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Efficacy and safety of transcranial magnetic stimulation on cognition in mild cognitive impairment, Alzheimer’s disease, Alzheimer’s disease-related dementias, and other cognitive disorders: a systematic review and meta-analysis

Published online by Cambridge University Press:  08 February 2024

Sandeep R. Pagali Open the ORCID record for Sandeep R. Pagali [Opens in a new window] ,
Rakesh Kumar ,
Allison M. LeMahieu ,
Michael R. Basso ,
Bradley F. Boeve ,
Paul E. Croarkin ,
Jennifer R. Geske ,
Leslie C. Hassett ,
John Huston III  and
Simon Kung
...Show all authors
Sandeep R. Pagali*
Affiliation:
Division of Hospital Internal Medicine, Mayo Clinic, Rochester, MN, USA Division of Community Internal Medicine, Geriatrics, and Palliative Care, Mayo Clinic, Rochester, MN, USA
Rakesh Kumar
Affiliation:
Department of Psychiatry and Psychology, Mayo Clinic School of Graduate Medical Education, Mayo Clinic College of Medicine and Science, Rochester, MN, USA
Allison M. LeMahieu
Affiliation:
Department of Quantitative Health Sciences, Mayo Clinic, Rochester, MN, USA
Michael R. Basso
Affiliation:
Department of Psychiatry and Psychology, Mayo Clinic, Rochester, MN, USA
Bradley F. Boeve
Affiliation:
Department of Neurology, Mayo Clinic, Rochester, MN, USA
Paul E. Croarkin
Affiliation:
Department of Psychiatry and Psychology, Mayo Clinic, Rochester, MN, USA
Jennifer R. Geske
Affiliation:
Department of Quantitative Health Sciences, Mayo Clinic, Rochester, MN, USA
Leslie C. Hassett
Affiliation:
Mayo Clinic Libraries, Mayo Clinic, Rochester, MN, USA
John Huston III
Affiliation:
Department of Radiology (Huston and Welker), Mayo Clinic, Rochester, MN, USA
Simon Kung
Affiliation:
Department of Psychiatry and Psychology, Mayo Clinic, Rochester, MN, USA
Brian N. Lundstrom
Affiliation:
Department of Neurology, Mayo Clinic, Rochester, MN, USA
Ronald C. Petersen
Affiliation:
Department of Neurology, Mayo Clinic, Rochester, MN, USA
Erik K. St. Louis
Affiliation:
Department of Neurology, Mayo Clinic, Rochester, MN, USA
Kirk M. Welker
Affiliation:
Department of Radiology (Huston and Welker), Mayo Clinic, Rochester, MN, USA
Gregory A. Worrell
Affiliation:
Department of Neurology, Mayo Clinic, Rochester, MN, USA
Alvaro Pascual-Leone
Affiliation:
Hinda and Arthur Marcus Institute for Aging Research and Deanna, Sidney Wolk Center for Memory Health, Hebrew SeniorLife, Roslindale, MA, USA Department of Neurology, Harvard Medical School, Cambridge, MA, USA
Maria I. Lapid
Affiliation:
Division of Community Internal Medicine, Geriatrics, and Palliative Care, Mayo Clinic, Rochester, MN, USA Department of Psychiatry and Psychology, Mayo Clinic, Rochester, MN, USA
*
Correspondence should be addressed to: Sandeep R. Pagali, MD, MPH, Division of Hospital Internal Medicine, Mayo Clinic, 200 First St. SW, Rochester, MN 55905, USA. E-mail: pagali.sandeep@mayo.edu.
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Abstract

Objective:

We aim to analyze the efficacy and safety of TMS on cognition in mild cognitive impairment (MCI), Alzheimer’s disease (AD), AD-related dementias, and nondementia conditions with comorbid cognitive impairment.

Design:

Systematic review, Meta-Analysis

Setting:

We searched MEDLINE, Embase, Cochrane database, APA PsycINFO, Web of Science, and Scopus from January 1, 2000, to February 9, 2023.

Participants and interventions:

RCTs, open-label, and case series studies reporting cognitive outcomes following TMS intervention were included.

Measurement:

Cognitive and safety outcomes were measured. Cochrane Risk of Bias for RCTs and MINORS (Methodological Index for Non-Randomized Studies) criteria were used to evaluate study quality. This study was registered with PROSPERO (CRD42022326423).

Results:

The systematic review included 143 studies (n = 5,800 participants) worldwide, encompassing 94 RCTs, 43 open-label prospective, 3 open-label retrospective, and 3 case series. The meta-analysis included 25 RCTs in MCI and AD. Collectively, these studies provide evidence of improved global and specific cognitive measures with TMS across diagnostic groups. Only 2 studies (among 143) reported 4 adverse events of seizures: 3 were deemed TMS unrelated and another resolved with coil repositioning. Meta-analysis showed large effect sizes on global cognition (Mini-Mental State Examination (SMD = 0.80 [0.26, 1.33], p = 0.003), Montreal Cognitive Assessment (SMD = 0.85 [0.26, 1.44], p = 0.005), Alzheimer’s Disease Assessment Scale–Cognitive Subscale (SMD = −0.96 [−1.32, −0.60], p < 0.001)) in MCI and AD, although with significant heterogeneity.

Conclusion:

The reviewed studies provide favorable evidence of improved cognition with TMS across all groups with cognitive impairment. TMS was safe and well tolerated with infrequent serious adverse events.

Keywords

cognitiondementiameta-analysisMCImild cognitive impairmentsystematic reviewTMStranscranial magnetic stimulation
Type
Review Article
Information
International Psychogeriatrics , First View , pp. 1 - 49
Copyright
© The Author(s), 2024. Published by Cambridge University Press on behalf of International Psychogeriatric Association

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Footnotes

Alvaro Pascual-Leone and Maria I. Lapid are contributing co-senior authors.

