Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Allergy, Asthma & Clinical Immunology
Published in: Allergy, Asthma & Clinical Immunology 1/2013

Open Access 01-12-2013 | Research

Infant gut microbiota and the hygiene hypothesis of allergic disease: impact of household pets and siblings on microbiota composition and diversity

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, CHILD Study Investigators

Published in: Allergy, Asthma & Clinical Immunology | Issue 1/2013

Login to get access

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.
Appendix
Available only for authorised users
Literature
1.
Ownby DR, Johnson CC, Peterson EL: 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: 963-972. 10.1001/jama.288.8.963.CrossRefPubMed
2.
Hesselmar B, Aberg N, Aberg B, Eriksson B, Bjorksten B: Does early exposure to cat or dog protect against later allergy development?. Clin Exp Allergy. 1999, 29: 611-617. 10.1046/j.1365-2222.1999.00534.x.CrossRefPubMed
3.
Litonjua AA, Milton DK, Celedon JC, Ryan L, Weiss ST, Gold DR: A longitudinal analysis of wheezing in young children: the independent effects of early life exposure to house dust endotoxin, allergens, and pets. J Allergy Clin Immunol. 2002, 110: 736-742. 10.1067/mai.2002.128948.CrossRefPubMed
4.
Ball TM, Castro-Rodriguez JA, Griffith KA, Holberg CJ, Martinez FD, Wright AL: Siblings, day-care attendance, and the risk of asthma and wheezing during childhood. N Engl J Med. 2000, 343: 538-543. 10.1056/NEJM200008243430803.CrossRefPubMed
5.
6.
Wold AE: The hygiene hypothesis revised: is the rising frequency of allergy due to changes in the intestinal flora?. Allergy. 1998, 53: 20-25.CrossRefPubMed
7.
Abrahamsson TR, Jakobsson HE, Andersson AF, Bjorksten B, Engstrand L, Jenmalm MC: Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol. 2012, 129: 434-440. 10.1016/j.jaci.2011.10.025. 440CrossRefPubMed
8.
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: 129-134. 10.1067/mai.2001.111237.CrossRefPubMed
9.
Vebo HC, Sekelja M, Nestestog R, Storro O, Johnsen R, Oien T: Temporal development of the infant gut microbiota in IgE sensitized and non-sensitized children determined by the GA-map infant array. Clin Vaccine Immunol. 2011, 18: 1326-1335. 10.1128/CVI.00062-11.PubMedCentralCrossRefPubMed
10.
Bisgaard H, Li N, Bonnelykke K, Chawes BL, Skov T, Paludan-Muller G: Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age. J Allergy Clin Immunol. 2011, 128: 646-652. 10.1016/j.jaci.2011.04.060.CrossRefPubMed
11.
Nakayama J, Kobayashi T, Tanaka S, Korenori Y, Tateyama A, Sakamoto N: Aberrant structures of fecal bacterial community in allergic infants profiled by 16S rRNA gene pyrosequencing. FEMS Immunol Med Microbiol. 2011, 63: 397-406. 10.1111/j.1574-695X.2011.00872.x.CrossRefPubMed
12.
Penders J, Thijs C, van den Brandt PA, Kummeling I, Snijders B, Stelma F: Gut microbiota composition and development of atopic manifestations in infancy: the KOALA Birth Cohort Study. Gut. 2007, 56: 661-667. 10.1136/gut.2006.100164.PubMedCentralCrossRefPubMed
13.
Vael C, Vanheirstraeten L, Desager KN, Goossens H: Denaturing gradient gel electrophoresis of neonatal intestinal microbiota in relation to the development of asthma. BMC Microbiol. 2011, 11: 68. 10.1186/1471-2180-11-68.PubMedCentralCrossRefPubMed
14.
Mulder IE, Schmidt B, Stokes CR, Lewis M, Bailey M, Aminov RI: Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces. BMC Biol. 2009, 7: 79. 10.1186/1741-7007-7-79.PubMedCentralCrossRefPubMed
15.
Dicksved J, Floistrup H, Bergstrom A, Rosenquist M, Pershagen G, Scheynius A: Molecular fingerprinting of the fecal microbiota of children raised according to different lifestyles. Appl Environ Microbiol. 2007, 73: 2284-2289. 10.1128/AEM.02223-06.PubMedCentralCrossRefPubMed
16.
van Nimwegen FA, Penders J, Stobberingh EE, Postma DS, Koppelman GH, Kerkhof M: Mode and place of delivery, gastrointestinal microbiota, and their influence on asthma and atopy. J Allergy Clin Immunol. 2011, 128: 948-955. 10.1016/j.jaci.2011.07.027.CrossRefPubMed
17.
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: 516-520. 10.1067/mai.2001.118130.CrossRefPubMed
18.
Johansson MA, Sjogren YM, Persson JO, Nilsson C, Sverremark-Ekstrom E: Early colonization with a group of Lactobacilli decreases the risk for allergy at five years of age despite allergic heredity. PLoS One. 2011, 6: e23031. 10.1371/journal.pone.0023031.PubMedCentralCrossRefPubMed
