FISH). Anaerobe. 2011; 17(6):478-82. DOI: 10.1016/j.anaerobe.2011.03.009. View

Strachan D . Hay fever, hygiene, and household size. BMJ. 1989; 299(6710):1259-60. PMC: 1838109. DOI: 10.1136/bmj.299.6710.1259. View

Wold A . The hygiene hypothesis revised: is the rising frequency of allergy due to changes in the intestinal flora?. Allergy. 1998; 53(46 Suppl):20-5. DOI: 10.1111/j.1398-9995.1998.tb04953.x. View

Bjorksten B, Sepp E, Julge K, Voor T, Mikelsaar M . Allergy development and the intestinal microflora during the first year of life. J Allergy Clin Immunol. 2001; 108(4):516-20. DOI: 10.1067/mai.2001.118130. View

10.

Ball T, Castro-Rodriguez J, Griffith K, Holberg C, Martinez F, Wright A . Siblings, day-care attendance, and the risk of asthma and wheezing during childhood. N Engl J Med. 2000; 343(8):538-43. DOI: 10.1056/NEJM200008243430803. View

11.

Azad M, Konya T, Maughan H, Guttman D, Field C, Chari R . Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ. 2013; 185(5):385-94. PMC: 3602254. DOI: 10.1503/cmaj.121189. View

12.

Lindberg E, Adlerberth I, Matricardi P, Bonanno C, Tripodi S, Panetta V . Effect of lifestyle factors on Staphylococcus aureus gut colonization in Swedish and Italian infants. Clin Microbiol Infect. 2010; 17(8):1209-15. DOI: 10.1111/j.1469-0691.2010.03426.x. View

13.

Hong P, Lee B, Aw M, Shek L, Yap G, Chua K . Comparative analysis of fecal microbiota in infants with and without eczema. PLoS One. 2010; 5(4):e9964. PMC: 2848600. DOI: 10.1371/journal.pone.0009964. View

14.

Johnson J, Clabots C, Kuskowski M . Multiple-host sharing, long-term persistence, and virulence of Escherichia coli clones from human and animal household members. J Clin Microbiol. 2008; 46(12):4078-82. PMC: 2593269. DOI: 10.1128/JCM.00980-08. View

15.

Roger L, Costabile A, Holland D, Hoyles L, McCartney A . Examination of faecal Bifidobacterium populations in breast- and formula-fed infants during the first 18 months of life. Microbiology (Reading). 2010; 156(Pt 11):3329-3341. DOI: 10.1099/mic.0.043224-0. View

16.

Bowers R, Sullivan A, Costello E, Collett Jr J, Knight R, Fierer N . Sources of bacteria in outdoor air across cities in the midwestern United States. Appl Environ Microbiol. 2011; 77(18):6350-6. PMC: 3187178. DOI: 10.1128/AEM.05498-11. View

17.

Ownby D, Johnson C, Peterson E . Exposure to dogs and cats in the first year of life and risk of allergic sensitization at 6 to 7 years of age. JAMA. 2002; 288(8):963-72. DOI: 10.1001/jama.288.8.963. View

18.

Minamoto Y, Hooda S, Swanson K, Suchodolski J . Feline gastrointestinal microbiota. Anim Health Res Rev. 2012; 13(1):64-77. DOI: 10.1017/S1466252312000060. View

19.

Abrahamsson T, Jakobsson H, Andersson A, Bjorksten B, Engstrand L, Jenmalm M . Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol. 2011; 129(2):434-40, 440.e1-2. DOI: 10.1016/j.jaci.2011.10.025. View

20.

Azad M, Kozyrskyj A . Perinatal programming of asthma: the role of gut microbiota. Clin Dev Immunol. 2011; 2012:932072. PMC: 3216351. DOI: 10.1155/2012/932072. View