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What Is the Longitudinal Profile of Impairments and Can We Predict Difficulty Caring for the Profoundly Affected Arm in the First Year Poststroke?

Open AccessPublished:August 30, 2017DOI:https://doi.org/10.1016/j.apmr.2017.07.016

      Abstract

      Objectives

      To establish the longitudinal profile of impairments of body functions and activity limitations of the arm, and to evaluate potential predictors of difficulty caring for the profoundly affected arm poststroke.

      Design

      Prospective cohort study.

      Setting

      Stroke services.

      Participants

      People unlikely to regain functional use of the arm (N=155) were recruited at 2 to 4 weeks poststroke, and followed up at 3, 6, and 12 months. Potential predictors at baseline were hypertonicity, pain, motor control, mood, sensation/perception, age, and stroke severity.

      Interventions

      Not applicable.

      Main Outcome Measures

      Difficulty caring for the arm (Leeds Arm Spasticity Impact Scale), pain, hypertonicity, range of movement, arm function, and skin integrity. Multivariable linear regression identified the best fitting model for predicting Leeds Arm Spasticity Impact Scale score at 12 months.

      Results

      There were 110 participants (71%) reviewed at 1 year. There was a large variation in the profile of arm functions and activity limitations. Inability or severe difficulty caring for the arm affected 29% of participants. Hypertonicity developed in 77%, with severe hypertonicity present in 25%. Pain was reported by 65%, 94% developed shoulder contracture, and 6% had macerated skin. Difficulty caring for the arm increased with age, greater level of hypertonicity, and stroke classification; collectively, these factors accounted for 33% of the variance in Leeds Arm Spasticity Impact Scale scores.

      Conclusions

      At 1 year poststroke, there was a high incidence of impairments of body functions and activity limitations in people with a profoundly affected arm. Individual profiles were very variable and although some predisposing factors have been identified, it remains difficult to predict who is at greatest risk.

      Keywords

      List of abbreviations:

      MMAS (Modified Modified Ashworth Scale), TACS (total anterior circulation stroke)
      Three quarters of people with stroke will experience arm weakness, and 62% of these will not recover dexterity at 6 months.
      • Kwakkel G.
      • Kollen B.J.
      • van der Grond J.
      • Prevo A.J.
      Probability of regaining dexterity in the flaccid upper limb: Impact of severity of paresis and time since onset in acute stroke.
      For the purposes of this research, the term profoundly affected arm is used to describe the situation where a stroke survivor has no movement in the affected arm or when movement is not functionally useful.
      • Allison R.
      • Shenton L.
      • Bamforth K.
      • Kilbride C.
      • Richards D.
      Incidence, time course and predictors of impairments relating to caring for the profoundly affected arm after stroke: a systematic review.
      Although current physical therapies in stroke rehabilitation are based predominantly on exercise and task-specific training,
      Royal Dutch Society for Physical Therapy
      KNGF guideline: stroke.
      Intercollegiate Stroke Working Party
      National clinical guideline for stroke.
      additional therapy and practice of tasks does not improve active function in those with the most significant weakness.
      • Parry R.H.
      • Lincoln N.B.
      • Vass C.D.
      Effect of severity of arm impairment on response to additional physiotherapy early after stroke.
      Hence, for those most unlikely to regain active function, a focus on managing activity limitations and avoiding secondary complications may be more appropriate. This approach involves maintaining the ability to care for the arm, including tasks such as handwashing and nail-cutting (ie, passive function activities
      • Sheean G.
      Botulinum treatment of spasticity: why is it difficult to show a functional benefit?.
      which may be conducted by the person themselves or their caregiver).
      Previous research shows that hypertonicity is present as early as 1 week poststroke
      • De Jong L.D.
      • Hoonhorst M.H.
      • Stuive I.
      • Dijkstra P.U.
      Arm motor control as predictor for hypertonia after stroke: a prospective cohort study.
      and affects up to 47% of survivors.
      • Kong K.H.
      • Lee J.
      • Chua K.S.
      Occurrence and temporal evolution of upper limb spasticity in stroke patients admitted to a rehabilitation unit.
      Pain can also occur within 1 week,
      • Ratnasabapathy Y.
      • Broad J.
      • Baskett J.
      • Pledger M.
      • Marshall J.
      • Bonita R.
      Shoulder pain in people with a stroke: a population based study.
      with an incidence up to 49%.
      • Lundstrom E.
      • Smits A.
      • Terent A.
      • Borg J.
      Risk factors for stroke-related pain 1 year after first-ever stroke.
      Contracture is apparent by 2 weeks and affects 50%.
      • Ada L.
      • O'Dwyer N.
      • O'Neill E.
      Relation between spasticity, weakness and contracture of the elbow flexors and upper limb activity after stroke: an observational study.
      Previously reported predictors of hypertonicity include reduced motor control
      • De Jong L.D.
      • Hoonhorst M.H.
      • Stuive I.
      • Dijkstra P.U.
      Arm motor control as predictor for hypertonia after stroke: a prospective cohort study.
      • Kong K.H.
      • Lee J.
      • Chua K.S.
      Occurrence and temporal evolution of upper limb spasticity in stroke patients admitted to a rehabilitation unit.
      and increased stroke severity.
      • Kong K.H.
      • Lee J.
      • Chua K.S.
      Occurrence and temporal evolution of upper limb spasticity in stroke patients admitted to a rehabilitation unit.
      • Lundström E.
      • Smits A.
      • Terent A.
      • Borg J.
      Time-course and determinants of spasticity during the first six months following first-ever stroke.
      The most common predictors of pain are reduced sensation
      • Gamble G.E.
      • Barberan E.
      • Bowsher D.
      • Tyrrell P.J.
      • Jones A.K.
      Post stroke shoulder pain: more common than previously realized.
      • Sommerfeld D.K.
      • Welmer A.K.
      Pain following stroke, initially and at 3 and 18 months after stroke, and its association with other disabilities.
      and weakness.
      • Gamble G.E.
      • Barberan E.
      • Bowsher D.
      • Tyrrell P.J.
      • Jones A.K.
      Post stroke shoulder pain: more common than previously realized.
      The significance of depression is not clear, with some studies identifying a positive link with pain,
      • O'Donnell M.J.
      • Diener H.C.
      • Sacco R.L.
      • et al.
      Chronic pain syndromes after ischaemic stroke: PRo-FESS trial.
      and others discounting this.
      • Kong K.H.
      • Lee J.
      • Chua K.S.
      Occurrence and temporal evolution of upper limb spasticity in stroke patients admitted to a rehabilitation unit.
      Contracture is most frequently predicted by weakness.
      • Pandyan A.D.
      • Cameron M.
      • Powell J.
      • Stott D.J.
      • Granat M.H.
      Contractures in the post-stroke wrist: a pilot study of its time course of development and its association with upper limb recovery.
      • Kwah L.K.
      • Harvey L.A.
      • Diong J.H.
      • Herbert R.D.
      Half of the adults who present to hospital with stroke develop at least one contracture within six months: an observational study.
      However, this previous research is limited because all these studies have been conducted on general populations of stroke survivors and not targeted at those with the most significant weakness. Furthermore, none of these previous studies have evaluated the profile or potential predictors of difficulty caring for the arm after stroke in a systematic way.
      • Allison R.
      • Shenton L.
      • Bamforth K.
      • Kilbride C.
      • Richards D.
      Incidence, time course and predictors of impairments relating to caring for the profoundly affected arm after stroke: a systematic review.
      Despite the high proportion of people with a profoundly affected arm poststroke (62%),
      • Kwakkel G.
      • Kollen B.J.
      • van der Grond J.
      • Prevo A.J.
      Probability of regaining dexterity in the flaccid upper limb: Impact of severity of paresis and time since onset in acute stroke.
      there is currently, to our knowledge, no targeted research on (1) the longitudinal profile of activity limitation in caring for the arm, (2) the proportion of people who develop associated impairments of body functions, and (3) the relation between initial clinical findings and subsequent difficulty caring for the arm. The aim of this study was to establish the longitudinal profile of impairment of body functions and activity limitation in people with a profoundly affected arm, and to evaluate potential predictors of difficulty caring for the arm, in the first year poststroke.

