Morphine withdrawal lowers host defense to enteric bacteria: Spontaneous sepsis and increased sensitivity to oral Salmonella enterica serovar typhimurium infection

Infection and Immunity

Volumn 74, Issue 9, 2006, Pages 5221-5226

  Feng, Pu ^a   Truant, Allan L ^a   Meissler Jr , Joseph J ^a   Gaughan, John P ^a   Adler, Martin W ^a   Eisenstein, Toby K ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CYTOKINE; MORPHINE; PLACEBO;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIUM CULTURE; BACTERIUM DETECTION; BACTERIUM IDENTIFICATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG IMPLANTATION; DRUG PELLET; DRUG WITHDRAWAL; ENTEROBACTERIACEAE; ENTEROCOCCUS FAECIUM; FEMALE; HORMONE BLOOD LEVEL; HOST RESISTANCE; IMMUNOREGULATION; INFECTION RESISTANCE; INFECTION SENSITIVITY; INOCULATION; INTESTINE FLORA; KLEBSIELLA PNEUMONIAE; LIVER; MESENTERY LYMPH NODE; MOUSE; MOUTH INFECTION; NONHUMAN; PERITONEAL CAVITY; PEYER PATCH; PRIORITY JOURNAL; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SEPSIS; SEPTIC SHOCK; SEROTYPE; SPLEEN;

ANIMALS; CYTOKINES; DISEASE SUSCEPTIBILITY; ENTEROCOCCUS FAECIUM; IMMUNE TOLERANCE; KLEBSIELLA PNEUMONIAE; LIVER; LYMPH NODES; MICE; MORPHINE DEPENDENCE; MOUTH; PERITONEAL CAVITY; PEYER'S PATCHES; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; SEPSIS; SPLEEN; SUBSTANCE WITHDRAWAL SYNDROME;

EID: 33748033394     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00208-06     Document Type: Article

References (40)

