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Chapter 2 : Late Manifestations of Lyme Borreliosis

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Late Manifestations of Lyme Borreliosis, Page 1 of 2

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Abstract:

In the early 1980s, W. Burgdorfer and colleagues were the first to culture the causative agent of the disease, at that time designated Lyme disease, from ticks in an area where it was endemic. has been shown to survive in the extracellular matrix, hiding from host immune responses and allowing for long-lasting infection. Coinfections with other tick-borne pathogens can occur; culture could be hampered by antibiotic treatment, and inhomogeneous distribution of the bacterium through infected tissues could affect the chance to obtain positive cultures. The course of Lyme borreliosis in experimentally infected dogs was first described by Appel and colleagues. The objective clinical manifestations of Lyme borreliosis are similar worldwide, but there are regional variations, especially between the symptoms found in the United States, where Lyme borreliosis is exclusively caused by , and those found in Europe, where Lyme borreliosis is primarily caused by and , but also . Erythema migrans is the most frequent clinical sign several days to weeks after infection and can be clinically diagnosed. Lyme borreliosis has become the most common vector-borne disease in the United States and Central Europe.

Citation: Hovius J, van Dam A, Fikrig E. 2009. Late Manifestations of Lyme Borreliosis, p 9-25. In Fratamico P, Smith J, Brogden K (ed), Sequelae and Long-Term Consequences of Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555815486.ch2

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Figures

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Figure 1.

The obligate enzootic life cycle of sensu lato. (We thank K. E. Hovius for the donation of the figure.)

Citation: Hovius J, van Dam A, Fikrig E. 2009. Late Manifestations of Lyme Borreliosis, p 9-25. In Fratamico P, Smith J, Brogden K (ed), Sequelae and Long-Term Consequences of Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555815486.ch2
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Image of Figure 2.
Figure 2.

The number of reported annual cases of Lyme borreliosis in the United States from 1991 to 2006. Patients were reported to the Centers for Disease Control and Prevention from 1991 to 2006, and cases were defined using stringent case definitions ( ). Numbers are likely to be an underestimation ( ). (The figure is published courtesy of the CDC.)

Citation: Hovius J, van Dam A, Fikrig E. 2009. Late Manifestations of Lyme Borreliosis, p 9-25. In Fratamico P, Smith J, Brogden K (ed), Sequelae and Long-Term Consequences of Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555815486.ch2
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References

