Lyme borreliosis: Clinical case definitions for diagnosis and management in Europe

Clinical Microbiology and Infection

Volumn 17, Issue 1, 2011, Pages 69-79

  Stanek, G ^a   Fingerle, V ^b   Hunfeld, K P ^c   Jaulhac, B ^d   Kaiser, R ^e   Krause, A ^f   Kristoferitsch, W ^g   O'Connell, S ^h   Ornstein, K ⁱ   Strle, F ^j   Gray, J ^k  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b Bavarian Health and Food Safety Authority   (Germany)

^c UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^d UNIVERSITY HOSPITAL OF STRASBOURG   (France)

^e Klinikum Pforzheim GmbH   (Germany)

^f MARTIN LUTHER KRANKENHAUS   (Germany)

^g DANUBE HOSPITAL   (Austria)

^h SOUTHAMPTON GENERAL HOSPITAL   (United Kingdom)

ⁱ LUND UNIVERSITY   (Sweden)

^j UNIVERSITY MEDICAL CENTRE LJUBLJANA   (Slovenia)

^k UNIVERSITY COLLEGE DUBLIN   (Ireland)

more..

Author keywords

Borrelia; Case definitions; Diagnosis; Europe; Lyme borreliosis

Indexed keywords

ANTIBIOTIC AGENT; BACTERIAL DNA; CROSS REACTING ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY;

ACRODERMATITIS CHRONICA ATROPHICANS; ANKYLOSING SPONDYLITIS; ANTIBIOTIC THERAPY; ANTIBODY BLOOD LEVEL; ARTICLE; ATRIOVENTRICULAR CONDUCTION; AUTOIMMUNE DISEASE; BACTERIAL ARTHRITIS; BACTERIUM CULTURE; BORRELIA BURGDORFERI; BORRELIAL LYMPHOCYTOMA; BRADYCARDIA; BRAIN VASCULITIS; CEREBROSPINAL FLUID ANALYSIS; CONGENITAL INFECTION; CONGESTIVE CARDIOMYOPATHY; CONJUNCTIVITIS; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST; DIFFERENTIAL DIAGNOSIS; EARLY INTERVENTION; ENCEPHALOMYELITIS; ENTHESITIS; EPIDEMIOLOGICAL DATA; EPISCLERITIS; ERYTHEMA CHRONICUM MIGRANS; ERYTHROCYTE SEDIMENTATION RATE; EUROPE; FACIAL NERVE PARALYSIS; FALSE NEGATIVE RESULT; FALSE POSITIVE RESULT; HEADACHE; HEART BUNDLE BRANCH BLOCK; HEART MUSCLE CONDUCTION DISTURBANCE; HEART PALPITATION; HUMAN; INFECTION COMPLICATION; KERATITIS; LABORATORY DIAGNOSIS; LYME DISEASE; LYMPHOCYTE TRANSFORMATION TEST; LYMPHOCYTOMA; MUSCULOSKELETAL DISEASE; MYELITIS; NEURASTHENIA; NEUROLOGIC DISEASE; PAPILLITIS; PERSISTENT INFECTION; POLYMERASE CHAIN REACTION; POST LYME SYNDROME; PRIORITY JOURNAL; RADICULOMYELITIS; SACROILIITIS; SENSITIVITY AND SPECIFICITY; SEROCONVERSION; SKIN BIOPSY; T LYMPHOCYTE SUBPOPULATION; TICK BITE; UVEITIS; VISUAL CONTRAST SENSITIVITY TEST;

BORRELIA; BORRELIA BURGDORFERI; IXODIDA; SPIROCHAETES;

EID: 78650085775     PISSN: 1198743X     EISSN: 14690691     Source Type: Journal    
DOI: 10.1111/j.1469-0691.2010.03175.x     Document Type: Article

References (98)

