Dexamethasone treatment of lipopolysaccharide-induced meningitis in rabbits that mimics magnification of inflammation following antibiotic therapy Free

Abstract

Summary

The objective of adjunct anti-inflammatory therapy of bacterial meningitis is the containment of heightened inflammation caused by lysis of bacteria by antibiotics. This can be modelled by giving two consecutive intra-cisternal injections of lipopolysaccharide (LPS) to rabbits, the first at 0 h to induce inflammation to mimic that occurring during the proliferation of bacteria in the cerebrospinal fluid (CSF). and the second at 6 h to mimic inflammation subsequent to antibiotic-induced bacterial lysis. Injection of 2.5 ng of LPS induced pleocytosis at 4 h which was preceded by a peak of tumour necrosis factor (TNF) activity at 2 h. A subsequent injection of 25 ng of LPS at 6 h induced second peaks of pleocytosis and CSF TNF. Dexamethasone (1.5 mg/kg, i.v.) administered 15 min or 1 h before the second injection of LPS tended only to reduce CSF TNF, but effectively prohibited further pleocytosis. Brain TNFα mRNA levels were unchanged at 6 and 7 h after LPS injection, and were unaffected by dexamethasone. These results indicate that the subarachnoid space is distinct from the general circulation in that the TNF-producing cells present do not display a hypo-responsive state towards LPS as occurs when LPS is injected systemically. Furthermore, dexamethasone is able to attenuate the secondary inflammatory response resulting from a second LPS injection without eliminating a second peak of TNF activity.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/00222615-43-1-37
1995-07-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jmm/43/1/medmicro-43-1-37.html?itemId=/content/journal/jmm/10.1099/00222615-43-1-37&mimeType=html&fmt=ahah

