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Review

The gut microbiome as a target for adjuvant therapy in obstructive sleep apnea

, &
Pages 1263-1282 | Received 01 Aug 2020, Accepted 21 Oct 2020, Published online: 04 Dec 2020

References

  • Remmers JE, DeGroot WJ, Sauerland EK, et al. Pathogenesis of upper airway occlusion during sleep. J Appl Physiol Respir Environ Exerc Physiol. 1978;44(6):931–938.
  • Young T, Palta M, Dempsey J, et al. Burden of sleep apnea: rationale, design, and major findings of the Wisconsin Sleep Cohort study. Wmj. 2009;108(5):246–249.
  • Burt VL, Cutler JA, Higgins M, et al. Trends in the prevalence, awareness, treatment, and control of hypertension in the adult US population. Data from the health examination surveys, 1960 to 1991. Hypertension. 1995;26(1):60–69.
  • Marshall NS, Wong KKH, Phillips CL, et al. Is sleep apnea an independent risk factor for prevalent and incident diabetes in the Busselton health study? J Clin Sleep Med. 2009;5(1):15–20.
  • Brunetti V, Ferilli MAN, Vollono C, et al. Sleep apneas trigger epilepsy. Sleep Med. 2017;39:23–24.
  • Xu W, Chi L, Row BW, et al. Increased oxidative stress is associated with chronic intermittent hypoxia-mediated brain cortical neuronal cell apoptosis in a mouse model of sleep apnea. Neuroscience. 2004;126(2):313–323.
  • Row BW, Liu R, Xu W, et al. Intermittent hypoxia is associated with oxidative stress and spatial learning deficits in the rat. Am J Respir Crit Care Med. 2003;167(11):1548–1553.
  • Kheirandish-Gozal L, Gozal D. Obstructive Sleep Apnea and Inflammation: proof of concept based on two illustrative cytokines. Int J Mol Sci. 2019;20(3):459.
  • Kheirandish-Gozal L, Gileles-Hillel A, Alonso-Alvarez ML, et al. Effects of adenotonsillectomy on plasma inflammatory biomarkers in obese children with obstructive sleep apnea: a community-based study. Int J Obes (Lond). 2015;39(7):1094–1100.
  • Neish AS. Microbes in gastrointestinal health and disease. Gastroenterology. 2009;136(1):65–80.
  • Kamada N, Seo S-U, Chen GY, et al. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol. 2013;13(5):321–335.
  • Bäckhed F, Ley RE, Sonnenburg JL, et al. Host-bacterial mutualism in the human intestine. Science. 2005;307(5717):1915–1920.
  • Natividad JM, Verdu EF. Modulation of intestinal barrier by intestinal microbiota: pathological and therapeutic implications. Pharmacol Res. 2013;69(1):42–51.
  • den Besten G, Van Eunen K, Groen AK, et al. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54(9):2325–2340.
  • Bäumler AJ, Sperandio V. Interactions between the microbiota and pathogenic bacteria in the gut. Nature. 2016;535(7610):85–93.
  • Gensollen T, Iyer SS, Kasper DL, et al. How colonization by microbiota in early life shapes the immune system. Science. 2016;352(6285):539–544.
  • Poroyko VA, Carreras A, Khalyfa A, et al. Chronic sleep disruption alters gut microbiota, induces systemic and adipose tissue inflammation and insulin resistance in mice. Sci Rep. 2016;6:35405.
  • Wu ZH, Tang Y, Niu X, et al. The role of nitric oxide (NO) levels in patients with obstructive sleep apnea-hypopnea syndrome: a meta-analysis. Sleep Breath. 2020. DOI:10.1007/s11325-020-02095-0.
  • Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464(7285):59–65.
  • Canani RB, Di Costanzo M, Leone L, et al. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J Gastroenterol. 2011;17(12):1519–1528.
  • Vinolo MA, Rodrigues HG, Nachbar RT, et al. Regulation of inflammation by short chain fatty acids. Nutrients. 2011;3(10):858–876.
  • Dominguez-Bello MG, Blaser MJ, Ley RE, et al. Development of the human gastrointestinal microbiota and insights from high-throughput sequencing. Gastroenterology. 2011;140(6):1713–1719.
  • Payne AN, Chassard C, Lacroix C. Gut microbial adaptation to dietary consumption of fructose, artificial sweeteners and sugar alcohols: implications for host-microbe interactions contributing to obesity. Obes Rev. 2012;13(9):799–809.
  • Moreno-Indias I, Torres M, Montserrat JM, et al. Intermittent hypoxia alters gut microbiota diversity in a mouse model of sleep apnoea. Eur Respir J. 2015;45(4):1055–1065.
  • de la Cuesta-zuluaga J, Corrales-Agudelo V, Velásquez-Mejía EP, et al. Gut microbiota is associated with obesity and cardiometabolic disease in a population in the midst of Westernization. Sci Rep. 2018;8(1):11356.
  • Scher JU, Sczesnak A, Longman RS, et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife. 2013;2:e01202.
  • Albenberg L, Esipova TV, Judge CP, et al. Correlation between intraluminal oxygen gradient and radial partitioning of intestinal microbiota. Gastroenterology. 2014;147(5):1055–63.e8.
  • Farre R, Montserrat JM, Gozal D, et al. Intermittent hypoxia severity in animal models of sleep apnea. Front Physiol. 2018;9:1556.
  • Schoorlemmer GH, Rossi MV, Tufik S, et al. A new method to produce obstructive sleep apnoea in conscious unrestrained rats. Exp Physiol. 2011;96(10):1010–1018.
  • Crossland RF, Durgan DJ, Lloyd EE, et al. A new rodent model for obstructive sleep apnea: effects on ATP-mediated dilations in cerebral arteries. Am J Physiol Regul Integr Comp Physiol. 2013;305(4):R334–42.
