Skip to main content
SpringerLink
Log in
Book cover

Microbial Endocrinology pp 191–212Cite as

Psychological Stress, Immunity, and the Effects on Indigenous Microflora

  • Chapter
  • First Online:

Abstract

Psychological stress is an intrinsic part of life that affects all organs of the body through direct nervous system innervation and the release of neuroendocrine hormones. The field of PsychoNeuroImmunology (PNI) has clearly demonstrated that the physiological response to psychological stressors can dramatically impact the functioning of the immune system, thus identifying one way in which susceptibility to or severity of diseases are exacerbated during stressful periods. This chapter describes research at the interface between the fields of PNI and Microbial Endocrinology to demonstrate that natural barrier defenses, such as those provided by the commensal microflora, can be disrupted by exposure to psychological stressors. These stress effects are evident in the development of the intestinal microflora in animals born from stressful pregnancy conditions, and in older animals with fully developed microbial populations. Moreover, data are presented demonstrating that exposure to different types of stressors results in the translocation of microflora from cutaneous and mucosal surfaces into regional lymph nodes. When considered together, a scenario emerges in which psychological stressors induce a neuroendocrine response that has the potential to directly or indirectly affect commensal microflora populations, the integrity of barrier defenses, and the internalization of microbes. Finally, a hypothesis is put forth in which stressor-induced alterations of the microflora contribute to the observed stressor-induced increases in inflammatory markers in the absence of overt infection.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   179.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   229.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Aberg, K. M., Radek, K. A., Choi, E. H., Kim, D. K., Demerjian, M., Hupe, M., Kerbleski, J., Gallo, R. L., Ganz, T., Mauro, T., Feingold, K. R., and Elias, P. M. 2007. Psychological stress downregulates epidermal antimicrobial peptide expression and increases severity of cutaneous infections in mice. J. Clin. Invest. 117:3339-3349.

    PubMed  CAS  Google Scholar 

  • Abreu, M. T., Vora, P., Faure, E., Thomas, L. S., Arnold, E. T., and Arditi, M. 2001. Decreased expression of Toll-like receptor-4 and MD-2 correlates with intestinal epithelial cell protection against dysregulated proinflammatory gene expression in response to bacterial lipopolysaccharide. J. Immunol. 167:1609-1616.

    PubMed  CAS  Google Scholar 

  • Altemus, M., Rao, B., Dhabhar, F. S., Ding, W., and Granstein, R. D. 2001. Stress-induced changes in skin barrier function in healthy women. J. Invest. Dermatol. 117:309-317.

    PubMed  CAS  Google Scholar 

  • Avitsur, R., Stark, J. L., and Sheridan, J. F. 2001. Social stress induces glucocorticoid resistance in subordinate animals. Horm. Behav. 39:247-257.

    PubMed  CAS  Google Scholar 

  • Avitsur, R., Stark, J. L., Dhabhar, F. S., and Sheridan, J. F. 2002. Social stress alters splenocyte phenotype and function. J. Neuroimmunol. 132:66-71.

    PubMed  CAS  Google Scholar 

  • Avitsur, R., Padgett, D. A., Dhabhar, F. S., Stark, J. L., Kramer, K. A., Engler, H., and Sheridan, J. F. 2003. Expression of glucocorticoid resistance following social stress requires a second signal. J. Leukoc. Biol. 74:507-513.

    PubMed  CAS  Google Scholar 

  • Badgley, L. E., Spiro, H. M., and Senay, E. C. 1969. Effect of mental arithmetic on gastric secretion. Psychophysiology 5:633-637.

    PubMed  CAS  Google Scholar 

  • Bailey, M. T., and Coe, C. L. 1999. Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev. Psychobiol. 35:146-155.

    PubMed  CAS  Google Scholar 

  • Bailey, M. T., Avitsur, R., Engler, H., Padgett, D. A., and Sheridan, J. F. 2004a. Physical defeat reduces the sensitivity of murine splenocytes to the suppressive effects of corticosterone. Brain Behav. Immun. 18:416-424.

    PubMed  CAS  Google Scholar 

  • Bailey, M. T., Lubach, G. R., and Coe, C. L. 2004b. Prenatal stress alters bacterial colonization of the gut in infant monkeys. J. Pediatr. Gastroenterol. Nutr. 38:414-421.

    PubMed  Google Scholar 

  • Bailey, M. T., Engler, H., and Sheridan, J. F. 2006. Stress induces the translocation of cutaneous and gastrointestinal microflora to secondary lymphoid organs of C57BL/6 mice. J. Neuroimmunol. 171:29-37.

    PubMed  CAS  Google Scholar 

  • Bailey, M. T., Engler, H., Powell, N. D., Padgett, D. A., and Sheridan, J. F. 2007. Repeated social defeat increases the bactericidal activity of splenic macrophages through a Toll-like receptor-dependent pathway. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293:R1180-R1190.