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1. Aalto, A.,, J. Sjowall,, L. Davidsson,, P. Forsberg, and, O. Smedby. 2007. Brain magnetic resonance imaging does not contribute to the diagnosis of chronic neuroborreliosis. Acta Radiol. 48:755762.
2. Aberer, E.,, H. Klade, and, G. Hobisch. 1991. A clinical, histological, and immunohistochemical comparison of acrodermatitis chronica atrophicans and morphea. Am. J. Dermatopathol. 13:334341.
3. Ackermann, R.,, P. Horstrup, and, R. Schmidt. 1984. Tick-borne meningopolyneuritis (Garin-Bujadoux, Bannwarth). Yale J. Biol. Med. 57:485490.
4. Ackermann, R.,, B. Rehse-Kupper,, E. Gollmer, and, R. Schmidt. 1988. Chronic neurologic manifestations of erythema migrans borreliosis. Ann. N. Y. Acad. Sci. 539:1623.
5. Afzelius, A. 1921. Erythema chronicum migrans. Acta Derm. Venereol. 2:120125.
6. Agosta, F.,, M. A. Rocca,, B. Benedetti,, R. Capra,, C. Cordioli, and, M. Filippi. 2006. MR imaging assessment of brain and cervical cord damage in patients with neuroborreliosis. AJNR Am. J. Neuroradiol. 27:892894.
7. Alban, P. S.,, P. W. Johnson, and, D. R. Nelson. 2000. Serum-starvation-induced changes in protein synthesis and morphology of Borrelia burgdorferi. Microbiology 146:119127.
8. Anderson, J. F.,, R. C. Johnson,, L. A. Magnarelli, and, F. W. Hyde. 1986. Involvement of birds in the epidemiology of the Lyme disease agent Borrelia burgdorferi. Infect. Immun. 51:394396.
9. Anderson, J. F.,, and L. A. Magnarelli. 1980. Vertebrate host relationships and distribution of ixodid ticks (Acari: Ixodidae) in Connecticut, USA. J. Med. Entomol. 17:314323.
10. Anguita, J.,, V. Thomas,, S. Samanta,, R. Persinski,, C. Hernanz,, S. W. Barthold, and, E. Fikrig. 2001. Borrelia burgdorferi-induced inflammation facilitates spirochete adaptation and variable major protein-like sequence locus recombination. J. Immunol. 167:33833390.
11. Anonymous. 1997. Case definitions for infectious conditions under public health surveillance. MMWR Recommend. Rep. 46:155.
12. Appel, M. J.,, S. Allan,, R. H. Jacobson,, T. L. Lauderdale,, Y. F. Chang,, S. J. Shin,, J. W. Thomford,, R. J. Todhunter, and, B. A. Summers. 1993. Experimental Lyme disease in dogs produces arthritis and persistent infection. J. Infect. Dis. 167:651664.
13. Armstrong, A. L.,, S. W. Barthold,, D. H. Persing, and, D. S. Beck. 1992. Carditis in Lyme disease susceptible and resistant strains of laboratory mice infected with Borrelia burgdorferi. Am. J. Trop. Med. Hyg. 47:249258.
14. Asbrink, E.,, E. Brehmer-Andersson, and, A. Hovmark. 1986. Acrodermatitis chronica atrophicans—a spirochetosis. Clinical and histopathological picture based on 32 patients; course and relationship to erythema chronicum migrans Afzelius. Am. J. Dermatopathol. 8:209219.
15. Asbrink, E.,, B. Hederstedt, and, A. Hovmark. 1984. The spirochetal etiology of erythema chronicum migrans Afzelius. Acta Derm. Venereol. 64:291295.
16. Asbrink, E.,, and A. Hovmark. 1985. Successful cultivation of spirochetes from skin lesions of patients with erythema chronicum migrans Afzelius and acrodermatitis chronica atrophicans. Acta Pathol. Microbiol. Immunol. Scand. Sect. B 93:161163.
17. Asbrink, E.,, A. Hovmark, and, B. Hederstedt. 1985. Serologic studies of erythema chronicum migrans Afzelius and acrodermatitis chronica atrophicans with indirect immunofluorescence and enzyme-linked immunosorbent assays. Acta Derm. Venereol. 65:509514.
18. Asbrink, E.,, A. Hovmark, and, I. Olsson. 1986. Clinical manifestations of acrodermatitis chronica atrophicans in 50 Swedish patients. Zentralbl. Bakteriol. Mikrobiol. Hyg. A 263:253261.
19. Asbrink, E.,, I. Olsson, and, A. Hovmark. 1986. Erythema chronicum migrans Afzelius in Sweden. A study on 231 patients. Zentralbl. Bakteriol. Mikrobiol. Hyg. A 263:229236.
20. Bai, Y.,, K. Narayan,, D. Dail,, M. Sondey,, E. Hodzic,, S. W. Barthold,, A. R. Pachner, and, D. Cadavid. 2004. Spinal cord involvement in the nonhuman primate model of Lyme disease. Lab. Invest. 84:160172.
21. Bannwarth A. 1941. Chronische lymphocytare meningitis, entzundliche polyneuritis un ‘Rheumatismus’: ein betrag zum problem ‘allergie und nervensystem’. Arch. Psych. Nervenkrank. 113:284376.
22. Barbour, A. G. 1984. Isolation and cultivation of Lyme disease spirochetes. Yale J. Biol. Med. 57:521525.
23. Barthold, S. W. 1991. Infectivity of Borrelia burgdorferi relative to route of inoculation and genotype in laboratory mice. J. Infect. Dis. 163:419420.
24. Barthold, S. W.,, D. S. Beck,, G. M. Hansen,, G. A. Terwilliger, and, K. D. Moody. 1990. Lyme borreliosis in selected strains and ages of laboratory mice. J. Infect. Dis. 162:133138.
25. Barthold, S. W.,, and M. de Souza. 1995. Exacerbation of Lyme arthritis in beige mice. J. Infect. Dis. 172:778784.
26. Barthold, S. W.,, M. S. de Souza,, J. L. Janotka,, A. L. Smith, and, D. H. Persing. 1993. Chronic Lyme borreliosis in the laboratory mouse. Am. J. Pathol. 143:959971.
27. Barthold, S. W.,, K. D. Moody,, G. A. Terwilliger,, P. H. Duray,, R. O. Jacoby, and, A. C. Steere. 1988. Experimental Lyme arthritis in rats infected with Borrelia burgdorferi. J. Infect. Dis. 157:842846.
28. Barthold, S. W.,, D. H. Persing,, A. L. Armstrong, and, R. A. Peeples. 1991. Kinetics of Borrelia burgdorferi dissemination and evolution of disease after intradermal inoculation of mice. Am. J. Pathol. 139:263273.
29. Barthold, S. W.,, C. L. Sidman, and, A. L. Smith. 1992. Lyme borreliosis in genetically resistant and susceptible mice with severe combined immunodeficiency. Am. J. Trop. Med. Hyg. 47:605613.
30. Berglund, J.,, R. Eitrem,, K. Ornstein,, A. Lindberg,, A. Ringer,, H. Elmrud,, M. Carlsson,, A. Runehagen,, C. Svanborg, and, R. Norrby. 1995. An epidemiologic study of Lyme disease in southern Sweden. N. Engl. J. Med. 333:13191327.
31. Brehmer-Andersson, E.,, A. Hovmark, and, E. Asbrink. 1998. Acrodermatitis chronica atrophicans: histopathologic findings and clinical correlations in 111 cases. Acta Derm. Venereol. 78:207213.
32. Brooks, C. S.,, P. S. Hefty,, S. E. Jolliff, and, D. R. Akins. 2003. Global analysis of Borrelia burgdorferi genes regulated by mammalian host-specific signals. Infect. Immun. 71:33713383.
