Cardiac vagal activity is associated with gut-microbiome patterns in women—An exploratory pilot study

References

• Al Bander Z, Nitert MD, Mousa A, Naderpoor N. 2020. The gut microbiota and inflammation: an overview. IJERPH. 17(20):7618.
   Web of Science ®Google Scholar
• Ayaz M, Subhan F, Ahmed J, Khan A-U, Ullah F, Ullah I, Ali G, Syed N-I-H, Hussain S. 2015. Sertraline enhances the activity of antimicrobial agents against pathogens of clinical relevance. J Biol Res. 22(1):4.
   Google Scholar
• Bastiaanssen TFS, Cowan CSM, Claesson MJ, Dinan TG, Cryan JF. 2019. Making sense of… the microbiome in psychiatry. Int J Neuropsychopharmacol. 22(1):37–52.
   PubMed Web of Science ®Google Scholar
• Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J. 1961. An inventory for measuring depression. Arch Gen Psychiatry. 4:561–571.
   PubMed Web of Science ®Google Scholar
• Berthoud HR, Neuhuber WL. 2000. Functional and chemical anatomy of the afferent vagal system. Auton Neurosci. 85(1–3):1–17.
   PubMed Web of Science ®Google Scholar
• Bohnert JA, Szymaniak-Vits M, Schuster S, Kern WV. 2011. Efflux inhibition by selective serotonin reuptake inhibitors in Escherichia coli. J Antimicrob Chemother. 66(9):2057–2060.
   PubMed Web of Science ®Google Scholar
• Bonaz B, Bazin T, Pellissier S. 2018. The vagus nerve at the interface of the microbiota-gut-brain axis. Front Neurosci. 12:49.
   PubMed Web of Science ®Google Scholar
• Bonaz B, Sinniger V, Hoffmann D, Clarençon D, Mathieu N, Dantzer C, Vercueil L, Picq C, Trocmé C, Faure P, et al. 2016. Chronic vagus nerve stimulation in Crohn’s disease: a 6-month follow-up pilot study. Neurogastroenterol Motil. 28(6):948–953.
   PubMed Web of Science ®Google Scholar
• Bonaz B, Sinniger V, Pellissier S. 2016. Vagal tone: effects on sensitivity, motility, and inflammation. Neurogastroenterol Motil. 28(4):455–462.
   PubMed Web of Science ®Google Scholar
• Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, Bienenstock J, Cryan JF. 2011. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci USA. 108(38):16050–16055.
   PubMed Web of Science ®Google Scholar
• Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. 2016. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 13(7):581–583.
   PubMed Web of Science ®Google Scholar
• Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 7(5):335–336.
   PubMed Web of Science ®Google Scholar
• Carabotti M, Scirocco A, Maselli MA, Severi C. 2015. The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Ann Gastroenterol. 28(2):203.
   PubMed Web of Science ®Google Scholar
• Carreno FR, Frazer A. 2017. Vagal nerve stimulation for treatment-resistant depression. Neurotherapeutics. 14(3):716–727.
   PubMed Web of Science ®Google Scholar
• Chao A. 1984. Nonparametric estimation of the number of classes in a population. Scand J Stat. 11:265–270.
   Web of Science ®Google Scholar
• Cussotto S, Strain CR, Fouhy F, Strain RG, Peterson VL, Clarke G, Stanton C, Dinan TG, Cryan JF. 2019. Differential effects of psychotropic drugs on microbiome composition and gastrointestinal function. Psychopharmacology. 236(5):1671–1685.
   PubMed Web of Science ®Google Scholar
• Daniel H. 2021. Diet and gut microbiome and the “chicken or egg” problem. Front Nutr. 8:828630.
   PubMed Web of Science ®Google Scholar
• de Lartigue G. 2016. Role of the vagus nerve in the development and treatment of diet-induced obesity. J Physiol. 594(20):5791–5815.
   PubMed Web of Science ®Google Scholar
• Fernandes AD, Macklaim JM, Linn TG, Reid G, Gloor GB. 2013. ANOVA-like differential gene expression analysis of single-organism and meta-RNA-seq. PLOS One. 8(7):e67019.
