Current knowledge and future research directions on fecal bacterial patterns and their association with asthma

Frontiers in Microbiology

Volumn 7, Issue JUN, 2016, Pages

  Claassen Weitz, Shantelle ^a   Wiysonge, Charles S ^b,c   Machingaidze, Shingai ^d   Thabane, Lehana ^e,f   Horsnell, William G C ^a,d   Zar, Heather J ^d,g   Nicol, Mark P ^a,d,h   Kaba, Mamadou ^a,d  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b UNIVERSITY OF STELLENBOSCH   (South Africa)

^c SOUTH AFRICAN MEDICAL RESEARCH COUNCIL   (South Africa)

^d UNIVERSITY OF CAPE TOWN   (South Africa)

^e MCMASTER UNIVERSITY   (Canada)

^f MCMASTER UNIVERSITY   (Canada)

^g RED CROSS WAR MEMORIAL CHILDREN S HOSPITAL   (South Africa)

^h UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

Asthma; Fecal bacteria; Mechanisms; Microbiome; Systematic review

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 17; PROBIOTIC AGENT; RNA 16S;

ALLERGIC AIRWAY INFLAMMATION; ASTHMA; BIFIDOBACTERIUM; CLOSTRIDIUM DIFFICILE INFECTION; DENATURING GRADIENT GEL ELECTROPHORESIS; FECES MICROFLORA; FLUORESCENCE IN SITU HYBRIDIZATION; HELIGMOSOMOIDES BAKERI; HUMAN; IMMUNE RESPONSE; INTESTINE FLORA; LACTOBACILLUS; MEDICAL RESEARCH; MICROBIAL DIVERSITY; NONHUMAN; NOTE; REAL TIME POLYMERASE CHAIN REACTION; RESPIRATORY TRACT INFECTION; WHEEZING;

EID: 84979997683     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00838     Document Type: Note

References (125)

