The DOI matches its Crossref record; 61 of the 61 references it cites were found in a registry or an index.
Stress induces the translocation of cutaneous and gastrointestinal microflora to secondary lymphoid organs of C57BL/6 mice
Abstract
Mammals are colonized by a vast array of bacteria that reside as part of the host's microflora. Despite their enormous levels, these microorganisms tend to be restricted to cutaneous and mucosal surfaces. In the current experiment, only a small percentage of non-stressed mice exhibited detectable levels of bacteria in their inguinal lymph nodes (ILN), spleen, liver, or mesenteric lymph nodes (MLN). However, after experiencing repeated social disruption (SDR), a significant increase in the number of animals having bacteria in their ILN and MLN was found. Since SDR involves fighting in which bite wounds on the skin could provide a portal of entry into the host, it was determined whether experimental wounding (full-thickness skin biopsy), chronic restraint (which is a potent stressor that does not disrupt the skin barrier), or wounding combined with restraint would increase the occurrence of bacteria in secondary lymphoid tissues and liver. Wounding did not significantly increase the prevalence of bacteria in the ILN, MLN, or liver. Interestingly, a larger percentage of restrained and restrained plus wounded mice, in comparison to controls, had bacteria in the ILN, MLN, and liver. Although the stressors increased the number of animals that became colonized, the levels of bacteria in the stressed mice were similar to the levels found in the few non-stressed mice that did become colonized. Our results indicate that psychological components of social stress facilitate the translocation of indigenous bacteria into the host, thus identifying an additional facet through which stressors may impact health.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Increased intestinal permeability caused by stress allows microbiota to cross the gut epithelial barrier to trigger the mucosal immune reactions (42) and then transfer to secondary lymphoid organs (46) to activate the innate immune system.”
From Stress triggers flare of inflammatory bowel disease in children and adults (2019) · cites this paper as [46]
In the citing paper
“Stress can also break the established tolerance and augments immune responses in chronic intestinal inflammation.”
From Stress triggers flare of inflammatory bowel disease in children and adults (2019) · cites this paper as [46]
Citations
Cites
The indigenous gastrointestinal microflora
Berg, R. (1996) · Trends in Microbiology · doi:10.1016/0966-842x(96)10057-3 · Cited by 1,153 · cited 2×
“skin, contain unique ecosystems of bacteria (Berg, 1996).”
BackgroundSkin Microflora and Bacterial Infections of the Skin
Chiller, K., Selkin, B. A., & Murakawa, G. J. (2001) · Journal of Investigative Dermatology Symposium Proceedings · doi:10.1046/j.0022-202x.2001.00043.x · Cited by 537
Aggressive behavioral phenotypes in mice
Miczek, K. A., Maxson, S. C., Fish, E. W., & Faccidomo, S. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00298-4 · Cited by 448
Bacterial Translocation from the Gastrointestinal Tract
Berg, R. D. (1999) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-4143-1_2 · Cited by 407
Kao, J. S., Fluhr, J. W., Man, M., Fowler, A. J., Hachem, J. P., Crumrine, D. A., Ahn, S. K., Brown, B. E., Elias, P. M., & Feingold, K. R. (2003) · Journal of Investigative Dermatology · doi:10.1046/j.1523-1747.2003.12053.x · Cited by 362
