The role of stroke-induced immunosuppression as a predictor of functional outcome in the neurorehabilitation setting.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
09 Apr 2024
Historique:
received: 31 01 2024
accepted: 01 04 2024
medline: 10 4 2024
pubmed: 10 4 2024
entrez: 9 4 2024
Statut: epublish

Résumé

Stroke affects the interconnection between the nervous and immune systems, leading to a down-regulation of immunity called stroke-induced immunosuppression (SII). The primary aim of this study is to investigate SII role as a predictor of functional, neurological, and motor outcomes in the neurorehabilitation setting (NRB). We conducted a prospective observational study enrolling post-acute stroke patients hospitalized for neurorehabilitation. At NRB admission (T

Identifiants

pubmed: 38594322
doi: 10.1038/s41598-024-58562-1
pii: 10.1038/s41598-024-58562-1
doi:

Banques de données

ClinicalTrials.gov
['NCT05889169']

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

8320

Subventions

Organisme : Ministero della Salute
ID : Ricerca Corrente 2022-2024

Informations de copyright

© 2024. The Author(s).

Références

Meisel, C., Schwab, J. M., Prass, K., Meisel, A. & Dirnagl, U. Central nervous system injury-induced immune deficiency syndrome. Nat. Rev. Neurosci. 6(10), 775–786. https://doi.org/10.1038/nrn1765 (2005).
doi: 10.1038/nrn1765 pubmed: 16163382
Shi, K., Wood, K., Shi, F.-D., Wang, X. & Liu, Q. Stroke-induced immunosuppression and poststroke infection. Stroke Vasc. Neurol. 3(1), 34–41. https://doi.org/10.1136/svn-2017-000123 (2018).
doi: 10.1136/svn-2017-000123 pubmed: 29600006 pmcid: 5870641
van Gemmeren, T. et al. Early post-stroke infections are associated with an impaired function of neutrophil granulocytes. J. Clin. Med. 9(3), 872. https://doi.org/10.3390/jcm9030872 (2020).
doi: 10.3390/jcm9030872 pubmed: 32209993 pmcid: 7141520
Fu, Y., Liu, Q., Anrather, J. & Shi, F. D. Immune interventions in stroke. Nat. Rev. Neurol. 11(9), 524–535. https://doi.org/10.1038/NRNEUROL.2015.144 (2015).
doi: 10.1038/NRNEUROL.2015.144 pubmed: 26303850 pmcid: 4851339
Zahorec, R. Neutrophil-to-lymphocyte ratio, past, present and future perspectives. Bratislava Med. J. 122(7), 474–488. https://doi.org/10.4149/BLL_2021_078 (2021).
doi: 10.4149/BLL_2021_078
Celikbilek, A., Ismailogullari, S. & Zararsiz, G. Neutrophil to lymphocyte ratio predicts poor prognosis in ischemic cerebrovascular disease. J. Clin. Lab. Anal. 28(1), 27–31. https://doi.org/10.1002/jcla.21639 (2014).
doi: 10.1002/jcla.21639 pubmed: 24375839
Ozgen, E. et al. The relationship between neutrophil/lymphocyte, monocyte/ /lymphocyte, platelet/lymphocyte ratios and clinical outcomes after ninety days in patients who were diagnosed as having acute ischemic stroke in the emergency room and underwent a mechanical throm. Bratislava Med. J. 121(09), 634–639. https://doi.org/10.4149/BLL_2020_102 (2020).
doi: 10.4149/BLL_2020_102
Giede-Jeppe, A. et al. Lymphocytopenia is an independent predictor of unfavorable functional outcome in spontaneous intracerebral hemorrhage. Stroke 47(5), 1239–1246. https://doi.org/10.1161/STROKEAHA.116.013003 (2016).
doi: 10.1161/STROKEAHA.116.013003 pubmed: 27073240
Wang, L. et al. Neutrophil to lymphocyte ratio predicts poor outcomes after acute ischemic stroke: A cohort study and systematic review. J. Neurol. Sci. 406, 116445. https://doi.org/10.1016/j.jns.2019.116445 (2019).
doi: 10.1016/j.jns.2019.116445 pubmed: 31521961
Li, W. et al. Prognostic value of neutrophil-to-lymphocyte ratio in stroke: A systematic review and meta-analysis. Front. Neurol. 12, 686983. https://doi.org/10.3389/fneur.2021.686983 (2021).
doi: 10.3389/fneur.2021.686983 pubmed: 34630275 pmcid: 8497704