33. Bunikis, J.,, and A. G. Barbour. 2002. Laboratory testing for suspected Lyme disease. Med. Clin. North Am. 86:311340.
34. Burgdorfer, W.,, A. G. Barbour,, S. F. Hayes,, J. L. Benach,, E. Grunwaldt, and, J. P. Davis. 1982. Lyme disease—a tick-borne spirochetosis? Science 216:13171319.
35. Busch, U.,, C. Hizo-Teufel,, R. Boehmer,, V. Fingerle,, H. Nitschko,, B. Wilske, and, V. Preac-Mursic. 1996. Three species of Borrelia burgdorferi sensu lato (B. burgdorferi sensu stricto, B afzelii, and B. garinii) identified from cerebrospinal fluid isolates by pulsed-field gel electrophoresis and PCR. J. Clin. Microbiol. 34:10721078.
36. Cabello, F. C.,, H. P. Godfrey, and, S. A. Newman. 2007. Hidden in plain sight: Borrelia burgdorferi and the extracellular matrix. Trends Microbiol. 15:350354.
37. Cadavid, D.,, Y. Bai,, D. Dail,, M. Hurd,, K. Narayan,, E. Hodzic,, S. W. Barthold, and, A. R. Pachner. 2003. Infection and inflammation in skeletal muscle from nonhuman primates infected with different genospecies of the Lyme disease spirochete Borrelia burgdorferi. Infect. Immun. 71:70877098.
38. Cadavid, D.,, Y. Bai,, E. Hodzic,, K. Narayan,, S. W. Barthold, and, A. R. Pachner. 2004. Cardiac involvement in non-human primates infected with the Lyme disease spirochete Borrelia burgdorferi. Lab. Invest. 84:14391450.
39. Cadavid, D.,, T. O’Neill,, H. Schaefer, and, A. R. Pachner. 2000. Localization of Borrelia burgdorferi in the nervous system and other organs in a nonhuman primate model of lyme disease. Lab. Invest. 80:10431054.
40. Carlson, D.,, J. Hernandez,, B. J. Bloom,, J. Coburn,, J. M. Aversa, and, A. C. Steere. 1999. Lack of Borrelia burgdorferi DNA in synovial samples from patients with antibiotic treatment-resistant Lyme arthritis. Arthritis Rheum. 42:27052709.
41. Casjens, S.,, N. Palmer,, R. van Vugt,, W. M. Huang,, B. Stevenson,, P. Rosa,, R. Lathigra,, G. Sutton,, J. Peterson,, R. J. Dodson,, D. Haft,, E. Hickey,, M. Gwinn,, O. White, and, C. M. Fraser. 2000. A bacterial genome in flux: the twelve linear and nine circular extrachromosomal DNAs in an infectious isolate of the Lyme disease spirochete Borrelia burgdorferi. Mol. Microbiol. 35:490516.
42. Coyle, P. K. 1989. Borrelia burgdorferi antibodies in multiple sclerosis patients. Neurology 39:760761.
43. Coyle, P. K.,, L. B. Krupp, and, C. Doscher. 1993. Significance of reactive Lyme serology in multiple sclerosis. Ann. Neurol. 34:745747.
44. 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, and, D. Maladorno. 1997. Ceftriaxone compared with doxycycline for the treatment of acute disseminated Lyme disease. N. Engl. J. Med. 337:289294.
45. de Koning, J.,, D. J. Tazelaar,, J. A. Hoogkamp-Korstanje, and, J. D. Elema. 1995. Acrodermatitis chronica atrophicans: a light and electron microscopic study. J. Cutan. Pathol. 22:2332.
46. Dhote, R.,, A. L. Basse-Guerineau,, V. Beaumesnil,, B. Christoforov, and, M. V. Assous. 2000. Full spectrum of clinical, serological, and epidemiological features of complicated forms of Lyme borreliosis in the Paris, France, area. Eur. J. Clin. Microbiol. Infect. Dis. 19:809815.
47. Dolan, M. C.,, G. O. Maupin,, B. S. Schneider,, C. Denatale,, N. Hamon,, C. Cole,, N. S. Zeidner, and, K. C. Stafford III. 2004. Control of immature Ixodes scapularis (Acari: Ixodidae) on rodent reservoirs of Borrelia burgdorferi in a residential community of southeastern Connecticut. J. Med. Entomol. 41:10431054.
48. Drouin, E. E.,, L. J. Glickstein, and, A. C. Steere. 2004. Molecular characterization of the OspA(161-175) T cell epitope associated with treatment-resistant Lyme arthritis: differences among the three pathogenic species of Borrelia burgdorferi sensu lato. J. Autoimmun. 23:281292.
49. England, J. D.,, R. P. Bohm, Jr.,, E. D. Roberts, and, M. T. Philipp. 1997. Lyme neuroborreliosis in the rhesus monkey. Semin. Neurol. 17:5356.
50. Fagrell, B.,, G. Stiernstedt, and, J. Ostergren. 1986. Acrodermatitis chronica atrophicans Herxheimer can often mimic a peripheral vascular disorder. Acta Med. Scand. 220:485488.
51. Fahrer, H.,, S. M. van der Linden,, M. J. Sauvain,, L. Gern,, E. Zhioua, and, A. Aeschlimann. 1991. The prevalence and incidence of clinical and asymptomatic Lyme borreliosis in a population at risk. J. Infect. Dis. 163:305310.
52. Fallon, B. A.,, J. G. Keilp,, K. M. Corbera,, E. Petkova,, C. B. Britton,, E. Dwyer,, I. Slavov,, J. Cheng,, J. Dobkin,, D. R. Nelson, and, H. A. Sackeim. 2008. A randomized, placebo-controlled trial of repeated IV antibiotic therapy for Lyme encephalopathy. Neurology 70:9921003.
53. Feder, H. M., Jr.,, M. Abeles,, M. Bernstein,, D. Whitaker-Worth, and, J. M. Grant-Kels. 2006. Diagnosis, treatment, and prognosis of erythema migrans and Lyme arthritis. Clin. Dermatol. 24:509520.
54. Feder, H. M., Jr.,, B. J. Johnson,, S. O’Connell,, E. D. Shapiro,, A. C. Steere, and, G. P. Wormser. 2007. A critical appraisal of “chronic Lyme disease.” N. Engl. J. Med. 357:14221430.
55. Foley, D. M.,, R. J. Gayek,, J. T. Skare,, E. A. Wagar,, C. I. Champion,, D. R. Blanco,, M. A. Lovett, and, J. N. Miller. 1995. Rabbit model of Lyme borreliosis: erythema migrans, infection-derived immunity, and identification of Borrelia burgdorferi proteins associated with virulence and protective immunity. J. Clin. Investig. 96:965975.
56. Franz, J. K.,, and A. Krause. 2003. Lyme disease (Lyme borreliosis). Best Pract. Res. Clin. Rheumatol. 17:241264.
57. Fraser, C. M.,, S. Casjens,, W. M. Huang,, G. G. Sutton,, R. Clayton,, R. Lathigra,, O. White,, K. A. Ketchum,, R. Dodson,, E. K. Hickey,, M. Gwinn,, B. Dougherty,, J. F. Tomb,, R. D. Fleischmann,, D. Richardson,, J. Peterson,, A. R. Kerlavage,, J. Quackenbush,, S. Salzberg,, M. Hanson,, R. van Vugt,, N. Palmer,, M. D. Adams,, J. Gocayne,, J. Weidman,, T. Utterback,, L. Watthey,, L. McDonald,, P. Artiach,, C. Bowman,, S. Garland,, C. Fuji,, M. D. Cotton,, K. Horst,, K. Roberts,, B. Hatch,, H. O. Smith, and, J. C. Venter. 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580586.
58. Gasser, R.,, J. Dusleag,, E. Reisinger,, R. Stauber,, B. Feigl,, S. Pongratz,, W. Klein,, C. Furian, and, K. Pierer. 1992. Reversal by ceftriaxone of dilated cardiomyopathy Borrelia burgdorferi infection. Lancet 339:11741175.
