Altered fecal microbiota composition associated with food allergy in infants

Applied and Environmental Microbiology

Volumn 80, Issue 8, 2014, Pages 2546-2554

  Ling, Zongxin ^a,b   Li, Zailing ^c   Liu, Xia ^a,b   Cheng, Yiwen ^a,b   Luo, Yueqiu ^a,b   Tong, Xiaojuan ^a,b   Yuan, Li ^a,b   Wang, Yuezhu ^d   Sun, Jinbo ^c   Li, Lanjuan ^a,b   Xiang, Charlie ^a,b,e  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c PEKING UNIVERSITY THIRD HOSPITAL   (China)

^d CHINESE NATIONAL HUMAN GENOME CENTER AT SHANGHAI   (China)

^e J CRAIG VENTER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGIES; RNA;

454-PYROSEQUENCING; FECAL MICROBIOTA; FOOD ALLERGIES; HEALTHY CONTROLS; INTERLEUKIN-10; MICROBIAL DIVERSITY; POSITIVE CORRELATIONS; PROTEOBACTERIA;

CLOSTRIDIUM;

ABUNDANCE; ALLERGY; CHILD HEALTH; COMMUNITY COMPOSITION; DOMINANCE; FOOD QUALITY; GENE EXPRESSION; HEALTH RISK; MICROBIAL COMMUNITY; PATHOGENICITY; RNA;

BIOTA; COMPLICATION; DYSBIOSIS; FECES; FOOD ALLERGY; HUMAN; INFANT; MICROBIOLOGY;

BIOTA; DYSBIOSIS; FECES; FOOD HYPERSENSITIVITY; HUMANS; INFANT;

EID: 84896965906     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00003-14     Document Type: Article

References (48)