1. Arnold, I. C., Dehzad, N., Reuter, S., Martin, H., Becher, B., Taube, C., et al. (2011). Helicobacter pylori infection prevents allergic asthma in mouse models through the induction of regulatory T cells. Clin. Invest J. 121, 3088-3093. doi: 10.1172/JCI45041
2. Arrieta, M., Stiemsma, L. T., Dimitriu, P. A., Thorson, L., Russell, S., Yurist-Doutsch, S., et al. (2015). Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci. Transl. Med. 7, 1-14. doi: 10.1126/scitranslmed.aab2271
3. Arshi, S., Fallahpour, M., Nabavi, M., Bemanian, M. H., Javad-Mousavi, S. A., Nojomi, M., et al. (2014). The effects of vitamin D supplementation on airway functions in mild to moderate persistent asthma. Ann. Allergy Asthma Immunol. 113, 404-409. doi: 10.1016/j.anai.2014.07.005
4. Arslanoglu, S., Moro, G. E., Boehm, G., Wienz, F., Stahl, B., and Bertino, E. (2012). Early Neutral Prebiotic Oligosaccharide Supplentation reduces the incidence of some allergic manifestations in the first 5 years of life. J. Biol. Regul. Homeost. Agents 26, 49-59
5. Atarashi, K., Tanoue, T., Shima, T., Imaoka, A., Kuwahara, T., Momose, Y., et al. (2011). Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331, 337-341. doi: 10.1126/science.1198469
6. Azad, M. B., and Kozyrskyj, A. L. (2012). Perinatal programming of asthma: the role of gut microbiota. Clin. Dev. Immunol. 2012:932072. doi: 10.1155/2012/932072
7. Bateman, E. D., Hurd, S. S., Barnes, P. J., Bousquet, J., Drazen, J. M., FitzGerald, M., et al. (2008). Global strategy for asthma management and prevention: GINA executive summary. Eur. Respir. J. 31, 143-178. doi: 10.1183/09031936.00138707
8. Bisgaard, H., Li, N., Bonnelykke, K., Chawes, B. L. K., Skov, T., Paludan-Müller, G., et al. (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. doi: 10.1016/j.jaci.2011.04.060
9. Blaser, M. J., and Falkow, S. (2009). What are the consequences of the disappearing human microbiota? Nat. Rev. Microbiol. 7, 887-894. doi: 10.1038/nrmicro2245
10. Bloomfield, S., Stanwell-Smith, R., Crevelz, R., and Pickup, J. (2006). Too clean, or not too clean: the Hygiene Hypothesis and home hygiene. Clin. Exp. Allergy 36, 402-425. doi: 10.1111/j.1365-2222.2006.02463.x
11. Brehm, J. M., Celedón, J. C., Soto-Quiros, M. E., Avila, L., Hunninghake, G. M., and Forno, E. (2009). Serum vitamin D levels and markers of severity of childhood asthma in Costa Rica. Am. J. Respir. Crit. Care Med. 179, 765-771. doi: 10.1164/rccm.200808-1361OC
12. Brehm, J. M., Schuemann, B., Fuhlbrigge, A. L., Hollis, B. W., Strunk, R. C., Zeiger, R. S., et al. (2010). Serum vitamin D levels and severe asthma exacerbations in the childhood Asthma management program study. J. Allergy Clin. Immunol. 126, 52-58. doi: 10.1016/j.jaci.2010.03.043
13. Brooks, C., Pearce, N., and Douwes, J. (2013). The hygiene hypothesis in allergy and asthma: an update. Curr. Opin. Allergy Clin. Immunol. 13, 70-77. doi: 10.1097/ACI.0b013e32835ad0d2
14. Caselli, M., Vaira, G., Calo, G., Papini, F., Holton, J., and Vaira, D. (2011). Structural bacterial molecules as potential candidates for an evolution of the classical concept of probiotics. Adv. Nutr. 2, 372-376. doi: 10.3945/an.111.000604
15. Castro-Rodriguez, J. A. (2010). The Asthma Predictive Index: a very useful tool for predicting asthma in young children. J. Allergy Clin. Immunol. 126, 212-216. doi: 10.1016/j.jaci.2010.06.032
16. Clemente, J. C., Ursell, L. K., Parfrey, L. W., and Knight, R. (2012). The impact of the gut microbiota on human health: an integrative view. Cell 148, 1258-1270. doi: 10.1016/j.cell.2012.01.035
17. De Filippo, C., Cavalieri, D., Di Paola, M., Ramazzotti, M., Poullet, J. B., Massart, S., et al. (2010). Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. U.S.A. 107, 14691-14696. doi: 10.1073/pnas.1005963107
18. De Kivit, S., Tobin, M. C., Forsyth, C. B., Keshavarzian, A., and Landay, A. L. (2014). Regulation of intestinal immune responses through TLR activation: Implications for pro-and prebiotics. Front. Immunol. 5:60. doi: 10.3389/fimmu.2014.00060