59. Gerber, M. A.,, E. D. Shapiro,, G. S. Burke,, V. J. Parcells,, G. L. Bell, et al. 1996. Lyme disease in children in southeastern Connecticut.. N. Engl. J. Med. 335:12701274.
60. Gerber, M. A.,, L. S. Zemel, and, E. D. Shapiro. 1998. Lyme arthritis in children: clinical epidemiology and long-term outcomes. Pediatrics 102:905908.
61. Gilmore, R. D., Jr.,, R. R. Howison,, V. L. Schmit,, A. J. Nowalk,, D. R. Clifton,, C. Nolder,, J. L. Hughes, and, J. A. Carroll. 2007. Temporal expression analysis of the Borrelia burgdorferi paralogous gene family 54 genes BBA64, BBA65, and BBA66 during persistent infection in mice. Infect. Immun. 75:27532764.
62. Gross, D. M.,, T. Forsthuber,, M. Tary-Lehmann,, C. Etling,, K. Ito,, Z. A. Nagy,, J. A. Field,, A. C. Steere, and, B. T. Huber. 1998. Identification of LFA-1 as a candidate autoantigen in treatment-resistant Lyme arthritis. Science 281:703706.
63. Gross, D. M.,, A. C. Steere, and, B. T. Huber. 1998. T helper 1 response is dominant and localized to the synovial fluid in patients with Lyme arthritis. J. Immunol 160:10221028.
64. Guo, B. P.,, S. J. Norris,, L. C. Rosenberg, and, M. Hook. 1995. Adherence of Borrelia burgdorferi to the proteoglycan decorin. Infect. Immun. 63:34673472.
65. Haddad, F. A.,, and R. B. Nadelman. 2003. Lyme disease and the heart. Front. Biosci. 8:s769s782.
66. Hajjar, R. J.,, and R. L. Kradin. 2002. 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. 346:17321738.
67. Halperin, J.,, B. J. Luft,, D. J. Volkman, and, R. J. Dattwyler. 1990. Lyme neuroborreliosis. Peripheral nervous system manifestations. Brain 113:12071221.
68. Halperin, J. J. 1995. Neuroborreliosis. Am. J. Med. 98:52S56S.
69. Halperin, J. J. 2002. Nervous system Lyme disease. Vector Borne Zoonotic Dis. 2:241247.
70. Halperin, J. J. 2008. Prolonged Lyme disease treatment. Neurology 70:986987.
71. Halperin, J. J.,, and M. P. Heyes. 1992. Neuroactive kynurenines in Lyme borreliosis. Neurology 42:4350.
72. Halperin, J. J.,, L. B. Krupp,, M. G. Golightly, and, D. J. Volkman. 1990. Lyme borreliosis-associated encephalopathy. Neurology 40:13401343.
73. Halperin, J. J.,, E. L. Logigian,, M. F. Finkel, and, R. A. Pearl. 1996. Practice parameters for the diagnosis of patients with nervous system Lyme borreliosis (Lyme disease). Quality Standards Subcommittee of the American Academy of Neurology. Neurology 46:619627.
74. Halperin, J. J.,, B. J. Luft,, A. K. Anand,, C. T. Roque,, O. Alvarez,, D. J. Volkman, and, R. J. Dattwyler. 1989. Lyme neuroborreliosis: central nervous system manifestations. Neurology 39:753759.
75. Halperin, J. J.,, D. J. Volkman, and, P. Wu. 1991. Central nervous system abnormalities in Lyme neuroborreliosis. Neurology 41:15711582.
76. Hansen, K.,, and E. Asbrink. 1989. Serodiagnosis of erythema migrans and acrodermatitis chronica atrophicans by the Borrelia burgdorferi flagellum enzyme-linked immunosorbent assay. J. Clin. Microbiol. 27:545551.
77. Hansen, K.,, and A. M. Lebech. 1991. Lyme neuroborreliosis: a new sensitive diagnostic assay for intrathecal synthesis of Borrelia burgdorferi-specific immunoglobulin G, A, and M. Ann. Neurol. 30:197205.
78. Hansen, K.,, and A. M. Lebech. 1992. The clinical and epidemiological profile of Lyme neuroborreliosis in Denmark 1985-1990. A prospective study of 187 patients with Borrelia burgdorferi specific intrathecal antibody production. Brain 115:399423.
79. Hemmer, B.,, B. Gran,, Y. Zhao,, A. Marques,, J. Pascal,, A. Tzou,, T. Kondo,, I. Cortese,, B. Bielekova,, S. E. Straus,, H. F. McFarland,, R. Houghten,, R. Simon,, C. Pinilla, and, R. Martin. 1999. Identification of candidate T-cell epitopes and molecular mimics in chronic Lyme disease. Nat. Med. 5:13751382.
80. Hofhuis, A.,, J. W. van der Giessen,, F. H. Borgsteede,, P. R. Wielinga,, D. W. Notermans, and, W. van Pelt. 2006. Lyme borreliosis in the Netherlands: strong increase in GP consultations and hospital admissions in past 10 years. Euro. Surveill. 11:E060622.
81. Hopf, H. C. 1975. Peripheral neuropathy in acrodermatitis chronica atrophicans (Herxheimer). J. Neurol. Neurosurg. Psychiatry 38:452458.
82. Hovius, J. W.,, A. P. van Dam, and, E. Fikrig. 2007. Tick-host-pathogen interactions in Lyme borreliosis. Trends Parasitol. 23:434438.
83. Hovius, K. E.,, B. Beijer,, S. G. Rijpkema,, N. M. Bleumink-Pluym, and, D. J. Houwers. 1998. Identification of four Borrelia burgdorferi sensu lato species in Ixodes ricinus ticks collected from Dutch dogs. Vet. Q. 20:143145.
84. Hovmark, A.,, E. Asbrink, and, I. Olsson. 1986. Joint and bone involvement in Swedish patients with Ixodes ricinus-borne Borrelia infection. Zentralbl. Bakteriol. Mikrobiol. Hyg. A 263:275284.
85. Hubalek, Z.,, and J. Halouzka. 1997. Distribution of Borrelia burgdorferi sensu lato genomic groups in Europe, a review. Eur. J. Epidemiol. 13:951957.
86. Hunfeld, K. P.,, and V. Brade. 2006. Antimicrobial susceptibility of Borrelia burgdorferi sensu lato: what we know, what we don’t know, and what we need to know. Wien. Klin. Wochenschr. 118:659668.
87. Huppertz, H. I.,, M. Bohme,, S. M. Standaert,, H. Karch, and, S. A. Plotkin. 1999. Incidence of Lyme borreliosis in the Wurzburg region of Germany. Eur. J. Clin. Microbiol. Infect. Dis. 18:697703.
88. Jaulhac, B.,, I. Chary-Valckenaere,, J. Sibilia,, R. M. Javier,, Y. Piemont,, J. L. Kuntz,, H. Monteil, and, J. Pourel. 1996. Detection of Borrelia burgdorferi by DNA amplification in synovial tissue samples from patients with Lyme arthritis. Arthritis Rheum. 39:736745.
89. Johnson, R. C.,, N. Marek, and, C. Kodner. 1984. Infection of Syrian hamsters with Lyme disease spirochetes. J. Clin. Microbiol. 20:10991101.
90. Kaiser, R. 1998. Neuroborreliosis. J. Neurol. 245:247255.
91. Kannian, P.,, E. E. Drouin,, L. Glickstein,, W. W. Kwok,, G. T. Nepom, and, A. C. Steere. 2007. Decline in the frequencies of Borrelia burgdorferi OspA161 175-specific T cells after antibiotic therapy in HLA-DRB1*0401-positive patients with antibiotic-responsive or antibiotic-refractory lyme arthritis. J. Immunol. 179:63366342.
