One in four people >25 yr old will suffer from a stroke in his or her lifetime, with >13 million new cases occurring worldwide annually.1 About a third of those will die from the stroke, and a third will be left with permanent disability.2 Along with physical disability, ∼35% of these patients have diabetes,3 up to 75% will have comorbid cardiac disease,4∼30% have stroke-related communication issues,5 up to 64% have at least mild cognitive impairment,6,7 up to 66% of people experience pain within the first 24 mo following stroke,8 fatigue occurs in up to 92%,9 and depressive symptoms in a third.10 In a cross section of 116 consecutively enrolled patients in an outpatient stroke rehabilitation (SR) program, patients had a mean of four and maximum of thirteen comorbidities.11
Given the complexity of these patients, it is not surprising that most people become sedentary following the event, which likely accounts, in part, for ∼25% of annual cases of stroke being repeat strokes.12 Acknowledging this complexity, physiotherapists report they are more likely to refer patients post-stroke to exercise programs with knowledgeable instructors.13 They also express concerns about risks to patients when referring them to community-based exercise because of limited monitoring during exerise.13 Patients have similar concerns as demonstrated by focus group data revealing that a prominent facilitator to exercise for community-dwelling patients was the presence of qualified personnel to ensure safety and guidance for stroke-specific needs.14 These concerns help explain the results of a recent systematic review that concluded that general lifestyle interventions on their own were insufficient in improving physical activity levels after stroke or transient ischemic attack (TIA).15
Cardiac rehabilitation (CR) is a setting where cardiac patients, and increasingly patients with stroke and peripheral arterial disease, receive comprehensive secondary prevention programming, including structured exercise.16,17 CR programs can help overcome the barriers expressed by patients and referring physiotherapists. CR offers a safe and medically supervised environment to refer patients following stroke. They include pre-participation graded exercise testing and blood pressure and glucose monitoring and offer education sessions on risk factor modification, nutrition, medication, psychosocial counseling, and falls risk assessment and education.18
There is growing support in the clinical and academic community for including patients post-stroke in CR. However, as described herein, there are barriers to patient participation and only very few patients attend CR. With CR offered in 111 of 123 countries,19 and growing research demonstrating the benefits to physical function, cognition, cardiorespiratory fitness (CRF), and cardiovascular risk factors, it is imperative that these barriers are overcome so that the burden of stroke can be reduced. There is an urgent need to create cross-program collaborations between hospitals, outpatient SR, CR, and community programs to facilitate participation and access to programming. Therefore, the purpose of this review is to investigate the barriers and facilitators to improving linkage between health services with a focus on increasing access to CR.
PROJECTED INCREASE IN STROKE PREVALENCE
The prevalence of coexisting chronic health conditions is increasing globally as the population ages.20 A recent meta-analysis and observational study reported that the prevalence of multimorbidity (two or more chronic diseases in the same individual) in global communities was 33%, with a higher prevalence in individuals >65 yr old.20 The aging population and accumulating risk factors lead some countries to project marked increases in stroke prevalence. In the next two decades, the number of Canadians living with disability post-stroke is projected to increase by 80%.21 In the United States, the projection is that stroke prevalence will increase by 3.4 million individuals from 2012 to 2030 and total direct annual stroke-related medical costs will increase from US $71.6 billion in 2012 to US $183.1 billion by 2030.22 Globally, the mean lifetime risk of stroke has increased from 23% in 1990 to 25% in 2016.23 Although much remains unknown, there is emerging evidence that there is a higher risk of thrombotic complications with COVID-19, including ischemic stroke.24,25 While there are not enough data yet to make any projections, this may affect prevalence worldwide in the future.
