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Cited by 83Gut microbiota and healthTryptophan and brain disordersGastrointestinal motility and disorders

Acute and repeated exposure to social stress reduces gut microbiota diversity in Syrian hamsters

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Partrick, Katherine A., Chassaing, Benoit, Beach, Linda Q., McCann, Katharine E., Gewirtz, Andrew T., Huhman, Kim L.·2018·Behavioural Brain Research
DOI 10.1016/j.bbr.2018.02.005PMC PMC6246037
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  • Stress impacts gut microbial composition in rodents, pigs, horses, and non-human primates.

    “Many preclinical studies have since demonstrated that stress impacts gut microbial composition in a number of different hosts, including rodents (Bharwani et al., 2016;Golubeva et al., 2015;Partrick et al., 2018), pigs (Mudd et al., 2016), horses (Mach and Fuster-Botella, 2017) and non-human primates (Bailey and Coe, 1999;Bailey et al., 2004) (see Table 1).”

    From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Partrick et al., 2018

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  1. Aguilera M, Vergara P, & Martinez V (2013). Stress and antibiotics alter luminal and wall-adhered microbiota and enhance the local expression of visceral sensory-related systems in mice. Neurogastroenterol Motil, 25(8), e515– 529. doi: 10.1111/nmo.12154 23711047 · DOI · Paper page
  2. Ait-Belgnaoui A, Durand H, Cartier C, Chaumaz G, Eutamene H, Ferrier L, … Theodorou V (2012). Prevention of gut leakiness by a probiotic treatment leads to attenuated HPA response to an acute psychological stress in rats. Psychoneuroendocrinology, 37(11), 1885– 1895. doi: 10.1016/j.psyneuen.2012.03.024 22541937 · DOI · Paper page
  3. Albers HE, Huhman KL, & Meisel RL (2002). 6 - Hormonal Basis of Social Conflict and Communication A2 - Pfaff, Donald W In Arnold AP, Fahrbach SE, Etgen AM, & Rubin RT (Eds.), Hormones, Brain and Behavior (pp. 393– 433). San Diego: Academic Press.
  4. Aronesty E (2013). Comparison of sequencing utility programs. The Open Bioinformatics Journal, 7(1).
  5. Bailey MT, & Coe CL (1999). Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol, 35(2), 146– 155. 10461128
  6. Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, & Lyte M (2011). Exposure to a Social Stressor Alters the Structure of the Intestinal Microbiota: Implications for Stressor-Induced Immunomodulation. Brain Behav Immun, 25(3), 397– 407. doi: 10.1016/j.bbi.2010.10.023 21040780 PMC3039072 · DOI · Paper page
  7. Bekhuis E, Boschloo L, Rosmalen JG, & Schoevers RA (2015). Differential associations of specific depressive and anxiety disorders with somatic symptoms. J Psychosom Res, 78(2), 116– 122. doi: 10.1016/j.jpsychores.2014.11.007 25524436 · DOI · Paper page
  8. Bharwani A, Mian MF, Foster JA, Surette MG, Bienenstock J, & Forsythe P (2016). Structural & functional consequences of chronic psychosocial stress on the microbiome & host. Psychoneuroendocrinology, 63, 217– 227. doi: 10.1016/j.psyneuen.2015.10.001 26479188 · DOI · Paper page
  9. Bjorkqvist K (2001). Social defeat as a stressor in humans. Physiol Behav, 73(3), 435– 442. 11438372
  10. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, … 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 U S A, 108(38), 16050– 16055. doi: 10.1073/pnas.1102999108 21876150 PMC3179073 · DOI · Paper page
  11. Brook I (2008). Infective endocarditis caused by anaerobic bacteria. Arch Cardiovasc Dis, 101(10), 665– 676. doi: 10.1016/j.acvd.2008.08.008 19056073 · DOI
  12. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, … Knight R (2010). QIIME allows analysis of high-throughput community sequencing data. Nat Methods, 7(5), 335– 336. doi: 10.1038/nmeth.f.303 20383131 PMC3156573 · DOI · Paper page
  13. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, … Knight R (2012). Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. Isme j, 6(8), 1621– 1624. doi: 10.1038/ismej.2012.8 22402401 PMC3400413 · DOI · Paper page
  14. Chassaing B, Koren O, Goodrich JK, Poole AC, Srinivasan S, Ley RE, & Gewirtz AT (2015). Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature, 519, 92. doi: 10.1038/nature14232 25731162 PMC4910713 · DOI · Paper page
  15. Collins SM, Kassam Z, & Bercik P (2013). The adoptive transfer of behavioral phenotype via the intestinal microbiota: experimental evidence and clinical implications. Curr Opin Microbiol, 16(3), 240– 245. doi: 10.1016/j.mib.2013.06.004 23845749 · DOI
  16. Cryan JF (2016). Stress and the Microbiota-Gut-Brain Axis: An Evolving Concept in Psychiatry. Can J Psychiatry, 61(4), 201– 203. doi: 10.1177/0706743716635538 27254411 PMC4794959 · DOI
  17. Desbonnet L, Clarke G, Shanahan F, Dinan TG, & Cryan JF (2014). Microbiota is essential for social development in the mouse. Mol Psychiatry, 19(2), 146– 148. doi: 10.1038/mp.2013.65 23689536 PMC3903109 · DOI · Paper page
