Easily Conducted Tests During the First Week Post-stroke Can Aid the Prediction of Arm Functioning at 6 Months

Emma Ghaziani, Christian Couppé, Volkert Siersma, Hanne Christensen, S Peter Magnusson, Katharina S Sunnerhagen, Hanna C Persson, Margit Alt Murphy, Emma Ghaziani, Christian Couppé, Volkert Siersma, Hanne Christensen, S Peter Magnusson, Katharina S Sunnerhagen, Hanna C Persson, Margit Alt Murphy

Abstract

Background: Prognostic models can estimate the recovery of arm functioning after stroke, guide the selection of individual training strategies, and inform patient selection in clinical trials. Several models for early prediction of arm recovery have been proposed, but their implementation has been hindered by insufficient external validation, limited evidence of their impact on patient outcomes, and reliance on predictors that are not feasible in regular clinical practice. Objectives: To determine the predictive value of new and previously reported tests that can be easily conducted in regular clinical settings for early prognosis of two levels of favorable arm recovery at 6 months post-stroke. Methods: We performed a secondary analysis of merged data (n = 223) from two Scandinavian prospective longitudinal cohorts. The candidate predictors were seven individual tests of motor function and the sensory function measured by the Fugl-Meyer Assessment of Upper Extremity within 7 days post-stroke, and the whole motor section of this assessment. For each candidate predictor, we calculated the adjusted odds ratio (OR) of two levels of residual motor impairment in the affected arm at 6 months post-stroke: moderate-to-mild (≥32 points on the motor section of the Fugl-Meyer Assessment of Upper Extremity, FMA-UE) and mild (FMA-UE ≥ 58 points). Results: Patients with partial shoulder abduction (OR 14.6), elbow extension (OR 15.9), and finger extension (OR 9.5) were more likely to reach FMA-UE ≥ 32. Patients with full function on all individual motor tests (OR 5.5-35.3) or partial elbow extension, pronation/supination, wrist dorsiflexion and grasping ability (OR 2.1-18.3) were more likely to achieve FMA-UE ≥ 58 compared with those with absent function. Intact sensory function (OR 2.0-2.2) and moderate motor impairment on the FMA-UE (OR 7.5) were also associated with favorable outcome. Conclusions: Easily conducted motor tests can be useful for early prediction of arm recovery. The added value of this study is the prediction of two levels of a favorable functional outcome from simple motor tests. This knowledge can be used in the development of prognostic models feasible in regular clinical settings, inform patient selection and stratification in future trials, and guide clinicians in the selection of individualized training strategies for improving arm functioning after stroke. Clinical Trial Registration: ClinicalTrials.gov: NCT02250365, NCT01115348.

Keywords: acute stroke; arm functioning; arm paresis; arm recovery; prediction; prognostic models.

Copyright © 2020 Ghaziani, Couppé, Siersma, Christensen, Magnusson, Sunnerhagen, Persson and Alt Murphy.

Figures

Figure 1
Figure 1
Flowchart of the inclusion process. ESS, the Electrical Somatosensory Stimulation trial; SALGOT, the Stroke Arm Longitudinal Study at the University of Gothenburg; FMA-UE, the motor section of the Fugl-Meyer Assessment of Upper Extremity (0–66 points).