CARDIAC COMPLICATIONS IN THE FIRST YEAR AFTER STROKE
The financial burden of stroke to health systems globally is staggering. The greatest health care costs are incurred in the first year, with much of the additional expenditure accounted for by repeat stroke and cardiac events.26 Indeed, cardiac-related complications are the second leading cause of mortality within 1 mo after the stroke event.27,28 One large study reported that 19% of patients experienced one or more serious cardiac adverse events within 3 mo of the stroke.29 In the chronic stage of stroke, physical activity levels fall well below recommended levels and CRF is just over half of age- and sex-predicted normative values for sedentary adults, falling below the necessary criterion for independent living.30 Thus, it is not surprising that 2-5 yr after a stroke the risk of mortality from a cardiac episode becomes almost twice as high as that of a neurological event.31
BENEFITS OF EXERCISE AND RISK FACTOR MODIFICATION
Therefore, aerobic and resistance training and risk factor modification programming should be started within the critical time frame of 1 yr post-event. Exercise and risk factor modification programming are associated with improved cardiovascular disease risk factors, reduced 3-yr risk for recurrent stroke, myocardial infarction, vascular death, and lower all-cause mortality.32–35 It has also been demonstrated that group-based exercise training when delivered by qualified exercise personnel is a cost-effective strategy for stroke survivors, with an acceptable incremental cost per quality-adjusted life year.36
CR programs are well positioned to provide post-stroke programming, given that they incorporate medically supervised aerobic and resistance training and risk factor modification services. A recent study measured the effect of integrating CR concurrently with outpatient SR on mortality outcome.37 Upon discharge from inpatient rehabilitation, 136 patients were recruited to participate in a 12-wk CR and outpatient SR intervention. Most of the participants (81%) completed the CR and demonstrated a lower 1 yr post-stroke mortality of 1.5% than the US national rate of 31%. In subgroup analysis, a comparison of matched CR participants (n = 76) with those who chose not to participate after inpatient discharge (n = 66) demonstrated a 13% difference in mortality: 1.3% in CR participants versus 15.2% in nonparticipants. While these and other data are promising, a recent systematic review concluded that more data are required to determine whether exercise interventions reduce mortality following stroke.38
CR and other exercise training studies have also demonstrated improvements in cognitive impairment, depressive symptoms, walking deficits, CRF, and cardiovascular risk factors following stroke.7,38–46 Regarding CRF and muscle fitness, Marzolini et al47 demonstrated in a randomized study of 73 patients post-stroke with mobility deficits that a 6-mo CR of combined aerobic and resistance training yielded almost five times more lean mass than aerobic training alone (1.23 ± 2.3 vs 0.27 ± 1.6 kg, P = .039) measured by dual-energy x-ray absorptiometry. In addition, there was a significantly greater improvement in combined versus aerobic training alone in ventilatory anaerobic threshold measured by cardiopulmonary exercise test (19.1 ± 26.8% vs 10.5 ± 28.9%, respectively, P =.046) and upper- and lower-limb muscular strength (P < .03, all limbs except affected side leg). An earlier study from the same group using similar methodology demonstrated markedly similar body composition improvements in 72 patients with coronary artery disease and no previous stroke randomized to combined versus aerobic training alone (Figure 1).48 Completion rate of the 6-mo CR for stroke was superior to the cohort with coronary artery disease (93% and 62%, respectively). The demonstrated inverse association between both lean mass and strength, with all-cause mortality in healthy and chronic disease populations,49–52 highlights the importance of this modality of training. Therefore, aerobic in combination with resistance training has been recommended in the American Heart and American Stroke Association Guidelines for Adult SR and Recovery as a class IIA, level A recommendation.53
;)
Figure 1.: Comparison of change in lean mass by modality of exercise between people post-stroke and following a cardiac event.
a P < .05. This figure is available in color online (
www.jcrpjournal.com).
CARDIAC REHABILITATION IS TEMPORALLY WELL POSITIONED TO PROVIDE EXERCISE AND RISK FACTOR MODIFICATION FOLLOWING STROKE
The transitions in care after a stroke are fairly rapid, with only a median of ∼4 d in acute care/inpatient rehabilitation and then up to 9-12 wk in outpatient SR11,53 (Figure 2). Although these transitions and services vary globally, there is generally little time for a focused exercise intervention as described previously.54,55 In programs that accept them, patients are typically referred to CR ∼10 wk following the stroke event or after completing all of the outpatient SR available to them. This coincides with the timing of when neurobiological protective mechanisms have recovered sufficiently to allow for higher-intensity exercise training at or above the anaerobic threshold.56 Without CR referral, there is little opportunity to foster independent exercise, optimize the exercise prescription, and receive risk factor modification interventions in a medically supervised environment.
Figure 2.: Conceptual model of the continuum of care: Recovery post-stroke. This figure is available in color online (
www.jcrpjournal.com).
Recently, Marzolini et al56 outlined a safety and efficacy framework for introducing higher-intensity exercise into the exercise regimen of people post-stroke. While it is recognized that animal studies show favorable effects of early aerobic exercise interventions that take advantage of the optimal time window for neural repair,57 this is likely not the case for humans. Indeed, based in part on the results of the A Very Early Rehabilitation Trial (AVERT), most contemporary stroke care guidelines and position papers advocate against “high-dose” or “intensive” out-of-bed activities within 24 hr of stroke onset.58–61 The AVERT study demonstrated a neutral or potentially negative effect of mobilization strategies (walking, sitting, standing), initiated within the first 24 hr.62
Activity prescription parameters in the first 10 wk of stroke are contingent on recovery of cerebral autoregulation, resting blood pressure, blood-brain barrier function, ischemic penumbra, cardiac complications, hemorrhagic stroke parameters (risk of hematoma expansion), and other physiological issues.56 As an example, cerebral autoregulation is a mechanism that maintains constant cerebral blood flow despite fluctuations in systemic arterial blood pressure over a wide range of pressures.63 When cerebral autoregulation is impaired, a rise in mean arterial pressure during exercise is passed onto the vulnerable cerebral circulation and may result in blood-brain barrier breakdown.56,64–66 Therefore, exercise that is prescribed at a high intensity may result in cerebral hyperperfusion and damage the neurovascular unit and consequently threaten survival of neurons and glial cells.64,67 While this sequela is largely untested in humans, it is prudent to consider the clinical implications.
Fortunately, cerebral autoregulation recovery occurs in the first 10-12 wk post-stroke.56 This suggests that over the first 10 wk, exercise prescriptions in SR settings should feature a gradual progression in duration and intensity from light to just less than moderate intensity (below the anaerobic threshold). Subsequently, upon initiation of CR at ∼10 wk, the first 2-4 wk should include a gradual progression from just less than moderate- up to moderate-intensity exercise without exceeding the anaerobic threshold. Three months following stroke (2- to 4-wk post-CR initiation), when cerebral autoregulation is intact, progression to high intensity continuous or high-intensity interval training can be prescribed, preferably based on the results of a graded exercise stress test with electrocardiographic monitoring.68
The rationale for maintaining exercise below the anaerobic threshold in the earlier stages is that during incremental aerobic exercise in healthy individuals, cerebral blood flow velocity gradually increases until ∼60-70% of maximal oxygen uptake or just below the ventilatory anaerobic threshold.69,70 As the intensity continues to increase, cerebral blood flow either plateaus or progressively declines toward resting values. In the earlier stages of stroke, when cerebral autoregulation is impaired, cerebral blood flow velocity may continue to increase past the anaerobic threshold and result in hyperperfusion injury. Although research is required to examine this in the stroke population, it is prudent to delay higher-intensity exercise until expected recovery, which coincides with CR initiation. In the earlier stages (before CR participation; <10 wk), a graded exercise test that is terminated at the anaerobic threshold can be used to inform the prescription; otherwise, a strategy for guiding exercise intensity below the anaerobic threshold is to use the Talk Test.71
GROWTH IN SUPPORT FROM THE SCIENTIFIC AND CLINICAL COMMUNITY FOR INCLUDING STROKE IN CARDIAC REHABILITATION
There is great potential to create impact on the lives of people post-stroke by increasing access to CR, and there is growing support for this from health organizations as well as in the scientific community. The American Heart and American Stroke Association guidelines proposed that there is need for supervised exercise by a physical therapist or CR professional at the onset of programming for individuals with disability after ischemic stroke.72 In Ontario, Canada, the Ontario Stroke Network merged with the Cardiac Care Network of Ontario to form CorHealth Ontario. One of their strategic priorities is to develop harmonized secondary prevention services for patients with heart disease, stroke, TIA, and peripheral vascular disease.
An examination of temporal patterns of published studies from MEDLINE from 1946 to March 9, 2020, that included the key words “stroke” (accident: cerebrovascular or brain vascular) and “CR” (cardiac or cardio or heart) offers valuable insights into the change in the research landscape (Figure 3). The first study that included these key words was published in 1964, titled “Rehabilitation of Patients With Cardiovascular Disease Other Than Stroke.”73 From that inauspicious start, there were only three studies published over the next 43 yr (to 2007) and subsequently an increase to 30 studies that have been published over the last 13 yr (2007 to March 2020). These studies describe the benefits, feasibility, barriers, and facilitators to including people with stroke in CR.
Figure 3.: Temporal pattern of published studies related to including stroke in cardiac rehabilitation. This figure is available in color online (
www.jcrpjournal.com).
BARRIERS AND FACILITATORS TO EXERCISE PROGRAMMING: THE ROLE OF CARDIAC REHABILITATION
While there is great potential for CR to provide stroke programming, provision of CR services for patients with stroke varies widely by country and region and much is not known about global access. It is primarily from national surveys that we ascertain barriers and facilitators to including stroke in CR that may help other countries plan for inclusion. While the data are based on high-income country experience, some of the information may pertain to lower-income countries.
In the United States, stroke is not a covered diagnosis for CR services and people post-myocardial infarction and coronary artery bypass graft ≥65 yr are significantly less likely to receive CR if they have had a previous stroke.74 In Australia, a national survey conducted in 2018 revealed that patients with a diagnosis of stroke are unlikely to participate in CR programs. Specifically, of 149 CR programs surveyed, only 6% had received a referral for people with primary stroke or TIA in the previous calendar year, with stroke/TIA representing <2% of the patient population in >90% of CR.75 The most frequently cited barriers to attending as indicated by program managers were safety (79%), limited staff to patient ratio (76%), integration difficulties (68%), and lack of referrals (66%).
In the largest survey of CR in Canada, we found that 65% of 114 CR programs managers reported accepting referrals for patients with a diagnosis of stroke.18 Most of the CR programs integrated patients into regular cardiac classes, but 10% provided stroke-specific classes. Yet, 63% of programs that included stroke reported that only <11 patients had participated in the previous calendar year despite 88% reporting no limit to the number they could enroll. The four most frequently cited barriers to including patients with stroke in CR were lack of funding (63%), additional staff required (61%), lack of equipment for assessing aerobic capacity (61%), and people post-stroke are not referred (60%). The most frequently cited facilitators by Canadian program managers were additional funding (91%), additional staff (89%), collaboration with health care professionals from SR units to ensure appropriate referrals (81%), a tool kit with instructions to prescribe resistance training (80%) and aerobic training (80%) to people post-stroke.