    PubMed  CAS  Google Scholar 

  • Balmer, S. E., and Wharton, B. A. 1991. Diet and faecal flora in the newborn: iron. Arch. Dis. Child. 66:1390-1394.

    PubMed  CAS  Google Scholar 

  • Beaumont, W. 1838. Experiments and observations on the gastric juice and the physiology of digestion. London: Edinburgh.

    Google Scholar 

  • Beerens, H., Romond, C., and Neut, C. 1980. Influence of breast-feeding on the bifid flora of the newborn intestine. Am. J. Clin. Nutr. 33:2434-2439.

    PubMed  CAS  Google Scholar 

  • Berg, R. D. 1996. The indigenous gastrointestinal microflora. Trends Microbiol. 4:430-435.

    PubMed  CAS  Google Scholar 

  • Berg, R. D. 1999. Bacterial translocation from the gastrointestinal tract. Adv. Exp. Med. Biol. 473:11-30.

    PubMed  CAS  Google Scholar 

  • Bernet, M. F., Brassart, D., Neeser, J. R., and Servin, A. L. 1993. Adhesion of human bifidobacterial strains to cultured human intestinal epithelial cells and inhibition of enteropathogen-cell interactions. Appl. Environ. Microbiol. 59:4121-4128.

    PubMed  CAS  Google Scholar 

  • Bernet-Camard, M. F., Lievin, V., Brassart, D., Neeser, J. R., Servin, A. L., and Hudault, S. 1997. The human Lactobacillus acidophilus strain LA1 secretes a nonbacteriocin antibacterial substance(s) active in vitro and in vivo. Appl. Environ. Microbiol. 63:2747-2753.

    PubMed  CAS  Google Scholar 

  • Bierhaus, A., Wolf, J., Andrassy, M., Rohleder, N., Humpert, P. M., Petrov, D., Ferstl, R., von Eynatten, M., Wendt, T., Rudofsky, G., Joswig, M., Morcos, M., Schwaninger, M., McEwen, B., Kirschbaum, C., and Nawroth, P. P. 2003. A mechanism converting psychosocial stress into mononuclear cell activation. Proc. Natl. Acad. Sci. USA 100:1920-1925.

    PubMed  CAS  Google Scholar 

  • Brydon, L., Edwards, S., Jia, H., Mohamed-Ali, V., Zachary, I., Martin, J. F., and Steptoe, A. 2005. Psychological stress activates interleukin-1beta gene expression in human mononuclear cells. Brain Behav. Immun. 19:540-546.

    PubMed  CAS  Google Scholar 

  • Brydon, L., Magid, K., and Steptoe, A. 2006. Platelets, coronary heart disease, and stress. Brain Behav. Immun. 20:113-119.

    PubMed  CAS  Google Scholar 

  • Campisi, J., Leem, T. H., and Fleshner, M. 2002. Acute stress decreases inflammation at the site of infection. A role for nitric oxide. Physiol. Behav. 77:291-299.

    PubMed  CAS  Google Scholar 

  • Cao, L., Hudson, C. A., and Lawrence, D. A. 2003. Acute cold/restraint stress inhibits host resistance to Listeria monocytogenes via beta1-adrenergic receptors. Brain Behav. Immun. 17:121-133.

    PubMed  CAS  Google Scholar 

  • Chen, C., Brown, D. R., Xie, Y., Green, B. T., and Lyte, M. 2003. Catecholamines modulate Escherichia coli O157:H7 adherence to murine cecal mucosa. Shock 20:183-188.

    PubMed  CAS  Google Scholar 

  • Chi, D. S., Qui, M., Krishnaswamy, G., Li, C., and Stone, W. 2003. Regulation of nitric oxide production from macrophages by lipopolysaccharide and catecholamines. Nitric Oxide 8:127-132.

    PubMed  CAS  Google Scholar 

  • Choi, E. H., Demerjian, M., Crumrine, D., Brown, B. E., Mauro, T., Elias, P. M., and Feingold, K. R. 2006. Glucocorticoid blockade reverses psychological stress-induced abnormalities in epidermal structure and function. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291:R1657-R1662.

    PubMed  CAS  Google Scholar 

  • Clarke, A. S., and Schneider, M. L. 1993. Prenatal stress has long-term effects on behavioral responses to stress in juvenile rhesus monkeys. Dev. Psychobiol. 26:293-304.

    PubMed  CAS  Google Scholar 

  • Coconnier, M. H., Bernet, M. F., Chauviere, G., and Servin, A. L. 1993a. Adhering heat-killed human Lactobacillus acidophilus, strain LB, inhibits the process of pathogenicity of diarrhoeagenic bacteria in cultured human intestinal cells. J. Diarrhoeal Dis. Res. 11:235-242.

