Neural metabolic activity in idiopathic tinnitus patients after repetitive transcranial magnetic stimulation
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摘要
BACKGROUND The central mechanism of idiopathic tinnitus is related to hyperactivity of cortical and subcortical auditory and non-auditory areas.Repetitive transcranial magnetic stimulation(rTMS)is a well-tolerated,non-invasive potential treatment option for tinnitus.AIM To investigate the changes of neural metabolic activity after rTMS in chronic idiopathic tinnitus(IT)patients.ME THODS Eleven patients underwent rTMS(1 Hz,90%motor threshold,1000 stimuli/day for consecutive 10 d)on the left temporoparietal region cortex.Tinnitus handicap inventory(THI)and visual analogue score(VAS)were assessed at baseline and posttreatment.All patients underwent 18 F-fluorodeoxyglucose(FDG)positron emission tomography to evaluate the neural metabolic activity.Data were preprocessed using statistical parametric mapping and Gretna software to extract the regions of interest(ROls).The correlation between brain areas involved and THI scores was analyzed.RESULTS Baseline and posttreatment parameters showed no significant difference regarding THI score(t=1.019,P=0.342>0.05)and VAS(t=0.00,P=1.0>0.05).Regions with the highest FDG uptake were the right inferior temporal gyrus(ITG),right parahippocampa gyrus(PHG),right hippocampus,rectus gyrus,left middle frontal gyrus,and right inferior frontal gyrus in IT patients.After rTMS treatment,IT patients showed increased activities in the right PHG,right superior temporal gyrus,right superior frontal gyrus,anterior insula,left inferior parietal lobule,and left precentral gyrus,and decreased activities in the left postcentral gyrus and left ITG.The ROIs in the right parahippocampa gyrus and right superior frontal gyrus were positively correlated with THI scores(r=0.737,P=0.037<0.05;r=0.735,P=0.038<0.05).CONCLUSION Our study showed that 1-Hz rTMS directed to the left temporo-parietal junction resulted no statistically significant symptom alleviation.After treatment,brain areas of the limbic and prefrontal system showed high neutral metabolic activity The auditory and non-auditory systems together will be the target for rTMS treatment.
BACKGROUND The central mechanism of idiopathic tinnitus is related to hyperactivity of cortical and subcortical auditory and non-auditory areas.Repetitive transcranial magnetic stimulation(rTMS)is a well-tolerated,non-invasive potential treatment option for tinnitus.AIM To investigate the changes of neural metabolic activity after rTMS in chronic idiopathic tinnitus(IT)patients.ME THODS Eleven patients underwent rTMS(1 Hz,90%motor threshold,1000 stimuli/day for consecutive 10 d)on the left temporoparietal region cortex.Tinnitus handicap inventory(THI)and visual analogue score(VAS)were assessed at baseline and posttreatment.All patients underwent 18 F-fluorodeoxyglucose(FDG)positron emission tomography to evaluate the neural metabolic activity.Data were preprocessed using statistical parametric mapping and Gretna software to extract the regions of interest(ROls).The correlation between brain areas involved and THI scores was analyzed.RESULTS Baseline and posttreatment parameters showed no significant difference regarding THI score(t=1.019,P=0.342>0.05)and VAS(t=0.00,P=1.0>0.05).Regions with the highest FDG uptake were the right inferior temporal gyrus(ITG),right parahippocampa gyrus(PHG),right hippocampus,rectus gyrus,left middle frontal gyrus,and right inferior frontal gyrus in IT patients.After rTMS treatment,IT patients showed increased activities in the right PHG,right superior temporal gyrus,right superior frontal gyrus,anterior insula,left inferior parietal lobule,and left precentral gyrus,and decreased activities in the left postcentral gyrus and left ITG.The ROIs in the right parahippocampa gyrus and right superior frontal gyrus were positively correlated with THI scores(r=0.737,P=0.037<0.05;r=0.735,P=0.038<0.05).CONCLUSION Our study showed that 1-Hz rTMS directed to the left temporo-parietal junction resulted no statistically significant symptom alleviation.After treatment,brain areas of the limbic and prefrontal system showed high neutral metabolic activity The auditory and non-auditory systems together will be the target for rTMS treatment.