RESOURCES
Lack of resources (funding, staff, space, equipment, etc) is consistently rated as a primary barrier to including stroke in CR and likely the most challenging to overcome. Data from the UK's National Audit of 229 CR databases indicated the need for increased CR staffing to support patients with comorbid stroke and cardiac disease.76 An analysis of 6342 patients from the electronic database revealed that higher-quality programs (multidisciplinary teams) and those with greater staff hours were more likely to include patients with comorbid stroke. Specifically, for every hour increase of CR staff time, there was a 1.9% increased likelihood of attendance by patients with comorbid stroke and cardiac disease. Indeed, limited staff to patient ratio was cited by CR managers in Australia as the second most frequently reported barrier to including people following stroke. However, the authors of the study point out that 70% of CR programs in Australia have a staff to patient ratio of ≤1:5 and people with mild stroke or TIA could safely participate. Adjustments to program models may be a strategy to mitigating resource barriers for inclusion of people with stroke. Our previously mentioned survey of CR in Canada demonstrated that programs with a hybrid model (ie, a combination of home-based exercise independent of rehabilitation staff and regular supervised center-based exercise) were significantly more likely to accept patients with stroke than CR with other models of care such as supervised on-site-only.18 Similar to CR in Australia, 79% of programs had a staff to patient ratio of 1:2-5, also indicating that patients with mild disability could be integrated into the regular program model. These data suggest that development of program eligibility criteria for inclusion of patients that are compatible with the resources available in the CR may address staffing concerns as discussed in the next section. However, this may create a treatment risk paradox where those who most require CR such as those with more severe stroke deficits do not get referred. Therefore, global strategies to advocate for increased funding to CR could significantly help integrate patients of all mobility levels following stroke.
REFERRALS
Lack of referrals was the fourth most cited barrier to including patients in both Australian and Canadian CR programs and represents a modifiable barrier. This barrier could, in part, be related to the restrictive and extensive eligibility criteria established by CR that could complicate or stall the referral process. For example, there were ≥20 different patient eligibility criteria reported by Canadian CR managers in survey results.18 Specifically, there were three to four different levels of mobility, cognitive, and communication deficits, requirement for caregiver/partner assistance, minimum number of days post-stroke, transportation requirement, falls risk level, and 25% of CR programs only accepted patients with a concurrent cardiac diagnosis. These criteria must be compatible with the experience and resources available in the CR programs and so are necessary from a safety and efficacy point of view. However, for referral sources such as physical therapists working in outpatient SR, the multiple and variable eligibility criteria between CR programs possibly from the same region pose a barrier to referral and may result in inappropriate referrals. Indeed, the third most frequently cited facilitator (81% of Canadian CR managers) was collaboration with health care professionals from SR units to ensure appropriate referrals. As described later, this has been demonstrated to be an effective strategy for increasing appropriate referrals.11
The Table provides a guide to determining referral eligibility criteria based primarily on mobility level. The Table reflects that mobility level eligibility (none, mild, moderate, moderately severe, severe) will vary on the basis of the exercise modalities available (overground walking, stationary equipment, functional electrical stimulation cycles), staff experience, type of pre-assessment and screening, length of program/number of exercise sessions offered, and number of available staff (staff to patient ratio). For example, people with severe mobility deficits post-stroke who rely on a wheelchair for day-to-day activities, with a high risk of falling, will require a higher staff to patient ratio than higher-functioning patients. They will also require access to stationary exercise equipment with adaptive pedals and other attachments. The more medically complex patients would require more extensive pre-assessment and screening procedures.