Tannock, G. W., & Savage, D. C. (1974) · Infection and Immunity · doi:10.1128/iai.9.3.591-598.1974 · Cited by 349
Prenatal Stress Alters Bacterial Colonization of the Gut in Infant Monkeys
Bailey, M. T., Lubach, G. R., & Coe, C. L. (2004) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-200404000-00009 · Cited by 339
Self-citationSocial stress induces glucocorticoid resistance in subordinate animals
Avitsur, R., Stark, J. L., & Sheridan, J. F. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2001.1653 · Cited by 321
Self-citationRole of mast cells in chronic stress induced colonic epithelial barrier dysfunction in the rat
Santos, J., Yang, P.-C., Söderholm, J. D., Benjamin, M., & Perdue, M. H. (2001) · Gut · doi:10.1136/gut.48.5.630 · Cited by 313
Social stress induces glucocorticoid resistance in macrophages
Stark, J. L., Avitsur, R., Padgett, D. A., Campbell, K. A., Beck, F. M., & Sheridan, J. F. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.280.6.r1799 · Cited by 295
Self-citationForestier, C., de Champs, C., Vatoux, C., & Joly, B. (2001) · Research in Microbiology · doi:10.1016/s0923-2508(01)01188-3 · Cited by 295
Restraint Stress Slows Cutaneous Wound Healing in Mice
Padgett, D. A., Marucha, P. T., & Sheridan, J. F. (1998) · Brain Behavior and Immunity · doi:10.1006/brbi.1997.0512 · Cited by 273
Self-citationChanges of microbial flora and wound colonization in burned patients
Erol, S., Altoparlak, Ü., Akçay, M. N., Çelebi, F., & Parlak, M. (2004) · Burns · doi:10.1016/j.burns.2003.12.013 · Cited by 255
Systemic bacterial invasion induced by sleep deprivation
Everson, C. A., & Toth, L. A. (2000) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2000.278.4.r905 · Cited by 248
Freestone, P. P. E., WILLIAMS, P. H., Haigh, R., Maggs, A. F., Neal, C. P., & Lyte, M. (2002) · Shock · doi:10.1097/00024382-200211000-00014 · Cited by 232
Choi, E., Brown, B. E., Crumrine, D. A., Chang, S., Man, M., Elias, P. M., & Feingold, K. R. (2005) · Journal of Investigative Dermatology · doi:10.1111/j.0022-202x.2005.23589.x · Cited by 212
Freestone, P. P. E., Lyte, M., Neal, C. P., Maggs, A. F., Haigh, R., & WILLIAMS, P. H. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.21.6091-6098.2000 · Cited by 210
Engler, H., Bailey, M. T., Engler, A., & Sheridan, J. F. (2004) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2003.11.011 · Cited by 209
Self-citationStimulation of Staphylococcus epidermidis growth and biofilm formation by catecholamine inotropes
Lyte, M., Freestone, P. P. E., Neal, C. P., Olson, B. A., Haigh, R., Bayston, R., & WILLIAMS, P. H. (2003) · The Lancet · doi:10.1016/s0140-6736(03)12231-3 · Cited by 209
Social defeat and subordination as models of social stress in laboratory rodents: A review
Martı́nez, M., Calvo-Torrent, A., & Pico-Alfonso, M. A. (1998) · Aggressive Behavior · doi:10.1002/(sici)1098-2337(1998)24:4 · Cited by 208
Stress-Induced Susceptibility to Bacterial Infection During Cutaneous Wound Healing
Rojas, I. G., Padgett, D. A., Sheridan, J. F., & Marucha, P. T. (2002) · Brain Behavior and Immunity · doi:10.1006/brbi.2000.0619 · Cited by 204
Self-citationFerrier, L., Mazelin, L., Cénac, N., Desreumaux, P., Janin, A., Émilie, D., Colombel, J., Villar, R. G., Fioramonti, J., & Bueno, L. P. (2003) · Gastroenterology · doi:10.1016/s0016-5085(03)01057-6 · Cited by 203
Stimulation of bacterial growth by heat-stable, norepinephrine-induced autoinducers
Freestone, P. P. E., Haigh, R. D., Williams, P. H., & Lyte, M. (1999) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1999.tb13449.x · Cited by 199