92. Kannian, P.,, G. McHugh,, B. J. Johnson,, R. M. Bacon,, L. J. Glickstein, and, A. C. Steere. 2007. Antibody responses to Borrelia burgdorferi in patients with antibiotic-refractory, antibiotic-responsive, or non-antibiotic-treated Lyme arthritis. Arthritis Rheum. 56:42164225.
93. Kaplan, R. F.,, M. E. Meadows,, L. C. Vincent,, E. L. Logigian, and, A. C. Steere. 1992. Memory impairment and depression in patients with Lyme encephalopathy: comparison with fibromyalgia and nonpsychotically depressed patients. Neurology 42:12631267.
94. Kaplan, R. F.,, R. P. Trevino,, G. M. Johnson,, L. Levy,, R. Dornbush,, L. T. Hu,, J. Evans,, A. Weinstein,, C. H. Schmid, and, M. S. Klempner. 2003. Cognitive function in posttreatment Lyme disease: do additional antibiotics help? Neurology 60:19161922.
95. Karussis, D.,, H. L. Weiner, and, O. Abramsky. 1999. Multiple sclerosis vs Lyme disease: a case presentation to a discussant and a review of the literature. Mult. Scler. 5:395402.
96. Keller, T. L.,, J. J. Halperin, and, M. Whitman. 1992. PCR detection of Borrelia burgdorferi DNA in cerebrospinal fluid of Lyme neuroborreliosis patients. Neurology 42:3242.
97. Kindstrand, E.,, B. Y. Nilsson,, A. Hovmark,, R. Pirskanen, and, E. Asbrink. 1997. Peripheral neuropathy in acrodermatitis chronica atrophicans—a late Borrelia manifestation. Acta Neurol. Scand. 95:338345.
98. Klein, J.,, G. Stanek,, R. Bittner,, R. Horvat,, C. Holzinger, and, D. Glogar. 1991. Lyme borreliosis as a cause of myocarditis and heart muscle disease. Eur. Heart J. 12(Suppl. D):7375.
99. Klempner, M. S. 2002. Controlled trials of antibiotic treatment in patients with post-treatment chronic Lyme disease. Vector Borne Zoonotic Dis. 2:255263.
100. Klempner, M. S.,, L. T. Hu,, J. Evans,, C. H. Schmid,, G. M. Johnson,, R. P. Trevino,, D. Norton,, L. Levy,, D. Wall,, J. McCall,, M. Kosinski, and, A. Weinstein. 2001. Two controlled trials of antibiotic treatment in patients with persistent symptoms and a history of Lyme disease. N. Engl. J. Med. 345:8592.
101. Kornblatt, A. N.,, A. C. Steere, and, D. G. Brownstein. 1984. Experimental Lyme disease in rabbits: spirochetes found in erythema migrans and blood. Infect. Immun. 46:220223.
102. Krupp, L. B.,, L. G. Hyman,, R. Grimson,, P. K. Coyle,, P. Melville,, S. Ahnn,, R. Dattwyler, and, B. Chandler. 2003. Study and treatment of post Lyme disease (STOP-LD): a randomized double masked clinical trial. Neurology 60:19231930.
103. Krupp, L. B.,, D. Masur,, J. Schwartz,, P. K. Coyle,, L. J. Langenbach,, S. K. Fernquist,, L. Jandorf, and, J. J. Halperin. 1991. Cognitive functioning in late Lyme borreliosis. Arch. Neurol. 48:11251129.
104. Kuiper, H.,, A. P. van Dam,, A. W. Moll van Charante,, N. P. Nauta, and, J. Dankert. 1993. One year follow-up study to assess the prevalence and incidence of Lyme borreliosis among Dutch forestry workers. Eur. J. Clin. Microbiol. Infect. Dis. 12:413418.
105. Lardieri, G.,, A. Salvi,, F. Camerini,, M. Cinco, and, G. Trevisan. 1993. Isolation of Borrelia burgdorferi from myocardium. Lancet 342:490.
106. Liang, F. T.,, E. L. Brown,, T. Wang,, R. V. Iozzo, and, E. Fikrig. 2004. Protective niche for Borrelia burgdorferi to evade humoral immunity. Am. J. Pathol. 165:977985.
107. Liang, F. T.,, M. B. Jacobs,, L. C. Bowers, and, M. T. Philipp. 2002. An immune evasion mechanism for spirochetal persistence in Lyme borreliosis. J. Exp. Med. 195:415422.
108. Liang, F. T.,, F. K. Nelson, and, E. Fikrig. 2002. Molecular adaptation of Borrelia burgdorferi in the murine host. J. Exp. Med. 196:275280.
109. Liang, F. T.,, J. M. Nowling, and, M. T. Philipp. 2000. Cryptic and exposed invariable regions of VlsE, the variable surface antigen of Borrelia burgdorferi sl. J. Bacteriol. 182:35973601.
110. Liang, F. T.,, A. C. Steere,, A. R. Marques,, B. J. Johnson,, J. N. Miller, and, M. T. Philipp. 1999. Sensitive and specific serodiagnosis of Lyme disease by enzyme-linked immunosorbent assay with a peptide based on an immunodominant conserved region of Borrelia burgdorferi VlsE. J. Clin. Microbiol. 37:39903996.
111. Livengood, J. A.,, and R. D. Gilmore, Jr. 2006. Invasion of human neuronal and glial cells by an infectious strain of Borrelia burgdorferi. Microbes Infect. 8:28322840.
112. Logigian, E. L.,, R. F. Kaplan, and, A. C. Steere. 1990. Chronic neurologic manifestations of Lyme disease. N. Engl. J. Med. 323:14381444.
113. Logigian, E. L.,, R. F. Kaplan, and, A. C. Steere. 1999. Successful treatment of Lyme encephalopathy with intravenous ceftriaxone. J. Infect. Dis. 180:377383.
114. Logigian, E. L., and A. C. Steere. 1992. Clinical and electrophysiologic findings in chronic neuropathy of Lyme disease. Neurology 42:303311.
115. Malawista, S. E.,, S. W. Barthold, and, D. H. Persing. 1994. Fate of Borrelia burgdorferi DNA in tissues of infected mice after antibiotic treatment. J. Infect. Dis. 170:13121316.
116. Marangoni, A.,, A. Moroni,, S. Accardo, and, R. Cevenini. 2008. Borrelia burgdorferi VlsE antigen for the serological diagnosis of Lyme borreliosis. Eur. J. Clin. Microbiol. Infect. Dis. 27:349354.
117. Marques, A. R.,, F. Stock, and, V. Gill. 2000. Evaluation of a new culture medium for Borrelia burgdorferi. J. Clin. Microbiol. 38:42394241.
118. Matyniak, J. E.,, and S. L. Reiner. 1995. T helper phenotype and genetic susceptibility in experimental Lyme disease. J. Exp. Med. 181:12511254.
119. Mayer, W.,, F. X. Kleber,, B. Wilske,, V. Preac-Mursic,, W. Maciejewski,, H. Sigl,, E. Holzer, and, W. Doering. 1990. Persistent atrioventricular block in Lyme borreliosis. Klin. Wochenschr. 68:431435.
120. McDowell, J. V.,, S. Y. Sung,, L. T. Hu, and, R. T. Marconi. 2002. Evidence that the variable regions of the central domain of VlsE are antigenic during infection with Lyme disease spirochetes. Infect. Immun. 70:41964203.
121. Moody, K. D.,, R. L. Adams, and, S. W. Barthold. 1994. Effectiveness of antimicrobial treatment against Borrelia burgdorferi infection in mice. Antimicrob. Agents Chemother. 38:15671572.
122. Muellegger, R. R.,, E. M. Schluepen,, M. M. Millner,, H. P. Soyer,, M. Volkenandt, and, H. Kerl. 1996. Acrodermatitis chronica atrophicans in an 11-year-old girl. Br. J. Dermatol. 135:609612.