    PubMed  CAS  Google Scholar 

  • Coconnier, M. H., Bernet, M. F., Kerneis, S., Chauviere, G., Fourniat, J., and Servin, A. L. 1993b. Inhibition of adhesion of enteroinvasive pathogens to human intestinal Caco-2 cells by Lactobacillus acidophilus strain LB decreases bacterial invasion. FEMS Microbiol. Lett. 110:299-305.

    PubMed  CAS  Google Scholar 

  • Coconnier, M. H., Lievin, V., Hemery, E., and Servin, A. L. 1998. Antagonistic activity against Helicobacter infection in vitro and in vivo by the human Lactobacillus acidophilus strain LB. Appl. Environ. Microbiol. 64:4573-4580.

    PubMed  CAS  Google Scholar 

  • Coe, C. L., and Lubach, G. R. 2003. Critical periods of special health relevance for psychoneuroimmunology. Brain Behav. Immun. 17:3-12.

    PubMed  Google Scholar 

  • Coe, C. L., Lubach, G. R., Karaszewski, J. W., and Ershler, W. B. 1996. Prenatal endocrine activation alters postnatal cellular immunity in infant monkeys. Brain Behav. Immun. 10:221-234.

    PubMed  CAS  Google Scholar 

  • Coe, C. L., Lubach, G. R., and Karaszewski, J. W. 1999. Prenatal stress and immune recognition of self and nonself in the primate neonate. Biol. Neonate 76:301-310.

    PubMed  CAS  Google Scholar 

  • Coe, C. L., Lulbach, G. R., and Schneider, M. L. 2002. Prenatal disturbance alters the size of the corpus callosum in young monkeys. Dev. Psychobiol. 41:178-185.

    PubMed  Google Scholar 

  • Coe, C. L., Kramer, M., Czeh, B., Gould, E., Reeves, A. J., Kirschbaum, C., and Fuchs, E. 2003. Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol. Psychiatry 54:1025-1034.

    PubMed  CAS  Google Scholar 

  • Coe, C. L., Lubach, G. R., and Shirtcliff, E. A. 2007. Maternal stress during pregnancy predisposes for iron deficiency in infant monkeys impacting innate immunity. Pediatr. Res. 61:520-524.

    PubMed  CAS  Google Scholar 

  • Cohen, S. 2005. Keynote Presentation at the Eight International Congress of Behavioral Medicine: the Pittsburgh common cold studies: psychosocial predictors of susceptibility to respiratory infectious illness. Int. J. Behav. Med. 12:123-131.

    PubMed  Google Scholar 

  • Cole, S. W., Hawkley, L. C., Arevalo, J. M., Sung, C. Y., Rose, R. M., and Cacioppo, J. T. 2007. Social regulation of gene expression in human leukocytes. Genome Biol. 8:R189.

    PubMed  Google Scholar 

  • Cooperstock, M. S., and Zed, A. J. 1983. Intestinal microflora of infants. In D. Hentges (Ed.), Human Intestinal Microflora in Health and Disease (pp. 79-99). New York: Academic.

    Google Scholar 

  • Coussons-Read, M. E., Okun, M. L., and Nettles, C. D. 2007. Psychosocial stress increases inflammatory markers and alters cytokine production across pregnancy. Brain Behav. Immun. 21:343-350.

    PubMed  CAS  Google Scholar 

  • De Champlain, J. 1971. Degeneration and regrowth of adrenergic nerve fibers in the rat peripheral tissues after 6-hydroxydopamine. Can. J. Physiol. Pharmacol. 49:345-355.

    Google Scholar 

  • Denda, M., Tsuchiya, T., Elias, P. M., and Feingold, K. R. 2000. Stress alters cutaneous permeability barrier homeostasis. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278:R367-R372.

    PubMed  CAS  Google Scholar 

  • Dobbs, C. M., Vasquez, M., Glaser, R., and Sheridan, J. F. 1993. Mechanisms of stress-induced modulation of viral pathogenesis and immunity. J. Neuroimmunol. 48:151-160.

    PubMed  CAS  Google Scholar 

  • Dobbs, C. M., Feng, N., Beck, F. M., and Sheridan, J. F. 1996. Neuroendocrine regulation of cytokine production during experimental influenza viral infection: effects of restraint stress-induced elevation in endogenous corticosterone. J. Immunol. 157:1870-1877.

    PubMed  CAS  Google Scholar 

  • Drasar, B. S., Shiner, M., and McLeod, G. M. 1969. Studies on the intestinal flora. I. The bacterial flora of the gastrointestinal tract in healthy and achlorhydric persons. Gastroenterology 56:71-79.

    PubMed  CAS  Google Scholar 

  • Elftman, M. D., Norbury, C. C., Bonneau, R. H., and Truckenmiller, M. E. 2007. Corticosterone impairs dendritic cell maturation and function. Immunology 122:279-290.