BACKGROUND The central mechanism of idiopathic tinnitus is related to hyperactivity of cortical and subcortical auditory and non-auditory areas.Repetitive transcranial magnetic stimulation(rTMS)is a well-tolerated,non-invasive potential treatment option for tinnitus.AIM To investigate the changes of neural metabolic activity after rTMS in chronic idiopathic tinnitus(IT)patients.ME THODS Eleven patients underwent rTMS(1 Hz,90%motor threshold,1000 stimuli/day for consecutive 10 d)on the left temporoparietal region cortex.Tinnitus handicap inventory(THI)and visual analogue score(VAS)were assessed at baseline and posttreatment.All patients underwent 18 F-fluorodeoxyglucose(FDG)positron emission tomography to evaluate the neural metabolic activity.Data were preprocessed using statistical parametric mapping and Gretna software to extract the regions of interest(ROls).The correlation between brain areas involved and THI scores was analyzed.RESULTS Baseline and posttreatment parameters showed no significant difference regarding THI score(t=1.019,P=0.342>0.05)and VAS(t=0.00,P=1.0>0.05).Regions with the highest FDG uptake were the right inferior temporal gyrus(ITG),right parahippocampa gyrus(PHG),right hippocampus,rectus gyrus,left middle frontal gyrus,and right inferior frontal gyrus in IT patients.After rTMS treatment,IT patients showed increased activities in the right PHG,right superior temporal gyrus,right superior frontal gyrus,anterior insula,left inferior parietal lobule,and left precentral gyrus,and decreased activities in the left postcentral gyrus and left ITG.The ROIs in the right parahippocampa gyrus and right superior frontal gyrus were positively correlated with THI scores(r=0.737,P=0.037<0.05;r=0.735,P=0.038<0.05).CONCLUSION Our study showed that 1-Hz rTMS directed to the left temporo-parietal junction resulted no statistically significant symptom alleviation.After treatment,brain areas of the limbic and prefrontal system showed high neutral metabolic activity The auditory and non-auditory systems together will be the target for rTMS treatment.
引文
1 Kaltenbach JA.Neurophysiologic mechanisms of tinnitus.J Am Acad Audiol 2000;11:125-137[PMID:10755809]
2 Ziai K,Moshtaghi O,Mahboubi H,Djalilian HR.Tinnitus Patients Suffering from Anxiety and Depression:A Review.Int Tinnitus J 2017;21:68-73[PMID:28723605 DOI:10.5935/0946-5448.20170013]
3 Burton H,Wineland A,Bhattacharya M,Nicklaus J,Garcia KS,Piccirillo JF.Altered networks in bothersome tinnitus:a functional connectivity study.BMC Neurosci 2012;13:3[PMID:22217183 DOI:10.1186/1471-2202-13-3]
4 Piccirillo JF,Kallogjeri D,Nicklaus J,Wineland A,Spitznagel EL,Vlassenko AG,Benzinger T,Mathews J,Garcia KS.Low-frequency repetitive transcranial magnetic stimulation to the temporoparietal junction for tinnitus:four-week stimulation trial.JAMA Otolaryngol Head Neck Surg 2013;139:388-395[PMID:23599075 DOI:10.1001/jamaoto.2013.233]
5 Eggermont JJ.Pathophysiology of tinnitus.Prog Brain Res 2007;166:19-35[PMID:17956768 DOI:10.1016/S0079-6123(07)66002-6]
6 Mennemeier M,Chelette KC,Allen S,Bartel TB,Triggs W,Kimbrell T,Crew J,Munn T,Brown GJ,Dornhoffer J.Variable changes in PET activity before and after rTMS treatment for tinnitus.Laryngoscope2011;121:815-822[PMID:21287564 DOI:10.1002/lary.21425]
7 De Ridder D.Should rTMS for tinnitus be performed left-sided,ipsilaterally or contralaterally,and is it a treatment or merely investigational?Eur J Neurol 2010;17:891-892[PMID:20236176 DOI:10.1111/j.1468-1331.2010.02967.x]
8 Kleinjung T,Eichhammer P,Langguth B,Jacob P,Marienhagen J,Hajak G,Wolf SR,Strutz J.Longterm effects of repetitive transcranial magnetic stimulation(rTMS)in patients with chronic tinnitus.Otolaryngol Head Neck Surg 2005;132:566-569[PMID:15806046 DOI:10.1016/j.otohns.2004.09.134]
