Advertisement
Review Article| Volume 35, ISSUE 4, P779-795, December 2015

Nervous System Lyme Disease

  • John J. Halperin
    Correspondence
    Department of Neurosciences, Overlook Medical Center, 99 Beauvoir Avenue, Summit, NJ 07902.
    Affiliations
    Department of Neurosciences, Overlook Medical Center, 99 Beauvoir Avenue, Summit, NJ 07902, USA

    Sidney Kimmel Medical College of Thomas Jefferson University, 132 South, 10th street, Philadelphia, PA 19107, USA
    Search for articles by this author
Published:September 17, 2015DOI:https://doi.org/10.1016/j.cll.2015.07.002

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribers receive full online access to your subscription and archive of back issues up to and including 2002.

      Content published before 2002 is available via pay-per-view purchase only.

      Subscribe:

      Subscribe to Clinics in Laboratory Medicine
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

      1. Marist.Poll. Alzheimer’s most feared disease. 2012. Available at: http://maristpoll.marist.edu/1114-alzheimers-most-feared-disease/. Accessed August 31, 2013.

        • Halperin J.J.
        Lyme disease – neurology, neurobiology and behavior.
        Clin Infect Dis. 2014; 58: 1267-1272
        • Pachner A.R.
        Neurologic manifestations of Lyme disease, the new “great imitator”.
        Rev Infect Dis. 1989; 6: S1482-S1486
        • Logigian E.L.
        • Kaplan R.F.
        • Steere A.C.
        Successful treatment of Lyme encephalopathy with intravenous ceftriaxone.
        J Infect Dis. 1999; 180: 377-383
      2. Washington, DC: U.S. Department of Defense, Office of the Assistant Secretary of Defense (Public Affairs); 2002.

