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Mild intermittent hypoxia exposure alters gut microbiota composition in men with overweight and obesity
in Beneficial MicrobesSearch for other papers by R.L.J. Van Meijel in
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Centre for Healthy Eating & Food Innovation (HEFI), Maastricht University – Campus Venlo, St. Jansweg 20, 5928 RC Venlo, the Netherlands.
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Results from high altitude studies in humans and controlled animal experiments suggest that hypoxia exposure induces alterations in gut microbiota composition, which may in turn affect host metabolism. However, well-controlled studies investigating the effects of normobaric hypoxia exposure on gut microbiota composition in humans are lacking. The aim of this study was to explore the impact of mild intermittent hypoxia (MIH) exposure on gut microbiota composition in men with overweight and/or obesity. We performed a randomised, single-blind crossover study, in which participants were exposed to MIH (FiO2: 15%, 3×2 h per day) and normoxia (FiO2: 21%) for seven consecutive days. Following the MIH and normoxia exposure regimens, faecal samples were collected for determination of faecal microbiota composition using 16S rRNA gene-amplicon sequencing in the morning of day 8. Paired faecal samples were available for five individuals. Furthermore, tissue-specific insulin sensitivity was determined using the gold-standard two-step hyperinsulinemic-euglycemic clamp. MIH did not affect microbial alpha and beta-diversity but reduced the relative abundance of Christensenellaceae and Clostridiaceae bacterial families. MIH significantly increased the abundances of obligate anaerobic bacterial genera including Fusicatenibacter, Butyricicoccus and Holdemania, whilst reducing Christensenellaceae R-7 group and Clostridium sensu stricto 1, although these findings were not statistically significant after correction for multiple testing. Furthermore, MIH-induced alterations in abundances of several genera were associated with changes in metabolic parameters such as adipose and peripheral insulin sensitivity, plasma levels of insulin, fatty acids, triacylglycerol and lactate, and substrate oxidation. In conclusion, we demonstrate for the first time that MIH exposure induces modest effects on faecal microbiota composition in humans, shifting several bacterial families and genera towards higher abundances of anaerobic butyrate-producing bacteria. Moreover, MIH-induced effects on faecal microbial composition were associated with parameters related to glucose and lipid homeostasis, supporting a link between MIH-induced alterations in faecal microbiota composition and host metabolism.
The study was registered at the Netherlands Trial Register: NL7120/NTR7325.
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-
Allegretti, J.R., Mullish, B.H., Kelly, C. and Fischer, M., 2019. The evolution of the use of faecal microbiota transplantation and emerging therapeutic indications. The Lancet 394: 420-431. https://doi.org/10.1016/S0140-6736(19)31266-8
-
Anderson, M.J., 2017. Permutational Multivariate Analysis of Variance (PERMANOVA). In: Balakrishnan, N., Colton, T., Everitt, B., Piegorsch, W., Ruggeri, F. and Teugels, J.L. (eds.), Wiley StatsRef: Statistics Reference Online. Wiley, Hoboken, NJ, USA.
'Permutational Multivariate Analysis of Variance (PERMANOVA)', ().
