Lyme Disease

  • Michael T. Osterholm
  • Kristine L. MacDonald
  • Craig W. Hedberg

Abstract

Lyme disease is a tickborne multisystem illness caused by the spirochete Borrelia burgdorferi.The clinical manifestations of illness are divided into three stages (Table 1). Stage I is predominantly characterized by erythema chronicum migrans (EM), a skin rash that classically begins as a single macule that expands to an annular lesion, frequently with subsequent secondary annular lesions. The occurrence of EM is often associated with minor constitutional symptoms. Stage II is characterized by neurologic involvement (particularly meningoencephalitis) or cardiovascular involvement (endocarditis, endomyocarditis, vasculitis, or fibrinous pericarditis), usually beginning several weeks after the appearance of EM. Stage III is characterized by recurrent migratory arthritis, primarily of the large joints, which occurs several weeks to 2 years after infection. Myositis, fasciitis, and peripheral neuropathies can also be associated with stage III Lyme disease. Patients may develop EM without further sequelae, or they may present with stage II or stage III disease without recalling prior EM or a tick bite. In some instances, Lyme disease can be severely debilitating without appropriate antimicrobial therapy; therefore, accurate diagnosis and treatment are critical to the clinical management and the public health control of this illness.

Keywords

Lyme Disease Borrelia Burgdorferi Tick Bite Tick Vector Lyme Arthritis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Afzelius, A., Erythema chronicum migrans, Acta Derm. Venereol. 2: 120–125 (1921).Google Scholar
  2. 2.
    Anderson, J., Mammalian and avian reservoirs for Borrelia burgdorferi, Ann. N.Y. Acad. Sci. 539: 180–191 (1988).PubMedCrossRefGoogle Scholar
  3. 3.
    Anderson, J., Johnson, R., Magnarelli, L., and Hyde, F., Identification of endemic foci of Lyme disease: Isolation of Borrelia burgdorferifrom feral rodents and ticks (Dermacentor variabilis), J. Clin. Microbiol. 22: 36–38 (1985).PubMedGoogle Scholar
  4. 4.
    Bannwarth, A., Chronische lymphocytare meningitis, entzundliche polyneuritis und “Rheumatismus” . Ein Beitrag zum problem “Allergie und Nervensystem,” Arch. Psychiatr. Nervenkr. 113: 284–376 (1941).CrossRefGoogle Scholar
  5. 5.
    Baranton, G., and Saint-Gibbons, I., Borrelia burgdorferisurvival in human blood samples, Ann. N.Y. Acad. Sci. 539: 444–445 (1988).CrossRefGoogle Scholar
  6. 6.
    Barbour, A., and Garon, C., The genes encoding major surface proteins of Borrelia burgdorferiare located on a plasmidAnn. N.Y. Acad. Sci. 539: 144–153 (1988).PubMedCrossRefGoogle Scholar
  7. 7.
    Barbour, A., Heiland, R., and Howe, T., Heterogeneity of major proteins in Lyme disease borreliae: A molecular analysis of North American isolates, J. Infect. Dis. 152: 478–484 (1985).PubMedCrossRefGoogle Scholar
  8. 8.
    Beck, G., Habicht, G., Benach, J., and Coleman, J., Chemical and biologic characterization of a lipopolysaccharide extracted from the Lyme disease spirochete (Borrelia burgdorferi), J. Infect. Dis. 152: 108–117 (1985).PubMedCrossRefGoogle Scholar
  9. 9.
    Benach, J., and Coleman, J., Clinical and geographical characteristics of Lyme disease in New York, Zentralbl. Bakteriol. Mikrobiol. Hyg. A 263: 477–482 (1986).Google Scholar
  10. 10.
    Benach, J., Bosler, E., Hanrahan, J., Coleman, J., Habicht, G., Bast, T., Cameron, D., Ziegler, J., Barbour, A., Burgdorfer, W., Edelman, R., and Kaslow, R., Spirochetes isolated from the blood of two patients with Lyme disease, N. Engl. J. Med. 308: 740–742 (1983).PubMedCrossRefGoogle Scholar
  11. 11.
    Bendig, J., and Ogilvie, D., Severe encephalopathy associated with Lyme disease, Lancet 1: 681–682 (1987).PubMedCrossRefGoogle Scholar
  12. 12.
    Benoit, P., Dournon, E., Destee, A., and Warot, P., Spirochaetes and Lyme disease, Lancet 2: 1223 (1986).PubMedCrossRefGoogle Scholar
  13. 13.