      Methods

      Participants

      In a prospective, longitudinal study, all adult patients with first or subsequent stroke admitted to 3 stroke units in the United Kingdom over 30 months from September 2011, and still under the care of the stroke team at 2 weeks poststroke, were screened for inclusion. Criteria included stroke within the last 2 to 4 weeks and a Fugl-Meyer upper extremity score of ≤11 points at 2 weeks, or 15 points at 3 weeks, or 19 points at 4 weeks poststroke. These scores are strongly associated with high probability of not regaining function in the arm.
      • Kwakkel G.
      • Kollen B.J.
      • van der Grond J.
      • Prevo A.J.
      Probability of regaining dexterity in the flaccid upper limb: Impact of severity of paresis and time since onset in acute stroke.
      Patients who were unable to use their arm before the stroke were excluded. Potential participants were assessed for their ability to consent using the Mental Capacity Act.
      Department of Health
      Mental capacity act.
      Those with capacity were asked for their consent to participate. If the potential participant was judged by the researcher not to have capacity to make this decision, a consultee was approached if available. A consultee is someone who knows the person well but is not acting in a professional capacity, who can consider the persons beliefs and provide assent on their behalf if this is in line with their interests.
      Department of Health
      Guidance on nominating a consultee for research involving adults who lack capacity to consent.
      Participants' baseline data were collected at the point of consent and at 3, 6, and 12 months later in the setting of their choice. These time scales allow comparison with previous studies.
      • De Jong L.D.
      • Hoonhorst M.H.
      • Stuive I.
      • Dijkstra P.U.
      Arm motor control as predictor for hypertonia after stroke: a prospective cohort study.
      • Kong K.H.
      • Lee J.
      • Chua K.S.
      Occurrence and temporal evolution of upper limb spasticity in stroke patients admitted to a rehabilitation unit.
      • Ratnasabapathy Y.
      • Broad J.
      • Baskett J.
      • Pledger M.
      • Marshall J.
      • Bonita R.
      Shoulder pain in people with a stroke: a population based study.
      • Lundstrom E.
      • Smits A.
      • Terent A.
      • Borg J.
      Risk factors for stroke-related pain 1 year after first-ever stroke.
      Throughout the study, all participants received usual care under the U.K. National Health Service.

