- Email: [email protected]
Functional outcome in brain stem stroke patients after rehabilitation
194
Functional Outcome in Brain Stem Stroke Patients After Rehabilitation Karen S.G. Chua, MBBS, Keng-He Kong, MBBS ABSTRACT. Chua KSG, Kong K-H. Functional outcome in brain stem stroke patients after rehabilitation. Arch Phys Med Rehabil 1996; 77: 194-7.
Objective: To document functional outcome before and after rehabilitation in a group of brain stem stroke patients and to analyze possible factors influencing outcome. Design and Setting: A case series of 53 consecutive inpatients admitted to a rehabilitation facility with confirmed brain stem strokes over a period of 6 years. Patients and Outcome Measures: Patients were selected by physiatrists for admission into the rehabilitation program. Outcome was measured by the Modified Barthel Index (MBI) for mobility and activities of daily living. Results: The mean age of this cohort was 57.9 ? 11.9 years and the ports was involved in 55% of cases. Ataxia (68%) and hemiplegia (70%) were the most frequent neurological deficits. Twenty-one patients (40%) had significant dysphagia with risk of aspiration and 16 patients (30%) were incontinent of urine. Aspiration pneumonia and urinary tract infection were present in 8 (15%) and 13 (25%) patients, respectively. Significant improvements in functional status, motor strength, swallowing, and continence status were documented on discharge (p < .05). The total admission MB1 was the only significant factor influencing total discharge Bartbel Index (p = .597, adjusted R2 = .476, p < .OOOl). Fifty-one (96%) were discharged home after rehabilitation. Conclusions: Despite multiple physical deficits, this cohort of brain stem stroke patients made functional gains during rehabilitation with significant improvements in mobility and selfcare skills, motor strength, severity of ataxia, continence and swallowing status. 0 1996 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation
S
TROKE was the third leading cause of death in Singapore in 1993, accounting for 54.9 deaths per 100,000 population.’ Although improved management of hypertension and coronary artery disease, as well as lifestyle changes, have resulted in declining stroke incidence, a significant number of stroke survivors are left with residual disabilities. Strokes affecting the brain stem are usually the result of infarction of the vertebral or basilar arteries. Mixed or incomplete clinical syndromes are usually encountered more often than the classical medial or lateral brain stem syndromes.’ From the Departnient of Rehabilitation Medicine, Singapore. Submitted for publication April I I, 1995. Accepted
Tan
Tack
in revised
Seng Hospital, form August
21,
199.5. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Reprint requests to Dr. Karen S.G. Chua, Department of Rehabilitation Medicine, Tan Tack Seng Hospital, c/o 17, Ang MO Kio Avenue 9, Singapore 2056, Singapore. 0 I996 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation
0003.9993/96i7702-3475$3,00/O
Arch
Phys Msd
Rehabil
Vol77,
February
1666
Hence, the clinical picture is often heterogenous. Patients with brain stem infarction may present with bilateral long tract motor and sensory signs, crossed motor and sensory signs, dissociated sensory loss with Homer syndrome (lateral medullary syndrome), cerebellar signs, stupor or coma, unilateral deafness, or pharyngeal weakness. Brain stem strokes are believed to be less common than strokes involving other regions of the brain and the true incidence of brain stem strokes is not known.’ The outcome of these patients depends on the site and nature (infarction/hemorrhage) of the stroke. In general, the survivors of brain stem strokes have excellent prognosis for functional recovery compared with survivors of hemispheric strokes because the vascular lesions affect smaller penetrating blood vessels that emerge directly from the vertebrobasilar arteries4 Survivors of brain stem strokes were also reported to have increased probability of long-term survival compared with survivors with hemispheric infarctions.5 The incidence of dysphagia, aspiration, and ataxia in these patients has not been well studied. To date, no detailed studies have been reported documenting functional outcome quantitatively in these patients. This study was conducted to objectively quantify the prerehabilitation and postrehabilitation functional outcomes of a group of brain stem strokes patients admitted for inpatient rehabilitation, define the types of neurological deficits present, determine factors influencing functional outcomes and suggest clinical implications for rehabilitation in this group of stroke patients.
METHODS Brain stem stroke was defined as an acute onset of neurological deficit with clinical features of brain stem or cerebellar dysfunction lasting more than 24 hours together with computed tomography (CT) or magnetic resonance imaging (MRI) evidence of ischemic infarction or parenchymal hemorrhage unrelated to tumour, arteriovenous malformation, or trauma in a region within tbe brain stem or cerebellum. The diagnosis of stroke was made clinically by admitting stroke unit neurologists and radiographically confirmed on CT or MRI scans of the brain within 24 to 48 hours of hospital admission. The charts of 53 consecutive inpatients with brain stem strokes admitted to an inpatient rehabilitation facility were retrospectively reviewed over a 6-year period from 1989 through 1994. Patients were individually selected for rehabilitation by physiatrists. Criteria for admission to the rehabilitation program were the same for all patients. These criteria included the ability to obey simple instructions and participate in therapy, stable medical course, and the clinical judgement of the admitting physiatrist regarding the potential benefits of an inpatient rehabilitation program. Timing of discharge from rehabilitation was determined by the rehabilitation team and was considered when the patients had attained their initial functional goals set at the commencement of the program, or had reached a plateau of improvement, or when outpatient therapy was more appropriate. Exclusion criteria included patients with neurological deficits resulting from vasculitides, arteriovenous malformations, hypoxic brain damage, and intracranial infections.
