Abstract
Previous studies have demonstrated that the urinary bladder is a consistent source for isolating the Lyme disease spirochete, Borrelia burgdorferi, from both experimentally infected and naturally exposed rodents. We examined histopathologic changes in the urinary bladder of different types of rodents experimentally infected with Lyme spirochetes, including BALB/c mice (Mus musculus), nude mice (M. musculus), white-footed mice (Peromyscus leucopus), and grasshopper mice (Onychomys leucogaster). Animals were inoculated intraperitoneally, subcutaneously, or intranasally with low-passaged spirochetes, high-passaged spirochetes, or phosphate-buffered saline. At various times after inoculation, animals were killed and approximately one-half of each urinary bladder and kidney were cultured separately in BSK-II medium while the other half of each organ was prepared for histologic examination. Spirochetes were cultured from the urinary bladder of all 35 mice inoculated with low-passaged spirochetes while we were unable to isolate spirochetes from any kidneys of the same mice. The pathologic changes observed most frequently in the urinary bladder of the infected mice were the presence of lymphoid aggregates, vascular changes, including an increase in the number of vessels and thickening of the vessel walls, and perivascular infiltrates. Our results demonstrate that nearly all individuals (93%) of the four types of mice examined had a cystitis associated with spirochetal infection.
Full text
PDF






Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Barbour A. G., Hayes S. F., Heiland R. A., Schrumpf M. E., Tessier S. L. A Borrelia-specific monoclonal antibody binds to a flagellar epitope. Infect Immun. 1986 May;52(2):549–554. doi: 10.1128/iai.52.2.549-554.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barbour A. G. Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med. 1984 Jul-Aug;57(4):521–525. [PMC free article] [PubMed] [Google Scholar]
- Barbour A. G., Tessier S. L., Todd W. J. Lyme disease spirochetes and ixodid tick spirochetes share a common surface antigenic determinant defined by a monoclonal antibody. Infect Immun. 1983 Aug;41(2):795–804. doi: 10.1128/iai.41.2.795-804.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barthold S. W., Beck D. S., Hansen G. M., Terwilliger G. A., Moody K. D. Lyme borreliosis in selected strains and ages of laboratory mice. J Infect Dis. 1990 Jul;162(1):133–138. doi: 10.1093/infdis/162.1.133. [DOI] [PubMed] [Google Scholar]
- Barthold S. W. Infectivity of Borrelia burgdorferi relative to route of inoculation and genotype in laboratory mice. J Infect Dis. 1991 Feb;163(2):419–420. doi: 10.1093/infdis/163.2.419. [DOI] [PubMed] [Google Scholar]
- Barthold S. W., Moody K. D., Terwilliger G. A., Duray P. H., Jacoby R. O., Steere A. C. Experimental Lyme arthritis in rats infected with Borrelia burgdorferi. J Infect Dis. 1988 Apr;157(4):842–846. doi: 10.1093/infdis/157.4.842. [DOI] [PubMed] [Google Scholar]
- Barthold S. W., Moody K. D., Terwilliger G. A., Jacoby R. O., Steere A. C. An animal model for Lyme arthritis. Ann N Y Acad Sci. 1988;539:264–273. doi: 10.1111/j.1749-6632.1988.tb31860.x. [DOI] [PubMed] [Google Scholar]
- Bosler E. M., Schulze T. L. The prevalence and significance of Borrelia burgdorferi in the urine of feral reservoir hosts. Zentralbl Bakteriol Mikrobiol Hyg A. 1986 Dec;263(1-2):40–44. doi: 10.1016/s0176-6724(86)80100-6. [DOI] [PubMed] [Google Scholar]
- Burgdorfer W., Barbour A. G., Hayes S. F., Benach J. L., Grunwaldt E., Davis J. P. Lyme disease-a tick-borne spirochetosis? Science. 1982 Jun 18;216(4552):1317–1319. doi: 10.1126/science.7043737. [DOI] [PubMed] [Google Scholar]