    Berger, B., Kaplan, M., Rothenberg, I., and Barbour, A., Isolation and characterization of the Lyme disease spirochete from the skin of patients with erythema chronicum migrans, J. Am. Acad. Dermatol. 13: 444–449 (1985).PubMedCrossRefGoogle Scholar
  14. 14.
    Binder, E., Doepfmer, R., and Hornstein, O., Experimentelle Übertragung des Erythema chronicum migrans von Mensch zu Mensch, Hautarzt 6: 494–496 (1955).PubMedGoogle Scholar
  15. 15.
    Bosler, E., and Schulze, T., The prevalence and significance of Borrelia burgdorferiin the urine of feral reservoir hosts, Zentralbl. Bakteriol. Mikrobiol. Hyg. A 263: 40–44 (1986).PubMedGoogle Scholar
  16. 16.
    Bosler, E., Ormiston, B., Coleman, J., Hanrahan, J., and Benach, J., Prevalence of the Lyme disease spirochete in populations of white-tailed deer and white-footed mice,Yale J. Biol. Med. 57: 651–659 (1984).PubMedGoogle Scholar
  17. 17.
    Bosler, E., Cohen, D., Schulze, T., Olsen, C., Bernard, W., and Lissman, B., Host responses to Borrelia burgdorferiin dogs and horses, Ann. N.Y. Acad. Sci. 539: 221–234 (1988).PubMedCrossRefGoogle Scholar
  18. 18.
    Burgdorfer, W., Barbour, A., Hayes, S., Benach, J., Grunwaldt, E., and Davis, J., Lyme disease-A tickborne spirochetosis? Science 216: 1319–1320 (1982).CrossRefGoogle Scholar
  19. 19.
    Burgdorfer, W., Lane, R., Barbour, A., Gresbink, J., and Anderson, J., The Western black-legged tick, Ixodes pacificus: A vector of Borrelia burgdorferi, Am. J. Trop. Med. Hyg. 34: 925–930 (1985).PubMedGoogle Scholar
  20. 20.
    Burgdorfer, W., Hayes, S., and Benach, J., Development of Borrelia burgdorferiin ixodid tick vectors, Ann. N. Y. Acad. Sci. 539: 172–179 (1988).PubMedCrossRefGoogle Scholar
  21. 21.
    Burgess, E., Borrelia burgdorferiinfection in Wisconsin horses and cows, Ann. N.Y. Acad. Sci. 539: 235–243 (1988).PubMedCrossRefGoogle Scholar
  22. 22.
    Burgess, E., Amundson, T., Davis, J., Kaslow, R., and Edelman, R., Experimental inoculation of Peromyscus spp. with Borrelia burgdorferi: Evidence of contact transmission, Am. J. Trop. Med. Hyg. 35: 355–359 (1986).PubMedGoogle Scholar
  23. 23.
    Centers for Disease Control, Update: Lyme disease-United States, Morbid. Mortal. Weekly Rep. 33: 268–270 (1984).Google Scholar
  24. 24.
    Centers for Disease Control, Lyme Disease-Connecticut, Morbid. Mortal. Weekly Rep. 37: 1–3 (1988).Google Scholar
  25. 25.
    Chengxu, A., Yuxin, W., Yongquo, Z., Shaoshan, W., Quicheng, Q., Zhixue, S., Deyou, L., Donguan, C., Ziaodung, L., and Jienhua, Z., Clinical manifestations and epidemiological characteristics of Lyme disease in Hailin County, Heilongjiang Province, China, Ann. N.Y. Acad. Sci. 539: 302–313 (1988).CrossRefGoogle Scholar
  26. 26.
    Ciesielski, C., Markowitz, L., Horsley, R., Hightower, A., Russel, H., and Broome, C., The geographic distribution of Lyme disease in the United States, Ann. N.Y. Acad. Sci. 539: 283–288 (1988).PubMedCrossRefGoogle Scholar
  27. 27.
    Cohen, D., Bosler, E., Bernard, W., Meirs, D., Eisner, R., and Schulze, T., Epidemiologic studies of Lyme disease in horses and their public health significance, Ann. N.Y. Acad. Sci. 539: 244–257 (1988).PubMedCrossRefGoogle Scholar
  28. 28.
    Craft, J., Grodzicki, R., and Steere, A., Antibody response in Lyme disease: Evaluation of diagnostic tests, J. Infect. Dis. 149: 789–795 (1984).PubMedCrossRefGoogle Scholar
  29. 29.
