Allergy, Asthma & Clinical Immunology | |
Infant gut microbiota and the hygiene hypothesis of allergic disease: impact of household pets and siblings on microbiota composition and diversity | |
Meghan B Azad5  Theodore Konya3  Heather Maughan1  David S Guttman1  Catherine J Field4  Malcolm R Sears2  Allan B Becker6  James A Scott3  Anita L Kozyrskyj6  CHILD Study Investigators6  | |
[1] Cell & Systems Biology, University of Toronto, Toronto, ON, Canada | |
[2] Department of Medicine, McMaster University, Hamilton, ON, Canada | |
[3] Dalla Lana School of Public Health, University of Toronto, Toronto, ON, Canada | |
[4] Agriculture, Food & Nutritional Sciences, University of Alberta, Edmonton, AB, Canada | |
[5] Department of Pediatrics, University of Alberta, 3-527 Edmonton Clinic Health Academy 11405 – 87th Avenue, Edmonton, AB, T6G IC9, Canada | |
[6] Manitoba Institute of Child Health, Winnipeg, Canada | |
关键词: Environmental exposures; Allergic disease; Atopy; Siblings; Pets; Microflora hypothesis; Hygiene hypothesis; Gut microbiome; Gut microbiota; Infants; | |
Others : 792322 DOI : 10.1186/1710-1492-9-15 |
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received in 2012-11-05, accepted in 2013-03-07, 发布年份 2013 | |
【 摘 要 】
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.
【 授权许可】
2013 Azad et al.; licensee BioMed Central Ltd.
【 预 览 】
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20140705030107655.pdf | 885KB | download | |
Figure 3. | 69KB | Image | download |
Figure 2. | 57KB | Image | download |
Figure 1. | 103KB | Image | download |
【 图 表 】
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【 参考文献 】
- [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.
- [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.
- [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.
- [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.
- [5]Strachan DP: Hay fever, hygiene, and household size. BMJ 1989, 299:1259-1260.
- [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.
- [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. 440
- [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.
- [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]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.
- [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.
- [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.
- [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. BioMed Central Full Text
- [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. BioMed Central Full Text
- [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.
- [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.
- [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.
- [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.
- [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.
- [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.
- [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.
- [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.
- [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.
- [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. BioMed Central Full Text
- [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.
- [26]Edgar RC: Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010, 26:2460-2461.
- [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.
- [28]Colwell RK: Biodiversity: Concepts, Patterns, and Measurement. Princeton University Press. The Princeton Guide to Ecology; 2009:257-263.
- [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.
- [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.
- [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.
- [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.
- [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.
- [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.
- [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.
- [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.
- [37]Konya T: Is house dust a reservoir for infant gut bacteria?. Dalla Lana School of Public Health, University of Toronto: Masters in Public Health; 2012.
- [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. BioMed Central Full Text
- [39]Ley RE, Peterson DA, Gordon JI: Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 2006, 124:837-848.
- [40]Minamoto Y, Hooda S, Swanson KS, Suchodolski JS: Feline gastrointestinal microbiota. Anim Health Res Rev 2012, 13:64-77.
- [41]Dewhirst FE, Klein EA, Thompson EC, Blanton JM, Chen T, Milella L: The canine oral microbiome. PLoS One 2012, 7:e36067.
- [42]Weese JS: The canine and feline skin microbiome in health and disease. Vet Dermatol 2013, 24:137-145.
- [43]Flores GE, Bates ST, Knights D, Lauber CL, Stombaugh J, Knight R: Microbial biogeography of public restroom surfaces. PLoS One 2011, 6:e28132.
- [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.
- [45]Bowers RM, Sullivan AP, Costello EK, Collett JL Jr, Knight R, Fierer N: Sources of bacteria in outdoor air across cities in the Midwestern United States. Appl Environ Microbiol 2011, 77:6350-6356.
- [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.
- [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.
- [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.
- [49]Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO: Development of the human infant intestinal microbiota. PLoS Biol 2007, 5:e177.
- [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.
- [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.
- [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.
- [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.