Sarejloo, S. et al. Neutrophil to lymphocyte ratio and platelet to lymphocyte ratio in poststroke depression: A systematic review and meta-analysis. Dis. Markers. 2022, 1–10. https://doi.org/10.1155/2022/5911408 (2022).
doi: 10.1155/2022/5911408
Sarejloo, S. et al. Neutrophil-to-lymphocyte ratio and early neurological deterioration in stroke patients: A systematic review and meta-analysis. Biomed. Res. Int. 1–8, 2022. https://doi.org/10.1155/2022/8656864 (2022).
doi: 10.1155/2022/8656864
Zawiah, M., Hayat Khan, A., Abu Farha, R., Usman, A. & Bitar, A. N. Neutrophil-lymphocyte ratio, monocyte-lymphocyte ratio, and platelet-lymphocyte ratio in stroke-associated pneumonia: A systematic review and meta-analysis. Curr. Med. Res. Opin. 39(3), 475–482. https://doi.org/10.1080/03007995.2023.2174327 (2023).
doi: 10.1080/03007995.2023.2174327 pubmed: 36710633
Wu, B., Liu, F., Sun, G. & Wang, S. Prognostic role of dynamic neutrophil-to-lymphocyte ratio in acute ischemic stroke after reperfusion therapy: A meta-analysis. Front. Neurol. 14(1), 1118563. https://doi.org/10.3389/fneur.2023.1118563 (2023).
doi: 10.3389/fneur.2023.1118563 pubmed: 36873451 pmcid: 9978711
Brooks, S. D. et al. Admission neutrophil-lymphocyte ratio predicts 90 day outcome after endovascular stroke therapy. J. Neurointerv. Surg. 6(8), 578–658. https://doi.org/10.1136/neurintsurg-2013-010780 (2014).
doi: 10.1136/neurintsurg-2013-010780 pubmed: 24122003
Tokgoz, S., Keskin, S., Kayrak, M., Seyithanoglu, A. & Ogmegul, A. Is neutrophil/lymphocyte ratio predict to short-term mortality in acute cerebral infarct independently from infarct volume?. J. Stroke Cerebrovasc. Dis. 23(8), 2163–2168. https://doi.org/10.1016/j.jstrokecerebrovasdis.2014.04.007 (2014).
doi: 10.1016/j.jstrokecerebrovasdis.2014.04.007 pubmed: 25106834
He, L. et al. Increased neutrophil-to-lymphocyte ratio predicts the development of post-stroke infections in patients with acute ischemic stroke. BMC Neurol. 20(1), 1–7. https://doi.org/10.1186/s12883-020-01914-x (2020).
doi: 10.1186/s12883-020-01914-x
Morotti, A. et al. Lymphopenia, infectious complications, and outcome in spontaneous intracerebral hemorrhage. Neurocrit. Care. 26(2), 160–166. https://doi.org/10.1007/s12028-016-0367-2 (2017).
doi: 10.1007/s12028-016-0367-2 pubmed: 28004330 pmcid: 5336513
Westendorp, W. F., Nederkoorn, P. J., Vermeij, J. D., Dijkgraaf, M. G. & van de Beek, D. Post-stroke infection: A systematic review and meta-analysis. BMC Neurol. 11, 1–7. https://doi.org/10.1186/1471-2377-11-110 (2011).
doi: 10.1186/1471-2377-11-110
Hug, A. et al. Infarct volume is a major determiner of post-stroke immune cell function and susceptibility to infection. Stroke 40(10), 3226–3232. https://doi.org/10.1161/STROKEAHA.109.557967 (2009).
doi: 10.1161/STROKEAHA.109.557967 pubmed: 19661470
Park, M. G. et al. Lymphocyte-to-monocyte ratio on day 7 is associated with outcomes in acute ischemic stroke. Neurol. Sci. 39(2), 243–249. https://doi.org/10.1007/s10072-017-3163-7 (2018).
doi: 10.1007/s10072-017-3163-7 pubmed: 29086124
Hoffmann, S. et al. Stroke-induced immunodepression and dysphagia independently predict stroke-associated pneumonia – The PREDICT study. J. Cereb. Blood Flow Metab. 37(12), 3671–3682. https://doi.org/10.1177/0271678X16671964 (2017).
doi: 10.1177/0271678X16671964 pubmed: 27733675
Carneiro, T. et al. Admission lymphocytopenia is associated with urinary tract infection and nosocomial infections in hemorrhagic stroke. J. Stroke Cerebrovasc. Dis. 30(11), 106079. https://doi.org/10.1016/j.jstrokecerebrovasdis.2021.106079 (2021).
doi: 10.1016/j.jstrokecerebrovasdis.2021.106079 pubmed: 34488005
Urra, X. et al. Monocytes are major players in the prognosis and risk of infection after acute stroke. Stroke 40(4), 1262–1268. https://doi.org/10.1161/STROKEAHA.108.532085 (2009).