1. Angerman, C. R., and T. K. Eisenstein. 1980. Correlation of the duration and magnitude of protection against Salmonella infection afforded by various vaccines with antibody titers. Infect. Immun. 27:435-443.
2. Angus, D. C., W. T. Linde-Zwirble, J. Lidicker, G. Clermont, J. Carcillo, and M. R. Pinsky. 2001. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 29:1303-1310.
3. Armitage, P., and G. Berry. 1994. Statistical methods in medical research, 3rd ed. Blackwell Science, Cambridge, Mass.
4. Barr, M. C., S. Huitron-Resendiz, M. Sanchez-Alavez, S. J. Henriksen, and T. R. Phillips. 2003. Escalating morphine exposures followed by withdrawal in feline immunodeficiency virus-infected cats: a model for HIV infection in chronic opiate abusers. Drug Alcohol Depend. 72:141-149.
5. Bergstrom, L., T. Sakurada, and L. Terenius. 1984. Substance P levels in various regions of the rat central nervous system after acute and chronic morphine treatment. Life Sci. 35:2375-2382.
6. Bhaskaran, M., K. Reddy, S. Sharma, J. Singh, N. Radhakrishnan, A. Kapasi, and P. C. Singhal. 2001. Morphine-induced degradation of the host defense barrier: role of macrophage injury. J. Infect. Dis. 184:1524-1531.
7. Bryant, H. U., E. W. Bernton, and J. W. Holaday. 1988. Morphine pellet-induced immunomodulation in mice: temporal relationships. J. Pharmacol. Exp. Ther. 245:913-920.
8. Bryant, H. U., B. C. Yoburn, C. E. Inturrisi, E. W. Bernton, and J. W. Holaday. 1988. Morphine-induced immunomodulation is not related to serum morphine concentrations. Eur. J. Pharmacol. 149:165-169.
9. Cerletti, C., S. H. Keinath, M. M. Reidenbery, and M. W. Adler. 1976. Chronic morphine administration: plasma levels and withdrawal syndrome in rats. Pharmacol. Biochem. Behav. 4:323-327.
10. Chao, C. C., B. M. Sharp, C. Pomeroy, G. A. Filice, and P. K. Peterson. 1990. Lethality of morphine in mice infected with Toxoplasma gondii. J. Pharmacol. Exp. Ther. 252:605-609.
11. Cheney, D. L., and A. Goldstein. 1971. Tolerance to opioid narcotics: time course and reversibility of physical dependence in mice. Nature 232:477-478.
12. Cicero, T. J., and E. R. Meyer. 1973. Morphine pellet implantation in rats: quantitative assessment of tolerance and dependence. J. Pharmacol. Exp. Ther. 184:404-408.
13. Conover, W. J., and R. L. Iman. 1981. Rank transformations as a bridge between parametric and nonparametric statistics. Am. Stat. 35:124-129.
14. Donahoe, R. M., L. D. Byrd, H. M. McClure, P. Fultz, M. Brantley, F. Marsteller, A. A. Ansari, D. Wenzel, and M. Aceto. 1993. Consequences of opiate-dependency in a monkey model of AIDS. Adv. Exp. Med. Biol. 335:21-28.
15. Eisenstein, T. K., L. M. Killar, and B. M. Sultzer. 1984. Immunity to infection with Salmonella typhimurium: mouse-strain differences in vaccine- and serum-mediated protection. J. Infect. Dis. 150:425-435.
16. Feng, P., J. J. Meissler, Jr., M. W. Adler, and T. K. Eisenstein. 2005. Morphine withdrawal sensitizes mice to lipopolysaccharide: elevated TNF-alpha and nitric oxide with decreased IL-12. J. Neuroimmunol. 164:57-65.
17. Feng, P., Q. M. Wilson, J. J. Meissler, Jr., M. W. Adler, and T. K. Eisenstein. 2005. Increased sensitivity to Salmonella enterica serovar Typhimurium infaction in mice undergoing withdrawal from morphine is associated with suppression of interleukin-12. Infect. Immun. 73:7953-7959.
18. Friedman, H., C. Newton, and T. W. Klein. 2003. Microbial infections, immunomodulation, and drugs of abuse. Clin. Microbiol. Rev. 16:209-219.
19. Harter, H. L. 1961. Expected values of normal order statistics. Biomtrika 48:151-165.
20. Haverkos, H. W., and W. R. Lange. 1990. Serious infections other than human immunodeficiency virus among intravenous drug abusers. J. Infect. Dis. 161:894-902.
21. Hilburger, M. E., M. W. Adler, A. L. Truant, J. J. Meissler, Jr., V. Satishchandran, T. J. Rogers, and T. K. Eisenstein. 1997. Morphine induces sepsis in mice. J. Infect. Dis. 176:183-188.
22. Horsburgh, C. R., Jr., J. R. Anderson, and E. J. Boyko. 1989. Increased incidence of infections in intravenous drug users. Infect. Control Hosp. Epidemiol. 10:211-215.
23. Kelschenbach, J., R. A. Barke, and S. Roy. 2005. Morphine withdrawal contributes to Th cell differentiation by biasing cells toward the Th2 lineage. J. Immunol. 175:2655-2665.
24. Louria, D. B., T. Hensle, and J. Rose. 1967. The major medical complications of heroin addiction. Ann. Intern. Med. 67:1-22.
25. MacFarlane, A. S., X. Peng, J. J. Meissler, Jr., T. J. Rogers, E. B. Geller, M. W. Adler, and T. K. Eisenstein. 2000. Morphine increases susceptibility to oral Salmonella typhimurium infection. J. Infect. Dis. 181:1350-1358.
26. McCarthy, L., M. Wetzel, J. K. Sliker, T. K. Eisenstein, and T. J. Rogers. 2001. Opioids, opioid receptors, and the immune response. Drug Alcohol Depend. 62:111-123.
27. Ocasio, F. M., Y. Jiang, S. D. House, and S. L. Chang. 2004. Chronic morphine accelerates the progression of lipopolysaccharide-induced sepsis to septic shock. J. Neuroimmunol. 149:90-100.
28. Paronis, C. A., and S. G. Holtzman. 1992. Development of tolerance to the analgesic activity of mu agonists after continuous infusion of morphine, meperidine or fentanyl in rats. J. Pharmacol. Exp. Ther. 262:1-9.
29. Patrick, G. A., W. L. Dewey, F. P. Huger, E. D. Daves, and L. S. Harris. 1978. Disposition of morphine in chronically infused rats: relationship to antinociception and tolerance. J. Pharmacol. Exp. Ther. 205:556-562.
30. Peng, X., J. J. Cebra, M. W. Adler, J. J. Meissler, Jr., A. Cowan, P. Feng, and T. K. Eisenstein. 2001. Morphine inhibits mucosal antibody responses and TGF-beta mRNA in gut-associated lymphoid tissue following oral cholera toxin in mice. J. Immunol. 167:3677-3681.
31. Rahim, R. T., M. W. Adler, J. J. Meissler, Jr., A. Cowan, T. J. Rogers, E. B. Geller, and T. K. Eisenstein. 2002. Abrupt or precipitated withdrawal from morphine induces immunosuppression. J. Neuroimmunol. 127:88-95.
32. Risdahl, J. M., K. V. Khanna, P. K. Peterson, and T. W. Molitor. 1998. Opiates and infection. J. Neuroimmunol. 83:4-18.
33. Risdahl, J. M., P. K. Peterson, C. C. Chao, C. Pijoan, and T. W. Molitor. 1993. Effects of morphine dependence on the pathogenesis of swine herpesvirus infection. J. Infect. Dis. 167:1281-1287.
34. Roy, S., R. G. Charboneau, and R. A. Barke. 1999. Morphine synergizes with lipopolysaccharide in a chronic endotoxemia model. J. Neuroimmunol. 95:107-114.
35. Schwacha, M. G., J. J. Meissler, Jr., and T. K. Eisenstein. 1998. Salmonella typhimurium infection in mice induces nitric oxide-mediated immunosuppression through a natural killer cell-dependent pathway. Infect. Immun. 66:5862-5866.
36. Singal, P., A. G. Kinhikar, S. Singh, and P. P. Singh. 2002. Neuroimmunomodulatory effects of morphine in Leishmania donovani-infected hamsters. Neuroimmunomodulation 10:261-269.
37. Singh, P. P., S. Singh, G. P. Dutta, and R. C. Srimal. 1994. Immunomodulation by morphine in Plasmodium berghei-infected mice. Life Sci. 54:331-339.
38. Tubaro, E., G. Borelli, C. Croce, G. Cavallo, and C. Santiangeli. 1983. Effect of morphine on resistance to infection. J. Infect. Dis. 148:656-666.
39. Wang, J., R. A. Barke, R. Charboneau, and S. Roy. 2005. Morphine impairs host innate immune response and increases susceptibility to Streptococcus pneumoniae lung infection. J. Immunol. 174:426-434.
40. Way, E. L., H. H. Loh, and F. H. Shen. 1969. Simultaneous quantitative assessment of morphine tolerance and physical dependence. J. Pharmacol. Exp. Ther. 167:1-8.