   PubMed Web of Science ®Google Scholar
• Fulling C, Dinan TG, Cryan JF. 2019. Gut microbe to brain signaling: what happens in vagus. Neuron. 101(6):998–1002.
   PubMed Web of Science ®Google Scholar
• Gholamrezaei A, Van Diest I, Aziz Q, Vlaeyen JWS, Van Oudenhove L. 2021. Psychophysiological responses to various slow, deep breathing techniques. Psychophysiology. 58(2):e13712.
   PubMed Web of Science ®Google Scholar
• Grote V, Frühwirth M, Lackner HK, Goswami N, Köstenberger M, Likar R, Moser M. 2021. Cardiorespiratory interaction and autonomic sleep quality improve during sleep in beds made from Pinus cembra (stone pine) solid wood. IJERPH. 18(18):9749.
   Web of Science ®Google Scholar
• Hamilton M. 1960. A rating scale for depression. J Neurol Neurosurg Psychiatry. 23:56–62.
   PubMed Web of Science ®Google Scholar
• Holmes I, Harris K, Quince C. 2012. Dirichlet multinomial mixtures: generative models for microbial metagenomics. PLOS One. 7(2):e30126.
   PubMed Web of Science ®Google Scholar
• Jiang H, Ling Z, Zhang Y, Mao H, Ma Z, Yin Y, Wang W, Tang W, Tan Z, Shi J, et al. 2015. Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav Immun. 48:186–194.
   PubMed Web of Science ®Google Scholar
• Kelly JR, Borre Y, O' Brien C, Patterson E, El Aidy S, Deane J, Kennedy PJ, Beers S, Scott K, Moloney G, et al. 2016. Transferring the blues: depression-associated gut microbiota induces neurobehavioural changes in the rat. J Psychiatr Res. 82:109–118.
   PubMed Web of Science ®Google Scholar
• Koch C, Wilhelm M, Salzmann S, Rief W, Euteneuer F. 2019. A meta-analysis of heart rate variability in major depression. Psychol Med. 49(12):1948–1957.
   PubMed Web of Science ®Google Scholar
• Koenig J, Thayer JF. 2016. Sex differences in healthy human heart rate variability: a meta-analysis. Neurosci Biobehav Rev. 64:288–310.
   PubMed Web of Science ®Google Scholar
• Kuo PH, Chung YE. 2019. Moody microbiome: challenges and chances. J Formos Med Assoc. 118 Suppl 1:S42–S54.
   PubMed Web of Science ®Google Scholar
• Laborde S, Mosley E, Thayer JF. 2017. Heart rate variability and cardiac vagal tone in psychophysiological research – recommendations for experiment planning, data analysis, and data reporting. Front Psychol. 8:213.
   PubMed Web of Science ®Google Scholar
• Lehofer M, Moser M, Hoehn-Saric R, McLeod D, Hildebrandt G, Egner S, Steinbrenner B, Liebmann P, Zapotoczky HG. 1999. Influence of age on the parasympatholytic property of tricyclic antidepressants. Psychiatry Res. 85(2):199–207.
   PubMed Web of Science ®Google Scholar
• Li J, Ma Y, Bao Z, Gui X, Li AN, Yang Z, Li MD. 2020. Clostridiales are predominant microbes that mediate psychiatric disorders. J Psychiatr Res. 130:48–56.
   PubMed Web of Science ®Google Scholar
• McGovern AS, Hamlin AS, Winter G. 2019. A review of the antimicrobial side of antidepressants and its putative implications on the gut microbiome. Aust N Z J Psychiatry. 53(12):1151–1166.
   PubMed Web of Science ®Google Scholar
• Michels N, Van de Wiele T, De Henauw S. 2017. Chronic psychosocial stress and gut health in children: associations with calprotectin and fecal short-chain fatty acids. Psychosom Med. 79(8):927–935.
   PubMed Web of Science ®Google Scholar
• Michels N, Van de Wiele T, Fouhy F, O'Mahony S, Clarke G, Keane J. 2019. Gut microbiome patterns depending on children’s psychosocial stress: reports versus biomarkers. Brain Behav Immun. 80:751–762.