        • Margos G.
        • Wilske B.
        • Sing A.
        • et al.
        Borrelia bavariensis sp. nov. is widely distributed in Europe and Asia.
        Int J Syst Evol Microbiol. 2013; 63: 4284-4288
        • Halperin J.J.
        • Krupp L.B.
        • Golightly M.G.
        • et al.
        Lyme borreliosis-associated encephalopathy.
        Neurology. 1990; 40: 1340-1343
        • Krupp L.B.
        • Masur D.
        • Schwartz J.
        • et al.
        Cognitive functioning in late Lyme borreliosis.
        Arch Neurol. 1991; 48: 1125-1129
        • Nadelman R.B.
        • Herman E.
        • Wormser G.P.
        Screening for Lyme disease in hospitalized psychiatric patients: prospective serosurvey in an endemic area.
        Mt Sinai J Med. 1997; 64: 409-412
        • Hassett A.L.
        • Radvanski D.C.
        • Buyske S.
        • et al.
        Psychiatric comorbidity and other psychological factors in patients with “chronic Lyme disease”.
        Am J Med. 2009; 122: 843-850
        • Lantos P.M.
        Chronic Lyme disease: the controversies and the science.
        Expert Rev Anti Infect Ther. 2011; 9: 787-797
        • Wormser G.P.
        • Dattwyler R.J.
        • Shapiro E.D.
        • 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
        • Garin C.
        • Bujadoux A.
        Paralysie par les tiques.
        J Med Lyon. 1922; 71: 765-767
        • Bannwarth A.
        Chronische lymphocytare meningitis, entzundliche polyneuritis und “rheumatismus”.
        Arch Psychiatr Nervenkr. 1941; 113: 284-376
        • Karlsson M.
        • Hovind H.K.
        • Svenungsson B.
        • et al.
        Cultivation and characterization of spirochetes from cerebrospinal fluid of patients with Lyme borreliosis.
        J Clin Microbiol. 1990; 28: 473-479
        • Avery R.A.
        • Frank G.
        • Eppes S.C.
        Diagnostic utility of Borrelia burgdorferi cerebrospinal fluid polymerase chain reaction in children with Lyme meningitis.
        Pediatr Infect Dis J. 2005; 24: 705-708
        • Roberts E.D.
        • Bohm Jr., R.P.
        • Lowrie Jr., R.C.
        • et al.
        Pathogenesis of Lyme neuroborreliosis in the rhesus monkey: the early disseminated and chronic phases of disease in the peripheral nervous system.
        J Infect Dis. 1998; 178: 722-732
        • Ogrinc K.
        • Lotric-Furlan S.
        • Maraspin V.
        • et al.
        Suspected early Lyme neuroborreliosis in patients with erythema migrans.
        Clin Infect Dis. 2013; 57: 501-509
        • Cerar T.
        • Ogrinc K.
        • Cimperman J.
        • et al.
        Validation of cultivation and PCR methods for diagnosis of Lyme neuroborreliosis.
        J Clin Microbiol. 2008; 46: 3375-3379
        • Meier C.
        • Grahmann F.
        • Engelhardt A.
        • et al.
        Peripheral nerve disorders in Lyme-Borreliosis. Nerve biopsy studies from eight cases.
        Acta Neuropathol (Berl). 1989; 79: 271-278
        • Vallat J.M.
        • Hugon J.
        • Lubeau M.
        • et al.
        Tick-bite meningoradiculoneuritis: clinical, electrophysiologic, and histologic findings in 10 cases.
        Neurology. 1987; 37: 749-753
        • Halperin J.J.
        • Little B.W.
        • Coyle P.K.
        • et al.
        Lyme disease - a treatable cause of peripheral neuropathy.
        Neurology. 1987; 37: 1700-1706
        • Aberer E.
        • Brunner C.
        • Suchanek G.
        • et al.
        Molecular mimicry and Lyme borreliosis: a shared antigenic determinant between Borrelia burgdorferi and human tissue.
        Ann Neurol. 1989; 26: 732-737
        • Sigal L.H.
        Molecular mimicry and Lyme borreliosis.
        Ann Neurol. 1990; 28 ([letter]): 195-196