19. Dogaru, C. M., Nyffenegger, D., Pescatore, A. M., Spycher, B. D., and Kuehni, C. E. (2014). Breastfeeding and childhood asthma: Systematic review and meta-analysis. Am. J. Epidemiol. 179, 1153-1167. doi: 10.1093/aje/kwu072
20. Edwards, M. R., Bartlett, N. W., Hussell, T., Openshaw, P., and Johnston, S. L. (2012). The microbiology of asthma. Nat. Rev. Microbiol. 10, 459-471. doi: 10.1038/nrmicro2801
21. Elazab, N., Mendy, A., Gasana, J., Vieira, E. R., Quizon, A., and Forno, E. (2013). Probiotic administration in early life, atopy, and asthma: a meta-analysis of clinical trials. Pediatrics 132, e666-e676. doi: 10.1542/peds.2013-0246
22. Eloe-Fadrosh, E. A., Brady, A., Crabtree, J., Drabek, E. F., Ma, B., Mahurkar, A., et al. (2015). Functional dynamics of the gut microbiome in elderly people during probiotic consumption. MBio 6, 1-12. doi: 10.1128/mBio.00231-15
23. Feleszko, W., Jaworska, J., Rha, R. D., Steinhausen, S., Avagyan, A., Jaudszus, A., et al. (2007). Probiotic-induced suppression of allergic sensitization and airway inflammation is associated with an increase of T regulatory-dependent mechanisms in a murine model of asthma. Clin. Exp. Allergy 37, 498-505. doi: 10.1111/j.1365-2222.2006.02629.x
24. Fijan, S. (2014). Microorganisms with claimed probiotic properties: an overview of recent literature. Int. J. Environ. Res. Public Health 11, 4745-4767. doi: 10.3390/ijerph110504745
25. Forsythe, P. (2011). Probiotics and lung diseases. Chest 139, 901-908. doi: 10.1378/chest.10-1861
26. Fraher, M. H., O'Toole, P. W., and Quigley, E. M. (2012). Techniques used to characterize the gut microbiota: a guide for the clinician. Nat. Rev. Gastroenterol. Hepatol. 9, 312-322. doi: 10.1038/nrgastro.2012.44
27. Gaboriau-Routhiau, V., Rakotobe, S., Lécuyer, E., Mulder, I., Lan, A., Bridonneau, C., et al. (2009). The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 31, 677-689. doi: 10.1016/j.immuni.2009.08.020
28. Goleva, E., Jackson, L. P., Harris, J. K., Robertson, C. E., Sutherland, E. R., Hall, C. F., et al. (2013). The effects of airway microbiome on corticosteroid responsiveness in asthma. Am. J. Respir. Crit. Care Med. 188, 1193-1201. doi: 10.1164/rccm.201304-0775OC
29. Gosalbes, M. J., Llop, S., Vallès, Y., Moya, A., Ballester, F., and Francino, M. P. (2012). 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. doi: 10.1111/cea.12063
30. Grzeskowiak, L., Collado, M. C., Mangani, C., Maleta, K., Laitinen, K., Ashorn, P., et al. (2012). Distinct gut microbiota in southeastern African and northern European infants. J. Paediatr. Gastroenterol. Nutr. 54, 812-816. doi: 10.1097/MPG.0b013e318249039c
31. Hanski, I., von Hertzen, L., Fyhrquist, N., Koskinen, K., Torppa, K., Laatikainen, T., et al. (2012). Environmental biodiversity, human microbiota, and allergy are interrelated. Proc. Natl. Acad. Sci. U.S.A. 109, 8334-8339. doi: 10.1073/pnas.1205624109
32. Herbst, T., Sichelstiel, A., Schär, C., Yadava, K., Bürki, K., Cahenzli, J., et al. (2011). Dysregulation of allergic airway inflammation in the absence of microbial colonization. Am. J. Respir. Crit. Care Med. 184, 198-205. doi: 10.1164/rccm.201010-1574OC
33. Hill, D. A., and Artis, D. (2010). Intestinal bacteria and the regulation of immune cell homeostasis. Annu. Rev. Immunol. 28, 623-667. doi: 10.1146/annurev-immunol-030409-101330
34. Hunter, P. (2012). The changing hypothesis of the gut. The intestinal microbiome is increasingly seen as vital to human health. EMBO Rep. 13, 498-500. doi: 10.1038/embor.2012.68
35. Ivanov, I. I., Frutos Rde, L., Manel, N., Yoshinaga, K., Rifkin, D. B., Sartor, R. B., et al. (2008). Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4, 337-349. doi: 10.1016/j.chom.2008.09.009
36. Jeurink, P. V., Van Esch, B. C., Rijnierse, A., Garssen, J., and Knippels, L. M. (2013). Mechanisms underlying immune effects of dietary oligosaccharides. Am. J. Clin. Nutr. 98, 572S-577S. doi: 10.3945/ajcn.112.038596
