Abstract
Purpose:
The purpose of this study was to assess the impact of time to initiation of acute rehabilitation therapy on disability following intracerebral hemorrhage (ICH) and to identify predictors of time to initiation of rehabilitation therapy.
Methods:
Consecutive adults admitted to a stroke center with ICH were prospectively identified. Disability was assessed with the modified Rankin Scale (mRS), with poor outcome defined as mRS 4-6 (dependence or worse). Time to initiation of acute rehabilitation therapy was defined as time from hospital admission to first acute rehabilitation therapy (physical, occupational, or speech) consult. A multivariable logistic regression model assessed the effect of time to initiation of rehabilitation therapy on poor outcome at 30 and 90 days. A multivariable linear regression model identified the predictors of time to initiation of rehabilitation therapy.
Results:
Among the 203 participants analyzed (mean age 63.7 years; 51.2% female; 52.7% white), the median number of days from hospital admission to initiation of acute rehabilitation therapy was 3 [2 – 7] days. Multivariable models indicated that each additional day between admission and initiation of acute rehabilitation therapy resulted in increased odds of poor outcome at 30 days (adjusted OR=1.151, 95% CI: 1.044-1.268, p=0.005) and at 90 days (adjusted OR=1.107, 95% CI: 1.003-1.222, p=0.044) for patients with ICH. Current alcohol use, lower Glasgow Coma Scale, pre-morbid mRS < 4, presence of pulmonary embolism and longer length of stay were independent predictors of later initiation of acute rehabilitation therapy.
Conclusions:
Longer time to initiation of acute rehabilitation therapy following ICH has persistent effects on post-stroke disability. Delays in acute rehabilitation therapy consults should be minimized and may improve outcomes after ICH.
Keywords: rehabilitation, intracerebral hemorrhage, MRS, health services research
Introduction
Rehabilitation therapy is a key component to reducing post-stroke disability, mortality, dependency, and institutionalization and to improving physical and cognitive function.1,2 Rehabilitation therapy is especially important for intracerebral hemorrhage (ICH) which typically leaves patients with substantial disability.3,4 While clinical practice guidelines and hospital quality measures indicate that post-stroke rehabilitation should be implemented in a timely manner to optimize recovery and reduce disability, particularly after ICH,2,5,6 the timing of initiation of rehabilitation therapy remains controversial.7–9 Current treatment trends show that patients admitted to rehabilitation facilities initiate rehabilitation therapy within 2 weeks of stroke onset and most clinical recommendations suggest that the first 30 days after stroke are critical for treatment initiation and function recovery.10,11
Less is known, however, about optimal time for initiation of acute rehabilitation therapy prior to admission to rehabilitation facilities (i.e., while receiving acute medical services within hospitals). Several studies have reported positive outcomes associated with early initiation of rehabilitation therapy,12–14 while others observed that early rehabilitation (e.g., within 24 hours) increases the odds of mortality, especially for patients with hemorrhagic strokes.7,15,16 Inconsistent definitions for what constitutes early initiation of acute rehabilitation likely contributes to the conflicting results reported in the literature. The current study aimed to answer two distinct questions: (1) what are the effects of time to initiation of acute rehabilitation therapy during hospitalization in terms of disability after ICH, and (2) which patient characteristics most impact time to initiation of acute rehabilitation therapy.
Methods
Participants:
The sample was comprised of adults with ICH admitted to a single large comprehensive stroke center who were enrolled in a longitudinal observational study of post-stroke outcomes between 2007 and 2015. Patients were prospectively assessed by a neurologist, with confirmation of ICH by computed tomography. Demographic (e.g., age, sex, race), clinical characteristics (e.g., risk factors, comorbidities, complications), and rehabilitation data (i.e., physical, occupational and speech therapy) were retrieved from the institution’s Enterprise Data Warehouse, an integrated electronic health-record database. Participants were excluded from the analysis if 1) they died within one day of admission; 2) left the hospital against medical advice; 3) their total length of stay (LOS) was less than one day; or 4) their total LOS was more than 30 days to mitigate bias from statistical outliers.
