Lyme disease and the heart

Frontiers in Bioscience

Volumn 8, Issue SUPPL., 2003, Pages

  Haddad, Fadi A ^a   Nadelman, Robert B ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

Atrioventricular conduction; Borrelia burgdorferi; Carditis; Heart; Lyme; Myocarditis; Pericarditis; Review

Indexed keywords

ANTIBIOTIC AGENT; ANTIINFLAMMATORY AGENT; CEFTRIAXONE; DIGOXIN; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; DIURETIC AGENT; DOXYCYCLINE;

ARTHRITIS; ASEPTIC MENINGITIS; ATRIOVENTRICULAR BLOCK; BORRELIA BURGDORFERI; CARDIOMYOPATHY; CARDITIS; CLINICAL FEATURE; CLINICAL TRIAL; CRANIAL NERVE PARALYSIS; DISEASE ASSOCIATION; ENDEMIC DISEASE; ERYTHEMA CHRONICUM MIGRANS; HUMAN; LABORATORY TEST; LYME DISEASE; MYOCARDITIS; NONHUMAN; PERICARDITIS; RADICULITIS; REVIEW; UNITED STATES; ANIMAL; DIFFERENTIAL DIAGNOSIS; DISEASE MODEL; MOUSE;

ACARI; BORRELIA; BORRELIA BURGDORFERI;

ANIMALS; DIAGNOSIS, DIFFERENTIAL; DISEASE MODELS, ANIMAL; HUMANS; LYME DISEASE; MICE; MYOCARDITIS;

EID: 4344643780     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: None     Document Type: Review

References (91)