1. Wormser GP, Dattwyler RJ, Shapiro ED et al. 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 2006; 43: 1089-1134. (IV)
2. Steere AC, Malawista SE, Snydman DR et al. Lyme arthritis: an epidemic of oligoarticular arthritis in children and adults in three Connecticut communities. Arthritis Rheum 1977; 20: 7-17. (II)
3. Burgdorfer W, Barbour AG, Hayes SF, Benach JL, Grunwaldt E, Davis JP. Lyme disease-a tick-borne spirochetosis? Science 1982; 216: 1317-1319. (II)
4. Johnson RC, Schmid GP, Hyde FW, Steigerwalt AG, Brenner DJ. Borrelia burgdorferi sp. nov.: etiologic agent of Lyme disease. Int J Syst Bacteriol 1984; 34: 496-497. (II)
5. Steere AC, Malawista SE, Hardin JA, Ruddy S, Askenase W, Andiman WA. Erythema chronicum migrans and Lyme arthritis. The enlarging clinical spectrum. Ann Intern Med 1977; 86: 685-698. (IV)
6. Stanek S, Strle F, Gray JS, Wormser G. History and characteristics of Lyme borreliosis. In: Gray JS, Kahl O, Lane RS, Stanek G, eds, Lyme Borreliosis: Biology, Epidemiology and Control. Wallingford, Oxon, UK: CAB International, 2002; 1-28. (IV)
7. Stanek G, Strle F. Lyme borreliosis. Lancet 2003; 362: 1639-1647. (IV)
8. Stanek G, Strle F. Lyme borreliosis - European perspective. Infect Dis Clin North Am 2008; 22: 327-339. (IV)
9. Strle F, Nadelman RB, Cimperman J et al. 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 1999; 130: 32-36. (II)
10. Strle F, Stanek G. Clinical manifestations and diagnosis of Lyme borreliosis. Curr Probl Dermatol 2009; 37: 51-110. (IV)
11. Lindgren E, Jaenson TG. Lyme borreliosis in Europe: influences of climate and climate change, epidemiology, ecology and adaptation measures, WHO Regional Office for Europe 2006: ISBN: 9289022914 (IV)
12. URL 1990. Lyme Disease (Borrelia burgdorferi) 1990 Case Definition. (IV)
13. URL 2008. Lyme Disease (Borrelia burgdorferi) 2008 Case Definition. (IV)
14. Stanek G, O'Connell S, Cimmino M et al. European Union Concerted Action on Risk Assessment in Lyme Borreliosis: clinical case definitions for Lyme borreliosis. Wien Klin Wochenschr 1996; 108: 741-747. (IV)
15. Vanousová D, Hercogová J. Lyme borreliosis treatment. Dermatol Ther 2008; 21: 101-109. (IV)
16. Fülöp B, Poggensee G. Epidemiological situation of Lyme borreliosis in Germany: surveillance data from six Eastern German States, 2002 to 2006. Parasitol Res 2008; 103 (Suppl 1): 117-120. (II)
17. Hofhuis A, van der Giessen JW, Borgsteede FH, Wielinga PR, Notermans DW, van Pelt W. Lyme borreliosis in the Netherlands: strong increase in GP consultations and hospital admissions in past 10 years. Euro Surveill 2006; 11: E060629. 5. (II)
18. Smith R, O'Connell S, Palmer S. Lyme disease surveillance in England and Wales, 1986-1998. Emerg Infect Dis 2000; 6: 404-407. (II)
19. Anonymous. Epidemiological report on communicable diseases in Slovenia. Ljubljana: Ministry of Health of the Republic of Slovenia, Institute of Public Health of the Republic of Slovenia, 2008; 62-65. (II)
20. Kish MA. Guide to development of practice guidelines. Clin Infect Dis 2001; 32: 851-854. (IV)
21. Strle F, Nelson JA, Ružić-Sabljić E et al. European Lyme borreliosis: 231 culture-confirmed cases involving patients with erythema migrans. Clin Infect Dis 1996; 23: 61-65. (II)
