Skip to main content
NCBI home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2004 Jan 7;271(1534):7–13. doi: 10.1098/rspb.2003.2558

The gall of subordination: changes in gall bladder function associated with social stress.

Ryan L Earley 1, Lawrence S Blumer 1, Matthew S Grober 1
PMCID: PMC1691567  PMID: 15002765

Abstract

Diverse physiological and behavioural mechanisms allow animals to effectively deal with stressors, but chronic activation of the stress axis can have severe consequences. We explored the effects of chronic social stress on agonistic behaviour and gall bladder function, a critical but widely neglected component of stress-induced gastrointestinal dysfunction. Prolonged cohabitation with dominant individuals elicited behavioural modifications and dramatically increased bile retention in subordinate convict cichlid fish (Archocentrus nigrofasciatum). The key predictor of gall bladder hypertrophy was social subordination rather than status-related differences in food intake or body size. Stress-induced inhibition of gall bladder emptying could affect energy assimilation such that subordinate animals would not be able to effectively convert energy-rich food into mass gain. These results parallel changes in gall bladder function preceding cholesterol gallstone formation in humans and other mammals. Thus, social stress may be an important diagnostic criterion in understanding pathologies associated with gall bladder dysfunction.

Full Text

The Full Text of this article is available as a PDF (270.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abbott D. H., Keverne E. B., Bercovitch F. B., Shively C. A., Mendoza S. P., Saltzman W., Snowdon C. T., Ziegler T. E., Banjevic M., Garland T., Jr Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav. 2003 Jan;43(1):67–82. doi: 10.1016/s0018-506x(02)00037-5. [DOI] [PubMed] [Google Scholar]
  2. Abou-Saif Alaa, Al-Kawas Firas H. Complications of gallstone disease: Mirizzi syndrome, cholecystocholedochal fistula, and gallstone ileus. Am J Gastroenterol. 2002 Feb;97(2):249–254. doi: 10.1111/j.1572-0241.2002.05451.x. [DOI] [PubMed] [Google Scholar]
  3. Albeck D. S., McKittrick C. R., Blanchard D. C., Blanchard R. J., Nikulina J., McEwen B. S., Sakai R. R. Chronic social stress alters levels of corticotropin-releasing factor and arginine vasopressin mRNA in rat brain. J Neurosci. 1997 Jun 15;17(12):4895–4903. doi: 10.1523/JNEUROSCI.17-12-04895.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Aldman G., Holmgren S. Intraduodenal fat and amino acids activate gallbladder motility in the rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol. 1995 Oct;100(1):27–32. doi: 10.1006/gcen.1995.1128. [DOI] [PubMed] [Google Scholar]
  5. Apstein M. D., Carey M. C. Pathogenesis of cholesterol gallstones: a parsimonious hypothesis. Eur J Clin Invest. 1996 May;26(5):343–352. doi: 10.1046/j.1365-2362.1996.148287.x. [DOI] [PubMed] [Google Scholar]
  6. Blanchard D. C., Spencer R. L., Weiss S. M., Blanchard R. J., McEwen B., Sakai R. R. Visible burrow system as a model of chronic social stress: behavioral and neuroendocrine correlates. Psychoneuroendocrinology. 1995;20(2):117–134. doi: 10.1016/0306-4530(94)e0045-b. [DOI] [PubMed] [Google Scholar]
  7. Cicala M., Guarino M. P., Vavassori P., Alloni R., Emerenziani S., Arullani A., Pallone F. Ultrasonographic assessment of gallbladder bile exchanges in healthy subjects and in gallstone patients. Ultrasound Med Biol. 2001 Nov;27(11):1445–1450. doi: 10.1016/s0301-5629(01)00452-5. [DOI] [PubMed] [Google Scholar]
