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vagus nerve stimulation in cerebral stroke:biological mechanisms,therapeutic modalities,clinical applications,and future directions

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Neural Regeneration Research 2024年第8期19卷 1707-1717页

作者： Li Du Xuan He Xiaoxing Xiong Xu Zhang Zhihong Jian Zhenxing Yang Department of Anesthesiology Renmin Hospital of Wuhan UniversityWuhanHubei ProvinceChina Department of Neurosurgery Renmin Hospital of Wuhan UniversityWuhanHubei ProvinceChina

Stroke is a major disorder of the central nervous system that poses a serious threat to human life and quality of life.Many stro ke victims are left with long-term neurological dysfunction,which adversely affects the well-being of the individual and the broader socioeconomic impact.Currently,poststroke brain dysfunction is a major and difficult area of treatment.vagus nerve stimulation is a Food and Drug Administration-approved exploratory treatment option for autis m,refractory depression,epilepsy,and Alzheimer’s disease.It is expected to be a novel therapeutic technique for the treatment of stroke owing to its association with multiple mechanisms such as alte ring neurotransmitters and the plasticity of central neuro ns.In animal models of acute ischemic stroke,vagus nerve stimulation has been shown to reduce infarct size,reduce post-stroke neurological damage,and improve learning and memory capacity in rats with stroke by reducing the inflammatory response,regulating bloodbrain barrier permeability,and promoting angiogenesis and neurogenesis.At present,vagus nerve stimulation includes both invasive and non-invasive vagus nerve stimulation.Clinical studies have found that invasive vagus nerve stimulation combined with rehabilitation therapy is effective in im proving upper limb motor and cognitive abilities in stroke patients.Further clinical studies have shown that non-invasive vagus nerve stimulation,including ear/ce rvical vagus nerve stimulation,can stimulate vagal projections to the central nervous system similarly to invasive vagus nerve stimulation and can have the same effect.In this paper,we first describe the multiple effects of vagus nerve stimulation in stroke,and then discuss in depth its neuroprotective mechanisms in ischemic stroke.We go on to outline the res ults of the current major clinical applications of invasive and non-invasive vagus nerve stimulation.Finally,we provide a more comprehensive evaluation of the advantages and disadvantages of different types of vagus nerve stimulation in the

关键词： cerebral stroke neuroplasticity non-invasive vagus nerve stimulation rehabilitation vagus nerve stimulation

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Research progress on the electrophysiological indicators to predict the efficacy of vagus nerve stimulation for drug-refractory epilepsy

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Acta Epileptologica 2024年第1期7卷 14-20页

作者： Guangli Li Zhenguang Li Yingting Liu Hunan University of Chinese Medicine Changsha410208Hunan ProvinceChina Epilepsy Center of Brain Hospital of Hunan Province Changsha410007Hunan ProvinceChina

vagus nerve stimulation(VNS)is an important treatment option for drug-refractory epilepsy(DRE),with well-established efficacy and safety in clinical practice for more than 20 years.However,it is very difficult to find the optimal electrophysiological indicators for the effectiveness of VNS on DRE because the mechanism of action is unknown.In this review,we provide an update of the potential applications of VNS outcomes in patients with drug-resistant epilepsy.Electroencephalographic(EEG)activity,event-related potentials,EEG synchronization levels,magnetoencephalographic,laryngeal muscle evoked potentials,and heart rate variability are potential biomarkers for VNS outcomes in people with DRE.

关键词： Electrophysiology vagus nerve stimulation Drug-refractory epilepsy Efficacy Predictive indicators Electroencephalogram Event-related potential Magnetoencephalography Aryngeal muscle evoked potential Heart rate variability

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vagus nerve stimulation protects against cerebral injury after cardiopulmonary resuscitation by inhibiting inflammation through the TLR4/NF-κB and α7nAChR/JAK2 signaling pathways

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World Journal of Emergency Medicine 2023年第6期14卷 462-470页

作者： Shuang Xu Lang Guo Weijing Shao Licai Liang Tingting Shu Yuhan Zhang He Huang Guangqi Guo Qing Zhang Peng Sun Department of Emergency Medicine Union HospitalTongji Medical CollegeHuazhong University of Science and TechnologyWuhan 430022China Department of Urology the Second Affiliated Hospital of Guangzhou University of Chinese MedicineGuangzhou 51000China Department of Emergency Medicine the Second Affiliated Hospital of Zhejiang University School of MedicineHangzhou 310009China Department of Intensive Care Unit Wuhan Hospital of Traditional Chinese MedicineWuhan 430000China Department of Intensive Care Unit Xiangyang Central HospitalAffiliated Hospital of Hubei University of Arts and ScienceXiangyang 441021China Department of Emergency General Hospital of Central Theatre Command of the Chinese People's Liberation ArmyWuhan 430070China Department of Anesthesiology Union HospitalTongji Medical CollegeHuazhong University of Science and Technology Wuhan 430022China