References

    1. Feigin VL, Krishnamurthi RV, Parmar P, Norrving B, Mensah GA, Bennett DA, et al. . Update on the global burden of ischemic and hemorrhagic stroke in 1990-2013: the GBD 2013 study. Neuroepidemiology. (2015) 45:161–76. 10.1159/000441085
    1. Lawrence ES, Coshall C, Dundas R, Stewart J, Rudd AG, Howard R, et al. . Estimates of the prevalence of acute stroke impairments and disability in a multiethnic population. Stroke. (2001) 32:1279–84. 10.1161/01.STR.32.6.1279
    1. Nakayama H, Jorgensen HS, Raaschou HO, Olsen TS. Recovery of upper extremity function in stroke patients: the Copenhagen Stroke Study. Arch Phys Med Rehabil. (1994) 75:394–8. 10.1016/0003-9993(94)90161-9
    1. Persson HC, Parziali M, Danielsson A, Sunnerhagen KS. Outcome and upper extremity function within 72 hours after first occasion of stroke in an unselected population at a stroke unit. A part of the SALGOT study. BMC Neurol. (2012) 12:162. 10.1186/1471-2377-12-162
    1. Chen CM, Tsai CC, Chung CY, Chen CL, Wu KP, Chen HC. Potential predictors for health-related quality of life in stroke patients undergoing inpatient rehabilitation. Health Qual Life Outcomes. (2015) 13:118. 10.1186/s12955-015-0314-5
    1. Sveen U, Bautz-Holter E, Sodring KM, Wyller TB, Laake K. Association between impairments, self-care ability and social activities 1 year after stroke. Disab Rehabil. (1999) 21:372–7. 10.1080/096382899297477
    1. Kwakkel G, Kollen BJ, van der Grond J, Prevo AJ. Probability of regaining dexterity in the flaccid upper limb: impact of severity of paresis and time since onset in acute stroke. Stroke. (2003) 34:2181–6. 10.1161/
    1. Nijland RH, van Wegen EE, Harmeling-van der Wel BC, Kwakkel G, Investigators E. Presence of finger extension and shoulder abduction within 72 hours after stroke predicts functional recovery: early prediction of functional outcome after stroke: the EPOS cohort study. Stroke. (2010) 41:745–50. 10.1161/STROKEAHA.109.572065
    1. Kwakkel G, Kollen BJ. Predicting activities after stroke: what is clinically relevant? Int J Stroke. (2013) 8:25–32. 10.1111/j.1747-4949.2012.00967.x
    1. Verheyden G, Nieuwboer A, De Wit L, Thijs V, Dobbelaere J, Devos H, et al. . Time course of trunk, arm, leg, and functional recovery after ischemic stroke. Neurorehabil Neural Repair. (2008) 22:173–9. 10.1177/1545968307305456
    1. Kwakkel G. Impact of intensity of practice after stroke: issues for consideration. Disab Rehabil. (2006) 28:823–30. 10.1080/09638280500534861
    1. Lee KB, Lim SH, Kim KH, Kim KJ, Kim YR, Chang WN, et al. . Six-month functional recovery of stroke patients: a multi-time-point study. Int J Rehabil Res. (2015) 38:173–80. 10.1097/MRR.0000000000000108
    1. van Kordelaar J, van Wegen E, Kwakkel G. Impact of time on quality of motor control of the paretic upper limb after stroke. Arch Phys Med Rehabil. (2014) 95:338–44. 10.1016/j.apmr.2013.10.006
    1. Steyerberg EW, Moons KG, van der Windt DA, Hayden JA, Perel P, Schroter S, et al. . Prognosis Research Strategy (PROGRESS) 3: prognostic model research. PLoS Med. (2013) 10:e1001381. 10.1371/journal.pmed.1001381
    1. Moons KG, Royston P, Vergouwe Y, Grobbee DE, Altman DG. Prognosis and prognostic research: what, why, and how? BMJ. (2009) 338:b375. 10.1136/bmj.b375
    1. Stinear CM, Barber PA, Petoe M, Anwar S, Byblow WD. The PREP algorithm predicts potential for upper limb recovery after stroke. Brain. (2012) 135:2527–35. 10.1093/brain/aws146
    1. Stinear CM, Byblow WD, Ackerley SJ, Smith MC, Borges VM, Barber PA. PREP2: a biomarker-based algorithm for predicting upper limb function after stroke. Ann Clin Transl Neurol. (2017) 4:811–20. 10.1002/acn3.488
    1. Persson HC, Alt Murphy M, Danielsson A, Lundgren-Nilsson A, Sunnerhagen KS. A cohort study investigating a simple, early assessment to predict upper extremity function after stroke - a part of the SALGOT study. BMC Neurol. (2015) 15:92. 10.1186/s12883-015-0349-6
    1. Winters C, Kwakkel G, Nijland R, van Wegen E. When does return of voluntary finger extension occur post-stroke? a prospective cohort study. PLoS ONE. (2016) 11:e0160528. 10.1371/journal.pone.0160528
    1. Prabhakaran S, Zarahn E, Riley C, Speizer A, Chong JY, Lazar RM, et al. . Inter-individual variability in the capacity for motor recovery after ischemic stroke. Neurorehabil Neural Repair. (2008) 22:64–71. 10.1177/1545968307305302
    1. Kwakkel G, Kollen B. Predicting improvement in the upper paretic limb after stroke: a longitudinal prospective study. Restor neurol Neurosci. (2007) 25:453–60.