Human Subjects Protection:
Informed consent to record data and identifiers was obtained from the patient or a legally authorized representative. The Institutional Review Board waived the requirement of consent for patients who could not be consented (e.g., due to coma) and for whom no legally authorized representative be located.
Measures:
Time to initiation of acute rehabilitation therapy was defined as the number of days between hospital admission and the first consult by any rehabilitation therapy specialist (e.g., physical therapy, occupational therapy, speech therapy) during the index stroke hospitalization. Disability status was assessed through a standardized telephone interview at 30 and 90 days with the modified Rankin Scale (mRS), a common post-stroke outcome measure of global disability with scores that range from 0 (no symptoms) to 6 (dead).17,18 A score of 4 through 6, dependence or worse, was considered to be a poor outcome, as is typical for hemorrhagic stroke studies. Modified ranking scale scores below 4 grouped individuals with no symptoms and those with moderate symptoms who are able to ambulate independently. Stroke severity at admission was assessed using the National Institute of Health Stroke Scale (NIHSS), the Glasgow Coma Scale (GCS), the ICH score, and ventilator free days.19–21 Because ventilator free days was so highly left skewed (with ceiling effects), this variable was discretized (i.e., ventilator free days = 14 or <14 days, which refers to intubation or no intubation within the first 14 days from admission.
Statistical analysis:
In order to quantify the effect of time to initiation of rehabilitation therapy on 30- and 90-day outcomes, we attempted to employ a multivariable ordinal regression model predicting post-stroke disability (ordinal mRS), but the model failed to meet the proportional odds assumption. Non-normally distributed data are presented as median and interquartile range. We subsequently fit a multivariable logistic regression model with poor outcome defined as mRS ≥ 4. Estimates of odds ratios (OR) and 95% confidence intervals (CI) were calculated controlling for covariates known to predict poor outcome at 30 days, specifically age, pre-morbid mRS score, GCS score, NIHSS score and ICH score.22,23 However, pre-morbid mRS was dropped from this analysis due to data sparseness (i.e., no participants with premorbid mRS ≥ 4 and follow-up mRS < 4). Post estimation assessment of variance inflation factors indicated that age and GCS scores were collinear with ICH scores, so these predictors were also dropped from this multivariable model (Table 2).
Table 2.
Effects of time to initiation of rehabilitation services and stroke severity on disability at 30 and 90 days
| mRS ≥ 4 at 30 days (n=183) |
mRS ≥ 4 at 90 days (n=162) |
|||||||
|---|---|---|---|---|---|---|---|---|
| OR | SE | p | 95% CI | OR | SE | p | 95% CI | |
| Days to evaluation | 1.151 | 0.057 | 0.005 | 1.044-1.268 | 1.107 | 0.056 | 0.044 | 1.003-1.222 |
| ICH score | 2.090 | 0.508 | 0.002 | 1.297-3.366 | 1.868 | 0.433 | 0.007 | 1.185-2.942 |
| NIHSS score | 1.190 | 0.052 | <0.001 | 1.092-1.296 | 1.164 | 0.045 | <0.001 | 1.078-1.256 |
OR, Odds Ratio; SE, Standard Error; CI, Confidence Interval; NIHSS, National Institute of Health Stroke Scale; ICH, intracerebral hemorrhage
Bivariate associations between clinical characteristics upon admission and time to initiation of acute rehabilitation therapy were tested to identify the strongest predictors of time to initiation of acute rehabilitation therapy. Statistically significant (α = 0.05) predictors were then included in a multivariable linear regression model predicting time to initiation of acute rehabilitation therapy, with 95% CIs reported for all adjusted effects. All statistical analyses were performed using STATA/IC 12.1 for Mac (College Station, TX).