22. Strle F, Videcnik J, Zorman P, Cimperman J, Lotric-Furlan S, Maraspin V. Clinical and epidemiological findings for patients with erythema migrans. Comparison of cohorts from the years 1993 and 2000. Wien Klin Wochenschr 2002; 114: 493-497. (II)
23. Maraspin V, Lotric-Furlan S, Cimperman J, Ružić-Sabljić E, Strle F. Erythema migrans in the immunocompromised host. Wien Klin Wochenschr 1999; 111: 923-932. (II)
24. Fürst B, Glatz M, Kerl H, Müllegger RR. The impact of immunosuppression on erythema migrans. A retrospective study of clinical presentation, response to treatment and production of borrelia antibodies in 33 patients. Clin Exp Dermatol 2006; 31: 509-514. (II)
25. Cetin E, Sotoudeh M, Auer H, Stanek G. Paradigm Burgenland: risk of Borrelia burgdorferi sensu lato infection indicated by variable seroprevalence rates in hunters. Wien Klin Wochenschr 2006; 118: 677-681. (II)
26. Bennet R, Lindgren V, Zweygberg WB. Borrelia antibodies in children evaluated for Lyme neuroborreliosis. Infection 2008; 36: 463-466. (II)
27. Glatz M, Golestani M, Kerl H, Müllegger RR. Clinical relevance of different IgG and IgM serum antibody responses to Borrelia burgdorferi after antibiotic therapy for erythema migrans: long-term follow-up study of 113 patients. Arch Dermatol 2006; 142: 862-868. (II)
28. Strle F, Pleterski-Rigler D, Stanek G, Pejovnik-Pustinek A, Ruzic E, Cimperman J. Solitary borrelial lymphocytoma: report of 36 cases. Infection 1992; 20: 201-206. (II)
29. Maraspin V, Cimperman J, Lotric-Furlan S et al. Solitary borrelial lymphocytoma in adult patients. Wien Klin Wochenschr 2002; 31: 515-523. (II)
30. Asbrink E, Hovmark A. Early and late cutaneous manifestations in Ixodes-borne borreliosis. Ann NY Acad Sci 1988; 539: 4-15. (IV)
31. Müllegger RR, Glatz M. Skin manifestations of Lyme borreliosis: diagnosis and management. Am J Clin Dermatol 2008; 9: 355-368. (IV)
32. Brehmer-Andersson E, Hovmark A, Asbrink E. Acrodermatitis chronica atrophicans: histopathologic findings and clinical correlations in 111 cases. Acta Derm Venereol 1998; 78: 207-213. (III)
33. Kristoferitsch W, Sluga E, Graf M et al. Neuropathy associated with acrodermatitis chronica atrophicans. Clinical and morphological features. Ann N Y Acad Sci 1988; 539: 35-45. (III)
34. Kindstrand E, Nilsson BY, Hovmark A et al. Polyneuropathy in late Lyme neuroborreliosis - a clinical, neurophysiological and morphological description. Acta Neurol Scand 2000; 101: 47-52. (III)
35. Christen HJ, Hanefeld F, Eiffert H, Thomssen R. Epidemiology and clinical manifestations of Lyme borreliosis in childhood. A prospective multicentre study with special regard to neuroborreliosis. Acta Paediatr 1993; 386 (suppl): 1-75. (II)
36. Hansen K, Lebech AM. Lyme neuroborreliosis: a new sensitive diagnostic assay for intrathecal synthesis of Borrelia burgdorferi-specific immunoglobulin G, A, and M. Ann Neurol 1991; 30: 197-205. (II)
37. Krüger H, Reuss K, Pulz M, Pflughaupt KW, Martin R, Mertens HG. Meningoradiculitis and encephalomyelitis due to Borrelia burgdorferi: a follow-up study of 72 patients over 27 years. J Neurol 1989; 236: 322-328. (III)
38. Mygland A, Skarpaas T, Ljostad U. Chronic polyneuropathy and Lyme disease. Eur J Neurol 2006; 13: 1213-1215. (II)
39. Ackermann R, Rehse-Kupper B, Gollmer E, Schmidt R. Chronic neurologic manifestations of erythema migrans borreliosis. Ann N Y Acad Sci 1988; 539: 16-23. (III)
40. Hansen K, Lebech AM. 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 1992; 115: 399-423. (II)