19.
Murray CS, Tannock GW, Simon MA, Harmsen HJ, Welling GW, Custovic A: Fecal microbiota in sensitized wheezy and non-sensitized non-wheezy children: a nested case–control study. Clin Exp Allergy. 2005, 35: 741-745. 10.1111/j.1365-2222.2005.02259.x.CrossRefPubMed
20.
Lodrup Carlsen KC, Roll S, Carlsen KH, Mowinckel P, Wijga AH, Brunekreef B: 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. 10.1371/journal.pone.0043214.PubMedCentralCrossRefPubMed
21.
Koplin JJ, Dharmage SC, Ponsonby AL, Tang ML, Lowe AJ, Gurrin LC: Environmental and demographic risk factors for egg allergy in a population-based study of infants. Allergy. 2012, 67: 1415-1422. 10.1111/all.12015.CrossRefPubMed
22.
Adlerberth I, Strachan DP, Matricardi PM, Ahrne S, Orfei L, Aberg N: Gut microbiota and development of atopic eczema in 3 European birth cohorts. J Allergy Clin Immunol. 2007, 120: 343-350. 10.1016/j.jaci.2007.05.018.CrossRefPubMed
23.
Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I: Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006, 118: 511-521. 10.1542/peds.2005-2824.CrossRefPubMed
24.
Ariefdjohan MW, Savaiano DA, Nakatsu CH: Comparison of DNA extraction kits for PCR-DGGE analysis of human intestinal microbial communities from fecal specimens. Nutr J. 2010, 9: 23. 10.1186/1475-2891-9-23.PubMedCentralCrossRefPubMed
25.
Maughan H, Wang PW, Diaz CJ, Fung P, Gong Y, Donaldson SL: Analysis of the cystic fibrosis lung microbiota via serial illumina sequencing of bacterial 16S rRNA hypervariable regions. PLoS One. 2012, 7: e45791. 10.1371/journal.pone.0045791.PubMedCentralCrossRefPubMed
26.
Edgar RC: Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010, 26: 2460-2461. 10.1093/bioinformatics/btq461.CrossRefPubMed
27.
Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J: SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007, 35: 7188-7196. 10.1093/nar/gkm864.PubMedCentralCrossRefPubMed
28.
Colwell RK: Biodiversity: Concepts, Patterns, and Measurement. 2009, Princeton University Press. The Princeton Guide to Ecology, 257-263.
29.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK: QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010, 7: 335-336. 10.1038/nmeth.f.303.PubMedCentralCrossRefPubMed
30.
Damborg P, Nielsen SS, 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: 1457-1464. 10.1017/S095026880900226X.CrossRefPubMed
31.
Johnson JR, Clabots C, Kuskowski MA: Multiple-host sharing, long-term persistence, and virulence of Escherichia coli clones from human and animal household members. J Clin Microbiol. 2008, 46: 4078-4082. 10.1128/JCM.00980-08.PubMedCentralCrossRefPubMed
32.
Stokholm J, Schjorring S, Pedersen L, Bischoff AL, Folsgaard N, Carson CG: Living with cat and dog increases vaginal colonization with E. Coli in pregnant women. PLoS One. 2012, 7: e46226. 10.1371/journal.pone.0046226.PubMedCentralCrossRefPubMed
33.
Ahrne S, Lonnermark E, Wold AE, Aberg N, Hesselmar B, Saalman R: Lactobacilli in the intestinal microbiota of Swedish infants. Microbes Infect. 2005, 7: 1256-1262. 10.1016/j.micinf.2005.04.011.CrossRefPubMed
34.
Nowrouzian F, Hesselmar B, Saalman R, Strannegard IL, Aberg N, Wold AE: Escherichia coli in infants' intestinal microflora: colonization rate, strain turnover, and virulence gene carriage. Pediatr Res. 2003, 54: 8-14. 10.1203/01.PDR.0000069843.20655.EE.CrossRefPubMed
35.
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. 2011, 17: 1209-1215. 10.1111/j.1469-0691.2010.03426.x.CrossRefPubMed
36.
Thum C, Cookson AL, Otter DE, McNabb WC, Hodgkinson AJ, Dyer J: Can nutritional modulation of maternal intestinal microbiota influence the development of the infant gastrointestinal tract?. J Nutr. 2012, 142: 1921-1928. 10.3945/jn.112.166231.CrossRefPubMed
37.
Konya T: Is house dust a reservoir for infant gut bacteria?. 2012, Dalla Lana School of Public Health, University of Toronto: Masters in Public Health
38.
Nylund L, Satokari R, Nikkila J, Rajili-Stojanovi M, Kalliomaki M, Isolauri E: Microarray analysis reveals marked intestinal microbiota aberrancy in infants having eczema compared to healthy children in at-risk for atopic disease. BMC Microbiol. 2013, 13: 12. 10.1186/1471-2180-13-12.PubMedCentralCrossRefPubMed
39.
Ley RE, Peterson DA, Gordon JI: Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006, 124: 837-848. 10.1016/j.cell.2006.02.017.CrossRefPubMed