123. Mullegger, R. R. 2004. Dermatological manifestations of Lyme borreliosis. Eur. J. Dermatol. 14:296309.
124. Nadelman, R. B.,, J. Nowakowski,, G. Forseter,, N. S. Goldberg,, S. Bittker,, D. Cooper,, M. Aguero-Rosenfeld, and, G. P. Wormser. 1996. The clinical spectrum of early Lyme borreliosis in patients with culture-confirmed erythema migrans. Am. J. Med. 100:502508.
125. Nadelman, R. B.,, J. Nowakowski,, G. P. Wormser, and, I. Schwartz. 1999. How should viability of Borrelia burgdorferi be demonstrated? Am. J. Med. 106:491492.
126. Nadelman, R. B.,, and G. P. Wormser. 1998. Lyme borreliosis. Lancet 352:557565.
127. Nadelman, R. B.,, and G. P. Wormser. 2007. Reinfection in patients with Lyme disease. Clin. Infect. Dis. 45:10321038.
128. Nocton, J. J.,, F. Dressler,, B. J. Rutledge,, P. N. Rys,, D. H. Persing, and, A. C. Steere. 1994. Detection of Borrelia burgdorferi DNA by polymerase chain reaction in synovial fluid from patients with Lyme arthritis. N. Engl. J. Med. 330:229234.
129. Olsson, I.,, E. Asbrink,, M. von Stedingk, and, L. V. von Stedingk. 1994. Changes in Borrelia burgdorferi-specific serum IgG antibody levels in patients treated for acrodermatitis chronica atrophicans. Acta Derm. Venereol. 74:424428.
130. Oschmann, P.,, W. Dorndorf,, C. Hornig,, C. Schafer,, H. J. Wellensiek, and, K. W. Pflughaupt. 1998. Stages and syndromes of neuroborreliosis. J. Neurol. 245:262272.
131. Pachner, A. R.,, K. Amemiya,, M. Bartlett,, H. Schaefer,, K. Reddy, and, W. F. Zhang. 2001. Lyme borreliosis in rhesus macaques: effects of corticosteroids on spirochetal load and isotype switching of anti-Borrelia burgdorferi antibody. Clin. Diagn. Lab. Immunol. 8:225232.
132. Pachner, A. R.,, S. T. Braswell,, E. Delaney,, K. Amemiya, and, E. Major. 1994. A rabbit model of Lyme neuroborreliosis: characterization by PCR, serology, and sequencing of the OspA gene from the brain. Neurology 44:19381943.
133. Pachner, A. R.,, D. Cadavid,, G. Shu,, D. Dail,, S. Pachner,, E. Hodzic, and, S. W. Barthold. 2001. Central and peripheral nervous system infection, immunity, and inflammation in the NHP model of Lyme borreliosis. Ann. Neurol. 50:330338.
134. Pachner, A. R.,, E. Delaney,, T. O’Neill, and, E. Major. 1995. Inoculation of nonhuman primates with the N40 strain of Borrelia burgdorferi leads to a model of Lyme neuroborreliosis faithful to the human disease. Neurology 45:165172.
135. Pachner, A. R.,, H. Gelderblom, and, D. Cadavid. 2001. The rhesus model of Lyme neuroborreliosis. Immunol. Rev. 183:186204.
136. Pachner, A. R.,, H. Schaefer,, K. Amemiya,, D. Cadavid,, W. F. Zhang,, K. Reddy, and, T. O’Neill. 1998. Pathogenesis of neuroborreliosis—lessons from a monkey model. Wien. Klin. Wochenschr. 110:870873.
137. Pachner, A. R.,, and A. C. Steere. 1984. Neurological findings of Lyme disease. Yale J. Biol. Med. 57:481483.
138. Pachner, A. R.,, and I. Steiner. 2007. Lyme neuroborreliosis: infection, immunity, and inflammation. Lancet Neurol. 6:544552.
139. Pal, U.,, and E. Fikrig. 2003. Adaptation of Borrelia burgdorferi in the vector and vertebrate host. Microbes Infect. 5:659666.
140. Philipp, M. T.,, M. K. Aydintug,, R. P. Bohm, Jr.,, F. B. Cogswell,, V. A. Dennis,, H. N. Lanners,, R. C. Lowrie, Jr.,, E. D. Roberts,, M. D. Conway,, M. Karacorlu,, G. A. Peyman,, D. J. Gubler,, B. J. Johnson,, J. Piesman, and, Y. Gu. 1993. Early and early disseminated phases of Lyme disease in the rhesus monkey: a model for infection in humans. Infect. Immun. 61:30473059.
141. Philipp, M. T.,, L. C. Bowers,, P. T. Fawcett,, M. B. Jacobs,, F. T. Liang,, A. R. Marques,, P. D. Mitchell,, J. E. Purcell,, M. S. Ratterree, and, R. K. Straubinger. 2001. Antibody response to IR6, a conserved immunodominant region of the VlsE lipoprotein, wanes rapidly after antibiotic treatment of Borrelia burgdorferi infection in experimental animals and in humans. J. Infect. Dis. 184:870878.
142. Philipp, M. T.,, G. P. Wormser,, A. R. Marques,, S. Bittker,, D. S. Martin,, J. Nowakowski, and, L. G. Dally. 2005. A decline in C6 antibody titer occurs in successfully treated patients with culture-confirmed early localized or early disseminated Lyme borreliosis. Clin. Diagn. Lab. Immunol. 12:10691074.
143. Phillips, S. E.,, L. H. Mattman,, D. Hulinska, and, H. Moayad. 1998. A proposal for the reliable culture of Borrelia burgdorferi from patients with chronic Lyme disease, even from those previously aggressively treated. Infection 26:364367.
144. Picken, M. M.,, R. N. Picken,, D. Han,, Y. Cheng,, E. Ruzic-Sabljic,, J. Cimperman,, V. Maraspin,, S. Lotric-Furlan, and, F. Strle. 1997. A two year prospective study to compare culture and polymerase chain reaction amplification for the detection and diagnosis of Lyme borreliosis. Mol. Pathol. 50:186193.
145. Piesman, J.,, K. L. Clark,, M. C. Dolan,, C. M. Happ, and, T. R. Burkot. 1999. Geographic survey of vector ticks (Ixodes scapularis and Ixodes pacificus) for infection with the Lyme disease spirochete, Borrelia burgdorferi. J. Vector Ecol. 24:9198.
146. Pinto, D. S. 2002. Cardiac manifestations of Lyme disease. Med. Clin. North Am. 86:285296.
147. Postic, D.,, M. Garnier, and, G. Baranton. 2007. Multilocus sequence analysis of atypical Borrelia burgdorferi sensu lato isolates—description of Borrelia californiensis sp. nov., and genomospecies 1 and 2. Int. J. Med. Microbiol. 297:263271.
148. Priem, S.,, G. R. Burmester,, T. Kamradt,, K. Wolbart,, M. G. Rittig, and, A. Krause. 1998. Detection of Borrelia burgdorferi by polymerase chain reaction in synovial membrane, but not in synovial fluid from patients with persisting Lyme arthritis after antibiotic therapy. Ann. Rheum. Dis. 57:118121.
149. Reid, M. C.,, R. T. Schoen,, J. Evans,, J. C. Rosenberg, and, R. I. Horwitz. 1998. The consequences of overdiagnosis and overtreatment of Lyme disease: an observational study. Ann. Intern. Med. 128:354362.
150. Richter, D.,, D. B. Schlee,, R. Allgower, and, F. R. Matuschka. 2004. Relationships of a novel Lyme disease spirochete, Borrelia spielmani sp. nov., with its hosts in Central Europe. Appl. Environ. Microbiol. 70:64146419.