1. Steere A. C: Lyme disease. N Engl J Med 345, 115-25 (2001)
2. Nadelman R. B., G. P. Wormser: Lyme borreliosis. Lancet 352, 557-65 (1998)
3. Tugwell P, D. T. Dennis, A. Weinstein, G. Wells, B. Shea, G. Nichol, R. Hayward, R. Lightfoot, P. Baker, A. C. Steere: Laboratory evaluation in the diagnosis of Lyme disease. Ann Intern Med 12, 1109-23 (1997)
4. Smith R. P., R. Schoen, D. W. Rahn, V. K. Sikand, J. Nowakowski, D. L. Parenti, M. S. Holman, D. H. Persing, A.C. Steere: Clinical characteristics and treatment outcome of early Lyme disease in patients with microbiologically confirmed erythema migrans. Ann Intern Med 136, 421-8 (2002)
5. Nadelman R. B., G. P. Wormser: Recognition and treatment of erythema migrans: are we off target? Ann Intern Med 136, 477-9 (2002)
6. Nadelman R. B., J. Nowakowski, G. Forseter, N. S. Goldberg, S. Bittker, D. Cooper, M. Aguero-Rosenfeld, G. P. Wormser: The clinical spectrum of early Lyme borreliosis in patients with culture-confirmed erythema migrans. Am J Med 100, 502-8 (1996)
7. Strle F, R. B. Nadelman, J. Cimperman, J. Nowakowski, R. Picken, I. Schwartz, V. Maraspin, M. Aguero-Rosenfeld, S. Varde, S. Lotric-Furlan, G.P. Wormser: Comparison of culture-confirmed erythema migrans caused by Borrelia burgdorferi sensu stricto in New York State and by Borrelia afzelii in Slovenia. Ann Intern Med 130, 32-6 (1999)
8. Luft B. J., R. J. Dattwyler , R. C. Johnson, S. W. Luger, E. M. Bosler, D. W. Rahn, E. J. Masters, E. Grunwaldt, S. D. Gadgil: Azithromycin compared with amoxicillin in the treatment of erythema migrans. A double-blind, randomized, controlled trial. Ann Intern Med 124, 785-91 (1996)
9. Nadelman R. B., S. W. Luger, E. Frank, M. Wisniewski, J. J. Collins, G. P. Wormser: Comparison of cefuroxime axetil and doxycycline in the treatment of early Lyme disease. Ann Intern Med 117, 273-80 (1992)
10. Steere A. C., R. T. Schoen, E. Taylor: The clinical evolution of Lyme arthritis. Ann Intern Med 107, 725-31 (1987)
11. Steere A. C., W. P. Batsford, M. Weinberg, J. Alexander, H. J. Berger, S. Wolfson, S.E. Malawista: Lyme carditis: cardiac abnormalities of Lyme disease. Ann Intern Med 93, 8-16 (1980)
12. Stanek G, J. Klein, R. Bittner, D. Glogar: Borrelia burgdorferi as an etiologic agent in chronic heart failure? Scand J Infect Dis 77, 85-7 (1991)
13. Klein G, G. Stanek, R.Bittner, R. Hovart, C. Holzinger, D. Glogar: Lyme borreliosis as a cause of myocarditis and heart muscle disease. Eur Heart Jour 12 suppl D, 73-75 (1991)
14. Pikelj-Pecnik A, S. Lotric-Furlan, V. Maraspin, J. Cimperman, M. Logar, T. Jurca, F. Strle: Electrocardiographic findings in patients with erythema migrans. Wien Klin Wochenschr 114, 510-4 (2002)
15. Steere A, T. F. Broderick, S. E. Malawista: erythema chronicum migrans and Lyme arthritis: epidemiologic evidence for a tick vector. Am J Epidemiol 108, 312-21 (1978)
16. Lyme disease - Connecticut, 2000. Connecticut Epidemiologist 21, 9-10 (2001)
17. Gerber M. A., E. D. Shapiro, G. S. Burke, V. J. Parcells, G. L. Bell: Lyme disease in children in southeastern Connecticut. Pediatric Lyme Disease Study Group. N Engl J Med 335, 1270-4 (1996)
18. Rubin D. A., C. Sorbera, P. Nikitin, A. McAllister, G. P. Wormser, R. B. Nadelman: Prospective evaluation of heart block complicating early Lyme disease. Pacing Clin Electrophysiol 15, 252-5 (1992)
19. Sangha O, C. B. Phillips, K. E. Fleischmann, T. J. Wang, A. H. Fossel, R. Lew, M.H. Liang, N.A. Shadick: Lack of cardiac manifestations among patients with previously treated Lyme disease. Ann Intern Med 128, 346-53 (1998)