FUNCTIONAL
OUTCOME
IN BRAIN
The focus of the rehabilitation program was to optimize functional independence while educating the patient and family regarding medical care and prevention of complications. The components of the rehabilitation program included 2 to 3 hours of physical, occupational, and speech therapy daily from Monday to Friday, with rest over the weekends. Weekly team goal setting, weekly team conferencing, and discharge planning were also essential components of the program. As the patients were studied retrospectively. minor variations in the rehabilitation program may have existed; however, the gross structure of the stroke rehabilitation program remained largely unmodified over the study period. Data studied included age, sex, ethnic group, acute and rchabihtation length of stay, discharge disposition, nature of stroke (ischcmic or hemorrhagic), site and side of stroke. motor strength in the upper and lower extremities (Medical Research Council grading), pattern of motor weakness (hemiplegia or tetraplegia), and presence of ataxia, dysarthria, bulbar palsy, dysphagia, urinary incontinence, aspiration pneumonia, and urinary tract infection (UTI). Bulbar palsy was deemed to be present when there was diminished pharyngeal sensation and palatal elevation. For purposes of analysis, the motor strength of the extremities was categorized into less than grade 4, and grade 4 and above. Dysarthria and ataxia, if present, were graded as either mild or severe. Clinical swallowing evaluations for dysphagia and aspiration risk were done by qualified speech pathologists. These included assessment of the patient’s gag reflex, voluntary and reflex cough, reflexive and volitional swallow. and vocal quality. Patients were considered to have significant dysphagia if nasogastric tube feeding was required on admission to the acute stroke facility. The occurrence of aspiration pneumonia was defined as the presence of fever associated with focal chest and radiological signs, and UT1 was defined as the presence of 2 100,000 colonyforming units of bacteria in the urine, associated with fever and/ or urinary symptoms. Functional status on admission and discharge from rchabilitation was assessed using the Modified Barthel Index (MBI) for mobility and activities of daily living (ADL), which has a range of 0 to 100.” Other discharge parameters studied included feeding outcome (oral, nasogastric tube, percutaneous enterogastrostomy tube) and bladder management (spontaneous voiding, clean intermittent catheterization, indwelling catheter). Data were analyzed statistically using the Statistical Package for Social Sciences (SPSS for Windows). The paired r test was used for comparison of MBI on admission with MB1 on discharge and Fisher’s exact test was used for analysis of association between clinical variables. Multiple regression analysis (stepwise) was used to determine the effects of independent variables on functional outcome as defined by the total discharge MBI. Because of the relatively small sample size, only certain variables were analyzed. These were age, pattern of motor weakness, presence or absence of ataxia and urinary incontinence, and total MB1 on admission. The level of statistical significance was set at p < .05 for all tests. RESULTS There were 53 patients in the study, 31 women (59%) and 22 men (4 I %); 70% (37) were 65 years or younger. The mean age was 57.9 ? 11.9 years, with a range of 32 to 82 years. The study population was predominantly Chinese (48). and them were 3 Malay and 2 Indian patients. The mean length of stay in the acute facility was 25.8 -C 17.8 days, and in rehabilitation was 35.7 + 20.3 days. Nine patients had suffered previous strokes not involving the brainstem. Fifty-one (96%) patients
STEM
STROKES,
Table
195
Chua
1: Site of Stroke
Variables
Site of stroke Pons Cerebellum Medulla Midbrain Multiple sites Lower limb power Grade 3 and below Grade 4 and above Upper limb power Grade 3 and below Grade 4 and above
and Motor
Strength
NO.
%
29 12 5 1 6
55 23 9 2
20 33
38 62
24 29
45 55
11
n - 53.
were discharged home on completion of rehabilitation and 2 patients needed institutional care because of severe functional limitations and inadequate family support. On CT scan of the brain, there were 33 (62%) ischemic and 20 (38%) hemorrhagic strokes. Thirty-eight (72%) strokes were unilateral and 15 (28%) were bilateral. There were 26 (49%) and 12 (23%) right- and left-sided strokes, respectively. The pons was the most commonly involved site in 29 (55%) patients, followed by the cerebellum in 12 (23%) patients. Six patients ( I I%) had multiple site involvement of the brainstem (table 1). Limb weakness was the most common neurological deficit occurring in 50 (94%) patients, of which 35 (70%) were hemiplegic and 15 (30%) were tetraplegic; 3 (6%) patients presented with ataxia as the sole motor deficit. Using Fisher’s exact test, statistically significant improvements in upper and lower extremity motor strength were found on completion of rehabihtation (p < .OOl) Ataxia was present in 36 (68%) patients. In terms of severity, 16 (44%) were mild and 20 (56%) severe. Postrehabilitation, the number of severely ataxic patients decreased from 20 to 1 I and this improvement was significant. There were 16 patients with mild grades of ataxia on admission compared with 25 patients with similar grade of ataxia on discharge (p < .OOl). The most common cranial nerve palsies were ninth and tenth nerve palsies, occurring in 21 (40%) patients, 12 (23%) had lower motor facial nerve palsy, 6 (I 1%) had abducens nerve palsy, 5 (9%) had ptosis, and 5 (9%) had multiple cranial nerve palsies. Four (8%) patients presented with Homer syndrome as part of the lateral mcdullary syndrome. No patients in this cohort presented with features of the locked-in syndrome. Dysarthria was present in 47 (89%) patients, and this was mild in 43 and severe in 7. Twenty-one patients (40%) were assessed to be significantly dysphagic with risk of aspiration and all required tube feeding initially. The presence of dysphagia did not appear to be related to stroke site. We found that pontine lesions occurred in 7 of the dysphagics, medullary lesions in 5, ccrebellar lesions in 4, multiple site involvements in 4, and midbrain lesion in I patient. Intensive dysphagia rehabilitation resulted in only 6 patients needing tube feeding (4 nasogastric tube, 2 percutaneous enterogastrostomy tube) on discharge, and this improvement in swallowing status postrehabilitation was statistically significant (p < .OOl). Bulbar palsy, which was present in 16 patients (300/o), was also significantly related to dysphagia (p < .OOOl). The prcscnce of dysarthria was also significantly related to dysphagia @ < .05). Aspiration pneumonia was diagnosed in 8 patients (15%). 6 of whom were dysphagic and 2 of whom were normal swallowers. The associations between clinical aspiration and aspiration pneumonia, and between dysphagia and aspiration pneumonia, were statistically significant (p < .05).
Arch
Phys
Mad Rehabil
Vol77,
February
1996
196
FUNCTIONAL
Table
2: Clinical
Characteristics
of Patients
With
Urinary
OUTCOME
Incontinence
Bladder Management Patient NO.