BACKGROUND: Our previous research proved that vagus nerve stimulation(VNS) improved the neurological outcome after cardiopulmonary resuscitation(CPR) by activating α7 nicotinic acetylcholine receptor(α7nAChR) in a rat model, but the underlying mechanism of VNS in neuroprotection after CPR remains unclear.METHODS: In vivo, we established a mouse model of cardiac arrest(CA)/CPR to observe the survival rate, and the changes in inflammatory factors and brain tissue after VNS treatment. In vitro, we examined the effects of α7nAChR agonist on ischemia/reperfusion(I/R)-induced inflammation in BV2 cells under oxygen-glucose deprivation/reoxygenation(OGD/R) conditions. We observed the changes in cell survival rate, the levels of inflammatory factors, and the expressions of α7nAChR/Janus kinase 2(JAK2) and toll-like receptor 4(TLR4)/nuclear factor-κB(NF-κB).RESULTS: In vivo, VNS preconditioning enhanced functional recovery, improved the survival rate, and reduced hippocampal CA1 cell damage, and the levels of inflammatory mediators after CA/CPR. The application of α7nAChR agonists provided similar effects against cerebral injury after the return of spontaneous circulation(ROSC), while α7nAChR antagonists reversed these neuroprotective impacts. The in vitro results mostly matched the findings in vivo. OGD/R increased the expression of tumor necrosis factor-alpha(TNF-α), TLR4 and NF-κB p65. When nicotine was added to the OGD/R model, the expression of TLR4, NF-κB p65, and TNF-α decreased, while the phosphorylation of JAK2 increased, which was prevented by preconditioning with α7nAChR or JAK2 antagonists.CONCLUSION: The neuroprotective effect of VNS correlated with the activation of α7nAChR. VNS may alleviate cerebral IR injury by inhibiting TLR4/NF-κB and activating the α7nAChR/JAK2 signaling pathway.

关键词： Cardiopulmonary resuscitation vagus nerve stimulation Inflammation Toll-like receptor 4 α7 nicotinic acetylcholine receptor

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vagus nerve stimulation is a potential treatment for ischemic stroke

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Neural Regeneration Research 2023年第4期18卷 825-831页

作者： Yi-Lin Liu San-Rong Wang Jing-Xi Ma Le-Hua Yu Gong-Wei Jia Department of Rehabilitation The Second Affiliated Hospital of Chongqing Medical UniversityChongqingChina The Second Clinical College Chongqing Medical UniversityChongqingChina Department of Neurology Chongqing General HospitalChongqingChina Chongqing Key Laboratory of Neurodegenerative Diseases ChongqingChina

Microglia are the brain’s primary innate immune cells,and they are activated and affect pro-inflammatory phenotype or regulatory phenotype after ischemic stroke.vagus nerve stimulation was shown to activate microglial phenotypic changes and exhibit neuroprotective effects in ischemia/reperfusion injury.In this study,we established rat models of ischemic stroke by occlusion of the middle cerebral artery and performed vagus nerve stimulation 30 minutes after modeling.We found that vagus nerve stimulation caused a shift from a pro-inflammatory phenotype to a regulatory phenotype in microglia in the ischemic penumbra.vagus nerve stimulation decreased the levels of pro-inflammatory phenotype markers inducible nitric oxide synthase and tumor necrosis factorαand increased the expression of regulatory phenotype markers arginase 1 and transforming growth factorβthrough activatingα7 nicotinic acetylcholine receptor expression.Additionally,α7 nicotinic acetylcholine receptor blockade reduced the inhibition of Toll-like receptor 4/nuclear factor kappa-B pathwayassociated proteins,including Toll-like receptor 4,myeloid differentiation factor 88,I kappa B alpha,and phosphorylated-I kappa B alpha,and also weakened the neuroprotective effects of vagus nerve stimulation in ischemic stroke.vagus nerve stimulation inhibited Toll-like receptor 4/nuclear factor kappa-B expression through activatingα7 nicotinic acetylcholine receptor and regulated microglial polarization after ischemic stroke,thereby playing a role in the treatment of ischemic stroke.Findings from this study confirm the mechanism underlying vagus nerve stimulation against ischemic stroke.