20. O'Connell S, M. Granstrom, J. S. Gray, G. Stanek: Epidemiology of European Lyme borreliosis. Zentralbl Bakteriol 287, 229-40 (1998)
21. van der Linde M. R.: Lyme carditis: clinical characteristics of 105 cases. Scand J Infect Dis Suppl. 77, 81-4 (1991)
22. Dennis D. T.: Lyme disease. Dermatol Clin 13, 537-51 (1995)
23. Liu S., Yuan S, O. Kongstad, S. B. Olsson: Gender differences in the electrophysiological characteristics of atrioventricular conduction system and their clinical implications. Scand Cardiovasc J 35, 313-7 (2001)
24. Rothrock S. G., P. Brandt, B. Godfrey, S. Silvestri, J. Pagane: Is there gender bias in the prehospital management of patients with acute chest pain? Prehosp Emerg Care 5, 331-4 (2001)
25. Li M., T. Masuzawa, N. Takada, F. Ishiguro, H. Fujita, A. Iwaki, H. Wang, J. Wang, M. Kawabata, Y. Yanagihara: Lyme disease Borrelia species in northeastern China resemble those isolated from far eastern Russia and Japan. Appl Environ Microbiol 64, 2705-9 (1998)
26. Strle F: Lyme borreliosis in Slovenia. Zentralbl Bakteriol 289, 643-52 (1999)
27. Schneider B. S., N. S. Zeidner, T. R. Burkot, G. O. Maupin, J. Piesman: Borrelia isolates in Northern Colorado identified as Borrelia bissettii. J Clin Microbiol 38, 3103-5 (2000)
28. van Dam A. P., H. Kuiper, K. Vos, A. Widjojokusumo, B. M. de Jongh, L. Spanjaard, A. C. Ramselaar, M. D. Kramer, J. Dankert: Different genospecies of Borrelia burgdorferi are associated with distinct clinical manifestations of Lyme borreliosis. Clin Infect Dis 17, 708-17 (1993)
29. Wormser G. P., D. Liveris, J. Nowakowski, R. B. Nadelman, L. F. Cavaliere, D. McKenna, D. Holmgren, I. Schwartz: Association of specific subtypes of Borrelia burgdorferi with hematogenous dissemination in early Lyme disease. J Infect Dis 180, 720-5 (1999)
30. Wang G., C. Ojaimi, H. Wu, V. Saksenberg, R. Iyer, D. Liveris, S. A. McClain, G. P. Wormser, I. Schwartz: Disease severity in a murine model of Lyme borreliosis is associated with the genotype of the infecting Borrelia burgdorferi sensu stricto strain. J Infect Dis 186, 782-91 (2002)
31. Case definitions for infectious conditions under public health surveillance: Centers for Disease Control and Prevention. MMWR Recomm Rep 46 (RR-10), 1-55 (1997)
32. Stanek G, S. O'Connell, M. Cimmino, E. Aberer, W. Kristoferitsch, M. Granstrom, E. Guy, J. Gray: European Union Concerted Action on Risk Assessment in Lyme Borreliosis: clinical case definitions for Lyme borreliosis. Wien Klin Wochenschr 108, 741-7 (1996)
33. Stanek G, J. Klein, R. Bittner, D. Glogar: Isolation of Borrelia burgdorferi from the myocardium of a patient with longstanding cardiomyopathy. N Engl J Med 322, 249-52 (1990)
34. Lardieri G, A. Salvi, F. Camerini, M. Cinco, G. Trevisan: Isolation of Borrelia burgdorferi from myocardium. Lancet 342 (8869), 490 (1993)
35. Reznick J. W., D. B. Braunstein, R. L. Walsh, C. R. Smith, P. M. Wolfson, L. W. Gierke, L. Gorelkin, F. W. Chandler: Lyme carditis. Electrophysiologic and histopathologic study. Am J Med 81, 923-7 (1986)
36. McAlister HF, P. T. Klementowicz, C. Andrews, J. D. Fisher, M. Feld, S. Furman: Lyme carditis: an important cause of reversible heart block. Ann Intern Med 110, 339-45 (1998)
37. Rey M. J., M. Zimmermann, R. Adamec, M. Fleisch, C. Viquerat, J. de Freudenreich: Intra-hisian 2:1 atrioventricular block secondary to Lyme disease. Eur Heart J 12, 1048-51 (1991)
38. Midttun M, A. M. Lebech, K. Hansen, J. Videbaek: Lyme carditis: a clinical presentation and long time follow-up. Scand J Infect Dis 29, 153-7 (1997)