Site of Stroke
1 2 3 4 5 6 7 8 9 10
Pons Midbrain Pons Pons Pons Pons Pons
11 12 13 14 15 16
Urodynamic Studies
Admission
Discharge
Polls
HC ND AC AC AC ND AC ND ND AC
RT RT IDC IDC IDC IDC IDC IDC RT IDC
RT RT CIC CIC RT RT IDC RT RT RT
Pons Cerebellum Pons Pons Cerebellum Pons
Normal AC ND ND ND AC
RT IDC RT RT RT IDC
RT LT RT RT RT
IN BRAIN
Urinary Retention Factors
FI FI DM FI DM DM FI DM FI FI DM DM FI
Abbreviations: HC, hypocontractility; ND, not done; AC, acontractility; RT, regular toiletting; IDC, indwelling catheter; CIC, clean intermittent catheterization; FI, fecal impaction; DM, diabetes mellitus.
Sixteen (30%) patients were incontinent of urine on admission to rehabilitation, 9 of whom were initially managed on indwelling catheters for poststroke retention of urine and the remaining 7 of whom were on external collecting devices. Urodynamic studies were performed in 9 of the 16 incontinents. Seven of these 9 who were initially managed on indwelling catheters had detrusor acontractility demonstrated by urodynamits. Six of 7 patients with acontractile bladders had pontine strokes, 1 had cerebellar involvement. Fecal impaction and diabetes mellitus were thought to be contributory to urinary retention in 7 and 6 cases, respectively (table 2). Ten patients remained incontinent on discharge despite starting bladder training programs (p < .05). Three patients were discharged on catheter programs for persistent detrusor acontractility (2 on intermittent catheterization and 1 on indwelling catheter), and the remaining 7 were on external collecting devices. Symptomatic UT1 was present in 7 of the 16 incontinent patients (44%) and this correlated significantly with the presence of urinary incontinence @ < .05). The mean MB1 on admission and discharge were 43.4 + 3 1.9 and 64.8 ? 32.4 respectively and this difference was significant @ < .OOl). Similar improvements were also noted when the ADL and mobility subsets of the MB1 were compared (table 3). On completion of rehabilitation, 96% (51) were discharged home except for 2 who needed institutional care because of severe functional limitations. Multiple regression analysis (stepwise) of selected factors believed to influence outcome was done. These factors included age, pattern of motor weakness (hemiplegia/tetraplegia), presence or absence of ataxia, and the total admission MBI. Multiple regression analysis of factors influencing functional outcome revealed that the only significant factor was total MB1 on admission (/I = 597, p < .OOOl). Thus, patients with lower MB1 scores on admission had worse functional outcome. When MB1 on admission was used as the sole variable to predict functional outcome, an adjusted R2 of .476 was obtained (p < .OOOl).
STEM
STROKES,
the same rehabilitation unit.’ Discharge disposition was favorable, with 96% (51) patients returning home on completion of rehabilitation. Several factors could have contributed to this favorable outcome: (1) physiatric preselection before admission to rehabilitation of patients with higher outcome expectations and rehabilitation potential; (2) the exclusion of patients with a higher likelihood of dependence on caregivers, ie, the severely cognitively impaired and those with minimally responsive states or locked-in syndromes who were unable to follow simple instructions, meant that the chances of institutionalization on discharge would be lower. The incidence of dysphagia in brain stem stroke patients has not been widely studied. Horner and colleagues8 found that 70% of a cohort of 23 brain stem strokes had dysphagia and aspiration on videofluoroscopic examination, compared with about 50% in a series of patients with bilateral strokes” and 30% in a mixed stroke sample.“’ The 40% incidence in our study is probably an underestimate, as videofluoroscopy was not performed. It has been well documented that clinical dysphagia assessment alone potentially underestimates the true incidence of aspiration by as much as 40%.” This is probably the reason for the 2 patients with aspiration pneumonia who were assessed to be safe swallowers, as they were probably silent aspirators. Future routine use of videofluoroscopy as part of the swallowing assessment may enhance the detection of silent aspirators. Homer’ found that aspiration was significantly correlated with ninth cranial nerve abnormality, severe dysarthria, vocal fold weakness, and the presence of postswallow pharyngeal residue on videofluroscopy. The results in our study concurred with hers, with significant correlations between bulbar palsy and dysphagia, dysarthria and dysphagia, and dysphagia and aspiration. It is not surprising that the number of patients with bulbar palsy is less that those with dysphagia because the mechanics of normal swallowing consist not only of intact palatal sensation and elevation, but involve complex, dynamic, and coordinated interactions between the oral, hypoglossal, and pharyngeal musculature. It was also not unexpected that the dysphagic patients in our study would have a significantly higher incidence of aspiration pneumonia, compared with normal swallowers. It is also encouraging to note that 15 out of 21 dysphagic patients were successfully weaned from tube feeding after dysphagia management. The fact that 69.8% of patients had ataxia is not surprising, given the concentration of cerebellar tracts in the brain stem. Whether the improvement in ataxia noted in our study is a result of therapeutic intervention or spontaneous recovery or both is unknown. The incidence of urinary incontinence of 30% in this study is lower compared with the incidence in other stroke studies.” This is partly because the continence status of our patients was assessed at the time of admission to rehabilitation when partial recovery from the initial poststroke drowsiness and mental confusion that are associated with a higher incidence of incontinence may have occurred. Although it was not possible to make meaningful correlations between detrusor behavior and lesion site in these patients because not all patients underwent urodynamics, it was noteworthy that 6 out of 7 patients with acontractile bladders had pontine involvement. It has been postulated Table
DISCUSSION This study demonstrates quantitatively the significant functional gains in mobility and ADL as measured by the Modified Barthel Index made by a cohort of brain stem stroke patients during inpatient rehabilitation. The length of stay in rehabilitation was comparable to other mixed stroke patients admitted to
Arch
Phys
Med Rehabil
Vol77,
February
1996
Chua
3: Mean Barthel Scores on Admission and Discharge from Rehabiliiation
Total Bar-the1 score ADL subset score Mobility subset score Scores
listed
as mean
(SD).