Saunders, P. R., Santos, J., Hanssen, N. P. M., Yates, D. A., Groot, J. A., & Perdue, M. H. (2002) · Digestive Diseases and Sciences · doi:10.1023/a:1013204612762 · Cited by 198
Stratum Corneum Structure and Function Correlates with Phenotype in Psoriasis
Ghadially, R., Reed, J. T., & Elias, P. M. (1996) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12582813 · Cited by 191
Stress alters cutaneous permeability barrier homeostasis
Denda, M., Tsuchiya, T., Elias, P. M., & Feingold, K. R. (2000) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2000.278.2.r367 · Cited by 166
Gupta, M., & Gupta, A. K. (1996) · Journal of American Academy of Dermatology · doi:10.1016/s0190-9622(96)90284-4 · Cited by 161
Norepinephrine-Induced Expression of the K99 Pilus Adhesin of EnterotoxigenicEscherichia coli
Lyte, M., Erickson, A. K., Arulanandam, B. P., Frank, C. D., Crawford, M., & Francis, D. H. (1997) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1997.6356 · Cited by 114
Stress exposure modulates peptidergic innervation and degranulates mast cells in murine skin
Peters, E. M. J., Kuhlmei, A., Tobin, D. J., Müller‐Röver, S., Klapp, B. F., & Arck, P. (2004) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2004.08.005 · Cited by 114
Hirano, J., Yoshida, T., Sugiyama, T., Koide, N., Mori, I., & Yokochi, T. (2003) · Microbiology and Immunology · doi:10.1111/j.1348-0421.2003.tb03377.x · Cited by 113
Dobbs, C. M., Feng, N., Beck, F. M., & Sheridan, J. F. (1996) · The Journal of Immunology · doi:10.4049/jimmunol.157.5.1870 · Cited by 109
Self-citationEngler, H., Engler, A., Bailey, M. T., & Sheridan, J. F. (2005) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2005.03.002 · Cited by 108
Self-citationFilho-Lima, J. V. M., Vieira, E., & Nicoli, J. R. (2000) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2000.00973.x · Cited by 93
Hermann, G. E., Tovar, C. A., Beck, F. M., & Sheridan, J. F. (1994) · Journal of Neuroimmunology · doi:10.1016/0165-5728(94)90177-5 · Cited by 92
Self-citationSocial disruption-induced glucocorticoid resistance: kinetics and site specificity
Avitsur, R., Stark, J. L., Dhabhar, F. S., Padgett, D. A., & Sheridan, J. F. (2002) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(02)00010-3 · Cited by 92
Self-citationSocial stress alters splenocyte phenotype and function
Avitsur, R., Stark, J. L., Dhabhar, F. S., & Sheridan, J. F. (2002) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(02)00310-7 · Cited by 91
Self-citationRisk factors of development of gut-derived bacterial translocation in thermally injured rats
Zhong-tang, W. (2004) · World Journal of Gastroenterology · doi:10.3748/wjg.v10.i11.1619 · Cited by 90
Hermann, G. E., Beck, F. M., & Sheridan, J. F. (1995) · Journal of Neuroimmunology · doi:10.1016/0165-5728(94)00145-e · Cited by 85
Self-citationLytinas, M., Kempuraj, D., Huang, M., Boucher, W. S., Esposito, P., & Theoharides, T. C. (2003) · International Archives of Allergy and Immunology · doi:10.1159/000069516 · Cited by 84
Immobilization‐induced and crowded environment‐induced stress delay barrier recovery in murine skin
Denda, Tsuchiya, Hosoi, & Koyama (1998) · British Journal of Dermatology · doi:10.1046/j.1365-2133.1998.02213.x · Cited by 81
Lyte, M., Arulanandam, B. P., Nguyen, K. T., Frank, C. D., Erickson, A., & Francis, D. H. (1997) · Advances in experimental medicine and biology · doi:10.1007/978-1-4899-1828-4_54 · Cited by 79
