Skip to main content
Gut logoLink to Gut
. 1996 Jan;38(1):59–65. doi: 10.1136/gut.38.1.59

Calcium in milk and fermentation by yoghurt bacteria increase the resistance of rats to Salmonella infection.

I Bovee-Oudenhoven 1, D Termont 1, R Dekker 1, R Van der Meer 1
PMCID: PMC1382980  PMID: 8566860

Abstract

Calcium in milk products stimulates gastric acid secretion and inhibits the cytolytic activity of intestinal contents. Based on these effects, it was hypothesised that calcium might lessen the severity of food borne intestinal infections. The possible differential effects of a low calcium milk and normal milk products (milk, acidified milk, and pasteurised yoghurt) on the resistance of rats to a salmonella infection was therefore studied. Rats were infected orally with Salmonella enteritidis just after food consumption. The first day after infection, faecal salmonella counts of the yoghurt fed rats were significantly lower than those of the other groups. Thereafter, faecal salmonella excretion declined rapidly in all high calcium groups, whereas rats fed the low calcium milk continued to excrete high numbers of salmonella. The reduced colonisation resistance to salmonella of rats fed low calcium milk might be caused by the high cytolytic activity of faecal water or a high iron concentration in faecal water, already present before infection, or both. The reduced resistance of these rats corresponded with a large infection induced increase in the cytolytic activity of faecal water, an appreciable reduction in apparent iron absorption, and a large increase in faecal mucin and alkaline phosphatase excretion. In yoghurt fed rats, only minor infection induced changes in luminal parameters were noticed. The rats fed milk and acidified milk always showed intermediate reactions. In conclusion, in addition to fermentation by yoghurt bacteria, calcium in milk products strongly enhanced the resistance to salmonella infection by lowering luminal cytolytic activity or diminishing the availability of iron for pathogen growth, or both.