  • Carreras A, Wang Y, Gozal D, et al. Non-invasive system for applying airway obstructions to model obstructive sleep apnea in mice. Respir Physiol Neurobiol. 2011;175(1):164–168.
  • Benedict C, Vogel H, Jonas W, et al. Gut microbiota and glucometabolic alterations in response to recurrent partial sleep deprivation in normal-weight young individuals. Mol Metab. 2016;5(12):1175–1186.
  • Reutrakul S, So-ngern A, Chirakalwasan N, et al. No changes in gut microbiota after two-week sleep extension in chronically sleep-deprived individuals. Sleep Med. 2020;68:27–30.
  • Matenchuk BA, Mandhane PJ, Kozyrskyj AL. Sleep, circadian rhythm, and gut microbiota. Sleep Med Rev. 2020;53:101340.
  • Mashaqi S, Gozal D. “Circadian misalignment and the gut microbiome. A bidirectional relationship triggering inflammation and metabolic disorders”- a literature review. Sleep Med. 2020;72:93–108.
  • Reynolds AC, Paterson JL, Ferguson SA, et al. The shift work and health research agenda: considering changes in gut microbiota as a pathway linking shift work, sleep loss and circadian misalignment, and metabolic disease. Sleep Med Rev. 2017;34:3–9.
  • Chaffron S, Rehrauer H, Pernthaler J, et al. A global network of coexisting microbes from environmental and whole-genome sequence data. Genome Res. 2010;20(7):947–959.
  • Faust K, Sathirapongsasuti JF, Izard J, et al. Microbial co-occurrence relationships in the human microbiome. PLoS Comput Biol. 2012;8(7):e1002606.
  • Sharpton TJ. An introduction to the analysis of shotgun metagenomic data. Front Plant Sci. 2014;5:209.
  • Nelson KE, Weinstock GM, Highlander SK, et al. A catalog of reference genomes from the human microbiome. Science. 2010;328(5981):994–999.
  • Fiehn O. Metabolomics–the link between genotypes and phenotypes. Plant Mol Biol. 2002;48(1–2):155–171.
  • Liu J, Li T, Wu H, et al. Lactobacillus rhamnosus GG strain mitigated the development of obstructive sleep apnea-induced hypertension in a high salt diet via regulating TMAO level and CD4+ T cell induced-type I inflammation. Biomed Pharmacother. 2019;112:108580.
  • Tripathi A, Xu ZZ, Xue J, et al. Intermittent hypoxia and hypercapnia reproducibly change the gut microbiome and metabolome across rodent model systems. mSystems. 2019;4(2). DOI:10.1128/mSystems.00058-19.
  • O’Connor KM, Lucking EF, Cryan JF, et al. Bugs, breathing and blood pressure: microbiota-gut-brain axis signalling in cardiorespiratory control in health and disease. J Physiol. 2020 Jul 11. doi: 10.1113/JP280279. Epub ahead of print. PMID: 32652603.
  • Moreno-Indias I, Torres M, Sanchez-Alcoholado L, et al. Normoxic recovery mimicking treatment of sleep apnea does not reverse intermittent hypoxia-induced bacterial dysbiosis and low-grade endotoxemia in mice. Sleep. 2016;39(10):1891–1897.
  • Lucking EF, O’Connor KM, Strain CR, et al. Chronic intermittent hypoxia disrupts cardiorespiratory homeostasis and gut microbiota composition in adult male guinea-pigs. EBioMedicine. 2018;38:191–205.
  • Durgan DJ, Ganesh BP, Cope JL, et al. Role of the gut microbiome in obstructive sleep apnea-induced hypertension. Hypertension. 2016;67(2):469–474.
  • Almendros I, Farre N. Obstructive sleep apnea and atherosclerosis: both the gut microbiome and hypercapnia matter. Am J Respir Cell Mol Biol. 2017;57(5):501–503.
  • Xue J, Zhou D, Poulsen O, et al. Intermittent hypoxia and hypercapnia accelerate atherosclerosis, partially via trimethylamine-oxide. Am J Respir Cell Mol Biol. 2017;57(5):581–588.
  • Turnbull CD, Lee LYW, Starkey T, et al. Transcriptomics identify a unique intermittent hypoxia-mediated profile in obstructive sleep apnea. Am J Respir Crit Care Med. 2020;201(2):247–250.
  • Sanderson JE, Fang F, Wei Y. Obstructive sleep apnoea and inflammation in age-dependent cardiovascular disease. Eur Heart J. 2020;41(26):2503.
  • Campos-Rodriguez F, Cordero-Guevara J, Asensio-Cruz MI, et al. Interleukin 6 as a marker of depression in women with sleep apnea. J Sleep Res. 2020;e13035. doi:10.1111/jsr.13035
  • Arnaud C, Bochaton T, Pépin J-L, et al. Obstructive sleep apnoea and cardiovascular consequences: pathophysiological mechanisms. Arch Cardiovasc Dis. 2020;113(5):350–358.
  • Wali SO, AL-Mughales J, Alhejalli F, et al. The utility of proinflammatory markers in patients with obstructive sleep apnea. Sleep Breath. 2020. DOI:10.1007/s11325-020-02149-3.
  • Kheirandish-Gozal L, Peris E, Wang Y, et al. Lipopolysaccharide-binding protein plasma levels in children: effects of obstructive sleep apnea and obesity. J Clin Endocrinol Metab. 2014;99(2):656–663.
  • Collado MC, Katila MK, Vuorela NM, et al. Dysbiosis in snoring children: an interlink to comorbidities? J Pediatr Gastroenterol Nutr. 2018 Feb;68(2):272-277. doi: 10.1097/MPG.0000000000002161. PMID: 30289820..