Admission
Discharge
p Value
43.4 (31.9) 28.7 (20.0) 14.6 (13.7)
64.8 (32.4) 41.6 (19.7) 24.7 (13.9)
c.001 <.OOl <.OOl
FUNCTIONAL
OUTCOME
IN BRAIN
from animal studies that facilitatory micturition centers exist in the anterior pons, hence damage to these centers by vascular lesions could result in detrusor acontractility or hypocontractility.” Treatable contributory factors such as fecal impaction and unrecognized bladder overdistension should be managed promptly. Outcome studies in strokes in general have shown that the most powerful predictor of functional recovery among stroke survivors is the initial severity of the stroke. Poorer functional outcomes are found in patients with more severe initial disabilities.” ” It was also not surprising that total MB1 on admission was the most significant clinical variable affecting outcome in our study. Its strong influence can be inferred from the fact that it accounted for almost 50% of the explained variance of MB1 on discharge. This study shows that despite the occurrence of multiple physical deficits after vascular insult to the brain stem, this group of brain stem stroke patients clearly makes significant functional gains in mobility and self-care skills with significant improvements in motor strength, severity of ataxia. continence, and swallowing status after rehabilitation. A comparison study by Tumey and associates’ of patients with hemispheric and brain stem infarctions also found that the survivors of brain stem infarctions had better functional outcomes compared with the outcomes of survivors of hemispheric infarction. They concluded that this may have been a consequence of a higher proportion of cognitive and sensory impairments present in the survivors of carotid strokes. The presence and dcgrec of cognitive and sensory impairments in our cohort of brain stem stroke patients was not studied and it would be interesting to determine if this had any influence on functional outcome and discharge placement, bearing in mind that those who could not obey simple instructions were excluded from the rehabilitation program. Brain stem stroke patients as a whole are a hetcrogcncous group in terms of pathophysiology, symptomatology, and prognosis. Large lesions (brain stem hemorrhages) may result in death in the first 30 days.” whereas patients with lacunar syndromes
may
have
only
mild
better functional outcome. The functional improvements tion could concurrently
have been because with therapeutic
motor
deficits
documented of spontaneous intervention
with
predictably
during rehabilita-
recovery occuring or solely due to reha-
bilitation or intrinsic recovery. Further studies arc needed to determine the relative contribution of each component to the recovery process. What clinical implications may we draw from this study? In our local context where rehabilitation beds and services arc limited, this study may imply that the survivors of potentially devastating brain stem strokes should not be denied early physiatric
intervention
and
inpatient
rehabilitation
because
of
their
STEM
multiple to make itation
STROKES,
initial significant
197
Chua
physical
impairments.
functional
as they
recovery
during
with future impact on reintegration
have
the
inpatient
potential rehabil-
hack into the commu-
nity. References I. Report on registration of births and deaths 1993. Singapore: Rcgistry of Births and Deaths. National Registration Department, 1993. 2. John CM. Brust L. Cerebral infarction. In: Rowland LP. editor. Men-it’s textbook of neurology. Philadelphia: Lea and Fcbiger. 1984: 162-9. .3 Wade DT. Langton Hewer R, Skilbeck CE, David RM. Epidcmiology of stroke. In: Wade DT. Langton Hewer R. Skilbcck CE. David RM. editors. Stroke: a critical approach to diagnosis. treatment and management. London: Chapman and Hall Ltd. 19855-20. 4. Garrison SJ. Rolak LA. Rehabilitation of the stroke patient. In: DeLisa JA. Cans BM. editors. Rehabilitation medicine: principles and praclicc. Philadelphia: Lippincott, 1993:801-24. 5. Tumey TM. Garraway MC. Whishnant JP. The natural history of hemispheric and brainstem infarction in Rochester, Minnesota. Stroke 1984; 15:790-4. 6. Shah A. Vanclay F, Cooper B. Improving the sensitivity of the Barthel index for stroke rehabilitation. J Clin Epidemiol 1989;42:703-9. 7. FR CH, Kwan PE. Tan ES. Stroke rehabilitation of elderly patients in Singapore. Singapore Med J 1991;32:55-60. 8. Homer J. Buoyer FG. Alberts MJ. Helms MJ. Dysphagia following brainstem stroke. Arch Ncurol I991 ;48: I 170-3. 9. Homer J, Massey EW. Brazer SR. Dysphagia after bilateral stroke. Neurology I990:40: 1686-8. IO. Homer J, Massey EW, Riski JE, Lathrop DL. Chase KN. Aspiration following stroke: clinical correlates and outcome. Neurology 1988; 38: 1359-62. 1 I. Splaingard ML. Hutchins B. Sulron LD, Chaudhuri G. Aspiration in rehabilitation patients: videolluoroscopy vs bedside clinical assessmcnl. Arch Phys Med Rchahil 1988;69:637-40. 12. Brocklchurst JC. Andrews K. Richards B. Laycock PJ. Incidence and correlates in continence in stroke patienrs. J Am Gcriatr Sot 1985;33:540-2. 13. Van Arslen K. Wcin AJ. Physiology of micturition and continence. In: Krane RJ, Siroky MB. editors. Clinical neurourology. Boston: LitlIe, Brown, 19X9:25-82. 14. Dombovy ML, Sandok BA. Basford JR. Rehabilitation for stroke: a review. Stroke 19X6: t7:363-9. IS. Jongbloed L. Prediction of function after stroke: a critical review. Stroke 1986; l7:765-76. 16. Wade DT, Langton-Hewer R. Funclional abilities after stroke: mcasurement. natural history and prognosis. J Neurol Ncurosurg Psychiatry 1987;50:177-82. 17. Granger CV. Hamilton BB, Grcsham GE. The stroke rehabilitation outcome study, Part I: general description. Arch Phys Mcd Rchahil 1988;69:5Of-9. 18. Anderson CS. Charkera TM. Stewart-Wynnc EC, Jamrozik KD. Spectrum of primary intracerebral haemorrhagc in Perth, Western Australia. 1989-90: incidence and outcome. J Neurol Neurosug Psychiatry 1994; 57:936-40.