      Baseline predictor variables and demographic variables

      Five potential predictors of difficulty caring for the arm and related impairments were identified
      • Allison R.
      • Shenton L.
      • Bamforth K.
      • Kilbride C.
      • Richards D.
      Incidence, time course and predictors of impairments relating to caring for the profoundly affected arm after stroke: a systematic review.
      : motor control, mood, sensation/perception, hypertonicity, and pain. Because the primary outcome related to passive care activities, hand dominance was not considered as a predictor. To maximize inclusivity wherever possible, the measures used were suitable for people with aphasia or cognitive impairment. This included using pictographic resources, observational tools, and measures with evidence of validity when completed by proxy. The predictor measures are summarized in table 1.
      • Hsieh Y.W.
      • Wu C.Y.
      • Lin K.C.
      • Chang Y.F.
      • Chen C.L.
      • Liu J.S.
      Responsiveness and validity of three outcome measures of motor function after stroke rehabilitation.
      • Paci M.
      • Nannetti L.
      • Taiti P.
      • Baccini M.
      • Pasquini J.
      • Rinaldi L.
      Shoulder subluxation after stroke: relationships with pain and motor recovery.
      • Ansari N.N.
      • Naghdi S.
      • Hasson S.
      • Mousakhani A.
      • Nouriyan A.
      • Omidvar Z.
      Inter-rater reliability of the Modified Modified Ashworth Scale as a clinical tool in measurements of post-stroke elbow flexor spasticity.
      • Prescott R.J.
      • Garraway W.M.
      • Akhtar A.J.
      Predicting functional outcome following acute stroke using a standard clinical examination.
      • Leeds L.
      • Meera R.J.
      • Hobson J.F.
      The utility of the Stroke Aphasic Depression Questionnaire in a stroke rehabilitation unit.
      Royal College Physicians
      Spasticity in adults: management using botulinum toxin: national guidelines.
      • Andrews A.W.
      • Bohannon R.W.
      Decreased shoulder range of motion on paretic side after stroke.
      • Uswatte G.
      • Taub E.
      • Morris D.
      • Vignolo M.
      • McCulloch K.
      Reliability and validity of the upper-extremity motor activity log-14 for measuring real-world arm use.
      Scores for hypertonicity with the Modified Modified Ashworth Scale (MMAS)
      • Ansari N.N.
      • Naghdi S.
      • Hasson S.
      • Mousakhani A.
      • Nouriyan A.
      • Omidvar Z.
      Inter-rater reliability of the Modified Modified Ashworth Scale as a clinical tool in measurements of post-stroke elbow flexor spasticity.
      were applied to the 5 arm muscles identified as commonly affected (ie, shoulder adductors and internal rotators, and elbow, wrist, and finger flexors).
      • Kong K.H.
      • Lee J.
      • Chua K.S.
      Occurrence and temporal evolution of upper limb spasticity in stroke patients admitted to a rehabilitation unit.
      The single worst score of any muscle group (worst hypertonicity) and the summed score of hypertonicity in all 5 groups (total hypertonicity) were considered (independently) as predictors. Summary scores of this type have been developed and validated.
      • Platz T.
      • Vuadens P.
      • Eickhof C.
      • Arnold P.
      • Van Kaick S.
      • Heise K.
      REPAS, a summary rating scale for resistance to passive movement: item selection, reliability and validity.
      Table 1Battery of predictor and outcome measures
      PredictorsNameScoring
      Motor controlFugl-Meyer Upper limb score
      • Sommerfeld D.K.
      • Welmer A.K.
      Pain following stroke, initially and at 3 and 18 months after stroke, and its association with other disabilities.
      0–66, higher score indicates better control
      PainYes/no response to pain at rest and on passive movement
      • O'Donnell M.J.
      • Diener H.C.
      • Sacco R.L.
      • et al.
      Chronic pain syndromes after ischaemic stroke: PRo-FESS trial.
      0, 1, or 2, higher score indicates more pain
      HypertonicityMMAS
      • Pandyan A.D.
      • Cameron M.
      • Powell J.
      • Stott D.J.
      • Granat M.H.
      Contractures in the post-stroke wrist: a pilot study of its time course of development and its association with upper limb recovery.
      0–4, higher score indicates higher tone
      Perception/sensationFind the thumb test
      • Kwah L.K.
      • Harvey L.A.
      • Diong J.H.
      • Herbert R.D.
      Half of the adults who present to hospital with stroke develop at least one contracture within six months: an observational study.
      0, 1, or 2, higher score indicates worse perception
      MoodStroke Aphasic Depression Questionnaire-10
      Department of Health
      Mental capacity act.
      0–30, higher score indicates lower mood
      Outcomes
       Difficulty caring for armLeeds Arm Spasticity Impact Scale
      Department of Health
      Guidance on nominating a consultee for research involving adults who lack capacity to consent.
      0–4, higher score indicates more difficulty
       PainYes/no response to pain at rest and on passive movement
      • O'Donnell M.J.
      • Diener H.C.
      • Sacco R.L.
      • et al.
      Chronic pain syndromes after ischaemic stroke: PRo-FESS trial.
      0, 1, or 2, higher score indicates more pain
       HypertonicityMMAS
      • Pandyan A.D.
      • Cameron M.
      • Powell J.
      • Stott D.J.
      • Granat M.H.
      Contractures in the post-stroke wrist: a pilot study of its time course of development and its association with upper limb recovery.
      0–4, higher score indicates higher tone
       Passive range of movementGoniometry of shoulder flexion, abduction, external rotation; elbow flexion, extension; wrist extension, index, little finger and thumb extension at each joint
      • Hsieh Y.W.
      • Wu C.Y.
      • Lin K.C.
      • Chang Y.F.
      • Chen C.L.
      • Liu J.S.
      Responsiveness and validity of three outcome measures of motor function after stroke rehabilitation.
      Range measured in degrees of movement
       Skin integrityAxilla, elbow and hand, classified as dry/intact; macerated or broken0, 1, or 2, higher score indicates worse skin condition
       Active arm functionMotor Activity Log-14
      • Paci M.
      • Nannetti L.
      • Taiti P.
      • Baccini M.
      • Pasquini J.
      • Rinaldi L.
      Shoulder subluxation after stroke: relationships with pain and motor recovery.
      0–70, higher score indicates better use
      In addition to these prespecified predictors, demographic data were also collected including age, sex, and type of stroke using the Oxfordshire Community Stroke Project classification.
      • Bamford J.
      • Sandercock P.
      • Dennis M.
      • Burn J.
      • Warlow C.
      Classification and natural history of clinically identifiable subtypes of cerebral infarction.