Full text

PDF
59

Selected References

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

  1. Arnold J. W., Klimpel G. R., Niesel D. W. Tumor necrosis factor (TNF alpha) regulates intestinal mucus production during salmonellosis. Cell Immunol. 1993 Oct 15;151(2):336–344. doi: 10.1006/cimm.1993.1243. [DOI] [PubMed] [Google Scholar]
  2. Bezkorovainy A. Biochemistry of nonheme iron in man. I. Iron proteins and cellular iron metabolism. Clin Physiol Biochem. 1989;7(1):1–17. [PubMed] [Google Scholar]
  3. Cabotaje L. M., Shinnick F. L., Lopéz-Guisa J. M., Marlett J. A. Mucin secretion in germfree rats fed fiber-free and psyllium diets and bacterial mass and carbohydrate fermentation after colonization. Appl Environ Microbiol. 1994 Apr;60(4):1302–1307. doi: 10.1128/aem.60.4.1302-1307.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cariani G., Vandelli A. Salmonellosis-induced hemorrhage and ulcerations of the colon. Endoscopy. 1993 Sep;25(7):488–488. doi: 10.1055/s-2007-1010377. [DOI] [PubMed] [Google Scholar]
  5. Cohen M. S. Molecular events in the activation of human neutrophils for microbial killing. Clin Infect Dis. 1994 Feb;18 (Suppl 2):S170–S179. doi: 10.1093/clinids/18.supplement_2.s170. [DOI] [PubMed] [Google Scholar]
  6. Collins F. M. Salmonellosis in orally infected specific pathogen-free C57B1 mice. Infect Immun. 1972 Feb;5(2):191–198. doi: 10.1128/iai.5.2.191-198.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Crowther R. S., Wetmore R. F. Fluorometric assay of O-linked glycoproteins by reaction with 2-cyanoacetamide. Anal Biochem. 1987 May 15;163(1):170–174. doi: 10.1016/0003-2697(87)90108-4. [DOI] [PubMed] [Google Scholar]
  8. Eastwood M. A. The physiological effect of dietary fiber: an update. Annu Rev Nutr. 1992;12:19–35. doi: 10.1146/annurev.nu.12.070192.000315. [DOI] [PubMed] [Google Scholar]
  9. Floor M. K., Jahangeer S., D'Ambrosio C., Alabaster O. Serum gastrin increases with increasing dietary calcium but not with increasing dietary fat or fiber in Fischer-344 rats. J Nutr. 1991 Jun;121(6):863–868. doi: 10.1093/jn/121.6.863. [DOI] [PubMed] [Google Scholar]
  10. Giaffer M. H., Holdsworth C. D., Duerden B. I. The assessment of faecal flora in patients with inflammatory bowel disease by a simplified bacteriological technique. J Med Microbiol. 1991 Oct;35(4):238–243. doi: 10.1099/00222615-35-4-238. [DOI] [PubMed] [Google Scholar]
  11. Gorden J., Small P. L. Acid resistance in enteric bacteria. Infect Immun. 1993 Jan;61(1):364–367. doi: 10.1128/iai.61.1.364-367.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Govers M. J., Termont D. S., Van der Meer R. Mechanism of the antiproliferative effect of milk mineral and other calcium supplements on colonic epithelium. Cancer Res. 1994 Jan 1;54(1):95–100. [PubMed] [Google Scholar]
  13. Hara H., Nishikawa H., Kiriyama S. Different effects of casein and soyabean protein on gastric emptying of protein and small intestinal transit after spontaneous feeding of diets in rats. Br J Nutr. 1992 Jul;68(1):59–66. doi: 10.1079/bjn19920066. [DOI] [PubMed] [Google Scholar]
  14. Hiraishi H., Terano A., Ota S., Mutoh H., Sugimoto T., Razandi M., Ivey K. J. Oxygen metabolites stimulate mucous glycoprotein secretion from cultured rat gastric mucous cells. Am J Physiol. 1991 Oct;261(4 Pt 1):G662–G668. doi: 10.1152/ajpgi.1991.261.4.G662. [DOI] [PubMed] [Google Scholar]
  15. Kent S., Weinberg E. D., Stuart-Macadam P. The etiology of the anemia of chronic disease and infection. J Clin Epidemiol. 1994 Jan;47(1):23–33. doi: 10.1016/0895-4356(94)90030-2. [DOI] [PubMed] [Google Scholar]
  16. Lapré J. A., De Vries H. T., Koeman J. H., Van der Meer R. The antiproliferative effect of dietary calcium on colonic epithelium is mediated by luminal surfactants and dependent on the type of dietary fat. Cancer Res. 1993 Feb 15;53(4):784–789. [PubMed] [Google Scholar]
  17. Lapré J. A., De Vries H. T., Termont D. S., Kleibeuker J. H., De Vries E. G., Van der Meer R. Mechanism of the protective effect of supplemental dietary calcium on cytolytic activity of fecal water. Cancer Res. 1993 Jan 15;53(2):248–253. [PubMed] [Google Scholar]
  18. Lapré J. A., De Vries H. T., Van der Meer R. Cytotoxicity of fecal water is dependent on the type of dietary fat and is reduced by supplemental calcium phosphate in rats. J Nutr. 1993 Mar;123(3):578–585. doi: 10.1093/jn/123.3.587. [DOI] [PubMed] [Google Scholar]
  19. Lapré J. A., Termont D. S., Groen A. K., Van der Meer R. Lytic effects of mixed micelles of fatty acids and bile acids. Am J Physiol. 1992 Sep;263(3 Pt 1):G333–G337. doi: 10.1152/ajpgi.1992.263.3.G333. [DOI] [PubMed] [Google Scholar]
  20. Levant J. A., Walsh J. H., Isenberg J. I. Stimulation of gastric secretion and gastrin release by single oral doses of calcium carbonate in man. N Engl J Med. 1973 Sep 13;289(11):555–558. doi: 10.1056/NEJM197309132891104. [DOI] [PubMed] [Google Scholar]
  21. MacDonald T. T., Spencer J. Evidence that activated mucosal T cells play a role in the pathogenesis of enteropathy in human small intestine. J Exp Med. 1988 Apr 1;167(4):1341–1349. doi: 10.1084/jem.167.4.1341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mahé S., Marteau P., Huneau J. F., Thuillier F., Tomé D. Intestinal nitrogen and electrolyte movements following fermented milk ingestion in man. Br J Nutr. 1994 Feb;71(2):169–180. doi: 10.1079/bjn19940124. [DOI] [PubMed] [Google Scholar]
  23. Mantle M., Thakore E., Hardin J., Gall D. G. Effect of Yersinia enterocolitica on intestinal mucin secretion. Am J Physiol. 1989 Feb;256(2 Pt 1):G319–G327. doi: 10.1152/ajpgi.1989.256.2.G319. [DOI] [PubMed] [Google Scholar]
  24. Mashige F., Imai K., Osuga T. A simple and sensitive assay of total serum bile acids. Clin Chim Acta. 1976 Jul 1;70(1):79–86. doi: 10.1016/0009-8981(76)90007-3. [DOI] [PubMed] [Google Scholar]
  25. Neal K. R., Briji S. O., Slack R. C., Hawkey C. J., Logan R. F. Recent treatment with H2 antagonists and antibiotics and gastric surgery as risk factors for Salmonella infection. BMJ. 1994 Jan 15;308(6922):176–176. doi: 10.1136/bmj.308.6922.176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Oudenhoven I. M., Klaasen H. L., Lapré J. A., Weerkamp A. H., Van der Meer R. Nitric oxide-derived urinary nitrate as a marker of intestinal bacterial translocation in rats. Gastroenterology. 1994 Jul;107(1):47–53. doi: 10.1016/0016-5085(94)90059-0. [DOI] [PubMed] [Google Scholar]
  27. Powell D. W. New paradigms for the pathophysiology of infectious diarrhea. Gastroenterology. 1994 Jun;106(6):1705–1707. doi: 10.1016/0016-5085(94)90430-8. [DOI] [PubMed] [Google Scholar]
  28. Rafferty J. F., Noguchi Y., Fischer J. E., Hasselgren P. O. Sepsis in rats stimulates cellular proliferation in the mucosa of the small intestine. Gastroenterology. 1994 Jul;107(1):121–127. doi: 10.1016/0016-5085(94)90069-8. [DOI] [PubMed] [Google Scholar]
  29. Rampling A. Salmonella enteritidis five years on. Lancet. 1993 Aug 7;342(8867):317–318. doi: 10.1016/0140-6736(93)91466-y. [DOI] [PubMed] [Google Scholar]
  30. Roomi N., Laburthe M., Fleming N., Crowther R., Forstner J. Cholera-induced mucin secretion from rat intestine: lack of effect of cAMP, cycloheximide, VIP, and colchicine. Am J Physiol. 1984 Aug;247(2 Pt 1):G140–G148. doi: 10.1152/ajpgi.1984.247.2.G140. [DOI] [PubMed] [Google Scholar]
  31. Sarker S. A., Gyr K. Non-immunological defence mechanisms of the gut. Gut. 1992 Jul;33(7):987–993. doi: 10.1136/gut.33.7.987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. VIRTUE R. W., VOGEL J. H., PRESS P., GROVER R. F. Respiratory and hemodynamic measurements during anesthesia. Use of trifluoroethyl vinyl ether and halothane. JAMA. 1962 Jan 20;179:224–225. doi: 10.1001/jama.1962.03050030038012. [DOI] [PubMed] [Google Scholar]

Articles from Gut are provided here courtesy of BMJ Publishing Group

RESOURCES