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Published in: Journal of Neurology 8/2019

Open Access 01-08-2019 | Magnetic Resonance Imaging | Original Communication

Neuronal loss or dysfunction in patients with early Lyme neuroborreliosis: a proton magnetic resonance spectroscopy study of the brain

Authors: Adam Garkowski, Bożena Kubas, Marcin Hładuński, Joanna Zajkowska, Olga Zajkowska, Dorota Jurgilewicz, Radosław Zawadzki, Ewa Garkowska, Sławomir Pancewicz, Urszula Łebkowska

Published in: Journal of Neurology | Issue 8/2019

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Abstract

Background

We hypothesized that since Borrelia burgdorferi causes systemic inflammation and infects the brain, it may lead to alterations in cerebral metabolism, as measured by 1H-magnetic resonance spectroscopy (1H-MRS). The purpose of our study was to determine whether 1H-MRS could detect brain metabolite alterations in patients with early Lyme neuroborreliosis (LNB) in normal-appearing brain tissue on the conventional magnetic resonance imaging (MRI).

Methods

Twenty-six patients diagnosed with early LNB and twenty-six healthy volunteers as a control group have been involved in the study. All of them underwent routine MRI protocol using 3.0-T MRI scanner. 1H-MRS examinations were performed with repetition time (TR) = 2000 ms, and echo time (TE) = 135 ms. Single voxels were positioned in the anterior and posterior parts of the right and left frontal lobes.

Results

We found a statistically significant decrease of the N-acetylaspartate/creatine ratio within the anterior part of the right and left frontal lobes (p ≤ 0.001 and p = 0.001 respectively) and in the posterior part of the right and left frontal lobes (p ≤ 0.001 and 0.031) in the patients with LNB.

