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Chronic Neuroborreliosis by B. Garinii: an Unusual Case Presenting with Epilepsy and Multifocal Brain MRI Lesions

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Chronic Neuroborreliosis by B. Garinii: an Unusual Case Presenting with Epilepsy and Multifocal Brain MRI Lesions NEW MICROBIOLOGICA, 37, 393-397, 2014 Chronic neuroborreliosis by B. garinii: an unusual case presenting with epilepsy and multifocal brain MRI lesions Giovanni Matera1, Angelo Labate2, Angela Quirino1, Angelo G. Lamberti1, Giuseppe Borzì2, Giorgio S. Barreca1, Laura Mumoli2, Cinzia Peronace1, Aida Giancotti1, Antonio Gambardella2, Alfredo Focà1, Aldo Quattrone2 1Institute of Microbiology, Department of Health Sciences, “Magna Graecia” University, Catanzaro, Italy; 2Institute of Neurology, “Magna Graecia” University, Catanzaro, Italy; SUMMARY Late/chronic Lyme neuroborreliosis (LNB) represents a challenging entity whose diagnosis requires a combination of clinical and laboratory findings, surrounded by much controversy. Here we describe a patient who had a peculiar form of late LNB with CNS lesions shown by magnetic resonance imaging (MRI), and epileptic seizures, etiologi- cally diagnosed by conventional and molecular methods. The current case provides evidence that patients present- ing with epileptic seizures and MRI-detected multifocal lesions, particularly when a facial palsy has also occurred, should raise the suspicion of LNB, as this diagnosis has important implications for treatment and prognosis. KEY WORDS: Neuroborreliosis, seizures, real-time PCR. Received December 11, 2013 Accepted June 2, 2014 INTRODUCTION Lyme borreliosis involves the nervous system (neuroborreliosis) in about 15% of patients, and Lyme borreliosis (LB) is a worldwide multisys- the most common manifestations of European tem infection transmitted to humans by the bite Lyme neuroborreliosis are painful radiculopa- of an infected tick of the genus Ixodes (Stanek thy and cranial neuropathy (especially of the et al., 2012). Borrelia burgdorferi sensu lato, the facial nerve) with pleocytosis in the cerebrospi- causative bacterium of LB, is genetically diver- nal fluid (CSF), while other neurological mani- gent and has been divided into several species festations are rare (Pfister et al., 2006). Regard- or genomic groups. B. burgdorferi sensu stricto, less of the type of neurological manifestations, B. garinii, and B. afzelii have been cultured from however, exclusion of Lyme neuroborreliosis as patients and are thought to be responsible for a trigger of disease is recommended in selected human Lyme borreliosis. Borrelia genospecies patients with demyelinating disease, hemipa- seem to be associated with distinct clinical syn- resis, or epilepsy (Oksi et al., 1996). Here we dromes (Floris et al., 2007), and the dominating describe a patient who had a peculiar form of species in Europe are B. garinii and B. afzelii. chronic neuroborreliosis with central nervous system (CNS) lesions shown by magnetic reso- nance imaging (MRI) and epileptic seizures. Corresponding author Prof. Giovanni Matera Institute of Microbiology CASE REPORT Department of Health Sciences University “Magna Graecia” of Catanzaro Viale Europa - 88100 Catanzaro, Italy A 26-year-old man had previously been healthy, E-mail: [email protected] apart from a right facial nerve paralysis that oc- 394 G. Matera, et al. curred two years before and resolved spontane- An ELFA kit, “VIDAS Lyme Screen” (bioMer- ously. On March 10, 2013 he had a generalized ieux, Marcy L’Étoile, France), was used as a seizure and was admitted to the hospital. An- screening test for Borrelia serology and a se- other seizure occurred on the day of admission. rum sample of our patient was found weakly He recalled no tick bites, erythema migrans, or positive for total Ig anti-Borrelia burgdorferi history of fatigue, myalgia, or arthralgia. Neu- B31 strain whole cell sonicates. Then a confir- rological examination was normal apart from mation Western blot test (recomLine Borrelia a minimal evidence of the previous right facial burgdorferi IgM and IgG immunoblots, Mi- nerve palsy. Extensive blood tests were normal, as were electroencephalography, electromyog- raphy and cortical visual and somatosensory evoked potentials. Brain MRI revealed hyperintense lesions in T2 and FLAIR sequences, with a bright appearance in diffusion-weighted images, not enhancing after gadolinium administration, and involv- ing the right temporal cortex, the left temporal pole, insula and hippocampus, as well as the periventricular white matter, semi-oval centers and corpus callosum (Figure 1). There was no evidence of contrast enhancement or restricted diffusion. Brain MRI angiography and tran- scranial Doppler studies were normal. A whole body 18F-FDG PET/CT examination study was unremarkable. The cerebrospinal fluid (CSF) revealed 2 white blood cells/ µl with normal glucose and increased total protein concentra- tions (0.544 g/l, normal range: 0.18 to 0.43), and absence of oligoclonal bands. Cytological anal- ysis was negative for malignant cells. CSF gram stain and