    Craft, J., Grodzicki, R., Shrestha, M., Fischer, D., Garcia-Blanco, M., and Steere, A., The antibody response in Lyme disease, Yale J. Biol. Med. 57: 561–565 (1984).PubMedGoogle Scholar
  30. 30.
    Craft, J., Fischer, D., Shimamoto, G., and Steere, A., Antigens of Borrelia burgdorferirecognized during Lyme disease, J. Clin. Invest. 78: 934–939 (1986).PubMedCrossRefGoogle Scholar
  31. 31.
    Dattwyler, R., Thomas, J., Benach, J., and Golightly, M., Cellular immune responses in Lyme disease, Zentralbl. Bakteriol. Mikrobiol. Hyg. A 263: 151 (1986).PubMedGoogle Scholar
  32. 32.
    Dattwyler, R., Halperin, J., Pass, H., and Luft, B., Ceftriaxone as effective therapy in refractory Lyme disease, J. Infect. Dis. 155: 1322–1325 (1987).PubMedCrossRefGoogle Scholar
  33. 33.
    Dattwyler, R., Volkman, D., Halperin, J., Luft, B., Thomas, J., and Golightly M., Seronegative Lyme disease: Specific immune responses in Lyme borreliosis. Characterization of T cell and B cell responses to Borrelia burgdorferi, Ann. N.Y. Acad. Sci. 539: 93–102 (1988).PubMedCrossRefGoogle Scholar
  34. 34.
    Dattwyler, R., Volkman, D., Luft, B., Halperin, J., Thomas, J., and Golightly, M., Seronegative Lyme disease: Dissociation of specific T- and B-lymphocyte responses to Borrelia burgdorferi, N. Engl. J. Med. 319: 1441–1446 (1988).PubMedCrossRefGoogle Scholar
  35. 35.
    Davis, J., Schell, W., Amundson, T., Godsey, M., Spielman, A., Burgdorfer, W., Barbour, A., Laventure, M., and Kaslow, R., Lyme disease in Wisconsin: Epidemiologic, clinical, serologic, and entomologic findings, Yale J. Biol. Med. 57: 685–696 (1984).PubMedGoogle Scholar
  36. 36.
    Dekonenko, E., Steere, A., Berardi, V., and Kravchuk, L., Lyme borreliosis in the Soviet Union: A cooperative Us-Ussr report, J. Infect. Dis. 158: 748–753 (1988).PubMedCrossRefGoogle Scholar
  37. 37.
    Dupont, H., Hornick, R., Dawkins, A., Heiner, G., Fabrikant, I., Wisseman, C., and Woodward, T., Rocky mountain spotted fever: A comparative study of the active immunity induced by inactivated and viable pathogenic Rickettsia rickettsii, J. Infect. Dis. 128: 340–344 (1973).PubMedCrossRefGoogle Scholar
  38. 38.
    Duray, P., and Steere, A., Clinical pathologic correlations of Lyme disease by stage, Ann. N.Y. Acad. Sci. 539: 65–79 (1988).PubMedCrossRefGoogle Scholar
  39. 39.
    Falco, R., and Fish, D., Prevalence of Ixodes dammininear the homes of Lyme disease patients in Westchester County, New York, Am. J. Epidemiol. 127: 826–830 (1988).PubMedGoogle Scholar
  40. 40.
    Falco, R., and Fish, D., Ticks parasitizing humans in a Lyme disease endemic area of southern New York state, Am. J. Epidemiol. 128: 1146–1152 (1988).PubMedGoogle Scholar
  41. 41.
    Fumarola, D., Munno, I., Marcuccio, C., and Miragliotta, G., Endotoxin-like activity associated with Lyme disease borrelia, Zentralbl. Bakteriol. Mikrobiol. Hyg. A 263: 137–141 (1986).Google Scholar
  42. 42.
    Garin Bujadoux, C., Paralysie par les tiques, J. Med. Lyon 71c: 765–767 (1922).Google Scholar
  43. 43.
    Goubau, P., and Biggignum, G., Lyme borreliosis: The new face of an old disease, Acta Clin. Belg. 42: 1–4 (1987).PubMedGoogle Scholar
  44. 44.
    Greene, R., Walker, R., Nicholson, W., Heidner, H., Levin, J., Burgess, E., Wyand, M., Breitschwerdt, E., and Berkhoff, H., Immunoblot analysis of immunoglobulin G response to the Lyme disease agent (Borrelia burgdorferi)in experimentally and naturally exposed dogs, J. Clin. Microbiol. 26: 648–653 (1988).PubMedGoogle Scholar
  45. 45.
