{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T02:34:56Z","timestamp":1788230096855,"version":"build-2803163510"},"reference-count":26,"publisher":"Springer Science and Business Media LLC","issue":"8","license":[{"start":{"date-parts":[[2019,5,10]],"date-time":"2019-05-10T00:00:00Z","timestamp":1557446400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100005297","name":"Medical University of Bia\u0142ystok","doi-asserted-by":"crossref","award":["N\/ST\/ZB\/16\/004\/1127"],"award-info":[{"award-number":["N\/ST\/ZB\/16\/004\/1127"]}],"id":[{"id":"10.13039\/501100005297","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["J Neurol"],"published-print":{"date-parts":[[2019,8]]},"DOI":"10.1007\/s00415-019-09359-0","type":"journal-article","created":{"date-parts":[[2019,5,10]],"date-time":"2019-05-10T16:51:25Z","timestamp":1557507085000},"page":"1937-1943","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Neuronal loss or dysfunction in patients with early Lyme neuroborreliosis: a proton magnetic resonance spectroscopy study of the brain"],"prefix":"10.1007","volume":"266","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6526-8276","authenticated-orcid":false,"given":"Adam","family":"Garkowski","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bo\u017cena","family":"Kubas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marcin","family":"H\u0142adu\u0144ski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joanna","family":"Zajkowska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olga","family":"Zajkowska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dorota","family":"Jurgilewicz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rados\u0142aw","family":"Zawadzki","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ewa","family":"Garkowska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S\u0142awomir","family":"Pancewicz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Urszula","family":"\u0141ebkowska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2019,5,10]]},"reference":[{"key":"9359_CR1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.2807\/ese.16.27.19906-en","volume":"16","author":"A Rizzoli","year":"2011","unstructured":"Rizzoli A, Hauffe H, Carpi G, Vourc HG, Neteler M, Rosa R (2011) Lyme borreliosis in Europe. Euro Surveill 16:1\u20138","journal-title":"Euro Surveill"},{"key":"9359_CR2","doi-asserted-by":"publisher","first-page":"446","DOI":"10.1038\/nrneurol.2015.121","volume":"11","author":"U Koedel","year":"2015","unstructured":"Koedel U, Fingerle V, Pfister HW (2015) Lyme neuroborreliosis\u2014epidemiology, diagnosis and management. Nat Rev Neurol 11:446\u2013456","journal-title":"Nat Rev Neurol"},{"key":"9359_CR3","doi-asserted-by":"publisher","first-page":"146","DOI":"10.3389\/fneur.2017.00146","volume":"8","author":"A Garkowski","year":"2017","unstructured":"Garkowski A, Zajkowska J, Zajkowska A, Ku\u0142akowska A, Zajkowska O, Kubas B, Jurgilewicz D, H\u0142adu\u0144ski M, \u0141ebkowska U (2017) Cerebrovascular manifestations of lyme neuroborreliosis\u2014a systematic review of published cases. Front Neurol 8:146","journal-title":"Front Neurol"},{"key":"9359_CR4","first-page":"43","volume":"37","author":"E Bertrand","year":"1999","unstructured":"Bertrand E, Szpak GM, Pi\u0142kowska E, Habib N, Lipczy\u0144ska-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\u201351","journal-title":"Folia Neuropathol"},{"key":"9359_CR5","doi-asserted-by":"publisher","first-page":"832","DOI":"10.1001\/archneur.1991.00530200072021","volume":"48","author":"T Kuntzer","year":"1991","unstructured":"Kuntzer T, Bogousslavsky J, Miklossy J, Steck AJ, Janzer R, Regli F (1991) Borrelia rhombencephalomyelopathy. Arch Neurol 48:832\u2013836","journal-title":"Arch Neurol"},{"key":"9359_CR6","doi-asserted-by":"publisher","first-page":"1344","DOI":"10.1016\/j.ajpath.2015.01.024","volume":"185","author":"G Ramesh","year":"2015","unstructured":"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\u20131360","journal-title":"Am J