Results
Demographic and clinical characteristics of the 203 participants who met study eligibility criteria are presented in Table 1. The mean age of the sample was 63.7 (SD=14.6) years, and most were female (51.2%) and white (52.7%). The majority had comorbid hypertension (71.9%) and was able to ambulate before hemorrhagic stroke onset (mRS <4: 94.6%). Most strokes were mild to moderate (median NIHSS score of 7, median ICH score of 1, and median GCS of 14). Modified Rankin scores (mRS) were available for 186 participants (91.6%) at 30 days and 164 (80.8%) at 90 days. Median time to initiation of acute rehabilitation therapy was 3 [2-7] days.
Table 1.
Demographic and clinical characteristics of study participants (n=203)
| n | Mean or Median | %, (SD), or [IQR]* | |
|---|---|---|---|
| Mean age in years | 203 | 63.7 | (14.6) |
| Female | 104 | - | 51.2% |
| Hispanic | 13 | - | 6.4% |
| Race | |||
| Caucasian/White | 107 | - | 52.7% |
| African-American/Black | 88 | - | 43.4% |
| Other | 8 | - | 3.9% |
| Risk factors | |||
| Ever smoked | 55 | - | 27.1% |
| Current alcohol abuse (> 5 drinks/day) | 14 | - | 6.9% |
| Prior ischemic stroke | 28 | - | 13.8% |
| Prior hemorrhagic stroke | 7 | - | 3.5% |
| Any prior stroke | 33 | - | 16.3% |
| Stroke severity | |||
| Median NIHSS score (missing: n=2) | 201 | 7 | [3–14] |
| Median GCS score | 203 | 14 | [12–15] |
| Median ICH score (missing: n=2) | 201 | 1 | [0–2] |
| Ventilator free through first 14 days (missing: n=10) | 193 | 118 | 58.13% |
| modified Rankin Scale ≥4 (unable to ambulate) | |||
| Pre-morbid | 11 | - | 5.4% |
| 30-day (missing: n=17) | 99 | - | 53.2% |
| 90-day (missing: n=39) | 78 | - | 47.6% |
| Comorbidities | |||
| Hypertension | 146 | - | 71.9% |
| Diabetes | 36 | - | 17.7% |
| Atrial fibrillation | 11 | - | 5.4% |
| Coronary artery disease | 21 | - | 10.3% |
| Complications | |||
| Deep vein thrombosis | 13 | - | 6.4% |
| Pulmonary embolism | 1 | - | 0.5% |
| Pneumonia | 19 | - | 9.4% |
| Length of stay (LOS) | |||
| Median LOS outside ICU in days | 203 | 4 | [2–7] |
| Median LOS inside ICU in days | 203 | 4 | [2–10] |
SD, standard deviation; IQR, interquartile range
Preliminary assessment of the relationship between days to initiation of therapy and disability at 30 days indicated that 80% of those who had rehab 7 days or later had poor outcome (Figure 1). With respect to the effects of time to initiation of acute rehabilitation therapy on post-stroke disability, multivariable effects from logistic regression models predicting disability (mRS ≥ 4) indicated that each additional day between admission and initiation of acute rehabilitation therapy was associated with increased odds of poor outcome at 30 days (adjusted OR=1.151, 95% CI= 1.044-1.268, p=0.005) and 90 days (adjusted OR=1.107, 95% CI= 1.003-1.222, p=0.044; Table 2). As expected, increased stroke severity was also associated with higher odds of poor outcome at 30 and 90 days post-ICH.
Figure 1.
Distribution of 30-day modified Rankin Scale (mRS) < 4 (i.e., good outcome) and mRS ≥4 (i.e, poor outcome) by time to initiation of acute rehabilitation therapy. (n=186)
With respect to identifying predictors of time to initiation of rehabilitation therapy, statistically significant univariable effects on time to initiation of acute rehabilitation therapy were observed for current alcohol use, NIHSS score, ICH score, GCS score, pre-morbid mRS score, ventilator free days (14 vs. fewer than 14 days not intubated), pulmonary embolism, pneumonia, and LOS (i.e., days in- and outside of intensive care units (ICU); Table 3; n=203). Only current alcohol abuse (b=3.581, 95% CI: 1.821-5.342, p<0.001), GCS (b=−0.494, 95% CI: −0.790 - −0.197, p=0.001), premorbid mRS (b= −2.711, 95%CI: −5.139- −0.284, p=0.029), pulmonary embolism (b=3.633, 95%CI: 0.732–6.535, p=0.014) and LOS (days spent in the ICU: b=0.499, 95% CI: 0.376-0.623, p<0.001; days spent outside of ICU: b=0.198, 95% CI: 0.092-0.304, p<0.001) remained independently associated with time to initiation of acute rehabilitation therapy in the multivariable model (Table 3).