  • Lu D, Yao X, Abulimiti A, et al. Profiling of lung microbiota in the patients with obstructive sleep apnea. Medicine (Baltimore). 2018;97(26):e11175.
  • Wu BG, Sulaiman I, Wang J, et al. Severe obstructive sleep apnea is associated with alterations in the nasal microbiome and increase in inflammation. Am J Respir Crit Care Med. 2019 Jan 1;199(1):99-109. doi: 10.1164/rccm.201801-0119OC. PMID: 29969291; PMCID: PMC6353011.
  • Ko CY, Fan J-M, Hu A-K, et al. Disruption of sleep architecture in Prevotella enterotype of patients with obstructive sleep apnea-hypopnea syndrome. Brain Behav. 2019;9(5):e01287.
  • Ko CY, Liu -Q-Q, Su H-Z, et al. Gut microbiota in obstructive sleep apnea-hypopnea syndrome: disease-related dysbiosis and metabolic comorbidities. Clin Sci (Lond). 2019;133(7):905–917.
  • Butel MJ. Probiotics, gut microbiota and health. Med Mal Infect. 2014;44(1):1–8.
  • Fijan S. Microorganisms with claimed probiotic properties: an overview of recent literature. Int J Environ Res Public Health. 2014;11(5):4745–4767.
  • El Aidy S, Dinan TG, Cryan JF. Gut microbiota: the conductor in the orchestra of immune-neuroendocrine communication. Clin Ther. 2015;37(5):954–967.
  • Patterson E, Ryan PM, Cryan JF, et al. Gut microbiota, obesity and diabetes. Postgrad Med J. 2016;92(1087):286–300.
  • Bermudez-Brito M, Plaza-Díaz J, Muñoz-Quezada S, et al. Probiotic mechanisms of action. Ann Nutr Metab. 2012;61(2):160–174.
  • Gibson GR, Hutkins R, Sanders ME, et al. Expert consensus document: the international scientific association for probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol. 2017;14(8):491–502.
  • Bindels LB, Delzenne NM, Cani PD, et al. Towards a more comprehensive concept for prebiotics. Nat Rev Gastroenterol Hepatol. 2015;12(5):303–310.
  • Douellou T, Montel MC, Thevenot Sergentet D. Invited review: anti-adhesive properties of bovine oligosaccharides and bovine milk fat globule membrane-associated glycoconjugates against bacterial food enteropathogens. J Dairy Sci. 2017;100(5):3348–3359.
  • Gibson GR, Probert HM, Van Loo J, et al. Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev. 2004;17(2):259–275.
  • McLoughlin RF, Berthon BS, Jensen ME, et al. Short-chain fatty acids, prebiotics, synbiotics, and systemic inflammation: a systematic review and meta-analysis. Am J Clin Nutr. 2017;106(3):930–945.
  • Stelmach-Mardas M, Mardas M, Iqbal K, et al. Dietary and cardio-metabolic risk factors in patients with Obstructive Sleep Apnea: cross-sectional study. PeerJ. 2017;5:e3259.
  • Flora GD, Nayak MK. A brief review of cardiovascular diseases, associated risk factors and current treatment regimes. Curr Pharm Des. 2019;25(38):4063–4084.
  • Sanchez-Rodriguez E, Egea-Zorrilla A, Plaza-Díaz J, et al. The gut microbiota and its implication in the development of atherosclerosis and related cardiovascular diseases. Nutrients. 2020;12(3):605.
  • Tang WHW, Bäckhed F, Landmesser U, et al. Intestinal microbiota in cardiovascular health and disease: JACC state-of-the-art review. J Am Coll Cardiol. 2019;73(16):2089–2105.
  • Libby P, Buring JE, Badimon L, et al. Atherosclerosis. Nat Rev Dis Primers. 2019;5(1):56. doi: 10.1038/s41572-019-0106-z. PMID: 31420554.
  • Ufnal M, Zadlo A, Ostaszewski R. TMAO: A small molecule of great expectations. Nutrition. 2015;31(11–12):1317–1323.
  • O’Morain VL, Ramji DP. The potential of probiotics in the prevention and treatment of atherosclerosis. Mol Nutr Food Res. 2020;64(4):e1900797.
  • Parada Venegas D, De la Fuente MK, Landskron G, et al. Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol. 2019;10:277.
  • Badran M, Ayas N, Laher I. Insights into obstructive sleep apnea research. Sleep Med. 2014;15(5):485–495.
  • Yacoub M, Youssef I, Salifu MO, et al. Cardiovascular disease risk in obstructive sleep apnea: an update. J Sleep Disord Ther. 2017;7(1):283.doi:10.4172/2167-0277.1000283. Epub 2018 Feb 12. PMID: 29644149; PMCID: PMC5891150.
  • Zheng HJ, Guo J, Wang Q, et al. Probiotics, prebiotics, and synbiotics for the improvement of metabolic profiles in patients with chronic kidney disease: a systematic review and meta-analysis of randomized controlled trials. Crit Rev Food Sci Nutr. 2020 Apr 24;1–22.doi:10.1080/10408398.2020.1740645. Epub ahead of print. PMID: 32329633.
  • Zheng HJ, Guo J, Jia Q, et al. The effect of probiotic and synbiotic supplementation on biomarkers of inflammation and oxidative stress in diabetic patients: A systematic review and meta-analysis of randomized controlled trials. Pharmacol Res. 2019;142:303–313.
  • Mo R, Zhang X, Yang Y. Effect of probiotics on lipid profiles in hypercholesterolaemic adults: a meta-analysis of randomized controlled trials. Med Clin (Barc). 2019;152(12):473–481.
