Ocular vestibular evoked myogenic potential (VEMP) reveals mesencephalic HTLV-1-associated neurological disease
Autoři:
Tatiana Rocha Silva aff001; Ludimila Labanca aff001; Júlia Fonseca de Morais Caporali aff001; Marco Aurélio Rocha Santos aff002; Luciana Macedo de Resende aff002; Rafael Teixeira Scoralick Dias aff001; Denise Utsch Gonçalves aff001
Působiště autorů:
Programa de Pós-Graduação em Infectologia e Medicina Tropical, Faculdade de Medicina da Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
aff001; Programa de Pós-Graduação em Ciências Fonoaudiológicas, Faculdade de Medicina da Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
aff002
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0217327
Souhrn
Purpose
Vestibular Myogenic Evoked Potential (VEMP) evaluates vestibulo-ocular and vestibulo-collic reflexes involved in the function of the otolithic organs and their afferent pathways. We compared the results of cervical and ocular VEMP in HTLV-1 associated myelopathy (HAM) and HTLV-1-asymptomatic infection.
Participants and methods
This cross-sectional study included 52 HTLV-1-infected individuals (26 HAM and 26 asymptomatic carriers) and 26 seronegative controls. The groups were similar regarding age and gender. Participants underwent simultaneous ocular and cervical VEMP. The stimulus to generate VEMP was a low-frequency tone burst sound tone burst, with an intensity of 120 decibels normalized hearing level, bandpass filter from 10 to 1,500 Hertz (Hz), with 100 stimuli at 500 Hz and 50 milliseconds recording time. The latencies of the electrophysiological waves P13 and N23 for cervical VEMP and N10 and P15 waves for ocular VEMP were compared among the groups. The absence or delay of the electrophysiological waves were considered abnormal results.
Results
Ocular VEMP was similar among the groups for N10 (p = 0.375) and different for P15 (p≤0.001). Cervical VEMP was different for P13 (p = 0.001) and N23 (p = 0.003). About ocular VEMP, in the HTLV-1-asymptomatic group, normal waves were found in 23(88.5%) individuals; in HAM group, normal waves were found in 7(26.9%). About cervical VEMP, 18(69.2%) asymptomatic carriers presented normal waves and only 3(11.5%) patients with HAM presented normal waves. Abnormalities in both VEMPs were found in 1(3.8%) asymptomatic carrier and in 16(61.5%) patients with HAM.
Conclusion
Neurological impairment in HAM was not restricted to the spinal cord. The mesencephalic connections, tested by ocular VEMP, have been also altered. Damage of the oculomotor system, responsible for eye stabilization during head and body movements, may explain why dizziness is such a frequent complaint in HAM.
Klíčová slova:
Central nervous system – Electrode recording – Evoked potentials – HTLV-1 – Reflexes – Spine – Reference electrodes
Zdroje
1. Gessain A, Cassar O. Epidemiological aspects and world distribution of HTLV-1 infection. Front Microbiol. 2012;3:1–23. doi: 10.3389/fmicb.2012.00001
2. Orland JR, Engstrom J, Fridey J, Sacher RA, Smith JW, Nass C, et al. Prevalence and clinical features of HTLV neurologic disease in HTLV outcomes study. Neurology. 2003;61:1588–1594. doi: 10.1212/01.wnl.0000096011.92542.da 14663047
3. Bhigjee AI, Wiley CA, Wachsman W, Amenomori T, Pirie D, Bill PL, et al. HTLV-I-associated myelopathy: clinicopathologic correlation with localization of provirus to spinal cord. Neurology. 1991;41(12):1990–1992. doi: 10.1212/wnl.41.12.1990 1745362
4. Gascón MRP, Cassebd J, Smid J, Vidal JE, Fonseca LAM, Paiva A, et al. Cognitive impairment is frequent among symptomatic carriers of human T-cell lymphotropic virus type 1 (HTLV-1), regardless of their clinical status. J Neurol Sci. 2017;377:185–189. doi: 10.1016/j.jns.2017.04.019 28477692
5. Mendes GB, Kalil RS, Rosadas C, de Freitas MRG, Puccioni-Sohler M. Neurological manifestations in human T-cell lymphotropic virus type 1 (HTLV-1)–infected individuals without HTLV-1–associated myelopathy/tropical spastic paraparesis: a longitudinal cohort study. CID. 2015;61:49–56.