  8. Condren R. M., O'Neill A., Ryan M. C. M., Barrett P., Thakore J. H. HPA axis response to a psychological stressor in generalised social phobia. Psychoneuroendocrinology. 2002 Aug;27(6):693–703. doi: 10.1016/s0306-4530(01)00070-1. [DOI] [PubMed] [Google Scholar]
  9. Coşkun T., Bozkurt A., Alican I., Ozkutlu U., Kurtel H., Yegen B. C. Pathways mediating CRF-induced inhibition of gastric emptying in rats. Regul Pept. 1997 Apr 30;69(3):113–120. doi: 10.1016/s0167-0115(96)02066-6. [DOI] [PubMed] [Google Scholar]
  10. Fox H. E., White S. A., Kao M. H., Fernald R. D. Stress and dominance in a social fish. J Neurosci. 1997 Aug 15;17(16):6463–6469. doi: 10.1523/JNEUROSCI.17-16-06463.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Guarraci Fay A., Pozo Maria J., Palomares Sara M., Firth Tracy A., Mawe Gary M. Opioid agonists inhibit excitatory neurotransmission in ganglia and at the neuromuscular junction in Guinea pig gallbladder. Gastroenterology. 2002 Feb;122(2):340–351. doi: 10.1053/gast.2002.31037. [DOI] [PubMed] [Google Scholar]
  12. Gullo L., Bolondi L., Scarpignato C., Priori P., Casanova P., Labò G. Effect of somatostatin and thyrotropin-releasing hormone on cholecystokinin-induced gallbladder emptying. Dig Dis Sci. 1986 Dec;31(12):1345–1350. doi: 10.1007/BF01299813. [DOI] [PubMed] [Google Scholar]
  13. Huhman K. L., Moore T. O., Mougey E. H., Meyerhoff J. L. Hormonal responses to fighting in hamsters: separation of physical and psychological causes. Physiol Behav. 1992 May;51(5):1083–1086. doi: 10.1016/0031-9384(92)90097-l. [DOI] [PubMed] [Google Scholar]
  14. Kaplan M. H., Wheeler W. F., Kelly M. J., Breaux F. W. Stress and diseases of the upper gut: III. Gallbladder disease. Mt Sinai J Med. 1983 Sep-Oct;50(5):398–399. [PubMed] [Google Scholar]
  15. Ko C. W., Lee S. P. Gallstone formation. Local factors. Gastroenterol Clin North Am. 1999 Mar;28(1):99–115. doi: 10.1016/s0889-8553(05)70045-5. [DOI] [PubMed] [Google Scholar]
  16. Lee C., Sarna S. K. Central regulation of gastric emptying of solid nutrient meals by corticotropin releasing factor. Neurogastroenterol Motil. 1997 Dec;9(4):221–229. doi: 10.1046/j.1365-2982.1997.d01-58.x. [DOI] [PubMed] [Google Scholar]
  17. Lenz H. J., Messmer B., Zimmerman F. G. Noradrenergic inhibition of canine gallbladder contraction and murine pancreatic secretion during stress by corticotropin-releasing factor. J Clin Invest. 1992 Feb;89(2):437–443. doi: 10.1172/JCI115603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lenz H. J., Zimmerman F. G., Messmer B. Regulation of canine gallbladder motility by brain peptides. Gastroenterology. 1993 Jun;104(6):1678–1685. doi: 10.1016/0016-5085(93)90645-s. [DOI] [PubMed] [Google Scholar]
  19. Mawe G. M. Noradrenaline as a presynaptic inhibitory neurotransmitter in ganglia of the guinea-pig gall-bladder. J Physiol. 1993 Feb;461:387–402. doi: 10.1113/jphysiol.1993.sp019519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mawe Gary M. Nerves and Hormones Interact to Control Gallbladder Function. News Physiol Sci. 1998 Apr;13(NaN):84–90. doi: 10.1152/physiologyonline.1998.13.2.84. [DOI] [PubMed] [Google Scholar]
  21. McEwen Bruce S., Wingfield John C. The concept of allostasis in biology and biomedicine. Horm Behav. 2003 Jan;43(1):2–15. doi: 10.1016/s0018-506x(02)00024-7. [DOI] [PubMed] [Google Scholar]