  • Zhang K, Chen X, Zhang L, et al. Fermented dairy foods intake and risk of cardiovascular diseases: a meta-analysis of cohort studies. Crit Rev Food Sci Nutr. 2020;60(7):1189–1194.
  • Freeman AM, Morris PB, Aspry K, et al. A clinician’s guide for trending cardiovascular nutrition controversies: part II. J Am Coll Cardiol. 2018;72(5):553–568.
  • Majewska K, Kręgielska-Narożna M, Jakubowski H, et al. The multispecies probiotic effectively reduces homocysteine concentration in obese women: a randomized double-blind placebo-controlled study. J Clin Med. 2020;9(4):998.
  • Madempudi RS, Ahire JJ, Neelamraju J, et al. Efficacy of UB0316, a multi-strain probiotic formulation in patients with type 2 diabetes mellitus: a double blind, randomized, placebo controlled study. PLoS One. 2019;14(11):e0225168.
  • Angelino D, Martina A, Rosi A, et al. Glucose- and lipid-related biomarkers are affected in healthy obese or hyperglycemic adults consuming a whole-grain pasta enriched in prebiotics and probiotics: a 12-week randomized controlled trial. J Nutr. 2019;149(10):1714–1723.
  • Kobyliak N, Abenavoli L, Falalyeyeva T, et al. Beneficial effects of probiotic combination with omega-3 fatty acids in NAFLD: a randomized clinical study. Minerva Med. 2018;109(6):418–428.
  • Pedret A, Valls RM, Calderón-Pérez L, et al. Effects of daily consumption of the probiotic Bifidobacterium animalis subsp. lactis CECT 8145 on anthropometric adiposity biomarkers in abdominally obese subjects: a randomized controlled trial. Int J Obes (Lond). 2019;43(9):1863–1868.
  • Ke X, Walker A, Haange S-B, et al. Synbiotic-driven improvement of metabolic disturbances is associated with changes in the gut microbiome in diet-induced obese mice. Mol Metab. 2019;22:96–109.
  • Lim PS, Loke CF, Ho YW, et al. Cholesterol homeostasis associated with probiotic supplementation in vivo. J Appl Microbiol. 2020;129:1374–1388.
  • Yao C, Tian W, Song J, et al. Antihyperlipidaemic effect of microencapsulated Lactobacillus plantarum LIP-1 on hyperlipidaemic rats. J Sci Food Agric. 2020;100(5):2007–2017.
  • Wang G, Si Q, Rong Yang S, et al. Lactic acid bacteria reduce diabetes symptoms in mice by alleviating gut microbiota dysbiosis and inflammation in different manners. Food Funct. 2020 Jul 1;11(7):5898-5914. doi: 10.1039/c9fo02761k. Epub 2020 Jun 23. PMID: 32572400.
  • Chan YK, El-Nezami H, Chen Y, et al. Probiotic mixture VSL#3 reduce high fat diet induced vascular inflammation and atherosclerosis in ApoE(-/-) mice. AMB Express. 2016;6(1):61.
  • Huang Y, Wang J, Quan G, et al. Lactobacillus acidophilus ATCC 4356 prevents atherosclerosis via inhibition of intestinal cholesterol absorption in apolipoprotein E-knockout mice. Appl Environ Microbiol. 2014;80(24):7496–7504.
  • Qiu L, Tao X, Xiong H, et al. Lactobacillus plantarum ZDY04 exhibits a strain-specific property of lowering TMAO via the modulation of gut microbiota in mice. Food Funct. 2018;9(8):4299–4309.
  • Vasquez EC, Pereira TMC, Peotta VA, et al. Probiotics as beneficial dietary supplements to prevent and treat cardiovascular diseases: uncovering their impact on oxidative stress. Oxid Med Cell Longev. 2019;2019:3086270.
  • Rashid SK, Khodja NI, Auger C, et al. Probiotics (VSL#3) prevent endothelial dysfunction in rats with portal hypertension: role of the angiotensin system. PLoS One. 2014;9(5):e97458.
  • Friques AG, Arpini CM, Kalil IC, et al. Chronic administration of the probiotic kefir improves the endothelial function in spontaneously hypertensive rats. J Transl Med. 2015;13:390.
  • Hashmi A, Naeem N, Farooq Z, et al. Effect of prebiotic galacto-oligosaccharides on serum lipid profile of hypercholesterolemics. Probiotics Antimicrob Proteins. 2016;8(1):19–30.
  • Fak F, Backhed F, Ratner AJ. Lactobacillus reuteri prevents diet-induced obesity, but not atherosclerosis, in a strain dependent fashion in Apoe-/- mice. PLoS One. 2012;7(10):e46837.
  • Cryan JF, O’Riordan KJ, Cowan CS, et al. The microbiota-gut-brain axis. Physiol Rev. 2019;99(4):1877–2013.
  • Fulling C, Dinan TG, Cryan JF. Gut microbe to brain signaling: what happens in vagus. Neuron. 2019;101(6):998–1002.
  • Bravo JA, Forsythe P, Chew MV, et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A. 2011;108(38):16050–16055.
  • Reinshagen M. [A gut-brain neural circuit for nutrient sensory transduction]. Z Gastroenterol. 2019;57(3):335.
  • Huuskonen J, Suuronen T, Nuutinen T, et al. Regulation of microglial inflammatory response by sodium butyrate and short-chain fatty acids. Br J Pharmacol. 2004;141(5):874–880.
  • Long-Smith C, O’Riordan KJ, Clarke G, et al. Microbiota-gut-brain axis: new therapeutic opportunities. Annu Rev Pharmacol Toxicol. 2020;60:477–502.