doi: 10.1161/STROKEAHA.108.532085 pubmed: 19164783
Zhang, D. P. et al. A decrease of human leucocyte antigen-DR expression on monocytes in peripheral blood predicts stroke-associated infection in critically-ill patients with acute stroke. Eur. J. Neurol. 16(4), 498–505. https://doi.org/10.1111/j.1468-1331.2008.02512.x (2009).
doi: 10.1111/j.1468-1331.2008.02512.x pubmed: 19187263
Gökhan, S. et al. Neutrophil lymphocyte ratios in stroke subtypes and transient ischemic attack. Eur. Rev. Med. Pharmacol. Sci. 17(5), 653–657 (2013).
pubmed: 23543449
Guo, Z. et al. Dynamic change of neutrophil to lymphocyte ratio and hemorrhagic transformation after thrombolysis in stroke. J. Neuroinflamm. 13(1), 1–8. https://doi.org/10.1186/s12974-016-0680-x (2016).
doi: 10.1186/s12974-016-0680-x
Pektezel, M. Y., Yilmaz, E., Arsava, E. M. & Topcuoglu, M. A. Neutrophil-to-lymphocyte ratio and response to intravenous thrombolysis in patients with acute ischemic stroke. J. Stroke Cerebrovasc. Dis. 28(7), 1853–1859. https://doi.org/10.1016/j.jstrokecerebrovasdis.2019.04.014 (2019).
doi: 10.1016/j.jstrokecerebrovasdis.2019.04.014 pubmed: 31072698
Adiguzel, A., Arsava, E. M. & Topcuoglu, M. A. Temporal course of peripheral inflammation markers and indexes following acute ischemic stroke: Prediction of mortality, functional outcome, and stroke-associated pneumonia. Neurol. Res. 44(3), 224–231. https://doi.org/10.1080/01616412.2021.1975222 (2022).
doi: 10.1080/01616412.2021.1975222 pubmed: 34514954
Mackintosh, S. Functional independence measure. Aust. J. Physiother. 55(1), 65. https://doi.org/10.1016/s0004-9514(09)70066-2 (2009).
doi: 10.1016/s0004-9514(09)70066-2 pubmed: 19226247
Pedraza, S. et al. Reliability of the ABC/2 method in determining acute infarct volume. J. Neuroimag. 22(2), 155–159. https://doi.org/10.1111/j.1552-6569.2011.00588.x (2012).
doi: 10.1111/j.1552-6569.2011.00588.x
Webb, A. J. S. et al. Accuracy of the ABC/2 score for intracerebral hemorrhage: Systematic review and analysis of MISTIE, CLEAR-IVH, and CLEAR III. Stroke 46(9), 2470–2476. https://doi.org/10.1161/STROKEAHA.114.007343 (2015).
doi: 10.1161/STROKEAHA.114.007343 pubmed: 26243227 pmcid: 4550520
Smith, C. J. et al. Diagnosis of stroke-associated pneumonia: Recommendations from the pneumonia in stroke consensus group. Stroke 46(8), 2335–2340. https://doi.org/10.1161/STROKEAHA.115.009617 (2015).
doi: 10.1161/STROKEAHA.115.009617 pubmed: 26111886
Poisson, S. N., Johnston, S. C. & Josephson, S. A. Urinary tract infections complicating stroke: Mechanisms, consequences, and possible solutions. Stroke 41(4), e180–e184. https://doi.org/10.1161/STROKEAHA.109.576413 (2010).
doi: 10.1161/STROKEAHA.109.576413 pubmed: 20167905
Panfili, Z., Metcalf, M. & Griebling, T. L. Contemporary evaluation and treatment of poststroke lower urinary tract dysfunction. Urol. Clin. N. Am. 44(3), 403–414. https://doi.org/10.1016/j.ucl.2017.04.007 (2017).
doi: 10.1016/j.ucl.2017.04.007
Stösser, S., Isakeit, J., Bode, F. J., Bode, C. & Petzold, G. C. Sepsis in patients with large vessel occlusion stroke-clinical characteristics and outcome. Front. Neurol. 13, 902809. https://doi.org/10.3389/fneur.2022.902809 (2022).
doi: 10.3389/fneur.2022.902809 pubmed: 35903123 pmcid: 9315268
Beninato, M. et al. Determination of the minimal clinically important difference in the FIM instrument in patients with stroke. Arch. Phys. Med. Rehabil. 87(1), 32–39. https://doi.org/10.1016/j.apmr.2005.08.130 (2006).
doi: 10.1016/j.apmr.2005.08.130 pubmed: 16401435
Noguchi, K., Gel, Y. R., Brunner, E. & Konietschke, F. nparLD: An R software package for the nonparametric analysis of longitudinal data in factorial experiments. J. Stat. Softw. https://doi.org/10.18637/jss.v050.i12 (2012).
doi: 10.18637/jss.v050.i12