    Grodzicki R., and Steere, A., Comparison of immunoblotting and indirect enzyme-linked immunosorbent assay using different antigen preparations for diagnosing early Lyme disease, J. Infect. Dis. 157: 790–797 (1988).PubMedCrossRefGoogle Scholar
  46. 46.
    Habicht, G., Beck, G., Benach, J., Coleman, J., and Leichtling, K., Lyme disease spirochetes induce human and murine interleukin-1 production, J. Immunol. 134: 3147–3154 (1985).PubMedGoogle Scholar
  47. 47.
    Habicht, G., Beck, G., Benach, J., and Coleman, J., Borrelia burgdorferilipopolysaccharide and its role in the pathogenesis of Lyme disease, Zentralbl. Bakteriol. Mikrobiol. Hyg. A 263: 137–141 (1986).PubMedGoogle Scholar
  48. 48.
    Hanrahan, J., Benach, J., Coleman, J., Bosler, E., Morse, D., Cameron, D., Edelman, R., and Kaslow, R., Incidence and cumulative frequency of endemic Lyme disease in a community, J. Infect. Dis. 150: 489–496 (1984).PubMedCrossRefGoogle Scholar
  49. 49.
    Hard, S., Erythema chronicum migrans (Afzelii) associated with mosquito bite, Acta Derm. Venereol. 46: 473–476 (1966).PubMedGoogle Scholar
  50. 50.
    Hardin, J., Steere, A., and Malawista, S., Immune complexes and the evolution of Lyme arthritis: Dissemination and localization of abnormal Clq binding activity, N. Engl. J. Med. 301: 1358–1363 (1979).PubMedCrossRefGoogle Scholar
  51. 51.
    Hardin, J., Steere, A., and Malawista, S., The pathogenesis of arthritis in Lyme disease: Humoral immune responses and the role of intraarticular immune complexes, Yale J. Biol. Med. 57: 589–593 (1984).PubMedGoogle Scholar
  52. 52.
    Hechemy, K., Harris, H., Duerr, M., Benach, J., and Reimer, C., Immunoglobulin G subclasses specific to Borrelia burgdorferiin patients with Lyme disease, Ann. N.Y. Acad. Sci. 539: 162–169 (1988).PubMedCrossRefGoogle Scholar
  53. 53.
    Hedberg, C., Osterholm, M., MacDonald, K., and White, K., An interlaboratory study of antibody to Borrelia burgdorferi, J. Infect. Dis. 154: 1325–1327 (1987).CrossRefGoogle Scholar
  54. 54.
    Hellerstrom, S., Erythema chronicum migrans Afzelii, Acta Derm. Venereol. 11: 315–321 (1930).Google Scholar
  55. 55.
    Hollströ, E., Successful treatment of erythema migrans Afzelius, Acta Derm. Venereol. 31: 235–243 (1951).Google Scholar
  56. 56.
    Johnson, R., Schmid, G., Hyde, F., Steigerwalt, G., and Brenner, D., Borrelia burgdorferisp. nov.: Etiologic agent of Lyme disease, Int. J. Syst. Bacteriol. 34: 496–497 (1984).CrossRefGoogle Scholar
  57. 57.
    Johnson, R., Kodner, C., and Russell, M., Active immunization of hamsters against experimental infection with Borrelia burgdorferi, Infect. Immun. 54: 897–898 (1986).Google Scholar
  58. 58.
    Johnson, R., Kodner, C., and Russell, M., In vitro and in vivo susceptibility of the Lyme disease spirochete, Borrelia burgdorferi,to four antimicrobial agents, Antimicrob. Agents Chemother. 31: 164–167 (1987).PubMedCrossRefGoogle Scholar
  59. 59.
    Johnson, S., Klein, G., Schmid, G., and Feeley, J., Susceptibility of the Lyme disease spirochete to seven antimicrobial agents, Yale J. Biol. Med. 57: 99–103 (1984).Google Scholar
  60. 60.
    Johnson, S., Klein, G., Schmid, G., Bowen, G., Feeley, J., and Schulze, T., Lyme disease: A selective medium for isolation of the suspected etiologic agent, a spirochete, J. Clin. Microbiol. 19: 81–82 (1984).PubMedGoogle Scholar
  61. 61.
    Kawabata, M., Baba, S., Iguchi, K., Yamaguti, N., and Russell, H., Lyme disease in Japan and its possible incriminated tick vector, Ixodes persulcatus, J. Infect. Dis. 156: 854 (1987).PubMedCrossRefGoogle Scholar
  62. 62.