bacterial cultures were all negative. In addition, Brucella, Rickettsia, CMV, EBV and HCV serology were all negative. FIGURE 1 - Cranial MRI showing a high T2 signal in FIGURE 2 - Western blot analysis of serum IgG (a), the brain subcortical area and white matter of the right CSF IgG (b) and serum IgM (c) of the studied patient. temporal lobe, as signs of inflammation and/or ische- The samples tested in strip (a) and in strip (b) were mia. Smaller lesions were found by MRI in the basal brought to the same concentration of total IgG (see ganglia, thalamus and lamina interna. text for details). Chronic neuroborreliosis 395 krogen, Neuried, Germany) was carried out. IgM (strip c, LBB15). Band p39 was clear-cut, Before Western blot test, both serum and CSF but exhibited low intensity in both serum and samples were diluted in order to bring them to CSF samples. OspC of B. garinii was a clear-cut the same concentration of total IgG (15 mg/l). band with a low intensity in serum IgG (strip In Western blot analysis band p41, shared by all a, LBB14). With the exception of p41 in serum Spirochetaceae, was very intense and clear-cut IgG (strip a, LBB14), all the remaining bands in serum IgG (strip a, LBB14), but it appeared observed were below the intensity of the cut- with a lower intensity in serum IgM (strip off/control band (Figure 2). Positivity to anti- c, LBB15) and in CSF IgG (strip b, LBB19). bodies against p100 and p39 are reported to be Moreover p100 in serum IgG (strip a, LBB14) strongly suggestive of late Borreliosis (Gruber, was an obvious band, while it was very weak 2013). Regarding the serology of Spirocheta- in CSF IgG (strip b, LBB19) and in in serum ceae, RPR, TPHA, anti-treponemal ELISA for FIGURE 3 - Amplification curves (A) and melting curve analysis (B) of B. burgdorferi s.s., B. afzelii, B. garinii and the CSF sample under investigation for the recA gene. The Tm values were: 84.49°C for B. burgdorferi s.s., 85.37 °C for B. afzelii, 82.08 °C for B. garinii and 82.07°C for the CSF sample. The negative control (CSF negative sample) melted at a temperature of 79.65°C. 396 G. Matera, et al. IgG and IgM and Western blot for IgG and IgM manifestation throughout his 4-month follow- were carried out in parallel, but were all nega- up period. tive. In addition, the complement fixation test for anti-Leptospira total Ig was performed with a negative result. DISCUSSION Real-time PCR assay PCR findings along with serology indicate that A volume of 500 µl of CSF specimens was cen- an isolate of the species B. garinii was the etio- trifuged (8000 x g for 10 min) and the pellet was logical agent of the investigated case. Chronic suspended in 100 µl QIAamp elution buffer and neuroborreliosis represents a challenging en- DNA extracted using a QIAamp DNA Blood Mini tity whose diagnosis requires a combination Kit (Qiagen, Hilden, Germany) following the of clinical and laboratory findings, still sur- manufacturer’s instructions. The LightCycler rounded by much controversy but with impor- system (Roche Diagnostics, Italy) with LightCy- tant implications for treatment and prognosis cler FastStart DNA Master SYBR Green I was (Ljøstad & Mygland, 2013). The clinical pic- used for amplification and real-time detection. ture of our patient is of interest for clinicians, For genus and species-specific real-time PCR as it did not conform to the classic clinical assay, the forward primer nTM17.F 5’-GTC- manifestations of chronic neuroborreliosis GATCTATTGTATTAGATGAGGCTCTCG-3’and that consist of progressive encephalomyelitis, reverse primer nTM17.R 5’-GCCAAAGTTCT- stroke-like symptoms due to vasculitis, ra- GCAACATTAACACCTAAAG-3’ (J. Pietila et al., diculitis, or mononeuritis multiplex (Ljøstad 2000; J.J Lazarus et al., 2012.) were used to am- & Mygland, 2013). Particularly noteworthy plify a 222 bp portion of the recA gene. in this regard was the occurrence in our pa- The PCR mixture contained 2 µl of extracted tient of facial nerve palsy two years prior to DNA, 0.5 µl of each primer, 1.6 µl of MgCl2, 2 the onset of epilepsy. In this way, the current µl of SYBR Green and 13.4 µl of H2O for PCR case provides evidence that patients present- supplied by the kit. The amplification PCR con- ing with epileptic seizures and MRI-detected ditions were: denaturation at 95°C for 10 min, multifocal lesions, particularly when a facial followed by 40 cycles consisting of 95°C for palsy has also occurred, should raise the sus- 10s, 59°C for 8s and 72°C for 11s. After ampli- picion of Lyme borreliosis as a trigger of the fication, melting curve analysis was carried out disease, as this diagnosis has important impli- by evaluating a Tm (melting temperature) of cations for treatment and prognosis. 84.49±0.13°C for B. burgdorferi s.s., 84.86±0.58 In addition to the pathophysiology, unusual as- for B. afzelii and 82.27±0.38 for B. garinii. The pects of our case are the cranial MRI scans that unspecific products, even primer-dimers, pro- showed ischemic lesions in the vascular terri- duced when little or no template is present, tory of the middle cerebral artery.
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