  22. Mönnikes H., Schmidt B. G., Taché Y. Psychological stress-induced accelerated colonic transit in rats involves hypothalamic corticotropin-releasing factor. Gastroenterology. 1993 Mar;104(3):716–723. doi: 10.1016/0016-5085(93)91006-4. [DOI] [PubMed] [Google Scholar]
  23. Nakeeb Attila, Comuzzie Anthony G., Martin Lisa, Sonnenberg Gabriele E., Swartz-Basile Debra, Kissebah Ahmed H., Pitt Henry A. Gallstones: genetics versus environment. Ann Surg. 2002 Jun;235(6):842–849. doi: 10.1097/00000658-200206000-00012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nielsen K. G., Bomgren P., Holmgren S., Johnsen A. H. Gastrin and cholecystokinin of the bullfrog, Rana catesbeiana, have distinct effects on gallbladder motility and gastric acid secretion in vitro. Gen Comp Endocrinol. 1998 Nov;112(2):247–254. doi: 10.1006/gcen.1998.7170. [DOI] [PubMed] [Google Scholar]
  25. Plourde V. Stress-induced changes in the gastrointestinal motor system. Can J Gastroenterol. 1999 Mar;13 (Suppl A):26A–31A. doi: 10.1155/1999/320626. [DOI] [PubMed] [Google Scholar]
  26. Schjoldager B., Jørgensen J. C., Johnsen A. H. Stimulation of rainbow trout gallbladder contraction by cionin, an ancestral member of the CCK/gastrin family. Gen Comp Endocrinol. 1995 Jun;98(3):269–278. doi: 10.1006/gcen.1995.1069. [DOI] [PubMed] [Google Scholar]
  27. Seasholtz A. F., Valverde R. A., Denver R. J. Corticotropin-releasing hormone-binding protein: biochemistry and function from fishes to mammals. J Endocrinol. 2002 Oct;175(1):89–97. doi: 10.1677/joe.0.1750089. [DOI] [PubMed] [Google Scholar]
  28. Sgoifo A., de Boer S. F., Haller J., Koolhaas J. M. Individual differences in plasma catecholamine and corticosterone stress responses of wild-type rats: relationship with aggression. Physiol Behav. 1996 Dec;60(6):1403–1407. doi: 10.1016/s0031-9384(96)00229-6. [DOI] [PubMed] [Google Scholar]
  29. Sloman K. A., Metcalfe N. B., Taylor A. C., Gilmour K. M. Plasma cortisol concentrations before and after social stress in rainbow trout and brown trout. Physiol Biochem Zool. 2001 May-Jun;74(3):383–389. doi: 10.1086/320426. [DOI] [PubMed] [Google Scholar]
  30. Taché Y., Martinez V., Million M., Rivier J. Corticotropin-releasing factor and the brain-gut motor response to stress. Can J Gastroenterol. 1999 Mar;13 (Suppl A):18A–25A. doi: 10.1155/1999/375916. [DOI] [PubMed] [Google Scholar]
  31. Tierney S., Qian Z., Burrow C., Lipsett P. A., Pitt H. A., Lillemoe K. D. Estrogen inhibits sphincter of Oddi motility. J Surg Res. 1994 Jul;57(1):69–73. doi: 10.1006/jsre.1994.1112. [DOI] [PubMed] [Google Scholar]
  32. Weinberg A., Creed F. Stress and psychiatric disorder in healthcare professionals and hospital staff. Lancet. 2000 Feb 12;355(9203):533–537. doi: 10.1016/S0140-6736(99)07366-3. [DOI] [PubMed] [Google Scholar]
  33. Xiao Z. L., Chen Q., Biancani P., Behar J. Mechanisms of gallbladder hypomotility in pregnant guinea pigs. Gastroenterology. 1999 Feb;116(2):411–419. doi: 10.1016/s0016-5085(99)70139-3. [DOI] [PubMed] [Google Scholar]
  34. Yoshidome H., Miyazaki M., Shimizu H., Ito H., Nakagawa K., Ambiru S., Nakajima N., Edwards M. J., Lentsch A. B. Obstructive jaundice impairs hepatic sinusoidal endothelial cell function and renders liver susceptible to hepatic ischemia/reperfusion. J Hepatol. 2000 Jul;33(1):59–67. doi: 10.1016/s0168-8278(00)80160-9. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES