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Journal of Integrative Neuroscience   2019, Vol. 18 Issue (4): 377-385    DOI: 10.31083/j.jin.2019.04.1192
Original Research Previous articles | Next articles
Efficacy of remote limb ischemic conditioning on poststroke cognitive impairment
Xiaofang Feng1, 2, Lihong Huang2, Zongwen Wang3, Luojun Wang2, Xunhao Du2, Qi Wang2, Shouru Xue1, *()
1 Department of Neurology, the First Affiliated Hospital of Soochow University, Jiangsu Province, 215006, P. R. China
2 Department of Neurology, Zhabei Central Hospital, Jing'an District, Shanghai 200070, P. R. China
3 Department of Neurology, Tianyou Hospital, Tongji University, Shanghai 200331, P. R. China
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Abstract  
The impact of remote limb ischemic conditioning on post-stroke cognitive impairment was evaluated with 104 first-time patients of noncardiac ischemic stroke. During the acute phase the patients were randomized into control and remote limb ischemic conditioning groups. Both groups received standard treatment, while the remote limb ischemic conditioning group received additional remote limb ischemic conditioning treatment for 6 months. All participants underwent neuropsychological evaluation, transcranial Doppler detection, P300 event-related potential and brachial-ankle pulse wave velocity measurements, and determination of serum intercellular adhesion molecule-1 and endothelin-1 levels both at admission and 6 months poststroke. The number of cases with poststroke cognitive impairment in each group was evaluated 6 months poststroke. No statistically significant difference was found in demographic data or baseline detection indices at admission between the two groups. However, at 6 months poststroke, the remote limb ischemic conditioning group had significantly higher total Montreal Cognitive Assessment score and its domains of visuospatial and executive functioning and attention scores, significantly lower activity of daily living scale score, shorter P300 latency, and higher amplitude compared with the control group. Moreover, the middle cerebral artery, average blood flow velocity was significantly higher, while the middle cerebral artery-pulsation index, basilar artery pulsation index, and the levels of brachial-ankle pulse wave velocity, intercellular adhesion molecule-1, and endothelin-1 were significantly lower in the remote limb ischemic conditioning group compared with the control group. These results demonstrate that remote limb ischemic conditioning causes a significant improvement in cognitive domains, such as visuospatial and executive functioning and attention, and is therefore linked with reduced incidence of poststroke cognitive impairment.
Key words:  Event-related potential P300      stroke      cognitive impairment      ischemic conditioning      remote limb      vascular neurology     
Submitted:  10 October 2019      Accepted:  28 November 2019      Published:  30 December 2019     
Fund: 
2018MS11/Foundation of Municipal Health Commission of Jing'an District, Shanghai
*Corresponding Author(s):  Shouru Xue     E-mail:  xueshouru@suda.edu.cn

Cite this article: 

Xiaofang Feng, Lihong Huang, Zongwen Wang, Luojun Wang, Xunhao Du, Qi Wang, Shouru Xue. Efficacy of remote limb ischemic conditioning on poststroke cognitive impairment. Journal of Integrative Neuroscience , 2019, 18(4): 377-385.

URL: 

https://jin.imrpress.com/EN/10.31083/j.jin.2019.04.1192     OR     https://jin.imrpress.com/EN/Y2019/V18/I4/377

Armentero, M. T., Levandis, G., Bazzini, E., Cerri, S., Ghezzi, C. and Blandini, F. (2011). Adhesion molecules as potential targets for neuroprotection in a rodent model of Parkinson's disease. Neurobiology of Disease 43, 663-668.
Blackburn, D. J., Bafadhel, L., Randall, M. and Harkness, K. A. (2013). Cognitive screening in the acute stroke setting. Age Ageing 42, 113-116.
Briyal, S., Philip, T. and Gulati, A. (2011). Endothelin-A receptor antagonists prevent amyloid-β-induced increase in ETA receptor expression, oxidative sstress, and cognitive impairment. Journal of Alzheimer's Disease 23, 491-503.
Brandli, A. (2015) Remote limb ischemic preconditioning: a neuroprotective technique in rodents. Journal of Visualized Experiments, e52213.