  18. Dinan TG, Stilling RM, Stanton C, & Cryan JF (2015). Collective unconscious: how gut microbes shape human behavior. Journal Of Psychiatric Research, 63, 1– 9. doi: 10.1016/j.jpsychires.2015.02.021 25772005 · DOI · Paper page
  19. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, … Relman DA (2005). Diversity of the human intestinal microbial flora. Science, 308(5728), 1635– 1638. doi: 10.1126/science.1110591 15831718 PMC1395357 · DOI · Paper page
  20. Edgar RC (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26(19), 2460– 2461. doi: 10.1093/bioinformatics/btq461 20709691 · DOI
  21. Felice VD, Moloney RD, Cryan JF, Dinan TG, & O’Mahony SM (2015). Visceral Pain and Psychiatric Disorders. Mod Trends Pharmacopsychiatri, 30, 103– 119. doi: 10.1159/000435936 26436661 · DOI
  22. Galley JD, Nelson MC, Yu Z, Dowd SE, Walter J, Kumar PS, … Bailey MT (2014). Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota. BMC Microbiol, 14, 189. doi: 10.1186/1471-2180-14-189 25028050 PMC4105248 · DOI
  23. Gilbert JA, Jansson JK, & Knight R (2014). The Earth Microbiome project: successes and aspirations. BMC Biol, 12, 69. doi: 10.1186/s12915-014-0069-1 25184604 PMC4141107 · DOI
  24. Haddad PM, Talbot PS, Anderson IM, & McAllister-Williams RH (2015). Managing inadequate antidepressant response in depressive illness. British Medical Bulletin, 115(1), 183– 201. doi: 10.1093/bmb/ldv034 26311502 · DOI
  25. Hanstock TL, Clayton EH, Li KM, & Mallet PE (2004). Anxiety and aggression associated with the fermentation of carbohydrates in the hindgut of rats. Physiol Behav, 82(2-3), 357– 368. doi: 10.1016/j.physbeh.2004.04.002 15276799 · DOI
  26. He Z, Shao T, Li H, Xie Z, & Wen C (2016). Alterations of the gut microbiome in Chinese patients with systemic lupus erythematosus. Gut Pathog, 8, 64. doi: 10.1186/s13099-016-0146-9 27980687 PMC5146896 · DOI
  27. Huhman KL, Bunnell BN, Mougey EH, & Meyerhoff JL (1990). Effects of social conflict on POMC-derived peptides and glucocorticoids in male golden hamsters. Physiol Behav, 47(5), 949– 956. 2167488
  28. Huhman KL, Moore TO, Ferris CF, Mougey EH, & Meyerhoff JL (1991). Acute and repeated exposure to social conflict in male golden hamsters: increases in plasma POMC-peptides and cortisol and decreases in plasma testosterone. Horm Behav, 25(2), 206– 216. 1648544
  29. Jasnow AM, Drazen DL, Huhman KL, Nelson RJ, & Demas GE (2001). Acute and chronic social defeat suppresses humoral immunity of male Syrian hamsters (Mesocricetus auratus). Horm Behav, 40(3), 428– 433. doi: 10.1006/hbeh.2001.1708 11673916 · DOI
  30. Jiang H, Ling Z, Zhang Y, Mao H, Ma Z, Yin Y, … Ruan B (2015). Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav Immun, 48, 186– 194. doi: 10.1016/j.bbi.2015.03.016 25882912 · DOI · Paper page
  31. Jones SE, & Versalovic J (2009). Probiotic Lactobacillus reuteri biofilms produce antimicrobial and anti-inflammatory factors. BMC Microbiol, 9, 35. doi: 10.1186/1471-2180-9-35 19210794 PMC2653509 · DOI
  32. Libby DB, & Bearman G (2009). Bacteremia due to Clostridium difficile--review of the literature. Int J Infect Dis, 13(5), e305– 309. doi: 10.1016/j.ijid.2009.01.014 19398213 · DOI
  33. Lozupone C, Hamady M, & Knight R (2006). UniFrac--an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics, 7, 371. doi: 10.1186/1471-2105-7-371 16893466 PMC1564154 · DOI
  34. Lozupone C, & Knight R (2005). UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol, 71(12), 8228– 8235. doi: 10.1128/aem.71.12.8228-8235.2005 16332807 PMC1317376 · DOI · Paper page
  35. Luczynski P, Whelan SO, O’Sullivan C, Clarke G, Shanahan F, Dinan TG, & Cryan JF (2016). Adult microbiota-deficient mice have distinct dendritic morphological changes: differential effects in the amygdala and hippocampus. Eur J Neurosci. doi: 10.1111/ejn.13291 PMC5113767 27256072 · DOI
  36. Lyte M, Vulchanova L, & Brown DR (2011). Stress at the intestinal surface: catecholamines and mucosa-bacteria interactions. Cell Tissue Res, 343(1), 23– 32. doi: 10.1007/s00441-010-1050-0 20941511 · DOI · Paper page
  37. Mackos AR, Maltz R, & Bailey MT (2017). The role of the commensal microbiota in adaptive and maladaptive stressor-induced immunomodulation. Horm Behav, 88, 70– 78. doi: 10.1016/j.yhbeh.2016.10.006 27760302 PMC5303636 · DOI
  38. Maes M (2008). The cytokine hypothesis of depression: inflammation, oxidative & nitrosative stress (IO&NS) and leaky gut as new targets for adjunctive treatments in depression. Neuro Endocrinol Lett, 29(3), 287– 291. 18580840
  39. Maes M, Kubera M, & Leunis JC (2008). The gut-brain barrier in major depression: intestinal mucosal dysfunction with an increased translocation of LPS from gram negative enterobacteria (leaky gut) plays a role in the inflammatory pathophysiology of depression. Neuro Endocrinol Lett, 29(1), 117– 124. 18283240