关键词： cerebral ischemia microglia neuroprotection nuclear factor kappa-B pro-inflammatory phenotype regulatory phenotype reperfusion Toll-like receptor 4 vagus nerve stimulation α7 nicotinic acetylcholine receptor

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Young children with multidrug-resistant epilepsy and vagus nerve stimulation responding to perampanel: A case report

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World Journal of Clinical Cases 2022年第11期10卷 3511-3517页

作者： Hua Yang Dan Yu Department of Pediatrics West China Second University HospitalSichuan UniversityChengdu 610041Sichuan ProvinceChina

BACKGROUND Perampanel(PER),a third-generation antiepileptic drug,is a selective and noncompetitiveα-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor antagonist,and has been approved for the treatment of adults and adolescents with focal epilepsy.However,there are only a few studies about the efficacy and tolerability of PER in young children with multidrug-resistant epilepsy.In this case,we aimed to share our clinical experience in this group.CASE SUMMARY A 4-year-old boy without perinatal asphyxia and familial history of epilepsy began to have ictal seizures from age 14 mo,with jerky movement of four limbs and head nodding.Abnormal multifocal discharge and background activity were recorded through electroencephalography,and no pathogenic mutation was found in the whole exome sequencing for the patient and his parents.He had received valproate,levetiracetam,topiramate,oxcarbazepine,clonazepam and lacosamide sequentially at different times,but he still had frequent seizures even after vagus nerve stimulation(VNS)implantation.He was diagnosed with idiopathic multidrug-resistant epilepsy.However,his seizure frequency was significantly reduced after PER administration in a dose-dependent manner,and better cognitive behavior was observed.In addition,the adverse reactions of anger and aggression also appeared.CONCLUSION PER is effective as add-on therapy for young children with multidrug-resistant epilepsy who have previously undergone VNS implantation.

关键词： Perampanel Young children Drug-resistant epilepsy vagus nerve stimulation Case report

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vagus nerve stimulation for Pediatric and Adult Patients with Pharmaco-resistant Epilepsy

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Chinese Medical Journal 2015年第19期128卷 2599-2604页

作者： Fan-Gang Meng Fu-Min Jia Xiao-Hui Ren Yan Ge Kai-Liang Wang Yan-Shan Ma Ming Ge Kai Zhang Wen-Han HU Xin Zhang Wei Hu Jian-Guo Zhang Department of Functional Neurosurgery Beijing Neurosurgical InstituteCapital Medical UniversityBeijing 100050China Beijing Key Laboratory of Neuromodulation Beijing Municipal Science and Technology CommissionBeijing 100050China National Engineering Laboratory for Neuromodulation School of Aerospace EngineeringTsinghua UniversityBeijing 100084China Department of Neurosurgery Beijing Tiantan HospitalCapital Medical UniversityBeijing 100050China Department of Neurosurgery Beijing Fengtai HospitalBeijing 100071China Beijing Key Laboratory of NeuromodulationBeijing Municipal Science and Technology CommissionBeijing 100050China Department of Neurology University of Florida Gainesvilie FL 32607 USA

Background：Over past two decades,vagus nerve stimulation （VNS） has been widely used and reported to alleviate seizure frequency worldwide,however,so far,only hundreds of patients with pharmaco-resistant epilepsy （PRE） have been treated with VNS in China's Mainland.The study aimed to evaluate the effectiveness of VNS for Chinese patients with PRE and compare its relationship with age cohort and gender.Methods：We retrospectively assessed the clinical outcome of 94 patients with PRE,who were treated with VNS at Beijing Fengtai Hospital and Beij ing Tiantan Hospital between November 2008 and April 2014 from our database of 106 consecutive patients.The clinical data analysis was retrospectively examined.Results：Seizure frequency significantly decreased with VNS therapy after intermittent stimulation of the vagus nerve.At last follow-up,we found McHugh classifications of Class Ⅰ in 33 patients （35.1％）,Class Ⅱ in 27 patients （28.7％）,Class Ⅲ in 20 patients （21.3％）,Class Ⅳ in 3 patients （3.2％）,and Class Ⅴ in 11 patients （l 1.7％）.Notably,8 （8.5％） patients were seizure-free while ≥50％ seizure frequency reduction occurred in as many as 60 patients （63.8％）.Furthermore,with regard to the modified Engel classification,12 patients （12.8％） were classified as Class Ⅰ,l l patients （11.7％） were classified as Class Ⅱ,37 patients （39.4％） were classified as Class Ⅲ,34 patients （36.2％） were classified as Class Ⅳ.We also found that the factors of gender or age are not associated with clinical outcome.Conclusions：This comparative study confirmed that VNS is a safe,well-tolerated,and effective treatment for Chinese PRE patients.VNS reduced the seizure frequency regardless of age or gender of studied patients.