    PubMed  CAS  Google Scholar 

  • Engler, H., Engler, A., Bailey, M. T., and Sheridan, J. F. 2005. Tissue-specific alterations in the glucocorticoid sensitivity of immune cells following repeated social defeat in mice. J. Neuroimmunol. 163:110-119.

    PubMed  CAS  Google Scholar 

  • Engler, H., Bailey, M. T., Engler, A., Stiner-Jones, L. M., Quan, N., and Sheridan, J. F. 2008. Interleukin-1 receptor type 1-deficient mice fail to develop social stress-associated glucocorticoid resistance in the spleen. Psychoneuroendocrinology 33:108-117.

    PubMed  CAS  Google Scholar 

  • Everson, C. A., and Toth, L. A. 2000. Systemic bacterial invasion induced by sleep deprivation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278:R905-R916.

    PubMed  CAS  Google Scholar 

  • Fagarasan, S., Muramatsu, M., Suzuki, K., Nagaoka, H., Hiai, H., and Honjo, T. 2002. Critical roles of activation-induced cytidine deaminase in the homeostasis of gut flora. Science 298:1424-1427.

    PubMed  CAS  Google Scholar 

  • Field, T., Sandberg, D., Quetel, T. A., Garcia, R., and Rosario, M. 1985. Effects of ultrasound feedback on pregnancy anxiety, fetal activity, and neonatal outcome. Obstet. Gynecol. 66:525-528.

    PubMed  CAS  Google Scholar 

  • Frank, D. N., St Amand, A. L., Feldman, R. A., Boedeker, E. C., Harpaz, N., and Pace, N. R. 2007. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. USA 104:13780-13785.

    PubMed  CAS  Google Scholar 

  • Freestone, P. P., Williams, P. H., Haigh, R. D., Maggs, A. F., Neal, C. P., and Lyte, M. 2002. Growth stimulation of intestinal commensal Escherichia coli by catecholamines: a possible contributory factor in trauma-induced sepsis. Shock 18:465-470.

    PubMed  Google Scholar 

  • Freestone, P. P., Sandrini, S. M., Haigh, R. D., and Lyte, M. 2008. Microbial endocrinology: how stress influences susceptibility to infection. Trends Microbiol. 16:55-64.

    PubMed  CAS  Google Scholar 

  • Garcia, J. J., del Carmen, S. M., De la, F. M., and Ortega, E. 2003. Regulation of phagocytic process of macrophages by noradrenaline and its end metabolite 4-hydroxy-3-metoxyphenyl-glycol. Role of alpha- and beta-adrenoreceptors. Mol. Cell. Biochem. 254:299-304.

    PubMed  CAS  Google Scholar 

  • Ge, Z., Feng, Y., Taylor, N. S., Ohtani, M., Polz, M. F., Schauer, D. B., and Fox, J. G. 2006. Colonization dynamics of altered Schaedler flora is influenced by gender, aging, and Helicobacter hepaticus infection in the intestines of Swiss Webster mice. Appl. Environ. Microbiol. 72:5100-5103.

    PubMed  CAS  Google Scholar 

  • Gill, S. R., Pop, M., Deboy, R. T., Eckburg, P. B., Turnbaugh, P. J., Samuel, B. S., Gordon, J. I., Relman, D. A., Fraser-Liggett, C. M., and Nelson, K. E. 2006. Metagenomic analysis of the human distal gut microbiome. Science 312:1355-1359.

    PubMed  CAS  Google Scholar 

  • Glaser, R., Kiecolt-Glaser, J. K., Bonneau, R. H., Malarkey, W., Kennedy, S., and Hughes, J. 1992. Stress-induced modulation of the immune response to recombinant hepatitis B vaccine. Psychosom. Med. 54:22-29.

    PubMed  CAS  Google Scholar 

  • Gordon, J. I., Hooper, L. V., McNevin, M. S., Wong, M., and Bry, L. 1997. Epithelial cell growth and differentiation. III. Promoting diversity in the intestine: conversations between the microflora, epithelium, and diffuse GALT. Am. J. Physiol. 273:G565-G570.

    PubMed  CAS  Google Scholar 

  • Green, B. T., Lyte, M., Kulkarni-Narla, A., and Brown, D. R. 2003. Neuromodulation of entero­pathogen internalization in Peyer’s patches from porcine jejunum. J. Neuroimmunol. 141:74-82.

    PubMed  CAS  Google Scholar 

  • Green, B. T., Lyte, M., Chen, C., Xie, Y., Casey, M. A., Kulkarni-Narla, A., Vulchanova, L., and Brown, D. R. 2004. Adrenergic modulation of Escherichia coli O157:H7 adherence to the colonic mucosa. Am. J. Physiol Gastrointest. Liver Physiol. 287:G1238-G1246.