      Outcome measures (3, 6, and 12mo poststroke)

      The primary outcome measure was a scale of difficulty caring for the arm: the Leeds Arm Spasticity Impact Scale.
      Royal College Physicians
      Spasticity in adults: management using botulinum toxin: national guidelines.
      This is an item bank of 12 tasks of caring for the arm, including aspects of washing, nail-cutting, and dressing. The participant rates each relevant task with degree of difficulty using a scale from 0 to 4, and scores are then averaged. Test-retest reliability has been established with a minimally detected change of 0.5.
      • O'Reilly F.
      • Meldrum D.
      Test re-test reliability of the Modified Leeds Arm Spasticity Impact Scale (MLASIS) and the minimum detectable change (MDC) scores.
      Secondary outcomes included passive range of movement, pain, hypertonicity, active function, and skin integrity. The measures are summarized in table 1. A protocol for conducting the predictor and outcome measure assessments was developed and demonstrated a good degree of interrater reliability, with kappa scores of .82 for MMAS scores, 1.0 for pain, and 0.8 for the Leeds Arm Spasticity Impact Scale, with 93% agreement for measuring range of movement to within 15°.

      Statistical analysis

      All statistical analyses were performed using the statistical programming language R.a Summary statistics were produced. Where the data were normally distributed, means and SDs were used. Otherwise, median and interquartile ranges were given. Individual profile plots were constructed to visualize each participant's Leeds Arm Spasticity Impact Scale score average across follow-up points. The linear association between each continuous predictor and Leeds Arm Spasticity Impact Scale score average at 12 months was summarized using Pearson correlation coefficient, whereas descriptive statistics for Leeds Arm Spasticity Impact Scale score average at 12 months are presented for each level of each categorical predictor.
      Multivariable linear regression was used to identify models of predictors for Leeds Arm Spasticity Impact Scale score average at 12 months poststroke. For brevity, this article reports only the overall best fitting model.

      Sample size

      Sample sizes for multivariable linear regression are based on the minimum R2 value of interest and the number of independent predictors. Although there were 5 potential predictors of interest, 3 are categorical: pain (3 categories), sensation/perception (3 categories), and hypertonicity (5 categories), with 2 continuous predictors (Fugl-Meyer and mood scores). After recoding categorical predictors as indicator variables, as required for modeling, statistically, it may be considered that there are 10 possible explanatory variables/predictors. Assuming a significance level of 10%, a sample size of 120 participants was required to detect a medium effect size of .15 (which corresponds to an R2 value of approximately 13%) with 90% power. Based on previous studies,
      • Sackley C.
      • Brittle N.
      • Patel S.
      • et al.
      The prevalence of joint contractures, pressure sores, painful shoulder, other pain, falls, and depression in the year after a severely disabling stroke.
      • Leathley M.J.
      • Gregson J.M.
      • Moore A.P.
      • Smith T.L.
      • Sharma A.K.
      • Watkins C.L.
      Predicting spasticity after stroke in those surviving to 12 months.
      it was estimated that there would be a potential drop-off of 10% per measurement session. Therefore, the recruitment target was set at 165 participants, with the aim of following-up at least 120 participants at the 12 months poststroke time point.

      Ethics

      The study was approved by the National Research Ethics Service South West Ethics Committee (reference no. 11/SW/0149).