        • Martin R.
        • Gran B.
        • Zhao Y.
        • et al.
        Molecular mimicry and antigen-specific T cell responses in multiple sclerosis and chronic CNS Lyme disease.
        J Autoimmun. 2001; 16: 187-192
        • Garcia-Monco J.C.
        • Seidman R.J.
        • Benach J.L.
        Experimental immunization with Borrelia burgdorferi induces development of antibodies to gangliosides.
        Infect Immun. 1995; 63: 4130-4137
        • Garcia Monco J.C.
        • Wheeler C.M.
        • Benach J.L.
        • et al.
        Reactivity of neuroborreliosis patients (Lyme disease) to cardiolipin and gangliosides.
        J Neurol Sci. 1993; 117: 206-214
        • Luft B.J.
        • Steinman C.R.
        • Neimark H.C.
        • et al.
        Invasion of the central nervous system by Borrelia burgdorferi in acute disseminated infection.
        JAMA. 1992; 267: 1364-1367
        • Ljostad U.
        • Mygland A.
        CSF B–lymphocyte chemoattractant (CXCL13) in the early diagnosis of acute Lyme neuroborreliosis.
        J Neurol. 2008; 255: 732-737
        • Rupprecht T.A.
        • Plate A.
        • Adam M.
        • et al.
        The chemokine CXCL13 is a key regulator of B cell recruitment to the cerebrospinal fluid in acute Lyme neuroborreliosis.
        J Neuroinflammation. 2009; 6: 42
        • Halperin J.J.
        • Pacheco-Quinto J.
        • Herdt A.
        • et al.
        [S37.007] serum and CSF cytokines in patients with active CNS Lyme disease, other inflammatory CNS diseases, encephalopathy following treated Lyme disease, other encephalopathies, and normal controls.
        Am Acad Neurol. 2015; (Washington, DC)
        • Hammers Berggren S.
        • Hansen K.
        • Lebech A.M.
        • et al.
        Borrelia burgdorferi-specific intrathecal antibody production in neuroborreliosis: a follow-up study.
        Neurology. 1993; 43: 169-175
        • Halperin J.J.
        • Heyes M.P.
        Neuroactive kynurenines in Lyme borreliosis.
        Neurology. 1992; 42: 43-50
        • Strle K.
        • Stupica D.
        • Drouin E.E.
        • et al.
        Elevated levels of IL-23 in a subset of patients with post-Lyme disease symptoms following erythema migrans.
        Clin Infect Dis. 2014; 58: 372-380
        • Soloski M.J.
        • Crowder L.A.
        • Lahey L.J.
        • et al.
        Serum inflammatory mediators as markers of human Lyme disease activity.
        PLoS One. 2014; 9: e93243
        • Schriefer M.E.
        Lyme Disease Diagnosis: Serology.
        Clin Lab Med. 2015; (in press)
        • Alby K.
        • Capraro G.A.
        Alternatives to Serologic Testing for Diagnosis of Lyme Disease.
        Clin Lab Med. 2015; (in press)
        • Halperin J.J.
        • Luft B.J.
        • Volkman D.J.
        • et al.
        Lyme neuroborreliosis - peripheral nervous system manifestations.
        Brain. 1990; 113: 1207-1221
        • Henriksson A.
        • Link H.
        • Cruz M.
        • et al.
        Immunoglobulin abnormalities in cerebrospinal fluid and blood over the course of lymphocytic meningoradiculitis (Bannwarth's syndrome).
        Ann Neurol. 1986; 20: 337-345
        • Stiernstedt G.T.
        • Granstrom M.
        • Hederstedt B.
        • et al.
        Diagnosis of spirochetal meningitis by enzyme linked immunosorbent assay and indirect immunofluorescence assay in serum and cerebrospinal fluid.
        J Clin Microbiol. 1985; 21: 819-825
      3. Hansen K, Lebech A-M. Intrathecal synthesis of Borrelia burgdorferi specific immunoglobulin G, A and M in neuroborreliosis - an antibody capture assay. Paper presented at: IV International Conference on Lyme Borreliosis 1990. Stockholm, Sweden, June 18–21, 1990.