Auteurs

Gloria Vaghi (G)

Department of Brain and Behavioral Sciences, University of Pavia, Via Mondino 2, 27100, Pavia, Italy.
Movement Analysis Research Section, IRCCS Mondino Foundation, Pavia, Italy.

Andrea Morotti (A)

Neurology Unit, Department of Clinical and Experimental Sciences, University of Brescia, Brescia, Italy.
Department of Continuity of Care and Frailty, ASST Spedali Civili, Brescia, Italy.

Elisa Maria Piella (EM)

Department of Brain and Behavioral Sciences, University of Pavia, Via Mondino 2, 27100, Pavia, Italy.
Movement Analysis Research Section, IRCCS Mondino Foundation, Pavia, Italy.

Micol Avenali (M)

Department of Brain and Behavioral Sciences, University of Pavia, Via Mondino 2, 27100, Pavia, Italy.
Movement Analysis Research Section, IRCCS Mondino Foundation, Pavia, Italy.

Daniele Martinelli (D)

Movement Analysis Research Section, IRCCS Mondino Foundation, Pavia, Italy.

Silvano Cristina (S)

Movement Analysis Research Section, IRCCS Mondino Foundation, Pavia, Italy.

Marta Allena (M)

Movement Analysis Research Section, IRCCS Mondino Foundation, Pavia, Italy.