References

Abo Aoun, M. P., Meek, B., & Modirrousta, M. (2019). Cognitive profiles in major depressive disorder: Comparing remitters and non-remitters to rTMS treatment. Psychiatry Research, 279, 55–61.CrossRefGoogle ScholarPubMed
Ahmed, M. A., Darwish, E. S., Khedr, E. M., El Serogy, Y. M., & Ali, A. M. (2012). Effects of low versus high frequencies of repetitive transcranial magnetic stimulation on cognitive function and cortical excitability in Alzheimer’s dementia. Journal of Neurology, 259(1), 83–92.CrossRefGoogle ScholarPubMed
Alcalá-Lozano, R., Morelos-Santana, E., Cortés-Sotres, J. F., Garza-Villarreal, E. A., Sosa-Ortiz, A. L., & González-Olvera, J. J. (2018). Similar clinical improvement and maintenance after rTMS at 5 Hz using a simple vs. complex protocol in Alzheimer’s disease. Brain Stimulation, 11(3), 625–627.CrossRefGoogle ScholarPubMed
Antczak, J., Kowalska, K., Klimkowicz-Mrowiec, A., Wach, B., Kasprzyk, K., Banach, M., Rzeźnicka-Brzegowy, K., Kubica, J., & Słowik, A. (2018). Repetitive transcranial magnetic stimulation for the treatment of cognitive impairment in frontotemporal dementia: An open-label pilot study. Neuropsychiatric Disease and Treatment, 14, 749–755.CrossRefGoogle ScholarPubMed
Arvanitakis, Z., Shah, R. C., & Bennett, D. A. (2019). Diagnosis and management of dementia: Review. JAMA, 322(16), 1589–1599.CrossRefGoogle ScholarPubMed
Avirame, K., Stehberg, J., & Todder, D. (2016). Benefits of deep transcranial magnetic stimulation in Alzheimer disease: Case series. The Journal of ECT, 32(2), 127–133.CrossRefGoogle ScholarPubMed
Bagattini, C., Zanni, M., Barocco, F., Caffarra, P., Brignani, D., Miniussi, C., & Defanti, C. A. (2020). Enhancing cognitive training effects in Alzheimer’s disease: rTMS as an add-on treatment. Brain Stimulation, 13(6), 1655–1664.CrossRefGoogle ScholarPubMed
Barwood, C. H. S., Murdoch, B. E., Riek, S., O’Sullivan, J. D., Wong, A., Lloyd, D., Coulthard, A., & Wood, R. L. (2013). Long term language recovery subsequent to low frequency rTMS in chronic non-fluent aphasia. NeuroRehabilitation, 32(4), 915–928.CrossRefGoogle ScholarPubMed
Begemann, M. J., Brand, B. A., Ćurčić-Blake, B., Aleman, A., & Sommer, I. E. (2020). Efficacy of non-invasive brain stimulation on cognitive functioning in brain disorders: A meta-analysis. Psychological Medicine, 50(15), 2465–2486.CrossRefGoogle ScholarPubMed
Bentwich, J., Dobronevsky, E., Aichenbaum, S., Shorer, R., Peretz, R., Khaigrekht, M., Marton, R. G., & Rabey, J. M. (2011). Beneficial effect of repetitive transcranial magnetic stimulation combined with cognitive training for the treatment of Alzheimer’s disease: A proof of concept study. Journal of Neural Transmission, 118(3), 463–471.CrossRefGoogle ScholarPubMed
Birba, A., Ibanez, A., Sedeno, L., Ferrari, J., Garcia, A. M., & Zimerman, M. (2017). Non-invasive brain stimulation: A new strategy in mild cognitive impairment? Frontiers in Aging Neuroscience, 9, 16.CrossRefGoogle ScholarPubMed
Borland, E., Edgar, C., Stomrud, E., Cullen, N., Hansson, O., & Palmqvist, S. (2022). Clinically relevant changes for cognitive outcomes in preclinical and prodromal cognitive stages: Implications for clinical Alzheimer trials. Neurology, 99(11), e1142–e53.CrossRefGoogle ScholarPubMed
Brem, A.-K., Di Iorio, R., Fried, P. J., Oliveira-Maia, A. J., Marra, C., Profice, P., Quaranta, D., Schilberg, L., Atkinson, N. J., Seligson, E. E., Rossini, P. M., & Pascual-Leone, A. (2020). Corticomotor plasticity predicts clinical efficacy of combined neuromodulation and cognitive training in Alzheimer’s disease. Frontiers in Aging Neuroscience, 12, 200.CrossRefGoogle ScholarPubMed
Buchholtz, P. E., Ashkanian, M., Hjerrild, S., Hauptmann, L. K., Devantier, T. A., Jensen, P., Wissing, S., Thorgaard, M. V., Bjerager, L., Lund, J., Alrø, A. J., Speed, M. S., Brund, R. B. K., & Videbech, P. (2020). Low-frequency rTMS inhibits the anti-depressive effect of ECT. A pilot study. Acta Neuropsychiatrica, 32(6), 328–338.CrossRefGoogle ScholarPubMed
Budak, M., Bayraktaroglu, Z., & Hanoglu, L. (2023). The effects of repetitive transcranial magnetic stimulation and aerobic exercise on cognition, balance and functional brain networks in patients with Alzheimer’s disease. Cognitive Neurodynamics, 17(1), 39–61.CrossRefGoogle ScholarPubMed
Cha, B., Kim, J., Kim, J. M., Choi, J.-W., Choi, J., Kim, K., Cha, J., & Kim, M. Y. (2022). Therapeutic effect of repetitive transcranial magnetic stimulation for post-stroke vascular cognitive impairment: A prospective pilot study. Frontiers in Neurology [Electronic Resource], 13, 813597.Google ScholarPubMed
Chen, J., Chen, R., Xue, C., Qi, W., Hu, G., Xu, W., Chen, S., Rao, J., Zhang, F., & Zhang, X. (2021). Hippocampal-subregion mechanisms of repetitive transcranial magnetic stimulation causally associated with amelioration of episodic memory in amnestic mild cognitive impairment. Journal of Alzheimer’s Disease, 17, 17.Google Scholar
Chen, J., Ma, N., Hu, G., Nousayhah, A., Xue, C., Qi, W., Xu, W., Chen, S., Rao, J., Liu, W., Zhang, F., & Zhang, X. (2020). rTMS modulates precuneus-hippocampal subregion circuit in patients with subjective cognitive decline. Sedentary Life and Nutrition, 13(1), 1314–1331.Google ScholarPubMed
Chen, X., Zhang, T., Shan, X., Yang, Q., Zhang, P., Zhu, H., Jiang, F., Liu, C., Li, Y., Li, W., Xu, J., & Shen, H. (2022). High-frequency repetitive transcranial magnetic stimulation alleviates the cognitive side effects of electroconvulsive therapy in major depression. Frontiers in Psychiatry Frontiers Research Foundation, 13, 1002809.CrossRefGoogle ScholarPubMed
Chen, Y.-C., Ton That, V., Ugonna, C., Liu, Y., Nadel, L., & Chou, Y.-H. (2022). Diffusion MRI-guided theta burst stimulation enhances memory and functional connectivity along the inferior longitudinal fasciculus in mild cognitive impairment. Proceedings of the National Academy of Sciences of the United States of America, 119(21), e2113778119.CrossRefGoogle ScholarPubMed
Cheng, C.-M., Juan, C.-H., Chen, M.-H., Chang, C.-F., Lu, H. J., Su, T.-P., Lee, Y.-C., & Li, C.-T. (2016). Different forms of prefrontal theta burst stimulation for executive function of medication- resistant depression: Evidence from a randomized sham-controlled study. Progress in Neuro-psychopharmacology & Biological Psychiatry, 66, 35–40.CrossRefGoogle ScholarPubMed
Cheng, C. P. W., Wong, C. S. M., Lee, K. K., Chan, A. P. K., Yeung, J. W. F., & Chan, W. C. (2018). Effects of repetitive transcranial magnetic stimulation on improvement of cognition in elderly patients with cognitive impairment: A systematic review and meta-analysis. International Journal of Geriatric Psychiatry, 33(1), e1–e13.CrossRefGoogle ScholarPubMed
Cheng, J., Fairchild, J. K., McNerney, M. W., Noda, A., Ashford, J. W., Suppes, T., Chao, S. Z., Taylor, J., Rosen, A. C., Durazzo, T. C., Lazzeroni, l. C., & Yesavage, J. (2021). Repetitive transcranial magnetic stimulation as a treatment for veterans with cognitive impairment and multiple comorbidities. Journal of Alzheimer’s Disease, 21, 21.Google Scholar
Cheng, T.-C., Huang, S.-F., Wu, S.-Y., Lin, F.-G., Lin, W.-S., & Tsai, P.-Y. (2021). Integration of virtual reality into transcranial magnetic stimulation improves cognitive function in patients with Parkinson’s disease with cognitive impairment: A proof-of-concept study. Journal of Parkinson’s Disease, 07, 07.Google Scholar
Chu, M., Zhang, Y., Chen, J., Chen, W., Hong, Z., Zhang, Y., Yu, H., Zhang, F., Ye, X., Li, J., & Yang, Y. (2022). Efficacy of intermittent theta-burst stimulation and transcranial direct current stimulation in treatment of post-stroke cognitive impairment. Journal of Integrative Neuroscience, 21(5), 130.CrossRefGoogle ScholarPubMed
Cooper, H., Hedges, L. V., & Valentine, J. C. (2009). The handbook of research synthesis and meta-analysis (2nd ed.). Russell Sage Foundation.Google Scholar