    Kirsch, M., Ruben, F., Steere, A., Duray, P., Norden, C., and Winkelstein, A., Fatal adult respiratory distress syndrome in a patient with Lyme disease, J. Am. Med. Assoc. 259: 2737–2739 (1988).CrossRefGoogle Scholar
  63. 63.
    Kramer, N., Rickert, R., Brodkin, R., and Rosenstein, E., Septal panniculitis as a manifestation of Lyme disease, Am. J. Med. 81: 149–157 (1986).PubMedCrossRefGoogle Scholar
  64. 64.
    Levine, J., Wilson, M., and Spielman, A., Mice as reservoirs of the Lyme disease spirochete, Am. J. Trop. Med. Hyg. 34: 355–360 (1985).PubMedGoogle Scholar
  65. 65.
    Lipschütz, B., Über eine seltene Erythemform (Erythema chronicum migrans), Arch. Dermatol. Syphilol. 118: 349–356 (1913).Google Scholar
  66. 66.
    Luft, B., Volkman, D., Halperin, J., and Dattwyler, R., New chemotherapeutic approaches in the treatment of Lyme borreliosis, Ann. N.Y. Acad. Sci. 539: 352–361 (1988).PubMedCrossRefGoogle Scholar
  67. 67.
    Magnarelli, L., and Anderson, J., Ticks and biting insects infected with the etiologic agent of Lyme disease, Borrelia burgdorferi, J. Clin. Microbiol. 26: 1482–1486 (1988).PubMedGoogle Scholar
  68. 68.
    Magnarelli, L., Anderson, J., Burgdorfer, W., and Chappell, W., Parasitism by Ixodes dammini(Acari: Ixodidae)and antibodies to spirochetes in mammals at Lyme disease foci in Connecticut, USA, J. Med. Entomol. 21: 52–57 (1984).PubMedGoogle Scholar
  69. 69.
    Magnarelli, L., Anderson, J., Kaufman, A., Lieberman, L., and Whitney, G., Borreliosis in dogs from southern Connecticut, J. Am. Vet. Med. Assoc. 186: 955–959 (1985).PubMedGoogle Scholar
  70. 70.
    Magnarelli, L., Anderson, J., and Barbour, A., The etiologic agent of Lyme disease in deer flies, horse flies, and mosquitoes, J. Infect. Dis. 154: 355–358 (1986).PubMedCrossRefGoogle Scholar
  71. 71.
    Magnarelli, L., Anderson, J., and Johnson, R., Crossreactivity in serological tests for Lyme disease and other spirochetal infections, J. Infect. Dis. 156: 183–188 (1987).PubMedCrossRefGoogle Scholar
  72. 72.
    Marcus, L., Patterson, M., Gilfillan, R., and Urband, P., Antibodies to Borrelia burgdorferiin New England horses: Serologic survey, Am. J. Vet. Res. 46: 2570–2571 (1985).PubMedGoogle Scholar
  73. 73.
    Marcus, L., Steere, A., Duray, P., Anderson, A., and Mahoney, E., Fatal pancarditis in a patient with coexistent Lyme disease and babesiosis. Demonstration of spirochetes in the myocardium, Ann. Intern. Med. 103: 374–376 (1985).PubMedGoogle Scholar
  74. 74.
    Markowitz, L., Steere, A., Benach, J., Slade, J., and Broome, C., Lyme disease during pregnancy, J. Am. Med. Assoc. 255: 3394–3396 (1986).CrossRefGoogle Scholar
  75. 75.
    Mather, T., Ribeiro, J., and Spielman, A., Lyme disease and babesiosis: Acaricide focussed on potentially infected ticks, Am. J. Trop. Med. Hyg. 36: 609–614 (1987).PubMedGoogle Scholar
  76. 76.
    Mertz, L., Wobig, G., Duffy, J., and Katzmann, J., Ticks, spirochetes and new diagnostic tests for Lyme disease, Mayo Clin. Proc. 60: 402–406 (1985).PubMedCrossRefGoogle Scholar
  77. 77.
    Neubert, U., Munchhoff, P., Volker, B., Reimers, C., and Pfluger, K., Borrelia burgdorferiinfections in Bavarian forest workers: A follow-up study, Ann. N.Y. Acad. Sci. 539: 476–479 (1988).CrossRefGoogle Scholar
  78. 78.
    Osterholm, M., Forfang, J., White, K., and Kuritsky, J., Lyme disease in Minnesota: Epidemiologic and serologic findings, Yale J. Biol. Med. 57: 677–683 (1984).PubMedGoogle Scholar
  79. 79.