41. Pourel J. [Clinical diagnosis of Lyme borreliosis in case of joint and muscular presentations] French. Med Mal Infect 2007; 37: 523-531. (IV)
42. Franz JK, Krause A. Lyme disease (Lyme borreliosis). Best Pract Res Clin Rheumatol 2003; 17: 241-264. (IV)
43. Lelovas P, Dontas I, Bassiakou E, Xanthos T. Cardiac implications of Lyme disease, diagnosis and therapeutic approach. Int J Cardiol 2008; 129: 15-21. (IV)
44. Steere AC, Batsford WP, Weinberg M et al. Lyme carditis: cardiac abnormalities of Lyme disease. Ann Intern Med 1980; 93: 8-16. (II)
45. van der Linde MR. Lyme carditis: clinical characteristics of 105 cases. Scand J Infect Dis 1991; 77 (Suppl): 81-84. (III)
46. Stanek G, Klein J, Bittner R, Glogar D. Isolation of Borrelia burgdorferi from the myocardium of a patient with longstanding cardiomyopathy. N Engl J Med 1990; 322: 249-252. (III)
47. Balcer LJ, Winterkorn JM, Galetta SL. Neuro-ophthalmic manifestations of Lyme disease. J Neuroophthalmol 1997; 17: 108-121. (IV)
48. Zagórski Z, Biziorek B, Haszcz D. Ophthalmic manifestations in Lyme borreliosis [Polish]. Przegl Epidemiol 2002; 56 (Suppl 1): 85-90. (IV)
49. Mikkilä HO, Seppälä IJ, Viljanen MK, Peltomaa MP, Karma A. The expanding clinical spectrum of ocular Lyme borreliosis. Ophthalmology 2000; 107: 581-587. (III)
50. Hickie I, Davenport T, Wakefield D et al. Post-infective and chronic fatigue syndromes precipitated by viral and non-viral pathogens: prospective cohort study. BMJ 2006; 333: 575-581. (II)
51. Lipsker D, Antoni-Bach N, Hansmann Y, Jaulhac B. Long term prognosis of patients treated for erythema migrans in France. Br J Dermatol 2002; 146: 872-876. (II)
52. Kaiser R. Clinical courses of acute and chronic neuroborreliosis following treatment with ceftriaxone [German]. Nervenarzt 2004; 75: 553-557. (II)
53. Steere AC, Angelis SM. Therapy for Lyme arthritis: strategies for the treatment of antibiotic-refractory arthritis. Arthritis Rheum 2006; 54: 3079-3086. (IV)
54. Bujak DI, Weinstein A, Dornbush RL. Clinical and neurocognitive features of the post Lyme syndrome. J Rheumatol 1996; 23: 1392-1397. (II)
55. Krupp LB, Hyman LG, Grimson R et al. Study and treatment of post Lyme disease (STOP-LD): a randomized double masked clinical trial. Neurology 2003; 60: 1923-1930. (I)
56. Kaplan RF, Trevino RP, Johnson GM et al. Cognitive function in post-treatment Lyme disease: do additional antibiotics help? Neurology 2003; 60: 1916-1922. (I)
57. Klempner MS, Hu LT, Evans J et al. Two controlled trials of antibiotic treatment in patients with persistent symptoms and a history of Lyme disease. New Eng J Med 2001; 345: 85-92. (I)
58. Seidel MF, Domene AB, Vetter H. Differential diagnoses of suspected Lyme borreliosis or post-Lyme-disease syndrome. Eur J Clin Microbiol Infect Dis 2007; 26: 611-617. (II)
59. Fallon BA, Keilp JG, Corbera KM et al. A randomized, placebo-controlled trial of repeated IV antibiotic therapy for Lyme encephalopathy. Neurology 2008; 70: 992-1003. (I)
60. Marques A. Chronic Lyme disease: a review. Infect Dis Clin North Am 2008; 22: 341-360. vii-viii. (IV)
61. Feder HM Jr, Johnson BJ, O'Connell S et al. A critical appraisal of "chronic" Lyme disease. N Engl J Med 2007; 357: 1422-1430. (IV)
62. Markowitz LE, Steere AC, Benach JL, Slade JD, Broome CV. Lyme disease during pregnancy. JAMA 1986; 255: 3394-3396. (II)