Table -
Considerations When Determining Criteria to Ensure Appropriate Referrals to Cardiac Rehabilitation After a Stroke (With or Without a Cardiac Diagnosis) Based on Stroke-Related Mobility Deficits (if Any)
| Stroke-Related Mobility Deficit, if Any |
Staff to Patient Ratioa (# New Patients) |
Class Size |
Equipment/Program |
Caregiver Support |
|
No mobility deficits: No difficulty with walking, or climbing stairs and no use of gait aids for stroke-related gait impairment. |
1 staff:10-15 patients (1 new patient every 1-2 wk/class) |
20-25 |
No exercise modality restrictions: Can be integrated with other CR patients |
None required |
|
Mild mobility deficits: A little difficulty with walking or climbing stairs, can walk ≥200 m (655 ft) (no time restriction and rest breaks are allowed) with or without a gait aid and does not interfere with lifestyle. A wheelchair is not required for day-to-day activities. |
1 staff:10 patients (1 new patient every 1-2 wk/class) |
20-25 |
No exercise modality restrictions: Can be integrated with other CR or neurological patients |
None required |
|
Moderate mobility deficits: Some difficulty with walking and climbing stairs but can walk ≥100 m (330 ft) (no time restriction and rest breaks are allowed) with a gait aid that leads to some restrictions in lifestyle. A wheelchair is not required for day-to-day activities. |
1 staff:7 patients + volunteers suggested (1 new patient every 1-2 wk/class) |
20 |
No restrictions. Stationary cycle ± adapted pedal may be used in combination with walking when needed. Treadmill if appropriate**c
Separate stroke or neurological diseases class preferred. |
None required but preferred for home exerciseb |
|
Moderately severe mobility deficits: Significant difficulty with walking and climbing stairs but can walk ≥10 m (32 ft) (no time restriction and rest breaks are allowed) with a gait aid that leads to significant restrictions in lifestyle. A wheelchair may be required for day-to-day activities. |
1 staff:3-5 patients + volunteers suggested (1 new patient every 2-3 wk/class) |
20 |
Track, treadmill with harnessc gait belt, stationary cycle with-below knee adapted pedal. Separate stroke or neurological diseases class suggested. |
Suggested for home exerciseb |
|
Severe mobility deficits: Inability to perform walking at all even with aids or without physical assistance from at least one other person and requiring a wheelchair and needing assistance with transfers (eg, wheelchair to toilet). |
1 staff:1 patient or 1 staff: 2 patients + volunteer suggested (1 new patient every 3 wk/class) |
5-10 |
FES bike, semi-recumbent cycle with below-knee adapted pedal (must be able to transfer onto stationary exercise equipment with/without assistance). Arm ergometer (if able to grasp the handle of an arm ergometer with at least one hand). |
Preferred during supervised trainingb |
Abbreviation: CR, cardiac rehabilitation; FES, functional electrical stimulation.
aIn a class of ≥20 patients, a case manager is required and the staff to patient ratio does not include the case manager. Intakes are rolling (eg. 1 new patient every 1-2 wk for a 6-mo program).
bCaregiver: When a caregiver is required or preferred, he or she should attend at least the first exercise session, when the aerobic exercise prescription and walking route is established and instruction on pulse taking, filling in exercise logs, etc, is taught. This person should also attend a resistance training session to observe and receive special instructions on lifting technique, safety procedures, setting up equipment, etc.
The aforementioned suggestions are based on clinical experience at Toronto Rehabilitation, Cardiovascular Prevention and Secondary Prevention Program.
cIf only treadmills are available patients must be able to walk at the slowest speed setting of the treadmill (typically 0.5-0.8 mi/hr).
OVERCOMING BARRIERS IDENTIFIED BY CARDIAC REHABILITATION PROGRAM MANAGERS TO INCLUDING PEOPLE WITH STROKE
The following are some of the modifiable barriers as well as facilitators to including people with stroke in CR identified by program managers in Canada and Australia.18,75 Some of the facilitators are based on clinical experience at Toronto Rehabilitation–University Health Network's Cardiovascular Prevention and Rehabilitation Program.
- Safety concerns
- Develop eligibility criteria for stroke admissions that are compatible with the number of staff available (Table).
- For patients at a high risk of falling, stationary cycling with low-cost adaptive pedals is a safe and effective modality of exercise. Resistance training can be performed in a seated position.
- Include volunteers to assist CR exercise therapists.
- Limited staff to patient ratio/additional staff required
- Develop eligibility criteria for stroke admissions that are compatible with the number of staff available (Table).
- Encourage caregivers and communication partners to attend sessions.
- Include volunteers to assist CR exercise therapists.
- Lack of referrals
- Create partnerships with outpatient SR programs close to the CR.
- Provide a referral form specific for people with stroke that includes program eligibility criteria and disseminate them.
- The referral form should include the option for the referral source to indicate a recommendation of exercise stress testing modality (if available) (ie, upright or semi-recumbent stationary cycle or treadmill). Results of assessments conducted prior to CR entry such as a 6-min walk test should be reported on the form as this assists with creating the exercise prescription and determining eligibility.
- Contact information for the CR intake lead should be provided to the referring practitioner should they have questions regarding eligibility of a patient.
- Provide in-services for potential referral sources on what is provided in a CR program, benefits, eligibility criteria, and exercise assessment options for people with stroke.
- Create a brochure for patients and families for dissemination by referral source that includes eligibility criteria, how to get referred, where the CR program is located, and a description and summary of benefits of a CR program following stroke.
- Lack of guidance for CR staff on exercise prescription, assessments, and use of adaptive equipment
- Provide a tool kit on how to prescribe aerobic and resistance training for patients following stroke with physical deficits.