-
Belkaid, Y. and Hand, T.W., 2014. Role of the microbiota in immunity and inflammation. Cell 157: 121-141. https://doi.org/10.1016/j.cell.2014.03.011
-
Canfora, E.E., Meex, R.C.R., Venema, K. and Blaak, E.E., 2019. Gut microbial metabolites in obesity, NAFLD and T2DM. Nature Reviews Endocrinology 15: 261-273. https://doi.org/10.1038/s41574-019-0156-z
-
Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Pena, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., Lozupone, C.A., McDonald, D., Muegge, B.D., Pirrung, M., Reeder, J., Sevinsky, J.R., Turnbaugh, P.J., Walters, W.A., Widmann, J., Yatsunenko, T., Zaneveld, J. and Knight, R., 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7: 335-336. https://doi.org/10.1038/nmeth.f.303
-
Contreras-Davila, C.A., Carrion, V.J., Vonk, V.R., Buisman, C.N.J. and Strik, D., 2020. Consecutive lactate formation and chain elongation to reduce exogenous chemicals input in repeated-batch food waste fermentation. Water Research 169: 115215. https://doi.org/10.1016/j.watres.2019.115215
-
Gerard, C. and Vidal, H., 2019. Impact of gut microbiota on host glycemic control. Frontiers in Endocrinology 10: 29. https://doi.org/10.3389/fendo.2019.00029
-
Goossens, G.H., Bizzarri, A., Venteclef, N., Essers, Y., Cleutjens, J.P., Konings, E., Jocken, J.W., Cajlakovic, M., Ribitsch, V., Clement, K. and Blaak, E.E., 2011. Increased adipose tissue oxygen tension in obese compared with lean men is accompanied by insulin resistance, impaired adipose tissue capillarization, and inflammation. Circulation 124: 67-76. https://doi.org/10.1161/CIRCULATIONAHA.111.027813
-
He, G., Shankar, R.A., Chzhan, M., Samouilov, A., Kuppusamy, P. and Zweier, J.L., 1999. Noninvasive measurement of anatomic structure and intraluminal oxygenation in the gastrointestinal tract of living mice with spatial and spectral EPR imaging. Proceedings of the National Academy of Sciences of the USA 96: 4586-4591. https://doi.org/10.1073/pnas.96.8.4586
-
Karl, J.P., Berryman, C.E., Young, A.J., Radcliffe, P.N., Branck, T.A., Pantoja-Feliciano, I.G., Rood, J.C. and Pasiakos, S.M., 2018. Associations between the gut microbiota and host responses to high altitude. American Journal of Physiology – Gastrointestinal and Liver Physiology 315: G1003-G1015. https://doi.org/10.1152/ajpgi.00253.2018
-
Khan, I., Ullah, N., Zha, L., Bai, Y., Khan, A., Zhao, T., Che, T. and Zhang, C., 2019. Alteration of gut microbiota in inflammatory bowel disease (IBD): cause or consequence? IBD treatment targeting the gut microbiome. Pathogens 8: 126. https://doi.org/10.3390/pathogens8030126
-
Li, L. and Zhao, X., 2015. Comparative analyses of fecal microbiota in Tibetan and Chinese Han living at low or high altitude by barcoded 454 pyrosequencing. Scientific Reports 5: 14682. https://doi.org/10.1038/srep14682
-
Marietta, E.V., Gomez, A.M., Yeoman, C., Tilahun, A.Y., Clark, C.R., Luckey, D.H., Murray, J.A., White, B.A., Kudva, Y.C. and Rajagopalan, G., 2013. Low incidence of spontaneous type 1 diabetes in non-obese diabetic mice raised on gluten-free diets is associated with changes in the intestinal microbiome. PLoS ONE 8: e78687. https://doi.org/10.1371/journal.pone.0078687
-
Markowiak, P. and Slizewska, K., 2017. Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients 9: 1021. https://doi.org/10.3390/nu9091021
-
Martin, A.M., Sun, E.W., Rogers, G.B. and Keating, D.J., 2019. The influence of the gut microbiome on host metabolism through the regulation of gut hormone release. Frontiers in Physiology 10: 428. https://doi.org/10.3389/fphys.2019.00428
-
Mazel, F., 2019. Living the high life: could gut microbiota matter for adaptation to high altitude? Molecular Ecology 28: 2119-2121. https://doi.org/10.1111/mec.15093
-
Moreno-Indias, I., Sanchez-Alcoholado, L., Garcia-Fuentes, E., Cardona, F., Queipo-Ortuno, M.I. and Tinahones, F.J., 2016. Insulin resistance is associated with specific gut microbiota in appendix samples from morbidly obese patients. American Journal of Translational Research 8: 5672-5684.