37. Jin, D., Wu, S., Zhang, Y. G., Lu, R., Xia, Y., Dong, H., et al. (2015). Lack of Vitamin D receptor causes dysbiosis and changes the functions of the murine intestinal microbiome. Clin. Ther. 37, 996-1009. doi: 10.1016/j.clinthera.2015.04.004
38. Karimi, K., Inman, M. D., Bienenstock, J., and Forsythe, P. (2009). Lactobacillus reuteri-induced regulatory T cells protect against an allergic airway response in mice. Am. J. Respir. Crit. Care Med. 179, 186-193. doi: 10.1164/rccm.200806-951OC
39. Kim, H. J., Kim, Y. J., Lee, S.-H., Kang, M. J., Yu, H.-S., Jung, Y. H., et al. (2013). Effects of Lactobacillus rhamnosus on asthma with an adoptive transfer of dendritic cells in mice. J. Appl. Microbiol. 115, 872-879. doi: 10.1111/jam.12268
40. Kim, Y. G., Udayanga, K. G., Totsuka, N., Weinberg, J. B., Núñez, G., and Shibuya, A. (2014). Gut dysbiosis promotes M2 macrophage polarization and allergic airway inflammation via fungi-induced PGE2. Cell Host Microbe 15, 95-102. doi: 10.1016/j.chom.2013.12.010
41. Kjer-Nielsen, L., Patel, O., Corbett, A. J., Le Nours, J., Meehan, B., Liu, L., et al. (2012). MR1 presents microbial vitamin B metabolites to MAIT cells. Nature 491, 717-723. doi: 10.1038/nature11605
42. Knights, D., Ward, T. L., Mckinlay, C. E., Miller, H., Gonzalez, A., and Mcdonald, D. (2014). Rethinking "Enterotypes." Cell Host Microbe 16, 433-437. doi: 10.1016/j.chom.2014.09.013
43. Konieczna, P., Groeger, D., Ziegler, M., Frei, R., Ferstl, R., Shanahan, F., et al. (2012). Bifidobacterium infantis 35624 administration induces Foxp3 T regulatory cells in human peripheral blood: potential role for myeloid and plasmacytoid dendritic cells. Gut 61, 354-366. doi: 10.1136/gutjnl-2011-300936
44. Koren, O., Knights, D., Gonzalez, A., Waldron, L., Segata, N., Knight, R., et al. (2013). A guide to enterotypes across the human body: meta-analysis of microbial community structures in human microbiome datasets. PLoS Comput. Biol. 9:e1002863. doi: 10.1371/journal.pcbi.1002863
45. Kozyrskyj, A. L., Bahreinian, S., and Azad, M. B. (2011). Early life exposures: impact on asthma and allergic disease. Curr. Opin. Allergy Clin. Immunol. 11, 400-406. doi: 10.1097/ACI.0b013e328349b166
46. Kramer, A., Bekeschus, S., Bröker, B. M., Schleibinger, H., Razavi, B., and Assadian, O. (2013). Maintaining health by balancing microbial exposure and prevention of infection: the hygiene hypothesis versus the hypothesis of early immune challenge. J. Hosp. Infect. 83, S29-S34. doi: 10.1016/S0195-6701(13)60007-9
47. Kurokawa, K., Itoh, T., Kuwahara, T., Oshima, K., Toh, H., Toyoda, A., et al. (2007). Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res. 14, 169-181. doi: 10.1093/dnares/dsm018
48. Kuzela, L., Vavrecka, A., Prikazska, M., Drugda, B., Hronec, J., Senkova, A., et al. (1999). Pulmonary complications in patients with inflammatory bowel disease. Hepatogastroenterology 46, 1714-1719
49. Le Bourhis, L., Guerri, L., Dusseaux, M., Martin, E., Soudais, C., and Lantz, O. (2011). Mucosal-associated invariant T cells: unconventional development and function. Trends Immunol. 32, 212-218. doi: 10.1016/j.it.2011.02.005
50. Le Bourhis, L., Mburu, Y. K., and Lantz, O. (2013). MAIT cells, surveyors of a new class of antigen: development and functions. Curr. Opin. Immunol. 25, 174-180. doi: 10.1016/j.coi.2013.01.005
51. Lin, A., Bik, E. M., Costello, E. K., Dethlefsen, L., Haque, R., Relman, D. A., et al. (2013). Distinct distal gut microbiome diversity and composition in healthy children from Bangladesh and the United States. PLoS ONE 8:e53838. doi: 10.1371/journal.pone.0053838
52. MacSharry, J., O'Mahony, C., Shalaby, K. H., Sheil, B., Karmouty-Quintana, H., Shanahan, F., et al. (2012). Immunomodulatory effects of feeding with Bifidobacterium longum on allergen-induced lung inflammation in the mouse. Pulm. Pharmacol. Ther. 25, 325-334. doi: 10.1016/j.pupt.2012.05.011