Providing a resistance training and aerobic training tool kit was a high priority for 80% of all Canadian CR managers, reported as the fourth and fifth most influential facilitator to including stroke in CR.18 As a result, we created a tool kit named “Stroke Online” that was launched on June 5, 2020 (https://www.healtheuniversity.ca/EN/CardiacCollege/Stroke). Stroke Online was designed to be used by patients in combination with guidance from a health care professional. It includes aerobic training, resistance training, and risk factor modification education sections. It guides patients and health care professionals on how to choose an effective and safe exercise program based on patient functional level and other health conditions using pre-participation health screening criteria. It guides the individual on type of exercise equipment, blood pressure monitors, adaptive cycling pedals, and other devices and equipment that may be needed and where to purchase them. Stroke Online is embedded in Toronto Rehab–University Health Network's Cardiac College platform and thus patients also have access to information and guidance on behavior change, diabetes management, and many other topics.
IS A PARTNERSHIP BETWEEN A CARDIAC REHABILITATION AND OUTPATIENT STROKE REHABILITATION PROGRAM EFFECTIVE FOR INCREASING REFERRALS?
In our previously described pan-Canadian survey of CR managers, a highly rated facilitator to help overcome the barriers of lack of referral and lack of appropriate referral to CR was to create collaboration and partnerships with referrals sources. To examine whether an outpatient SR-CR partnership provides an effective continuum of care, Marzolini et al11 tracked 116 consecutively enrolled patients from a single outpatient SR program. Barriers to eligibility, enrollment, and completion of the CR were examined. All of the suggestions to overcome lack of referrals and integration difficulties mentioned in the “Overcoming Barriers” section earlier were instituted over 15 yr that patients post-stroke were being including in the CR. In this model, the stroke therapists had the option of referring patients to either the traditional CR or stroke-adapted CR. To be eligible for either stream, (i) patients had to have the ability to walk ≥100 m independently with/without an assistive device (no time restriction and rest breaks allowed) with no severe limitations due to pain, (ii) were ≥10 wk post-stroke, (iii) not reliant on a wheelchair, and (iv) able to exercise at home independently or with assistance. Patients with a hemiparetic gait pattern attended the CR adapted for patients with stroke known as TRI-REPS, while higher-functioning patients (no gait impairment) were integrated into the regular CR stream.
This study demonstrated that 72% of all patients from outpatient SR were eligible to participate in CR. Of all eligible patients, 71% (n = 60) participated and >80% completed CR. The participation and completion rate was markedly superior to that reported historically in the cardiac populations from the United States and Canada where 40% of eligible patients participate and 60-70% complete CR.77–79 Indeed, participation reached the recommended target of 70-80% set by CR associations and national initiatives.80 Regarding the CR streams, the majority were referred to stroke-adapted CR (67%), with 33% to the traditional CR stream. Stroke-adapted CR versus traditional CR resulted in superior attendance (87 ± 17% vs 66 ± 23% of pre-scheduled sessions, P = .001) and completion (90% vs 67%, P =.04). These results demonstrate that the outpatient SR-CR partnership provides an effective continuum of care using the suggestions to overcome barriers to referral provided in this article.
Unfortunately, Marzolini et al11 also revealed that of 116 SR outpatients, women were twice as likely as men to decline to participate in CR (46% vs 24%, respectively, P = .02). The sex difference was not related to eligibility to participate, age, mobility, or motor recovery level. Indeed, this may, in part, explain why women after stroke are underrepresented in exercise studies, with only 2481-34%54,82,83 of participants being women. Yet, once men and women started CR, there was a high completion rate (80 and 82%, respectively) with no sex difference.11 Sex disparities in referral, enrollment, and completion of CR have been recognized for decades in the cardiac literature,84–86 but this was the first study to report a sex difference post-stroke. A recent study has since reported similar findings from the United Kingdom where only 39% of women following stroke were referred to CR versus 47% of men.76
FUTURE RESEARCH
Future research should include a focused examination of sex differences in participation in exercise programming throughout the continuum of care. This would help develop facilitators that would reduce the previously identified disparities in access between men and women following stroke. In addition, socioeconomic status and language barriers have previously been identified as barriers to attending pre-scheduled CR classes for people post-stroke.87 These are also likely to pose barriers to referral to CR and should be examined. Furthermore, the effect of different models of CR care,88 such as virtual delivery or home-based versus on-site center-based programs, should be explored. Gaining experience with using remotely delivered CR may open spaces for people who are in greater need of supervised on-site care beyond the pandemic such as those with mobility deficits. Finally, there is a dearth of randomized controlled studies examining the effects of CR on mortality, physical function, brain health, and quality of life for people following stroke and should be a research priority.
SUMMARY
Removing barriers and expanding access to CR following stroke will expose more people to benefits such as improved CRF, muscle mass, strength, mobility, and cognition. With the greatest health care cost being incurred in the first year post-stroke, referral to a CR program will target this critical time frame. Indeed, referral to a CR program after patients have completed all of the SR available to them (∼10 wk post-event) coincides with neurobiological recovery, allowing for the safe prescription of higher-intensity exercise. Unfortunately, SR care pathways are highly variable, with some disparities in access to care. With multiple access points to CR and numerous CR referral criteria, few patients are referred and attend. Forging outpatient SR partnerships with CR has been demonstrated to provide an effective continuum of care, with approximately three-fourths of eligible patients participating and >80% completing. Communication between the referral source and CR regarding eligibility criteria that are compatible with experience and resources available in CR is essential, as is making inclusion of people post-stroke an institutional strategic priority. Global strategies to subsidize CR for staffing and equipment would impact the integration of patients with stroke with mobility deficits and have a significant effect on health outcomes and health services utilization. This would be a step toward mitigating the projection of future increased stroke-related medical costs and reduce the burden on patients and their caregivers.