Conclusion

A significant reduction in NAA/Cr ratio in comparison with the controls suggests the presence of diffuse neuronal loss in patients with early LNB.
Literature
1.
go back to reference Rizzoli A, Hauffe H, Carpi G, Vourc HG, Neteler M, Rosa R (2011) Lyme borreliosis in Europe. Euro Surveill 16:1–8 Rizzoli A, Hauffe H, Carpi G, Vourc HG, Neteler M, Rosa R (2011) Lyme borreliosis in Europe. Euro Surveill 16:1–8
2.
go back to reference Koedel U, Fingerle V, Pfister HW (2015) Lyme neuroborreliosis—epidemiology, diagnosis and management. Nat Rev Neurol 11:446–456CrossRefPubMed Koedel U, Fingerle V, Pfister HW (2015) Lyme neuroborreliosis—epidemiology, diagnosis and management. Nat Rev Neurol 11:446–456CrossRefPubMed
3.
go back to reference Garkowski A, Zajkowska J, Zajkowska A, Kułakowska A, Zajkowska O, Kubas B, Jurgilewicz D, Hładuński M, Łebkowska U (2017) Cerebrovascular manifestations of lyme neuroborreliosis—a systematic review of published cases. Front Neurol 8:146CrossRefPubMedPubMedCentral Garkowski A, Zajkowska J, Zajkowska A, Kułakowska A, Zajkowska O, Kubas B, Jurgilewicz D, Hładuński M, Łebkowska U (2017) Cerebrovascular manifestations of lyme neuroborreliosis—a systematic review of published cases. Front Neurol 8:146CrossRefPubMedPubMedCentral
4.
go back to reference Bertrand E, Szpak GM, Piłkowska E, Habib N, Lipczyńska-Lojkowska W, Rudnicka A, Tylewska-Wierzbanowska S, Kulczycki J (1999) Central nervous system infection caused by Borrelia burgdorferi. Clinico-pathological correlation of three post-mortem cases. Folia Neuropathol 37:43–51PubMed Bertrand E, Szpak GM, Piłkowska E, Habib N, Lipczyńska-Lojkowska W, Rudnicka A, Tylewska-Wierzbanowska S, Kulczycki J (1999) Central nervous system infection caused by Borrelia burgdorferi. Clinico-pathological correlation of three post-mortem cases. Folia Neuropathol 37:43–51PubMed
5.
go back to reference Kuntzer T, Bogousslavsky J, Miklossy J, Steck AJ, Janzer R, Regli F (1991) Borrelia rhombencephalomyelopathy. Arch Neurol 48:832–836CrossRefPubMed Kuntzer T, Bogousslavsky J, Miklossy J, Steck AJ, Janzer R, Regli F (1991) Borrelia rhombencephalomyelopathy. Arch Neurol 48:832–836CrossRefPubMed
6.
go back to reference Ramesh G, Didier PJ, England JD, Santana-Gould L, Doyle-Meyers LA, Martin DS, Jacobs MB, Philipp MT (2015) Inflammation in the pathogenesis of lyme neuroborreliosis. Am J Pathol 185:1344–1360CrossRefPubMedPubMedCentral Ramesh G, Didier PJ, England JD, Santana-Gould L, Doyle-Meyers LA, Martin DS, Jacobs MB, Philipp MT (2015) Inflammation in the pathogenesis of lyme neuroborreliosis. Am J Pathol 185:1344–1360CrossRefPubMedPubMedCentral
8.
go back to reference Hildenbrand P, Craven DE, Jones R, Nemeskal P (2009) Lyme neuroborreliosis: manifestations of a rapidly emerging zoonosis. AJNR Am J Neuroradiol 30:1079–1087CrossRefPubMed Hildenbrand P, Craven DE, Jones R, Nemeskal P (2009) Lyme neuroborreliosis: manifestations of a rapidly emerging zoonosis. AJNR Am J Neuroradiol 30:1079–1087CrossRefPubMed
9.
go back to reference Oz G, Alger JR, Barker PB, Bartha R, Bizzi A, Boesch C et al (2014) Clinical proton MR spectroscopy in central nervous system disorders. Radiology 270:658–679CrossRefPubMedPubMedCentral Oz G, Alger JR, Barker PB, Bartha R, Bizzi A, Boesch C et al (2014) Clinical proton MR spectroscopy in central nervous system disorders. Radiology 270:658–679CrossRefPubMedPubMedCentral
10.
go back to reference Mygland A, Ljøstad U, Fingerle V, Rupprecht T, Schmutzhard E, Steiner I, European Federation of Neurological Societies (2010) EFNS guidelines on the diagnosis and management of European Lyme neuroborreliosis. Eur J Neurol 17(8–16):e1–4 Mygland A, Ljøstad U, Fingerle V, Rupprecht T, Schmutzhard E, Steiner I, European Federation of Neurological Societies (2010) EFNS guidelines on the diagnosis and management of European Lyme neuroborreliosis. Eur J Neurol 17(8–16):e1–4
