Reduced Akkermansia muciniphila and Faecalibacterium prausnitzii levels in the gut microbiota of children with allergic asthma
Main Article Content
Keywords
Asthmatic children, Akkermansia muciniphila, Faecalibacterium prausnitzii, Hygiene hypothesis, qPCR
Abstract
Introduction and objectives: The amounts of Akkermansia muciniphila and Faecalibacterium prausnitzii in gut microbiota are reduced in patients with allergic diseases compared to healthy controls. We aimed to quantify levels of A. muciniphila and F. prausnitzii amounts using real-time quantitative PCR (qPCR) in the gut microbiota of children with allergic asthma and in healthy controls.
Materials and methods: In total, 92 children between the ages of three and eight who were diagnosed with asthma and 88 healthy children were included in the study and bacterial DNA was isolated from the stool samples using the stool DNA isolation Kit. qPCR assays were studied with the microbial DNA qPCR Kit for A. muciniphila and microbial DNA qPCR Kit for F. prausnitzii.
Results: Both bacterial species showed a reduction in the patient group compared to healthy controls. A. muciniphila and F. prausnitzii were found to be 5.45 ± 0.004, 6.74 ± 0.01 and 5.71 ± 0.002, 7.28 ± 0.009 in the stool samples of the asthma and healthy control groups, respectively.
Conclusions: F. prausnitzii and A. muciniphila may have induced anti-inflammatory cytokine IL-10 and prevented the secretion of pro-inflammatory cytokines like IL-12. These findings suggest that A. muciniphila and F. prausnitzii may suppress inflammation through its secreted metabolites.
References
1. Arrieta MC, Stiemsma LT, Dimitriu PA, Thorson L, Russell S, Yurist-Doutsch S, et al. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci Transl Med. 2015;307:307ra152, http://dx.doi.org/10.1126/scitranslmed.aab2271 [PMID: 26424567].
2. Andersen YMF, Egeberg A, Skov L, Thyssen JP. Comorbidities of atopic dermatitis: beyond rhinitis and asthma. Curr Dermatol Rep. 2017;6:35-41, http://dx.doi.org/10.1007/s13671-017-0168-7 [PMID: 28890845].
3. Ober C, Yao T-C. The genetics of asthma and allergic disease: a 21st-century perspective. Immunol rev. 2011;242:10-30, http://dx.doi.org/10.1111/j.1600-065X. 2011.01029.x [PMID: 21682736].
4. Piacentini S, Polimanti R, Moscatelli B, Re MA, Manfellotto D, Fuciarelli M, et al. Lack of association between GSTM1 GSTP1, and GSTT1 gene polymorphisms and asthma in adult patients from Rome, central Italy. J Investig Allergol Clin Immunol. 2012;22:252-6 [PMID: 22812193].
5. Koga Y, Tokunaga S, Nagano J, Sato F, Konishi K. Age-associated effect of kestose on Faecalibacterium prausnitzii and symptoms in the atopic dermatitis infants. Pediatr Res. 2016;80:844-51, http://dx.doi.org/10.1038/pr.2016.167 [PMID: 27537603].
6. Miquel S, Martín R, Rossi O, Bermúdez-Humarán LG, Chatel JM, Sokol H, et al. Faecalibacterium prausnitzii and human intestinal health. Curr Opin Microbiol. 2013;16:255-61, http://dx.doi.org/10.1016/j.mib.2013.06.003 [PMID: 23831042].
7. Tsuda A, Suda W, Morita H. Influence of Proton-Pump Inhibitors on the Luminal Microbiota in the Gastrointestinal Tract. Clin Transl Gastroenterol. 2015;6:e89, http://dx.doi.org/10.1038/ctg.2015.20 [PMID: 26065717].
8. Gałecka M, Szachta P, Bartnicka A, Łykowska-Szuber L, Eder P, Schwiertz A. Faecalibacterium prausnitzii and Crohn’s disease- is there any connection? Pol J Microbiol. 2013;62:91-5 [PMID: 23829084].
9. Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, Beaugerie L, et al. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis. 2009;15:1183-9, http://dx.doi.org/10.1002/ibd.20903 [PMID: 19235886].
10. Song H, Yoo Y, Hwang J, Na YC, Kim HS. Faecalibacterium prausnitzii subspecies-level dysbiosis in the human gut microbiome underlying atopic dermatitis. J Allergy Clin Immunol. 2016;137:852-60, http://dx.doi.org/10.1016/j.jaci.2015.08.021 [PMID: 26431583].
11. Nabizadeh E, Jazani NH, Bagheri M, Shahabi S. Association of altered gut microbiota composition with chronic urticaria. Ann Allergy Asthma Immunol. 2017;119:48-53, http://dx.doi.org/10.1016/j.anai.2017.05.006 [PMID: 28668239].
12. Candela M, Rampelli S, Turroni S, Severgnini M, Consolandi C, De Bellis G, et al. Unbalance of intestinal microbiota in atopic children. BMC Microbiol. 2012;12:95, http://dx.doi.org/10.1186/1471-2180-12-95 [PMID: 22672413].
13. Duncan SH, Hold GL, Harmsen HJ, Stewart CS, Flint HJ. Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as Faecalibacterium prausnitzii gen. nov., comb. nov. Int J Syst Evol Microbiol. 2002;52:2141-6, http://dx.doi.org/10.1099/00207713-52-6-2141 [PMID: 12508881].
14. Cani PD, de Vos WM. Next-generation beneficial microbes: the case of Akkermansia muciniphila. Front Microbiol. 2017;8:1765, http://dx.doi.org/10.3389/fmicb.2017.01765 [PMID: 29018410].
15. Lukovac S, Belzer C, Pellis L, Keijser BJ, de Vos WM, Montijn RC, et al. Differential modulation by Akkermansia muciniphila and Faecalibacterium prausnitzii of host peripheral lipid metabolism and histone acetylation in mouse gut organoids. mBio. 2014;5:e01438-1514, http://dx.doi.org/10.1128/mBio.01438-14 [PMID: 25118238].
16. National Asthma Education and Prevention Program. Expert Panel Report 3 (EPR-3): Guidelines for the Diagnosis and Management of Asthma-Summary Report 2007. J Allergy Clin Immunol. 2007;120:S94-138, http://dx.doi.org/10.1016/j.jaci.2007.09.043 [PMID: 17983880].
17. Strachan DP. Family size, infection and atopy: the first decade of the ‘‘hygiene hypothesis’’. Thorax. 2000;55:S2-10, http://dx.doi.org/10.1136/thorax.55.suppl 1.S2 [PMID: 10943631].
18. Karakullukcu A, Tokman HB, Nepesov S, Demirci M, Saribas S. The protective role of Helicobacter pylori neutrophil-activating protein in childhood asthma. Allergol Immunopathol (Madr). 2017;45:521-7, http://dx.doi.org/10.1016/j.aller.2017.01.008 [PMID: 28579087].
19. Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system. Science. 2012;336:1268-73, http://dx.doi.org/10.1126/science.1223490 [PMID: 22674334].
20. Fieten KB, Totté JEE, Levin E, Reyman M, Meijer Y, Knulst A, et al. Fecal microbiome and food allergy in pediatric atopic dermatitis: a cross-sectional pilot study. Int Arch Allergy Immunol. 2018;175:77-84, http://dx.doi.org/10.1159/000484897 [PMID: 29393195].
21. Egert M, de Graaf AA, Smidt H, de Vos WM, Venema K. Beyond diversity: functional microbiomics of the human colon. Trends Microbiol. 2006;14:86-91, http://dx.doi.org/10.1016/j.tim.2005.12.007 [PMID: 16406528].
22. Louis P, Flint HJ. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett. 2009;294:1-8, http://dx.doi.org/10.1111/j.1574-6968.2009.01514.x [PMID: 19222573].
23. Kabeerdoss J, Sankaran V, Pugazhendhi S, Ramakrishna BS. Clostridium leptum group bacteria abundance and diversity in the fecal microbiota of patients with inflammatory bowel disease: a case-control study in India. BMC Gastroenterol. 2013;26:20, http://dx.doi.org/10.1186/1471-230X-13-20 [PMID: 23351032].