  • Miller AH, Raison CL. The role of inflammation in depression: from evolutionary imperative to modern treatment target. Nat Rev Immunol. 2016;16(1):22–34.
  • Goshen I, Yirmiya R. Interleukin-1 (IL-1): a central regulator of stress responses. Front Neuroendocrinol. 2009;30(1):30–45.
  • DiSabato DJ, Nemeth DP, Liu X, et al. Interleukin-1 receptor on hippocampal neurons drives social withdrawal and cognitive deficits after chronic social stress. Mol Psychiatry. 2020 Jun 30. doi: 10.1038/s41380-020-0833-2. Epub ahead of print. Erratum for: Mol Psychiatry. 2020 May 22: PMID: 32606375.
  • Bauer ME, Teixeira AL. Inflammation in psychiatric disorders: what comes first? Ann N Y Acad Sci. 2019;1437(1):57–67.
  • Paiva IHR, Duarte-Silva E, Peixoto CA. The role of prebiotics in cognition, anxiety, and depression. Eur Neuropsychopharmacol. 2020;34:1–18.
  • Sarkar A, Lehto SM, Harty S, et al. Psychobiotics and the manipulation of bacteria-gut-brain signals. Trends Neurosci. 2016;39(11):763–781.
  • Liu RT, Walsh RFL, Sheehan AE. Prebiotics and probiotics for depression and anxiety: a systematic review and meta-analysis of controlled clinical trials. Neurosci Biobehav Rev. 2019;102:13–23.
  • Goh KK, Liu Y-W, Kuo P-H, et al. Effect of probiotics on depressive symptoms: a meta-analysis of human studies. Psychiatry Res. 2019;282:112568.
  • Kruger JF, Hillesheim E, Pereira ACSN, et al. Probiotics for dementia: a systematic review and meta-analysis of randomized controlled trials. Nutr Rev. 2020. DOI:10.1093/nutrit/nuaa037.
  • Ng QX, Soh A, Venkatanarayanan N, et al. A systematic review of the effect of probiotic supplementation on schizophrenia symptoms. Neuropsychobiology. 2019;78(1):1–6.
  • Wang P, Yin X, Chen G, et al. Perioperative probiotic treatment decreased the incidence of postoperative cognitive impairment in elderly patients following non-cardiac surgery: a randomised double-blind and placebo-controlled trial. Clin Nutr. 2020. DOI:10.1016/j.clnu.2020.05.001.
  • Kim CS, Cha L, Sim M, et al. Probiotic supplementation improves cognitive function and mood with changes in gut microbiota in community-dwelling elderly: A randomized, double-blind, placebo-controlled, multicenter trial. J Gerontol A Biol Sci Med Sci. 2020. DOI:10.1093/gerona/glaa090.
  • Venkataraman R, Madempudi RS, Neelamraju J, et al. Effect of multi-strain probiotic formulation on students facing examination stress: a double-blind, placebo-controlled study. Probiotics Antimicrob Proteins. 2020. DOI:10.1007/s12602-020-09681-4.
  • Xiao J, Katsumata N, Bernier F, et al. Probiotic bifidobacterium breve in improving cognitive functions of older adults with suspected mild cognitive impairment: a randomized, double-blind, placebo-controlled trial. J Alzheimers Dis. 2020;77(1):139-147. doi: 10.3233/JAD-200488. PMID: 32623402; PMCID: PMC7592675.
  • Rudzki L, Ostrowska L, Pawlak D, et al. Probiotic Lactobacillus Plantarum 299v decreases kynurenine concentration and improves cognitive functions in patients with major depression: a double-blind, randomized, placebo controlled study. Psychoneuroendocrinology. 2019;100:213–222.
  • Dugyala S, Ptacek TS, Simon JM, et al. Putative modulation of the gut microbiome by probiotics enhances preference for novelty in a preliminary double-blind placebo-controlled study in ferrets. Anim Microbiome. 2020;2:14. doi: 10.1186/s42523-020-00030-y. Epub 2020 May 5. PMID: 32490353; PMCID: PMC7266289.
  • Hoffman JD, Yanckello LM, Chlipala G, et al. Dietary inulin alters the gut microbiome, enhances systemic metabolism and reduces neuroinflammation in an APOE4 mouse model. PLoS One. 2019;14(8):e0221828.
  • Barros-Santos T, Silva KSO, Libarino-Santos M, et al. Effects of chronic treatment with new strains of Lactobacillus plantarum on cognitive, anxiety- and depressive-like behaviors in male mice. PLoS One. 2020;15(6):e0234037.
  • Hsieh TH, Kuo C-W, Hsieh K-H, et al. Probiotics alleviate the progressive deterioration of motor functions in a mouse model of Parkinson’s disease. Brain Sci. 2020;10(4):206.
  • Lu J, Lu L, Yu Y, et al. Maternal administration of probiotics promotes brain development and protects offspring’s brain from postnatal inflammatory insults in C57/BL6J mice. Sci Rep. 2020;10(1):8178.
  • Liu YW, Liu W-H, Wu -C-C, et al. Psychotropic effects of Lactobacillus plantarum PS128 in early life-stressed and naive adult mice. Brain Res. 2016;1631:1–12.
  • Mehrabadi S, Sadr SS. Assessment of probiotics mixture on memory function, inflammation markers, and oxidative stress in an alzheimer’s disease model of rats. Iran Biomed J. 2020;24(4):220–228.
  • Chen D, Yang X, Yang J, et al. Prebiotic effect of fructooligosaccharides from morinda officinalis on alzheimer’s disease in rodent models by targeting the microbiota-gut-brain axis. Front Aging Neurosci. 2017;9:403.
  • Greiner TU, Backhed F. Microbial regulation of GLP-1 and L-cell biology. Mol Metab. 2016;5(9):753–758.