    1. Snickars J, Persson HC, Sunnerhagen KS. Early clinical predictors of motor function in the upper extremity one month post-stroke. J Rehabil Med. (2017) 49:216–22. 10.2340/16501977-2205
    1. Higgins J, Mayo NE, Desrosiers J, Salbach NM, Ahmed S. Upper-limb function and recovery in the acute phase poststroke. J Rehabil Res Dev. (2005) 42:65–76. 10.1682/JRRD.2003.10.0156
    1. Winters C, van Wegen EE, Daffertshofer A, Kwakkel G. Generalizability of the proportional recovery model for the upper extremity after an ischemic stroke. Neurorehabil Neural Repair. (2015) 29:614–22. 10.1177/1545968314562115
    1. Stinear CM, Byblow WD, Ackerley SJ, Barber PA, Smith MC. Predicting recovery potential for individual stroke patients increases rehabilitation efficiency. Stroke. (2017) 48:1011–9. 10.1161/STROKEAHA.116.015790
    1. Smania N, Paolucci S, Tinazzi M, Borghero A, Manganotti P, Fiaschi A, et al. . Active finger extension: a simple movement predicting recovery of arm function in patients with acute stroke. Stroke. (2007) 38:1088–90. 10.1161/01.STR.0000258077.88064.a3
    1. Katrak P, Bowring G, Conroy P, Chilvers M, Poulos R, McNeil D. Predicting upper limb recovery after stroke: the place of early shoulder and hand movement. Arch Phys Med Rehabil. (1998) 79:758–61. 10.1016/S0003-9993(98)90352-5
    1. Gebruers N, Truijen S, Engelborghs S, De Deyn PP. Prediction of upper limb recovery, general disability, and rehabilitation status by activity measurements assessed by accelerometers or the Fugl-Meyer score in acute stroke. Am J Phys Med Rehabil. (2014) 93:245–52. 10.1097/PHM.0000000000000045
    1. Au-Yeung SS, Hui-Chan CW. Predicting recovery of dextrous hand function in acute stroke. Disab Rehabil. (2009) 31:394–401. 10.1080/09638280802061878
    1. Feys H, De Weerdt W, Nuyens G, van de Winckel A, Selz B, Kiekens C. Predicting motor recovery of the upper limb after stroke rehabilitation: value of a clinical examination. Physiother Res Int. (2000) 5:1–18. 10.1002/pri.180
    1. Koh CL, Pan SL, Jeng JS, Chen BB, Wang YH, Hsueh IP, et al. . Predicting recovery of voluntary upper extremity movement in subacute stroke patients with severe upper extremity paresis. PLoS ONE. (2015) 10:e0126857. 10.1371/journal.pone.0126857
    1. Kong KH, Chua KS, Lee J. Recovery of upper limb dexterity in patients more than 1 year after stroke: frequency, clinical correlates and predictors. NeuroRehabilitation. (2011) 28:105–11. 10.3233/NRE-2011-0639
    1. Kong KH, Lee J. Temporal recovery and predictors of upper limb dexterity in the first year of stroke: a prospective study of patients admitted to a rehabilitation centre. NeuroRehabilitation. (2013) 32:345–50. 10.3233/NRE-130854
    1. Coupar F, Pollock A, Rowe P, Weir C, Langhorne P. Predictors of upper limb recovery after stroke: a systematic review and meta-analysis. Clin Rehabil. (2012) 26:291–313. 10.1177/0269215511420305
    1. Kwah LK, Herbert RD. Prediction of walking and arm recovery after stroke: a critical review. Brain Sci. (2016) 6:53. 10.3390/brainsci6040053
    1. Harvey RL. Predictors of functional outcome following stroke. Phys Med Rehabil Clin N Am. (2015) 26:583–98. 10.1016/j.pmr.2015.07.002
    1. von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP, et al. . The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. J Clin Epidemiol. (2008) 61:344–9. 10.1016/j.jclinepi.2007.11.008
    1. Alt Murphy M, Persson HC, Danielsson A, Broeren J, Lundgren-Nilsson A, Sunnerhagen KS. SALGOT–stroke arm longitudinal study at the University of Gothenburg, prospective cohort study protocol. BMC Neurol. (2011) 11:56. 10.1186/1471-2377-11-56
    1. National Guidelines for Stroke [Nationella riktlinjer för vård vid stroke] Stockholm: National Board of Health and Welfare; Socialstyrelsen (2009). Available online at: (accessed November 5, 2019).
    1. Ghaziani E, Couppe C, Henkel C, Siersma V, Sondergaard M, Christensen H, et al. . Electrical somatosensory stimulation followed by motor training of the paretic upper limb in acute stroke: study protocol for a randomized controlled trial. Trials. (2017) 18:84. 10.1186/s13063-017-1815-9
    1. Ghaziani E. Early therapeutic management of the affected arm functioning after stroke: prediction and intervention (Ph.D. thesis). Bispebjerg Hospital's website, Copenhagen, Denmark; (2018).