    PubMed  CAS  Google Scholar 

  • Heine, W., Mohr, C., and Wutzke, K. D. 1992. Host-microflora correlations in infant nutrition. Prog. Food Nutr. Sci. 16:181-197.

    PubMed  CAS  Google Scholar 

  • Hermann, G., Beck, F. M., and Sheridan, J. F. 1995. Stress-induced glucocorticoid response modulates mononuclear cell trafficking during an experimental influenza viral infection. J. Neuroimmunol. 56:179-186.

    PubMed  CAS  Google Scholar 

  • Holdeman, L. V., Good, I. J., and Moore, W. E. 1976. Human fecal flora: variation in bacterial composition within individuals and a possible effect of emotional stress. Appl. Environ. Microbiol. 31:359-375.

    PubMed  CAS  Google Scholar 

  • Holtmann, G., Kriebel, R., and Singer, M. V. 1990. Mental stress and gastric acid secretion. Do personality traits influence the response? Dig. Dis. Sci. 35:998-1007.

    PubMed  CAS  Google Scholar 

  • Hudault, S., Lievin, V., Bernet-Camard, M. F., and Servin, A. L. 1997. Antagonistic activity exerted in vitro and in vivo by Lactobacillus casei (strain GG) against Salmonella typhimurium C5 infection. Appl. Environ. Microbiol. 63:513-518.

    PubMed  CAS  Google Scholar 

  • Jabaaij, L., van Hattum, J., Vingerhoets, J. J., Oostveen, F. G., Duivenvoorden, H. J., and Ballieux, R. E. 1996. Modulation of immune response to rDNA hepatitis B vaccination by psychological stress. J. Psychosom. Res. 41:129-137.

    PubMed  CAS  Google Scholar 

  • Jarillo-Luna, A., Rivera-Aguilar, V., Garfias, H. R., Lara-Padilla, E., Kormanovsky, A., and Campos-Rodriguez, R. 2007. Effect of repeated restraint stress on the levels of intestinal IgA in mice. Psychoneuroendocrinology 32:681-692.

    PubMed  CAS  Google Scholar 

  • Johnson-Henry, K. C., Mitchell, D. J., Avitzur, Y., Galindo-Mata, E., Jones, N. L., and Sherman, P. M. 2004. Probiotics reduce bacterial colonization and gastric inflammation in H. pylori-infected mice. Dig. Dis. Sci. 49:1095-1102.

    PubMed  Google Scholar 

  • Johnson-Henry, K. C., Nadjafi, M., Avitzur, Y., Mitchell, D. J., Ngan, B. Y., Galindo-Mata, E., Jones, N. L., and Sherman, P. M. 2005. Amelioration of the effects of Citrobacter rodentium infection in mice by pretreatment with probiotics. J. Infect. Dis. 191:2106-2117.

    PubMed  Google Scholar 

  • Kellow, J. E., Langeluddecke, P. M., Eckersley, G. M., Jones, M. P., and Tennant, C. C. 1992. Effects of acute psychologic stress on small-intestinal motility in health and the irritable bowel syndrome. Scand. J. Gastroenterol. 27:53-58.

    PubMed  CAS  Google Scholar 

  • Kiecolt-Glaser, J. K., Glaser, R., Gravenstein, S., Malarkey, W. B., and Sheridan, J. 1996. Chronic stress alters the immune response to influenza virus vaccine in older adults. Proc. Natl. Acad. Sci. USA 93:3043-3047.

    PubMed  CAS  Google Scholar 

  • Knowles, S. R., Nelson, E. A., and Palombo, E. A. 2008. Investigating the role of perceived stress on bacterial flora activity and salivary cortisol secretion: a possible mechanism underlying susceptibility to illness. Biol. Psychol. 77:132-137.

    PubMed  Google Scholar 

  • Korneva, E. A., Rybakina, E. G., Orlov, D. S., Shamova, O. V., Shanin, S. N., and Kokryakov, V. N. 1997. Interleukin-1 and defensins in thermoregulation, stress, and immunity. Ann. NY Acad. Sci. 813:465-473.

    PubMed  CAS  Google Scholar 

  • Lederman, R. P. 1986. Maternal anxiety in pregnancy: relationship to fetal and newborn health status. Annu. Rev. Nurs. Res. 4:3-19.

    PubMed  CAS  Google Scholar 

  • Lederman, E., Lederman, R. P., Work, B. A., Jr., and McCann, D. S. 1981. Maternal psychological and physiologic correlates of fetal-newborn health status. Am. J. Obstet. Gynecol. 139:956-958.

    PubMed  CAS  Google Scholar 

  • Lenz, H. J., Raedler, A., Greten, H., Vale, W. W., and Rivier, J. E. 1988. Stress-induced gastrointestinal secretory and motor responses in rats are mediated by endogenous corticotropin-releasing factor. Gastroenterology 95:1510-1517.