Cotelli, M., Calabria, M., Manenti, R., Rosini, S., Zanetti, O., Cappa, S. F., & Miniussi, C. (2011). Improved language performance in Alzheimer disease following brain stimulation. Journal of Neurology, Neurosurgery, and Psychiatry, 82(7), 794–797.CrossRefGoogle ScholarPubMed
Cotelli, M., Manenti, R., Alberici, A., Brambilla, M., Cosseddu, M., Zanetti, O., Miozzo, A., Padovani, A., Miniussi, C., & Borroni, B. (2012). Prefrontal cortex rTMS enhances action naming in progressive non-fluent aphasia. European Journal of Neurology, 19(11), 1404–1412.CrossRefGoogle ScholarPubMed
Cotelli, M., Manenti, R., Cappa, S. F., Geroldi, C., Zanetti, O., Rossini, P. M., & Miniussi, C. (2006). Effect of transcranial magnetic stimulation on action naming in patients with Alzheimer disease. Archives of Neurology, 63(11), 1602–1604.CrossRefGoogle ScholarPubMed
Cotelli, M., Manenti, R., Cappa, S. F., Zanetti, O., & Miniussi, C. (2008). Transcranial magnetic stimulation improves naming in Alzheimer disease patients at different stages of cognitive decline. European Journal of Neurology, 15(12), 1286–1292.CrossRefGoogle ScholarPubMed
Cotelli, M., Manenti, R., Rosini, S., Calabria, M., Brambilla, M., Bisiacchi, P. S., Zanetti, O., & Miniussi, C. (2010). Action and object naming in physiological aging: An rTMS study. Frontiers in Aging Neuroscience, 2, 151.CrossRefGoogle ScholarPubMed
Cui, H., Ren, R., Lin, G., Zou, Y., Jiang, L., Wei, Z., Li, C., Wang, G., & Yu, J.-T. (2019). Repetitive transcranial magnetic stimulation induced hypoconnectivity within the default mode network yields cognitive improvements in amnestic mild cognitive impairment: A randomized controlled study. Journal of Alzheimer’s Disease: JAD, 69(4), 1137–1151.CrossRefGoogle ScholarPubMed
Demiroz, D., Cicek, I. E., Kurku, H., & Eren, I. (2022). Neurotrophic factor levels and cognitive functions before and after the repetitive transcranial magnetic stimulation in treatment resistant depression. Journal of the College of Physicians & Surgeons - Pakistan, 32(3), 335–339.Google ScholarPubMed
Devi, G., Voss, H. U., Levine, D., Abrassart, D., Heier, L., Halper, J., Martin, L., & Lowe, S. (2014). Open-label, short-term, repetitive transcranial magnetic stimulation in patients with Alzheimer’s disease with functional imaging correlates and literature review. American Journal of Alzheimer’s Disease and Other Dementias, 29(3), 248–255.CrossRefGoogle ScholarPubMed
Di Lorenzo, F., Motta, C., Casula, E. P., Bonnì, S., Assogna, M., Caltagirone, C., Martorana, A., & Koch, G. (2020). LTP-like cortical plasticity predicts conversion to dementia in patients with memory impairment. Brain Stimulation, 13(5), 1175–1182.CrossRefGoogle ScholarPubMed
Dong, X., Yan, L., Huang, L., Guan, X., Dong, C., Tao, H., Wang, T., Qin, X., Wan, Q., & Chen, K. (2018). Repetitive transcranial magnetic stimulation for the treatment of Alzheimer’s disease: A systematic review and meta-analysis of randomized controlled trials. PLoS One, 13(10), e0205704.CrossRefGoogle ScholarPubMed
Drumond Marra, H. L., Myczkowski, M. L., Maia Memória, C., Arnaut, D., Leite Ribeiro, P., Sardinha Mansur, C. G., Lancelote Alberto, R., Boura Bellini, B., Alves Fernandes da Silva, A., Tortella, G., Ciampi de Andrade, D., Teixeira, M. J., Forlenza, O. V., & Marcolin, M. A. (2015). Transcranial magnetic stimulation to address mild cognitive impairment in the elderly: A randomized controlled study. Behavioural Neurology, 2015, 287843–13.CrossRefGoogle ScholarPubMed
Du, X.-D., Li, Z., Yuan, N., Yin, M., Zhao, X.-L., Lv, X.-L., Zou, S.-Y., Zhang, J., Zhang, G.-Y., Li, C.-W., Pan, H., Yang, L., Wu, S.-Q., Yue, Y., Wu, Y.-X., & Zhang, X.-Y. (2022). Delayed improvements in visual memory task performance among chronic schizophrenia patients after high-frequency repetitive transcranial magnetic stimulation. World Journal of Psychiatry, 12(9), 1169–1182.CrossRefGoogle ScholarPubMed
Eliasova, I., Anderkova, L., Marecek, R., & Rektorova, I. (2014). Non-invasive brain stimulation of the right inferior frontal gyrus may improve attention in early Alzheimer’s disease: A pilot study. Journal of the Neurological Sciences, 346(1-2), 318–322.CrossRefGoogle ScholarPubMed
Esang, M., & Gupta, M. (2021). Aducanumab as a novel treatment for Alzheimer’s disease: A decade of hope, controversies, and the future. Cureus, 13(8), e17591.Google ScholarPubMed
Eshel, N., Keller, C. J., Wu, W., Jiang, J., Mills-Finnerty, C., Huemer, J., Wright, R., Fonzo, G. A., Ichikawa, N., Carreon, D., Wong, M., Yee, A., Shpigel, E., Guo, Y., McTeague, L., Maron-Katz, A., & Etkin, A. (2020). Global connectivity and local excitability changes underlie antidepressant effects of repetitive transcranial magnetic stimulation. Neuropsychopharmacology, 45(6), 1018–1025.CrossRefGoogle ScholarPubMed
Esmaeili, S., Abbasi, M. H., Malekdar, E., Joghataei, M. T., & Mehrpour, M. (2020). A pilot clinical trial of repetitive transcranial magnetic stimulation in mild cognitive impairment. Journal of Neurology Research, 10(5), 188–192.CrossRefGoogle Scholar
Esposito, S., Trojsi, F., Cirillo, G., de Stefano, M., Di Nardo, F., Siciliano, M., Caiazzo, G., Ippolito, D., Ricciardi, D., Buonanno, D., Atripaldi, D., Pepe, R., D’Alvano, G., Mangione, A., Bonavita, S., Santangelo, G., Iavarone, A., Cirillo, M., Esposito, F., Sorbi, S., & Tedeschi, G. (2022). Repetitive transcranial magnetic stimulation (rTMS) of dorsolateral prefrontal cortex may influence semantic fluency and functional connectivity in fronto-parietal network in mild cognitive impairment (MCI). Biomedicines, 10(5), 25.CrossRefGoogle ScholarPubMed
Eydi-Baygi, M., Aflakseir, A., Imani, M., Goodarzi, M. A., & Harirchian, M. H. (2022). Mindfulness-based cognitive therapy combined with repetitive transracial magnetic stimulation (rTMS) on information processing and working memory of patients with multiple sclerosis. Caspian Journal of Internal Medicine, 13(3), 607–616.Google ScholarPubMed
Fried, P. J., Santarnecchi, E., Antal, A., Bartres-Faz, D., Bestmann, S., Carpenter, L. L., Celnik, P., Edwards, D., Farzan, F., Fecteau, S., George, M. S., He, B., Kim, Y.-H., Leocani, L., Lisanby, S. H., Loo, C., Luber, B., Nitsche, M. A., Paulus, W., Rossi, S., Rossini, P. M., Rothwell, J., Sack, A. T., Thut, G., Ugawa, Y., Ziemann, U., Hallett, M., & Pascual-Leone, A. (2021). Training in the practice of noninvasive brain stimulation: Recommendations from an IFCN committee. Clinical Neurophysiology, 132(3), 819–837.CrossRefGoogle ScholarPubMed
Furtado, C. P., Hoy, K. E., Maller, J. J., Savage, G., Daskalakis, Z. J., & Fitzgerald, P. B. (2013). An investigation of medial temporal lobe changes and cognition following antidepressant response: A prospective rTMS study. Brain Stimulation, 6(3), 346–354.CrossRefGoogle ScholarPubMed
Galletly, C., Gill, S., Rigby, A., Carnell, B. L., & Clarke, P. (2016). Assessing the effects of repetitive transcranial magnetic stimulation on cognition in major depressive disorder using computerized cognitive testing. The Journal of ECT, 32(3), 169–173.CrossRefGoogle ScholarPubMed
Gandelman-Marton, R., Aichenbaum, S., Dobronevsky, E., Khaigrekht, M., & Rabey, J. M. (2017). Quantitative EEG after brain stimulation and cognitive training in alzheimer disease. Journal of Clinical Neurophysiology: Official Publication of the American Electroencephalographic Society, 34(1), 49–54.CrossRefGoogle ScholarPubMed
Gaugler, J., Bryan James, T., Reimer, J., Weuve, J., & Alzheimer’s Association (2021). 2021 Alzheimer’s disease facts and figures. Alzheimer’s Dementia, 17, 327–406.Google Scholar
Gauthier, S., Rosa-Neto, P., Morais, J., & Webster, C. (2021). World Alzheimer report 2021: Journey through the diagnosis of dementia. Alzheimer’s Disease International (p. 19).Google Scholar
Golaszewski, S., Kunz, A., Schwenker, K., Sebastianelli, L., Versace, V., Ferrazzoli, D., Saltuari, L., Trinka, E., & Nardone, R. (2021). Effects of intermittent theta burst stimulation on the clock drawing test performances in patients with Alzheimer’s disease. Brain Topography, 34(4), 461–466.CrossRefGoogle ScholarPubMed