Cavalcante, J. L., Lima, J. A., Redheuil, A. and Al-Mallah, M. H. (2011). Aortic stiffness: current understanding and future directions. Journal of the American College of Cardiology 57, 1511-1522.
Cheng, C. Y., Su, S. Y., Tang, N. Y., Ho, T. Y., Chiang, S. Y. and Hsieh, C. L. (2008). Ferulic acid provides neuroprotection against oxidative stress-related apoptosis after cerebral ischemia/reperfusion injury by inhibiting ICAM-1 mRNA expression in rats. Brain Research 1209, 136-150.
Cumming, T. B., Churilov, L., Linden, T. and Bernhardt, J. (2013). Montreal cognitive assessment and mini-mental state examination are both valid cognitive tools in stroke. Acta Neurologica Scandinavica 128, 122-129.
Deweese, J. A., May, A. G., Lipchik, E. O. and Rob, C. G. (1970). Anatomic and hemodynamic correlations in carotid artery stenosis. Stroke 1, 149-157.
England, T. J., Hedstrom, A., O'Sullivan, S., Donnelly, R., Barrett, D. A., Sarmad, S., Sprigg, N. and Bath, P. (2017). RECAST (Remote ischemic conditioning after stroke trial): a pilot randomized placebo controlled Phase II trial in acute ischemic Stroke. Stroke 48, 1412-1415.
Fabrizio, V. and Sara, M. (2011). The use of auditory event-related potentials in Alzheimer's disease diagnosis. International Journal of Alzheimer's Disease 2011, 1-7.
Fang, W., Geng, X., Deng, Y., Li, Y., Shang, E., Cen, J. and Lv, P. (2011). Platelet activating factor induces blood brain barrier permeability alteration in vitro. Journal of Neuroimmunology 230, 42-47.
Gonzalez, N. R., Connolly, M., Dusick, J. R., Bhakta, H. and Vespa, P. (2014). Phase I clinical trial for the feasibility and safety of remote ischemic conditioning for aneurysmal subarachnoid hemorrhage. Neurosurgery 75, 590-598.
He, Z., Nan, X. and Qi, S. (2017). Remote ischemic preconditioning improves the cognitive function of elderly patients following colon surgery: A randomized clinical trial. Medicine 96, e6719.
Hess, D. C., Blauenfeldt, R. A., Andersen, G., Hougaard, K. D., Hoda, M. N., Ding, Y. and Ji, X. (2015). Remote ischaemic conditioning-a new paradigm of self-protection in the brain. Nature Reviews Neurology 11, 698–710.
Hougaard, K. D., Hjort, N., Zeidler, D., Sørensen, L., Nørgaard, A., Thomsen, R. B., Jonsdottir, K., Mouridsen, K., Hansen, T. M., Cho, T. H., Nielsen, T. T., Bøtker, H. E., Østergaard, L. and Andersen, G. (2013). Remote ischemic perconditioning in thrombolysed stroke patients: randomized study of activating endogenous neuroprotection-design and MRI measurements. International Journal of Stroke 8, 141-146.
Hudetz, J. A., Patterson, K. M., Iqbal, Z., Gandhi, S. D. and Pagel, P. S. (2015). Remote ischemic preconditioning prevents deterioration of short-term postoperative cognitive function after cardiac surgery using cardiopulmonary bypass: results of a pilot investigation. Journal of Cardiothoracic and Vascular Anesthesia 29, 382-388.
Jin, X. L., Li, P. F., Zhang, C. B., Wu, J. P., Feng, X. L., Zhang, Y. and Shen, M. H. (2016). Electroacupuncture alleviates cerebral ischemia and reperfusion injury via modulation of the ERK1/2 signaling pathway. Neural Regeneration Research 11, 1090-1098.
Khan, M. B., Hoda, M. N., Vaibhav, K., Giri, S., Wang, P., Waller, J. L., Ergul, A., Dhandapani, K. M., Fagan, S. C. and Hess, D., C. (2015). Remote ischemic postconditioning: harnessing endogenous protection in a murine model of vascular cognitive impairment. Translational Stroke Research 6, 69-77.
Koch, S., Katsnelson, M., Dong, C. and Perez-Pinzon, M. (2011). Remote ischemic limb preconditioning after subarachnoid hemorrhage:a phase Ib study of safety and feasibility. Stroke 42, 1387-1391.