6. Schütze M, Romanelli LC, Rosa DV, Carneiro-Proietti AB, Nicolato R, Romano-Silva MA, et al. Brain metabolism changes in patients infected with HTLV-1. Front Mol Neurosci. 2017;10:1–8. doi: 10.3389/fnmol.2017.00001
7. Ferraz AC, Gabbai AA, Abdala N, Nogueira RG. Ressonância magnética na mielopatia associada ao HTLV-I: Leucoencefalopatia e atrofia medular. Arq. Neuro-Psiquiatr. [online]. 1997;55(4):728–736.
8. Felipe L, Gonçalves DU, Santos MA, Proietti FA, Ribas JG, Carneiro-Proietti AB, et al. Vestibular evoked myogenic potential (VEMP) to evaluate cervical myelopathy in human T-cell lymphotropic virus type i infection. Spine (Phila Pa 1976). 2008;33:1180–1184.
9. Labanca L, Starling AL, de Sousa-Pereira SR, Romanelli LC, de Freitas Carneiro-Proietti AB, Carvalho LN, et al. Electrophysiological analysis shows dizziness as the first symptom in human T cell lymphotropic Virus type-associated myelopathy/tropical spastic paraparesis. AIDS Res Hum Retroviruses. 2015;31(6):649–654. doi: 10.1089/AID.2014.0153 25760424
10. De Castro-Costa CM, Araújo AQ, Barreto MM, Takayanagui OM, Sohler MP, da Silva EL, et al. Proposal for diagnostic criteria of tropical spastic paraparesis/HTLV1-associated myelopathy (TSP/HAM). AIDS Res Hum Retroviruses. 2006;22(10):931–935. doi: 10.1089/aid.2006.22.931 17067261
11. Oh SY, Kim JS, Lee JM, Shin BS, Hwang SB, Kwak KC et al. Ocular vestibular evoked myogenic potentials induced by air-conducted sound in patients with acute brainstem lesions. Clin Neuro-physiol. 2013;124:770–778.
12. Kantner C, Gürkov R. Characteristics and clinical applications of ocular vestibular evoked myogenic potentials. Hearing Research. 2012;294(1–2):55–63. doi: 10.1016/j.heares.2012.10.008 23123220
13. Felipe L, Kingma H, Lambertucci JR, Carneiro-Proietti AB, Gonçalves DU. Testing the vestibular evoked myogenic potential (VEMP) to identify subclinical neurological alterations in different phases of human T-lymphotropic virus type 1 infection. Spine J. 2013;13(4):397–401. doi: 10.1016/j.spinee.2012.11.015 23267739
14. Cunha LC, Labanca L, Tavares MC, Gonçalves DU. Vestibular evoked myogenic potential (VEMP) with galvanic stimulation in normal subjects. Braz J Otorhinolaryngol. 2014;80(1):48–53. doi: 10.5935/1808-8694.20140011 24626892
15. Park HJ, Lee IS, Shin JE, Lee YJ, Park MS. Frequency-tuning characteristics of cervical and ocular vestibular evoked myogenic potentials induced by air-conducted tone bursts. Clin Neurophysiol. 2010;121(1):85–89. doi: 10.1016/j.clinph.2009.10.003 19892592
16. Labanca L, de Morais Caporali JF, da Silva Carvalho SA, Lambertucci JR, Carneiro Proietti ABF, Romanelli LCF, et al. Vestibular-evoked myogenic potential triggered by galvanic vestibular stimulation may reveal subclinical alterations in human T-cell lymphotropic virus type 1-associated myelopathy. PLoS One. 2018;13(7):1–17.
17. Caporali JFM, Labanca L, Florentino KR, Souza BO, Utsch Gonçalves D. Intrarater and interrater agreement and reliability of vestibular evoked myogenic potential triggered by galvanic vestibular stimulation (galvanic-VEMP) for HTLV-1 associated myelopathy testing. PLoS One. 2018;13(9):1–13.