      Results

      Figure 1 illustrates the process of recruitment and follow-up, including reasons for participants lost to follow-up: 833 people were screened for inclusion of which 216 (26%) fulfilled the inclusion criteria, and 155 gave consent or consultee assent to participate (72% of those eligible). At 1 year, 110 participants (71%) were reviewed. Of the remaining 45 participants, 6 declined reassessment, 33 had died, and 6 were unavailable.
      Figure thumbnail gr1
      Fig 1Flow diagram detailing recruitment and progression of participants.
      Participant demographic data at baseline and the predictor measures are summarized in table 2. The average age of participants was 74.7 years, with a higher proportion of women than men, and almost half of the participants had a total anterior circulation stroke (TACS). At baseline, 82.6% had already developed some hypertonicity, with 17.4% exhibiting pain and 31.8% demonstrating impairment of sensation/perception. Outcome measures at each follow-up are summarized in table 3 and subsequently briefly summarized.
      Table 2Descriptive statistics of participant characteristics and potential predictors at baseline (N=155)
      CharacteristicValue
      Age, y
       Mean ± SD74.7±12.8
       Range38.0–96.0
      Sex
       Female89 (57)
       Male66 (43)
      Stroke classification
       Not reported1 (0.6)
       Hemorrhage25 (16.2)
       TACS73 (47.4)
       Partial anterior circulation stroke30 (19.5)
       Lacunar stroke23 (14.9)
       Posterior circulation stroke3 (1.9)
      Fugl-Meyer upper limb score
       Median (quartile 1–quartile 3)2.0 (2.0–6.0)
       Range0.0–16.0
      Hypertonicity (worse MMAS score)
       027 (17.4)
       152 (33.5)
       253 (34.2)
       323 (14.8)
       40 (0)
      Hypertonicity (total score)
       Median (quartile 1–quartile 3)3.0 (1.0–5.0)
       Range0.0–12.0
      Pain
       No pain at rest or movement128 (82.6)
       Pain on movement only21 (13.5)
       Pain at rest and on movement6 (3.9)
      Mood (SADQ-10)
       Mean ± SD8.2±4.5
       Range0.0–23.0
      Sensation/perception (find the thumb test)
       Not reported1 (0.6)
       Able to find affected thumb105 (68.2)
       Able to find affected arm only19 (12.3)
       Unable to find affected arm30 (19.5)
      NOTE. Values are n (%) or as otherwise indicated.
      Abbreviation: SADQ-10, Stroke aphasic depression questionnaire.
      Table 3Descriptive statistics of outcome measures at each follow-up time point
      Outcome Measure3mo (n=120)6mo (n=113)12mo (n=110)
      LASIS average
       Mean ± SD1.7±1.01.6±1.12.0±1.3
       Range0.08–4.000.00–4.000.00–4.00
      Hypertonicity (worse score)
       Not reported2 (1.7)4 (3.5)1 (0.9)
       016 (13.6)19 (17.4)24 (22)
       131 (26.3)33 (30.3)29 (26.4)
       252 (44.1)32 (29.4)29 (26.4)
       319 (16.1)22 (20.2)24 (22)
       40 (0)3 (2.8)3 (2.7)
      Hypertonicity (total score)
       Median (quartile 1–quartile 3)4.0 (2.0–8.0)4.0 (1.0–9.0)4.0 (1.0–7.8)
       Range0.0–15.00.0–16.00.0–15.0
      Pain
       No pain at rest or movement32 (26.7)31 (27.4)38 (34.5)
       Pain on movement only60 (50)56 (49.6)56 (50.9)
       Pain at rest and on movement28 (23.3)26 (23.0)16 (14.5)
      Passive range shoulder abduction, deg
       Mean ± SD76.8±24.474.3±22.679.9±28.8
       Range25.0–170.010.0–160.020.0–180.0
      Passive range shoulder external rotation, deg
       Mean ± SD22.8±24.824.8±22.725.0±27.4
       Range−80 to 65.0−70.0 to 75.0−60.0 to 90.0
      Passive range elbow extension, deg
       Mean ± SD165.0±20.0165.0±20.8164.8±21.0
       Range100.0–180.090.0–180.0100.0–180.0
      Passive range wrist extension
       Mean ± SD38.6±21.637.7±26.743.7±26.6
       Range−60.0 to 90.0−50.0 to 80.0−60.0 to 80.0
      Passive range index PIP extension
       Mean ± SD175.3±11.5172.1±17.3174.2±16.3
       Range100.0–180.090.0–180.0100.0–180.0
      Skin integrity
       Not reported0 (0)2 (1.8)0 (0)
       Dry intact118 (98.4)105 (92.9)103 (93.6)
       Macerated2 (1.6)6 (5.3)7 (6.4)
       Broken0 (0)0 (0)0 (0)
      Active function (MAL-14)
       Median (quartile 1–quartile 3)0.0 (0.0–0.8)0.1 (0.0–1.0)0 (0.0–1.2)
       Range0–4.210.0–5.000.0–4.38
      NOTE. Values are n (%) or as otherwise indicated.
      Abbreviations: LASIS, Leeds Arm Spasticity Impact Scale; MAL-14, Motor Activity Log; PIP, proximal inter-phalangeal.