Bailey, M. T., Avitsur, R., Engler, H., Padgett, D. A., & Sheridan, J. F. (2003) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2003.09.012 · Cited by 74
Self-citationHermann, G. E., Tovar, C. A., Beck, F. M., Allen, C. M., & Sheridan, J. F. (1993) · Journal of Neuroimmunology · doi:10.1016/0165-5728(93)90287-9 · Cited by 73
Self-citationInnate and adaptive immune responses in a social conflict paradigm
Lyte, M., Nelson, S. G., & Thompson, M. L. (1990) · Clinical Immunology and Immunopathology · doi:10.1016/0090-1229(90)90029-p · Cited by 72
Tausk, F., & Nousari, H. C. (2001) · Archives of Dermatology · doi:10.1001/archderm.137.1.78 · Cited by 67
Deitch, E. A., Kemper, A. C., Specian, R. D., & Berg, R. D. (1992) · The Journal of Trauma: Injury, Infection, and Critical Care · doi:10.1097/00005373-199202000-00005 · Cited by 67
Valencia, I. C., Kirsner, R. S., & Kerdel, F. A. (2004) · Journal of the American Academy of Dermatology · doi:10.1016/j.jaad.2003.11.064 · Cited by 60
Stress and influenza viral infection: modulation of proinflammatory cytokine responses in the lung
Konstantinos, A. P., & Sheridan, J. F. (2001) · Respiration Physiology · doi:10.1016/s0034-5687(01)00266-3 · Cited by 53
Self-citationIntestinal barrier damage caused by trauma and lipopolysaccharide
Ding, L.-A. (2004) · World Journal of Gastroenterology · doi:10.3748/wjg.v10.i16.2373 · Cited by 48
Yang, R., Gallo, D. J., Baust, J., Watkins, S. C., Delude, R. L., & Fink, M. P. (2002) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00278.2002 · Cited by 45
Ando, T., Brown, R. F., Berg, R. D., & Dunn, A. J. (2000) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2000.279.6.r2164 · Cited by 37
Odorant inhalation affects skin barrier homeostasis in mice and humans
Denda, M., Tsuchiya, T., Shoji, K., & Tanida, M. (2000) · British Journal of Dermatology · doi:10.1046/j.1365-2133.2000.03486.x · Cited by 35
Zwilling, B. S., Brown, D., & Pearl, D. K. (1992) · Journal of Neuroimmunology · doi:10.1016/0165-5728(92)90162-e · Cited by 33
Bacterial colonization and the expression of inducible nitric oxide synthase in murine wounds
Mahoney, E., Reichner, J., Robinson Bostom, L., Mastrofrancesco, B., Henry, W., & Albina, J. (2002) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)64492-6 · Cited by 33
Eradication of Methicillin-Resistant Staphylococcus aureus from Pressure Sores Using Warming Therapy
Ellis, S. L., Finn, P., Noone, M., & Leaper, D. J. (2003) · Surgical Infections · doi:10.1089/109629603764655281 · Cited by 32
Bailey, M. T., Karaszewski, J. W., Lubach, G. R., Coe, C. L., & Lyte, M. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(99)00087-6 · Cited by 31
Self-citationOrtiz, G. C., Sheridan, J. F., & Marucha, P. T. (2003) · Brain Behavior and Immunity · doi:10.1016/s0889-1591(03)00027-8 · Cited by 27
Self-citationThe Effect Of Food And Water Deprivation (Stress) On Salmonella-Carrier Mice
Tannock, G. W., & Smith, J. M. B. (1972) · Journal of Medical Microbiology · doi:10.1099/00222615-5-3-283 · Cited by 21
Lee, D. C., Barlas, D., Ryan, J. G., Ward, M. F., Sama, A. E., & Farber, B. F. (2002) · Journal of the American Geriatrics Society · doi:10.1046/j.1532-5415.2002.50377.x · Cited by 16
Persistence of Staphylococcus aureus colonization on the skin of NC/Nga mice
Hashimoto, Y., Kaneda, Y., Akashi, T., Arai, I., & Nakaike, S. (2004) · Journal of Dermatological Science · doi:10.1016/j.jdermsci.2004.04.003 · Cited by 15
Skin and soft tissues. Management of four common infections in the nursing home patient.