Table 3.
Univariable and multivariable effects on time to rehabilitation evaluations
| Univariable (n=203) |
Multivariable (n=190) |
|||||||
|---|---|---|---|---|---|---|---|---|
| b | SE | p | 95% CI | b | SE | p | 95% CI | |
| Age per year | −0.005 | 0.020 | 0.823 | −0.044-0.035 | ||||
| Female | −0.793 | 0.624 | 0.205 | −2.023-0.437 | ||||
| Hispanic | −0.809 | 1.047 | 0.440 | −2.873-1.255 | ||||
| Race | ||||||||
| Black (vs. white) | 0.631 | 0.650 | 0.333 | −0.651-1.913 | ||||
| Other (vs. white) | −1.369 | 1.072 | 0.203 | −3.484-0.746 | ||||
| Risk factors | ||||||||
| Ever-smoked | −0.620 | 0.649 | 0.340 | −1.900-0.659 | ||||
| Current alcohol abuse | 3.280 | 1.465 | 0.026 | 0.392-6.169 | 3.581 | 0.892 | <0.001 | 1.821-5.342 |
| Prior ischemic stroke | −0.310 | 0.925 | 0.738 | −2.134-1.514 | ||||
| Prior hemorrhagic stroke | −0.092 | 1.243 | 0.941 | −2.542-2.359 | ||||
| Any prior stroke | −0.395 | 0.821 | 0.631 | −2.015-1.224 | ||||
| Clinical characteristics at admission | ||||||||
| NIHSS score | 0.189 | 0.049 | <0.001 | 0.092-0.287 | −0.085 | 0.055 | 0.121 | −0.193-0.023 |
| ICH score | 1.061 | 0.346 | 0.002 | 0.379-1.743 | −0.294 | 0.364 | 0.419 | −1.012-0.423 |
| GCS score | −0.573 | 0.119 | <0.001 | −0.808 - −0.339 | −0.494 | 0.150 | 0.001 | −0.790 - −0.197 |
| pre-morbid mRS ≥ 4 | −1.632 | 0.782 | 0.038 | −3.176 - −0.089 | −2.711 | 1.230 | 0.029 | −5.139 - −0.284 |
| Ventilator free through 14 days | −2.821 | 0.697 | <0.001 | −4.196 - −1.446 | 0.467 | 0.586 | 0.426 | −0.689-1.624 |
| Comorbidities | ||||||||
| Hypertension | −0.828 | 0.720 | 0.252 | −2.248-0.592 | ||||
| Diabetes | 1.108 | 0.876 | 0.207 | −0.619-2.835 | ||||
| Atrial fibrillation | −0.382 | 1.300 | 0.769 | −2.946-2.181 | ||||
| Coronary artery disease | −0.099 | 1.041 | 0.924 | −2.151-1.953 | ||||
| Complications | ||||||||
| Deep vein thrombosis | 3.275 | 1.772 | 0.066 | −0.218-6.768 | ||||
| Pulmonary embolism | 2.926 | 0.312 | <0.001 | 2.311-3.541 | 3.633 | 1.470 | 0.014 | 0.732-6.535 |
| Pneumonia | 2.922 | 1.186 | 0.015 | 0.582-5.261 | −1.174 | 1.032 | 0.257 | −3.210-0.863 |
| Length of stay | ||||||||
| Days inside ICU | 0.457 | 0.060 | <0.001 | 0.338-0.577 | 0.499 | 0.063 | <0.001 | 0.376-0.623 |
| Days outside ICU | 0.206 | 0.070 | 0.004 | 0.068-0.344 | 0.198 | 0.054 | <0.001 | 0.092-0.304 |
SE, Standard Error; CI, Confidence Interval; NIHSS, National Institute of Health Stroke Scale; ICH, intracerebral hemorrhage; GCS, Glasgow Coma Scale; ICU, Intensive Care Unit
Discussion
Longer time to initiation of acute rehabilitation therapy was associated with increased odds of disability (mRS ≥4) after ICH, independent of stroke severity. These findings suggest that acute rehabilitation therapy should be initiated promptly to reduce long-term disability after ICH. Our data also showed that patients with longer stays in the ICU also had longer delays to initiation of acute rehabilitation therapy, even when controlling for stroke severity. For rehabilitation consultations and initiation of services, considerations of patient location in addition to patient’s functional needs and readiness may further improve patient outcomes. However, detailed clinical guidelines to determine patient readiness for participation in rehabilitation therapy are scarce.24