24. Scheppach W, Weiler F. The butyrate story: old wine in new bottles? Curr Opin Clin Nutr Metab Care. 2004;7:563-7 [PMID: 15295277].
25. Melli LC, do Carmo-Rodrigues MS, Araújo-Filho HB, Solé D, de Morais MB. Intestinal microbiota and allergic diseases: a systematic review. Allergol Immunopathol (Madr). 2016;44:177-88, http://dx.doi.org/10.1016/j.aller.2015.01.013 [PMID: 25985709].
26. Zheng H, Liang H, Wang Y, Miao M, Shi T, Yang F, et al. Altered gut microbiota composition associated with eczema in infants. PLOS ONE. 2016;11:e0166026, http://dx.doi.org/10.1371/journal.pone.0166026 [PMID: 27812181].
27. Szachta P, Bartnicka A, Gałecka ˛ M. Microbiota - a key to healing the gastrointestinal tract? Pomeranian J Life Sci. 2016;62:21-4 [PMID: 29533578].
28. Le Bastard Q, Ward T, Sidiropoulos D, Hillmann BM, Chun CL, Sadowsky MJ, et al. Fecal microbiota transplantation reverses antibiotic and chemotherapy-induced gut dysbiosis in mice. Sci Rep. 2018;18:6219, http://dx.doi.org/10.1038/s41598-018-24342-x [PMID: 29670191].
29. Sokol H, Pigneur B, Watterlot L, Lakhdari O, BermúdezHumarán LG, Gratadoux JJ, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA. 2008;105:1673, http://dx.doi.org/10.1073/pnas.0804812105 [PMID: 18936492].
30. Murai M, Turovskaya O, Kim G, Madan R, Karp CL, Cheroutre H, et al. Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat Immunol. 2009;10:1178e84, http://dx.doi.org/10.1038/ni.1791 [PMID: 19783988].
31. Martín R, Miquel S, Ulmer J, Kechaou N, Langella P, Bermudez-Humaran LG. Role of commensal and probiotic bacteria in human health: a focus on inflammatory bowel disease. Microb Cell Fact. 2013;12:71, http://dx.doi.org/10.1186/1475-2859-12-71 [PMID: 23876056].
32. Quevrain E, Maubert MA, Michon C, Chain F, Marquant R, Tailhades J, et al. Identification of an anti-inflammatory protein from Faecalibacterium prausnitzii, a commensal bacterium deficient in Crohn’s disease. Gut. 2016;65:415-25, http://dx.doi.org/10.1136/gutjnl-2014-307649 [PMID: 26045134].
33. Geerlings SY, Kostopoulos I, de Vos WM, Belzer C. Akkermansia muciniphila in the Human Gastrointestinal Tract: When, Where, and How? Microorganisms. 2018;23:E75, http://dx.doi.org/10.3390/microorganisms6030075 [PMID: 30041463].
34. Png CW, Lindén SK, Gilshenan KS, Zoetendal EG, McSweeney CS, Sly LI, et al. Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol. 2010;105:2420-8, http://dx.doi.org/10.1038/ajg.2010.281 [PMID: 20648002].
35. Ottman N, Reunanen J, Meijerink M, Pietilä TE, Kainulainen V, Klievink J, et al. Pili-like proteins of Akkermansia muciniphila modulate host immune responses and gut barrier function. PLOS ONE. 2017;12:e0173004, http://dx.doi.org/10.1371/journal.pone.0173004 [PMID: 28249045].
36. Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci USA. 2010;107:12204-9, http://dx.doi.org/10.1073/pnas.0909122107 [PMID: 20566854].
37. Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504:446-50, http://dx.doi.org/10.1038/nature12721 [PMID: 24226770].
38. Fujimura KE, Sitarik AR, Havstad S, Lin LD, Levan S, Fadrosh D, et al. Neonatal gut microbiota associates with childhood multisensitized atopy and T cell differentiation. Nat Med. 2016;22:1187-91, http://dx.doi.org/10.1038/nm.4176 [PMID: 27618652].