1. Sackeyfio A, Senthinathan A, Kandaswamy P, Barry PW, Shaw B, Baker M. 2011. Diagnosis and assessment of food allergy in children and young people: summary of NICE guidance. BMJ 342:d747. http://dx.doi.org/10.1136/bmj.d747.
2. Sicherer SH, Sampson HA. 2010. Food allergy. J. Allergy Clin. Immunol. 125:S116-S125. http://dx.doi.org/10.1016/j.jaci.2009.08.028.
3. Noti M, Wojno ED, Kim BS, Siracusa MC, Giacomin PR, Nair MG, Benitez AJ, Ruymann KR, Muir AB, Hill DA, Chikwava KR, Moghaddam AE, Sattentau QJ, Alex A, Zhou C, Yearley JH, Menard-Katcher P, Kubo M, Obata-Ninomiya K, Karasuyama H, Comeau MR, Brown-Whitehorn T, de Waal Malefyt R, Sleiman PM, Hakonarson H, Cianferoni A, Falk GW, Wang ML, Spergel JM, Artis D. 2013. Thymic stromal lymphopoietin-elicited basophil responses promote eosinophilic esophagitis. Nat. Med. 19:1005-1013. http://dx.doi.org/10.1038/nm.3281.
4. Wang M, Karlsson C, Olsson C, Adlerberth I, Wold AE, Strachan DP, Martricardi PM, Aberg N, Perkin MR, Tripodi S, Coates AR, Hesselmar B, Saalman R, Molin G, Ahrne S. 2008. Reduced diversity in the early fecal microbiota of infants with atopic eczema. J. Allergy Clin. Immunol. 121:129-134. http://dx.doi.org/10.1016/j.jaci.2007.09.011.
5. Noval Rivas M, Burton OT, Wise P, Zhang YQ, Hobson SA, Garcia Lloret M, Chehoud C, Kuczynski J, DeSantis T, Warrington J, Hyde ER, Petrosino JF, Gerber GK, Bry L, Oettgen HC, Mazmanian SK, Chatila TA. 2013. A microbiota signature associated with experimental food allergy promotes allergic sensitization and anaphylaxis. J. Allergy Clin. Immunol. 131:201-212. http://dx.doi.org/10.1016/j.jaci.2012.10.026.
6. Bisgaard H, Li N, Bonnelykke K, Chawes BL, Skov T, Paludan-Muller G, Stokholm J, Smith B, Krogfelt KA. 2011. Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age. J. Allergy Clin. Immunol. 128:646-652. http://dx.doi.org/10.1016/j.jaci.2011.04.060.
7. Russell SL, Gold MJ, Hartmann M, Willing BP, Thorson L, Wlodarska M, Gill N, Blanchet MR, Mohn WW, McNagny KM, Finlay BB. 2012. Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep. 13:440-447. http://dx.doi.org/10.1038/embor.2012.32.
8. Bjorksten B, Sepp E, Julge K, Voor T, Mikelsaar M. 2001. Allergy development and the intestinal microflora during the first year of life. J. Allergy Clin. Immunol. 108:516-520. http://dx.doi.org/10.1067/mai.2001.118130.
9. Penders J, Thijs C, van den Brandt PA, Kummeling I, Snijders B, Stelma F, Adams H, van Ree R, Stobberingh EE. 2007. Gut microbiota composition and development of atopic manifestations in infancy: the KOALA birth cohort study. Gut 56:661-667. http://dx.doi.org/10.1136/gut.2006.100164.
10. Thompson-Chagoyan OC, Vieites JM, Maldonado J, Edwards C, Gil A. 2010. Changes in faecal microbiota of infants with cow's milk protein allergy-a Spanish prospective case-control 6-month follow-up study. Pediatr. Allergy Immunol. 21:e394-e400. http://dx.doi.org/10.1111/j.1399-3038.2009.00961.x.
11. Penders J, Gerhold K, Stobberingh EE, Thijs C, Zimmermann K, Lau S, Hamelmann E. 2013. Establishment of the intestinal microbiota and its role for atopic dermatitis in early childhood. J. Allergy Clin. Immunol. 132:601-607. http://dx.doi.org/10.1016/j.jaci.2013.05.043.
12. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. 2005. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122:107-118. http://dx.doi.org/10.1016/j.cell.2005.05.007.
13. Rolinck-Werninghaus C, Staden U, Mehl A, Hamelmann E, Beyer K, Niggemann B. 2005. Specific oral tolerance induction with food in children: transient or persistent effect on food allergy? Allergy 60:1320-1322. http://dx.doi.org/10.1111/j.1398-9995.2005.00882.x.
14. Hooper LV, Littman DR, Macpherson AJ. 2012. Interactions between the microbiota and the immune system. Science 336:1268-1273. http://dx.doi.org/10.1126/science.1223490.
15. Walsh J, O'Flynn N. 2011. Diagnosis and assessment of food allergy in children and young people in primary care and community settings: NICE clinical guideline. Br. J. Gen. Pract. 61:473-475. http://dx.doi.org/10.3399/bjgp11X583498.