- Callister S. M., Agger W. A., Schell R. F., Brand K. M. Efficacy of the urinary bladder for isolation of Borrelia burgdorferi from naturally infected, wild Peromyscus leucopus. J Clin Microbiol. 1989 Apr;27(4):773–774. doi: 10.1128/jcm.27.4.773-774.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chancellor M. B., Dato V. M., Yang J. Y. Lyme disease presenting as urinary retention. J Urol. 1990 Jun;143(6):1223–1224. doi: 10.1016/s0022-5347(17)40231-x. [DOI] [PubMed] [Google Scholar]
- Donahue J. G., Piesman J., Spielman A. Reservoir competence of white-footed mice for Lyme disease spirochetes. Am J Trop Med Hyg. 1987 Jan;36(1):92–96. doi: 10.4269/ajtmh.1987.36.92. [DOI] [PubMed] [Google Scholar]
- Dorward D. W., Schwan T. G., Garon C. F. Immune capture and detection of Borrelia burgdorferi antigens in urine, blood, or tissues from infected ticks, mice, dogs, and humans. J Clin Microbiol. 1991 Jun;29(6):1162–1170. doi: 10.1128/jcm.29.6.1162-1170.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Duray P. H. Histopathology of clinical phases of human Lyme disease. Rheum Dis Clin North Am. 1989 Nov;15(4):691–710. [PubMed] [Google Scholar]
- Duray P. H., Johnson R. C. The histopathology of experimentally infected hamsters with the Lyme disease spirochete, Borrelia burgdorferi. Proc Soc Exp Biol Med. 1986 Feb;181(2):263–269. doi: 10.3181/00379727-181-42251. [DOI] [PubMed] [Google Scholar]
- Duray P. H., Steere A. C. The spectrum of organ and systems pathology in human Lyme disease. Zentralbl Bakteriol Mikrobiol Hyg A. 1986 Dec;263(1-2):169–178. doi: 10.1016/s0176-6724(86)80120-1. [DOI] [PubMed] [Google Scholar]
- Fikrig E., Barthold S. W., Kantor F. S., Flavell R. A. Protection of mice against the Lyme disease agent by immunizing with recombinant OspA. Science. 1990 Oct 26;250(4980):553–556. doi: 10.1126/science.2237407. [DOI] [PubMed] [Google Scholar]
- Finlay B. B., Falkow S. Common themes in microbial pathogenicity. Microbiol Rev. 1989 Jun;53(2):210–230. doi: 10.1128/mr.53.2.210-230.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fitzgerald T. J. Pathogenesis and immunology of Treponema pallidum. Annu Rev Microbiol. 1981;35:29–54. doi: 10.1146/annurev.mi.35.100181.000333. [DOI] [PubMed] [Google Scholar]
- Gardiner R. A., Seymour G. J., Lavin M. F., Strutton G. M., Gemmell E., Hazan G. Immunohistochemical analysis of the human bladder. Br J Urol. 1986 Feb;58(1):19–25. doi: 10.1111/j.1464-410x.1986.tb05420.x. [DOI] [PubMed] [Google Scholar]
- Goodman J. L., Jurkovich P., Kramber J. M., Johnson R. C. Molecular detection of persistent Borrelia burgdorferi in the urine of patients with active Lyme disease. Infect Immun. 1991 Jan;59(1):269–278. doi: 10.1128/iai.59.1.269-278.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Holm-Bentzen M., Lose G. Pathology and pathogenesis of interstitial cystitis. Urology. 1987 Apr;29(4 Suppl):8–13. [PubMed] [Google Scholar]
- Hyde F. W., Johnson R. C., White T. J., Shelburne C. E. Detection of antigens in urine of mice and humans infected with Borrelia burgdorferi, etiologic agent of Lyme disease. J Clin Microbiol. 1989 Jan;27(1):58–61. doi: 10.1128/jcm.27.1.58-61.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson R. C., Kodner C., Russell M. Active immunization of hamsters against experimental infection with Borrelia burgdorferi. Infect Immun. 1986 Dec;54(3):897–898. doi: 10.1128/iai.54.3.897-898.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson R. C., Kodner C., Russell M. In vitro and in vivo susceptibility of the Lyme disease spirochete, Borrelia burgdorferi, to four antimicrobial agents. Antimicrob Agents Chemother. 1987 Feb;31(2):164–167. doi: 10.1128/aac.31.2.164. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson R. C., Marek N., Kodner C. Infection of Syrian hamsters with Lyme disease spirochetes. J Clin Microbiol. 1984 Dec;20(6):1099–1101. doi: 10.1128/jcm.20.6.1099-1101.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kimsey R. B., Spielman A. Motility of Lyme disease spirochetes in fluids as viscous as the extracellular matrix. J Infect Dis. 1990 Nov;162(5):1205–1208. doi: 10.1093/infdis/162.5.1205. [DOI] [PubMed] [Google Scholar]