   PubMed Web of Science ®Google Scholar
• Mörkl S, Lackner S, Müller W, Gorkiewicz G, Kashofer K, Oberascher A, Painold A, Holl A, Holzer P, Meinitzer A, et al. 2017. Gut microbiota and body composition in anorexia nervosa inpatients in comparison to athletes, overweight, obese, and normal weight controls. Int J Eat Disord. 50(12):1421–1431.
   PubMed Web of Science ®Google Scholar
• Mosca A, Leclerc M, Hugot JP. 2016. Gut microbiota diversity and human diseases: should we reintroduce key predators in our ecosystem? Front Microbiol. 7:455.
   PubMed Web of Science ®Google Scholar
• Moser M, Fruhwirth M, Kenner T. 2008. The symphony of life. IEEE Eng Med Biol Mag. 27(1):29–37.
   PubMedGoogle Scholar
• Moser M, Lehofer M, Sedminek A, Lux M, Zapotoczky HG, Kenner T, Noordergraaf A. 1994. Heart rate variability as a prognostic tool in cardiology. A contribution to the problem from a theoretical point of view. Circulation. 90(2):1078–1082.
   PubMed Web of Science ®Google Scholar
• O'Connor KM, Lucking EF, Golubeva AV, Strain CR, Fouhy F, Cenit MC, Dhaliwal P, Bastiaanssen TFS, Burns DP, Stanton C, et al. 2019. Manipulation of gut microbiota blunts the ventilatory response to hypercapnia in adult rats. EBioMedicine. 44:618–638.
   PubMed Web of Science ®Google Scholar
• O'Toole PW, Claesson MJ. 2010. Gut microbiota: changes throughout the lifespan from infancy to elderly. Int Dairy J. 20(4):281–291.
   Web of Science ®Google Scholar
• Parada Venegas D, De la Fuente MK, Landskron G, González MJ, Quera R, Dijkstra G, Harmsen HJM, Faber KN, Hermoso MA. 2019. Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol. 10:277.
   PubMed Web of Science ®Google Scholar
• Pavlov VA, Tracey KJ. 2012. The vagus nerve and the inflammatory reflex–linking immunity and metabolism. Nat Rev Endocrinol. 8(12):743–754.
   PubMed Web of Science ®Google Scholar
• Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41(Database issue):D590–D596.
   PubMed Web of Science ®Google Scholar
• Rawenwaaij-Arts C, Kallee L, Hopman J. 1996. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Heart rate variability. Standards of measurement, physiologic interpretation, and clinical use. Circulation. 93(1065):436–447.
   Google Scholar
• Roager HM, Hansen LBS, Bahl MI, Frandsen HL, Carvalho V, Gøbel RJ, Dalgaard MD, Plichta DR, Sparholt MH, Vestergaard H, et al. 2016. Colonic transit time is related to bacterial metabolism and mucosal turnover in the gut. Nat Microbiol. 1(9):16093.
   PubMed Web of Science ®Google Scholar
• Rosas-Ballina M, Tracey KJ. 2009. Cholinergic control of inflammation. J Intern Med. 265(6):663–679.
   PubMed Web of Science ®Google Scholar
• Sarkar A, Harty S, Lehto SM, Moeller AH, Dinan TG, Dunbar RIM, Cryan JF, Burnet PWJ. 2018. The microbiome in psychology and cognitive neuroscience. Trends Cogn Sci. 22(7):611–636.
   PubMed Web of Science ®Google Scholar
• Schwerdtfeger AR, Schwarz G, Pfurtscheller K, Thayer JF, Jarczok MN, Pfurtscheller G. 2020. Heart rate variability (HRV): from brain death to resonance breathing at 6 breaths per minute. Clin Neurophysiol. 131(3):676–693.
   PubMed Web of Science ®Google Scholar
• Seebauer M, Fruhwirth M, Moser M. 2002. Changes of respiratory sinus arrhythmia during the menstrual cycle depend on average heart rate. Eur J Appl Physiol. 87(4–5):309–314.
   PubMed Web of Science ®Google Scholar
• Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. 2011. Metagenomic biomarker discovery and explanation. Genome Biol. 12(6):R60.