        • Halperin J.J.
        • Luft B.J.
        • Anand A.K.
        • et al.
        Lyme neuroborreliosis: central nervous system manifestations.
        Neurology. 1989; 39: 753-759
        • Steere A.C.
        • Berardi V.P.
        • Weeks K.E.
        • et al.
        Evaluation of the intrathecal antibody response to Borrelia burgdorferi as a diagnostic test for Lyme neuroborreliosis.
        J Infect Dis. 1990; 161: 1203-1209
        • Mygland A.
        • Ljostad U.
        • Fingerle V.
        • et al.
        EFNS guidelines on the diagnosis and management of European Lyme neuroborreliosis.
        Eur J Neurol. 2010; 17 (e11–14): 8-16
        • Halperin J.J.
        • Volkman D.J.
        • Wu P.
        Central nervous system abnormalities in Lyme neuroborreliosis.
        Neurology. 1991; 41: 1571-1582
        • Logigian E.L.
        • Kaplan R.F.
        • Steere A.C.
        Chronic neurologic manifestations of Lyme disease.
        N Engl J Med. 1990; 323: 1438-1444
        • Sanders L.
        Think like a doctor: mirror, mirror solved.
        New York Times. 2014; 2014
        • Bacon R.M.
        • Kugeler K.J.
        • Mead P.S.
        Surveillance for Lyme disease — United States, 1992–2006.
        MMWR Morb Mortal Wkly Rep. 2008; 57: 1-9
        • England J.D.
        • Bohm R.P.
        • Roberts E.D.
        • et al.
        Mononeuropathy multiplex in rhesus monkeys with chronic Lyme disease.
        Ann Neurol. 1997; 41: 375-384
        • Hopf H.C.
        Peripheral neuropathy in acrodermatitis chronica atrophicans (Herxheimer).
        J Neurol Neurosurg Psychiatry. 1975; 38: 452-458
        • Logigian E.L.
        • Steere A.C.
        Clinical and electrophysiologic findings in chronic neuropathy of Lyme disease.
        Neurology. 1992; 42: 303-311
        • Krishnamurthy K.B.
        • Liu G.T.
        • Logigian E.L.
        Acute Lyme neuropathy presenting with polyradicular pain, abdominal protrusion, and cranial neuropathy.
        Muscle Nerve. 1993; 16: 1261-1264
        • Sibony P.
        • Halperin J.
        • Coyle P.
        • et al.
        Reactive Lyme serology in patients with optic neuritis and papilledema.
        J Neuro Ophthal. 2005; 25: 71-82
        • Blanc F.
        • Ballonzoli L.
        • Marcel C.
        • et al.
        Lyme optic neuritis.
        J Neurol Sci. 2010; 295: 117-119
        • Djukic M.
        • Larsen J.
        • Lingor P.
        • et al.
        Unilateral phrenic nerve lesion in Lyme neuroborreliosis.
        BMC Pulm Med. 2013; 13: 4
        • Nord J.A.
        • Karter D.
        Lyme disease complicated with pseudotumor cerebri.
        Clin Infect Dis. 2003; 37: e25-e26
        • Zemel L.
        Lyme disease and pseudotumor.
        Mayo Clin Proc. 2000; 75: 315
        • Jacobson D.M.
        • Frens D.B.
        Pseudotumor cerebri syndrome associated with Lyme disease.
        Am J Ophthalmol. 1989; 107: 81-82
        • Ackermann R.
        • Rehse K.B.
        • Gollmer E.
        • et al.
        Chronic neurologic manifestations of erythema migrans borreliosis.
        Ann N Y Acad Sci. 1988; 539: 16-23
        • Ackermann R.
        • Gollmer E.
        • Rehse K.B.
        Progressive Borrelia encephalomyelitis. Chronic manifestation of erythema chronicum migrans disease of the nervous system.
        Dtsch Med Wochenschr. 1985; 110: 1039-1042
        • Halperin J.J.
        • Pass H.L.
        • Anand A.K.
        • et al.
        Nervous system abnormalities in Lyme disease.
        Ann N Y Acad Sci. 1988; 539: 24-34
        • Cameron D.J.
        • Johnson L.B.
        • Maloney E.L.
        Evidence assessments and guideline recommendations in Lyme disease: the clinical management of known tick bites, erythema migrans rashes and persistent disease.
        Expert Rev Anti Infect Ther. 2014; 12: 1103-1135
        • Seltzer E.G.
        • Gerber M.A.
        • Cartter M.L.
        • et al.
        Long-term outcomes of persons with Lyme disease.
        JAMA. 2000; 283: 609-616
        • Skogman B.H.
        • Croner S.
        • Odkvist L.
        Acute facial palsy in children–a 2-year follow-up study with focus on Lyme neuroborreliosis.
        Int J Pediatr Otorhinolaryngol. 2003; 67: 597-602
        • Shadick N.A.
        • Phillips C.B.
        • Sangha O.
        • et al.
        Musculoskeletal and neurologic outcomes in patients with previously treated Lyme disease.
        Ann Intern Med. 1999; 131: 919-926
        • Wormser G.P.
        • Weitzner E.
        • McKenna D.
        • et al.
        Long-term assessment of fatigue in patients with culture-confirmed Lyme Disease.
        Am J Med. 2015; 128: 181-184
        • Klempner M.S.
        • Hu L.T.
        • Evans J.
        • et al.
        Two controlled trials of antibiotic treatment in patients with persistent symptoms and a history of Lyme disease.
        N Engl J Med. 2001; 345: 85-92
        • Krupp L.B.
        • Hyman L.G.
        • Grimson R.
        • et al.
        Study and treatment of post Lyme disease (STOP-LD): a randomized double masked clinical trial.
        Neurology. 2003; 60: 1923-1930
        • Fallon B.A.
        • Keilp J.G.
        • Corbera K.M.
        • et al.
        A randomized, placebo-controlled trial of repeated IV antibiotic therapy for Lyme encephalopathy.
        Neurology. 2008; 70: 992-1003
        • Committee on the Diagnostic Criteria for Myalgic Encephalomyelitis/Chronic Fatigue Syndrome
        Beyond myalgic encephalomyelitis/chronic fatigue syndrome: redefining an illness.
        The National Academies Press, Washington, DC2015
        • Luo N.
        • Johnson J.
        • Shaw J.
        • et al.
        Self-reported health status of the general adult U.S. population as assessed by the EQ-5D and Health Utilities Index.
        Med Care. 2005; 43: 1078-1086
        • Telford 3rd, S.R.
        • Wormser G.P.
        Bartonella spp. transmission by ticks not established.
        Emerg Infect Dis. 2010; 16: 379-384
        • Dattwyler R.J.
        • Halperin J.J.
        • Volkman D.J.
        • et al.
        Treatment of late Lyme disease.
        Lancet. 1988; 1: 1191-1193
        • Halperin J.J.
        • Shapiro E.D.
        • Logigian E.L.
        • et al.
        Practice parameter: treatment of nervous system Lyme disease.
        Neurology. 2007; 69: 91-102