      Longitudinal profiles of difficulty caring for the arm

      Leeds Arm Spasticity Impact Scale outcomes were collected from 104 participants at all time points. The mean Leeds Arm Spasticity Impact Scale scores at 3 and 6 months were similar (1.7 and 1.6, respectively) and by 12 months had increased to 2.0. However, there was a large variation in the profiles of each participant's scores, as shown in the individual profile plots in figure 2, with some showing increasing difficulty over time, some showing decreasing difficulty, and some showing broader variation. At the 12-month time point, over half (59%) of the participants reported no or little difficulty with care tasks, 12% reported moderate difficulty, and 29% indicated they either had a great deal of difficulty or were unable to perform tasks (eg, washing, dressing).
      Figure thumbnail gr2
      Fig 2Individual participant LASIS scores at each time point. Each box contains 5 participants in their order of recruitment. Where data are missing, the participant was lost to follow-up. (n=127 at 3mo, n=117 at 6mo, and n=111 at 12mo). Abbreviation: LASIS, Leeds Arm Spasticity Impact Scale.

      Longitudinal profiles of related impairments of body functions and activity limitation

      Active function

      As anticipated, most participants had not recovered active use of the arm at 12 months, with 73% scoring between 0 and 1 (inclusive) on the Motor Activity Log-14, and median values remaining at 0 across time points. However, 15 participants (14%) regained some use of the arm (scoring ≥2 on the Motor Activity Log). The baseline characteristics of those who regained some use are shown in table 4.
      Table 4Descriptive statistics at baseline by functionality at 12 months (n=109)
      CharacteristicParticipants With MAL Score <2 at 12mo (n=94)Participants With MAL Score ≥2 at 12mo (n=15)
      Age, y
       Mean ± SD72.7±12.968.1±13.7
       Range38.0–95.040.0–96.0
      Sex
       Female49 (52)9 (60)
       Male45 (48)6 (40)
      Stroke classification
       Not reported0 (0)0 (0)
       Hemorrhage19 (20.2)1 (6.7)
       TACS45 (47.9)6 (40.0)
       Partial anterior circulation stroke16 (17.0)4 (26.7)
       Lacunar stroke12 (12.8)4 (26.7)
       Posterior circulation stroke2 (2.1)0 (0)
      Fugl-Meyer upper limb scores
       Median (quartile 1–quartile 3)2.0 (2.0–5.0)5.0 (4.0–10.5)
       Range0.0–15.02.0–15.0
      Hypertonicity (worse MMAS score)
       016 (17.0)3 (20.0)
       126 (27.7)6 (40.0)
       238 (40.4)5 (33.3)
       314 (14.9)1 (6.7)
       40 (0)0 (0)
      Hypertonicity (total score)
       Median (quartile 1–quartile 3)3.0 (1.0–5.8)2.0 (1.0–3.0)
       Range0.0–12.00.0–7.0
      Pain
       No pain at rest or movement77 (81.9)13 (86.7)
       Pain on movement only12 (12.8)1 (6.7)
       Pain at rest and on movement5 (5.3)1 (6.7)
      Mood (SADQ-10)
       Mean ± SD8.3±4.86.1±4.2
       Range0.0–23.01.0–16.0
      Sensation/perception (find the thumb test)
       Not reported1 (1.1)0 (0)
       Able to find affected thumb68 (72.3)11 (73.3)
       Able to find affected arm only10 (10.6)2 (13.3)
       Unable to find affected arm15 (16.0)2 (13.3)
      NOTE. Values are n (%) or as otherwise indicated.
      Abbreviations: MAL-14, Motor Activity Log; SADQ-10, Stroke aphasic depression questionnaire.

      Hypertonicity

      Individual profiles of hypertonicity were very variable over the 3 time points; however, median hypertonicity total score was 4.0 at all time points (see table 3). Some participants showed trends for increasing hypertonicity over time, some showed decreasing, and some showed no discernible pattern. At 1 year, 77% of survivors had developed some hypertonicity in at least 1 muscle group (MMAS score of at least 1), with severe hypertonicity in at least 1 muscle group present in 25% of participants (MMAS score of at least 3). The muscle groups most commonly affected by severe hypertonicity were elbow and wrist flexors (affecting 14% of participants each), shoulder internal rotators (13%), finger flexors (10%), and shoulder adductors (6%).

      Pain

      Profiles of pain were also very variable within the group of participants; however, a larger proportion reported pain at follow-up compared with baseline, when most (83%) were pain free. At 12 months, pain in some parts of the arm was reported by 65% of participants.

      Range of movement

      Individual profiles of range of movement were variable over time at all the joints assessed, with some participants having increasing and some having decreasing range between 3 and 12 months. However, over the 3 time points, the mean range of movement, particularly at the shoulder and wrist, was less than would be expected in healthy older adults.
      • Kalscheur J.A.
      • Emery L.J.
      • Costello P.S.
      Range of motion in older women.
      Range of movement in the fingers was less reduced. Table 3 includes range for the index finger proximal interphalangeal joint as an example. Other studies have defined contracture as the loss of at least 30% of the available range of movement.
      • Kwah L.K.
      • Harvey L.A.
      • Diong J.H.
      • Herbert R.D.
      Half of the adults who present to hospital with stroke develop at least one contracture within six months: an observational study.
      Using these criteria, 94% of participants had developed shoulder contracture, 9% had elbow contracture, 54% had wrist contracture, and 7% had finger contracture at 1 year.