53. Mai, V., McCrary, Q. M., Sinha, R., and Glei, M. (2009). Associations between dietary habits and body mass index with gut microbiota composition and fecal water genotoxicity: an observational study in African American and Caucasian American volunteers. Nutr. J. 8:49. doi: 10.1186/1475-2891-8-49
54. Mallol, J. (2008). Asthma in Latin America: where the asthma causative/protective hypotheses fail. Allergol. Immunopathol. (Madr). 36, 150-153. doi: 10.1016/S0301-0546(08)72540-0
55. Mann, E. H., Chambers, E. S., Pfeffer, P. E., and Hawrylowicz, C. M. (2014). Immunoregulatory mechanisms of vitamin D relevant to respiratory health and asthma. Ann. N.Y. Acad. Sci. 1317, 57-69. doi: 10.1111/nyas.12410
56. Mansson, I., and Colldahl, H. (1965). The intestinal flora in patients with bronchial asthma and rheumatoid arthritis. Allergy 20, 94-104. doi: 10.1111/j.1398-9995.1965.tb03360.x
57. Marra, F., Marra, C. A., Richardson, K., Lynd, L. D., Kozyrskyj, A., Patrick, D. M., et al. (2009). Antibiotic use in children is associated with increased risk of asthma. Pediatrics 123, 1003-1010. doi: 10.1542/peds.2008-1146
58. Masoli, M., Fabian, D., Holt, S., and Beasley, R. (2004). The global burden of asthma: executive summary of the GINA Dissemination Committee report. Allergy 59, 469-478. doi: 10.1111/j.1398-9995.2004.00526.x
59. McLoughlin, R. M., and Mills, K. H. (2011). Influence of gastrointestinal commensal bacteria on the immune responses that mediate allergy and asthma. J. Allergy Clin. Immunol. 127, 1097. doi: 10.1016/j.jaci.2011.02.012
60. Mohamed-Hussein, A. A., Mohamed, N. A., and Ibrahim, M. E. (2007). Changes in pulmonary function in patients with ulcerative colitis. Respir. Med. 101, 977-982. doi: 10.1016/j.rmed.2006.09.005
61. Morgan, X. C., and Huttenhower, C. (2014). Meta'omic analytic techniques for studying the intestinal microbiome. Gastroenterology 146, 1437-1448. doi: 10.1053/j.gastro.2014.01.049
62. Murk, W., Risnes, K. R., and Bracken, M. B. (2011). Prenatal or early-life exposure to antibiotics and risk of childhood asthma: a systematic review. Pediatrics 127, 1125-1138. doi: 10.1542/peds.2010-2092
63. Nambu, M., Shintaku, N., and Ohta, S. (2008). Intestinal microflora at 4 months of age and the development of allergy. Allergol. Int. 53, 121-126. doi: 10.1111/j.1440-1592.2004.00315.x
64. Navarro, S., Cossalter, G., Chiavaroli, C., Kanda, A., Fleury, S., Lazzari, A., et al. (2011). The oral administration of bacterial extracts prevents asthma via the recruitment of regulatory T cells to the airways. Mucosal Immunol. 4, 53-65. doi: 10.1038/mi.2010.51
65. Oertli, M., Sundquist, M., Hitzler, I., Engler, D. B., Arnold, I. C., Reuter, S., et al. (2012). DC-derived IL-18 drives Treg differentiation, murine Helicobacter pylori-specific immune tolerance, and asthma protection. J. Clin. Invest. 122, 1082-1096. doi: 10.1172/JCI61029
66. Osborn, D., and Sinn, J. (2013). Prebiotics in infants for prevention of allergy. Cochrane Database Syst. Rev. 3:CD006474. doi: 10.1002/14651858.CD006474.pub3
67. Ou, J., Carbonero, F., Zoetendal, E. G., Delany, J. P., Wang, M., Newton, K., et al. (2013). Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am. J. Clin. Nutr. 98, 111-120. doi: 10.3945/ajcn.112.056689
68. Palm, N. W., De Zoete, M. R., Cullen, T. W., Barry, N. A., Stefanowski, J., Hao, L., et al. (2014). Immunoglobulin A coating identifies colitogenic bacteria in inflammatory bowel disease. Cell 158, 1000-1010. doi: 10.1016/j.cell.2014.08.006
69. Patel, O., Kjer-Nielsen, L., Le Nours, J., Eckle, S. B. G., Birkinshaw, R., Beddoe, T., et al. (2013). Recognition of vitamin B metabolites by mucosal-associated invariant T cells. Nat. Commun. 4, 2142. doi: 10.1038/ncomms3142
70. Pedersen, S. (2007). Preschool asthma-not so easy to diagnose. Prim. Care Respir. 16, 4-6. doi: 10.3132/pcrj.2007.00011