Arch
Phys Med
Rehabil
Vol77,
February
1996
Functional Outcome in Brain Stem Stroke Patients After Rehabilitation Karen S.G. Chua, MBBS, Keng-He Kong, MBBS ABSTRACT. Chua KSG, Kong K-H. Functional outcome in brain stem stroke patients after rehabilitation. Arch Phys Med Rehabil 1996; 77: 194-7.
Objective: To document functional outcome before and after rehabilitation in a group of brain stem stroke patients and to analyze possible factors influencing outcome. Design and Setting: A case series of 53 consecutive inpatients admitted to a rehabilitation facility with confirmed brain stem strokes over a period of 6 years. Patients and Outcome Measures: Patients were selected by physiatrists for admission into the rehabilitation program. Outcome was measured by the Modified Barthel Index (MBI) for mobility and activities of daily living. Results: The mean age of this cohort was 57.9 ? 11.9 years and the ports was involved in 55% of cases. Ataxia (68%) and hemiplegia (70%) were the most frequent neurological deficits. Twenty-one patients (40%) had significant dysphagia with risk of aspiration and 16 patients (30%) were incontinent of urine. Aspiration pneumonia and urinary tract infection were present in 8 (15%) and 13 (25%) patients, respectively. Significant improvements in functional status, motor strength, swallowing, and continence status were documented on discharge (p < .05). The total admission MB1 was the only significant factor influencing total discharge Bartbel Index (p = .597, adjusted R2 = .476, p < .OOOl). Fifty-one (96%) were discharged home after rehabilitation. Conclusions: Despite multiple physical deficits, this cohort of brain stem stroke patients made functional gains during rehabilitation with significant improvements in mobility and selfcare skills, motor strength, severity of ataxia, continence and swallowing status. 0 1996 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation
S
TROKE was the third leading cause of death in Singapore in 1993, accounting for 54.9 deaths per 100,000 population.’ Although improved management of hypertension and coronary artery disease, as well as lifestyle changes, have resulted in declining stroke incidence, a significant number of stroke survivors are left with residual disabilities. Strokes affecting the brain stem are usually the result of infarction of the vertebral or basilar arteries. Mixed or incomplete clinical syndromes are usually encountered more often than the classical medial or lateral brain stem syndromes.’ From the Departnient of Rehabilitation Medicine, Singapore. Submitted for publication April I I, 1995. Accepted
Tan
Tack
in revised
Seng Hospital, form August
21,
199.5. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Reprint requests to Dr. Karen S.G. Chua, Department of Rehabilitation Medicine, Tan Tack Seng Hospital, c/o 17, Ang MO Kio Avenue 9, Singapore 2056, Singapore. 0 I996 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation
0003.9993/96i7702-3475$3,00/O
Arch
Phys Msd
Rehabil
Vol77,
February
1666
Hence, the clinical picture is often heterogenous. Patients with brain stem infarction may present with bilateral long tract motor and sensory signs, crossed motor and sensory signs, dissociated sensory loss with Homer syndrome (lateral medullary syndrome), cerebellar signs, stupor or coma, unilateral deafness, or pharyngeal weakness. Brain stem strokes are believed to be less common than strokes involving other regions of the brain and the true incidence of brain stem strokes is not known.’ The outcome of these patients depends on the site and nature (infarction/hemorrhage) of the stroke. In general, the survivors of brain stem strokes have excellent prognosis for functional recovery compared with survivors of hemispheric strokes because the vascular lesions affect smaller penetrating blood vessels that emerge directly from the vertebrobasilar arteries4 Survivors of brain stem strokes were also reported to have increased probability of long-term survival compared with survivors with hemispheric infarctions.5 The incidence of dysphagia, aspiration, and ataxia in these patients has not been well studied. To date, no detailed studies have been reported documenting functional outcome quantitatively in these patients. This study was conducted to objectively quantify the prerehabilitation and postrehabilitation functional outcomes of a group of brain stem strokes patients admitted for inpatient rehabilitation, define the types of neurological deficits present, determine factors influencing functional outcomes and suggest clinical implications for rehabilitation in this group of stroke patients.
METHODS Brain stem stroke was defined as an acute onset of neurological deficit with clinical features of brain stem or cerebellar dysfunction lasting more than 24 hours together with computed tomography (CT) or magnetic resonance imaging (MRI) evidence of ischemic infarction or parenchymal hemorrhage unrelated to tumour, arteriovenous malformation, or trauma in a region within tbe brain stem or cerebellum. The diagnosis of stroke was made clinically by admitting stroke unit neurologists and radiographically confirmed on CT or MRI scans of the brain within 24 to 48 hours of hospital admission. The charts of 53 consecutive inpatients with brain stem strokes admitted to an inpatient rehabilitation facility were retrospectively reviewed over a 6-year period from 1989 through 1994. Patients were individually selected for rehabilitation by physiatrists. Criteria for admission to the rehabilitation program were the same for all patients. These criteria included the ability to obey simple instructions and participate in therapy, stable medical course, and the clinical judgement of the admitting physiatrist regarding the potential benefits of an inpatient rehabilitation program. Timing of discharge from rehabilitation was determined by the rehabilitation team and was considered when the patients had attained their initial functional goals set at the commencement of the program, or had reached a plateau of improvement, or when outpatient therapy was more appropriate. Exclusion criteria included patients with neurological deficits resulting from vasculitides, arteriovenous malformations, hypoxic brain damage, and intracranial infections.