   PubMed Web of Science ®Google Scholar
• Shaffer F, Ginsberg J. 2017. An overview of heart rate variability metrics and norms. Front Public Health. 5:258.
   PubMed Web of Science ®Google Scholar
• Soares-Miranda L, Negrao CE, Antunes-Correa LM, Nobre TS, Silva P, Santos R, Vale S, Mota J. 2012. High levels of C-reactive protein are associated with reduced vagal modulation and low physical activity in young adults. Scand J Med Sci Sports. 22(2):278–284.
   PubMed Web of Science ®Google Scholar
• Tatschl JM, Hochfellner SM, Schwerdtfeger AR. 2020. Implementing mobile HRV biofeedback as adjunctive therapy during inpatient psychiatric rehabilitation facilitates recovery of depressive symptoms and enhances autonomic functioning short-term: a 1-year pre–post-intervention follow-up pilot study. Front Neurosci. 14:738.
   PubMed Web of Science ®Google Scholar
• Tatschl JM, Schwerdtfeger AR. 2022. Squeeze the beat: enhancing cardiac vagal activity during resonance breathing via coherent pelvic floor recruitment. Psychophysiology. e14129. doi:10.1111/psyp.14129
   PubMed Web of Science ®Google Scholar
• Topçu Ç, Frühwirth M, Moser M, Rosenblum M, Pikovsky A. 2018. Disentangling respiratory sinus arrhythmia in heart rate variability records. Physiol Meas. 39(5):054002.
   PubMed Web of Science ®Google Scholar
• Tracey KJ. 2002. The inflammatory reflex. Nature. 420(6917):853–859.
   PubMed Web of Science ®Google Scholar
• Umetani K, Singer DH, McCraty R, Atkinson M. 1998. Twenty-four hour time domain heart rate variability and heart rate: relations to age and gender over nine decades. J Am Coll Cardiol. 31(3):593–601.
   PubMed Web of Science ®Google Scholar
• Valkanova V, Ebmeier KP, Allan CL. 2013. CRP, IL-6 and depression: a systematic review and meta-analysis of longitudinal studies. J Affect Disord. 150(3):736–744.
   PubMed Web of Science ®Google Scholar
• Valladares EM, Eljammal SM, Motivala S, Ehlers CL, Irwin MR. 2008. Sex differences in cardiac sympathovagal balance and vagal tone during nocturnal sleep. Sleep Med. 9(3):310–316.
   PubMed Web of Science ®Google Scholar
• Valles-Colomer M, Falony G, Darzi Y, Tigchelaar EF, Wang J, Tito RY, Schiweck C, Kurilshikov A, Joossens M, Wijmenga C, et al. 2019. The neuroactive potential of the human gut microbiota in quality of life and depression. Nat Microbiol. 4(4):623–632.
   PubMed Web of Science ®Google Scholar
• van Zyl LT, Hasegawa T, Nagata K. 2008. Effects of antidepressant treatment on heart rate variability in major depression: a quantitative review. Biopsychosoc Med. 2(1):12.
   PubMedGoogle Scholar
• Williams DP, Koenig J, Carnevali L, Sgoifo A, Jarczok MN, Sternberg EM, Thayer JF. 2019. Heart rate variability and inflammation: a meta-analysis of human studies. Brain Behav Immun. 80:219–226.
   PubMed Web of Science ®Google Scholar
• Wu C, Liu P, Fu H, Chen W, Cui S, Lu L, Tang C. 2018. Transcutaneous auricular vagus nerve stimulation in treating major depressive disorder: a systematic review and meta-analysis. Medicine. 97(52):e13845.
   PubMed Web of Science ®Google Scholar
• Yoon K, Kim N. 2021. Roles of sex hormones and gender in the gut microbiota. J Neurogastroenterol Motil. 27(3):314–325.
   PubMed Web of Science ®Google Scholar
• Younis W, AbdelKhalek A, Mayhoub AS, Seleem MN. 2017. In vitro screening of an FDA-approved library against ESKAPE pathogens. Curr Pharm Des. 23(14):2147–2157.
   PubMed Web of Science ®Google Scholar