Kwan, A. L., Lin, C.L., Chang, C.Z,, Winardi, D., Yen, C. P., Wu, S.C., Lee, K., S., Kassell, N., F., Howng, S., L., Savage, P. and Jeng, A., Y. (2002). Oral administration of an inhibitor of endothelin-converting enzyme attenuates cerebral vasospasm following experimental subarachnoid haemorrhage in rabbits. Clinical Science 103, 414S-417S.
Masaki, T., Kimura, S., Yanagisawa, M. and Goto, K. (1991). Molecular and cellular mechanism of endothelin regulation. Implications for vascular function. Circulation 84, 1457-1468.
Meng, R., Asmaro, K., Meng, L., Liu, Y., Ma, C., Xi, C., Li, G., Ren, C., Luo, Y., Ling, F., Jia, J., Hua, Y., Wang, X., Ding, Y., Lo, E. and Ji, X. (2012). Upper limb ischemic preconditioning prevents recurrent stroke in intracranial arterial stenosis. Neurology 79, 1853-1861.
Meng, R., Ding, Y., Asmaro, K., Brogan, D., Meng, L., Sui, M., Shi, J., Duan, Y., Sun, Z., Yu, Y., Jia, J. and Ji, X. (2015). Ischemic conditioning is safe and effective for octo- and nonagenarians in stroke prevention and treatment. Neurotherapeutics 12, 667-677.
Michiels, C. (2003). Endothelial cell functions. Journal of Cellular Physiology 196, 430-443.
Najjar, S. S., Scuteri, A., Shetty, V., Wright, J. G., Muller, D. C., Fleg, J. L., Fleg, Jerome L., Spurgeon, H. P., Ferrucci, L. and Lakatta, E. G. (2008) Pulse wave velocity is an independent predictor of the longitudinal increase in systolic blood pressure and of incident hypertension in the baltimore longitudinal study of aging. Journal of the American College of Cardiology 51, 1377-1383.
Nikkola, E., Laiwalla, A., Ko, A., Alvarez, M., Connolly, M., Ooi, Y. C., Hsu, W., Bui, A., Pajukanta, P. and Gonzalez, N. R. (2015). Remote ischemic conditioning alters methylation and expression of cell cycle genes in aneurysmal subarachnoid Hemorrhage. Stroke 46, 2445-2451.
O'Sullivan, C., Duggan, J., Lyons, S., Thornton, J., Lee, M. and O'Brien, E. (2003). Hypertensive target-organ damage in the very elderly. Hypertension 42, 130-135.
Pan, J., Li, X. and Peng, Y. (2016) Remote ischemic conditioning for acute ischemic stroke: dawn in the darkness. Reviews in the Neurosciences 27, 501-510.
Parra, M. A., Ascencio, L. L., Urquina, H. F., Manes, F. and Ibáñez, A. M. (2012). P300 and neuropsychological assessment in mild cognitive impairment and Alzheimer dementia. Frontiers in Neurology 3, 172.
Pasi, M., Poggesi, A., Salvadori, E. and Pantoni, L. (2012). Post-stroke dementia and cognitive impairment. Frontiers of Neurology and Neuroscience 30, 65-69.
Pendlebury, S. T. and Rothwell, P. M. (2009). Prevalence, incidence, and factors associated with pre-stroke and post-stroke dementia: a systematic review and meta-analysis. The Lancet Neurology 8, 1006-1018.
Qu, Y., Zhuo, L. , Li, N. , Hu, Y. , Chen, W. , & Zhou, Y. , Wang, J., Tao, Q., Hu, J., Nie, X. and Zhan, S. (2015). Prevalence of post-stroke cognitive impairment in china: a community-based, cross-sectional study. Plos One 10, e0122864.
Rothwell, P. M., Howard, S. C., Dolan, E., O'Brien, E., Dobson, J. E., Dahlöf, B., Sever, P. S. and Poulter, N. R. (2010). Prognostic significance of visit-to-visit variability, maximum systolic blood pressure and episodic hypertension. Lancet 375, 895-905.