  • Burokas A, Arboleya S, Moloney RD, et al. Targeting the microbiota-gut-brain axis: prebiotics have anxiolytic and antidepressant-like effects and reverse the impact of chronic stress in mice. Biol Psychiatry. 2017;82(7):472–487.
  • Daulatzai MA. Death by a thousand cuts in Alzheimer’s disease: hypoxia–the prodrome. Neurotox Res. 2013;24(2):216–243.
  • Zhang X, Le W. Pathological role of hypoxia in Alzheimer’s disease. Exp Neurol. 2010;223(2):299–303.
  • Gozal D, Kheirandish L. Sleepiness and neurodegeneration in sleep-disordered breathing: convergence of signaling cascades. Am J Respir Crit Care Med. 2005;171(12):1325–1327.
  • Vincken WG, Gauthier SG, Dollfuss RE, et al. Involvement of upper-airway muscles in extrapyramidal disorders. A cause of airflow limitation. N Engl J Med. 1984;311(7):438–442.
  • Shimohata T, Shinoda H, Nakayama H, et al. Daytime hypoxemia, sleep-disordered breathing, and laryngopharyngeal findings in multiple system atrophy. Arch Neurol. 2007;64(6):856–861.
  • Zimmerman ME, Arnedt JT, Stanchina M, et al. Normalization of memory performance and positive airway pressure adherence in memory-impaired patients with obstructive sleep apnea. Chest. 2006;130(6):1772–1778.
  • Kushida CA, Nichols DA, Holmes TH, et al. Effects of continuous positive airway pressure on neurocognitive function in obstructive sleep apnea patients: the apnea positive pressure long-term efficacy study (APPLES). Sleep. 2012;35(12):1593–1602.
  • Canessa N, Castronovo V, Cappa SF, et al. Obstructive sleep apnea: brain structural changes and neurocognitive function before and after treatment. Am J Respir Crit Care Med. 2011;183(10):1419–1426.
  • Ancoli-Israel S, Palmer BW, Cooke JR, et al. Cognitive effects of treating obstructive sleep apnea in Alzheimer’s disease: a randomized controlled study. J Am Geriatr Soc. 2008;56(11):2076–2081.
  • Neikrug AB, Liu L, Avanzino JA, et al. Continuous positive airway pressure improves sleep and daytime sleepiness in patients with Parkinson disease and sleep apnea. Sleep. 2014;37(1):177–185.
  • Gupta MA, Simpson FC. Obstructive sleep apnea and psychiatric disorders: a systematic review. J Clin Sleep Med. 2015;11(2):165–175.
  • Ni J, Wu GD, Albenberg L, et al. Gut microbiota and IBD: causation or correlation? Nat Rev Gastroenterol Hepatol. 2017;14(10):573–584.
  • Kim ER, Chang DK. Colorectal cancer in inflammatory bowel disease: the risk, pathogenesis, prevention and diagnosis. World J Gastroenterol. 2014;20(29):9872–9881.
  • Lloyd-Price J, Arze C, Ananthakrishnan AN, et al. Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases. Nature. 2019;569(7758):655–662.
  • Liu S, Zhao W, Lan P, et al. The microbiome in inflammatory bowel diseases: from pathogenesis to therapy. Protein Cell. 2020 Jun 29. doi: 10.1007/s13238-020-00745-3. Epub ahead of print. PMID: 32601832.
  • Vich Vila A, Imhann F, Collij V, et al. Gut microbiota composition and functional changes in inflammatory bowel disease and irritable bowel syndrome. Sci Transl Med. 2018;10(472):eaap8914.
  • Schirmer M, Garner A, Vlamakis H, et al. Microbial genes and pathways in inflammatory bowel disease. Nat Rev Microbiol. 2019;17(8):497–511.
  • Song X, Sun X, Oh SF, et al. Microbial bile acid metabolites modulate gut RORgamma(+) regulatory T cell homeostasis. Nature. 2020;577(7790):410–415.
  • Zhang J, Wu HM, Wang X, et al. Efficacy of prebiotics and probiotics for functional dyspepsia: a systematic review and meta-analysis. Medicine (Baltimore). 2020;99(7):e19107.
  • Wilson B, Rossi M, Dimidi E, et al. Prebiotics in irritable bowel syndrome and other functional bowel disorders in adults: a systematic review and meta-analysis of randomized controlled trials. Am J Clin Nutr. 2019;109(4):1098–1111.
  • Asto E, Méndez I, Audivert S, et al. The efficacy of probiotics, prebiotic inulin-type fructans, and synbiotics in human ulcerative colitis: a systematic review and meta-analysis. Nutrients. 2019;11(2):293.
  • Jia K, Tong X, Wang R, et al. The clinical effects of probiotics for inflammatory bowel disease: a meta-analysis. Medicine (Baltimore). 2018;97(51):e13792.
  • Fan H, Du J, Liu X, et al. Effects of pentasa-combined probiotics on the microflora structure and prognosis of patients with inflammatory bowel disease. Turk J Gastroenterol. 2019;30(8):680–685.
  • Bjarnason I, Sission G, Hayee B. A randomised, double-blind, placebo-controlled trial of a multi-strain probiotic in patients with asymptomatic ulcerative colitis and Crohn’s disease. Inflammopharmacology. 2019;27(3):465–473.
  • Bajramagic S, Hodzic E, Mulabdic A, et al. Usage of probiotics and its clinical significance at surgically treated patients sufferig from colorectal carcinoma. Med Arch. 2019;73(5):316–320.
  • Trifan A, Burta O, Tiuca N, et al. Efficacy and safety of Gelsectan for diarrhoea-predominant irritable bowel syndrome: a randomised, crossover clinical trial. United European Gastroenterol J. 2019;7(8):1093–1101.