18. Allain JP, Stramer SL, Carneiro-Proietti AB, Martins ML, Lopes da Silva SN, Ribeiro M. Transfusion-transmitted infectious diseases. Biologicals. 2009;37(2):71–77. doi: 10.1016/j.biologicals.2009.01.002 19231236
19. Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology. 1983;33(11):1444–1452. doi: 10.1212/wnl.33.11.1444 6685237
20. Osame M. Review of WHO Kagoshima meeting and diagnostic guidelines for HAM/TSP. In: Blattner W. (ed) Human retrovirology: HTLV. Raven. 1990:191–197.
21. American Eeg Society. Clinical evoked potentials guidelines. Recommended standards for normative studies of evoked potentials, statistical analysis of results and criteria for clinically significant abnormality. Journal of Clinical Neurophysiology. 1994;11:45–47.
22. Wang SJ, Yeh TH, Chang CH, Young YH. Consistent latencies of vestibular evoked myogenic potentials. Ear Hear. 2008;29(6):923–929. doi: 10.1097/AUD.0b013e3181853019 18685495
23. Li C, Zuniga MG, Nguyen KD, Carey JP, Agrawal Y. How to interpret latencies of cervical and ocular vestibular-evoked myogenic potentials: Our experience in fifty-three participants. Clin Otolaryngol. 2014;39(5):297–301. doi: 10.1111/coa.12277 24962335
24. Lim CL, Clouston P, Sheean G, Yiannikas C. The influence of voluntary EMG activity and click intensity on the vestibular click evoked myogenic potential. Muscle Nerve. 1995;18(10):1210–1213. doi: 10.1002/mus.880181021 7659119
25. Murofushi T, Matsuzaki M, Wu CH. Short tone burst-evoked myogenic potentials on the sternocleidomastoid muscle: are these potentials also of vestibular origin? Arch. Otolaryngol. Head Neck Surg. 1999;125(6):660–664. doi: 10.1001/archotol.125.6.660 10367923
26. Akin FW, Murnane OD, Panus PC, Caruthers SK, Wilkinson AE, Proffitt TM. The influence of voluntary tonic EMG level on the vestibular-evoked myogenic potential. J Rehabil Res Dev. 2004;41:473–480. doi: 10.1682/jrrd.2003.04.0060 15543465
27. De Waele C, Tran Ba Huy P, Diart JP, Freyss G, Vidal PP. Saccular dysfunction in Meniere’s disease. Am J Otol. 1999;20:223–232. 10100527
28. Young YH, Huang TW, Cheng PW. Assessing the stage of Meniere’s disease using vestibular evoked myogenic potentials. Arch Otolaryngol Head Neck Surg. 2003;129:815–818. doi: 10.1001/archotol.129.8.815 12925337
29. Mcnerney K. S. The use of 64-channel electroencephalography and positron emission tomography to study vestibular evoked myogenic potentials. (Thesis). New York: Department of Communicative Disorders and Sciences; 2007.
30. Bangham CRM, Osame M. Cellular immune response to HTLV-1. Oncogene. 2005;24:6035–6046. doi: 10.1038/sj.onc.1208970 16155610
31. Shimizu K, Murofushi T, Sakurai M, Halmagyi M. Vestibular evoked myogenic potentials in multiple sclerosis. J Neurol Neurosurg Psychiatry. 2000;69:276–277. doi: 10.1136/jnnp.69.2.276 10960289
32. Murofushi T, Shimizu K, Takegoshi H, Cheng PW. Diagnostic value of prolonged latencies in the vestibular evoked myogenic potential. Arch Otolaryngol Head Neck Surg. 2001;27(9):1069–1072.
33. Colebatch JG, Rothwell JC, Bronstein A, Ludman H. Click-evoked vestibular activation in the Tullio phenomenon. J Neurol Neurosurg Psychiatry. 1994;57(12):1538–1540. doi: 10.1136/jnnp.57.12.1538 7798988
34. Akizuki S, Nakazato O, Higuchi Y, Tanabe K, Setoguchi M, Yoshida S, et al. Necropsy findings in HTLV-I associated myelopathy. Lancet. 1987;17(1):156–157.