  40. Mah KW, Bjorksten B, Lee BW, van Bever HP, Shek LP, Tan TN, … Chua KY (2006). Distinct pattern of commensal gut microbiota in toddlers with eczema. Int Arch Allergy Immunol, 140(2), 157– 163. doi: 10.1159/000092555 16601353 · DOI
  41. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, … Hugenholtz P (2012). An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. Isme j, 6(3), 610– 618. doi: 10.1038/ismej.2011.139 22134646 PMC3280142 · DOI
  42. Mika A, Rumian N, Loughridge AB, & Fleshner M (2016). Exercise and Prebiotics Produce Stress Resistance: Converging Impacts on Stress-Protective and Butyrate-Producing Gut Bacteria. Int Rev Neurobiol, 131, 165– 191. doi: 10.1016/bs.irn.2016.08.004 27793217 · DOI
  43. Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, & Monteggia LM (2002). Neurobiology of Depression. Neuron, 34(1), 13– 25. http://dx.doi.org/10.1016/S0896-6273(02)00653-0 11931738 · DOI · Paper page
  44. Parashar A, & Udayabanu M (2016). Gut microbiota regulates key modulators of social behavior. Eur Neuropsychopharmacol, 26(1), 78– 91. doi: 10.1016/j.euroneuro.2015.11.002 26613639 · DOI · Paper page
  45. Potegal M, Huhman K, Moore T, & Meyerhoff J (1993). Conditioned defeat in the Syrian golden hamster (Mesocricetus auratus). Behavioral and Neural Biology, 60(2), 93– 102. doi: http://dx.doi.org/10.1016/0163-1047(93)90159-F 8117243 · DOI
  46. Price MN, Dehal PS, & Arkin AP (2009). FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol, 26(7), 1641– 1650. doi: 10.1093/molbev/msp077 19377059 PMC2693737 · DOI · Paper page
  47. Qiao H, Li MX, Xu C, Chen HB, An SC, & Ma XM (2016). Dendritic Spines in Depression: What We Learned from Animal Models. Neural Plast, 2016, 8056370. doi: 10.1155/2016/8056370 26881133 PMC4736982 · DOI
  48. Qin HY, Cheng CW, Tang XD, & Bian ZX (2014). Impact of psychological stress on irritable bowel syndrome. World J Gastroenterol, 20(39), 14126– 14131. doi: 10.3748/wjg.v20.i39.14126 25339801 PMC4202343 · DOI
  49. Ramakrishna BS (2013). Role of the gut microbiota in human nutrition and metabolism. J Gastroenterol Hepatol, 28 Suppl 4, 9– 17. doi: 10.1111/jgh.12294 24251697 · DOI
  50. Rosenhauer AM, McCann KE, Norvelle A, & Huhman KL (2017). An acute social defeat stressor in early puberty increases susceptibility to social defeat in adulthood. Horm Behav. doi: 10.1016/j.yhbeh.2017.04.002 28390864 · DOI
  51. Ross AP, Norvelle A, Choi DC, Walton JC, Albers HE, & Huhman KL (2017). Social housing and social isolation: Impact on stress indices and energy balance in male and female Syrian hamsters (Mesocricetus auratus). Physiol Behav, 777(Supplement C), 264– 269. doi: https://doi.org/10.1016/i.physbeh.2017.05.015 PMC5538356 28511867 · DOI
  52. Saveanu RV, & Nemeroff CB (2012). Etiology of depression: genetic and environmental factors. Psychiatr Clin North Am, 35(1), 51– 71. doi: 10.1016/j.psc.2011.12.001 22370490 · DOI
  53. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, & Huttenhower C (2011). Metagenomic biomarker discovery and explanation. Genome Biol, 72(6), R60. doi: 10.1186/gb-2011-12-6-r60 PMC3218848 21702898 · DOI · Paper page
  54. Sekirov I, Russell SL, Antunes LC, & Finlay BB (2010). Gut microbiota in health and disease. Physiol Rev, 90(3), 859– 904. doi: 10.1152/physrev.00045.2009 20664075 · DOI · Paper page
  55. Seksik P, Rigottier-Gois L, Gramet G, Sutren M, Pochart P, Marteau P, … Dore J (2003). Alterations of the dominant faecal bacterial groups in patients with Crohn’s disease of the colon. Gut, 52(2), 237– 242. 12524406 PMC1774977
  56. Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N, Yu XN, … Koga Y (2004). Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol, 558(Pt 1), 263– 275. doi: 10.1113/jphysiol.2004.063388 15133062 PMC1664925 · DOI · Paper page
  57. Thompson RS, Roller R, Mika A, Greenwood BN, Knight R, Chichlowski M, … Fleshner M (2016). Dietary Prebiotics and Bioactive Milk Fractions Improve NREM Sleep, Enhance REM Sleep Rebound and Attenuate the Stress-Induced Decrease in Diurnal Temperature and Gut Microbial Alpha Diversity. Front Behav Neurosci, 70, 240. doi: 10.3389/fnbeh.2016.00240 PMC5223485 28119579 · DOI
  58. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, & Gordon JI (2006). An obesity-associated gut microbiome with increased capacity for energy harvest. Nature, 444(7122), 1027– 1031. doi: 10.1038/nature05414 17183312 · DOI · Paper page
  59. Vaahtovuo J, Munukka E, Korkeamaki M, Luukkainen R, & Toivanen P (2008). Fecal microbiota in early rheumatoid arthritis. J Rheumatol, 35(8), 1500– 1505. 18528968
  60. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, … Gordon JI (2012). Human gut microbiome viewed across age and geography. Nature, 486(7402), 222– 227. doi: 10.1038/nature11053 22699611 PMC3376388 · DOI · Paper page