References

  1. Tunkel A. R., Scheld W. M. Pathogenesis and pathophysiology of bacterial meningitis. Clin Microbiol Rev 1993; 6:118–136
    [Google Scholar]
  2. Sharief M. K., Ciardi M., Thompson E. J. Blood-brain barrier damage in patients with bacterial meningitis: association with tumour necrosis factor-α but not interleukin-1ß. J Infect Dis 1992; 166:350–358
    [Google Scholar]
  3. Chavanet P., Bonnotte B., Guiguet M. High concentrations of intrathecal interleukin-6 in human bacterial and non-bacterial meningitis. J Infect Dis 1992; 166:428–431
    [Google Scholar]
  4. Mertsola J., Kennedy W. A., Waagner D. Endotoxin concentrations in cerebrospinal fluid correlate with clinical severity and neurologic outcome of Haemophilus influenzae type b meningitis. Am J Dis Child 1991; 145:1099–1103
    [Google Scholar]
  5. Arditi M., Manogue K. R., Caplan M., Yogev R. Cerebrospinal fluid cachetin/tumor necrosis factor-a and platelet-activating factor concentrations and severity of bacterial meningitis in children. J Infect Dis 1990; 162:139–147
    [Google Scholar]
  6. Mustafa M. M., Level M. H., Ramilo O. Correlation of interleukin-1ß and cachectin concentrations in cerebrospinal fluid and outcome from bacterial meningitis. J Pediatr 1989; 115:208–213
    [Google Scholar]
  7. Mustafa M. M., Ramilo O., Saez-Llorens X., Olsen K. D., Magness R. R., McCracken G. H. Cerebrospinal fluid prostaglandins, interleukin 1ß and tumor necrosis factor in bacterial meningitis. Clinical and laboratory correlations in placebo-treated and dexamethasone-treated patients. Am J Dis Child 1990; 144:883–887
    [Google Scholar]
  8. Kennedy W. A., Hoyt M. J., McCracken G. H. The role of corticosteroid therapy in children with pneumococcal meningitis. Am J Dis Child 1991; 145:1374–1378
    [Google Scholar]
  9. Odio C. M., Faingezicht I., Paris M. The beneficial effects of early dexamethasone administration in infants and children with bacterial meningitis. N Engl J Med 1991; 324:1525–1531
    [Google Scholar]
  10. Girgis N. I., Farid Z., Mikhail I. A., Farrag I., Sultan Y., Kilpatrick M. E. Dexamethasone treatment for bacterial meningitis in children and adults. Pediatr Infect Dis J 1989; 8:848–851
    [Google Scholar]
  11. Lebel M. H., Hoyt J., Waagner D. C., Rollins N. K., Finitzo T., McCracken G. H. Magnetic resonance imaging and dexa-methasone therapy for bacterial meningitis. Am J Dis Child 1988; 143:301–306
    [Google Scholar]
  12. Level M. H., Freij B. J., Syrogiannopoulos G. A. Dexamethasone therapy for bacterial meningitis. Results of two double-blind, placebo controlled trials. N Engl J Med 1988; 319:964–971
    [Google Scholar]
  13. McGowan J. E., Chesney P. J., Crossley K. B., LaForce F. M. Guidelines for the use of systemic glucocorticosteroids in the management of selected infections. J Infect Dis 1992; 165:1–13
    [Google Scholar]
  14. Tarlow M. J. Adjunct therapy in bacterial meningitis. J Anti-microb Chemother 1991; 28:329–332
    [Google Scholar]
  15. American Academy of Pediatrics Committee on Infectious Diseases. Dexamethasone therapy for bacterial meningitis in infants and children. Pediatrics 1990; 86:130–133
    [Google Scholar]
  16. Kaplan S. L. Corticosteroids and bacterial meningitis. Scand J Infect Dis Suppl 1990; 73:43–54
    [Google Scholar]
  17. Tauber M. G., Sande M. A. Dexamethasone in bacterial meningitis: increasing evidence for a beneficial effect. Pediatr Infect Dis J 1989; 8:842–844
    [Google Scholar]
  18. Havens P. L., Wendelberger K. J., Hoffman G. M., Lee M. B., Chusid M. J. Corticosteroids as adjunctive therapy in bacterial meningitis. A meta-analysis of clinical trials. Am J Dis Child 1989; 143:1051–1055
    [Google Scholar]
  19. Kaplan S. L. Dexamethasone for children with bacterial meningitis. Should it be routine therapy?. Am J Dis Child 1989; 143:290–292
    [Google Scholar]
  20. Havens P. L. Meta-analysis redux-steroids and meningitis re-visited. West Med J 1992; 157:84–86
    [Google Scholar]
  21. Geiman B. J., Smith A. L. Dexamethasone and bacterial meningitis. A meta-analysis of randomized controlled trials. West Med J 1992; 157:27–31
    [Google Scholar]
  22. Mathison J. C., Virca G. D., Wolfson E., Tobias P. S., Glaser K., Ulevitch R. J. Adaptation to bacterial lipopolysaccharide controls lipopolysaccharide-induced tumor necrosis factor production in rabbit macrophages. J Clin Invest 1990; 85:1108–1118
    [Google Scholar]