Groiss, S. J., Netz, J., Lange, H. W., & Buetefisch, C. M. (2012). Frequency dependent effects of rTMS on motor and cognitive functions in Huntington’s disease. Basal Ganglia, 2(1), 41–48.CrossRefGoogle Scholar
Guan, H. Y., Zhao, J. M., Wang, K. Q., Su, X. R., Pan, Y. F., Guo, J. M., Jiang, L., Wang, Y. H., Liu, H. Y., Sun, S. G., Wu, H. R., Ren, Y. P., Geng, H. S., Liu, X. W., Yu, H. J., Wei, B. C., Li, X. P., Wu, H. E., Tan, S. P., Xiu, M. H., & Zhang, X. Y. (2020). High-frequency neuronavigated rTMS effect on clinical symptoms and cognitive dysfunction: A pilot double-blind, randomized controlled study in veterans with schizophrenia. Translational Psychiatry, 10(1), 79.CrossRefGoogle ScholarPubMed
Guo, Y., Dang, G., Hordacre, B., Su, X., Yan, N., Chen, S., Ren, H., Shi, X., Cai, M., Zhang, S., & Lan, X. (2021). Repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex modulates electroencephalographic functional connectivity in Alzheimer’s disease. Frontiers in Aging Neuroscience, 13, 679585.CrossRefGoogle ScholarPubMed
Guse, B., Falkai, P., Gruber, O., Whalley, H., Gibson, L., Hasan, A., Obst, K., Dechent, P., McIntosh, A., Suchan, B., & Wobrock, T. (2013). The effect of long-term high frequency repetitive transcranial magnetic stimulation on working memory in schizophrenia and healthy controls-A randomized placebo-controlled, double-blind fMRI study. Behavioural Brain Research, 237, 300–307.CrossRefGoogle ScholarPubMed
Guse, B., Falkai, P., & Wobrock, T. (2010). Cognitive effects of high-frequency repetitive transcranial magnetic stimulation: A systematic review. Journal of Neural Transmission (Vienna), 117(1), 105–122.CrossRefGoogle ScholarPubMed
Gy, R. R., López, R. I. V., J, R. G., López, M. H., Fé, A. L., G, T. C., Cñizares GómezS, S., Cón, M. A. R., F, O. C., A, O. D.., NA, A. G.. D., Cés, E. M., Hández, M. H., & Gález, O. J. (2021). Effect of transcranial magnetic stimulation as an enhancer of cognitive stimulation sessions on mild cognitive impairment: Preliminary results. Psychiatry Research, 304, 114151.CrossRefGoogle ScholarPubMed
Hanoglu, L., Toplutas, E., Saricaoglu, M., Velioglu, H. A., Yildiz, S., & Yulug, B. (2022). Therapeutic role of repetitive transcranial magnetic stimulation in Alzheimer’s and Parkinson’s disease: Electroencephalography microstate correlates. Frontiers in Neuroscience, 16, 798558.CrossRefGoogle ScholarPubMed
Hasan, A., Guse, B., Cordes, J., Wölwer, W., Winterer, G., Gaebel, W., Langguth, B., Landgrebe, M., Eichhammer, P., Frank, E., Hajak, Göran, Ohmann, C., Verde, P. E., Rietschel, M., Ahmed, R., Honer, W. G., Malchow, B., Karch, S., Schneider-Axmann, T., Falkai, P., & Wobrock, T. (2016). Cognitive effects of high-frequency rTMS in schizophrenia patients with predominant negative symptoms: Results from a multicenter randomized sham-controlled trial. Schizophrenia Bulletin, 42(3), 608–618.CrossRefGoogle ScholarPubMed
Hausmann, A., Pascual-Leone, A., Kemmler, G., Rupp, C. I., Lechner-Schoner, T., Kramer-Reinstadler, K., Walpoth, M., Mechtcheriakov, S., Conca, A., & Weiss, E. M. (2004). No deterioration of cognitive performance in an aggressive unilateral and bilateral antidepressant rTMS add-on trial. Journal of Clinical Psychiatry, 65(6), 772–782.CrossRefGoogle Scholar
He, W., Wang, J.-C., & Tsai, P.-Y. (2021). Theta burst magnetic stimulation improves Parkinson’s-related cognitive impairment: A randomised controlled study. Neurorehabilitation and Neural Repair, 35(11), 986–995.CrossRefGoogle ScholarPubMed
Hensel, A., Angermeyer, M. C., & Riedel-Heller, S. G. (2007). Measuring cognitive change in older adults: reliable change indices for the mini-mental state examination. Journal of Neurology, Neurosurgery and Psychiatry, 78(12), 1298–1303.CrossRefGoogle ScholarPubMed
Hermiller, M. S., Dave, S., Wert, S. L., VanHaerents, S., Riley, M., Weintraub, S., Mesulam, M. M., & Voss, J. L. (2022). Evidence from theta-burst stimulation that age-related de-differentiation of the hippocampal network is functional for episodic memory. Neurobiology of Aging, 109, 145–157.CrossRefGoogle ScholarPubMed
Higgins, J. P. T., & Green, S. (2011). Cochrane handbook for systematic reviews of interventions. Version, 5(1.0). The Cochrane Collaboration, pp. 243–272.Google Scholar
Hill, A. T., McModie, S., Fung, W., Hoy, K. E., Chung, S.-W., & Bertram, K. L. (2020). Impact of prefrontal intermittent theta-burst stimulation on working memory and executive function in Parkinson’s disease: A double-blind sham-controlled pilot study. Brain Research, 1726, 146506.CrossRefGoogle ScholarPubMed
Holczer, A., Németh, V. L., Vékony, T., Kocsis, K., Király, A., Kincses, Z. T., Vécsei, L., Klivényi, P., & Must, A. (2021). The effects of bilateral theta-burst stimulation on executive functions and affective symptoms in major depressive disorder. Neuroscience, 461, 130–139.CrossRefGoogle ScholarPubMed
Hopman, H. J., Choy, H. Y., Ho, W. S., Lu, H., Wang, W. H. O., & Chan, S. M. S. (2021). The effects of repetitive transcranial magnetic stimulation antidepressant response on cold cognition: A single-arm prospective longitudinal study. Neuropsychiatr, 17, 1647–1658.Google ScholarPubMed
Hou, G., Chen, Y., Zhu, H., Li, J., Song, Q., Lu, J., Han, Q., Wang, J., & Zhang, F. (2022). Cortical plasticity mechanism and efficacy prediction of repeated transcranial magnetic stimulation in the treatment of depression with continuous short bursts of rapid pulse stimulation (cTBS). Mediators of Inflammation, 2022, 5741114–13.CrossRefGoogle ScholarPubMed
Hoy, K. E., McQueen, S., Elliot, D., Herring, S. E., Maller, J. J., & Fitzgerald, P. B. (2019). A pilot investigation of repetitive transcranial magnetic stimulation for post-traumatic brain injury depression: Safety, tolerability, and efficacy. Journal of Neurotrauma, 36(13), 2092–2098.CrossRefGoogle ScholarPubMed
Hoy, K. E., Segrave, R. A., Daskalakis, Z. J., & Fitzgerald, P. B. (2012). Investigating the relationship between cognitive change and antidepressant response following rTMS: A large scale retrospective study. Brain Stimulation, 5(4), 539–546.CrossRefGoogle ScholarPubMed
Hu, X.-Y., Zhang, T., Rajah, G. B., Stone, C., Liu, L.-X., He, J.-J., Shan, L., Yang, L.-Y., Liu, P., Gao, F., Yang, Y.-Q., Wu, X.-L., Ye, C.-Q., & Chen, Y.-D. (2018). Effects of different frequencies of repetitive transcranial magnetic stimulation in stroke patients with non-fluent aphasia: a randomized, sham-controlled study. Neurological Research, 40(6), 459–465.CrossRefGoogle ScholarPubMed
Hu, Y., Jia, Y., Sun, Y., Ding, Y., Huang, Z., Liu, C., & Wang, Y. (2022). Efficacy and safety of simultaneous rTMS-tDCS over bilateral angular gyrus on neuropsychiatric symptoms in patients with moderate Alzheimer’s disease: A prospective, randomized, sham-controlled pilot study. Brain Stimulation, 15(6), 1530–1537.CrossRefGoogle ScholarPubMed
Huang, Y., Tan, Y., Hao, H., Li, J., Liu, C., Hu, Y., Wu, Y., Ding, Q., Zhou, Y., Li, Y., & Guan, Y. (2023). Treatment of primary progressive aphasia by repetitive transcranial magnetic stimulation: A randomized, double-blind, placebo-controlled study. Journal of Neural Transmission, 130(2), 111–123.CrossRefGoogle ScholarPubMed
Iriarte, I. G., & George, M. S. (2018). Transcranial magnetic stimulation (TMS) in the elderly. Current Psychiatry Reports, 20(1), 6.CrossRefGoogle ScholarPubMed
Iznak, A. F., Iznak, E. V., Damyanovich, E. V., Oleichik, I. V., Bologov, P. V., Kazachinskaya, I. I., & Medvedeva, T. I. (2015). Transcranial magnetic stimulation in combined treatment of pharmacoresistant depression: Dynamics of clinical, psychological, and EEG parameters. Human Physiology, 41(5), 503–509.CrossRefGoogle ScholarPubMed