39. van der Linde M. R., H. J. Crijns, J. de Koning, J. A. Hoogkamp-Korstanje, J. J. de Graaf, D. A. Piers, A. van der Galien, K. I. Lie: Range of atrioventricular conduction disturbances in Lyme borreliosis: a report of four cases and review of other published reports. Br Heart J 63, 162-8 (1990)
40. Cornuau C, M. Bardet, P. Baudoin, P. L. Daumas, B. Oblet, G. Poirot, M. Valois: Acute syncopal auriculoventricular block in Lyme disease. Presse Med 13, 888 (1984)
41. Nadelman R. B., J. Nowakowski, D. Fish, R. C. Falco, K. Freeman, D. McKenna, P. Welch, R. Marcus, M. E. Aguero-Rosenfeld, D. T. Dennis, G. P. Wormser; Tick Bite Study Group: Prophylaxis with single-dose doxycycline for the prevention of Lyme disease after an Ixodes scapularis tick bite. N Engl J Med 345, 79-84 (2001)
42. Nadelman R. B., H. W. Horowitz, T. C. Hsieh, J. M. Wu, M. E. Aguero-Rosenfeld, I. Schwartz, J. Nowakowski, S. Varde, G. P. Wormser: Simultaneous human granulocytic ehrlichiosis and Lyme borreliosis. N Engl J Med 337, 27-30 (1997)
43. Sweeney C. J., M. Ghassemi, W. A. Agger, D. H. Persing: Coinfection with Babesia microti and Borrelia burgdorferi in a western Wisconsin resident. Mayo Clin Proc 73, 338-41 (1998)
44. Kapusta P., J. P. Fauchier, P. Cosnay, R. Huguet, O. Grezard, P. Rouesnel: Sinoatrial and atrioventricular conduction disorders in Lyme disease. Apropos of 2 case reports. Arch Mal Coeur Vaiss 79, 1361-6 (1986)
45. Dunica S, J. C. Piette, N. Nassar, P. Beaufils: A new cause of acute transitory auriculoventricular block: Lyme disease. Arch Mal Coeur Vaiss 79, 1251-5 (1986)
46. Vidaillet H. J. Jr, S. K. Broste, J. J. Marx Jr, P. A. McCarty, P. M. Layde, P. D. Mitchell, A. Dlesk: The 12-lead electrocardiogram of "healthy" ambulatory subjects with positive Lyme immunoserology. Am J Cardiol 71, 1249-51 (1993)
47. Rosenfeld M. E., B. Beckerman, M. F. Ward, A. Sama: Lyme carditis: complete AV dissociation with episodic asystole presenting as syncope in the emergency department. J Emerg Med 17, 661-4 (1999)
48. Vlay SC, J. P. Dervan, J. Elias, P. P. Kane, R. Dattwyler: Ventricular tachycardia associated with Lyme carditis. Am Heart J 121, 1558-60 (1991)
49. Kimball SA, P. A. Janson, P. J. LaRaia: Complete heart block as the sole presentation of Lyme disease. Arch Intern Med 149, 1897-8 (1989)
50. Baylac-Domengetroy F, C. Vieyres, R. Barraine: Complete heart block as the sole presentation of Lyme disease. Arch Intern Med 151, 1240 (1991)
51. Marcus L. C., A.C. Steere, P. Duray, A. Anderson, E. Mahoney: Fatal pancarditis in a patient with coexistent Lyme disease and babesiosis. Demonstration of spirochetes in the myocardium. Ann Intern Med 103, 374-6 (1985)
52. Cary NR, B. Fox, D. Wright, S. Cutler, L. Shapiro, A. Grace: Fatal Lyme carditis and endodermal heterotopia of the atrioventricular node. Postgrad Med J 66, 134-6 (1990)
53. Horowitz H, R. Belkin: Acute myopericarditis resulting from Lyme disease. Am Heart J 130, 176-8 (1995)
54. Bergler-Klein J, H. Sochor, G. Stanek, S. Globits, R. Ullrich, D. Glogar: Indium 111- monoclonal antimyosin antibody and magnetic resonance imaging in the diagnosis of acute Lyme myopericarditis. Arch Intern Med 153, 2696-2700 (1993)
55. Ciesielski C. A., L. E. Markowitz, R. Horsley, A. W. Hightower, H. Russell, C. V. Broome: Lyme disease surveillance in the United States, 1983-1986. Rev Infect Dis. 11 Suppl 6, S1435-41 (1989)
56. Bruyn G, J. de Koning, F. Reijsoo, P. Houtman, J. Hoogkamp-Korstanje: Lyme pericarditis leading to tamponade. Br J Rheumatol 33, 862-6 (1994)