Sabayan, B., Wijsman, L. W., Foster-Dingley, J. C., Stott, D. J., Ford, I., Buckley, B. M., Sattar, N., Jukema, J. W., van Osch, M. J., van der Grond, J., van Buchem, M. A., Westendorp, R. G., de Craen, A. J. and Mooijaart, S. P. (2013). Association of visit-to-visit variability in blood pressure with cognitive function in old age: prospective cohort study. BMJ 347, f4600.
Salido, E. M., Dorfman, D., Bordone, M., Chianelli, M., González Fleitas, M. F. and Rosenstein, R. E. (2013). Global and ocular hypothermic preconditioning protect the rat retina from ischemic damage. Plos One 8, e61656.
Selnes, O. A. and Vinters, H. V. (2006). Vascular cognitive impairment. Nature Clinical Practice. Neurology 2, 538-547.
Shen, A., Yang, J., Gu, Y., Zhou, D., Sun, L., Qin, Y., Chen, J., Wang, P., Xiao, F., Zhang, L. and Cheng, C. (2008) Lipopolysaccharide-evoked activation of p38 and JNK leads to an increase in ICAM-1 expression in Schwann cells of sciatic nerves. The FEBS Journal 275, 4343-4353.
Sun, J. H., Tan, L. and Yu, J. T. (2014). Post-stroke cognitive impairment: epidemiology, mechanisms and management. Annals of Translational Medicine 2, 80.
Tidball, A. M., Neely, M. D., Chamberlin, R., Aboud, A. A., Kumar, K. K., Han, B., Bryan, M. R., Aschner, M., Ess, K. C. and Bowman, A. B. (2016). Genomic instability associated with p53 knockdown in the generation of huntington's disease human induced pluripotent stem cells. Plos One 11, e0150372.
Wang, H., Zhang, Q., Xu, Y., Bian, H., Si, C., Yan, Z. and Zhu, M. (2017a). Remote ischemic conditioning improves cognitive function during cerebral vascular injury through the induction of autophagy. Current Neurovascular Research 14, 250-257.
Wang, Y., Meng, R., Song, H., Liu, G., Hua, Y., Cui, D,, Zheng, L., Feng, W., Liebeskind, D. S., Fisher, M. and Ji, X. (2017b). Remote ischemic conditioning may improve outcomes of patients with cerebral small-vessel disease. Stroke 48, 3064-3072.
Xu, T., Gong, Z., Zhu, W. Z., Wang, J. F., Li, B., Chen, F. and Deng, X. (2011). Remote ischemic preconditioning protects neurocognitive function of rats following cerebral hypoperfusion. Medical Science Monitor 17, BR299-BR304.
Yoshida, S., Aihara, K. I., Azuma, H., Uemoto, R., Sumitomo-Ueda, Y., Yagi, S., Ikeda, Y., Iwase, T., Nishio, S., Kawano, H., Miki, J., Yamada, H., Hirata, Y., Akaike, M., Sata, M. and Matsumoto, T. (2010). Dehydroepiandrosterone sulfate is inversely associated with sex-dependent diverse carotid atherosclerosis regardless of endothelial function. Atherosclerosis 212, 310-315.
Yu, J. , Li, J. and Huang, X. (2012). The Beijing version of the montreal cognitive assessment as a brief screening tool for mild cognitive impairment: a community-based study. BMC Psychiatry 12, 156.
Yu, K. H. Cho, S. J., Oh, M. S., Jung, S., Lee, J. H., Shin, J. H., Koh, I. S., Cha, J. K., Park, J. M., Bae, H. J., Kang, Y. and Lee, B. C. (2013). Cognitive impairment evaluated with vascular cognitive impairment harmonization standards in a multicenter prospective stroke cohort in korea. Stroke 44, 786.
Zhao, L., Barlinn, K., Sharma, V. K., Tsivgoulis, G., Cava, L. F., Vasdekis, S. N., Teoh, H. L., Triantafyllou, N., Chan, B. P.L., Sharma, A., Voumvourakis, K., Stamboulis, E., Saqqur, M., Harrigan, M. R., Albright, K. C. and Alexandrov, A. V. (2011). Velocity criteria for intracranial stenosis revisited: aninternational multicenter study of transcranial Doppler and digital subtraction angiography. Stroke 42, 3429-3434.
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