'Insulin resistance is associated with specific gut microbiota in appendix samples from morbidly obese patients ' () 8 American Journal of Translational Research : 5672 -5684.
-
Moreno-Indias, I., Torres, M., Montserrat, J.M., Sanchez-Alcoholado, L., Cardona, F., Tinahones, F.J., Gozal, D., Poroyko, V.A., Navajas, D., Queipo-Ortuno, M.I. and Farre, R., 2015. Intermittent hypoxia alters gut microbiota diversity in a mouse model of sleep apnoea. European Respiratory Journal 45: 1055-1065. https://doi.org/10.1183/09031936.00184314
-
Murphy, R., Tsai, P., Jullig, M., Liu, A., Plank, L. and Booth, M., 2017. Differential changes in gut microbiota after gastric bypass and sleeve gastrectomy bariatric surgery vary according to diabetes remission. Obesity Surgery 27: 917-925. https://doi.org/10.1007/s11695-016-2399-2
-
Peng, L., Li, Z.R., Green, R.S., Holzman, I.R. and Lin, J., 2009. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. Journal of Nutrition 139: 1619-1625. https://doi.org/10.3945/jn.109.104638
-
Rogers, G.B., Keating, D.J., Young, R.L., Wong, M.L., Licinio, J. and Wesselingh, S., 2016. From gut dysbiosis to altered brain function and mental illness: mechanisms and pathways. Molecular Psychiatry 21: 738-748. https://doi.org/10.1038/mp.2016.50
-
Sheridan, W.G., Lowndes, R.H. and Young, H.L., 1990. Intraoperative tissue oximetry in the human gastrointestinal tract. American Journal of Surgery 159: 314-319. https://doi.org/10.1016/s0002-9610(05)81226-7
-
Suski, M.D., Zabel, D., Levin, V., Scheuenstuhl, H. and Hunt, T.K., 1997. Effect of hypoxic hypoxia on transmural gut and subcutaneous tissue oxygen tension. Advances in Experimental Medicine and Biology 411: 319-322. https://doi.org/10.1007/978-1-4615-5865-1_39
-
Tian, Y.M., Guan, Y., Tian, S.Y., Yuan, F., Zhang, L. and Zhang, Y., 2018. Short-term chronic intermittent hypobaric hypoxia alters gut microbiota composition in rats. Biomedical and Environmental Sciences 31: 898-901. https://doi.org/10.3967/bes2018.122
-
Van Meijel, R.L.J., Vogel, M.A.A., Jocken, J.W.E., Vliex, L.M.M., Smeets, J.S.J., Hoebers, N., Hoeks, J., Essers, Y., Schoffelen, P.F.M., Sell, H., Kersten, S., K, M.A.R., Blaak, E.E. and Goossens, G.H., 2021. Mild intermittent hypoxia exposure induces metabolic and molecular adaptations in men with obesity. Molecular Metabolism 53: 101287. https://doi.org/10.1016/j.molmet.2021.101287
-
Vojinovic, D., Radjabzadeh, D., Kurilshikov, A., Amin, N., Wijmenga, C., Franke, L., Ikram, M.A., Uitterlinden, A.G., Zhernakova, A., Fu, J., Kraaij, R. and van Duijn, C.M., 2019. Relationship between gut microbiota and circulating metabolites in population-based cohorts. Nature Communications 10: 5813. https://doi.org/10.1038/s41467-019-13721-1
-
Yamashita, M., Okubo, H., Kobuke, K., Ohno, H., Oki, K., Yoneda, M., Tanaka, J. and Hattori, N., 2019. Alteration of gut microbiota by a Westernized lifestyle and its correlation with insulin resistance in non-diabetic Japanese men. Journal of Diabetes Investigation 10: 1463-1470. https://doi.org/10.1111/jdi.13048
-
Zheng, L., Kelly, C.J. and Colgan, S.P., 2015. Physiologic hypoxia and oxygen homeostasis in the healthy intestine. A review in the theme: cellular responses to hypoxia. American Journal of Physiology – Cell Physiology 309: C350-C360. https://doi.org/10.1152/ajpcell.00191.2015
-
Zhu, X., Zhou, Y., Wang, Y., Wu, T., Li, X., Li, D. and Tao, Y., 2017. Production of high-concentration n-caproic acid from lactate through fermentation using a newly isolated Ruminococcaceae bacterium CPB6. Biotechnology for Biofuels 10: 102. https://doi.org/10.1186/s13068-017-0788-y