    Pachner, A., and Steere, A., The triad of neurologic manifestations of Lyme disease: Meningitis, cranial neuritis, and radiculoneuritis, Neurology 35: 47–53 (1985).PubMedCrossRefGoogle Scholar
  80. 80.
    Pfister, H.-W., Neubert, U., Wilske, B., Preac-Mursic, V., Einhaupl, K., and Borasio, G., Reinfection with Borrelia burgdorferi, Lancet 2: 984–985 (1986).CrossRefGoogle Scholar
  81. 81.
    Piesman, J., and Sinsky, R., Ability of Ixodes scapularis, Dermacentor variabilis,and Amblyomma americanum(Acari: Ixodidae) to acquire, maintain, and transmit Lyme disease spirochetes (Borrelia burgdorferi), J. Med. Entomol. 25: 336–339 (1988).PubMedGoogle Scholar
  82. 82.
    Reik, L., Steere, A., Bartenhagen, N., Shope, R., and Malawista, S., Neurologic abnormalities of Lyme disease, Medicine 58: 281–294 (1979).PubMedCrossRefGoogle Scholar
  83. 83.
    Reik, L., Burgdorfer, W., and Donaldson, J., Neurologic abnormalities in Lyme disease without erythema chronicum migrans, Am. J. Med. 81: 73–78 (1986).PubMedCrossRefGoogle Scholar
  84. 84.
    Reznick, J., Braunstein, D., Walsh, R., Smith, C., Wolfson, P., Gierke, L., Gorelkin, L., and Chandler, F., Lyme carditis: Electrophysiologic and histopathologic study, Am. J. Med. 81: 923–927 (1986).PubMedCrossRefGoogle Scholar
  85. 85.
    Ribeiro, J., Mather, T., Piesman, J., and Spielman, A., Dissemination and salivary delivery of Lyme disease spirochetes in vector ticks (Acari: Ixodidae), J. Med. Entomol. 24: 201–205 (1987).PubMedGoogle Scholar
  86. 86.
    Schechter, S., Lyme disease associated with optic neuropathy, Am. J. Med. 81: 143–145 (1986).PubMedCrossRefGoogle Scholar
  87. 87.
    Schlesinger, P., Duray, P., Burke, B., Steere, A., and Stillman, M., Maternal-fetal transmission of the Lyme disease spirochete, Borrelia burgdorferi, Ann. Intern. Med. 103: 67–68 (1985).PubMedGoogle Scholar
  88. 88.
    Schmid, G., The global distribution of Lyme disease, Rev. Infect. Dis. 7: 741–750 (1985).CrossRefGoogle Scholar
  89. 89.
    Schmid, G., Horsley, R., Steere, A., Hanrahan, J., Davis, J., Bowen, S., Osterholm, M., Weisfeld, J., Hightower, A., and Broome, C., Surveillance of Lyme disease in the United States, 1982, J. Infect. Dis. 151: 1144–1148 (1985).PubMedCrossRefGoogle Scholar
  90. 90.
    Schulze, T., Bowen, G., Bosler, E., Lakat, M., Ormiston, B., and Shisler, J., Amblyomma americanum: A potential vector of Lyme disease in New Jersey, Science 224: 601–603 (1984).PubMedCrossRefGoogle Scholar
  91. 91.
    Schulze, T., Bowen, G., Lakat, M., Parkin, W., and Shisler, J., The role of adult Ixodes dammini(Acari: Ixodidae) in the transmission of Lyme disease in New Jersey, USA, J. Med. Entomol. 22: 88–93 (1985).PubMedGoogle Scholar
  92. 92.
    Schulze, T., McDevitt, W., Parkin, W., and Shilser, J., Effectiveness of two insecticides in controlling Ixodes dammini(Acari: Ixodidiae) following an outbreak of Lyme disease in New Jersey, J. Med. Entomol. 24: 420–424 (1987).PubMedGoogle Scholar
  93. 93.
    Schwan, T., and Burgdorfer, W., Antigenic changes of Borrelia burgdorferi asa result of in vitro cultivation, J. Infect. Dis. 156: 852–853 (1987).PubMedCrossRefGoogle Scholar
  94. 94.
    Scrimenti, R., Erythema chronicum migrans, Arch. Dermatol. 102: 104–105 (1970).PubMedCrossRefGoogle Scholar
  95. 95.
    Shrestha, M., Grodzicki, R., and Steere, A., Diagnosing early Lyme disease, Am. J. Med. 78: 235–240 (1985).PubMedCrossRefGoogle Scholar
  96. 96.
    Smith, L., Burgdorfer, W., and Katz, H., Erythema chronicum migrans, Cutis 17(S): 962–964 (1976).PubMedGoogle Scholar
  97. 97.