Our results also suggest that earlier acute rehabilitation therapy (although not necessarily within 24 hours) could potentially reduce long-term disability after ICH. Our data do not provide evidence for an optimal time point for initiation of acute rehabilitation therapy. However, it appears from our data that initiating acute rehabilitation after 6 days is more likely to lead to poor outcome at 30 and 90 days. In detail, we found that each day between admission and rehabilitation evaluation resulted in increased odds of poor outcome at 30 and 90 days. This finding highlights the need to identify optimal time frames for initiation of acute rehabilitation therapy that are specific to each stroke subtype. Also, in our sample, time to initiation of acute rehabilitation therapy was longer for patients with current alcohol use, pulmonary embolism, lower GCS scores (i.e., lower level of consciousness), pre-morbid mRS lower than 4 (i.e., those able to ambulate pre-morbid), as well as those with longer lengths of stay. Our results highlight a practice pattern that prioritizes initiation of acute rehabilitation for patients that are deemed ready for participation in rehabilitation services (i.e., higher level of consciousness measured with GCS) and who were unable to ambulate prior to their stroke (i.e., mRS ≥4). In acute rehabilitation therapy, these patients are often given priority in an attempt to help them recover a level of physical function equal or similar to their pre-morbid status to reduce long-term disability. Also, these patients are at increased risk of further functional decline due to prolonged bedrest attributable to their pre-morbid status (i.e., unable to walk).25,26Therefore, these patients require skilled rehabilitation services that can, in a safe environment, identify their current functional needs, assist in the recovery of function, reduce bedrest, while also recognizing and accommodating their prior level of function.27 This practice seems to be in accordance with recent initiatives that target the appropriate use of rehabilitation services, by avoiding overuse of services for patients with lower levels of impairment and underuse of rehabilitation services for those with high levels impairment and needs.28
Interestingly, neither ICH nor NIHSS scores reached significance as factors associated with time to rehabilitation initiation, but both were associated with poor outcome (mRS ≥4) at 30- and 90-days after stroke. This suggests that rehabilitation specialists may find level of consciousness (i.e., GCS score) as a more useful indicator of when to initiate rehabilitation services than ICH or NIHSS scores. While ICH score was not a significant predictor of time to initiation of rehabilitation services, it is conceivable that it was not predictive because ICH score includes other indicators such as age, and stroke volume and location that are not as informative in terms of patient readiness for participation in rehabilitation. In terms of NIHSS score, it is a measure of stroke severity that is reassessed often during the patients’ length of stay.29 Since no one in our sample was evaluated for rehabilitation services within 24 hours of admission, it is plausible that NIHSS score upon admission (the only available value in our study) did not accurately reflect the patients’ status at the time of initiation of rehabilitation and that it was not used as an indicator to determine time to initiation of rehabilitation services. Nevertheless, it remains unclear which of these or other clinical benchmarks would serve a better indicators of patient readiness for initiation of rehabilitation services.