71. Pedersen, S. E., Hurd, S. S., Lemanske, R. F., Becker, A., Zar, H. J., Sly, P. D., et al. (2011). Global strategy for the diagnosis and management of asthma in children 5 years and younger. Pediatr. Pulmonol. 46, 1-17. doi: 10.1002/ppul.21321
72. Penders, J., Kummeling, I., and Thijs, C. (2011). Infant antibiotic use and wheeze and asthma risk: a systematic review and meta-analysis. Eur. Respir. J. 38, 295-302. doi: 10.1183/09031936.00105010
73. Penders, J., Stobberingh, E. E., Van den Brandt, P. A., and Thijs, C. (2007). The role of the intestinal microbiota in the development of atopic disorders. Allergy 62, 1223-1236. doi: 10.1111/j.1398-9995.2007.01462.x
74. Peng, Y. H., Liao, W. C., Su, C. H., Chen, H. J., Hsia, T. C., Chu, C. C., et al. (2015). Association of inflammatory bowel disease with asthma risk: a nationwide cohort study. Allergy Asthma Proc. 36, e92-e98. doi: 10.2500/aap.2015.36.3869
75. Qin, J., Li, Y., Cai, Z., Li, S. S., Zhu, J., Zhang, F., et al. (2012). A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490, 55-60. doi: 10.1038/nature11450
76. Quince, C., Ijaz, U. Z., Loman, N., Eren, A. M., Saulnier, D., Russell, J., et al. (2015). Extensive modulation of the fecal metagenome in children with Crohn's Disease during exclusive enteral nutrition. Am. J. Gastroenterol. 1-12. doi: 10.1038/ajg.2015.357
77. Rajilic-Stojanovic, M., Smidt, H., and De Vos, W. M. (2007). Diversity of the human gastrointestinal tract microbiota revisited. Environ. Microbiol. 9, 2125-2136. doi: 10.1111/j.1462-2920.2007.01369.x
78. Ranjan, R., Rani, A., Metwally, A., McGee, H. S., and Perkens, D. L. (2015). Analysis of the microbiome: advantages of whole genome shotgun versus 16S amplicon sequencing. Biochem. Biophys. Res. Commun. 469, 967-977. doi: 10.1016/j.bbrc.2015.12.083
79. Risnes, K. R., Belanger, K., Murk, W., and Bracken, M. B. (2010). Antibiotic exposure by 6 months and asthma and allergy at 6 years: Findings in a cohort of 1, 401 US children. Am. J. Epidemiol. 173, 310-318. doi: 10.1093/aje/kwq400
80. Rook, G. (2012). Hygiene hypothesis and autoimmune diseases. Clin. Rev. Allergy Immunol. 42, 5-15. doi: 10.1007/s12016-011-8285-8
81. Round, J. L., Lee, S. M., Li, J., Tran, G., Jabri, B., Chatila, T. A., et al. (2011). The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 332, 974. doi: 10.1126/science.1206095
82. Russell, S. L., and Finlay, B. B. (2012). The impact of gut microbes in allergic diseases. Curr. Opin. Gastroenterol. 28, 563-569. doi: 10.1097/MOG.0b013e3283573017
83. Russell, S. L., Gold, M. J., Hartmann, M., Willing, B. P., Thorson, L., Wlodarska, M., et al. (2012). Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep. 13, 440-447. doi: 10.1038/embor.2012.32
84. Russell, S. L., Gold, M. J., Willing, B. P., Thorson, L., McNagny, K. M., and Finlay, B. B. (2013). Perinatal antibiotic treatment affects murine microbiota, immune responses and allergic asthma. Gut Microbes 4, 158-164. doi: 10.4161/gmic.23567
85. Salminen, S., Gibson, G. R., McCartney, A. L., and Isolauri, E. (2004). Influence of mode of delivery on gut microbiota composition in seven year old children. Gut 53, 1388-1389. doi: 10.1136/gut.2004.041640
86. Salzman, N. H. (2011). Microbiota-immune system interaction: an uneasy alliance. Curr. Opin. Microbiol. 14, 99-105. doi: 10.1016/j.mib.2010.09.018
87. Samuelson, D. R., Welsch, D. A., and Shellito, J. E. (2015). Regulation of lung immunity and host defense by the intestinal microbiota. Front. Microbiol. 6:1085. doi: 10.3389/fmicb.2015.01085
88. Sankar, S. A., Lagier, J. C., Pontarotti, P., Raoult, D., and Fournier, P. E. (2015). The human gut microbiome, a taxonomic conundrum. Syst. Appl. Microbiol. 38, 276-286. doi: 10.1016/j.syapm.2015.03.004
89. Schippa, S., and Conte, M. (2014). Dysbiotic events in gut microbiota: Impact on human health. Nutrients 6, 5786-5805. doi: 10.3390/nu6125786