39. Molloy J, Allen K, Collier F, Tang ML, Ward AC, Vuillermin P:. The potential link between gut microbiota and IgE-mediated food allergy in early life. Int J Environ Res Public Health. 2013;10:7235-56, http://dx.doi.org/10.3390/ijerph10127235 [PMID: 24351744].
2. Andersen YMF, Egeberg A, Skov L, Thyssen JP. Comorbidities of atopic dermatitis: beyond rhinitis and asthma. Curr Dermatol Rep. 2017;6:35-41, http://dx.doi.org/10.1007/s13671-017-0168-7 [PMID: 28890845].
3. Ober C, Yao T-C. The genetics of asthma and allergic disease: a 21st-century perspective. Immunol rev. 2011;242:10-30, http://dx.doi.org/10.1111/j.1600-065X. 2011.01029.x [PMID: 21682736].
4. Piacentini S, Polimanti R, Moscatelli B, Re MA, Manfellotto D, Fuciarelli M, et al. Lack of association between GSTM1 GSTP1, and GSTT1 gene polymorphisms and asthma in adult patients from Rome, central Italy. J Investig Allergol Clin Immunol. 2012;22:252-6 [PMID: 22812193].
5. Koga Y, Tokunaga S, Nagano J, Sato F, Konishi K. Age-associated effect of kestose on Faecalibacterium prausnitzii and symptoms in the atopic dermatitis infants. Pediatr Res. 2016;80:844-51, http://dx.doi.org/10.1038/pr.2016.167 [PMID: 27537603].
6. Miquel S, Martín R, Rossi O, Bermúdez-Humarán LG, Chatel JM, Sokol H, et al. Faecalibacterium prausnitzii and human intestinal health. Curr Opin Microbiol. 2013;16:255-61, http://dx.doi.org/10.1016/j.mib.2013.06.003 [PMID: 23831042].
7. Tsuda A, Suda W, Morita H. Influence of Proton-Pump Inhibitors on the Luminal Microbiota in the Gastrointestinal Tract. Clin Transl Gastroenterol. 2015;6:e89, http://dx.doi.org/10.1038/ctg.2015.20 [PMID: 26065717].
8. Gałecka M, Szachta P, Bartnicka A, Łykowska-Szuber L, Eder P, Schwiertz A. Faecalibacterium prausnitzii and Crohn’s disease- is there any connection? Pol J Microbiol. 2013;62:91-5 [PMID: 23829084].
9. Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, Beaugerie L, et al. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis. 2009;15:1183-9, http://dx.doi.org/10.1002/ibd.20903 [PMID: 19235886].
10. Song H, Yoo Y, Hwang J, Na YC, Kim HS. Faecalibacterium prausnitzii subspecies-level dysbiosis in the human gut microbiome underlying atopic dermatitis. J Allergy Clin Immunol. 2016;137:852-60, http://dx.doi.org/10.1016/j.jaci.2015.08.021 [PMID: 26431583].
11. Nabizadeh E, Jazani NH, Bagheri M, Shahabi S. Association of altered gut microbiota composition with chronic urticaria. Ann Allergy Asthma Immunol. 2017;119:48-53, http://dx.doi.org/10.1016/j.anai.2017.05.006 [PMID: 28668239].
12. Candela M, Rampelli S, Turroni S, Severgnini M, Consolandi C, De Bellis G, et al. Unbalance of intestinal microbiota in atopic children. BMC Microbiol. 2012;12:95, http://dx.doi.org/10.1186/1471-2180-12-95 [PMID: 22672413].
13. Duncan SH, Hold GL, Harmsen HJ, Stewart CS, Flint HJ. Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as Faecalibacterium prausnitzii gen. nov., comb. nov. Int J Syst Evol Microbiol. 2002;52:2141-6, http://dx.doi.org/10.1099/00207713-52-6-2141 [PMID: 12508881].