9 Plewnia C,Reimold M,Najib A,Reischl G,Plontke SK,Gerloff C.Moderate therapeutic efficacy of positron emission tomography-navigated repetitive transcranial magnetic stimulation for chronic tinnitus:a randomised,controlled pilot study.J Neurol Neurosurg Psychiatry 2007;78:152-156[PMID:16891384DOI:10.1136/jnnp.2006.095612]
10 Kimbrell TA,Little JT,Dunn RT,Frye MA,Greenberg BD,Wassermann EM,Repella JD,Danielson AL,Willis MW,Benson BE,Speer AM,Osuch E,George MS,Post RM.Frequency dependence of antidepressant response to left prefrontal repetitive transcranial magnetic stimulation(rTMS)as a function of baseline cerebral glucose metabolism.Biol Psychiatry 1999;46:1603-1613[PMID:10624541]
11 Marcondes RA,Sanchez TG,Kii MA,Ono CR,Buchpiguel CA,Langguth B,Marcolin MA.Repetitive transcranial magnetic stimulation improve tinnitus in normal hearing patients:a double-blind controlled,clinical and neuroimaging outcome study.Eur J Neurol 2010;17:38-44[PMID:19614962 DOI:10.1111/j.1468-1331.2009.02730.x]
12 Perrachione TK,Ghosh SS.Optimized design and analysis of sparse-sampling FMRI experiments.Front Neurosci 2013;7:55[PMID:23616742 DOI:10.3389/fnins.2013.00055]
13 Bestmann S,Ruff CC,Blankenburg F,Weiskopf N,Driver J,Rothwell JC.Mapping causal interregional influences with concurrent TMS-fMRI.Exp Brain Res 2008;191:383-402[PMID:18936922 DOI:10.1007/s00221-008-1601-8]
14 Newman CW,Sandridge SA,Jacobson GP.Psychometric adequacy of the Tinnitus Handicap Inventory(THI)for evaluating treatment outcome.J Am Acad Audiol 1998;9:153-160[PMID:9564679]
15 Zeman F,Koller M,Schecklmann M,Langguth B,Landgrebe M;TRI database study group.Tinnitus assessment by means of standardized self-report questionnaires:psychometric properties of the Tinnitus Questionnaire(TQ),the Tinnitus Handicap Inventory(THI),and their short versions in an international and multi-lingual sample.Health Qual Life Outcomes 2012;10:128[PMID:23078754 DOI:10.1186/1477-7525-10-128]
16 Rossi S,De Capua A,Ulivelli M,Bartalini S,Falzarano V,Filippone G,Passero S.Effects of repetitive transcranial magnetic stimulation on chronic tinnitus:a randomised,crossover,double blind,placebo controlled study.J Neurol Neurosurg Psychiatry 2007;78:857-863[PMID:17314192 DOI:10.1136/jnnp.2006.105007]
17 Khedr EM,Rothwell JC,Ahmed MA,El-Atar A.Effect of daily repetitive transcranial magnetic stimulation for treatment of tinnitus:comparison of different stimulus frequencies.J Neurol Neurosurg Psychiatry 2008;79:212-215[PMID:18202212 DOI:10.1136/jnnp.2007.127712]
18 Rossini PM,Burke D,Chen R,Cohen LG,Daskalakis Z,Di Iorio R,Di Lazzaro V,Ferreri F,Fitzgerald PB,George MS,Hallett M,Lefaucheur JP,Langguth B,Matsumoto H,Miniussi C,Nitsche MA,PascualLeone A,Paulus W,Rossi S,Rothwell JC,Siebner HR,Ugawa Y,Walsh V,Ziemann U.Non-invasive electrical and magnetic stimulation of the brain,spinal cord,roots and peripheral nerves:Basic principles and procedures for routine clinical and research application.An updated report from an I.F.C.N.Committee.Clin Neurophysiol 2015;126:1071-1107[PMID:25797650 DOI:10.1016/j.clinph.2015.02.001]
19 Song JJ,De Ridder D,Van de Heyning P,Vanneste S.Mapping tinnitus-related brain activation:an activation-likelihood estimation metaanalysis of PET studies.J Nucl Med 2012;53:1550-1557[PMID:22917883 DOI:10.2967/jnumed.112.102939]
20 Ko JH,Tang CC,Eidelberg D.Brain stimulation and functional imaging with fMRI and PET.Handb Clin Neurol 2013;116:77-95[PMID:24112887 DOI:10.1016/B978-0-444-53497-2.00008-5]