关键词： Epilepsy Surgery Pharmaco-resistant Epilepsy vagus nerve stimulation

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Development of localized interictal epileptiform discharges following vagus nerve stimulation for lennox-gastaut syndrome: a case report

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Acta Epileptologica 2022年第4期5卷 286-291页

作者： Renli Qi Wei Wang Yaoduan Xu Zongling Shen Xin Geng Na Li Jinghui Li Hualin Yu Second Department of Neurosurgery First Affiliated Hospital of Kunming Medical UniversityKunming650032China Department of Neurosurgery The Third People’s Hospital of Honghe PrefectureGejiu661000China Department of Psychiatry First Affiliated Hospital of Kunming Medical UniversityKunming650032China Yunnan Provincial Clinical Research Center for Neurological Disease Kunming650032China

Background Lennox-gastaut syndrome(LGS)is an epileptic encephalopathy often associated with behavioral and psychiatric disorders.vagus nerve stimulation(VNS)has been approved effective for LGS treatment.Surgical resection is also an option for LGS patients with focal pathology,offering a high probability of seizure control.However,it is challenging to accurately localize the seizure focus.Case presentation The case presented here is a 19-year-old male with a 16-year history of epilepsy with comorbid severe cognitive and psychiatric disorders.He was diagnosed with LGS due to generalized slow spike-wave discharges and multiple seizure types.He was treated with VNS in 2017 at the age of 15.After that,the frequency of the short tonic seizures decreased from 4–5 times per day to 2–5 times per year,and the generalized tonic–clonic seizure pattern did not recur,which had a frequency of 2–4 times per month before the surgery.In 2019,the generalized abnormal interictal epileptiform discharges changed to be localized in the right frontal–temporal lobe at the age of 17 years(2019).Conclusions This case report suggested that the generalized epileptiform discharges evolve into localized discharges after VNS treatment,which may help reveal the primary seizure focus for resection surgery in patients with LGS.

关键词： vagus nerve stimulation Lennox-gastaut syndrome Epileptiform discharges

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Long-term follow-up of vagus nerve stimulation in drug-resistant KCNT1-related epilepsy: a case presentation

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Acta Epileptologica 2022年第4期5卷 275-280页

作者： Meng Wang Guifu Geng Yao Meng Hongwei Zhang Zaifen Gao Jianguo Shi Department of Epilepsy Center Children’s Hospital Affiliated to Shandong UniversityJinan Children’s HospitalJinan250000China Department of Functional Neurosurgery Children’s Hospital Affiliated to Shandong UniversityJinan Children’s HospitalJinan250000China

Background The KCNT1 gene encodes a Na+-activated K+channel.Gain-of-function mutations of KCNT1 lead to autosomal dominant sleep-related hypermotor epilepsy,early-onset epileptic encephalopathy,focal epilepsy and other epileptic encephalopathies.In this paper,we report a boy carrying a KCNT1 gene mutation,who presented with drug-resistant focal-onset seizures.He had decreased seizure frequency and improvement of background changes in electroencephalography(EEG)after vagus nerve stimulation(VNS).Case presentation The case was a nonverbal 9-year-old male who presented with drug-resistant focal-onset seizures since age 3 and had underwent VNS therapy for 2 years.He had hypermotor symptoms,automatism and bilateral asymmetric tonic seizures with cognitive decline and aphasis from age 3.The patient had a variety of seizure types that only occurred at night.The most common seizure type was automatisms,and ictal video EEG showed high-amplitude delta waves,followed by a fast rhythmic sharp activity in the mesial frontal and bitemporal regions.The patient was diagnosed with KCNT1-related epilepsy,epileptic encephalopathy and cognitive disorder.He was refractory to multiple anti-seizure medicines(ASM)and ketogenic diet.After VNS treatment at age 7,the frequency of seizures was reduced significantly and EEG was improved in background slowing.Conclusions Children with KCNT1-related epilepsy usually have early onset of disease,are nonverbal,and are refractory to ASM.This boy with drug-resistant KCNT1-related epilepsy showed significantly reduced seizure frequency after VNS.This report may provide reference for management of cases of KCNT1-related epilepsy.