16. Chen W, Liu F, Ling Z, Tong X, Xiang C. 2012. Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. PLoS One 7:e39743. http://dx.doi.org/10.1371/journal.pone.0039743.
17. Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ. 2011. Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12:38. http://dx.doi.org/10.1186/1471-2105-12-38.
18. Quince C, Lanzen A, Curtis TP, Davenport RJ, Hall N, Head IM, Read LF, Sloan WT. 2009. Accurate determination of microbial diversity from 454 pyrosequencing data. Nat. Methods 6:639-641. http://dx.doi.org/10.1038/nmeth.1361.
19. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335-336. http://dx.doi.org/10.1038/nmeth.f.303.
20. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methe B, DeSantis TZ, Petrosino JF, Knight R, Birren BW. 2011. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 21: 494-504. http://dx.doi.org/10.1101/gr.112730.110.
21. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541. http://dx.doi.org/10.1128/AEM.01541-09.
22. Charland MB. 1995. Sigma Plot for scientists. McGraw-Hill Professional, Brown Communications, Inc., Dubuque, IA.
23. Wang Q, Garrity GM, Tiedje JM, Cole JR. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73:5261-5267. http://dx.doi.org/10.1128/AEM.00062-07.
24. White JR, Nagarajan N, Pop M. 2009. Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput. Biol. 5:e1000352. http://dx.doi.org/10.1371/journal.pcbi.1000352.
25. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. 2011. Metagenomic biomarker discovery and explanation. Genome Biol. 12:R60. http://dx.doi.org/10.1186/gb-2011-12-6-r60.
26. Ling Z, Liu X, Luo Y, Yuan L, Nelson KE, Wang Y, Xiang C, Li L. 2013. Pyrosequencing analysis of the human microbiota of healthy Chinese undergraduates. BMC Genomics 14:390. http://dx.doi.org/10.1186/1471-2164-14-390.
27. Kim HB, Borewicz K, White BA, Singer RS, Sreevatsan S, Tu ZJ, Isaacson RE. 2012. Microbial shifts in the swine distal gut in response to the treatment with antimicrobialgrowthpromoter, tylosin. Proc. Natl. Acad. Sci.U.S. A. 109:15485-15490. http://dx.doi.org/10.1073/pnas.1205147109.
28. Veiga P, Gallini CA, Beal C, Michaud M, Delaney ML, DuBois A, Khlebnikov A, van Hylckama Vlieg JE, Punit S, Glickman JN, Onderdonk A, Glimcher LH, Garrett WS. 2010. Bifidobacterium animalis subsp. lactis fermented milk product reduces inflammation by altering a niche for colitogenic microbes. Proc. Natl. Acad. Sci. U. S. A. 107:18132-18137. http://dx.doi.org/10.1073/pnas.1011737107.
29. Gore C, Munro K, Lay C, Bibiloni R, Morris J, Woodcock A, Custovic A, Tannock GW. 2008. Bifidobacterium pseudocatenulatum is associated with atopic eczema: a nested case-control study investigating the fecal microbiota of infants. J. Allergy Clin. Immunol. 121:135-140. http://dx.doi.org/10.1016/j.jaci.2007.07.061.
30. Abrahamsson TR, Jakobsson HE, Andersson AF, Bjorksten B, Engstrand L, Jenmalm MC. 2012. Low diversity of the gut microbiota in infants with atopic eczema. J. Allergy Clin. Immunol. 129:434-440. http://dx.doi.org/10.1016/j.jaci.2011.10.025.
31. Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR, Arrieta JM, Herndl GJ. 2006. Microbial diversity in the deep sea and the underexplored "rare biosphere." Proc. Natl. Acad. Sci. U. S. A. 103:12115-12120. http://dx.doi.org/10.1073/pnas.0605127103.
32. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R. 2010. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl. Acad. Sci. U. S. A. 107:11971-11975. http://dx.doi.org/10.1073/pnas.1002601107.
33. van Nimwegen FA, Penders J, Stobberingh EE, Postma DS, Koppelman GH, Kerkhof M, Reijmerink NE, Dompeling E, van den Brandt PA, Ferreira I, Mommers M, Thijs C. 2011. Mode and place of delivery, gastrointestinal microbiota, and their influence on asthma and atopy. J. Allergy Clin. Immunol. 128: 948-971. http://dx.doi.org/10.1016/j.jaci.2011.07.027.