O’Donnell, J. A., & Hofmann, M. T. (2001) · PubMed · Cited by 10
Cited by
Sorted by citations
Bailey, M. T., Dowd, S. E., Galley, J. D., Hufnagle, A. R., Allen, R. G., & Lyte, M. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.10.023 · Cited by 1,123
“, 2010), and induces bacterial translocation (Bailey et al., 2006), and because microbiota products have been shown to be necessary for priming of innate immunity (Clarke et al.”
BackgroundInfluentialSelf-citationHaroon, E., Raison, C. L., & Miller, A. H. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.205 · Cited by 1,000
“Interestingly, in the context of stress, bacteria have been shown to translocate from the gut to lymphoid organs in laboratory mice (Bailey et al, 2006), and treatment of mice with a cocktail of antibiotics was found to both reduce intestinal microflora while eliminating the capacity of a social…”
BackgroundBrain-gut-microbe communication in health and disease
Grenham, S., Clarke, G., Cryan, J. F., & Dinan, T. G. (2011) · Frontiers in Physiology · doi:10.3389/fphys.2011.00094 · Cited by 952
“The psychological components of social stress was shown to facilitate the translocation of indigenous bacteria into the host (Bailey et al., 2006).”
BackgroundBrain–Gut Interactions in Inflammatory Bowel Disease
Bonaz, B. L., & Bernstein, C. N. (2013) · Gastroenterology · doi:10.1053/j.gastro.2012.10.003 · Cited by 667
“Stress-increased intestinal permeability allows bacteria to cross the epithelial barrier to activate mucosal immune response (57) and to translocate to secondary lymphoid organs (58) to stimulate the innate immune system.”
BackgroundRao, A. V., Bested, A. C., Beaulne, T. M., Katzman, M. A., Iorio, C., Berardi, J. M., & Logan, A. C. (2009) · Gut Pathogens · doi:10.1186/1757-4749-1-6 · Cited by 577
“tive alterations in the make-up of gastrointestinal microbes are a consequence of states of stress and fear, and alterations in the gut microflora have recently been associated with impaired glucose control and obesity [18,19].”
Background
Metadata
- Authors
- Bailey, M. T., Engler, H., & Sheridan, J. F.
- Affiliations
- The Ohio State University (US)
- Corresponding author
- Bailey, Michael T.
- Venue
- Journal of Neuroimmunology
- Publisher
- Elsevier BV
- Published
- 2006-02
- Volume
- 171
- Issue
- 1-2
- Pages
- 29-37
- ISSN
- 0165-5728 (ISSN-L)
- OpenAlex
- W2038270610
- Cited by
- 133
- References
- 61
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 4 · 2023: 4 · 2022: 5 · 2021: 6 · 2020: 7 · 2019: 7 · 2018: 4 · 2017: 5 · 2016: 10 · 2015: 8 · 2014: 3 · 2013: 9 · 2012: 10
- FWCI
- 2.50
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neuroimmunology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (R01MH046801, R01-MH46801)
- National Institute of Dental and Craniofacial Research (T32 DE14320, T32DE014320)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Stress, Anesthesia, and Immune Response
- Keywords
- psychological stress, bacterial translocation, secondary lymphoid organs, gut microbiota, skin microbiome, social stress, social disruption, inguinal lymph nodes, mesenteric lymph nodes, spleen, liver colonization, C57BL/6 mice
- MeSH terms
- Animals, Biopsy, Cell Movement, Digestive System, Lymph Nodes, Male, Mice, Inbred C57BL, Random Allocation, Restraint, Physical, Skin, Specific Pathogen-Free Organisms, Stress, Physiological, Bacterial Translocation, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