151. Roberts, E. D.,, R. P. Bohm, Jr.,, F. B. Cogswell,, H. N. Lanners,, R. C. Lowrie, Jr.,, L. Povinelli,, J. Piesman, and, M. T. Philipp. 1995. Chronic lyme disease in the rhesus monkey. Lab. Invest. 72:146160.
152. Roberts, E. D.,, R. P. Bohm, Jr.,, R. C. Lowrie, Jr.,, G. Habicht,, L. Katona,, J. Piesman, and, M. T. Philipp. 1998. Pathogenesis of Lyme neuroborreliosis in the rhesus monkey: the early disseminated and chronic phases of disease in the peripheral nervous system. J. Infect. Dis. 178:722732.
153. Rubin, D. A.,, C. Sorbera,, P. Nikitin,, A. McAllister,, G. P. Wormser, and, R. B. Nadelman. 1992. Prospective evaluation of heart block complicating early Lyme disease. Pacing Clin. Electrophysiol. 15:252255.
154. Schmitz, J. L.,, R. F. Schell,, A. Hejka,, D. M. England, and, L. Konick. 1988. Induction of Lyme arthritis in LSH hamsters. Infect. Immun. 56:23362342.
155. Schwan, T. G.,, J. Piesman,, W. T. Golde,, M. C. Dolan, and, P. A. Rosa. 1995. Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc. Natl. Acad. Sci. USA 92:29092913.
156. Schwartz, I.,, G. P. Wormser,, J. J. Schwartz,, D. Cooper,, P. Weissensee,, A. Gazumyan,, E. Zimmermann,, N. S. Goldberg,, S. Bittker,, G. L. Campbell, and, C. S. Pavia. 1992. Diagnosis of early Lyme disease by polymerase chain reaction amplification and culture of skin biopsies from erythema migrans lesions. J. Clin. Microbiol. 30:30823088.
157. Seltzer, E. G.,, M. A. Gerber,, M. L. Cartter,, K. Freudigman, and, E. D. Shapiro. 2000. Long-term outcomes of persons with Lyme disease. JAMA 283:609616.
158. Shapiro, E. D. 2002. Long-term outcomes of persons with Lyme disease. Vector Borne Zoonotic Dis. 2:279281.
159. Shin, J. J.,, L. J. Glickstein, and, A. C. Steere. 2007. High levels of inflammatory chemokines and cytokines in joint fluid and synovial tissue throughout the course of antibiotic-refractory lyme arthritis. Arthritis Rheum. 56:13251335.
160. Sigal, L. H. 1990. Summary of the first 100 patients seen at a Lyme disease referral center. Am. J. Med. 88:577581.
161. Skoldenberg, B.,, G. Stiernstedt,, M. Karlsson,, B. Wretlind, and, B. Svenungsson. 1988. Treatment of Lyme borreliosis with emphasis on neurological disease. Ann. N. Y. Acad. Sci. 539:317323.
162. Stanek, G.,, J. Klein,, R. Bittner, and, D. Glogar. 1990. Isolation of Borrelia burgdorferi from the myocardium of a patient with longstanding cardiomyopathy. N. Engl. J. Med. 322:249252.
163. Stanek, G.,, J. Klein,, R. Bittner, and, D. Glogar. 1991. Borrelia burgdorferi as an etiologic agent in chronic heart failure? Scand. J. Infect. Dis. Suppl 77:8587.
164. Steere, A. C. 1989. Lyme disease. N. Engl. J. Med. 321:586596.
165. Steere, A. C. 2001. Lyme disease. N. Engl. J. Med. 345:115125.
166. Steere, A. C. 2003. Duration of antibiotic therapy for Lyme disease. Ann. Intern. Med. 138:761762.
167. Steere, A. C. 2006. Lyme borreliosis in 2005, 30 years after initial observations in Lyme Connecticut. Wien. Klin. Wochenschr. 118:625633.
168. Steere, A. C.,, and S. M. Angelis. 2006. Therapy for Lyme arthritis: strategies for the treatment of antibiotic-refractory arthritis. Arthritis Rheum. 54:30793086.
169. Steere, A. C.,, W. P. Batsford,, M. Weinberg,, J. Alexander,, H. J. Berger,, S. Wolfson, and, S. E. Malawista. 1980. Lyme carditis: cardiac abnormalities of Lyme disease. Ann. Intern. Med. 93:816.
170. Steere, A. C.,, V. P. Berardi,, K. E. Weeks,, E. L. Logigian, and, R. Ackermann. 1990. Evaluation of the intrathecal antibody response to Borrelia burgdorferi as a diagnostic test for Lyme neuroborreliosis. J. Infect. Dis. 161:12031209.
171. Steere, A. C.,, J. Coburn, and, L. Glickstein. 2004. The emergence of Lyme disease. J. Clin. Investig. 113:10931101.
172. Steere, A. C.,, R. L. Grodzicki,, A. N. Kornblatt,, J. E. Craft,, A. G. Barbour,, W. Burgdorfer,, G. P. Schmid,, E. Johnson, and, S. E. Malawista. 1983. The spirochetal etiology of Lyme disease. N. Engl. J. Med. 308:733740.
173. Steere, A. C.,, R. E. Levin,, P. J. Molloy,, R. A. Kalish,, J. H. Abraham III,, N. Y. Liu, and, C. H. Schmid. 1994. Treatment of Lyme arthritis. Arthritis Rheum. 37:878888.
174. Steere, A. C.,, S. E. Malawista,, D. R. Snydman,, R. E. Shope,, W. A. Andiman,, M. R. Ross, and, F. M. Steele. 1977. Lyme arthritis: an epidemic of oligoarticular arthritis in children and adults in three Connecticut communities. Arthritis Rheum. 20:717.
175. Steere, A. C.,, R. T. Schoen, and, E. Taylor. 1987. The clinical evolution of Lyme arthritis. Ann. Intern. Med. 107:725731.
176. Steere, A. C.,, V. K. Sikand,, R. T. Schoen, and, J. Nowakowski. 2003. Asymptomatic infection with Borrelia burgdorferi. Clin. Infect. Dis. 37:528532.
177. Steere, A. C.,, E. Taylor,, G. L. McHugh, and, E. L. Logigian. 1993. The overdiagnosis of Lyme disease. JAMA 269:18121816.
178. Steere, A. C.,, E. Taylor,, M. L. Wilson,, J. F. Levine, and, A. Spielman. 1986. Longitudinal assessment of the clinical and epidemiological features of Lyme disease in a defined population. J. Infect. Dis. 154:295300.
179. Stiernstedt, G.,, R. Gustafsson,, M. Karlsson,, B. Svenungsson, and, B. Skoldenberg. 1988. Clinical manifestations and diagnosis of neuroborreliosis. Ann. N. Y. Acad. Sci. 539:4655.
180. Straubinger, R. K. 2000. PCR-based quantification of Borrelia burgdorferi organisms in canine tissues over a 500-day postinfection period. J. Clin. Microbiol. 38:21912199.
181. Straubinger, R. K.,, A. F. Straubinger,, L. Harter,, R. H. Jacobson,, Y. F. Chang,, B. A. Summers,, H. N. Erb, and, M. J. Appel. 1997. Borrelia burgdorferi migrates into joint capsules and causes an up-regulation of interleukin-8 in synovial membranes of dogs experimentally infected with ticks. Infect. Immun. 65:12731285.
182. Straubinger, R. K.,, A. F. Straubinger,, B. A. Summers, and, R. H. Jacobson. 2000. Status of Borrelia burgdorferi infection after antibiotic treatment and the effects of corticosteroids: an experimental study. J. Infect. Dis. 181:10691081.
183. Straubinger, R. K.,, B. A. Summers,, Y. F. Chang, and, M. J. Appel. 1997. Persistence of Borrelia burgdorferi in experimentally infected dogs after antibiotic treatment. J. Clin. Microbiol. 35:111116.