    Smith, P., Benach, J., White, D., Stroup, D., and Morse, D., Occupational risk of Lyme disease in endemic areas of New York State, Ann. N.Y. Acad. Sci. 539: 289–301 (1988).PubMedCrossRefGoogle Scholar
  98. 98.
    Snydman, D., Schenkein, D., Berardi, V., Lastavica, C., and Pariser, K., Borrelia burgdorferi injoint fluid in chronic Lyme arthritis, Ann. Intern. Med. 104: 798–800 (1986).PubMedGoogle Scholar
  99. 99.
    Spielman, A., Prospects for suppressing transmission of Lyme disease, Ann. N.Y. Acad. Sci. 539: 212–220 (1988).PubMedCrossRefGoogle Scholar
  100. 100.
    Stanek, G., Pletschette, M., Flamm, H., Hirschl, A., Aberer, E., Kristoferitsch, W., and Schmutzhard, E., European Lyme borreliosis, Ann. N.Y. Acad. Sci. 539: 274–282 (1988).PubMedCrossRefGoogle Scholar
  101. 101.
    Steere, A., and Malawista, S., Cases of Lyme disease in the United States: Locations correlated with distribution of Ixodes dammini, Ann. Intern. Med. 91: 730–733 (1979).PubMedGoogle Scholar
  102. 102.
    Steere, A., Hardin, J., and Malawista, S., Erythema chronicum migrans and Lyme arthritis: Cryoimmunoglobulins and clinical activity of skin and joints, Science 196: 1121–1122 (1977).PubMedCrossRefGoogle Scholar
  103. 103.
    Steere, A., Malawista, S., Hardin, J., Ruddy, S., Askenase, P., and Andiman, W., Erythema chronicum migrans and Lyme arthritis: The enlarging clinical spectrum, Ann. Intern. Med. 86: 685–698 (1977).PubMedCrossRefGoogle Scholar
  104. 104.
    Steere, A., Malawista, S., Snydman, D., Shope, R., Andiman, W., Ross, M., and Steele, F., Lyme arthritis: An epidemic of oligoarticular arthritis in children and adults in three Connecticut communities, Arthritis Rheum. 20: 7–17 (1977).PubMedCrossRefGoogle Scholar
  105. 105.
    Steere, A., Broderick, T., and Malawista, S., Erythema chronicum migrans and Lyme arthritis: Epidemiologic evidence for a tick vector, Am. J. Epidemiol. 108: 312–321 (1978).PubMedGoogle Scholar
  106. 106.
    Steere, A., Batsford, W., Weinberg, M., Alexander, J., Berger, H., Wolfson, S., and Malawista, S., Lyme carditis: Cardiac abnormalities of Lyme disease, Ann. Intern. Med. 93: 8–16 (1980).PubMedGoogle Scholar
  107. 107.
    Steere, A., Malawista, S., Newman, J., Spieler, P., and Bartenhagen, N., Antibiotic therapy in Lyme disease, Ann. Intern. Med. 93: 1–8 (1980).PubMedGoogle Scholar
  108. 108.
    Steere, A., Bartenhagen, N., Craft, J., Hutchinson, G., Newman, J., Rahn, D., Sigal, L., Spieler, P., Stenn, K., and Malawista, S., The early clinical manifestations of Lyme disease, Ann. Intern. Med. 99: 76–82 (1983).PubMedGoogle Scholar
  109. 109.
    Steere, A., Grodzicki, R., Kornblatt, A., Craft, J., Barbour, A., Burgdorfer, W., Schmid, G., Johnson, E., and Malawista, S., The spirochetal etiology of Lyme disease, N. Engl. J. Med. 308: 733–740 (1983).PubMedCrossRefGoogle Scholar
  110. 110.
    Steere, A., Hutchinson, G., Rahn, D., Sigal, L., Craft, J., Desanna, E., and Malawista, S., Treatment of the early manifestations of Lyme disease, Ann. Intern. Med. 99: 22–26 (1983).PubMedGoogle Scholar
  111. 111.
    Steere, A., Pachner, A., and Malawista, S., Neurologic abnormalities of Lyme disease: Successful treatment with high-dose intravenous penicillin, Ann. Intern. Med. 99: 767–772 (1983).PubMedGoogle Scholar
  112. 112.
    Steere, A., Grodzicki, R., Craft, J., Shrestha, M., Kornblatt, A., and Malawista, S., Recovery of Lyme disease spirochetes from patients, Yale J. Biol. Med. 57 : 557–560 (1984).PubMedGoogle Scholar
  113. 113.