35. Ribas JGR, Melo GCN. Mielopatia associada ao vírus linfotrópicos humano de células T do tipo 1 (HTLV-1). Rev Soc Bras Med Trop. 2002;35(4):377–384. doi: 10.1590/s0037-86822002000400015 12170334
36. Rosengren SM, Welgampola MS, Colebatch JG. Vestibular evoked myogenic potentials: past, present and future. Clin Neurophysiol. 2010;121(5):636–651. doi: 10.1016/j.clinph.2009.10.016 20080441
37. Chihara Y, Iwasaki S, Ushio M, Murofushi T. Vestibular evoked extraocular potentials by air-conducted sound: another clinical test for vestibular function. Clin Neurophysiol. 2007;118(12):2745–2751. doi: 10.1016/j.clinph.2007.08.005 17905655
38. De Natale ER, Ginatempo F, Paulus KS, Pes GM, Manca A, Tolu E, et al. Abnormalities of vestibular-evoked myogenic potentials in idiopathic Parkinson’s disease are associated with clinical evidence of brainstem involvement. Neurol Sci. 2015;36(6):995–1001. doi: 10.1007/s10072-014-2054-4 25567081
39. Fuzii HT, da Silva Dias GA, de Barros RJ, Falcão LF, Quaresma JA. Immunopathogenesis of HTLV-1-assoaciated myelopathy/tropical spastic paraparesis (HAM/TSP). Life Sci. 2014;104(1–2):9–14. doi: 10.1016/j.lfs.2014.03.025 24704970
40. Coler-Reilly ALG, Sato T, Matsuzaki T, Nakagawa M, Niino M, Nagai M, Nakamura T, Takenouchi N, Araya N, Yagishita N, Inoue E, Yamano Y. Effectiveness of Daily Prednisolone to Slow Progression of Human T-Lymphotropic Virus Type 1-Associated Myelopathy/Tropical Spastic Paraparesis: A Multicenter Retrospective Cohort Study. Neurotherapeutics. 2017;14(4):1084–1094. doi: 10.1007/s13311-017-0533-z 28536850
41. Martins ML, de Freitas Carneiro-Proietti AB, Nicolato R, de Miranda DM, Romanelli LCF. HTLV-1 proviral load in cerebrospinal fluid may not be a good marker to differentiate asymptomatic carriers with high proviral load in blood from HAM/TSP patients. J Neurovirol. 2018;24(4):432–438. doi: 10.1007/s13365-018-0632-6 29589290
42. Romanelli LCF, Miranda DM, Carneiro-Proietti ABF, Mamede M, Vasconcelos HMM, Martins ML, et al. Spinal cord hypometabolism associated with infection by human T-cell lymphotropic virus type 1(HTLV-1). PLoS Negl Trop Dis. 2018;12(8):e0006720. doi: 10.1371/journal.pntd.0006720 30148843
43. Liu W, Bakshi A, Massoud R, Brunetto GS, Reich DS, Nair G, et al. Quantifying spinal cord cross-sectional area in HTLV-1 associated myelopathy/tropical spastic paraparesis (HAM/TSP). Retrovirology. 2014; 11(Suppl 1): 22.
44. Taniguchi A, Mochizuki H, Yamashita A, Shiomi K, Asada Y, Nakazato M. Spinal cord anteroposterior atrophy in HAM/TSP: Magnetic resonance imaging and neuropathological analyses. J Neurol Sci. 2017;381:135–140. doi: 10.1016/j.jns.2017.08.3243 28991665
45. Starling AL, Coelho-Dos-Reis JG, Peruhype-Magalhães V, Pascoal-Xavier MA, Gonçalves DU, Béla SR, et al. Immunological signature of the different clinical stages of the HTLV-1 infection: establishing serum biomarkers for HTLV-1-associated disease morbidity. Biomarkers. 2015;20(6–7):502–512. doi: 10.3109/1354750X.2015.1094141 26474234
46. Rosa DV, Magno LA, Pereira NC, Romanelli LC, Albuquerque MR, Martins ML, et al. Plasma and cerebrospinal fluid levels of cytokines as disease markers of neurologic manifestation in long-term HTLV-1 infected individuals. Biomark Med. 2018;12(5):447–454. doi: 10.2217/bmm-2017-0313 29737866
47. Champs APS, de Azeredo Passos VM, Carvalho G, Barreto SM, Meirelles C, Caramelli P. Cognitive impairment in HTLV-1-associated myelopathy, proviral load and inflammatory markers. Int J Infect Dis. 2019;84:121–126. doi: 10.1016/j.ijid.2019.05.010 31085316
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