34. Hanski I, von Hertzen L, Fyhrquist N, Koskinen K, Torppa K, Laatikainen T, Karisola P, Auvinen P, Paulin L, Makela MJ, Vartiainen E, Kosunen TU, Alenius H, Haahtela T. 2012. Environmental biodiversity, human microbiota, and allergy are interrelated. Proc. Natl. Acad. Sci. U. S. A. 109:8334-8339. http://dx.doi.org/10.1073/pnas.1205624109.
35. Jakobsson HE, Abrahamsson TR, Jenmalm MC, Harris K, Quince C, Jernberg C, Bjorksten B, Engstrand L, Andersson AF. 7 August 2013. Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by Caesarean section. Gut http://dx.doi.org/10.1136/gutjnl-2012-303249.
36. Human Microbiome Project Consortium. 2012. Structure, function and diversity of the healthy human microbiome. Nature 486:207-214. http://dx.doi.org/10.1038/nature11234.
37. Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf H, Goodman AL, Clemente JC, Knight R, Heath AC, Leibel RL, Rosenbaum M, Gordon JI. 2013. The long-term stability of thehumangut microbiota. Science 341:1237439. http://dx.doi.org/10.1126/science.1237439.
38. Elinav E, Strowig T, Kau AL, Henao-Mejia J, Thaiss CA, Booth CJ, Peaper DR, Bertin J, Eisenbarth SC, Gordon JI, Flavell RA. 2011. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 145:745-757. http://dx.doi.org/10.1016/j.cell.2011.04.022.
39. Liu B, Tonkonogy SL, Sartor RB. 2011. Antigen-presenting cell production of IL-10 inhibits T-helper 1 and 17 cell responses and suppresses colitis in mice. Gastroenterology 141:653-662. http://dx.doi.org/10.1053/j.gastro.2011.04.053.
40. Nakayama J, Kobayashi T, Tanaka S, Korenori Y, Tateyama A, Sakamoto N, Kiyohara C, Shirakawa T, Sonomoto K. 2011. Aberrant structures of fecal bacterial community in allergic infants profiled by 16S rRNA gene pyrosequencing. FEMS Immunol. Med. Microbiol. 63:397-406. http://dx.doi.org/10.1111/j.1574-695X.2011.00872.x.
41. Hayashi A, Sato T, Kamada N, Mikami Y, Matsuoka K, Hisamatsu T, Hibi T, Roers A, Yagita H, Ohteki T, Yoshimura A, Kanai T. 2013. A single strain of Clostridium butyricum induces intestinal IL-10-producing macrophages to suppress acute experimental colitis in mice. Cell Host Microbe 13:711-722. http://dx.doi.org/10.1016/j.chom.2013.05.013.
42. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ, Blugeon S, Bridonneau C, Furet JP, Corthier G, Grangette C, Vasquez N, Pochart P, Trugnan G, Thomas G, Blottiere HM, Dore J, Marteau P, Seksik P, Langella P. 2008. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. U. S. A. 105:16731-16736. http://dx.doi.org/10.1073/pnas.0804812105.
43. Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, Cheng G, Yamasaki S, Saito T, Ohba Y, Taniguchi T, Takeda K, Hori S, Ivanov II, Umesaki Y, Itoh K, Honda K. 2011. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331:337-341. http://dx.doi.org/10.1126/science.1198469.
44. Chiba T, Seno H. 2011. Indigenous clostridium species regulate systemic immune responses by induction of colonic regulatory T cells. Gastroenterology 141:1114-1116. http://dx.doi.org/10.1053/j.gastro.2011.07.013.
45. Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, Fukuda S, Saito T, Narushima S, Hase K, Kim S, Fritz JV, Wilmes P, Ueha S, Matsushima K, Ohno H, Olle B, Sakaguchi S, Taniguchi T, Morita H, Hattori M, Honda K. 2013. Treg induction by a rationally selected mixture of clostridia strains from the human microbiota. Nature 500:232-236. http://dx.doi.org/10.1038/nature12331.
46. Klaenhammer TR, Kleerebezem M, Kopp MV, Rescigno M. 2012. The impact of probiotics and prebiotics on the immune system. Nat. Rev. Immunol. 12:728-734. http://dx.doi.org/10.1038/nri3312.
47. Gosalbes MJ, Llop S, Valles Y, Moya A, Ballester F, Francino MP. 2013. Meconium microbiota types dominated by lactic acid or enteric bacteria are differentially associated with maternal eczema and respiratory problems in infants. Clin. Exp. Allergy 43:198-211. http://dx.doi.org/10.1111/cea.12063.
48. Zhang Z, Zhai H, Geng J, Yu R, Ren H, Fan H, Shi P. 2013. Large-scale survey of gut microbiota associated with MHE via 16S rRNA-based pyrosequencing. Am. J. Gastroenterol. 108:1601-1611. http://dx.doi.org/10.1038/ajg.2013.221.