21 Johnsrude IS,Giraud AL,Frackowiak RS.Functional imaging of the auditory system:the use of positron emission tomography.Audiol Neurootol 2002;7:251-276[PMID:12232496 DOI:10.1159/000064446]
22 Vanneste S,De Ridder D.Deafferentation-based pathophysiological differences in phantom sound:Tinnitus with and without hearing loss.Neuroimage 2016;129:80-94[PMID:26708013 DOI:10.1016/j.neuroimage.2015.12.002]
23 Langguth B,Landgrebe M,Frank E,Schecklmann M,Sand PG,Vielsmeier V,Hajak G,Kleinjung T.Efficacy of different protocols of transcranial magnetic stimulation for the treatment of tinnitus:Pooled analysis of two randomized controlled studies.World J Biol Psychiatry 2014;15:276-285[PMID:22909265 DOI:10.3109/15622975.2012.708438]
24 De Ridder D,Perera S,Vanneste S.State of the Art:Novel Applications for Cortical Stimulation.Neuromodulation 2017;20:206-214[PMID:28371170 DOI:10.1111/ner.12593]
25 Lee M,Kim SE,Kim WS,Han J,Kim HJ,Kim BS,Kim JY,Hong SB,Kim BG,Lee HW.Corticocortical modulation induced by 1-Hz repetitive transcranial magnetic stimulation of the temporal cortex.JClin Neurol 2013;9:75-82[PMID:23626644 DOI:10.3988/jcn.2013.9.2.75]
2 Ziai K,Moshtaghi O,Mahboubi H,Djalilian HR.Tinnitus Patients Suffering from Anxiety and Depression:A Review.Int Tinnitus J 2017;21:68-73[PMID:28723605 DOI:10.5935/0946-5448.20170013]
3 Burton H,Wineland A,Bhattacharya M,Nicklaus J,Garcia KS,Piccirillo JF.Altered networks in bothersome tinnitus:a functional connectivity study.BMC Neurosci 2012;13:3[PMID:22217183 DOI:10.1186/1471-2202-13-3]
4 Piccirillo JF,Kallogjeri D,Nicklaus J,Wineland A,Spitznagel EL,Vlassenko AG,Benzinger T,Mathews J,Garcia KS.Low-frequency repetitive transcranial magnetic stimulation to the temporoparietal junction for tinnitus:four-week stimulation trial.JAMA Otolaryngol Head Neck Surg 2013;139:388-395[PMID:23599075 DOI:10.1001/jamaoto.2013.233]
5 Eggermont JJ.Pathophysiology of tinnitus.Prog Brain Res 2007;166:19-35[PMID:17956768 DOI:10.1016/S0079-6123(07)66002-6]
6 Mennemeier M,Chelette KC,Allen S,Bartel TB,Triggs W,Kimbrell T,Crew J,Munn T,Brown GJ,Dornhoffer J.Variable changes in PET activity before and after rTMS treatment for tinnitus.Laryngoscope2011;121:815-822[PMID:21287564 DOI:10.1002/lary.21425]
7 De Ridder D.Should rTMS for tinnitus be performed left-sided,ipsilaterally or contralaterally,and is it a treatment or merely investigational?Eur J Neurol 2010;17:891-892[PMID:20236176 DOI:10.1111/j.1468-1331.2010.02967.x]
8 Kleinjung T,Eichhammer P,Langguth B,Jacob P,Marienhagen J,Hajak G,Wolf SR,Strutz J.Longterm effects of repetitive transcranial magnetic stimulation(rTMS)in patients with chronic tinnitus.Otolaryngol Head Neck Surg 2005;132:566-569[PMID:15806046 DOI:10.1016/j.otohns.2004.09.134]
9 Plewnia C,Reimold M,Najib A,Reischl G,Plontke SK,Gerloff C.Moderate therapeutic efficacy of positron emission tomography-navigated repetitive transcranial magnetic stimulation for chronic tinnitus:a randomised,controlled pilot study.J Neurol Neurosurg Psychiatry 2007;78:152-156[PMID:16891384DOI:10.1136/jnnp.2006.095612]
10 Kimbrell TA,Little JT,Dunn RT,Frye MA,Greenberg BD,Wassermann EM,Repella JD,Danielson AL,Willis MW,Benson BE,Speer AM,Osuch E,George MS,Post RM.Frequency dependence of antidepressant response to left prefrontal repetitive transcranial magnetic stimulation(rTMS)as a function of baseline cerebral glucose metabolism.Biol Psychiatry 1999;46:1603-1613[PMID:10624541]
11 Marcondes RA,Sanchez TG,Kii MA,Ono CR,Buchpiguel CA,Langguth B,Marcolin MA.Repetitive transcranial magnetic stimulation improve tinnitus in normal hearing patients:a double-blind controlled,clinical and neuroimaging outcome study.Eur J Neurol 2010;17:38-44[PMID:19614962 DOI:10.1111/j.1468-1331.2009.02730.x]