    1. Ghaziani E, Couppe C, Siersma V, Sondergaard M, Christensen H, Magnusson SP. Electrical somatosensory stimulation in early rehabilitation of arm paresis after stroke: a randomized controlled trial. Neurorehabil Neural Repair. (2018) 32:899–912. 10.1177/1545968318799496
    1. Fugl-Meyer AR, Jaasko L, Leyman I, Olsson S, Steglind S. The post-stroke hemiplegic patient. 1. a method for evaluation of physical performance. Scand J Rehabil Med. (1975) 7:13–31.
    1. Pang MY, Harris JE, Eng JJ. A community-based upper-extremity group exercise program improves motor function and performance of functional activities in chronic stroke: a randomized controlled trial. Arch Phys Med Rehabil. (2006) 87:1–9. 10.1016/j.apmr.2005.08.113
    1. Alt Murphy M, Willen C, Sunnerhagen KS. Kinematic variables quantifying upper-extremity performance after stroke during reaching and drinking from a glass. Neurorehabil Neural Repair. (2011) 25:71–80. 10.1177/1545968310370748
    1. Fleming MK, Newham DJ, Roberts-Lewis SF, Sorinola IO. Self-perceived utilization of the paretic arm in chronic stroke requires high upper limb functional ability. Arch Phys Med Rehabil. (2014) 95:918–24. 10.1016/j.apmr.2014.01.009
    1. Alt Murphy M, Resteghini C, Feys P, Lamers I. An overview of systematic reviews on upper extremity outcome measures after stroke. BMC Neurol. (2015) 15:29. 10.1186/s12883-015-0292-6
    1. Gladstone DJ, Danells CJ, Black SE. The fugl-meyer assessment of motor recovery after stroke: a critical review of its measurement properties. Neurorehabil Neural Repair. (2002) 16:232–40. 10.1177/154596802401105171
    1. Thrane G, Sunnerhagen KS, Persson HC, Opheim A, Alt Murphy M. Kinematic upper extremity performance in people with near or fully recovered sensorimotor function after stroke. Physiother Theory Pract. (2018) 35:822–32. 10.1080/09593985.2018.1458929
    1. Barak S, Duncan PW. Issues in selecting outcome measures to assess functional recovery after stroke. NeuroRx. (2006) 3:505–24. 10.1016/j.nurx.2006.07.009
    1. Fugl-Meyer, Assessment - Upper Extremity (FMA-UE),. University of Gothenburg; Sahlgrenska Academy; Institute of Neuroscience and Physiology. Available online at: (updated January 4, 2019).
    1. Multicenter trial of hemodilution in ischemic stroke–background and study protocol Scandinavian Stroke Study Group. Stroke. (1985) 16:885–90. 10.1161/01.STR.16.5.885
    1. Grimby G, Borjesson M, Jonsdottir IH, Schnohr P, Thelle DS, Saltin B. The “Saltin-Grimby Physical Activity Level Scale” and its application to health research. Scand J Med Sci Sports. (2015) 25(Suppl 4):119–25. 10.1111/sms.12611
    1. Brott T, Adams HP, Jr, Olinger CP, Marler JR, Barsan WG, Biller J, et al. . Measurements of acute cerebral infarction: a clinical examination scale. Stroke. (1989) 20:864–70. 10.1161/01.STR.20.7.864
    1. Grimby G. Physical activity and muscle training in the elderly. Acta Med Scand Suppl. (1986) 711:233–7. 10.1111/j.0954-6820.1986.tb08956.x
    1. Gray LJ, Ali M, Lyden PD, Bath PM, Virtual international stroke trials archive C. Interconversion of the National Institutes of Health Stroke Scale and Scandinavian Stroke Scale in acute stroke. J Stroke Cerebrovasc Dis. (2009) 18:466–8. 10.1016/j.jstrokecerebrovasdis.2009.02.003
    1. Dufouil C, Brayne C, Clayton D. Analysis of longitudinal studies with death and drop-out: a case study. Stat Med. (2004) 23:2215–26. 10.1002/sim.1821
    1. Morecraft RJ, Herrick JL, Stilwell-Morecraft KS, Louie JL, Schroeder CM, Ottenbacher JG, et al. . Localization of arm representation in the corona radiata and internal capsule in the non-human primate. Brain. (2002) 125(Pt 1):176–98. 10.1093/brain/awf011
    1. Stinear CM, Barber PA, Smale PR, Coxon JP, Fleming MK, Byblow WD. Functional potential in chronic stroke patients depends on corticospinal tract integrity. Brain. (2007) 130(Pt 1):170–80. 10.1093/brain/awl333
    1. Ward NS, Newton JM, Swayne OB, Lee L, Thompson AJ, Greenwood RJ, et al. Motor system activation after subcortical stroke depends on corticospinal system integrity. Brain. (2006) 29(Pt 3):809–19. 10.1093/brain/awl002
    1. Smania N, Gambarin M, Tinazzi M, Picelli A, Fiaschi A, Moretto G, et al. . Are indexes of arm recovery related to daily life autonomy in patients with stroke? Eur J Phys Rehabil Med. (2009) 45:349–54.
    1. Houwink A, Nijland RH, Geurts AC, Kwakkel G. Functional recovery of the paretic upper limb after stroke: who regains hand capacity? Arch Phys Med Rehabil. (2013) 94:839–44. 10.1016/j.apmr.2012.11.031

Source: PubMed

Sponsorer og samarbeidspartnere

Medisinsk tilstand

Legemiddelintervensjoner

3
Abonnere