90. Sekirov, I., Russell, S. L., Antunes, L. C. M., and Finlay, B. B. (2010). Gut microbiota in health and disease. Physiol. Rev. 90, 859-904. doi: 10.1152/physrev.00045.2009
91. Shenderov, B. A. (2013). Metabiotics: novel idea or natural development of probiotic conception. Microb. Ecol. Health Dis. 24, 1-8. doi: 10.3402/mehd.v24i0.20399
92. Sim, K., Cox, M. J., Wopereis, H., Martin, R., Knol, J., Li, M. S., et al. (2012). Improved detection of bifidobacteria with optimised 16S rRNA-gene based pyrosequencing. PLoS ONE 7:e32543. doi: 10.1371/journal.pone.0032543
93. Sly, P. D., Boner, A. L., Björksten, B., Bush, A., Custovic, A., Eigenmann, P. A., et al. (2008). Early identification of atopy in the prediction of persistent asthma in children. Lancet 372, 1100-1106. doi: 10.1016/S0140-6736(08)61451-8
94. Stockert, K. (2001). Physiologische Darmflora bei 6-bis 12-jaehrigen kindern mit asthma bronchiale. Dt. Ztschr. F. Akup. 44, 268-271. doi: 10.1055/s-2001-19471
95. Strachan, D. P. (1989). Hay fever, hygiene, and household size. BMJ 299, 1259-1260. doi: 10.1136/bmj.299.6710.1259
96. Strachan, D. P. (2000). Family size, infection and atopy: the first decade of the 'hygiene hypothesis'. Thorax 55:S2. doi: 10.1136/thorax.55.suppl_1.S2
97. Štšepetova, J., Sepp, E., Julge, K., Vaughan, E., Mikelsaar, M., and De Vos, W. M. (2007). Molecularly assessed shifts of Bifidobacterium ssp. and less diverse microbial communities are characteristic of 5-year-old allergic children. FEMS Immunol. Med. Microbiol 51, 260-269. doi: 10.1111/j.1574-695X.2007.00306.x
98. Suau, A., Bonnet, R., Sutren, M., Godon, J. J., Gibson, G. R., Collins, M. D., et al. (1999). Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl. Environ. Microbiol. 65, 4799-4807
99. Suzuki, T. A., and Worobey, M. (2014). Geographical variation of human gut microbial composition Geographical variation of human gut microbial composition. Biol. Lett. 10, 20131037. doi: 10.1098/rsbl.2013.1037
100. Taube, C., and Müller, A. (2012). The role of Helicobacter pylori infection in the development of allergic asthma. Expert Rev. Respir. Med. 6, 441-449. doi: 10.1586/ers.12.40
101. Taylor, A. L., Dunstan, J. A., and Prescott, S. L. (2007). Probiotic supplementation for the first 6 months of life fails to reduce the risk of atopic dermatitis and increases the risk of allergen sensitization in high-risk children: a randomized controlled trial. J. Allergy Clin. Immunol. 119, 184-191. doi: 10.1016/j.jaci.2006.08.036
102. Thavagnanam, S., Fleming, J., Bromley, A., Shields, M. D., and Cardwell, C. R. (2008). A meta-analysis of the association between Caesarean section and childhood asthma. Clin. Exp. Allergy 38, 629-633. doi: 10.1111/j.1365-2222.2007.02780.x
103. Treiner, E., Duban, L., Bahram, S., Radosavljevic, M., Wanner, V., Tilloy, F., et al. (2003). Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature 422, 164-169. doi: 10.1038/nature01433
104. Trompette, A., Gollwitzer, E. S., Yadava, K., Sichelstiel, A. K., Sprenger, N., Ngom-Bru, C., et al. (2014). Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat. Med. 20, 159-166. doi: 10.1038/nm.3444
105. Tulic, M. K., Piche, T., and Verhasselt, V. (2016). Lung-gut crosstalk: evidence, mechanisms and implications for the mucosal inflammatory diseases. Clin. Exp. Allergy 46, 519-528. doi: 10.1111/cea.12723
106. Vael, C., Nelen, V., Verhulst, S. L., Goossens, H., and Desager, K. N. (2008). Early intestinal Bacteroides fragilis colonisation and development of asthma. BMC Pulm. Med. 8:19. doi: 10.1186/1471-2466-8-19
107. Vael, C., Vanheirstraeten, L., Desager, K. N., and Goossens, H. (2011). Denaturing gradient gel electrophoresis of neonatal intestinal microbiota in relation to the development of asthma. BMC Microbiol. 11:68. doi: 10.1186/1471-2180-11-68
108. Van de Pol, M. A., Lutter, R., Smids, B. S., Weersink, E. J. M., and Van der Zee, J. S. (2011). Synbiotics reduce allergen-induced T-helper 2 response and improve peak expiratory flow in allergic asthmatics. Allergy 66, 39-47. doi: 10.1111/j.1398-9995.2010.02454.x