Pathol"},{"key":"9359_CR7","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1148\/radiol.2531081103","volume":"253","author":"R Agarwal","year":"2009","unstructured":"Agarwal R, Sze G (2009) Neuro-lyme disease: MR imaging findings. Radiology 253:167\u2013173","journal-title":"Radiology"},{"key":"9359_CR8","doi-asserted-by":"publisher","first-page":"1079","DOI":"10.3174\/ajnr.A1579","volume":"30","author":"P Hildenbrand","year":"2009","unstructured":"Hildenbrand P, Craven DE, Jones R, Nemeskal P (2009) Lyme neuroborreliosis: manifestations of a rapidly emerging zoonosis. AJNR Am J Neuroradiol 30:1079\u20131087","journal-title":"AJNR Am J Neuroradiol"},{"key":"9359_CR9","doi-asserted-by":"publisher","first-page":"658","DOI":"10.1148\/radiol.13130531","volume":"270","author":"G Oz","year":"2014","unstructured":"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\u2013679","journal-title":"Radiology"},{"issue":"8\u201316","key":"9359_CR10","first-page":"e1","volume":"17","author":"A Mygland","year":"2010","unstructured":"Mygland A, Lj\u00f8stad 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\u201316):e1\u20134","journal-title":"Eur J Neurol"},{"key":"9359_CR11","doi-asserted-by":"publisher","first-page":"773","DOI":"10.1097\/00006231-200208000-00011","volume":"23","author":"A Newberg","year":"2002","unstructured":"Newberg A, Hassan A, Alavi A (2002) Cerebral metabolic changes associated with Lyme disease. Nucl Med Commun 23:773\u2013777","journal-title":"Nucl Med Commun"},{"key":"9359_CR12","doi-asserted-by":"publisher","first-page":"e219","DOI":"10.1097\/RLU.0b013e318262ad9b","volume":"37","author":"ST Donta","year":"2012","unstructured":"Donta ST, Noto RB, Vento JA (2012) SPECT brain imaging in chronic Lyme disease. Clin Nucl Med 37:e219\u2013e222","journal-title":"Clin Nucl Med"},{"key":"9359_CR13","doi-asserted-by":"publisher","first-page":"672","DOI":"10.1002\/mrm.1910300604","volume":"30","author":"SW Provencher","year":"1993","unstructured":"Provencher SW (1993) Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med 30:672\u2013679","journal-title":"Magn Reson Med"},{"key":"9359_CR14","doi-asserted-by":"publisher","first-page":"205","DOI":"10.2119\/2007-00091.Rupprecht","volume":"14","author":"TA Rupprecht","year":"2008","unstructured":"Rupprecht TA, Koedel U, Fingerle V, Pfister HW (2008) The pathogenesis of lyme neuroborreliosis: from infection to inflammation. Mol Med 14:205\u2013212","journal-title":"Mol Med"},{"key":"9359_CR15","doi-asserted-by":"publisher","first-page":"534","DOI":"10.1016\/j.nbd.2009.11.016","volume":"37","author":"BA Fallon","year":"2010","unstructured":"Fallon BA, Levin ES, Schweitzer PJ, Hardesty D (2010) Inflammation and central nervous system Lyme disease. Neurobiol Dis 37:534\u2013541","journal-title":"Neurobiol Dis"},{"key":"9359_CR16","doi-asserted-by":"publisher","first-page":"1415","DOI":"10.2353\/ajpath.2008.080483","volume":"173","author":"G Ramesh","year":"2008","unstructured":"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\u20131427","journal-title":"Am J Pathol"},{"key":"9359_CR17","first-page":"265","volume":"38","author":"M Kondrusik","year":"2004","unstructured":"Kondrusik M, Swierzbi\u0144ska 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\u2013270","journal-title":"Neurol Neurochir Pol"},{"key":"9359_CR18","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1093\/brain\/117.1.49","volume":"117","author":"CA Davie","year":"1994","unstructured":"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\u201358","journal-title":"Brain"},{"key":"9359_CR19","doi-asserted-by":"publisher","first-page":"2933","DOI":"10.1093\/brain\/awh646","volume":"128","author":"S Appenzeller","year":"2005","unstructured":"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\u20132940","journal-title":"Brain"},{"key":"9359_CR20","doi-asserted-by":"publisher","first-page":"3190","DOI":"10.1002\/art.24932","volume":"60","author":"BJ Emmer","year":"2009","unstructured":"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\u20133195","journal-title":"Arthritis