57. Gasser R, S. Horn, E. Reisinger, L. Fischer, R. Pokan, I. Wendelin, W. Klein: First description of recurrent pericardial effusion associated with Borrelia burgdorferi infection. Int J Cardiol 64, 309-10 (1998)
58. Klein G, R.Bittner, R. Hovart, C. Holzinger, D. Glogar: Lyme borreliosis as a cause of myocarditis and heart muscle disease. Eur Heart Jour 12 suppl D, 73-75 (1991)
59. Duray P. H: Clinical pathologic correlations of Lyme disease. Rev Infect Dis 11 Suppl 6, S1487-93 (1989)
60. de Koning J, J. A. Hoogkamp-Korstanje, M. R. van der Linde, H. J. Crijns: Demonstration of spirochetes in cardiac biopsies of patients with Lyme disease. J Infect Dis 160, 150-3 (1989)
61. Case records of the Massachusetts General Hospital. Weekly clinicopathological exercises. Case 17-2002. A 55-year-old man with second-degree atrioventricular block and chest pain. N Engl J Med 346, 1732-8 (2002)
62. Gasser R., F. Fruhwald, M. Schumacher, G. Seinost, E. Reisinger, B. Eber, A. Keplinger, R. Horvath, B. Sedaj, W. Klein, K. Pierer: Reversal of Borrelia burgdorferi associated dilated cardiomyopathy by antibiotic treatment? Cardiovasc Drugs Ther 10, 351-60 (1996)
63. Gasser R, J. Dusleag, E. Reisinger, R. Stauber, B. Feigl, S. Pongratz, W. Klein, C. Furian, K. Pierer: Reversal by ceftriaxone of dilated cardiomyopathy Borrelia burgdorferi infection. Lancet 339 (8802), 1174-5 (1992)
64. Sonnesyn S. W., S. C. Diehl, R. C. Johnson, S. H. Kubo, J. L. Goodman: A prospective study of the seroprevalence of Borrelia burgdorferi infection in patients with severe heart failure. Am J Cardiol 76, 97-100 (1995)
65. Suedkamp M, C. Lissel, H. Eiffert, M. Flesch, M. Boehm, U. Mehlhorn, R. Thomssen, E. R. de Vivie: Cardiac myocytes of hearts from patients with end-stage dilated cardiomyopathy do not contain Borrelia burgdorferi DNA. Am Heart J 138, 269-72 (1999)
66. Canver CC, J. Chanda, D. M. DeBellis, J. M. Kelley: Possible relationship between degenerative cardiac valvular pathology and Lyme disease. Ann Thorac Surg 2000 70, 283-5 (2000)
67. Oksi J, L. M. Voipio-Pulkki, J. Uksila, K. Pulkki, P. Laippala, M. K. Viljanen: Borrelia burgdorferi infection in patients with suspected acute myocardial infarction. Lancet 350, 1447-8 (1997)
68. Anish S. A.: Case report: possible Lyme endocarditis. N J Med 90, 599-601 (1993)
69. Kaell A. T., D. J. Volkman, P. D. Gorevic, R. J. Dattwyler: Positive Lyme serology in subacute bacterial endocarditis. A study of four patients. JAMA 264, 2916-8 (1990)
70. Kaell A. T., P. R. Redecha, K. B. Elkon, M. G. Golightly, P. E. Schulman, R. J. Dattwyler, D. L. Kaell, R. D. Inman, C. L. Christian, D. J. Volkman: Occurrence of antibodies to Borrelia burgdorferi in patients with nonspirochetal subacute bacterial endocarditis. Ann Intern Med 119, 1079-83 (1993)
71. Armstrong A. L., S. W. Barthold, D. H. Persing, D. S. Beck: Carditis in Lyme disease susceptible and resistant strains of laboratory mice infected with Borrelia burgdorferi. Am J Trop Med Hyg 47, 249-58 (1992)
72. Ruderman E. M., J. S. Kerr, S. R. Telford, A. Spielman, L. H. Glimcher, E. M. Gravallese: Early murine Lyme carditis has a macrophage predominance and is independent of major histocompatibility complex class II-CD4+ T-cell interactions. J Infect Dis 171, 362-70 (1995)
73. McKisic M. D., L. W. Redmond, S. W. Barthold: Cutting edge: T cell-mediated pathology in murine Lyme borreliosis. J Immunol 164, 6096-9 (2000)