63. Strobino BA, Williams CL, Abid S, Chalson R, Spierling P. Lyme disease and pregnancy outcome: a prospective study of two thousand prenatal patients. Am J Obstet Gynecol 1993; 169: 367-374. (II)
64. Maraspin V, Cimperman J, Lotric-Furlan S, Pleterski-Rigler D, Strle F. Erythema migrans in pregnancy. Wien Klin Wochenschr 1999; 111: 933-940. (II)
65. Strobino B, Abid S, Gewitz M. Maternal Lyme disease and congenital heart disease: A case-control study in an endemic area. Am J Obstet Gynecol 1999; 180: 711-716. (II)
66. Hunfeld K-P, Oschmann P, Kaiser R, Schulze J, Brade V. Diagnostics. In: Oschmann P, Kraiczy P, Halperin J, Brade V, eds, Lyme-Borreliosis and Tick-Borne Encephalitis, 1st revised English edition. Bremen, Germany: Unimed Verlag AG, International Medical Publishers, 1999; 80-108.
67. Priem S, Klimberg T, Franz J et al. Comparison of reculture and PCR for the detection of Borrelia burgdorferi in cell and tissue cultures after antibiotic treatment. Arthritis Rheum 2001; 44: S1766. (II)
68. Ornstein K, Berglund J, Nilsson I, Norrby R, Bergström S. Characterization of Lyme borreliosis isolates from patients with erythema migrans and neuroborreliosis in southern Sweden. J Clin Microbiol 2001; 39: 1294-1298. (II)
69. Aguero-Rosenfeld ME. Lyme disease: laboratory issues. Infect Dis Clin North Am 2008; 22: 301-313. (IV).
70. Strle F, Ruzic-Sabljic E, Cimperman J et al. Comparison of findings for patients with Borrelia garinii and Borrelia afzelii isolated from cerebrospinal fluid. Clin Infect Dis 2006; 43: 704-710. (II)
71. Wilske B, Fingerle V, Schulte-Spechtel U. Microbiological and serological diagnosis of Lyme borreliosis. FEMS Immunol Med Microbiol 2007; 49: 13-21. (IV)
72. Wilske B. Diagnosis of Lyme borreliosis in Europe. Vector Borne Zoonotic Dis 2003; 3: 215-227. (IV)
73. Brouqui P, Bacellar F, Baranton G et al. Guidelines for the diagnosis of tick-borne bacterial diseases in Europe. Clin Microbiol Infect 2004; 10: 1108-1132. (IV)
74. Aguero-Rosenfeld ME, Wang G, Schwartz I, Wormser GP. Diagnosis of Lyme borreliosis. Clin Microbiol Rev 2005; 18: 484-509. (IV)
75. Lebech AM, Hansen K, Brandrup F, Clemmensen O, Halkier-Sørensen L. Diagnostic value of PCR for detection of Borrelia burgdorferi DNA in clinical specimens from patients with erythema migrans and Lyme neuroborreliosis. Mol Diagn 2000; 5: 139-150. (II)
76. Steere AC, McHugh G, Damle N, Sikand VK. Prospective study of serologic tests for Lyme disease. Clin Infect Dis 2008; 47: 188-195. (II)
77. Kalish RA, McHugh G, Granquist J, Shea B, Ruthazer R, Steere AC. Persistence of immunoglobulin M or immunoglobulin G antibody responses to Borrelia burgdorferi 10-20 years after active Lyme disease. Clin Infect Dis 2001; 33: 780-785. (II)
78. Müllegger RR, Glatz M. Is serological follow-up useful for patients with cutaneous Lyme borreliosis? Curr Probl Dermatol 2009; 37: 178-182. (IV)
79. Evison J, Aebi C, Francioli P et al. Lyme disease part I: epidemiology and diagnosis. Rev Med Suisse 2006; 2: 919-924. (IV)
80. URL 2007. Société de Pathologie Infectieuse de Langue Française (SPILF). Lyme borreliosis: diagnosis, treatment and prevention. 16th consensus conference on anti-infective therapy.
81. Hunfeld KP, Kraiczy P. When to order a western blot and how to interpret it. Curr Probl Dermatol, Basel Karger 2009; 37: 169-179. (IV)