Rheum"},{"key":"9359_CR21","first-page":"152","volume":"9","author":"Z Tyrakowska-Dade\u0142\u0142o","year":"2017","unstructured":"Tyrakowska-Dade\u0142\u0142o Z, Ku\u0142akowska A, Zajkowska J, Pancewicz S, Taras\u00f3w E (2017) Herpes simplex encephalitis\u2014diagnostic imaging. Prog Health Sci 9:152\u2013160","journal-title":"Prog Health Sci"},{"key":"9359_CR22","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1186\/s12883-016-0628-x","volume":"16","author":"D Bairwa","year":"2016","unstructured":"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 16:99","journal-title":"BMC Neurol"},{"key":"9359_CR23","doi-asserted-by":"publisher","first-page":"845","DOI":"10.1016\/j.jhep.2004.07.022","volume":"41","author":"K Weissenborn","year":"2004","unstructured":"Weissenborn K, Krause J, Bokemeyer M, Hecker H, Sch\u00fcler A, Ennen JC, Ahl B, Manns MP, B\u00f6ker KW (2004) Hepatitis C virus infection affects the brain-evidence from psychometric studies and magnetic resonance spectroscopy. J Hepatol 41:845\u2013851","journal-title":"J Hepatol"},{"key":"9359_CR24","doi-asserted-by":"publisher","first-page":"651","DOI":"10.1016\/j.jhep.2013.05.008","volume":"59","author":"J Bladowska","year":"2013","unstructured":"Bladowska J, Zimny A, Knysz B, Ma\u0142yszczak K, Ko\u0142towska A, Szewczyk P, G\u0105siorowski J, Furdal M, S\u0105siadek MJ (2013) Evaluation of early cerebral metabolic, perfusion and microstructural changes in HCV-positive patients: a pilot study. J Hepatol 59:651\u2013657","journal-title":"J Hepatol"},{"key":"9359_CR25","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1007\/s00234-002-0851-6","volume":"46","author":"A Ustymowicz","year":"2004","unstructured":"Ustymowicz A, Taras\u00f3w E, Zajkowska J, Walecki J, Hermanowska-Szpakowicz T (2004) Proton MR spectroscopy in neuroborreliosis: a preliminary study. Neuroradiology 46:26\u201330","journal-title":"Neuroradiology"},{"key":"9359_CR26","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1016\/j.pnmrs.2006.06.002","volume":"49","author":"PB Barker","year":"2006","unstructured":"Barker PB, Lin DDM (2006) In vivo proton MR spectroscopy of the human brain. Prog Nucl Magn Reson Spectrosc 49:99\u2013128","journal-title":"Prog Nucl Magn Reson Spectrosc"}],"container-title":["Journal of Neurology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00415-019-09359-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s00415-019-09359-0\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00415-019-09359-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,9,17]],"date-time":"2022-09-17T21:13:07Z","timestamp":1663449187000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s00415-019-09359-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,5,10]]},"references-count":26,"journal-issue":{"issue":"8","published-print":{"date-parts":[[2019,8]]}},"alternative-id":["9359"],"URL":"https:\/\/doi.org\/10.1007\/s00415-019-09359-0","relation":{},"ISSN":["0340-5354","1432-1459"],"issn-type":[{"value":"0340-5354","type":"print"},{"value":"1432-1459","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,5,10]]},"assertion":[{"value":"21 January 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 April 2019","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"3 May 2019","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"10 May 2019","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Compliance with ethical standards"}},{"value":"The authors declare that they have no conflict of interest.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflicts of interest"}},{"value":"The study was approved by the institutional review board of the Medical University of Bia\u0142ystok (Poland) (approval no. R-I-002\/340\/2015), and was consistent with the Declaration of Helinski.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethical standards"}},{"value":"All participants provided their written informed consent to participate in the study after detailed oral and written information about the study.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Informed consent"}}]}}