11.
go back to reference Newberg A, Hassan A, Alavi A (2002) Cerebral metabolic changes associated with Lyme disease. Nucl Med Commun 23:773–777CrossRefPubMed Newberg A, Hassan A, Alavi A (2002) Cerebral metabolic changes associated with Lyme disease. Nucl Med Commun 23:773–777CrossRefPubMed
12.
go back to reference Donta ST, Noto RB, Vento JA (2012) SPECT brain imaging in chronic Lyme disease. Clin Nucl Med 37:e219–e222CrossRefPubMed Donta ST, Noto RB, Vento JA (2012) SPECT brain imaging in chronic Lyme disease. Clin Nucl Med 37:e219–e222CrossRefPubMed
13.
go back to reference Provencher SW (1993) Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med 30:672–679CrossRef Provencher SW (1993) Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med 30:672–679CrossRef
14.
go back to reference Rupprecht TA, Koedel U, Fingerle V, Pfister HW (2008) The pathogenesis of lyme neuroborreliosis: from infection to inflammation. Mol Med 14:205–212CrossRefPubMed Rupprecht TA, Koedel U, Fingerle V, Pfister HW (2008) The pathogenesis of lyme neuroborreliosis: from infection to inflammation. Mol Med 14:205–212CrossRefPubMed
15.
go back to reference Fallon BA, Levin ES, Schweitzer PJ, Hardesty D (2010) Inflammation and central nervous system Lyme disease. Neurobiol Dis 37:534–541CrossRefPubMed Fallon BA, Levin ES, Schweitzer PJ, Hardesty D (2010) Inflammation and central nervous system Lyme disease. Neurobiol Dis 37:534–541CrossRefPubMed
16.
go back to reference Ramesh G, Borda JT, Dufour J, Kaushal D, Ramamoorthy R, Lackner AA, Philipp MT (2008) Interaction of the Lyme disease spirochete Borrelia burgdorferi with brain parenchyma elicits inflammatory mediators from glial cells as well as glial and neuronal apoptosis. Am J Pathol 173:1415–1427CrossRefPubMedPubMedCentral Ramesh G, Borda JT, Dufour J, Kaushal D, Ramamoorthy R, Lackner AA, Philipp MT (2008) Interaction of the Lyme disease spirochete Borrelia burgdorferi with brain parenchyma elicits inflammatory mediators from glial cells as well as glial and neuronal apoptosis. Am J Pathol 173:1415–1427CrossRefPubMedPubMedCentral
17.
go back to reference Kondrusik M, Swierzbińska R, Pancewicz S, Zajkowska J, Grygorczuk S, Hermanowska-Szpakowicz T (2004) Evaluation of proinflammatory cytokine (TNF-alpha, IL-1beta, IL-6, IFN-gamma) concentrations in serum and cerebrospinal fluid of patients with neuroborreliosis. Neurol Neurochir Pol 38:265–270PubMed Kondrusik M, Swierzbińska R, Pancewicz S, Zajkowska J, Grygorczuk S, Hermanowska-Szpakowicz T (2004) Evaluation of proinflammatory cytokine (TNF-alpha, IL-1beta, IL-6, IFN-gamma) concentrations in serum and cerebrospinal fluid of patients with neuroborreliosis. Neurol Neurochir Pol 38:265–270PubMed
18.
go back to reference Davie CA, Hawkins CP, Barker GJ, Brennan A, Tofts PS, Miller DH, McDonald WI (1994) Serial proton magnetic resonance spectroscopy in acute multiple sclerosis lesions. Brain 117:49–58CrossRefPubMed Davie CA, Hawkins CP, Barker GJ, Brennan A, Tofts PS, Miller DH, McDonald WI (1994) Serial proton magnetic resonance spectroscopy in acute multiple sclerosis lesions. Brain 117:49–58CrossRefPubMed
19.
go back to reference Appenzeller S, Li LM, Costallat LT, Cendes F (2005) Evidence of reversible axonal dysfunction in systemic lupus erythematosus: a proton MRS study. Brain 128:2933–2940CrossRefPubMed Appenzeller S, Li LM, Costallat LT, Cendes F (2005) Evidence of reversible axonal dysfunction in systemic lupus erythematosus: a proton MRS study. Brain 128:2933–2940CrossRefPubMed