Cited by

Sorted by citations

Authors
Partrick, K. A., Chassaing, B., Beach, L. Q., McCann, K. E., Gewirtz, A. T., & Huhman, K. L.
Affiliations
Georgia State University (US)
Corresponding author
Partrick, Katherine A.
ORCID
Venue
Behavioural Brain Research
Publisher
Elsevier BV
Published
2018-06
Volume
345
Pages
39-48
ISSN
0166-4328 (ISSN-L)
DOI
10.1016/j.bbr.2018.02.005
PMC
PMC6246037
OpenAlex
W2789821755
Cited by
83
References
11
Citations by year
2026: 3 · 2025: 11 · 2024: 11 · 2023: 5 · 2022: 9 · 2021: 14 · 2020: 18 · 2019: 8 · 2018: 4
FWCI
3.91
Type
journal article
Language
en
Update notices
erratum (2018-08-01)
Open access
Licence
Locations
  • Behavioural Brain Research (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health (R01MH062044)
  • Brains and Behavior Seed
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
  • Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Keywords
gut microbiota, depression, social stress, microbiome diversity, microbiota-gut-brain axis, psychobiotics, probiotics, prebiotics, short-chain fatty acids, kynurenine metabolites, endocannabinoids, brain-derived neurotrophic factor, hypothalamic-pituitary-adrenal axis, intestinal barrier integrity, hyperinflammation, treatment-resistant depression, golden hamster
MeSH terms
Gastrointestinal Microbiome, Animals, Dominance-Subordination, Feces, Male, Mesocricetus, RNA, Bacterial, RNA, Ribosomal, 16S, Stress, Psychological, Time Factors, Biodiversity

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