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PMID: 7768612 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Reactivation of arthritis induced by small bowel bacterial overgrowth in rats: role of cytokines, bacteria, and bacterial polymers.

Infection and immunity ·Vol. 63 ·No. 6 ·1995-06-00 ·Pages 2295-301

Lichtman SN, Wang J, Sartor RB, Zhang C, Bender D, Dalldorf FG, Schwab JH

Abstract

Arthritis is often associated with intestinal diseases, but the etiology is not known. We developed a rat model whereby arthritis was reactivated by experimental small bowel bacterial overgrowth (SBBO). Self-limited monoarticular arthritis was induced by intra-articular injection of 2 micrograms of rhamnose peptidoglycan-polysaccharide derived from group A streptococci into the ankle joints in female Lewis rats. Eleven days after intra-articular injection, when swelling was resolving, experimental SBBO induced by surgical creation of jejunal self-filling blind loops reactivated arthritis, but SBBO induced by creation of self-emptying blind loops, which minimally increases luminal bacteria, and sham operation did not (P < 0.001). Increased joint diameters in rats with self-filling blind loops persisted for at least 56 days after surgery. Reactivation of arthritis due to SBBO was prevented by anti-tumor necrosis factor alpha antiserum and interleukin 1 receptor antagonist (P < 0.001), indicating that these cytokines mediate joint swelling secondary to intestinal injury. Recombinant bactericidal/permeability-increasing protein, an agent which neutralizes endotoxin, and metronidazole, which is active against anaerobic bacteria, prevented arthritis (P < 0.001), but polymyxin B (which also neutralizes endotoxin) and gentamicin had no effect. Mutanolysin, an enzyme which degrades peptidoglycan-polysaccharide from group A streptococci, exacerbated arthritis for the first 6 days but then diminished joint swelling from 12 to 21 days after surgery (P < 0.001). These studies introduce a reproducible animal model of reactivation of arthritis secondary to intestinal injury and demonstrate a role for bacterial products from endogenous enteric organisms.