82. Goettner G, Schulte-Spechtel U, Hillermann R, Liegl G, Wilske B, Fingerle V. Improvement of Lyme borreliosis serodiagnosis by a newly developed recombinant immunoglobulin G (IgG) and IgM line immunoblot assay and addition of VlsE and DbpA homologues. J Clin Microbiol 2005; 43: 3602-3609. (II)
83. Sillanpää H, Lahdenne P, Sarvas H et al. Immune responses to borrelial VlsE IR6 peptide variants. Int J Med Microbiol 2007; 297: 45-52. (II)
84. Seltzer EG, Shapiro ED. Misdiagnosis of Lyme disease: when not to order serologic tests. Pediatr Infect Dis J 1996; 15: 762-763. (IV)
85. Gordis L. Assessing the validity and reliability of diagnostic and screening tests. In: Gordis L, ed, Epidemiology, 2nd edn. Philadelphia, London, New York: WB Saunders, 2000; 63-80. (IV)
86. Rothman KL, Greenland S, eds. Modern Epidemiology, 2nd edn. Philadelphia, PA: Lippincott-Raven, 1998. (IV)
87. Hunfeld KP, Stanek G, Straube E et al. V. Quality of Lyme disease serology. Lessons from the German Proficiency Testing Program 1999-2001. A preliminary report. Wien Klin Wochenschr 2002; 31: 591-600. (II)
88. Oschmann P, Kaiser R. Clinical Symptoms. In: Oschmann P, Kraiczy P, Halperin J, Brade V, eds, Lyme-Borreliosis and Tick-Borne Encephalitis. Germany: Unimed Verlag AG, International Medical Publishers Bremen, 1999; 52-75. (IV)
89. Issakainen J, Gnehm HE, Lucchini GM, Zbinden R.J. Value of clinical symptoms, intrathecal specific antibody production and PCR in CSF in the diagnosis of childhood Lyme neuroborreliosis. Klin Paediatr 1996; 208: 106-109. (II)
90. Berger TG, Schoerner C, Schell H et al. Two unusual cases of diffuse acrodermatitis chronica atrophicans seronegative for Lyme borreliosis. Eur J Clin Microbiol Infect Dis 2003; 22: 392-395. (III)
91. Holl-Wieden A, Suerbaum S, Girschick HJ. Seronegative Lyme arthritis. Rheumatol Int 2007; 27: 1091-1093. (III)
92. Cerar T, Ruzic-Sabljic E, Glinsek U. Comparison of PCR methods and culture for the detection of Borrelia spp. in patients with erythema migrans. Clin Microbiol Infect 2008; 14: 653-658. (II)
93. Cerar T, Ogrinc K, Cimperman J, Lotric-Furlan S, Strle F, Ruzić-Sabljić E. Validation of cultivation and PCR methods for diagnosis of Lyme neuroborreliosis. J Clin Microbiol 2008; 46: 3375-3379. (II)
94. Jaulhac B, Chary-Valckenaere I, Sibilia J et al. Detection of Borrelia burgdorferi by DNA amplification in synovial tissue samples from patients with Lyme arthritis. Arthritis Rheum 1996; 39: 736-745. (III)
95. Priem S, Rittig MG, Kamradt T, Burmester GR, Krause A. An optimized PCR leads to rapid and highly sensitive detection of Borrelia burgdorferi in patients with Lyme borreliosis. J Clin Microbiol 1997; 35: 685-690. (II)
96. Ornstein K, Berglund J, Bergstrom S, Norrby R, Barbour A. Three major Lyme Borrelia genospecies (Borrelia burgdorferi sensu stricto, B. afzelii and B. garinii) identified by PCR in cerebrospinal fluid from patients with neuroborreliosis in Sweden. Scand J Inf Dis 2002; 34: 341-346. (II)
97. Rauter C, Mueller M, Diterich I et al. Critical evaluation of urine-based PCR assay for diagnosis of Lyme borreliosis. Clin Diagn Lab Immunol 2005; 12: 910-917. (II)
98. Marques A, Brown MR, Fleisher TA. Natural killer cell counts are not different between patients with post-Lyme disease syndrome and controls. Clin Vaccine Immunol 2009; 16: 1249-1250. (II).