20.
go back to reference Emmer BJ, van der Bijl AE, Huizinga TW, Breedveld FC, Steens SC, Th Bosma GP, van Buchem MA, van der Grond J (2009) Brain involvement in rheumatoid arthritis: a magnetic resonance spectroscopy study. Arthritis Rheum 60:3190–3195CrossRefPubMed Emmer BJ, van der Bijl AE, Huizinga TW, Breedveld FC, Steens SC, Th Bosma GP, van Buchem MA, van der Grond J (2009) Brain involvement in rheumatoid arthritis: a magnetic resonance spectroscopy study. Arthritis Rheum 60:3190–3195CrossRefPubMed
21.
go back to reference Tyrakowska-Dadełło Z, Kułakowska A, Zajkowska J, Pancewicz S, Tarasów E (2017) Herpes simplex encephalitis—diagnostic imaging. Prog Health Sci 9:152–160 Tyrakowska-Dadełło Z, Kułakowska A, Zajkowska J, Pancewicz S, Tarasów E (2017) Herpes simplex encephalitis—diagnostic imaging. Prog Health Sci 9:152–160
22.
go back to reference Bairwa D, Kumar V, Vyas S, Das BK, Srivastava AK, Pandey RM, Sharma SK, Jagannathan NR, Sinha S (2016) Case control study: magnetic resonance spectroscopy of brain in HIV infected patients. BMC Neurol 16:99CrossRefPubMedPubMedCentral Bairwa D, Kumar V, Vyas S, Das BK, Srivastava AK, Pandey RM, Sharma SK, Jagannathan NR, Sinha S (2016) Case control study: magnetic resonance spectroscopy of brain in HIV infected patients. BMC Neurol 16:99CrossRefPubMedPubMedCentral
23.
go back to reference Weissenborn K, Krause J, Bokemeyer M, Hecker H, Schüler A, Ennen JC, Ahl B, Manns MP, Böker KW (2004) Hepatitis C virus infection affects the brain-evidence from psychometric studies and magnetic resonance spectroscopy. J Hepatol 41:845–851CrossRefPubMed Weissenborn K, Krause J, Bokemeyer M, Hecker H, Schüler A, Ennen JC, Ahl B, Manns MP, Böker KW (2004) Hepatitis C virus infection affects the brain-evidence from psychometric studies and magnetic resonance spectroscopy. J Hepatol 41:845–851CrossRefPubMed
24.
go back to reference Bladowska J, Zimny A, Knysz B, Małyszczak K, Kołtowska A, Szewczyk P, Gąsiorowski J, Furdal M, Sąsiadek MJ (2013) Evaluation of early cerebral metabolic, perfusion and microstructural changes in HCV-positive patients: a pilot study. J Hepatol 59:651–657CrossRefPubMed Bladowska J, Zimny A, Knysz B, Małyszczak K, Kołtowska A, Szewczyk P, Gąsiorowski J, Furdal M, Sąsiadek MJ (2013) Evaluation of early cerebral metabolic, perfusion and microstructural changes in HCV-positive patients: a pilot study. J Hepatol 59:651–657CrossRefPubMed
25.
go back to reference Ustymowicz A, Tarasów E, Zajkowska J, Walecki J, Hermanowska-Szpakowicz T (2004) Proton MR spectroscopy in neuroborreliosis: a preliminary study. Neuroradiology 46:26–30CrossRefPubMed Ustymowicz A, Tarasów E, Zajkowska J, Walecki J, Hermanowska-Szpakowicz T (2004) Proton MR spectroscopy in neuroborreliosis: a preliminary study. Neuroradiology 46:26–30CrossRefPubMed
26.
go back to reference Barker PB, Lin DDM (2006) In vivo proton MR spectroscopy of the human brain. Prog Nucl Magn Reson Spectrosc 49:99–128CrossRef Barker PB, Lin DDM (2006) In vivo proton MR spectroscopy of the human brain. Prog Nucl Magn Reson Spectrosc 49:99–128CrossRef
Metadata
Title
Neuronal loss or dysfunction in patients with early Lyme neuroborreliosis: a proton magnetic resonance spectroscopy study of the brain
Authors
Adam Garkowski
Bożena Kubas
Marcin Hładuński
Joanna Zajkowska
Olga Zajkowska
Dorota Jurgilewicz
Radosław Zawadzki
Ewa Garkowska
Sławomir Pancewicz
Urszula Łebkowska
Publication date
01-08-2019
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 8/2019
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-019-09359-0

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