Jagawat, T., Jagawat, S., Sandu, M., Sinha, M., & Hazari, N. (2022). A double-blind randomized sham control study to assess the effects of rTMS (repetitive transcranial magnetic stimulation) on executive functioning in treatment resistant depression. International Journal of Pharmaceutical and Clinical Research, 14(5), 328–340.Google Scholar
Jia, Y., Xu, L., Yang, K., Zhang, Y., Lv, X., Zhu, Z., Chen, Z., Zhu, Y., Wei, L., Li, X., Qian, M., Shen, Y., Hu, W., & Chen, W. (2021). Precision repetitive transcranial magnetic stimulation over the left parietal cortex improves memory in Alzheimer’s disease: A randomized, double-blind, sham-controlled study. Frontiers in Aging Neuroscience, 13, 693611.CrossRefGoogle ScholarPubMed
Jiang, W., Wu, Z., Wen, L., Sun, L., Zhou, M., Jiang, X., & Gui, Y. (2021). The efficacy of high- or low-frequency transcranial magnetic stimulation in Alzheimer’s disease patients with behavioral and psychological symptoms of dementia. Advances in Therapy, 29, 29.Google Scholar
Kayasandik, C. B., Velioglu, H. A., & Hanoglu, L. (2022). Predicting the effects of repetitive transcranial magnetic stimulation on cognitive functions in patients with Alzheimer’s disease by automated EEG analysis. Frontiers in Cellular Neuroscience, 16, 845832.CrossRefGoogle ScholarPubMed
Khedr, E. M., Mohamed, K. O., Ali, A. M., & Hasan, A. M. (2020). The effect of repetitive transcranial magnetic stimulation on cognitive impairment in Parkinson’s disease with dementia: Pilot study. Restorative Neurology and Neuroscience, 38(1), 55–66.CrossRefGoogle ScholarPubMed
Koch, G., Bonnì, S., Pellicciari, M. C., Casula, E. P., Mancini, M., Esposito, R., Ponzo, V., Picazio, S., Di Lorenzo, F., Serra, L., Motta, C., Maiella, M., Marra, C., Cercignani, M., Martorana, A., Caltagirone, C., & Bozzali, M. (2018). Transcranial magnetic stimulation of the precuneus enhances memory and neural activity in prodromal Alzheimer’s disease. Neuroimage, 169, 302–311.CrossRefGoogle ScholarPubMed
Koch, G., Casula, E. P., Bonni, S., Borghi, I., Assogna, M., Minei, M., Pellicciari, M. C., Motta, C., D’Acunto, A., Porrazzini, F., Maiella, M., Ferrari, C., Caltagirone, C., Santarnecchi, E., Bozzali, M., & Martorana, A. (2022). Precuneus magnetic stimulation for Alzheimer’s disease: a randomized, sham-controlled trial. Brain, 145(11), 3776–3786.CrossRefGoogle ScholarPubMed
Kumar, S., Zomorrodi, R., Ghazala, Z., Goodman, M. S., Blumberger, D. M., Daskalakis, Z. J., Fischer, C. E., Mulsant, B. H., Pollock, B. G., &Rajji, T. K. (2020). Effects of repetitive paired associative stimulation on brain plasticity and working memory in Alzheimer’s disease: A pilot randomized double-blind-controlled trial. International Psychogeriatrics, 35(3), 1–13.Google ScholarPubMed
Leblhuber, F., Geisler, S., Ehrlich, D., Steiner, K., Kurz, K., & Fuchs, D. (2022). High frequency repetitive transcranial magnetic stimulation improves cognitive performance parameters in patients with Alzheimer’s disease - An exploratory pilot study. Current Alzheimer Research, 09(9), 20–688.Google Scholar
Lee, J., Choi, B. H., Oh, E., Sohn, E. H., & Lee, A. Y. (2016). Treatment of Alzheimer’s disease with repetitive transcranial magnetic stimulation combined with cognitive training: A prospective, randomized, double-blind, placebo-controlled study. Journal of Clinical Neurology (Seoul, 12(1), 57–64.CrossRefGoogle ScholarPubMed
Lee, J., Sohn, E. H., Oh, E., Jeong, S.-H., Lee, A. Y., & Song, C. J. (2020). Cognitive effect of repetitive transcranial magnetic stimulation with cognitive training: Long-term mitigation neurodegenerative effects of mild Alzheimer’s disease. International Journal of Gerontology, 14(2), 133–137.Google Scholar
Leocani, L., Dalla Costa, G., Coppi, E., Santangelo, R., Pisa, M., Ferrari, L., Bernasconi, M. P., Falautano, M., Zangen, A., Magnani, G., & Comi, G. (2020). Repetitive transcranial magnetic stimulation with H-coil in Alzheimer’s disease: A double-blind, placebo-controlled pilot study. Frontiers in Neurology, 11, 614351.CrossRefGoogle ScholarPubMed
Li, H., Ma, J., Zhang, J., Shi, W.-Y., Mei, H.-N., & Xing, Y. (2021). Repetitive transcranial magnetic stimulation (rTMS) modulates thyroid hormones level and cognition in the recovery stage of stroke patients with cognitive dysfunction. Medical Science Monitor, 27, e931914.CrossRefGoogle ScholarPubMed
Li, X., Qi, G., Yu, C., Lian, G., Zheng, H., Wu, S., Yuan, T.-F., & Zhou, D. (2021). Cortical plasticity is correlated with cognitive improvement in Alzheimer’s disease patients after rTMS treatment. Brain Stimulation, 14(3), 503–510.CrossRefGoogle ScholarPubMed
Li, Y., Luo, H., Yu, Q., Yin, L., Li, K., Li, Y., & Fu, J. (2020). Cerebral functional manipulation of repetitive transcranial magnetic stimulation in cognitive impairment patients after stroke: An fMRI study. Frontiers in Neurology, 11, 977.CrossRefGoogle ScholarPubMed
Lin, Y., Jiang, W.-J., Shan, P.-Y., Lu, M., Wang, T., Li, R.-H., Zhang, N., & Ma, L. (2019). The role of repetitive transcranial magnetic stimulation (rTMS) in the treatment of cognitive impairment in patients with Alzheimer’s disease: A systematic review and meta-analysis. Journal of the Neurological Sciences, 398, 184–191.CrossRefGoogle ScholarPubMed
Lithgow, B. J., Dastgheib, Z., & Moussavi, Z. (2021). Baseline prediction of rTMS efficacy in Alzheimer patients. Psychiatry Research, 308, 114348.CrossRefGoogle ScholarPubMed
Liu, C., Han, T., Xu, Z., Liu, J., Zhang, M., Du, j., Zhou, Q., Duan, Y., Li, Y., Wang, J., Cui, D., & Wang, Y. (2021). Modulating gamma oscillations promotes brain connectivity to improve cognitive impairment. Cerebral Cortex, 9, 9.Google Scholar
Liu, M., Nie, Z.-Y., Li, R.-R., Zhang, W., Huang, L.-H., Wang, J.-Q., Xiao, W.-X., Zheng, J. C., & Li, Y.-X. (2021). Neural mechanism of repeated transcranial magnetic stimulation to enhance visual working memory in elderly individuals with subjective cognitive decline. Frontiers in Neurology, 12, 665218.CrossRefGoogle ScholarPubMed
Lu, H., Chan, S. S. M., Ma, S., Lin, C., Mok, V. C. T., Shi, L., Wang, D., Mak, A. D.‐P., & Lam, L. C. W. (2022). Clinical and radiomic features for predicting the treatment response of repetitive transcranial magnetic stimulation in major neurocognitive disorder: Results from a randomized controlled trial. Human Brain Mapping, 43(18), 5579–5592.CrossRefGoogle ScholarPubMed
Lv, T., You, S., Qin, R., Hu, Z., Ke, Z., Yao, W., Zhao, H., Xu, Y., & Bai, F. (2023). Distinct reserve capacity impacts on default-mode network in response to left angular gyrus-navigated repetitive transcranial magnetic stimulation in the prodromal Alzheimer disease. Behavioural Brain Research, 439, 114226.CrossRefGoogle ScholarPubMed
Mano, T. (2022). Application of repetitive transcranial magnetic stimulation over the dorsolateral prefrontal cortex in Alzheimer’s disease: A pilot study. Journal of Clinical Medicine, 11(3), 798.CrossRefGoogle ScholarPubMed
Margolis, S. A., Festa, E. K., Papandonatos, G. D., Korthauer, L. E., Gonsalves, M. A., Oberman, L., Heindel, W. C., & Ott, B. R. (2019). A pilot study of repetitive transcranial magnetic stimulation in primary progressive aphasia. Brain Stimulation, 12(5), 1340–1342.CrossRefGoogle ScholarPubMed
Medina, J., Norise, C., Faseyitan, O., Coslett, H. B., Turkeltaub, P. E., & Hamilton, R. H. (2012). Finding the right words: Transcranial magnetic stimulation improves discourse productivity in non-fluent aphasia after stroke. Aphasiology, 26(9), 1153–1168.CrossRefGoogle ScholarPubMed
Mittrach, M., Thünker, J., Winterer, G., Agelink, M. W., Regenbrecht, G., Arends, M., Mobascher, A., Kim, S.-J., Wölwer, W., Brinkmeyer, J., Gaebel, W., & Cordes, J. (2010). The tolerability of rTMS treatment in schizophrenia with respect to cognitive function. Pharmacopsychiatry, 43(3), 110–117.CrossRefGoogle ScholarPubMed
Moher, D., Liberati, A., Tetzlaff, J., & Altman, D. G. (2009). Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. Journal of Clinical Epidemiology, 62(10), 1006–1012.CrossRefGoogle ScholarPubMed