74. Saba S, B. A. VanderBrink, G. Perides, L. J. Glickstein, M. S. Link, M. K. Homoud, R. T. Bronson, M. Estes, P. J. Wang: Cardiac conduction abnormalities in a mouse model of Lyme borreliosis. J Interv Card Electrophysiol 5, 137-43 (2001)
75. Recommendations for test performance and interpretation from the second national conference on serologic diagnosis of Lyme disease. MMWR 44, 590-591 (1997)
76. Wormser G. P., M. E. Aguero-Rosenfeld, R. B. Nadelman: Lyme disease serology: problems and opportunities. JAMA 282, 79-80 (1999)
77. Aguero-Rosenfeld M. E., J. Nowakowski, S. Bittker, D. Cooper, R. B. Nadelman, G. P. Wormser: Evolution of the serologic response to Borrelia burgdorferi in treated patients with culture-confirmed erythema migrans. J Clin Microbiol 34, 1-9 (1996)
78. Wormser G. P., S. Bittker, D. Cooper, J. Nowakowski, R. B. Nadelman, C. Pavia: Yield of large-volume blood cultures in patients with early Lyme disease. J Infect Dis 184, 1070-2 (2001)
79. Sigal L.: Lyme Disease: A review of aspects of its immunology and immunopathogenesis. Annu Rev Immun 15, 63-92 (1997)
80. Schwartz I, Wormser G. P., J. J. Schwartz, D. Cooper, P. Weissensee, A. Gazumyan, E. Zimmermann, N. S. Goldberg, S. Bittker, G. L. Campbell, et al. Diagnosis of early Lyme disease by polymerase chain reaction amplification and culture of skin biopsies from erythema migrans lesions. J Clin Microbiol 30, 3082-8 (1992)
81. Wormser G. P., C. Carbonaro, S. Miller, J. Nowakowski, R. B. Nadelman, S. Sivak, M. E. Aguero-Rosenfeld: A limitation of 2-stage serological testing for Lyme disease: enzyme immunoassay and immunoblot assay are not independent tests. Clin Infect Dis 30, 545-8 (2000)
82. Feder H. M. Jr, M.A. Gerber, S. W. Luger, R. W. Ryan: Persistence of serum antibodies to Borrelia burgdorferi in patients treated for Lyme disease. Clin Infect Dis 15, 788-93 (1992)
83. Veluvolu P., A. A. Balian, R. Goldsmith, T. E. Gallant, L. Barthel, H. J. Vidaillet, J. W. Melski: Lyme carditis. Evaluation by Ga-67 and MRI. Clin Nucl Med 17, 823 (1992)
84. Rienzo R. J., D. E. Morel, D. Prager, L. Barron, R. Post: Gallium avid Lyme myocarditis. Clin Nucl Med 12, 475-6 (1987)
85. Globits S., J. Bergler-Klein, G. Stanek, R. Ullrich, D. Glogar: Magnetic resonance imaging in the diagnosis of acute Lyme carditis. Cardiology 85, 415-7 (1994)
86. Jacobs J. C., J. M. Rosen, I. S. Szer: Lyme myocarditis diagnosed by gallium scan. J Pediatr 105, 950-2 (1984)
87. Wormser G. P., R. B. Nadelman, R. J. Dattwyler, D. T. Dennis, E. D. Shapiro, A. C.Steere, T. J. Rush, D. W. Rahn, P. K. Coyle, D. H. Persing, D. Fish, B. J. Luft: Practice guidelines for the treatment of Lyme disease. The Infectious Diseases Society of America. Clin Infect Dis 31 Suppl 1, 1-14 (2000)
88. Wormser G. P., R. Ramanathan, J. Nowakowski, D. McKenna, D. Holmgren, P. Visintainer, R. Dornbush, B. Singh, R. B. Nadelman: Duration of antibiotic therapy for early Lyme disease: a prospective, double-blind, randomized study. Ann Intern Med. In press
89. Dattwyler R. J., B. J. Luft, M. J. Kunkel, M. F. Finkel, G. P. Wormser, T. J. Rush, E. Grunwaldt, W. A. Agger, M. Franklin, D. Oswald, L. Cockey, D. Maladorno: Ceftriaxone compared with doxycycline for the treatment of acute disseminated Lyme disease. N Engl J Med 337, 289-94 (1997)
90. Nagi K. S., R. K. Thakur: Lyme carditis: indications for cardiac pacing. Can J Cardiol 11, 335-8 (1995)
91. Lorincz L, A. Lakos, P. Kovacs, C. Varvolgyi, P. Polgar, F. Worum: Temporary pacing in complete heart block due to Lyme disease: a case report. Pacing Clin Electrophysiol 12, 1433-6 (1989)