Initiation of rehabilitation early after stroke also remains controversial, especially within intensive care units.7–9 Previous studies of patients with medically acute conditions have shown that rehabilitation within ICUs is feasible, safe, cost-effective, and results in better patient outcomes.30–33 The AVERT trial, the only large international randomized controlled trial that assessed early initiation of rehabilitation therapy, defined early rehabilitation as initiation within 24 hours after stroke.15 Their findings suggest that receipt of rehabilitation at an early stage was detrimental (i.e., increased odds of disability and mortality).15,34 However, it is also important to note that the difference in time to initiation of rehabilitation between the early initiation group (i.e., experimental) and the usual care group (i.e., control) was approximately 4 hours, and those receiving usual care had a median time to first rehabilitation mobilization of 22.4 hours. This finding highlights the need for clarity in the conceptual definition of “early rehabilitation” when attempting to identify optimal time frames for initiation of acute rehabilitation therapy. In our study, no patient received rehabilitation within 24 hours of admission, and the median time to initiation of acute rehabilitation therapy was 2 days. Also noteworthy, the AVERT trial showed that early mobilization was particularly harmful for patients with ICH, although not significant by interaction testing. Since the AVERT trial was not powered to detect different between stroke subtypes those results should be interpreted with caution.
As seen in these results, longer time to initiation of acute rehabilitation therapy was associated with increased odds of disability, regardless of stroke severity, which suggests that patients after ICH would benefit from initiatives aimed at reducing wait times to initiation of acute rehabilitation therapy, regardless of severity. This could be accomplished by modifying the amount or the intensity of resources used according to level of severity. While the Joint Commission only requires that patients admitted to primary and comprehensive stroke centers be assessed for rehabilitation,35 our findings suggest that time to initiation of acute rehabilitation therapy may also represent an important factor for post-stroke recovery.
This study has important limitations. Our study did not account for rehabilitation services provided outside of acute hospitalization; yet, we think that our results are in line with recent findings. Studies showed that functional status at discharge from acute hospitalization36,37 or at admission at inpatient rehabilitation38 predicts hospital readmission and long-term quality of life, respectively. This suggests that improving functional status during acute hospitalization is critical and the prompt initiation of acute rehabilitation services is the first step to do so. This study was carried out at a single acute care center in a large metropolitan area. While pre-morbid mRS scores were collected, examination of change in mRS scores as the primary outcome was not appropriate since mRS score is not an adequate measure of patient functional status during acute hospitalization. Also, some degree of attrition on mRS was observed between pre-morbid and follow-up at 30 and 90 days. However, if participants were lost to follow-up due to death or disability, stronger effects would be expected if follow-up scores were to be available. Others have also noted substantial limitations to using the mRS as a measure of patient disability, as this measure mainly focuses on mobility and function, but does not consider cognitive or executive function impairments.39 In future studies, implementation of additional objective measures, such as gait speed and arm motor testing that yield performance-level information should also be incorporated to better characterize functional recovery and the effect of rehabilitation therapy after ICH.
Summary/Conclusion
These findings suggest that earlier acute rehabilitation therapy (between 2-6 days) could reduce disability after ICH; hence, minimizing delays to initiating rehabilitation therapy may improve long-term patient outcomes. Moreover, we identified GCS and pre-morbid functional status as the strongest predictors of early initiation of rehabilitation services. Future studies should further explore optimal predictors of long-term disability risk to allow better prioritization of rehabilitation services.
Acknowledgements
NUCATS
Sources of Funding
Study funded in part by the National Institutes of Health’s National Center for Advancing Translational Sciences, Grant Number UL1TR000150 and UL1TR001422.
Conflict of Interest/Disclosure
CCL is currently funded by AHRQ fellowship # 3F32HS024366-01S1 and NIDILRR grant # 90SF0010. RAL, KM, and MM report no disclosures. EL receives support from the National Institutes of Health National Center for Advancing Translational Sciences grant KL2TR001424 and the National Institute of Health grant L30 NS098427. SP receives support from the National Institutes of Health and Patient Centered Outcomes Research Institute. AN receives support from the Agency for Healthcare Research and Quality (PI: Andrew Naidech; HS023437), as well as by the National Institutes of Health’s National Center for Advancing Translational Sciences, Grant Number UL1TR000150.
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