MeSH Terms
Animals Ankle Joint/pathology Arthritis, Reactive/etiology,pathology Cytokines/physiology Female Intestine, Small/microbiology Lipopolysaccharides/toxicity Metronidazole/pharmacology Peptidoglycan/toxicity Polysaccharides, Bacterial/toxicity Rabbits Rats Rats, Inbred Lew Weight Gain
Chemicals
Cytokines Lipopolysaccharides Peptidoglycan Polysaccharides, Bacterial Metronidazole
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Lichtman S N
Department of Pediatrics, University of North Carolina at Chapel Hill 27599, USA.
Wang J
Sartor R B
Zhang C
Bender D
Dalldorf F G
Schwab J H
References (35)
35 references, click to expand
  1. Suppression of cell-mediated immunity by metronidazole.
    Int Arch Allergy Appl Immunol. 1977;54(5):422-7 PMID: 328408
  2. Reactivation of streptococcal cell wall-induced arthritis by homologous and heterologous cell wall polymers.
    Arthritis Rheum. 1985 Dec;28(12):1402-11 PMID: 3910050
  3. Development of an experimental animal model for reactive arthritis induced by Yersinia enterocolitica infection.
    Infect Immun. 1987 Mar;55(3):721-6 PMID: 3493220
  4. Lipopolysaccharide induces recurrence of arthritis in rat joints previously injured by peptidoglycan-polysaccharide.
    J Exp Med. 1987 Jun 1;165(6):1688-702 PMID: 3295108
  5. Small bowel bacterial overgrowth syndrome.
    Dig Dis. 1987;5(3):157-71 PMID: 3311488
  6. Exacerbation of arthritis by IL-1 in rat joints previously injured by peptidoglycan-polysaccharide.
    J Immunol. 1988 May 1;140(9):2964-9 PMID: 3283241
  7. Phase I study of a murine monoclonal anti-lipid A antibody in bacteremic and nonbacteremic patients.
    Antimicrob Agents Chemother. 1988 May;32(5):710-6 PMID: 3395101
  8. Crohn's disease associated with arthritis: a possible role for cross-reactivity between gut bacteria and cartilage in the pathogenesis of arthritis.
    Arthritis Rheum. 1988 Aug;31(8):1077-9 PMID: 3408509
  9. Yersinia antigens in synovial-fluid cells from patients with reactive arthritis.
    N Engl J Med. 1989 Jan 26;320(4):216-21 PMID: 2643047
  10. Anticachectin/tumor necrosis factor-alpha antibodies attenuate development of cachexia in tumor models.
    FASEB J. 1989 Jun;3(8):1956-62 PMID: 2721856
  11. Arthritis and the gut.
    Postgrad Med. 1989 Aug;86(2):229-30, 233-4 PMID: 2474160
  12. Molecular mimicry in HLA-B27-related arthritis.
    Ann Intern Med. 1989 Oct 1;111(7):581-91 PMID: 2672931
  13. Hepatic inflammation in rats with experimental small intestinal bacterial overgrowth.
    Gastroenterology. 1990 Feb;98(2):414-23 PMID: 2295397
  14. Association between protective efficacy of anti-lipopolysaccharide (LPS) antibodies and suppression of LPS-induced tumor necrosis factor alpha and interleukin 6. Comparison of O side chain-specific antibodies with core LPS antibodies.
    J Exp Med. 1990 Mar 1;171(3):889-96 PMID: 2307935
  15. Hepatic injury associated with small bowel bacterial overgrowth in rats is prevented by metronidazole and tetracycline.
    Gastroenterology. 1991 Feb;100(2):513-9 PMID: 1985047
  16. Evidence for peptidoglycan absorption in rats with experimental small bowel bacterial overgrowth.
    Infect Immun. 1991 Feb;59(2):555-62 PMID: 1987073
  17. A controlled clinical trial of E5 murine monoclonal IgM antibody to endotoxin in the treatment of gram-negative sepsis. The XOMA Sepsis Study Group.
    JAMA. 1991 Aug 28;266(8):1097-102 PMID: 1865542
  18. Endotoxin-neutralizing properties of the 25 kD N-terminal fragment and a newly isolated 30 kD C-terminal fragment of the 55-60 kD bactericidal/permeability-increasing protein of human neutrophils.
    J Exp Med. 1991 Sep 1;174(3):649-55 PMID: 1875165
  19. Pro- and anti-inflammatory roles of interleukin-1 in recurrence of bacterial cell wall-induced arthritis in rats.
    Infect Immun. 1991 Dec;59(12):4436-42 PMID: 1834576
  20. High-affinity binding of the bactericidal/permeability-increasing protein and a recombinant amino-terminal fragment to the lipid A region of lipopolysaccharide.
    Infect Immun. 1992 Nov;60(11):4754-61 PMID: 1398985
  21. Degradation of endogenous bacterial cell wall polymers by the muralytic enzyme mutanolysin prevents hepatobiliary injury in genetically susceptible rats with experimental intestinal bacterial overgrowth.
    J Clin Invest. 1992 Oct;90(4):1313-22 PMID: 1401067
  22. Superantigen can reactivate bacterial cell wall-induced arthritis.
    J Immunol. 1993 May 1;150(9):4151-9 PMID: 8473753
  23. Role of bactericidal permeability-increasing protein in the treatment of gram-negative pneumonia.
    Surgery. 1993 Aug;114(2):140-6 PMID: 8342120
  24. Phlogistic properties of peptidoglycan-polysaccharide polymers from cell walls of pathogenic and normal-flora bacteria which colonize humans.
    Infect Immun. 1993 Nov;61(11):4535-9 PMID: 8406849
  25. Comparison of peptidoglycan-polysaccharide and lipopolysaccharide stimulation of Kupffer cells to produce tumor necrosis factor and interleukin-1.
    Hepatology. 1994 Apr;19(4):1013-22 PMID: 8138241
  26. Tissue interleukin 1 and interleukin-1 receptor antagonist expression in enterocolitis in resistant and susceptible rats.
    Gastroenterology. 1994 Apr;106(4):960-72 PMID: 8144001
  27. Metronidazole inhibits leukocyte-endothelial cell adhesion in rat mesenteric venules.
    Gastroenterology. 1994 May;106(5):1271-6 PMID: 8174888
  28. The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats.
    J Exp Med. 1994 Dec 1;180(6):2359-64 PMID: 7964509
  29. Arthritis in rats after systemic injection of streptococcal cells or cell walls.
    J Exp Med. 1977 Dec 1;146(6):1585-602 PMID: 336836
  30. The intestinal bypass: arthritis-dermatitis syndrome.
    Arthritis Rheum. 1981 May;24(5):684-90 PMID: 7236324
  31. Arthritis associated with bowel disease.
    Clin Gastroenterol. 1983 Sep;12(3):767-95 PMID: 6193911
  32. Reiter's syndrome and reactive arthritis in perspective.
    N Engl J Med. 1983 Dec 29;309(26):1606-15 PMID: 6358890
  33. Treatment of experimental erosive arthritis in rats by injection of the muralytic enzyme mutanolysin.
    J Exp Med. 1984 Nov 1;160(5):1360-74 PMID: 6387033
  34. Arthropathic properties of cell wall polymers from normal flora bacteria.
    Infect Immun. 1986 Jan;51(1):240-9 PMID: 3940996
  35. Chlamydia trachomatis and reactive arthritis: the missing link.
    Lancet. 1987 Jan 10;1(8524):72-4 PMID: 2879176
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
1995-06-00
Pages
2295-301
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC173300
Subset
IM
Grants
NIAMS NIH HHS · AR 39480 · United States
NIDDK NIH HHS · DK 34987 · United States
NIDDK NIH HHS · DK 40249 · United States
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