      Skin integrity

      Seven participants (6%) developed macerated skin in the hand or elbow crease at 12 months. None of the participants had broken skin at any point.

      Predicting difficulty caring for the arm

      Table 5 summarizes the bivariate relations between the Leeds Arm Spasticity Impact Scale score average at 12 months and each of the predictors. There was evidence of a positive relation between the Leeds Arm Spasticity Impact Scale score average and age, hypertonicity total score, and mood; however, only the linear association between the Leeds Arm Spasticity Impact Scale score average and age was statistically significant. We used hypertonicity total scores in the best fitting model because they explained a greater percentage of variance for the Leeds Arm Spasticity Impact Scale score average than worst hypertonicity.
      Table 5Summary statistics of bivariate relations between predictors and Leeds Arm Spasticity Impact Scale score average at 12 months
      CharacteristicMean ± SD (Range)Correlation Coefficient (95% CI)
      AgeNA0.39 (0.22 to 0.54)
      SexNA
       Female2.2±1.4 (0.00–4.00)
       Male1.7±1.3 (0.00–4.00)
      Stroke classificationNA
       Lacunar stroke1.4±0.9 (0.00–3.82)
       Partial anterior circulation stroke1.5±1.3 (0.09–4.00)
       Posterior circulation stroke0.9±0.7 (0.42–1.44)
       TACS2.3±1.4 (0.00–4.00)
       Hemorrhage2.2±1.3 (0.45–4.00)
      Fugl-Meyer upper limb scoreNA−0.18 (−0.36 to 0.01)
      Hypertonicity (worse MMAS score)NA
       01.7±1.3 (0.27–4.00)
       11.9±1.4 (0.00–4.00)
       21.9±1.3 (0.00–4.00)
       32.8±1.3 (0.55–4.00)
       4NA
      Hypertonicity (total score)NA0.19 (0.00 to 0.37)
      PainNA
       No pain at rest or movement1.9±1.4 (0.00–4.00)
       Pain on movement only2.6±1.3 (0.10–4.00)
       Pain at rest and on movement1.7±0.6 (0.80–2.27)
      Mood (SADQ-10)NA0.19 (0.00 to 0.36)
      Sensation/perception (find the thumb)NA
       Able to find affected thumb1.8±1.3 (0.00–4.00)
       Able to find affected arm only2.3±1.1 (0.25–4.00)
       Unable to find affected arm2.3±1.5 (0.36–4.00)
      Abbreviations: CI, confidence interval; NA, not applicable.
      The overall best fitting linear model was derived from the 5 prespecified predictors and the 4 additional baseline variables. After the removal of 3 outliers, the final model was fitted to data from 106 participants and included age (P<.001), hypertonicity total (P=.002), and stroke classification (participants who had lacunar stroke
      • Bamford J.
      • Sandercock P.
      • Dennis M.
      • Burn J.
      • Warlow C.
      Classification and natural history of clinically identifiable subtypes of cerebral infarction.
      compared with participants who had TACS
      • Bamford J.
      • Sandercock P.
      • Dennis M.
      • Burn J.
      • Warlow C.
      Classification and natural history of clinically identifiable subtypes of cerebral infarction.
      [P=.004] and hemorrhage [P=.010]) (table 6). Collectively, these 3 variables explained approximately one third (adjusted R2=33%) of the variance in the Leeds Arm Spasticity Impact Scale score average at 12 months. From the linear regression coefficients from this final best fitting model, (1) a 1-year increase in age at baseline increases the Leeds Arm Spasticity Impact Scale score average at 12 months by an average of .050 units (SE, .008); (2) a 1-unit increase in hypertonicity total at baseline increases the Leeds Arm Spasticity Impact Scale score average at 12 months by an average of .109 units (SE, .035); and (3) the mean Leeds Arm Spasticity Impact Scale score average for the group of participants who had lacunar stroke was .935 units (SE, .314) lower than participants who had TACS and .962 units (SE, .367) lower than participants who had hemorrhage.
      Table 6Regression statistics for the overall best fitting model for Leeds Arm Spasticity Impact Scale score average at 12 months
      PredictorCoefficient95% Confidence IntervalP
      Intercept−2.658−4.028 to −1.288<.001
      Age0.0500.034 to 0.066<.001
      Hypertonicity total0.1090.040 to 0.178.002
      Stroke class POCS−0.200−1.809 to 1.409.808
      Stroke class PACS0.121−0.608 to 0.850.744
      Stroke class TACS0.9350.320 to 1.550.004
      Stroke class HAEM0.9620.243 to 1.681.010
      NOTE. Lacunar stroke is the baseline level for stroke classification. Residual SE: 1.091 on 99 df. Multiple R2: .37. Adjusted R2: .33 F statistic: 9.6 on 6 and 99 df. P<.001.
      Abbreviations: HAEM, hemorrhage stroke; PACS, partial anterior circulation stroke; POCS, posterior circulation ischemic stroke.