  23. Syrogiannopoulos G. A., Hansen E. J., Erwin A. L. Haemophilus influenzae type b lipooligosaccharide induces meningeal inflammation. J Infect Dis 1988; 157:237–244
    [Google Scholar]
  24. Dacey R. G., Sande M. A. Effect of probenecid on cerebrospinal fluid concentrations of penicillin and cephalosporin derivatives. Antimicrob Agents Chemother 1974; 6:437–441
    [Google Scholar]
  25. Spector R., Lorenzo A. V. Inhibition of penicillin transport from the cerebrospinal fluid after intra-cisternal inoculation of bacteria. J Clin Invest 1974; 54:316–325
    [Google Scholar]
  26. Espevik T., Nissen-Meyer J. A highly sensitive cell line. WEHI 164 clone 13. for measuring cytotoxic factor/tumor necrosis factor from human monocytes. J Immunol Methods 1986; 95:99–105
    [Google Scholar]
  27. Tuomanen E., Tomasz A., Hengstler B., Zak O. The relative role of bacterial cell wall and capsule in the induction of inflammation in pneumococcal meningitis. J Infect Dis 1985; 151:535–540
    [Google Scholar]
  28. Lowry O. H., Rosebrough N. J., Farr A. L., Randall R. J. Protein measurement with the folin phenol reagent. J Biol Chem 1951; 193:265–275
    [Google Scholar]
  29. Ito H., Yamamoto S., Kuroda S. Molecular cloning and expression in Escherichia coli of the cDNA coding for rabbit tumor necrosis factor. DMA 1986; 5:149–156
    [Google Scholar]
  30. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162:156–159
    [Google Scholar]
  31. Zwickl M., Zaninetta D., McMaster G. K., Hardman N. Selective cloning of B cell hybridoma-specific rearranged immunoglobulin gene loci using the polymerase chain reaction. J Immunol Methods 1990; 130:49–55
    [Google Scholar]
  32. Sambrook J., Fritsch E. F., Maniatis T. Molecular cloning. A laboratory manual. 2nd edn Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 1989
    [Google Scholar]
  33. Nielson P. J., McMaster G. K., Trachsel H. Cloning of eukaryotic protein synthesis initiation factor genes: isolation and characterization of cDNA clones encoding elF-4a. Nucleic Acids Res 1985; 13:6867–6880
    [Google Scholar]
  34. Kadurugamuwa J. L., Hengstler B., Zak O. Cerebrospinal fluid protein profile in experimental pneumococcal meningitis and its alteration by ampicillin and anti-inflammatory agents. J Infect Dis 1989; 159:26–34
    [Google Scholar]
  35. Syrogiannopoulos G. A., Olsen K. D., Reisch J. S. McCracken GH. Dexamethasone in the treatment of experimental Haemophilus influenzae tvpe b meningitis. J Infect Dis 1987; 155:213–219
    [Google Scholar]
  36. Mustafa M. M., Ramilo O., Olsen K. D. Tumor necrosis factor in mediating experimental Haemophilus influenzae type b meningitis. J Clin Invest 1989; 84:1253–1259
    [Google Scholar]
  37. Saez-Llorens X., Ramilo O., Mustafa M. M. Pentoxifylline modulates meningeal inflammation in experimental bacterial meningitis. Antimicrob Agents Chemother 1990; 34:837–843
    [Google Scholar]
  38. Waage A., Halstensen A., Shalaby R., Brandtzaeg P., Kierulf P., Espevik T. Local production of tumor necrosis factor x. interleukin 1. and interleukin 6 in meningococcal meningitis. Relation to the inflammatory response. J Exp Med 1989; 170:1859–1867
    [Google Scholar]
  39. Kim K. S., Wass C. A., Cross A. S., Opal S. M. Modulation of blood-brain barrier permeability by tumor necrosis factor and antibody to tumor necrosis factor in the rat. Lvmphokine Cvtokine Res 1992; 11:293–298
    [Google Scholar]
  40. Velasco S., Tarlow M., Olsen K., Shay J. W., McCracken G. H., Nisen P. D. Temperature-dependent modulation of lipo-polysaccharide-induced interleukin-If and tumor necrosis factor x expression in cultured human astroglial cells by dexamethasone and indomethacin. J Clin Invest 1991; 87:1674–1680
    [Google Scholar]
  41. Chung I. Y., Benvemste E. N. Tumor necrosis factor-x production by astrocytes. Induction by lipopolysaccharide. IFN-γ and IL-1. ß J Immunol 1990; 144:2999–3007
    [Google Scholar]
  42. Robbins D. S., Shirazi Y., Drysdale B. E., Lieberman A., Shin H. S., Shin M. L. Production of cytotoxic factor for oligodendrocytes by stimulated astrocytes. J Immunol 1987; 139:2593–2597
    [Google Scholar]
  43. Chao C. C., Hu S., Close K. Cytokine release from microglia: differential inhibition by pentoxifylline and dexamethasone. J Infect Dis 1992; 166:847–853
    [Google Scholar]
  44. Tarlow M. J., Jenkins R., Comis S. D. Ependymal cells of the choroid plexus express tumour necrosis factor-x. Neuropathol AppI Neurobiol 1993; 19:324–328