Supplementary Materials
| Insgesamt | Letzte 365 Tage | In den letzten 30 Tagen | |
|---|---|---|---|
| Aufrufe von Kurzbeschreibungen | 1595 | 362 | 33 |
| Gesamttextansichten | 42 | 13 | 3 |
| PDF-Downloads | 60 | 22 | 4 |
Mild intermittent hypoxia exposure alters gut microbiota composition in men with overweight and obesity
in Beneficial MicrobesSearch for other papers by R.L.J. Van Meijel in
Current site
Google Scholar
PubMed
Centre for Healthy Eating & Food Innovation (HEFI), Maastricht University – Campus Venlo, St. Jansweg 20, 5928 RC Venlo, the Netherlands.
Search for other papers by K. Venema in
Current site
Google Scholar
PubMed
Search for other papers by E.E. Canfora in
Current site
Google Scholar
PubMed
Search for other papers by E.E. Blaak in
Current site
Google Scholar
PubMed
Search for other papers by G.H. Goossens in
Current site
Google Scholar
PubMed
Results from high altitude studies in humans and controlled animal experiments suggest that hypoxia exposure induces alterations in gut microbiota composition, which may in turn affect host metabolism. However, well-controlled studies investigating the effects of normobaric hypoxia exposure on gut microbiota composition in humans are lacking. The aim of this study was to explore the impact of mild intermittent hypoxia (MIH) exposure on gut microbiota composition in men with overweight and/or obesity. We performed a randomised, single-blind crossover study, in which participants were exposed to MIH (FiO2: 15%, 3×2 h per day) and normoxia (FiO2: 21%) for seven consecutive days. Following the MIH and normoxia exposure regimens, faecal samples were collected for determination of faecal microbiota composition using 16S rRNA gene-amplicon sequencing in the morning of day 8. Paired faecal samples were available for five individuals. Furthermore, tissue-specific insulin sensitivity was determined using the gold-standard two-step hyperinsulinemic-euglycemic clamp. MIH did not affect microbial alpha and beta-diversity but reduced the relative abundance of Christensenellaceae and Clostridiaceae bacterial families. MIH significantly increased the abundances of obligate anaerobic bacterial genera including Fusicatenibacter, Butyricicoccus and Holdemania, whilst reducing Christensenellaceae R-7 group and Clostridium sensu stricto 1, although these findings were not statistically significant after correction for multiple testing. Furthermore, MIH-induced alterations in abundances of several genera were associated with changes in metabolic parameters such as adipose and peripheral insulin sensitivity, plasma levels of insulin, fatty acids, triacylglycerol and lactate, and substrate oxidation. In conclusion, we demonstrate for the first time that MIH exposure induces modest effects on faecal microbiota composition in humans, shifting several bacterial families and genera towards higher abundances of anaerobic butyrate-producing bacteria. Moreover, MIH-induced effects on faecal microbial composition were associated with parameters related to glucose and lipid homeostasis, supporting a link between MIH-induced alterations in faecal microbiota composition and host metabolism.
The study was registered at the Netherlands Trial Register: NL7120/NTR7325.
| Insgesamt | Letzte 365 Tage | In den letzten 30 Tagen | |
|---|---|---|---|
| Aufrufe von Kurzbeschreibungen | 1595 | 362 | 33 |
| Gesamttextansichten | 42 | 13 | 3 |
| PDF-Downloads | 60 | 22 | 4 |