关键词： vagus nerve stimulation KCNT1 gene Epileptic encephalopathy KCNT1-related epilepsy

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Long-term outcomes and prognosis factors of vagus nerve stimulation in patients with refractory epilepsy

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Acta Epileptologica 2022年第3期5卷 201-207页

作者： Cuiping Xu Hua Lin Jiwen Xu Xiaohua Zhang Guiliang Hao Qiang Qiang Liu Chengyun Ding Shan Wang Quanjun Zhao Xiaojun Bai Kui Chen Duanyu Ni Yongjie Li Tao Yu Yuping Wang Department of Functional Neurosurgery Xuanwu HospitalCapital Medical UniversityBeijing 100053China Department of Neurology Xuanwu HospitalCapital Medical UniversityBeijing 100053China Department of Functional Neurosurgery Renji HospitalSchool of MedicineShanghai Jiao Tong UniversityShanghai 200127China Department of Epilepsy First Affiliated HospitalGeneral Hospital of People’s Liberation ArmyBeijing 100048China Department of Neurosurgery The 306th Hospital of PLABeijing 100101China Department of Neurology Beijing Friendship HospitalBeijing 100050China

Background:vagus nerve stimulation(VNS)is an effective treatment for patients with refractory epilepsy,yet with varied predictive factors and heterogeneous long-term outcomes.Adjustment of VNS parameters is critical for obtaining favorable efficacy.In this study,we aimed to investigate the long-term outcomes and the possible predictive factors of VNS in patients with refractory epilepsy.Methods:Eighty-six patients(59 males and 27 females)who underwent VNS implantation for treatment of refractory epilepsy between May 2016 and May 2017 at five Epilepsy Centers were enrolled.The clinical data,including sex,age at epilepsy onset,VNS implantation,epilepsy duration,seizure type,MRI findings,history of neurosurgical operations,and responder rate(responders were those with≥50%seizure reduction),were analyzed.Results:Four-year follow-up data were available for 76 patients(53 males and 23 females).The mean current intensity at the last follow-up was 1.8±0.3 mA(range:0.75–2.5 mA).The mean seizure reduction was 36.2%at 6 months,38.5%at 1 year,69.4%at 3 years,and 56.7%at 4 years.A favorable outcome of≥50%reduction in seizure frequency occurred in 40.0%of the patients at 6 months,55.9%at 1 year with 4 patients being seizure-free,63.2%at 3 years with 5 patients being seizure-free,and 68.4%at 4 years with 5 patients being seizure-free.Earlier onset age(Pstimulation efficacy increases over time after implantation,and earlier exposure to VNS improves the prognosis.

关键词： Refractory epilepsy vagus nerve stimulation Generalized seizures Long-term efficacy

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Neuroprotective effects of vagus nerve stimulation on traumatic brain injury

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Neural Regeneration Research 2014年第17期9卷 1585-1591页

作者： Long Zhou Jinhuang Lin Junming Lin Guoju Kui Jianhua Zhang Yigang Yu Affiliated Dongnan Hospital of Xiamen University the 175 Hospital of Chinese PLA Trauma Neurosurgery Center of Nanjing Military Region The 73131 Corps of Chinese PLA

Previous studies have shown that vagus nerve stimulation can improve the prognosis of trau- matic brain injury. The aim of this study was to elucidate the mechanism of the neuroprotective effects of vagus nerve stimulation in rabbits with brain explosive injury. Rabbits with brain ex- plosive injury received continuous stimulation （10 V, 5 Hz, 5 ms, 20 minutes） of the right cervical vagus nerve. Tumor necrosis factor-a, interleukin-l~ and interleukin-10 concentrations were detected in serum and brain tissues, and water content in brain tissues was measured. Results showed that vagus nerve stimulation could reduce the degree of brain edema, decrease tumor necrosis factor-a and interleukin-1β concentrations, and increase interleukin-10 concentration after brain explosive injury in rabbits. These data suggest that vagus nerve stimulation may exert neuroprotective effects against explosive injury via regulating the expression of tumor necrosis factor-a, interleukin-1 β and interleukin-10 in the serum and brain tissue.

关键词： nerve regeneration brain injury vagus nerve stimulation tumor necrosis factor-a interleukin- lβ interleukin-10 brain tissue pathology protection explosive injury mechanisms hydrocephalus neural regeneration

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