    PubMed  CAS  Google Scholar 

  • Lizko, N. N. 1987. Stress and intestinal microflora. Nahrung 31:443-447.

    PubMed  CAS  Google Scholar 

  • Lyte, M. 2004. Microbial endocrinology and infectious disease in the 21st century. Trends Microbiol. 12:14-20.

    PubMed  CAS  Google Scholar 

  • Lyte, M., and Bailey, M. T. 1997. Neuroendocrine-bacterial interactions in a neurotoxin-induced model of trauma. J. Surg. Res. 70:195-201.

    PubMed  CAS  Google Scholar 

  • Lyte, M., Nelson, S. G., and Thompson, M. L. 1990. Innate and adaptive immune responses in a social conflict paradigm. Clin. Immunol. Immunopathol. 57:137-147.

    PubMed  CAS  Google Scholar 

  • MacFarlane, A. S., Peng, X., Meissler, J. J., Jr., Rogers, T. J., Geller, E. B., Adler, M. W., and Eisenstein, T. K. 2000. Morphine increases susceptibility to oral Salmonella typhimurium infection. J. Infect. Dis. 181:1350-1358.

    PubMed  CAS  Google Scholar 

  • Marshall, J. C., Christou, N. V., Horn, R., and Meakins, J. L. 1988. The microbiology of multiple organ failure. The proximal gastrointestinal tract as an occult reservoir of pathogens. Arch. Surg. 123:309-315.

    PubMed  CAS  Google Scholar 

  • Martinez, V., Rivier, J., Wang, L., and Tache, Y. 1997. Central injection of a new corticotropin-releasing factor (CRF) antagonist, astressin, blocks CRF- and stress-related alterations of gastric and colonic motor function. J. Pharmacol. Exp. Ther. 280:754-760.

    PubMed  CAS  Google Scholar 

  • Metchnikoff, E. 1908. The prolongation of life. New York: GP Putnam’s Sons.

    Google Scholar 

  • Meynell, G. G. 1963. Antibacterial mechanisms of the mouse gut. II. The role of Eh and volatile fatty acids in the normal gut. Br. J. Exp. Pathol. 44:209-219.

    PubMed  CAS  Google Scholar 

  • Miller, G. E., Chen, E., Sze, J., Marin, T., Arevalo, J. M., Doll, R., Ma, R., and Cole, S. W. 2008. A functional genomic fingerprint of chronic stress in humans: blunted glucocorticoid and increased NF-kappaB signaling. Biol. Psychiatry 64(4):266-272.

    PubMed  CAS  Google Scholar 

  • Murakami, M., Lam, S. K., Inada, M., and Miyake, T. 1985. Pathophysiology and pathogenesis of acute gastric mucosal lesions after hypothermic restraint stress in rats. Gastroenterology 88:660-665.

    PubMed  CAS  Google Scholar 

  • Nakade, Y., Tsuchida, D., Fukuda, H., Iwa, M., Pappas, T. N., and Takahashi, T. 2005. Restraint stress delays solid gastric emptying via a central CRF and peripheral sympathetic neuron in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288:R427-R432.

    PubMed  CAS  Google Scholar 

  • Nieuwenhuijzen, G. A., Deitch, E. A., and Goris, R. J. 1996a. Infection, the gut and the development of the multiple organ dysfunction syndrome. Eur. J. Surg. 162:259-273.

    PubMed  CAS  Google Scholar 

  • Nieuwenhuijzen, G. A., Deitch, E. A., and Goris, R. J. 1996b. The relationship between gut-derived bacteria and the development of the multiple organ dysfunction syndrome. J. Anat. 189 (Pt 3):537-548.

    PubMed  Google Scholar 

  • O’Hara, A. M., and Shanahan, F. 2006. The gut flora as a forgotten organ. EMBO Rep. 7:688-693.

    PubMed  Google Scholar 

  • Otte, J. M., Cario, E., and Podolsky, D. K. 2004. Mechanisms of cross hyporesponsiveness to Toll-like receptor bacterial ligands in intestinal epithelial cells. Gastroenterology 126:1054-1070.

    PubMed  CAS  Google Scholar 

  • Padgett, D. A., and Glaser, R. 2003. How stress influences the immune response. Trends Immunol. 24:444-448.

    PubMed  CAS  Google Scholar 

  • Porlier, G. A., Nadeau, R. A., De, C. J., and Bichet, D. G. 1977. Increased circulating plasma catecholamines and plasma renin activity in dogs after chemical sympathectomy with 6-hydroxydopamine. Can. J. Physiol. Pharmacol. 55:724-733.