184. Strle, F.,, R. B. Nadelman,, J. Cimperman,, J. Nowakowski,, R. N. Picken,, I. Schwartz,, V. Maraspin,, M. E. Aguero-Rosenfeld,, S. Varde,, S. Lotric-Furlan, and, G. P. Wormser. 1999. 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. 130:3236.
185. Strle, F.,, J. A. Nelson,, E. Ruzic-Sabljic,, J. Cimperman,, V. Maraspin,, S. Lotric-Furlan,, Y. Cheng,, M. M. Picken,, G. M. Trenholme, and, R. N. Picken. 1996. European Lyme borreliosis: 231 culture-confirmed cases involving patients with erythema migrans. Clin. Infect. Dis. 23:6165.
186. Strle, F.,, R. N. Picken,, Y. Cheng,, J. Cimperman,, V. Maraspin,, S. Lotric-Furlan,, E. Ruzic-Sabljic, and, M. M. Picken. 1997. Clinical findings for patients with Lyme borreliosis caused by Borrelia burgdorferi sensu lato with genotypic and phenotypic similarities to strain 25015. Clin. Infect. Dis. 25:273280.
187. Strle, F.,, E. Ruzic-Sabljic,, J. Cimperman,, S. Lotric-Furlan, and, V. Maraspin. 2006. Comparison of findings for patients with Borrelia garinii and Borrelia afzelii isolated from cerebrospinal fluid. Clin. Infect. Dis. 43:704710.
188. Tilton, R. C.,, D. Barden, and, M. Sand. 2001. Culture of Borrelia burgdorferi. J. Clin. Microbiol. 39:2747.
189. Tonks, A. 2007. Lyme wars. BMJ 335:910912.
190. van Dam, A. P. 2002. Diversity of Ixodes-borne Borrelia species—clinical, pathogenetic, and diagnostic implications and impact on vaccine development. Vector Borne Zoonotic Dis. 2:249254.
191. van Dam, A. P.,, H. Kuiper,, K. Vos,, A. Widjojokusumo,, B. M. de Jongh,, L. Spanjaard,, A. C. Ramselaar,, M. D. Kramer, and, J. Dankert. 1993. Different genospecies of Borrelia burgdorferi are associated with distinct clinical manifestations of Lyme borreliosis. Clin. Infect. Dis. 17:708717.
192. van der Linde, M. R. 1991. Lyme carditis: clinical characteristics of 105 cases. Scand. J. Infect. Dis. Suppl. 77:8184.
193. Vos, K.,, A. P. van Dam,, H. Kuiper,, H. Bruins,, L. Spanjaard, and, J. Dankert. 1994. Seroconversion for Lyme borreliosis among Dutch military. Scand. J. Infect. Dis. 26:427434.
194. Wang, G.,, A. P. van Dam, and, J. Dankert. 1999. Phenotypic and genetic characterization of a novel Borrelia burgdorferi sensu lato isolate from a patient with Lyme borreliosis. J. Clin. Microbiol. 37:30253028.
195. Wang, G.,, A. P. van Dam, and, J. Dankert. 2001. Analysis of a VMP-like sequence (vls) locus in Borrelia garinii and Vls homologues among four Borrelia burgdorferi sensu lato species. FEMS Microbiol. Lett. 199:3945.
196. Wang, G.,, A. P. van Dam,, A. Le Fleche,, D. Postic,, O. Peter,, G. Baranton,, R. de Boer,, L. Spanjaard, and, J. Dankert. 1997. Genetic and phenotypic analysis of Borrelia valaisiana sp. nov. (Borrelia genomic groups VS116 and M19). Int. J. Syst. Bacteriol. 47:926932.
197. Wang, G.,, A. P. van Dam,, I. Schwartz, and, J. Dankert. 1999. Molecular typing of Borrelia burgdorferi sensu lato: taxonomic, epidemiological, and clinical implications. Clin. Microbiol. Rev. 12:633653.
198. Weis, J. J. 2002. Host-pathogen interactions and the pathogenesis of murine Lyme disease. Curr. Opin. Rheumatol. 14:399403.
199. Wilske, B. 2002. Microbiological diagnosis in Lyme borreliosis. Int. J. Med. Microbiol. 291(Suppl 33):114119.
200. Wilske, B.,, V. Fingerle, and, U. Schulte-Spechtel. 2007. Microbiological and serological diagnosis of Lyme borreliosis. FEMS Immunol. Med. Microbiol. 49:1321.
201. Wormser, G. P.,, S. W. Barthold,, E. D. Shapiro,, R. J. Dattwyler,, J. S. Bakken,, A. C. Steere,, L. K. Bockenstedt, and, J. D. Radolf. 2007. Anti-tumor necrosis factor-alpha activation of Borrelia burgdorferi spirochetes in antibiotic-treated murine Lyme borreliosis: an unproven conclusion. J. Infect. Dis. 196:18651866.
202. Wormser, G. P.,, R. J. Dattwyler,, E. D. Shapiro,, J. J. Halperin,, A. C. Steere,, M. S. Klempner,, P. J. Krause,, J. S. Bakken,, F. Strle,, G. Stanek,, L. Bockenstedt,, D. Fish,, J. S. Dumler, and, R. B. Nadelman. 2006. The clinical assessment, treatment, and prevention of lyme disease, human granulocytic anaplasmosis, and babesiosis: clinical practice guidelines by the Infectious Diseases Society of America. Clin. Infect. Dis. 43:10891134.
203. Wormser, G. P.,, R. Ramanathan,, J. Nowakowski,, D. McKenna,, D. Holmgren,, P. Visintainer,, R. Dornbush,, B. Singh, and, R. B. Nadelman. 2003. Duration of antibiotic therapy for early Lyme disease. A randomized, double-blind, placebo-controlled trial. Ann. Intern. Med. 138:697704.
204. Yrjanainen, H.,, J. Hytonen,, X. Y. Song,, J. Oksi,, K. Hartiala, and, M. K. Viljanen. 2007. Anti-tumor necrosis factor-alpha treatment activates Borrelia burgdorferi spirochetes 4 weeks after ceftriaxone treatment in C3H/He mice. J. Infect. Dis. 195:14891496.
205. Zeidner, N. S.,, M. S. Nuncio,, B. S. Schneider,, L. Gern,, J. Piesman,, O. Brandao, and, A. R. Filipe. 2001. A Portuguese isolate of Borrelia lusitaniae induces disease in C3H/HeN mice. J. Med. Microbiol. 50:10551060.
206. Zhang, J. R.,, J. M. Hardham,, A. G. Barbour, and, S. J. Norris. 1997. Antigenic variation in Lyme disease borreliae by promiscuous recombination of VMP-like sequence cassettes. Cell 89:275285.
207. Zhang, J. R.,, and S. J. Norris. 1998. Genetic variation of the Borrelia burgdorferi gene vlsE involves cassette-specific, segmental gene conversion. Infect. Immun. 66:36983704.

Tables

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Table 1.

The different sensu lato species in the United States, Asia, and Europe

Citation: Hovius J, van Dam A, Fikrig E. 2009. Late Manifestations of Lyme Borreliosis, p 9-25. In Fratamico P, Smith J, Brogden K (ed), Sequelae and Long-Term Consequences of Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555815486.ch2
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Table 2.

Predominant clinical manifestations of human Lyme borreliosis in the United States and Europe

Citation: Hovius J, van Dam A, Fikrig E. 2009. Late Manifestations of Lyme Borreliosis, p 9-25. In Fratamico P, Smith J, Brogden K (ed), Sequelae and Long-Term Consequences of Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555815486.ch2

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