109. Van der Aa, L. B., Van Aalderen, W. M. C., Heymans, H. S. A., Henk Sillevis Smitt, J., Nauta, A. J., Knippels, L. M. J., et al. (2011). Synbiotics prevent asthma-like symptoms in infants with atopic dermatitis. Allergy 66, 170-177. doi: 10.1111/j.1398-9995.2010.02416.x
110. Van der Waaij, L. A., Kroese, F. G., Visser, A., Nelis, G. F., Westerveld, B. D., Jansen, P. L., et al. (2004). Immunoglobulin coating of faecal bacteria in inflammatory bowel disease. Eur. J. Gastroenterol. Hepatol. 16, 669-674. doi: 10.1097/01.meg.0000108346.41221.19
111. Van Dijk, E. L., Auger, H., Jaszczyszyn, Y., and Thermes, C. (2014). Ten years of next-generation sequencing technology. Trends Genet. 30, 418-426. doi: 10.1016/j.tig.2014.07.001
112. Van Nimwegen, F. A., Penders, J., Stobberingh, E. E., Postma, D. S., Koppelman, G. H., Kerkhof, M., et al. (2011). Mode and place of delivery, gastrointestinal microbiota, and their influence on asthma and atopy. J. Allergy Clin. Immunol. 128, 948-955. doi: 10.1016/j.jaci.2011.07.027
113. Viljanen, M., Pohjavuori, E., Haahtela, T., Korpela, R., Kuitunen, M., Sarnesto, A., et al. (2005). Induction of inflammation as a possible mechanism of probiotic effect in atopic eczema-dermatitis syndrome. J. Allergy Clin. Immunol. 115, 1254-1259. doi: 10.1016/j.jaci.2005.03.047
114. Vital, M., Harkema, J. R., Rizzo, M., Tiedje, J., and Brandenberger, C. (2015). Alterations of the murine gut microbiome with age and allergic airway disease. J. Immunol. Res. 2015, 1-8. doi: 10.1155/2015/892568
115. Vliagoftis, H., Kouranos, V. D., Betsi, G. I., and Falagas, M. E. (2008). Probiotics for the treatment of allergic rhinitis and asthma: systematic review of randomized controlled trials. Ann. Allergy Asthma Immunol. 101, 570-579. doi: 10.1016/S1081-1206(10)60219-0
116. Vos, A. P., Van Esch, B. C., Stahl, B., M'Rabet, L., Folkerts, G., Nijkamp, F. P., et al. (2007). Dietary supplementation with specific oligosaccharide mixtures decreases parameters of allergic asthma in mice. Int. Immunopharmacol. 7, 1582-1587. doi: 10.1016/j.intimp.2007.07.024
117. Walker, A. W., Martin, J. C., Scott, P., Parkhill, J., Flint, H. J., and Scott, K. P. (2015). 16S rRNA gene-based profiling of the human infant gut microbiota is strongly influenced by sample processing and PCR primer choice. Microbiome 3:26. doi: 10.1186/s40168-015-0087-4
118. West, C. E. (2014). Gut microbiota and allergic disease: new findings. Curr. Opin. Clin. Nutr. Metab. Care 17, 261-266. doi: 10.1097/MCO.0000000000000044
119. Wold, A. E. (1998). The hygiene hypothesis revised: is the rising frequency of allergy due to changes in the intestinal flora? Allergy 53, 20-25 doi: 10.1111/j.1398-9995.1998.tb04953.x
120. Yatsunenko, T., Rey, F. E., Manary, M. J., Trehan, I., Dominguez-Bello, M. G., Contreras, M., et al. (2012). Human gut microbiome viewed across age and geography. Nature 486, 222-227. doi: 10.1038/nature11053
121. Zaiss, M. M., Rapin, A., Lebon, L., Dubey, L. K., Mosconi, I., Sarter, K., et al. (2015). The intestinal microbiota contributes to the ability of helminths to modulate allergic inflammation. Immunity 43, 998-1010. doi: 10.1016/j.immuni.2015.09.012
122. Zar, H. J., and Levin, M. E. (2012). Challenges in treating pediatric asthma in developing countries. Pediatr. Drugs 14, 353-359. doi: 10.2165/11597420-000000000-00000
123. Zhang, Q., Cox, M., Liang, Z., Brinkmann, F., Cardenas, P. A., and Duff, R. (2016). Airway microbiota in severe asthma and relationship to asthma severity and phenotypes. PLoS ONE 11:e0152724. doi: 10.1371/journal.pone.0152724
124. Zhao, L. (2013). The gut microbiota and obesity: from correlation to causality. Nat. Rev. Microbiol. 11, 639-647. doi: 10.1038/nrmicro3089
125. Zoetendal, E. G., Vaughan, E. E., and De Vos, W. M. (2006). A microbial world within us. Mol. Microbiol. 59, 1639-1650. doi: 10.1111/j.1365-2958.2006.05056.x