  • Zaharuddin L, Mokhtar NM, Nawawi KN, et al. A randomized double-blind placebo-controlled trial of probiotics in post-surgical colorectal cancer. BMC Gastroenterol. 2019;19(1):131.
  • Biagioli M, Carino A, Di Giorgio C, et al. Discovery of a novel multi-strains probiotic formulation with improved efficacy toward intestinal inflammation. Nutrients. 2020;12(7):1945.
  • Liu Z, Liu F, Wang W, et al. Study of the alleviation effects of a combination of Lactobacillus rhamnosus and inulin on mice with colitis. Food Funct. 2020;11(5):3823–3837.
  • Shinde T, Perera AP, Vemuri R, et al. Synbiotic supplementation with prebiotic green banana resistant starch and probiotic Bacillus coagulans spores ameliorates gut inflammation in mouse model of inflammatory bowel diseases. Eur J Nutr. 2020. DOI:10.1007/s00394-020-02200-9.
  • Parisa A, Roya G, Mahdi R, et al. Anti-cancer effects of Bifidobacterium species in colon cancer cells and a mouse model of carcinogenesis. PLoS One. 2020;15(5):e0232930.
  • Lee CW, Chen H-J, Chien Y-H, et al. Synbiotic combination of djulis (Chenopodium formosanum) and lactobacillus acidophilus inhibits colon carcinogenesis in rats. Nutrients. 2019;12(1):103.
  • Jakubczyk D, Leszczynska K, Gorska S. The effectiveness of probiotics in the treatment of inflammatory bowel disease (IBD)-a critical review. Nutrients. 2020;12(7):1973.
  • Chou YC, Ho PY, Chen WJ, et al. Lactobacillus fermentum V3 ameliorates colitis-associated tumorigenesis by modulating the gut microbiome. Am J Cancer Res. 2020;10(4):1170–1181.
  • Yue Y, Ye K, Lu J, et al. Probiotic strain Lactobacillus plantarum YYC-3 prevents colon cancer in mice by regulating the tumour microenvironment. Biomed Pharmacother. 2020;127:110159.
  • Chen D, Jin D, Huang S, et al. Clostridium butyricum, a butyrate-producing probiotic, inhibits intestinal tumor development through modulating Wnt signaling and gut microbiota. Cancer Lett. 2020;469:456–467.
  • Ivanovska TP, Mladenovska K, Zhivikj Z, et al. Synbiotic loaded chitosan-Ca-alginate microparticles reduces inflammation in the TNBS model of rat colitis. Int J Pharm. 2017;527(1–2):126–134.
  • Rotenberg BW, Murariu D, Pang KP. Trends in CPAP adherence over twenty years of data collection: a flattened curve. J Otolaryngol Head Neck Surg. 2016;45(1):43.
  • Ramar K, Dort LC, Katz SG, et al. Clinical practice guideline for the treatment of obstructive sleep apnea and snoring with oral appliance therapy: an update for 2015. J Clin Sleep Med. 2015;11(7):773–827.
  • Peppard PE, Young T, Palta M, et al. Longitudinal study of moderate weight change and sleep-disordered breathing. JAMA. 2000;284(23):3015–3021.
  • Seganfredo FB, Blume CA, Moehlecke M, et al. Weight-loss interventions and gut microbiota changes in overweight and obese patients: a systematic review. Obes Rev. 2017;18(8):832–851.
  • Ganesh BP, Nelson JW, Eskew JR, et al. Prebiotics, probiotics, and acetate supplementation prevent hypertension in a model of obstructive sleep apnea. Hypertension. 2018;72(5):1141–1150.
  • Xu H, Wang J, Cai J, et al. Protective effect of lactobacillus rhamnosus GG and its supernatant against myocardial dysfunction in obese mice exposed to intermittent hypoxia is associated with the activation of nrf2 pathway. Int J Biol Sci. 2019;15(11):2471–2483.
  • Liu Q, Liu Y, Li F, et al. Probiotic culture supernatant improves metabolic function through FGF21-adiponectin pathway in mice. J Nutr Biochem. 2020;75:108256.
  • Gupta A, Khanna S. Fecal Microbiota Transplantation, JAMA. 2017 Jul 4;318(1):102. doi: 10.1001/jama.2017.6466. PMID: 28672320.
  • Kelly CR, Kahn S, Kashyap P, et al. Update on fecal microbiota transplantation 2015: indications, methodologies, mechanisms, and outlook. Gastroenterology. 2015;149(1):223–237.
  • Cammarota G, Ianiro G, Tilg H, et al. European consensus conference on faecal microbiota transplantation in clinical practice. Gut. 2017;66(4):569–580.
  • Turnbaugh PJ, Ley RE, Mahowald MA, et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027–1031.
  • Vrieze A, Van Nood E, Holleman F, et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology. 2012;143(4):913–6.e7.
  • Liou AP, Paziuk M, Luevano J-M, et al. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Transl Med. 2013;5(178):178ra41.
  • Wang H, Lu Y, Yan Y, et al. Promising treatment for type 2 diabetes: fecal microbiota transplantation reverses insulin resistance and impaired islets. Front Cell Infect Microbiol. 2019;9:455.
  • Adnan S, Nelson JW, Ajami NJ, et al. Alterations in the gut microbiota can elicit hypertension in rats. Physiol Genomics. 2017;49(2):96–104.
  • Li J, Zhao F, Wang Y, et al. Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome. 2017;5(1):14.
  • Juraschek SP, Bower JK, Selvin E, et al. Plasma lactate and incident hypertension in the atherosclerosis risk in communities study. Am J Hypertens. 2015;28(2):216–224.