FUNCTIONAL
OUTCOME
IN BRAIN
The focus of the rehabilitation program was to optimize functional independence while educating the patient and family regarding medical care and prevention of complications. The components of the rehabilitation program included 2 to 3 hours of physical, occupational, and speech therapy daily from Monday to Friday, with rest over the weekends. Weekly team goal setting, weekly team conferencing, and discharge planning were also essential components of the program. As the patients were studied retrospectively. minor variations in the rehabilitation program may have existed; however, the gross structure of the stroke rehabilitation program remained largely unmodified over the study period. Data studied included age, sex, ethnic group, acute and rchabihtation length of stay, discharge disposition, nature of stroke (ischcmic or hemorrhagic), site and side of stroke. motor strength in the upper and lower extremities (Medical Research Council grading), pattern of motor weakness (hemiplegia or tetraplegia), and presence of ataxia, dysarthria, bulbar palsy, dysphagia, urinary incontinence, aspiration pneumonia, and urinary tract infection (UTI). Bulbar palsy was deemed to be present when there was diminished pharyngeal sensation and palatal elevation. For purposes of analysis, the motor strength of the extremities was categorized into less than grade 4, and grade 4 and above. Dysarthria and ataxia, if present, were graded as either mild or severe. Clinical swallowing evaluations for dysphagia and aspiration risk were done by qualified speech pathologists. These included assessment of the patient’s gag reflex, voluntary and reflex cough, reflexive and volitional swallow. and vocal quality. Patients were considered to have significant dysphagia if nasogastric tube feeding was required on admission to the acute stroke facility. The occurrence of aspiration pneumonia was defined as the presence of fever associated with focal chest and radiological signs, and UT1 was defined as the presence of 2 100,000 colonyforming units of bacteria in the urine, associated with fever and/ or urinary symptoms. Functional status on admission and discharge from rchabilitation was assessed using the Modified Barthel Index (MBI) for mobility and activities of daily living (ADL), which has a range of 0 to 100.” Other discharge parameters studied included feeding outcome (oral, nasogastric tube, percutaneous enterogastrostomy tube) and bladder management (spontaneous voiding, clean intermittent catheterization, indwelling catheter). Data were analyzed statistically using the Statistical Package for Social Sciences (SPSS for Windows). The paired r test was used for comparison of MBI on admission with MB1 on discharge and Fisher’s exact test was used for analysis of association between clinical variables. Multiple regression analysis (stepwise) was used to determine the effects of independent variables on functional outcome as defined by the total discharge MBI. Because of the relatively small sample size, only certain variables were analyzed. These were age, pattern of motor weakness, presence or absence of ataxia and urinary incontinence, and total MB1 on admission. The level of statistical significance was set at p < .05 for all tests. RESULTS There were 53 patients in the study, 31 women (59%) and 22 men (4 I %); 70% (37) were 65 years or younger. The mean age was 57.9 ? 11.9 years, with a range of 32 to 82 years. The study population was predominantly Chinese (48). and them were 3 Malay and 2 Indian patients. The mean length of stay in the acute facility was 25.8 -C 17.8 days, and in rehabilitation was 35.7 + 20.3 days. Nine patients had suffered previous strokes not involving the brainstem. Fifty-one (96%) patients
STEM
STROKES,
Table
195
Chua
1: Site of Stroke
Variables
Site of stroke Pons Cerebellum Medulla Midbrain Multiple sites Lower limb power Grade 3 and below Grade 4 and above Upper limb power Grade 3 and below Grade 4 and above
and Motor
Strength
NO.
%
29 12 5 1 6
55 23 9 2
20 33
38 62
24 29
45 55
11
n - 53.
were discharged home on completion of rehabilitation and 2 patients needed institutional care because of severe functional limitations and inadequate family support. On CT scan of the brain, there were 33 (62%) ischemic and 20 (38%) hemorrhagic strokes. Thirty-eight (72%) strokes were unilateral and 15 (28%) were bilateral. There were 26 (49%) and 12 (23%) right- and left-sided strokes, respectively. The pons was the most commonly involved site in 29 (55%) patients, followed by the cerebellum in 12 (23%) patients. Six patients ( I I%) had multiple site involvement of the brainstem (table 1). Limb weakness was the most common neurological deficit occurring in 50 (94%) patients, of which 35 (70%) were hemiplegic and 15 (30%) were tetraplegic; 3 (6%) patients presented with ataxia as the sole motor deficit. Using Fisher’s exact test, statistically significant improvements in upper and lower extremity motor strength were found on completion of rehabihtation (p < .OOl) Ataxia was present in 36 (68%) patients. In terms of severity, 16 (44%) were mild and 20 (56%) severe. Postrehabilitation, the number of severely ataxic patients decreased from 20 to 1 I and this improvement was significant. There were 16 patients with mild grades of ataxia on admission compared with 25 patients with similar grade of ataxia on discharge (p < .OOl). The most common cranial nerve palsies were ninth and tenth nerve palsies, occurring in 21 (40%) patients, 12 (23%) had lower motor facial nerve palsy, 6 (I 1%) had abducens nerve palsy, 5 (9%) had ptosis, and 5 (9%) had multiple cranial nerve palsies. Four (8%) patients presented with Homer syndrome as part of the lateral mcdullary syndrome. No patients in this cohort presented with features of the locked-in syndrome. Dysarthria was present in 47 (89%) patients, and this was mild in 43 and severe in 7. Twenty-one patients (40%) were assessed to be significantly dysphagic with risk of aspiration and all required tube feeding initially. The presence of dysphagia did not appear to be related to stroke site. We found that pontine lesions occurred in 7 of the dysphagics, medullary lesions in 5, ccrebellar lesions in 4, multiple site involvements in 4, and midbrain lesion in I patient. Intensive dysphagia rehabilitation resulted in only 6 patients needing tube feeding (4 nasogastric tube, 2 percutaneous enterogastrostomy tube) on discharge, and this improvement in swallowing status postrehabilitation was statistically significant (p < .OOl). Bulbar palsy, which was present in 16 patients (300/o), was also significantly related to dysphagia (p < .OOOl). The prcscnce of dysarthria was also significantly related to dysphagia @ < .05). Aspiration pneumonia was diagnosed in 8 patients (15%). 6 of whom were dysphagic and 2 of whom were normal swallowers. The associations between clinical aspiration and aspiration pneumonia, and between dysphagia and aspiration pneumonia, were statistically significant (p < .05).
Arch
Phys
Mad Rehabil
Vol77,
February
1996
196
FUNCTIONAL
Table
2: Clinical
Characteristics
of Patients
With
Urinary
OUTCOME
Incontinence
Bladder Management Patient NO.