    Steere, A., Malawista, S., Bartenhagen, N., Spieler, P., Rahn, D., Hutchinson, G., Green, J., Snydman, D., and Taylor, E., The clinical spectrum and treatment of Lyme disease, Yale J. Biol. Med. 57: 453–461 (1984).Google Scholar
  114. 114.
    Steere, A., Duray, P., Kauffmann, D., and Wormser, G., Unilateral blindness caused by infection with the Lyme disease spirochete, Borrelia burgdorferi, Ann. Intern. Med. 103: 382–384 (1985).PubMedGoogle Scholar
  115. 115.
    Steere, A., Green, J., Schoen, R., Taylor, E., Hutchinson, G., Rahn, D., and Malawista, S., Successful parenteral penicillin therapy of established Lyme arthritis, N. Engl. J. Med. 312: 869–874 (1985).PubMedCrossRefGoogle Scholar
  116. 116.
    Steere, A., Taylor, E., Wilson, M., Levine, J., and Spielman, A., Longitudinal assessment of the clinical and epidemiological features of Lyme disease in a community, J. Infect. Dis. 154: 295–300 (1986).PubMedCrossRefGoogle Scholar
  117. 117.
    Telford, S., Mather, T., Moore, S., Wilson, M., and Spielman, A., Incompetence of deer as reservoirs of the Lyme disease spirochete, Am. J. Trop. Med. Hyg. 39: 105–109 (1988).PubMedGoogle Scholar
  118. 118.
    Weber, K., Schierz, G., Wilske, B., and Preac-Mursic, V., European erythema migrans disease and related disorders, Yale J. Biol. Med. 57: 463–471 (1984).PubMedGoogle Scholar
  119. 119.
    Weder, B., Wiedersheim, P., Matter, L., Steck, A., and Otto, F., Chronic progressive neurological involvement in Borrelia burgdorferiinfection, J. Neurol. 234: 40–43 (1987).PubMedCrossRefGoogle Scholar
  120. 120.
    Williams, C., Curran, A., Lee, A., and Sousa, V., Lyme disease: Epidemiologic characteristics of an outbreak in Westchester County, Ny, Am. J. Public Health 76: 62–65 (1986).PubMedCrossRefGoogle Scholar
  121. 121.
    Wilske, B., Schierz, G., Preac-Mursic, V., Von Busch, K., Kuhbeck, R., Pfister, H., and Einhaupl, K., Intrathecal production of specific antibodies against Borrelia burgdorferiin patients with lymphocytic meningoradiculitis (Bannworth’s syndrome), J. Infect. Dis. 153: 304–314 (1986).PubMedCrossRefGoogle Scholar
  122. 122.
    Wilske, B., Preac-Mursic, V., Schierz, G., Kuhbeck, R., Barbour, A., and Kramer, M., Antigenic variability of Borrelia burgdorferi, Ann. N. Y. Acad. Sci. 539: 126–143 (1988).PubMedCrossRefGoogle Scholar
  123. 123.
    Wilson, M., and Spielman, A., Seasonal activity of immature Ixodes dammini(Acari: Ixodidae), J. Med. Entomol. 22: 408–414 (1985).PubMedGoogle Scholar
  124. 124.
    Wilson, M., Levine, J., and Spielman, A., Effect of deer reduction on abundance of the deer tick (Ixodes dammini), Yale J. Biol. Med. 57: 5697–5705 (1984).Google Scholar
  125. 125.
    Wilson, M., Telford, S., Presman, J., and Spielman, A., Reduced abundance of immature Ixodes dammini(Acari: Ixodidae) following elimination of deer, J. Med. Entomol. 25: 224–228 (1988).PubMedGoogle Scholar

Suggested Reading

  1. Lyme Disease and Related Disorders, Ann. N.Y. Acad. Sci. 539(1988).Google Scholar
  2. Proceedings of the First International Symposium on Lyme Disease, Yale J. Biol. Med. 54(4) (1984).Google Scholar
  3. Proceedings of the Second International Symposium on Lyme Disease and Related Disorders, Zentralbl. Bakteriol. Mikrobiol. Hyg. A. Google Scholar

Copyright information

© Springer Science+Business Media New York 1991

Authors and Affiliations

  • Michael T. Osterholm
    • 1
  • Kristine L. MacDonald
    • 1
  • Craig W. Hedberg
    • 1
  1. 1.Acute Disease Epidemiology SectionMinnesota Department of HealthMinneapolisUSA

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