12 Perrachione TK,Ghosh SS.Optimized design and analysis of sparse-sampling FMRI experiments.Front Neurosci 2013;7:55[PMID:23616742 DOI:10.3389/fnins.2013.00055]
13 Bestmann S,Ruff CC,Blankenburg F,Weiskopf N,Driver J,Rothwell JC.Mapping causal interregional influences with concurrent TMS-fMRI.Exp Brain Res 2008;191:383-402[PMID:18936922 DOI:10.1007/s00221-008-1601-8]
14 Newman CW,Sandridge SA,Jacobson GP.Psychometric adequacy of the Tinnitus Handicap Inventory(THI)for evaluating treatment outcome.J Am Acad Audiol 1998;9:153-160[PMID:9564679]
15 Zeman F,Koller M,Schecklmann M,Langguth B,Landgrebe M;TRI database study group.Tinnitus assessment by means of standardized self-report questionnaires:psychometric properties of the Tinnitus Questionnaire(TQ),the Tinnitus Handicap Inventory(THI),and their short versions in an international and multi-lingual sample.Health Qual Life Outcomes 2012;10:128[PMID:23078754 DOI:10.1186/1477-7525-10-128]
16 Rossi S,De Capua A,Ulivelli M,Bartalini S,Falzarano V,Filippone G,Passero S.Effects of repetitive transcranial magnetic stimulation on chronic tinnitus:a randomised,crossover,double blind,placebo controlled study.J Neurol Neurosurg Psychiatry 2007;78:857-863[PMID:17314192 DOI:10.1136/jnnp.2006.105007]
17 Khedr EM,Rothwell JC,Ahmed MA,El-Atar A.Effect of daily repetitive transcranial magnetic stimulation for treatment of tinnitus:comparison of different stimulus frequencies.J Neurol Neurosurg Psychiatry 2008;79:212-215[PMID:18202212 DOI:10.1136/jnnp.2007.127712]
18 Rossini PM,Burke D,Chen R,Cohen LG,Daskalakis Z,Di Iorio R,Di Lazzaro V,Ferreri F,Fitzgerald PB,George MS,Hallett M,Lefaucheur JP,Langguth B,Matsumoto H,Miniussi C,Nitsche MA,PascualLeone A,Paulus W,Rossi S,Rothwell JC,Siebner HR,Ugawa Y,Walsh V,Ziemann U.Non-invasive electrical and magnetic stimulation of the brain,spinal cord,roots and peripheral nerves:Basic principles and procedures for routine clinical and research application.An updated report from an I.F.C.N.Committee.Clin Neurophysiol 2015;126:1071-1107[PMID:25797650 DOI:10.1016/j.clinph.2015.02.001]
19 Song JJ,De Ridder D,Van de Heyning P,Vanneste S.Mapping tinnitus-related brain activation:an activation-likelihood estimation metaanalysis of PET studies.J Nucl Med 2012;53:1550-1557[PMID:22917883 DOI:10.2967/jnumed.112.102939]
20 Ko JH,Tang CC,Eidelberg D.Brain stimulation and functional imaging with fMRI and PET.Handb Clin Neurol 2013;116:77-95[PMID:24112887 DOI:10.1016/B978-0-444-53497-2.00008-5]
21 Johnsrude IS,Giraud AL,Frackowiak RS.Functional imaging of the auditory system:the use of positron emission tomography.Audiol Neurootol 2002;7:251-276[PMID:12232496 DOI:10.1159/000064446]
22 Vanneste S,De Ridder D.Deafferentation-based pathophysiological differences in phantom sound:Tinnitus with and without hearing loss.Neuroimage 2016;129:80-94[PMID:26708013 DOI:10.1016/j.neuroimage.2015.12.002]
23 Langguth B,Landgrebe M,Frank E,Schecklmann M,Sand PG,Vielsmeier V,Hajak G,Kleinjung T.Efficacy of different protocols of transcranial magnetic stimulation for the treatment of tinnitus:Pooled analysis of two randomized controlled studies.World J Biol Psychiatry 2014;15:276-285[PMID:22909265 DOI:10.3109/15622975.2012.708438]
24 De Ridder D,Perera S,Vanneste S.State of the Art:Novel Applications for Cortical Stimulation.Neuromodulation 2017;20:206-214[PMID:28371170 DOI:10.1111/ner.12593]
25 Lee M,Kim SE,Kim WS,Han J,Kim HJ,Kim BS,Kim JY,Hong SB,Kim BG,Lee HW.Corticocortical modulation induced by 1-Hz repetitive transcranial magnetic stimulation of the temporal cortex.JClin Neurol 2013;9:75-82[PMID:23626644 DOI:10.3988/jcn.2013.9.2.75]