14. Cani PD, de Vos WM. Next-generation beneficial microbes: the case of Akkermansia muciniphila. Front Microbiol. 2017;8:1765, http://dx.doi.org/10.3389/fmicb.2017.01765 [PMID: 29018410].
15. Lukovac S, Belzer C, Pellis L, Keijser BJ, de Vos WM, Montijn RC, et al. Differential modulation by Akkermansia muciniphila and Faecalibacterium prausnitzii of host peripheral lipid metabolism and histone acetylation in mouse gut organoids. mBio. 2014;5:e01438-1514, http://dx.doi.org/10.1128/mBio.01438-14 [PMID: 25118238].
16. National Asthma Education and Prevention Program. Expert Panel Report 3 (EPR-3): Guidelines for the Diagnosis and Management of Asthma-Summary Report 2007. J Allergy Clin Immunol. 2007;120:S94-138, http://dx.doi.org/10.1016/j.jaci.2007.09.043 [PMID: 17983880].
17. Strachan DP. Family size, infection and atopy: the first decade of the ‘‘hygiene hypothesis’’. Thorax. 2000;55:S2-10, http://dx.doi.org/10.1136/thorax.55.suppl 1.S2 [PMID: 10943631].
18. Karakullukcu A, Tokman HB, Nepesov S, Demirci M, Saribas S. The protective role of Helicobacter pylori neutrophil-activating protein in childhood asthma. Allergol Immunopathol (Madr). 2017;45:521-7, http://dx.doi.org/10.1016/j.aller.2017.01.008 [PMID: 28579087].
19. Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system. Science. 2012;336:1268-73, http://dx.doi.org/10.1126/science.1223490 [PMID: 22674334].
20. Fieten KB, Totté JEE, Levin E, Reyman M, Meijer Y, Knulst A, et al. Fecal microbiome and food allergy in pediatric atopic dermatitis: a cross-sectional pilot study. Int Arch Allergy Immunol. 2018;175:77-84, http://dx.doi.org/10.1159/000484897 [PMID: 29393195].
21. Egert M, de Graaf AA, Smidt H, de Vos WM, Venema K. Beyond diversity: functional microbiomics of the human colon. Trends Microbiol. 2006;14:86-91, http://dx.doi.org/10.1016/j.tim.2005.12.007 [PMID: 16406528].
22. Louis P, Flint HJ. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett. 2009;294:1-8, http://dx.doi.org/10.1111/j.1574-6968.2009.01514.x [PMID: 19222573].
23. Kabeerdoss J, Sankaran V, Pugazhendhi S, Ramakrishna BS. Clostridium leptum group bacteria abundance and diversity in the fecal microbiota of patients with inflammatory bowel disease: a case-control study in India. BMC Gastroenterol. 2013;26:20, http://dx.doi.org/10.1186/1471-230X-13-20 [PMID: 23351032].
24. Scheppach W, Weiler F. The butyrate story: old wine in new bottles? Curr Opin Clin Nutr Metab Care. 2004;7:563-7 [PMID: 15295277].
25. Melli LC, do Carmo-Rodrigues MS, Araújo-Filho HB, Solé D, de Morais MB. Intestinal microbiota and allergic diseases: a systematic review. Allergol Immunopathol (Madr). 2016;44:177-88, http://dx.doi.org/10.1016/j.aller.2015.01.013 [PMID: 25985709].
26. Zheng H, Liang H, Wang Y, Miao M, Shi T, Yang F, et al. Altered gut microbiota composition associated with eczema in infants. PLOS ONE. 2016;11:e0166026, http://dx.doi.org/10.1371/journal.pone.0166026 [PMID: 27812181].
27. Szachta P, Bartnicka A, Gałecka ˛ M. Microbiota - a key to healing the gastrointestinal tract? Pomeranian J Life Sci. 2016;62:21-4 [PMID: 29533578].
28. Le Bastard Q, Ward T, Sidiropoulos D, Hillmann BM, Chun CL, Sadowsky MJ, et al. Fecal microbiota transplantation reverses antibiotic and chemotherapy-induced gut dysbiosis in mice. Sci Rep. 2018;18:6219, http://dx.doi.org/10.1038/s41598-018-24342-x [PMID: 29670191].