ACKNOWLEDGMENTS
The author gratefully acknowledges Maureen Pakosh and Christopher Cooper for help with the manuscript.
REFERENCES
1. Feigin VL, Nichols E, Alam T, et al. Global, regional, and national burden of neurological disorders, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol. 2019;18:459–480.
2. World Health Organization. Global Health Estimates: Deaths by Cause, Age, Sex and Country, 2000-2012. Geneva, Switzerland: World Health Organization; 2014.
3. Scott JF, Robinson GM, French JM, O'Connell JE, Alberti KG, Gray CS. Prevalence of admission hyperglycaemia across clinical subtypes of acute stroke. Lancet. 1999;353:376–377.
4. Amarenco P, Lavallee PC, Labreuche J, et al. Prevalence of coronary atherosclerosis in patients with cerebral infarction. Stroke. 2011;42:22–29.
5. Engelter ST, Gostynski M, Papa S, et al. Epidemiology of aphasia attributable to first ischemic stroke: incidence, severity, fluency, etiology, and thrombolysis. Stroke. 2006;37:1379–1384.
6. Ya-Ping J, Di Legge S, Ostbye T, Feightner JW, Hachinski V. The reciprocal risks of stroke and cognitive impairment in an elderly population. Alzheimers Dement. 2006;2:171–178.
7. Marzolini S, Oh PI, McIlroy W, Brooks D. The effects of an aerobic and resistance exercise training program on cognition following stroke. Neurorehabil Neural Repair. 2013;27:392–402.
8. Hansen AP, Marcussen NS, Klit H, Andersen G, Finnerup NB, Jensen TS. Pain following stroke: a prospective study. Eur J Pain. 2012;16:1128–1136.
9. Duncan F, Wu S, Mead GE. Frequency and natural history of fatigue after stroke: a systematic review of longitudinal studies. J Psychosom Res. 2012;73:18–27.
10. Hackett ML, Pickles K. Part I: frequency of depression after stroke: an updated systematic review and meta-analysis of observational studies. Int J Stroke. 2014;9:1017–1025.
11. Marzolini S, Fong K, Jagroop D, et al. Eligibility, enrollment, and completion of exercise-based cardiac rehabilitation following stroke rehabilitation: what are the barriers? Phys Ther. 2020;100:44–56.
12. Virani SS, Alonso A, Benjamin EJ, et al. Heart disease and stroke statistics—2020 update: a report from the American Heart Association. Circulation. 2020;141:e139–e596.
13. Wiles R, Demain S, Robison J, Kileff J, Ellis-Hill C, McPherson K. Exercise on prescription schemes for stroke patients post-discharge from physiotherapy. Disabil Rehabil. 2008;30:1966–1975.
14. Simpson LA, Eng JJ, Tawashy AE. Exercise perceptions among people with stroke: barriers and facilitators to participation. Int J Ther Rehabil. 2011;18:520–529.
15. Hendrickx W, Vlietstra L, Valkenet K, et al. General lifestyle interventions on their own seem insufficient to improve the level of physical activity after stroke or TIA: a systematic review. BMC Neurol. 2020;20:1–13.
16. Tang A, Closson V, Marzolini S, Oh P, McIlroy WE, Brooks D. Cardiac rehabilitation after stroke-need and opportunity. J Cardiopulm Rehabil. 2009;29:97–104.
17. Nguyen CH, Marzolini S, Oh P, Thomas SG. Entering cardiac rehabilitation with peripheral artery disease: a retrospective comparison to coronary artery disease. J Cardiopulm Rehabil Prev. 2020;40(4):255–262.
18. Toma J, Hammond B, Chan V, et al. Inclusion of people poststroke in cardiac rehabilitation programs in Canada: a missed opportunity for referral. Can J Cardiol Open. 2020;2:195–206.
19. Supervía M, Turk-Adawi P, Pesah E, et al. Availability and quality of cardiac rehabilitation around the globe: patients served, providers, and core components. J Am Coll Cardiol. 2018;71:1881.
20. Nguyen H, Manolova G, Daskalopoulou C, Vitoratou S, Prince M, Prina AM. Prevalence of multimorbidity in community settings: a systematic review and meta-analysis of observational studies. J Comorb. 2019;9:2235042X19870934.
21. Krueger H, Koot J, Hall RE, O'Callaghan C, Bayley M, Corbett D. Prevalence of individuals experiencing the effects of stroke in Canada: trends and projections. Stroke. 2015;46:2226–2231.