  • Cammarota G, Ianiro G, Gasbarrini A. Fecal microbiota transplantation for the treatment of Clostridium difficile infection: a systematic review. J Clin Gastroenterol. 2014;48(8):693–702.
  • Suzuki T, Yoshida S, Hara H. Physiological concentrations of short-chain fatty acids immediately suppress colonic epithelial permeability. Br J Nutr. 2008;100(2):297–305.
  • Donohoe DR, Garge N, Zhang X, et al. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab. 2011;13(5):517–526.
  • Säemann MD, Böhmig GA, Österreicher CH, et al. Anti-inflammatory effects of sodium butyrate on human monocytes: potent inhibition of IL-12 and up-regulation of IL-10 production. Faseb J. 2000;14(15):2380–2382.
  • Ni YF, Wang J, Yan XL, et al. Histone deacetylase inhibitor, butyrate, attenuates lipopolysaccharide-induced acute lung injury in mice. Respir Res. 2010;11(1):33.
  • Maslowski KM, Mackay CR. Diet, gut microbiota and immune responses. Nat Immunol. 2011;12(1):5–9.
  • Nakamura M, Saito H, Ebinuma H, et al. Reduction of telomerase activity in human liver cancer cells by a histone deacetylase inhibitor. J Cell Physiol. 2001;187(3):392–401.
  • Borthakur A, Priyamvada S, Kumar A, et al. A novel nutrient sensing mechanism underlies substrate-induced regulation of monocarboxylate transporter-1. Am J Physiol Gastrointest Liver Physiol. 2012;303(10):G1126–33.
  • Cherbut C, Ferrier L, Roze C, et al. Short-chain fatty acids modify colonic motility through nerves and polypeptide YY release in the rat. Am J Physiol. 1998;275(6):G1415–22.
  • Burger-van Paassen N, Vincent A, Puiman PJ, et al. The regulation of intestinal mucin MUC2 expression by short-chain fatty acids: implications for epithelial protection. Biochem J. 2009;420(2):211–219.
  • Balda MS, Matter K. Tight junctions at a glance. J Cell Sci. 2008;121(Pt 22):3677–3682.
  • Tolhurst G, Heffron H, Lam YS, et al. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes. 2012;61(2):364–371.
  • Xiong Y, Miyamoto N, Shibata K, et al. Short-chain fatty acids stimulate leptin production in adipocytes through the G protein-coupled receptor GPR41. Proc Natl Acad Sci U S A. 2004;101(4):1045–1050.
  • Bartolomaeus H, Balogh A, Yakoub M, et al. Short-chain fatty acid propionate protects from hypertensive cardiovascular damage. Circulation. 2019;139(11):1407–1421.
  • Holmes E, Loo RL, Stamler J, et al. Human metabolic phenotype diversity and its association with diet and blood pressure. Nature. 2008;453(7193):396–400.
  • Marques FZ, Nelson E, Chu P-Y, et al. High-fiber diet and acetate supplementation change the gut microbiota and prevent the development of hypertension and heart failure in hypertensive mice. Circulation. 2017;135(10):964–977.
  • Lin HV, Frassetto A, Kowalik Jr, EJ, et al. Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS One. 2012;7(4):e35240.
  • Gao Z, Yin J, Zhang J, et al. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes. 2009;58(7):1509–1517.
  • Khan S, Jena GB. Protective role of sodium butyrate, a HDAC inhibitor on beta-cell proliferation, function and glucose homeostasis through modulation of p38/ERK MAPK and apoptotic pathways: study in juvenile diabetic rat. Chem Biol Interact. 2014;213:1–12.
  • Hong J, Jia Y, Pan S, et al. Butyrate alleviates high fat diet-induced obesity through activation of adiponectin-mediated pathway and stimulation of mitochondrial function in the skeletal muscle of mice. Oncotarget. 2016;7(35):56071–56082.
  • Yadav L, Puri N, Rastogi V, et al. Matrix metalloproteinases and cancer - roles in threat and therapy. Asian Pac J Cancer Prev. 2014;15(3):1085–1091.
  • Thangaraju M, Cresci GA, Liu K, et al. GPR109A is a G-protein-coupled receptor for the bacterial fermentation product butyrate and functions as a tumor suppressor in colon. Cancer Res. 2009;69(7):2826–2832.
  • Ji B, Nielsen J. From next-generation sequencing to systematic modeling of the gut microbiome. Front Genet. 2015;6:219.
  • Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol. 2009;9(5):313–323.
  • Omary MB, Cohen DE, El-Omar EM, et al. Not all mice are the same: standardization of animal research data presentation. Cell Mol Gastroenterol Hepatol. 2016;2(4):391–393.
  • Eisenstein M. The hunt for a healthy microbiome. Nature. 2020;577(7792):S6–S8.
  • Ley RE, Turnbaugh PJ, Klein S, et al. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444(7122):1022–1023.
  • De Filippo C, Cavalieri D, Di Paola M, et al. 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. 2010;107(33):14691–14696.
  • Chen Y, Yang F, Lu H, et al. Characterization of fecal microbial communities in patients with liver cirrhosis. Hepatology. 2011;54(2):562–572.
  • Mashaqi S, Gozal D. Obstructive sleep apnea and systemic hypertension: gut dysbiosis as the mediator? J Clin Sleep Med. 2019;15(10):1517–1527.
  • Sanders ME, Merenstein DJ, Reid G, et al. Probiotics and prebiotics in intestinal health and disease: from biology to the clinic. Nat Rev Gastroenterol Hepatol. 2019;16(10):605–616.
  • Dronkers TMG, Krist L, Van Overveld FJ, et al. The ascent of the blessed: regulatory issues on health effects and health claims for probiotics in Europe and the rest of the world. Benef Microbes. 2018;9(5):717–723.

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