29. Sokol H, Pigneur B, Watterlot L, Lakhdari O, BermúdezHumarán LG, Gratadoux JJ, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA. 2008;105:1673, http://dx.doi.org/10.1073/pnas.0804812105 [PMID: 18936492].
30. Murai M, Turovskaya O, Kim G, Madan R, Karp CL, Cheroutre H, et al. Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat Immunol. 2009;10:1178e84, http://dx.doi.org/10.1038/ni.1791 [PMID: 19783988].
31. Martín R, Miquel S, Ulmer J, Kechaou N, Langella P, Bermudez-Humaran LG. Role of commensal and probiotic bacteria in human health: a focus on inflammatory bowel disease. Microb Cell Fact. 2013;12:71, http://dx.doi.org/10.1186/1475-2859-12-71 [PMID: 23876056].
32. Quevrain E, Maubert MA, Michon C, Chain F, Marquant R, Tailhades J, et al. Identification of an anti-inflammatory protein from Faecalibacterium prausnitzii, a commensal bacterium deficient in Crohn’s disease. Gut. 2016;65:415-25, http://dx.doi.org/10.1136/gutjnl-2014-307649 [PMID: 26045134].
33. Geerlings SY, Kostopoulos I, de Vos WM, Belzer C. Akkermansia muciniphila in the Human Gastrointestinal Tract: When, Where, and How? Microorganisms. 2018;23:E75, http://dx.doi.org/10.3390/microorganisms6030075 [PMID: 30041463].
34. Png CW, Lindén SK, Gilshenan KS, Zoetendal EG, McSweeney CS, Sly LI, et al. Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol. 2010;105:2420-8, http://dx.doi.org/10.1038/ajg.2010.281 [PMID: 20648002].
35. Ottman N, Reunanen J, Meijerink M, Pietilä TE, Kainulainen V, Klievink J, et al. Pili-like proteins of Akkermansia muciniphila modulate host immune responses and gut barrier function. PLOS ONE. 2017;12:e0173004, http://dx.doi.org/10.1371/journal.pone.0173004 [PMID: 28249045].
36. Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci USA. 2010;107:12204-9, http://dx.doi.org/10.1073/pnas.0909122107 [PMID: 20566854].
37. Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504:446-50, http://dx.doi.org/10.1038/nature12721 [PMID: 24226770].
38. Fujimura KE, Sitarik AR, Havstad S, Lin LD, Levan S, Fadrosh D, et al. Neonatal gut microbiota associates with childhood multisensitized atopy and T cell differentiation. Nat Med. 2016;22:1187-91, http://dx.doi.org/10.1038/nm.4176 [PMID: 27618652].
39. Molloy J, Allen K, Collier F, Tang ML, Ward AC, Vuillermin P:. The potential link between gut microbiota and IgE-mediated food allergy in early life. Int J Environ Res Public Health. 2013;10:7235-56, http://dx.doi.org/10.3390/ijerph10127235 [PMID: 24351744].
Article Sidebar
Published
Aug 15, 2019
Article Details
How to Cite
Demirci, M., Tokman, H., Uysal, H., Demiryas, S., Karakullukcu, A., Saribas, S., Cokugras, H., & Kocazeybek, B. (2019). Reduced Akkermansia muciniphila and Faecalibacterium prausnitzii levels in the gut microbiota of children with allergic asthma. Allergologia Et Immunopathologia, 47(4), 365-371. https://www.all-imm.com/index.php/aei/article/view/306
Issue
Section
Original Articles
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
How to Cite
Demirci, M., Tokman, H., Uysal, H., Demiryas, S., Karakullukcu, A., Saribas, S., Cokugras, H., & Kocazeybek, B. (2019). Reduced Akkermansia muciniphila and Faecalibacterium prausnitzii levels in the gut microbiota of children with allergic asthma. Allergologia Et Immunopathologia, 47(4), 365-371. https://www.all-imm.com/index.php/aei/article/view/306