      Discussion

      This is the first longitudinal study, to our knowledge, of people with a profoundly affected arm after stroke. Although the sample included a high proportion of people with more severe classifications of stroke, this was not surprising given the target population. Many studies restrict recruitment and do not involve people with severe communication or cognitive limitations, but we have demonstrated it was possible to include them, by supporting them with enhanced communication resources or using proxies.
      Given that participants were those with severe arm weakness at 2 to 4 weeks poststroke, observable patterns between impairments and activity limitation were thought to be a possibility. However, this was not the case, and longitudinal profiles of these factors were highly individual.
      The incidence of impairments in the arm was high compared with studies that have included general populations of stroke survivors. For example, 77% of our participants who had severe weakness at baseline presented with hypertonicity at 1 year compared with 49% of those who initially presented with milder weakness at baseline.
      • Kong K.H.
      • Lee J.
      • Chua K.S.
      Occurrence and temporal evolution of upper limb spasticity in stroke patients admitted to a rehabilitation unit.
      In addition, 65% of our participants reported pain in the arm compared with 49% of a general population of stroke survivors reporting pain in any part of the body.
      • Ratnasabapathy Y.
      • Broad J.
      • Baskett J.
      • Pledger M.
      • Marshall J.
      • Bonita R.
      Shoulder pain in people with a stroke: a population based study.
      Incidence of contracture of the shoulder and wrist were also higher than that recorded in general populations of stroke survivors
      • Kwah L.K.
      • Harvey L.A.
      • Diong J.H.
      • Herbert R.D.
      Half of the adults who present to hospital with stroke develop at least one contracture within six months: an observational study.
      ; however, this was not the case for the elbow. It is unclear why so many of our participants developed loss of range of the shoulder and wrist while the elbow and fingers remained less severely affected. The shoulder is typically held in adduction and internal rotation at rest so may be more vulnerable, whereas gravity may assist with extension of the elbow. The wrist is a complex joint, and contracture of the finger flexor muscle-tendon units may effect on range of movement at the wrist in addition to the fingers. Differences in muscle architecture surrounding connective tissue may also contribute to the variation in contracture between muscles. Recent work in animal studies suggests that there is a direct relation between muscle atrophy and fibrosis. Cytokine myostatin, for example, is not only central to the pathways that mediate muscle atrophy but can also activate fibroblasts and stimulate fibrosis.
      • Li Z.B.
      • Kollias H.D.
      • Wagner K.R.
      Myostatin directly regulates skeletal muscle fibrosis.
      • Desgeorges M.M.
      • Devillard X.
      • Toutain J.
      • et al.
      Molecular mechanisms of skeletal muscle atrophy in a mouse model of cerebral ischemia.
      Therefore, differences in the weakness of individual muscles may effect on their relative degree of contracture development and increase in passive stiffness.
      • Li Z.B.
      • Kollias H.D.
      • Wagner K.R.
      Myostatin directly regulates skeletal muscle fibrosis.
      • Bo Li Z.
      • Zhang J.
      • Wagner K.R.
      Inhibition of myostatin reverses muscle fibrosis through apoptosis.
      The incidence of difficulty caring for the arm was high because 29% of participants were either unable to care for their arm or described significant difficulty. A number of predictors of difficulty caring for the arm that can be assessed early after stroke were evaluated. The best linear predictive model based on these included age, hypertonicity, and stroke classification; however, these factors explained only 33% of the total variability in the Leeds Arm Spasticity Impact Scale score average at 1 year poststroke. Our previous review did not identify other impairments that are likely to influence longer-term outcome in caring for the arm.
      • Allison R.
      • Shenton L.
      • Bamforth K.
      • Kilbride C.
      • Richards D.
      Incidence, time course and predictors of impairments relating to caring for the profoundly affected arm after stroke: a systematic review.
      Previous studies have not considered the use of biomarkers as predictors of outcome in this targeted group, and it is possible they may add to the predictive value.
      There are a number of clinical implications of this work. Although recognizing that people with profoundly affected arm gain little from active exercise to improve function,
      Intercollegiate Stroke Working Party
      National clinical guideline for stroke.
      given the high incidence of pain, hypertonicity, and contracture, they may benefit from an educational intervention to reduce the effect of these impairments, and from longer-term monitoring. Regarding the important risk factors identified, age and stroke classification cannot be influenced in treatment after stroke, but it is possible that early manifestations of hypertonicity can be altered and research could explore if targeting hypertonicity early after stroke can reduce the risk of difficulty caring for the arm longer term, particularly in those with other risk factors.

      Study limitations

      This study has a number of limitations. Although every attempt was made to include measures that had been validated in people with aphasia and cognitive impairment, this was not always possible. The Fugl-Meyer score in particular has not been validated in this group. Equally, the anticipated sample size of 120 participants at 1 year was not achieved; therefore, adequate statistical power may be lacking. Hand dominance was not considered as a predictor variable, and this may have an influence in self-care. Finally, no attempt was made to assess the amount or content of rehabilitation that participants received; therefore, it is possible that any such interventions may have effected on outcomes. Therefore, conclusions should be drawn with caution.

      Conclusions

      At 1 year poststroke, there was a high incidence of difficulty caring for the arm (measured with the Leeds Arm Spasticity Impact Scale) and pain, hypertonicity, and contracture. Notably, individual profiles were very variable and although some predisposing factors have been identified, it remains difficult to predict who is at greatest risk.

      Supplier

      • a.
        R (version 3.1.3); R Foundation for Statistical Computing.

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