Myczkowski, M. L., Fernandes, A., Moreno, M., Valiengo, L., Lafer, B., Moreno, R. A., Padberg, F., Gattaz, W., & Brunoni, A. R. (2018). Cognitive outcomes of TMS treatment in bipolar depression: Safety data from a randomized controlled trial. Journal of Affective Disorders, 235, 20–26.CrossRefGoogle ScholarPubMed
Nadeau, S. E., Bowers, D., Jones, T. L., Wu, S. S., Triggs, W. J., & Heilman, K. M. (2014). Cognitive effects of treatment of depression with repetitive transcranial magnetic stimulation. Cognitive and Behavioral Neurology: Official Journal of the Society for Behavioral and Cognitive Neurology, 27(2), 77–87.CrossRefGoogle ScholarPubMed
Nardone, R., Tezzon, F., Holler, Y., Golaszewski, S., Trinka, E., & Brigo, F. (2014). Transcranial magnetic stimulation (TMS)/repetitive TMS in mild cognitive impairment and Alzheimer’s disease. Acta Neurologica Scandinavica, 129(6), 351–366.CrossRefGoogle ScholarPubMed
Neri, F., Romanella, S. M., Tomai Pitinca, M. L., Taddei, S., Monti, L., Benocci, S., Santarnecchi, E., Cappa, S. F., & Rossi, S. (2021). rTMS-induced language improvement and brain connectivity changes in logopenic/phonological variant of primary progressive Aphasia. Clinical Neurophysiology, 132(10), 2481–2484.CrossRefGoogle ScholarPubMed
Nguyen, J.-P., Suarez, A., Kemoun, G., Meignier, M., Le Saout, E., Damier, P., Nizard, J., & Lefaucheur, J.-P. (2017). Repetitive transcranial magnetic stimulation combined with cognitive training for the treatment of Alzheimer’s disease. Neurophysiologie clinique = Clinical neurophysiology, 47(1), 47–53.CrossRefGoogle ScholarPubMed
Noda, Y., Sato, A., Shichi, M., Sato, A., Fujii, K., Iwasa, M., Nagano, Y., Kitahata, R., & Osawa, R. (2022). Real world research on transcranial magnetic stimulation treatment strategies for neuropsychiatric symptoms with long-COVID in Japan. Asian Journal of Psychiatry, 81, 103438.CrossRefGoogle ScholarPubMed
Padala, P. R., Boozer, E. M., Lensing, S. Y., Parkes, C. M., Hunter, C. R., Dennis, R. A., Caceda, R., Padala, K. P., & Lanctôt, K. (2020). Neuromodulation for apathy in Alzheimer’s disease: A double-blind, randomized, sham-controlled pilot study. Journal of Alzheimer’s Disease, 77(4), 1483–1493.CrossRefGoogle ScholarPubMed
Padala, P. R., Padala, K. P., Lensing, S. Y., Jackson, A. N., Hunter, C. R., Parkes, C. M., Dennis, R. A., Bopp, M. M., Caceda, R., Mennemeier, M. S., Roberson, P. K., & Sullivan, D. H. (2018). Repetitive transcranial magnetic stimulation for apathy in mild cognitive impairment: A double-blind, randomized, sham-controlled, cross-over pilot study. Psychiatry Research, 261, 312–318.CrossRefGoogle ScholarPubMed
Pan, L., Li, X., Lu, X., Yang, Z., Meng, Y., Qie, H., Dai, C., Yu, W., Han, J., Ding, N., Wang, X., & Wang, S. (2020). Beneficial effects of repetitive transcranial magnetic stimulation on cognitive function and self-care ability in patients with non-dementia vascular cognitive impairment. International Journal of Clinical and Experimental Medicine, 13(5), 3197–3204.Google Scholar
Pandis, D., & Scarmeas, N. (2012). Seizures in Alzheimer disease: Clinical and epidemiological data. Epilepsy Currents, 12(5), 184–187.CrossRefGoogle ScholarPubMed
Petersen, R. C., Lopez, O., Armstrong, M. J., Getchius, T. S. D., Ganguli, M., Gloss, D., Gronseth, G. S., Marson, D., Pringsheim, T., Day, G. S., Sager, M., Stevens, J., & Rae-Grant, A. (2018). Practice guideline update summary: Mild cognitive impairment: Report of the guideline development, dissemination, and implementation subcommittee of the American academy of neurology. Neurology, 90(3), 126–135.CrossRefGoogle Scholar
Pitrou, I., Vasiliadis, H. M., & Hudon, C. (2022). Body mass index and cognitive decline among community-living older adults: The modifying effect of physical activity. European Review of Aging and Physical Activity, 19(1), 3.CrossRefGoogle ScholarPubMed
Pytel, V., Cabrera-Martín, M. D.N., Delgado-Álvarez, A., Ayala, J. L., Balugo, P., Delgado-Alonso, C., Yus, M., Carreras, M. D. T., Carreras, J. L., Matías-Guiu, J., & Matías-Guiu, J. A. (2021). Personalized repetitive transcranial magnetic stimulation for primary progressive aphasia. Journal of Alzheimer’s Disease, 84(1), 151–167.CrossRefGoogle ScholarPubMed
Qin, Y., Zhang, F., Zhang, M., & Zhu, W. (2022). Effects of repetitive transcranial magnetic stimulation combined with cognitive training on resting-state brain activity in Alzheimer’s disease. Neuroradiology, 35(5), 566–572.CrossRefGoogle ScholarPubMed
Rabey, J. M., & Dobronevsky, E. (2016). Repetitive transcranial magnetic stimulation (rTMS) combined with cognitive training is a safe and effective modality for the treatment of Alzheimer’s disease: Clinical experience. Journal of Neural Transmission, 123(12), 1449–1455.CrossRefGoogle ScholarPubMed
Rabey, J. M., Dobronevsky, E., Aichenbaum, S., Gonen, O., Marton, R. G., & Khaigrekht, M. (2013). Repetitive transcranial magnetic stimulation combined with cognitive training is a safe and effective modality for the treatment of Alzheimer’s disease: A randomized, double-blind study. Journal of Neural Transmission, 120(5), 813–819.CrossRefGoogle ScholarPubMed
Rektorova, I., Megova, S., Bares, M., & Rektor, I. (2005). Cognitive functioning after repetitive transcranial magnetic stimulation in patients with cerebrovascular disease without dementia: A pilot study of seven patients. Journal of the Neurological Sciences, 229-230, 157–161.CrossRefGoogle ScholarPubMed
Riley, R. D., Higgins, J. P., & Deeks, J. J. (2011). Interpretation of random effects meta-analyses. BMJ, 342(feb10 2), d549–d549.CrossRefGoogle ScholarPubMed
Rossi, S., Antal, A., Bestmann, S., Bikson, M., Brewer, C., Brockmöller, J. C., Carpenter, L. L., Cincotta, M., Chen, R., Daskalakis, J. D., Di Lazzaro, V., Fox, M. D., George, M. S., Gilbert, D., Kimiskidis, V. K., Koch, G., Ilmoniemi, R. J., Lefaucheur, J. P., Leocani, L., Lisanby, S. H., Miniussi, C., Padberg, F., Pascual-Leone, A., Paulus, W., Peterchev, A. V., Quartarone, A., Rotenberg, A., Rothwell, J., Rossini, P. M., Santarnecchi, E., Shafi, M. M., Siebner, H. R., Ugawa, Y., Wassermann, E. M., Zangen, A., Ziemann, U., & Hallett, M. (2021). Safety and recommendations for TMS use in healthy subjects and patient populations, with updates on training, ethical and regulatory issues: Expert guidelines. Clinical Neurophysiology, 132(1), 269–306.CrossRefGoogle ScholarPubMed
Rostami, R., Kazemi, R., Nasiri, Z., Ataei, S., Hadipour, A. L., & Jaafari, N. (2022). Cold cognition as predictor of treatment response to rTMS; A retrospective study on patients with unipolar and bipolar depression. Frontiers in Human Neuroscience, 16, 888472.CrossRefGoogle ScholarPubMed
Rutherford, G., Lithgow, B., & Moussavi, Z. (2015). Short and long-term effects of rTMS treatment on Alzheimer’s disease at different stages: A pilot study. Journal of Experimental Neuroscience, 9, 43–51.CrossRefGoogle Scholar
Sabbagh, M., Sadowsky, C., Tousi, B., Agronin, M. E., Alva, G., Armon, C., Bernick, C., Keegan, A. P., Karantzoulis, S., Baror, E., Ploznik, M., & Pascual-Leone, A. (2020). Effects of a combined transcranial magnetic stimulation (TMS) and cognitive training intervention in patients with Alzheimer’s disease. Alzheimer’s & Dementia, 16(4), 641–650.CrossRefGoogle ScholarPubMed
Saitoh, Y., Hosomi, K., Mano, T., Takeya, Y., Tagami, S., Mori, N., Matsugi, A., Jono, Y., Harada, H., Yamada, T., & Miyake, A. (2022). Randomized, sham-controlled, clinical trial of repetitive transcranial magnetic stimulation for patients with Alzheimer’s dementia in Japan. Frontiers in Aging Neuroscience, 14, 993306.CrossRefGoogle ScholarPubMed
Schaffer, D. R., Okhravi, H. R., & Neumann, S. A. (2020). Low-frequency transcranial magnetic stimulation (LF-TMS) in treating depression in patients with impaired cognitive functioning. Archives of Clinical Neuropsychology: The Official Journal of the National Academy of Neuropsychologists, 36, 801–814.CrossRefGoogle Scholar