- Kindred B. Nude mice in immunology. Prog Allergy. 1979;26:137–238. [PubMed] [Google Scholar]
- Levine J. F., Wilson M. L., Spielman A. Mice as reservoirs of the Lyme disease spirochete. Am J Trop Med Hyg. 1985 Mar;34(2):355–360. doi: 10.4269/ajtmh.1985.34.355. [DOI] [PubMed] [Google Scholar]
- McInnes A., Rennick D. M. Interleukin 4 induces cultured monocytes/macrophages to form giant multinucleated cells. J Exp Med. 1988 Feb 1;167(2):598–611. doi: 10.1084/jem.167.2.598. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moody K. D., Barthold S. W., Terwilliger G. A., Beck D. S., Hansen G. M., Jacoby R. O. Experimental chronic Lyme borreliosis in Lewis rats. Am J Trop Med Hyg. 1990 Feb;42(2):165–174. doi: 10.4269/ajtmh.1990.42.165. [DOI] [PubMed] [Google Scholar]
- Oravisto K. J. Interstitial cystitis as an autoimmune disease. A review. Eur Urol. 1980;6(1):10–13. doi: 10.1159/000473278. [DOI] [PubMed] [Google Scholar]
- Schaible U. E., Kramer M. D., Museteanu C., Zimmer G., Mossmann H., Simon M. M. The severe combined immunodeficiency (scid) mouse. A laboratory model for the analysis of Lyme arthritis and carditis. J Exp Med. 1989 Oct 1;170(4):1427–1432. doi: 10.1084/jem.170.4.1427. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schmitz J. L., Schell R. F., Hejka A., England D. M., Konick L. Induction of lyme arthritis in LSH hamsters. Infect Immun. 1988 Sep;56(9):2336–2342. doi: 10.1128/iai.56.9.2336-2342.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schwan T. G., Burgdorfer W., Garon C. F. Changes in infectivity and plasmid profile of the Lyme disease spirochete, Borrelia burgdorferi, as a result of in vitro cultivation. Infect Immun. 1988 Aug;56(8):1831–1836. doi: 10.1128/iai.56.8.1831-1836.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schwan T. G., Burgdorfer W., Schrumpf M. E., Karstens R. H. The urinary bladder, a consistent source of Borrelia burgdorferi in experimentally infected white-footed mice (Peromyscus leucopus). J Clin Microbiol. 1988 May;26(5):893–895. doi: 10.1128/jcm.26.5.893-895.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schwan T. G., Karstens R. H., Schrumpf M. E., Simpson W. J. Changes in antigenic reactivity of Borrelia burgdorferi, the Lyme disease spirochete, during persistent infection in mice. Can J Microbiol. 1991 Jun;37(6):450–454. doi: 10.1139/m91-074. [DOI] [PubMed] [Google Scholar]
- Schwan T. G., MacDonald A. B. Interstitial cystitis and Borrelia burgdorferi. Ann Intern Med. 1989 Sep 15;111(6):537–537. doi: 10.7326/0003-4819-111-6-537_1. [DOI] [PubMed] [Google Scholar]
- Steere A. C., Grodzicki R. L., Kornblatt A. N., Craft J. E., Barbour A. G., Burgdorfer W., Schmid G. P., Johnson E., Malawista S. E. The spirochetal etiology of Lyme disease. N Engl J Med. 1983 Mar 31;308(13):733–740. doi: 10.1056/NEJM198303313081301. [DOI] [PubMed] [Google Scholar]
- Steere A. C. Lyme disease. N Engl J Med. 1989 Aug 31;321(9):586–596. doi: 10.1056/NEJM198908313210906. [DOI] [PubMed] [Google Scholar]
- Thomas D. D., Comstock L. E. Interaction of Lyme disease spirochetes with cultured eucaryotic cells. Infect Immun. 1989 Apr;57(4):1324–1326. doi: 10.1128/iai.57.4.1324-1326.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thomas D. D., Navab M., Haake D. A., Fogelman A. M., Miller J. N., Lovett M. A. Treponema pallidum invades intercellular junctions of endothelial cell monolayers. Proc Natl Acad Sci U S A. 1988 May;85(10):3608–3612. doi: 10.1073/pnas.85.10.3608. [DOI] [PMC free article] [PubMed] [Google Scholar]