    PubMed  CAS  Google Scholar 

  • Quan, N., Avitsur, R., Stark, J. L., He, L., Lai, W., Dhabhar, F., and Sheridan, J. F. 2003. Molecular mechanisms of glucocorticoid resistance in splenocytes of socially stressed male mice. J. Neuroimmunol. 137:51-58.

    PubMed  CAS  Google Scholar 

  • Rawls, J. F., Mahowald, M. A., Ley, R. E., and Gordon, J. I. 2006. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell 127:423-433.

    PubMed  CAS  Google Scholar 

  • Sakata, H., Yoshioka, H., and Fujita, K. 1985. Development of the intestinal flora in very low birth weight infants compared to normal full-term newborns. Eur. J. Pediatr. 144:186-190.

    PubMed  CAS  Google Scholar 

  • Salzman, N. H., Underwood, M. A., and Bevins, C. L. 2007. Paneth cells, defensins, and the commensal microbiota: a hypothesis on intimate interplay at the intestinal mucosa. Semin. Immunol. 19:70-83.

    PubMed  CAS  Google Scholar 

  • Sangild, P. T., Hilsted, L., Nexo, E., Fowden, A. L., and Silver, M. 1994. Secretion of acid, gastrin, and cobalamin-binding proteins by the fetal pig stomach: developmental regulation by cortisol. Exp. Physiol. 79:135-146.

    PubMed  CAS  Google Scholar 

  • Saunders, P. R., Kosecka, U., McKay, D. M., and Perdue, M. H. 1994. Acute stressors stimulate ion secretion and increase epithelial permeability in rat intestine. Am. J. Physiol. 267:G794-G799.

    PubMed  CAS  Google Scholar 

  • Saunders, P. R., Hanssen, N. P., and Perdue, M. H. 1997. Cholinergic nerves mediate stress-induced intestinal transport abnormalities in Wistar-Kyoto rats. Am. J. Physiol. 273:G486-G490.

    PubMed  CAS  Google Scholar 

  • Saunders, P. R., Santos, J., Hanssen, N. P., Yates, D., Groot, J. A., and Perdue, M. H. 2002. Physical and psychological stress in rats enhances colonic epithelial permeability via peripheral CRH. Dig. Dis. Sci. 47:208-215.

    PubMed  Google Scholar 

  • Schaedler, R. W., and Dubos, R. J. 1962. The fecal flora of various strains of mice. Its bearing on their susceptibility to endotoxin. J. Exp. Med. 115:1149-1160.

    PubMed  CAS  Google Scholar 

  • Schiffrin, E. J., Carter, E. A., Walker, W. A., Frieberg, E., Benjamin, J., and Israel, E. J. 1993. Influence of prenatal corticosteroids on bacterial colonization in the newborn rat. J. Pediatr. Gastroenterol. Nutr. 17:271-275.

    PubMed  CAS  Google Scholar 

  • Schneider, M. L., and Coe, C. L. 1993. Repeated social stress during pregnancy impairs neuromotor development of the primate infant. J. Dev. Behav. Pediatr. 14:81-87.

    PubMed  CAS  Google Scholar 

  • Schneider, M. L., Clarke, A. S., Kraemer, G. W., Roughton, E. C., Lubach, G. R., Rimm-Kaufman, S., Schmidt, D., and Ebert, M. 1998. Prenatal stress alters brain biogenic amine levels in primates. Dev. Psychopathol. 10:427-440.

    PubMed  CAS  Google Scholar 

  • Scott, L. D., and Cahall, D. L. 1982. Influence of the interdigestive myoelectric complex on enteric flora in the rat. Gastroenterology 82:737-745.

    PubMed  CAS  Google Scholar 

  • Shanahan, F. 2002. The host-microbe interface within the gut. Best Pract. Res. Clin. Gastroenterol. 16:915-931.

    PubMed  Google Scholar 

  • Soderholm, J. D., and Perdue, M. H. 2001. Stress and gastrointestinal tract. II. Stress and intestinal barrier function. Am. J. Physiol. Gastrointest. Liver Physiol. 280:G7-G13.

    PubMed  CAS  Google Scholar 

  • Stark, J. L., Avitsur, R., Padgett, D. A., Campbell, K. A., Beck, F. M., and Sheridan, J. F. 2001. Social stress induces glucocorticoid resistance in macrophages. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280:R1799-R1805.

    PubMed  CAS  Google Scholar 

  • Steffen, E. K., and Berg, R. D. 1983. Relationship between cecal population levels of indigenous bacteria and translocation to the mesenteric lymph nodes. Infect. Immun. 39:1252-1259.

    PubMed  CAS  Google Scholar 

  • Stepankova, R., Sinkora, J., Hudcovic, T., Kozakova, H., and Tlaskalova-Hogenova, H. 1998. Differences in development of lymphocyte subpopulations from gut-associated lymphatic tissue (GALT) of germfree and conventional rats: effect of aging. Folia Microbiol. (Praha) 43:531-534.