Site of Stroke
1 2 3 4 5 6 7 8 9 10
Pons Midbrain Pons Pons Pons Pons Pons
11 12 13 14 15 16
Urodynamic Studies
Admission
Discharge
Polls
HC ND AC AC AC ND AC ND ND AC
RT RT IDC IDC IDC IDC IDC IDC RT IDC
RT RT CIC CIC RT RT IDC RT RT RT
Pons Cerebellum Pons Pons Cerebellum Pons
Normal AC ND ND ND AC
RT IDC RT RT RT IDC
RT LT RT RT RT
IN BRAIN
Urinary Retention Factors
FI FI DM FI DM DM FI DM FI FI DM DM FI
Abbreviations: HC, hypocontractility; ND, not done; AC, acontractility; RT, regular toiletting; IDC, indwelling catheter; CIC, clean intermittent catheterization; FI, fecal impaction; DM, diabetes mellitus.
Sixteen (30%) patients were incontinent of urine on admission to rehabilitation, 9 of whom were initially managed on indwelling catheters for poststroke retention of urine and the remaining 7 of whom were on external collecting devices. Urodynamic studies were performed in 9 of the 16 incontinents. Seven of these 9 who were initially managed on indwelling catheters had detrusor acontractility demonstrated by urodynamits. Six of 7 patients with acontractile bladders had pontine strokes, 1 had cerebellar involvement. Fecal impaction and diabetes mellitus were thought to be contributory to urinary retention in 7 and 6 cases, respectively (table 2). Ten patients remained incontinent on discharge despite starting bladder training programs (p < .05). Three patients were discharged on catheter programs for persistent detrusor acontractility (2 on intermittent catheterization and 1 on indwelling catheter), and the remaining 7 were on external collecting devices. Symptomatic UT1 was present in 7 of the 16 incontinent patients (44%) and this correlated significantly with the presence of urinary incontinence @ < .05). The mean MB1 on admission and discharge were 43.4 + 3 1.9 and 64.8 ? 32.4 respectively and this difference was significant @ < .OOl). Similar improvements were also noted when the ADL and mobility subsets of the MB1 were compared (table 3). On completion of rehabilitation, 96% (51) were discharged home except for 2 who needed institutional care because of severe functional limitations. Multiple regression analysis (stepwise) of selected factors believed to influence outcome was done. These factors included age, pattern of motor weakness (hemiplegia/tetraplegia), presence or absence of ataxia, and the total admission MBI. Multiple regression analysis of factors influencing functional outcome revealed that the only significant factor was total MB1 on admission (/I = 597, p < .OOOl). Thus, patients with lower MB1 scores on admission had worse functional outcome. When MB1 on admission was used as the sole variable to predict functional outcome, an adjusted R2 of .476 was obtained (p < .OOOl).
STEM
STROKES,
the same rehabilitation unit.’ Discharge disposition was favorable, with 96% (51) patients returning home on completion of rehabilitation. Several factors could have contributed to this favorable outcome: (1) physiatric preselection before admission to rehabilitation of patients with higher outcome expectations and rehabilitation potential; (2) the exclusion of patients with a higher likelihood of dependence on caregivers, ie, the severely cognitively impaired and those with minimally responsive states or locked-in syndromes who were unable to follow simple instructions, meant that the chances of institutionalization on discharge would be lower. The incidence of dysphagia in brain stem stroke patients has not been widely studied. Horner and colleagues8 found that 70% of a cohort of 23 brain stem strokes had dysphagia and aspiration on videofluoroscopic examination, compared with about 50% in a series of patients with bilateral strokes” and 30% in a mixed stroke sample.“’ The 40% incidence in our study is probably an underestimate, as videofluoroscopy was not performed. It has been well documented that clinical dysphagia assessment alone potentially underestimates the true incidence of aspiration by as much as 40%.” This is probably the reason for the 2 patients with aspiration pneumonia who were assessed to be safe swallowers, as they were probably silent aspirators. Future routine use of videofluoroscopy as part of the swallowing assessment may enhance the detection of silent aspirators. Homer’ found that aspiration was significantly correlated with ninth cranial nerve abnormality, severe dysarthria, vocal fold weakness, and the presence of postswallow pharyngeal residue on videofluroscopy. The results in our study concurred with hers, with significant correlations between bulbar palsy and dysphagia, dysarthria and dysphagia, and dysphagia and aspiration. It is not surprising that the number of patients with bulbar palsy is less that those with dysphagia because the mechanics of normal swallowing consist not only of intact palatal sensation and elevation, but involve complex, dynamic, and coordinated interactions between the oral, hypoglossal, and pharyngeal musculature. It was also not unexpected that the dysphagic patients in our study would have a significantly higher incidence of aspiration pneumonia, compared with normal swallowers. It is also encouraging to note that 15 out of 21 dysphagic patients were successfully weaned from tube feeding after dysphagia management. The fact that 69.8% of patients had ataxia is not surprising, given the concentration of cerebellar tracts in the brain stem. Whether the improvement in ataxia noted in our study is a result of therapeutic intervention or spontaneous recovery or both is unknown. The incidence of urinary incontinence of 30% in this study is lower compared with the incidence in other stroke studies.” This is partly because the continence status of our patients was assessed at the time of admission to rehabilitation when partial recovery from the initial poststroke drowsiness and mental confusion that are associated with a higher incidence of incontinence may have occurred. Although it was not possible to make meaningful correlations between detrusor behavior and lesion site in these patients because not all patients underwent urodynamics, it was noteworthy that 6 out of 7 patients with acontractile bladders had pontine involvement. It has been postulated Table
DISCUSSION This study demonstrates quantitatively the significant functional gains in mobility and ADL as measured by the Modified Barthel Index made by a cohort of brain stem stroke patients during inpatient rehabilitation. The length of stay in rehabilitation was comparable to other mixed stroke patients admitted to
Arch
Phys
Med Rehabil
Vol77,
February
1996
Chua
3: Mean Barthel Scores on Admission and Discharge from Rehabiliiation
Total Bar-the1 score ADL subset score Mobility subset score Scores
listed
as mean
(SD).