40.
Minamoto Y, Hooda S, Swanson KS, Suchodolski JS: Feline gastrointestinal microbiota. Anim Health Res Rev. 2012, 13: 64-77. 10.1017/S1466252312000060.CrossRefPubMed
41.
Dewhirst FE, Klein EA, Thompson EC, Blanton JM, Chen T, Milella L: The canine oral microbiome. PLoS One. 2012, 7: e36067. 10.1371/journal.pone.0036067.PubMedCentralCrossRefPubMed
42.
Weese JS: The canine and feline skin microbiome in health and disease. Vet Dermatol. 2013, 24: 137-145. 10.1111/j.1365-3164.2012.01076.x.CrossRefPubMed
43.
Flores GE, Bates ST, Knights D, Lauber CL, Stombaugh J, Knight R: Microbial biogeography of public restroom surfaces. PLoS One. 2011, 6: e28132. 10.1371/journal.pone.0028132.PubMedCentralCrossRefPubMed
44.
Knights D, Kuczynski J, Charlson ES, Zaneveld J, Mozer MC, Collman RG: Bayesian community-wide culture-independent microbial source tracking. Nat Methods. 2011, 8: 761-763. 10.1038/nmeth.1650.PubMedCentralCrossRefPubMed
45.
Bowers RM, Sullivan AP, Costello EK, Collett JL, Knight R, Fierer N: Sources of bacteria in outdoor air across cities in the Midwestern United States. Appl Environ Microbiol. 2011, 77: 6350-6356. 10.1128/AEM.05498-11.PubMedCentralCrossRefPubMed
46.
Bezirtzoglou E, Tsiotsias A, Welling GW: Microbiota profile in feces of breast- and formula-fed newborns by using Fluorescence In situ Hybridization (FISH). Anaerobe. 2011, 17: 478-482. 10.1016/j.anaerobe.2011.03.009.CrossRefPubMed
47.
Harmsen HJ, Wildeboer-Veloo AC, Raangs GC, Wagendorp AA, Klijn N, Bindels JG: Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J Pediatr Gastroenterol Nutr. 2000, 30: 61-67. 10.1097/00005176-200001000-00019.CrossRefPubMed
48.
Hong PY, Lee BW, Aw M, Shek LP, Yap GC, Chua KY: Comparative analysis of fecal microbiota in infants with and without eczema. PLoS One. 2010, 5: e9964. 10.1371/journal.pone.0009964.PubMedCentralCrossRefPubMed
49.
Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO: Development of the human infant intestinal microbiota. PLoS Biol. 2007, 5: e177. 10.1371/journal.pbio.0050177.PubMedCentralCrossRefPubMed
50.
Roger LC, Costabile A, Holland DT, Hoyles L, McCartney AL: Examination of faecal Bifidobacterium populations in breast- and formula-fed infants during the first 18 months of life. Microbiology. 2010, 156: 3329-3341. 10.1099/mic.0.043224-0.CrossRefPubMed
51.
Stark PL, Lee A: The microbial ecology of the large bowel of breast-fed and formula-fed infants during the first year of life. J Med Microbiol. 1982, 15: 189-203. 10.1099/00222615-15-2-189.CrossRefPubMed
52.
Turroni F, Peano C, Pass DA, Foroni E, Severgnini M, Claesson MJ: Diversity of Bifidobacteria within the Infant Gut Microbiota. PLoS One. 2012, 7: e36957. 10.1371/journal.pone.0036957.PubMedCentralCrossRefPubMed
53.
Azad MB, Kozyrskyj AL: Perinatal programming of asthma: the role of gut microbiota. Clin Dev Immunol. 2012, 201 (2): 932072.
54.
Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Chari RS: Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ. 2013, 185 (5): 385-394. 10.1503/cmaj.121189.PubMedCentralCrossRefPubMed
Metadata
Title
Infant gut microbiota and the hygiene hypothesis of allergic disease: impact of household pets and siblings on microbiota composition and diversity
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
CHILD Study Investigators
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Allergy, Asthma & Clinical Immunology / Issue 1/2013
Electronic ISSN: 1710-1492
DOI
https://doi.org/10.1186/1710-1492-9-15

Other articles of this Issue 1/2013

Allergy, Asthma & Clinical Immunology 1/2013 Go to the issue

Short report

Evaluation of nasal symptoms induced by platelet activating factor, after nasal challenge in both healthy and allergic rhinitis subjects pretreated with rupatadine, levocetirizine or placebo in a cross-over study design

Review

Drug provocation tests: up-date and novel approaches

Research

Reduction in oral corticosteroid use in patients receiving omalizumab for allergic asthma in the real-world setting

Research

IL-17-producing peripheral blood CD177+ neutrophils increase in allergic asthmatic subjects

Research

Exploring the impact of elevated depressive symptoms on the ability of a tailored asthma intervention to improve medication adherence among urban adolescents with asthma

Research

Role of T cells in a gp91phox knockout murine model of acute allergic asthma