Valentina Grillo (V)

Department of Brain and Behavioral Sciences, University of Pavia, Via Mondino 2, 27100, Pavia, Italy.
Movement Analysis Research Section, IRCCS Mondino Foundation, Pavia, Italy.

Michele Corrado (M)

Department of Brain and Behavioral Sciences, University of Pavia, Via Mondino 2, 27100, Pavia, Italy.
Movement Analysis Research Section, IRCCS Mondino Foundation, Pavia, Italy.

Federico Bighiani (F)

Department of Brain and Behavioral Sciences, University of Pavia, Via Mondino 2, 27100, Pavia, Italy.
Movement Analysis Research Section, IRCCS Mondino Foundation, Pavia, Italy.

Francescantonio Cammarota (F)

Department of Brain and Behavioral Sciences, University of Pavia, Via Mondino 2, 27100, Pavia, Italy.
Movement Analysis Research Section, IRCCS Mondino Foundation, Pavia, Italy.

Alessandro Antoniazzi (A)

Department of Brain and Behavioral Sciences, University of Pavia, Via Mondino 2, 27100, Pavia, Italy.
Movement Analysis Research Section, IRCCS Mondino Foundation, Pavia, Italy.

Federica Ferrari (F)

Department of Brain and Behavioral Sciences, University of Pavia, Via Mondino 2, 27100, Pavia, Italy.
Department of Emergency Neurology and Stroke Unit, IRCCS Mondino Foundation, Pavia, Italy.

Federico Mazzacane (F)

Department of Brain and Behavioral Sciences, University of Pavia, Via Mondino 2, 27100, Pavia, Italy.
Department of Emergency Neurology and Stroke Unit, IRCCS Mondino Foundation, Pavia, Italy.

Anna Cavallini (A)

Department of Emergency Neurology and Stroke Unit, IRCCS Mondino Foundation, Pavia, Italy.

Anna Pichiecchio (A)

Department of Brain and Behavioral Sciences, University of Pavia, Via Mondino 2, 27100, Pavia, Italy.
Neuroradiology Department, Advanced Imaging and AI Center, IRCCS Mondino Foundation, Pavia, Italy.

Elisa Rognone (E)

Neuroradiology Department, Advanced Imaging and AI Center, IRCCS Mondino Foundation, Pavia, Italy.

Luca Martinis (L)

Movement Analysis Research Section, IRCCS Mondino Foundation, Pavia, Italy.
Sports Science Unit, Department of Public Health, Experimental Medicine and Forensic Sciences, University of Pavia, Pavia, Italy.

Luca Correale (L)

Sports Science Unit, Department of Public Health, Experimental Medicine and Forensic Sciences, University of Pavia, Pavia, Italy.

Stefano Filippo Castiglia (SF)

Department of Medical and Surgical Sciences and Biotechnologies, "Sapienza" University of Rome, Latina, Italy.
Movement Analysis Laboratory, Policlinico Italia, Rome, Italy.

Dante Trabassi (D)

Department of Medical and Surgical Sciences and Biotechnologies, "Sapienza" University of Rome, Latina, Italy.

Mariano Serrao (M)

Department of Medical and Surgical Sciences and Biotechnologies, "Sapienza" University of Rome, Latina, Italy.
Movement Analysis Laboratory, Policlinico Italia, Rome, Italy.

Cristina Tassorelli (C)

Department of Brain and Behavioral Sciences, University of Pavia, Via Mondino 2, 27100, Pavia, Italy.
Movement Analysis Research Section, IRCCS Mondino Foundation, Pavia, Italy.

Roberto De Icco (R)

Department of Brain and Behavioral Sciences, University of Pavia, Via Mondino 2, 27100, Pavia, Italy. roberto.deicco@unipv.it.
Movement Analysis Research Section, IRCCS Mondino Foundation, Pavia, Italy. roberto.deicco@unipv.it.

Classifications MeSH