    [Google Scholar]
  45. Warner S. J. C., Libby P. Human vascular smooth muscle cells. Target for and source of tumor necrosis factor. J Immunol 1989; 142:100–109
    [Google Scholar]
  46. Ming W. J., Bersani L., Mantovani A. Tumor necrosis factor is chemotactic for monocytes and polymorphonuclear leukocytes. J Immunol 1987; 138:1469–1474
    [Google Scholar]
  47. Cybulsky M. I., McComb D. J., Movat H. Z. Neutrophil leukocyte emigration induced by endotoxin. Mediator roles of interleukin I and tumor necrosis factor a. J Immunol 1988; 140:3144–3149
    [Google Scholar]
  48. Mason M. J., Van Epps D. E. In vivo neutrophil emigration in response to interleukin-1 and tumor necrosis factor-alpha. J Leukoc Biol 1989; 4:62–68
    [Google Scholar]
  49. Shalaby M. R., Palladino M. A., Hirabayashi S. E. Receptor binding and activation of polymorphonuclear neutrophils bv tumor necrosis factor-alpha. J Leukoc Biol 1987; 41:196–204
    [Google Scholar]
  50. Saukkonen K., Sande S., Cioffe C. The role of cytokines in the generation of inflammation and tissue damage in experimental gram-positive meningitis. J Exp Med 1990; 171:439–448
    [Google Scholar]
  51. Ramilo O., Saez-Llorens X., Mertsola J. Tumor necrosis factor x/cachetin and interleukin 1ßinitiate meningeal inflammation. J Exp Med 1990; 172:497–507
    [Google Scholar]
  52. Quagiiarello V. J., Wispelwey B., Long W. J., Scheld W. M. Recombinant human interleukin-1 induces meningitis and blood-brain barrier injury in the rat. Characterization and comparison with tumor necrosis factor. J Clin Invest 1991; 87:1360–1366
    [Google Scholar]
  53. Boccazzi A., Erroi A., Mantegazza M., Bellosta C., Ghezzi P. TNF and IL-1 in a rabbit model of meningitis. Int J Immunopathol Pharmacol 1993; 6:85–91
    [Google Scholar]
  54. Mustafa M. M., Ramilo O., Mertsola J. Modulation of inflammation and cachectin activity in relation to treatment of experimental Haemophilus influenzae type b meningitis. J Infect Dis 1989; 160:818–825
    [Google Scholar]
  55. Selmja K. W., Raine C. S. Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann Neurol 1988; 23:339–346
    [Google Scholar]
  56. Selmja K., Raine C. S., Fargooq M., Norton W. T., Brosnan C. F. Cytokine cytotoxicity against oligodendrocytes. Apoptosis induced by lymphotoxin. J Immunol 1991; 147:1522–1529
    [Google Scholar]
  57. Morganti-Kossmann M. C., Kossmann T., Wahl S. M. Cytokines and neuropathology. Trends Pharmacol Sci 1992; 13:286–291
    [Google Scholar]
  58. Ulich T. R., Guo K. Z., Irwin B., Remick D. G., Davatelis G. N. Endotoxin-induced cytokine gene expression in vivo. 2. Regulation of tumor necrosis factor and interleukin-1 α\β expression and suppression. Am J Pathol 1990; 137:1173–1185
    [Google Scholar]
  59. Remick D. G., Stricter R. M., Lynch J. P., Nguyen D., Eskandari M., Kunkel S. L. In vivo dynamics of murine tumor necrosis factor-x gene expression. Kinetics of dexamethasone-induced suppression. Lab Invest 1989; 60:766–771
    [Google Scholar]
  60. Sariban E., Imamura K., Leubbers R., Kufe D. Transcriptional and posttranscriptional regulation of tumor necrosis factor gene expression in human monocytes. J Clin Invest 1988; 81:1506–1510
    [Google Scholar]
  61. Beutler B., Krochin N., Milsark I. W., Luedke C., Cerami A. Control of cachectin (tumor necrosis factor) synthesis: mechanisms of endotoxin resistance. Science 1986; 232:977–980
    [Google Scholar]
  62. Han J., Thompson P., Beutler B. Dexamethasone and pentoxi-fylline inhibit endotoxin-induced cachectin/tumor necrosis factor synthesis at separate points in the signaling pathway. J Exp Med 1990; 172:391–394
    [Google Scholar]
  63. Brooke Williams R. D. Alterations in the glucose transport mechanism in patients with complications of bacterial meningitis. Pediatrics 1964; 34:491–502
    [Google Scholar]
  64. Moxon E. R., Smith A. L., Averill D. R. Brain carbohydrate metabolism during experimental Haemophilus influenzae meningitis. Pediatr Res 1979; 13:52–59
    [Google Scholar]
  65. Guerra-Romero L., Tauber M. G., Fournier M. A., Tureen J. H. Lactate and glucose concentrations in brain interstitial fluid, cerebrospinal fluid, and serum during experimental pneumococcal meningitis. J Infect Dis 1992; 166:546–550
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/00222615-43-1-37
Loading
/content/journal/jmm/10.1099/00222615-43-1-37
Loading

Data & Media loading...

Most cited Most Cited RSS feed