Admission
Discharge
p Value
43.4 (31.9) 28.7 (20.0) 14.6 (13.7)
64.8 (32.4) 41.6 (19.7) 24.7 (13.9)
c.001 <.OOl <.OOl
FUNCTIONAL
OUTCOME
IN BRAIN
from animal studies that facilitatory micturition centers exist in the anterior pons, hence damage to these centers by vascular lesions could result in detrusor acontractility or hypocontractility.” Treatable contributory factors such as fecal impaction and unrecognized bladder overdistension should be managed promptly. Outcome studies in strokes in general have shown that the most powerful predictor of functional recovery among stroke survivors is the initial severity of the stroke. Poorer functional outcomes are found in patients with more severe initial disabilities.” ” It was also not surprising that total MB1 on admission was the most significant clinical variable affecting outcome in our study. Its strong influence can be inferred from the fact that it accounted for almost 50% of the explained variance of MB1 on discharge. This study shows that despite the occurrence of multiple physical deficits after vascular insult to the brain stem, this group of brain stem stroke patients clearly makes significant functional gains in mobility and self-care skills with significant improvements in motor strength, severity of ataxia. continence, and swallowing status after rehabilitation. A comparison study by Tumey and associates’ of patients with hemispheric and brain stem infarctions also found that the survivors of brain stem infarctions had better functional outcomes compared with the outcomes of survivors of hemispheric infarction. They concluded that this may have been a consequence of a higher proportion of cognitive and sensory impairments present in the survivors of carotid strokes. The presence and dcgrec of cognitive and sensory impairments in our cohort of brain stem stroke patients was not studied and it would be interesting to determine if this had any influence on functional outcome and discharge placement, bearing in mind that those who could not obey simple instructions were excluded from the rehabilitation program. Brain stem stroke patients as a whole are a hetcrogcncous group in terms of pathophysiology, symptomatology, and prognosis. Large lesions (brain stem hemorrhages) may result in death in the first 30 days.” whereas patients with lacunar syndromes
may
have
only
mild
better functional outcome. The functional improvements tion could concurrently
have been because with therapeutic
motor
deficits
documented of spontaneous intervention
with
predictably
during rehabilita-
recovery occuring or solely due to reha-
bilitation or intrinsic recovery. Further studies arc needed to determine the relative contribution of each component to the recovery process. What clinical implications may we draw from this study? In our local context where rehabilitation beds and services arc limited, this study may imply that the survivors of potentially devastating brain stem strokes should not be denied early physiatric
intervention
and
inpatient
rehabilitation
because
of
their
STEM
multiple to make itation
STROKES,
initial significant
197
Chua
physical
impairments.
functional
as they
recovery
during
with future impact on reintegration
have
the
inpatient
potential rehabil-
hack into the commu-
nity. References I. Report on registration of births and deaths 1993. Singapore: Rcgistry of Births and Deaths. National Registration Department, 1993. 2. John CM. Brust L. Cerebral infarction. In: Rowland LP. editor. Men-it’s textbook of neurology. Philadelphia: Lea and Fcbiger. 1984: 162-9. .3 Wade DT. Langton Hewer R, Skilbeck CE, David RM. Epidcmiology of stroke. In: Wade DT. Langton Hewer R. Skilbcck CE. David RM. editors. Stroke: a critical approach to diagnosis. treatment and management. London: Chapman and Hall Ltd. 19855-20. 4. Garrison SJ. Rolak LA. Rehabilitation of the stroke patient. In: DeLisa JA. Cans BM. editors. Rehabilitation medicine: principles and praclicc. Philadelphia: Lippincott, 1993:801-24. 5. Tumey TM. Garraway MC. Whishnant JP. The natural history of hemispheric and brainstem infarction in Rochester, Minnesota. Stroke 1984; 15:790-4. 6. Shah A. Vanclay F, Cooper B. Improving the sensitivity of the Barthel index for stroke rehabilitation. J Clin Epidemiol 1989;42:703-9. 7. FR CH, Kwan PE. Tan ES. Stroke rehabilitation of elderly patients in Singapore. Singapore Med J 1991;32:55-60. 8. Homer J. Buoyer FG. Alberts MJ. Helms MJ. Dysphagia following brainstem stroke. Arch Ncurol I991 ;48: I 170-3. 9. Homer J, Massey EW. Brazer SR. Dysphagia after bilateral stroke. Neurology I990:40: 1686-8. IO. Homer J, Massey EW, Riski JE, Lathrop DL. Chase KN. Aspiration following stroke: clinical correlates and outcome. Neurology 1988; 38: 1359-62. 1 I. Splaingard ML. Hutchins B. Sulron LD, Chaudhuri G. Aspiration in rehabilitation patients: videolluoroscopy vs bedside clinical assessmcnl. Arch Phys Med Rchahil 1988;69:637-40. 12. Brocklchurst JC. Andrews K. Richards B. Laycock PJ. Incidence and correlates in continence in stroke patienrs. J Am Gcriatr Sot 1985;33:540-2. 13. Van Arslen K. Wcin AJ. Physiology of micturition and continence. In: Krane RJ, Siroky MB. editors. Clinical neurourology. Boston: LitlIe, Brown, 19X9:25-82. 14. Dombovy ML, Sandok BA. Basford JR. Rehabilitation for stroke: a review. Stroke 19X6: t7:363-9. IS. Jongbloed L. Prediction of function after stroke: a critical review. Stroke 1986; l7:765-76. 16. Wade DT, Langton-Hewer R. Funclional abilities after stroke: mcasurement. natural history and prognosis. J Neurol Ncurosurg Psychiatry 1987;50:177-82. 17. Granger CV. Hamilton BB, Grcsham GE. The stroke rehabilitation outcome study, Part I: general description. Arch Phys Mcd Rchahil 1988;69:5Of-9. 18. Anderson CS. Charkera TM. Stewart-Wynnc EC, Jamrozik KD. Spectrum of primary intracerebral haemorrhagc in Perth, Western Australia. 1989-90: incidence and outcome. J Neurol Neurosug Psychiatry 1994; 57:936-40.
Arch
Phys Med
Rehabil
Vol77,
February
1996