Schulze-Rauschenbach, S. C., Harms, U., Schlaepfer, T. E., Maier, W., Falkai, P., & Wagner, M. (2005). Distinctive neurocognitive effects of repetitive transcranial magnetic stimulation and electroconvulsive therapy in major depression. The British Journal of Psychiatry: The Journal of Mental Science, 186, 410–416.CrossRefGoogle ScholarPubMed
Schunemann, H. J., Higgins, J. P. T., Thomas, J., Chandler, J., Cumpston, M., Li, T., Page, M. J., & Welch, V. A. (2019). Completing summary of findings tables and grading the certainty of the evidence. Cochrane Handbook for Systematic Reviews of Interventions, 375–402.CrossRefGoogle Scholar
Sedlackova, S., Rektorova, I., Fanfrdlova, Z., & Rektor, I. (2008). Neurocognitive effects of repetitive transcranial magnetic stimulation in patients with cerebrovascular disease without dementia. Journal of Psychophysiology, 22(1), 14–19.CrossRefGoogle Scholar
Shehata, H. S., Shalaby, N. M., Fahmy, E., & Esmail, E. H. (2015). Corticobasal degeneration: Clinical characteristics and multidisciplinary therapeutic approach in 26 patients. Neurological Sciences, 36(9), 1651–1657.CrossRefGoogle ScholarPubMed
Slim, K., Nini, E., Forestier, D., Kwiatkowski, F., Panis, Y., & Chipponi, J. (2003). Methodological index for non-randomized studies (minors): Development and validation of a new instrument. ANZ Journal of Surgery, 73(9), 712–716.CrossRefGoogle ScholarPubMed
Solé-Padullés, C., Bartrés-Faz, D., Junqué, C., Clemente, I. C., Molinuevo, Jé L., Bargalló, N. A., Sánchez-Aldeguer, J., Bosch, B., Falcón, C., & Valls-Solé, J. (2006). Repetitive transcranial magnetic stimulation effects on brain function and cognition among elders with memory dysfunction. A randomized sham-controlled study. Cerebral Cortex, 16(10), 1487–1493.CrossRefGoogle ScholarPubMed
Srovnalova, H., Marecek, R., Kubikova, R., & Rektorova, I. (2012). The role of the right dorsolateral prefrontal cortex in the tower of London task performance: Repetitive transcranial magnetic stimulation study in patients with Parkinson’s disease. Experimental Brain Research, 223(2), 251–257.CrossRefGoogle Scholar
Suarez Moreno, A., Nguyen, J.-P., Calmelet, A., Le Saout, E., Damier, P., de Decker, L., Malineau, C., Nizard, J., Canoui-Poitrine, F., & Lefaucheur, J.-P. (2022). Multi-site rTMS with cognitive training improves apathy in the long term in Alzheimer’s disease: A 4-year chart review. Clinical Neurophysiology, 137, 75–83.CrossRefGoogle Scholar
Tao, Y., Lei, B., Zhu, Y., Fang, X., Liao, L., Chen, D., & Gao, C. (2022). Repetitive transcranial magnetic stimulation decreases serum amyloid-beta and increases ectodomain of p75 neurotrophin receptor in patients with Alzheimer’s disease. Journal of Integrative Neuroscience, 21(5), 140.CrossRefGoogle ScholarPubMed
Targa Dias Anastacio, H., Matosin, N., & Ooi, L. (2022). Neuronal hyperexcitability in Alzheimer’s disease: What are the drivers behind this aberrant phenotype? Translational Psychiatry, 12(1), 257.CrossRefGoogle ScholarPubMed
Teselink, J., Bawa, K. K., Koo, G. K. Y., Sankhe, K., Liu, C. S., Rapoport, M., Oh, P., Marzolini, S., Gallagher, D., Swardfager, W., Herrmann, N., & Lanctôt, K. L. (2021). Efficacy of non-invasive brain stimulation on global cognition and neuropsychiatric symptoms in Alzheimer’s disease and mild cognitive impairment: A meta-analysis and systematic review. Ageing Research Reviews, 72, 101499.CrossRefGoogle ScholarPubMed
Teti Mayer, J., Masse, C., Chopard, G., Nicolier, M., Bereau, M., Magnin, E., Monnin, J., Tio, G., Haffen, E., Vandel, P., & Bennabi, D. (2021). Repetitive transcranial magnetic stimulation as an add-on treatment for cognitive impairment in Alzheimer’s disease and its impact on self-rated quality of life and caregiver’s burden. Brain Science, 11(6), 03.CrossRefGoogle ScholarPubMed
Traikapi, A., Kalli, I., Kyriakou, A., Stylianou, E., Tereza Symeou, R., Kardama, A., Panayiota Christou, Y., Phylactou, P., & Konstantinou, N. (2022). Episodic memory effects of gamma frequency precuneus transcranial magnetic stimulation in Alzheimer’s disease: A randomized multiple baseline study. Journal of Neuropsychology, 09, 09.Google Scholar
Trebbastoni, A., Pichiorri, F., D’Antonio, F., Campanelli, A., Onesti, E., Ceccanti, M., de Lena, C., & Inghilleri, M. (2016). Altered cortical synaptic plasticity in response to 5-Hz repetitive transcranial magnetic stimulation as a new electrophysiological finding in amnestic mild cognitive impairment converting to Alzheimer’s disease: Results from a 4-year prospective cohort study. Frontiers in Aging Neuroscience, 7, 253.CrossRefGoogle ScholarPubMed
Trung, J., Hanganu, A., Jobert, S., Degroot, C., Mejia-Constain, B., Kibreab, M., Andrée Bruneau, M., Lafontaine, A.- L., Strafella, A., & Monchi, O. (2019). Transcranial magnetic stimulation improves cognition over time in Parkinson’s disease. Parkinsonism & Related Disorders, 66, 3–8.CrossRefGoogle ScholarPubMed
Tsai, P.-Y., Wang, C.-P., Ko, J. S., Chung, Y.-M., Chang, Y.-W., & Wang, J.-X. (2014). The persistent and broadly modulating effect of inhibitory rTMS in nonfluent aphasic patients: A sham-controlled, double-blind study. Neurorehabilitation and Neural Repair, 28(8), 779–787.CrossRefGoogle ScholarPubMed
Tsai, P. Y., Lin, W. S., Tsai, K. T., Kuo, C. Y., & Lin, P. H. (2020). High-frequency versus theta burst transcranial magnetic stimulation for the treatment of poststroke cognitive impairment in humans. Journal of Psychiatry Neuroscience, 45(4), 262–270.CrossRefGoogle ScholarPubMed
Tumasian, R. A., & Devi, G. (2021). Off-label transcranial magnetic stimulation in amnestic mild cognitive impairment and Alzheimer’s disease: A twelve-year case series in a single clinic. Brain Stimulation, 14(4), 751–753.CrossRefGoogle Scholar
Turriziani, P., Smirni, D., Mangano, G. R., Zappalà, G., Giustiniani, A., Cipolotti, L., & Oliveri, M. (2019). Low-frequency repetitive transcranial magnetic stimulation of the right dorsolateral prefrontal cortex enhances recognition memory in Alzheimer’s disease. Journal of Alzheimer’s Disease: JAD, 72(2), 613–622.CrossRefGoogle ScholarPubMed
Turriziani, P., Smirni, D., Zappalà, G., Mangano, G. R., Oliveri, M., & Cipolotti, L. (2012). Enhancing memory performance with rTMS in healthy subjects and individuals with mild cognitive impairment: The role of the right dorsolateral prefrontal cortex. Frontiers in Human Neuroscience, 6, 62.CrossRefGoogle ScholarPubMed
van Dyck, C. H., Swanson, C. J., Aisen, P., Bateman, R. J., Chen, C., Gee, M., Kanekiyo, M., Li, D., Reyderman, L., Cohen, S., Froelich, L., Katayama, S., Sabbagh, M., Vellas, M., Watson, D., Dhadda, S., Irizarry, M., Kramer, L. D., & Iwatsubo, T. (2022). Lecanemab in early Alzheimer’s disease. The New England Journal of Medicine, 388(1), 9–21.CrossRefGoogle ScholarPubMed
Vecchio, F., Quaranta, D., Miraglia, F., & Pappalettera, C. (2021). Neuronavigated magnetic stimulation combined with cognitive training for Alzheimer’s patients: An EEG graph study. Geroscience, 31, 31.Google Scholar
Velioglu, H. A., Hanoglu, L., Bayraktaroglu, Z., Toprak, G., Guler, E. M., Bektay, M. Y., Mutlu-Burnaz, O., & Yulug, B. (2021). Left lateral parietal rTMS improves cognition and modulates resting brain connectivity in patients with Alzheimer’s disease: Possible role of BDNF and oxidative stress. Neurobiology of Learning and Memory, 180, 107410.CrossRefGoogle ScholarPubMed
Watt, J. A., Veroniki, A. A., Tricco, A. C., & Straus, S. E. (2021). Using a distribution-based approach and systematic review methods to derive minimum clinically important differences. BMC Medical Research Methodology, 21(1), 41.CrossRefGoogle ScholarPubMed
Wei, L., Zhang, Y., Wang, J., Xu, L., Yang, K., Lv, X., Zhu, Z., Gong, Q., Hu, W., Li, X., Qian, M., Shen, Y., & Chen, W. (2022). Parietal-hippocampal rTMS improves cognitive function in Alzheimer’s disease and increases dynamic functional connectivity of default mode network. Psychiatry Research, 315, 114721.CrossRefGoogle ScholarPubMed