    CAS  Google Scholar 

  • Steptoe, A., Hamer, M., and Chida, Y. 2007. The effects of acute psychological stress on circulating inflammatory factors in humans: a review and meta-analysis. Brain Behav. Immun. 21:901-912.

    PubMed  CAS  Google Scholar 

  • Sternberg, E. M. 2006. Neural regulation of innate immunity: a coordinated nonspecific host response to pathogens. Nat. Rev. Immunol. 6:318-328.

    PubMed  CAS  Google Scholar 

  • Tache, Y., Martinez, V., Million, M., and Wang, L. 2001. Stress and the gastrointestinal tract III. Stress-related alterations of gut motor function: role of brain corticotropin-releasing factor receptors. Am. J. Physiol. Gastrointest. Liver Physiol. 280:G173-G177.

    PubMed  CAS  Google Scholar 

  • Tan, K. S., Nackley, A. G., Satterfield, K., Maixner, W., Diatchenko, L., and Flood, P. M. 2007. Beta2 adrenergic receptor activation stimulates pro-inflammatory cytokine production in macrophages via PKA- and NF-kappaB-independent mechanisms. Cell Signal. 19:251-260.

    PubMed  CAS  Google Scholar 

  • Tannock, G. W., Fuller, R., Smith, S. L., and Hall, M. A. 1990. Plasmid profiling of members of the family Enterobacteriaceae, lactobacilli, and bifidobacteria to study the transmission of bacteria from mother to infant. J. Clin. Microbiol. 28:1225-1228.

    PubMed  CAS  Google Scholar 

  • Trahair, J. F., and Sangild, P. T. 1997. Systemic and luminal influences on the perinatal development of the gut. Equine Vet. J. Suppl. (24):40-50.

    Google Scholar 

  • Truckenmiller, M. E., Princiotta, M. F., Norbury, C. C., and Bonneau, R. H. 2005. Corticosterone impairs MHC class I antigen presentation by dendritic cells via reduction of peptide generation. J. Neuroimmunol. 160:48-60.

    PubMed  CAS  Google Scholar 

  • Truckenmiller, M. E., Bonneau, R. H., and Norbury, C. C. 2006. Stress presents a problem for dendritic cells: corticosterone and the fate of MHC class I antigen processing and presentation. Brain Behav. Immun. 20:210-218.

    PubMed  CAS  Google Scholar 

  • Umesaki, Y., Setoyama, H., Matsumoto, S., and Okada, Y. 1993. Expansion of alpha beta T-cell receptor-bearing intestinal intraepithelial lymphocytes after microbial colonization in germ-free mice and its independence from thymus. Immunology 79:32-37.

    PubMed  CAS  Google Scholar 

  • Umesaki, Y., Okada, Y., Matsumoto, S., Imaoka, A., and Setoyama, H. 1995. Segmented filamentous bacteria are indigenous intestinal bacteria that activate intraepithelial lymphocytes and induce MHC class II molecules and fucosyl asialo GM1 glycolipids on the small intestinal epithelial cells in the ex-germ-free mouse. Microbiol. Immunol. 39:555-562.

    PubMed  CAS  Google Scholar 

  • Wharton, B. A., Balmer, S. E., and Scott, P. H. 1994a. Faecal flora in the newborn. Effect of lactoferrin and related nutrients. Adv. Exp. Med. Biol. 357:91-98.

    PubMed  CAS  Google Scholar 

  • Wharton, B. A., Balmer, S. E., and Scott, P. H. 1994b. Sorrento studies of diet and fecal flora in the newborn. Acta Paediatr. Jpn. 36:579-584.

    PubMed  CAS  Google Scholar 

  • Yang, H., Yuan, P. Q., Wang, L., and Tache, Y. 2000. Activation of the parapyramidal region in the ventral medulla stimulates gastric acid secretion through vagal pathways in rats. Neuroscience 95:773-779.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Oral Biology, College of Dentistry, The Ohio State University, 305 W. 12th Ave, Columbus, OH, 43210, USA

    Michael T. Bailey

Authors
  1. Michael T. Bailey
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael T. Bailey .

Editor information

Editors and Affiliations

  1. Health Sciences Center, School of Pharmacy, Texas Tech University, 4th Street 3601, Lubbock, 79430, USA

    Mark Lyte

  2. School of Medicine, Dept. Infection, Immunity & Inflammation, University of Leicester, Leicester, United Kingdom

    Primrose P.E. Freestone

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag New York

About this chapter

Cite this chapter

Bailey, M.T. (2010). Psychological Stress, Immunity, and the Effects on Indigenous Microflora. In: Lyte, M., Freestone, P. (eds) Microbial Endocrinology. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-5576-0_11

Download citation

Publish with us

Policies and ethics

Search

Navigation