Wei, W., Yi, X., Wu, Z., Ruan, J., Luo, H., & Duan, X. (2021). Acute improvement in the attention network with repetitive transcranial magnetic stimulation in Parkinson’s disease. Disability and Rehabilitation, 44(25), 7958–7966.CrossRefGoogle ScholarPubMed
Wen, N., Chen, L., Miao, X., Zhang, M., Zhang, Y., Liu, J., Xu, Y., Tong, S., Tang, W., Wang, M., Liu, J., Zhou, S., Fang, X., & Zhao, K. (2021). Effects of high-frequency rTMS on negative symptoms and cognitive function in hospitalized patients with chronic schizophrenia: A double-blind, sham-controlled pilot trial. Frontiers in Psychiatry, 12, 736094.CrossRefGoogle ScholarPubMed
Wölwer, W., Lowe, A., Brinkmeyer, J. C., Streit, M., Habakuck, M., Agelink, M. W., Mobascher, A., Gaebel, W., Cordes, J. (2014). Repetitive transcranial magnetic stimulation (rTMS) improves facial affect recognition in schizophrenia. Brain Stimulation, 7(4), 559–563.CrossRefGoogle ScholarPubMed
Wu, X., Ji, G.-J., Geng, Z., Zhou, S., Yan, Y., Wei, L., Qiu, B., Tian, Y., & Wang, K. (2020). Strengthened theta-burst transcranial magnetic stimulation as an adjunctive treatment for Alzheimer’s disease: An open-label pilot study. Brain Stimulation, 13(2), 484–486.CrossRefGoogle ScholarPubMed
Wu, X., Ji, G.-J., Geng, Z., Wang, L., Yan, Y., Wu, Y., Xiao, G., Gao, L., Wei, Q., Zhou, S., Wei, L., Tian, Y., & Wang, K. (2022). Accelerated intermittent theta-burst stimulation broadly ameliorates symptoms and cognition in Alzheimer’s disease: A randomized controlled trial. Brain Stimulation, 15(1), 35–45.CrossRefGoogle ScholarPubMed
Wu, Y., Xu, W., Liu, X., Xu, Q., Tang, L., & Wu, S. (2015). Adjunctive treatment with high frequency repetitive transcranial magnetic stimulation for the behavioral and psychological symptoms of patients with Alzheimer’s disease: A randomized, double-blind, sham-controlled study. Shanghai Archives of Psychiatry, 27(5), 280–288.Google ScholarPubMed
Xiao, G., Wu, Y., Yan, Y., Gao, L., Geng, Z., Qiu, B., Zhou, S., Ji, G., Wu, X., Hu, P., & Wang, K. (2022). Optimized magnetic stimulation induced hypoconnectivity within the executive control network yields cognition improvements in Alzheimer’s patients. Frontiers in Aging Neuroscience, 14, 847223.CrossRefGoogle ScholarPubMed
Xiu, M. H., Guan, H. Y., Zhao, J. M., Wang, K. Q., Pan, Y. F., Su, X. R., Wang, Y. H., Guo, J. M., Jiang, L., Liu, H. Y., Sun, S. G., Wu, H. R., Geng, H. S., Liu, X. W., Yu, H. J., Wei, B. C., Li, X. P., Trinh, T., Tan, S. P., & Zhang, X. Y. (2020). Cognitive enhancing effect of high-frequency neuronavigated rTMS in chronic schizophrenia patients with predominant negative symptoms: A double-blind controlled 32-week follow-up study. Schizophrenia Bulletin, 46(5), 1219–1230.CrossRefGoogle ScholarPubMed
Yan, Y., Tian, M., Wang, T., Wang, X., Wang, Y., & Shi, J. (2023). Transcranial magnetic stimulation effects on cognitive enhancement in mild cognitive impairment and Alzheimer’s disease: A systematic review and meta-analysis. Frontiers in Neurology, 14, 1209205.CrossRefGoogle ScholarPubMed
Yang, Z., Sheng, X., Qin, R., Chen, H., Shao, P., Xu, H., Yao, W., Zhao, H., Xu, Y., & Bai, F. (2022). Cognitive improvement via left angular gyrus-navigated repetitive transcranial magnetic stimulation inducing the neuroplasticity of thalamic system in amnesic mild cognitive impairment patients. Journal of Alzheimer’s Disease, 86(2), 537–551.CrossRefGoogle ScholarPubMed
Yao, Q., Tang, F., Wang, Y., Yan, Y., Dong, L., Wang, T., Zhu, D., Tian, M., Lin, X., & Shi, J. (2022). Effect of cerebellum stimulation on cognitive recovery in patients with Alzheimer disease: A randomized clinical trial. Brain Stimulation, 15(4), 910–920.CrossRefGoogle ScholarPubMed
Yin, M., Liu, Y., Zhang, L., Zheng, H., Peng, L., Ai, Y., Luo, J., & Hu, X. (2020). Effects of rTMS treatment on cognitive impairment and resting-state brain activity in stroke patients: A randomized clinical trial. Frontiers in Neural Circuits, 14, 563777.CrossRefGoogle ScholarPubMed
Yingli, B., Zunke, G., Wei, C., & Shiyan, W. (2022). Cerebral activity manipulation of low-frequency repetitive transcranial magnetic stimulation in post-stroke patients with cognitive impairment. Frontiers in Neurology [Electronic Resource], 13, 951209.Google ScholarPubMed
Yu, F., Huang, Y., Chen, T., Wang, X., Guo, Y., Fang, Y., He, K., Zhu, C., Wang, K., & Zhang, L. (2022). Repetitive transcranial magnetic stimulation promotes response inhibition in patients with major depression during the stop-signal task. Journal of Psychiatric Research, 151, 427–438.CrossRefGoogle ScholarPubMed
Yuan, L.-Q., Zeng, Q., Wang, D., Wen, X.-Y., Shi, Y., Zhu, F., Chen, S.-J., & Huang, G.-Z. (2021). Neuroimaging mechanisms of high-frequency repetitive transcranial magnetic stimulation for treatment of amnestic mild cognitive impairment: A double-blind randomized sham-controlled trial. Neural Regeneration Research, 16(4), 707–713.Google ScholarPubMed
Zeng, S., Tang, C., Su, M., Luo, X., Liang, H., Yang, L., & Zhang, B. (2022). Infralow-frequency transcranial magnetic stimulation as a therapy for generalized anxiety disorder: A randomized clinical trial. Comprehensive Psychiatry, 117, 152332.CrossRefGoogle ScholarPubMed
Zhang, F., Qin, Y., Xie, L., Zheng, C., Huang, X., & Zhang, M. (2019). High-frequency repetitive transcranial magnetic stimulation combined with cognitive training improves cognitive function and cortical metabolic ratios in Alzheimer’s disease. Journal of Neural Transmission (Vienna, Austria, 126(8), 1081–1094.CrossRefGoogle ScholarPubMed
Zhang, S., Liu, L., Zhang, L., Ma, L., Wu, H., He, X., Cao, M., & Li, R. (2022). Evaluating the treatment outcomes of repetitive transcranial magnetic stimulation in patients with moderate-to-severe Alzheimer’s disease. Frontiers in Aging Neuroscience, 14, 1070535.CrossRefGoogle ScholarPubMed
Zhang, X., Ren, H., Pei, Z., Lian, C., Su, X. L., Lan, X., Chen, C., Lei, Y. H., Li, B., & Guo, Y. (2022). Dual-targeted repetitive transcranial magnetic stimulation modulates brain functional network connectivity to improve cognition in mild cognitive impairment patients. Frontiers in Physiology, 13, 1066290.CrossRefGoogle ScholarPubMed
Zhao, J., Li, Z., Cong, Y., Zhang, J., Tan, M., Zhang, H., Geng, N., Li, M., Yu, W., & Shan, P. (2017). Repetitive transcranial magnetic stimulation improves cognitive function of Alzheimer’s disease patients. Oncotarget, 8(20), 33864–33871.CrossRefGoogle ScholarPubMed
Zhou, L., Huang, X., Li, H., Guo, R., Wang, J., Zhang, Y., & Lu, Z. (2021). Rehabilitation effect of rTMS combined with cognitive training on cognitive impairment after traumatic brain injury. American Journal of Translational Research, 13(10), 11711–11717.Google ScholarPubMed
Zhou, X., Wang, Y., Lv, S., Li, Y., Jia, S., Niu, X., & Peng, D. (2022). Transcranial magnetic stimulation for sleep disorders in Alzheimer’s disease: A double-blind, randomized, and sham-controlled pilot study. Neuroscience Letters, 766, 136337.CrossRefGoogle ScholarPubMed
Zhuo, C., Tian, H., Zhou, C., Sun, Y., Chen, X., Li, R., Chen, J., Yang, L., Li, Q., Zhang, Q., Xu, Y., & Song, X. (2022). Transcranial direct current stimulation of the occipital lobes with adjunct lithium attenuates the progression of cognitive impairment in patients with first episode schizophrenia. Frontiers in Psychiatry Frontiers Research Foundation, 13, 962918.CrossRefGoogle ScholarPubMed
Zhuo, K., Tang, Y., Song, Z., Wang, Y., Wang, J., Qian, Z., Li, H., Xiang, Q., Chen, T., Yang, Z., Xu, Y., Fan, X., Wang, J., & Liu, D. (2019). Repetitive transcranial magnetic stimulation as an adjunctive treatment for negative symptoms and cognitive impairment in patients with schizophrenia: A randomized, double-blind, sham-controlled trial. Neuropsychiatric Disease and Treatment, 15, 1141–1150.CrossRefGoogle ScholarPubMed
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