22. Ovbiagele B, Goldstein LB, Higashida RT, et al. Forecasting the future of stroke in the United States: a policy statement from the American Heart Association and American Stroke Association. Stroke. 2013;44:2361–2375.
23. GBD 2016 Lifetime Risk of Stroke Collaborators; Feigin VL, Nguyen G, Cercy K, et al. Global, regional, and country-specific lifetime risks of stroke, 1990 and 2016. N Engl J Med. 2018;379:2429–2437.
24. Mao L, Jin H, Wang M, et al. Neurologic manifestations of hospitalized patients with coronavirus disease 2019 in Wuhan, China. JAMA Neurol. 2020;77(6):1–9.
25. Hess DC, Eldahshan W, Rutkowski E. COVID-19-related stroke. Transl Stroke Res. 2020;11:322–325.
26. Luengo-Fernandez R, Gray AM, Rothwell PM. A population-based study of hospital care costs during 5 years after transient ischemic attack and stroke. Stroke. 2012;43:3343–3351.
27. Vernino S, Brown RD, Sejvar JJ, Sicks JD, Petty GW, O'Fallon WM. Cause-specific mortality after first cerebral infarction: a population-based study. Stroke. 2003;34:1828–1832.
28. Hartmann A, Rundek T, Mast H, et al. Mortality and causes of death after first ischemic stroke: the Northern Manhattan Stroke Study. Neurology. 2001;57:2000–2005.
29. Prosser J, MacGregor L, Lees KR, Diener HC, Hacke W, Davis S. Predictors of early cardiac morbidity and mortality after ischemic stroke. Stroke. 2007;38:2295–2302.
30. Fini NA, Holland AE, Keating J, Simek J, Bernhardt J. How physically active are people following stroke? Systematic review and quantitative synthesis. Phys Ther. 2017;97:707–717.
31. Dhamoon MS, Sciacca RR, Rundek T, Sacco RL, Elkind MS. Recurrent stroke and cardiac risks after first ischemic stroke: the Northern Manhattan Study. Neurology. 2006;66:641–646.
32. Hackam DG, Spence JD. Combining multiple approaches for the secondary prevention of vascular events after stroke: a quantitative modeling study. Stroke. 2007;38:1881–1885.
33. Towfighi A, Markovic D, Ovbiagele B. Impact of a healthy lifestyle on all-cause and cardiovascular mortality after stroke in the USA. J Neurol Neurosurg Psychiatry. 2012;83:146–151.
34. Naci H, Ioannidis JP Comparative effectiveness of exercise and drug interventions on mortality outcomes: metaepidemiological study. BMJ. 2013;347:f5577.
35. Derdeyn CP, Chimowitz MI, Lynn MJ, et al. Aggressive medical treatment with or without stenting in high-risk patients with intracranial artery stenosis (SAMMPRIS): the final results of a randomised trial. The Lancet. 2014;383:333–341.
36. Collins M, Clifton E, van Wijck F, Mead G. Cost-effectiveness of physical fitness training for stroke survivors. J R Coll Phys Edinb. 2018;48:62–68.
37. Cuccurullo SJ, Fleming TK, Kostis WJ, et al. Impact of a stroke recovery program integrating modified cardiac rehabilitation on all-cause mortality, cardiovascular performance and functional performance. Am J Phys Med Rehabil. 2019;98:953–963.
38. Saunders DH, Sanderson M, Hayes S, et al. Physical fitness training for stroke patients. Cochrane Database Syst Rev. 2020;3: CD003316.
39. Quaney BM, Boyd LA, McDowd JM, et al. Aerobic exercise improves cognition and motor function poststroke. Neurorehabil Neural Repair. 2009;23:879–885.
40. Marzolini S, Tang A, McIlroy W, Oh PI, Brooks D. Outcomes in people after stroke attending an adapted cardiac rehabilitation exercise program: does time from stroke make a difference? J Stroke Cerebrovasc. 2014;23:1648–1656.
41. Patterson SL, Rodgers MM, Macko RF, Forrester LW. Effect of treadmill exercise training on spatial and temporal gait parameters in subjects with chronic stroke: a preliminary report. J Rehabil Res Dev. 2008;45:221–228.
42. Tang A, Marzolini S, Oh PI, McIlroy WE, Brooks D. Feasibility and effects of adapted cardiac rehabilitation after stroke: a prospective trial. BMC Neurol. 2010;10:40.
43. Liu-Ambrose T, Eng JJ. Exercise training and recreational activities to promote executive functions in chronic stroke: a proof-of-concept study. J Stroke Cerebrovasc Dis. 2015;24:130–137.
44. Prior PL, Hachinski V, Unsworth K, et al. Comprehensive cardiac rehabilitation for secondary prevention after transient ischemic attack or mild stroke I: feasibility and risk factors. Stroke. 2011;42:3207–3213.
45. Regan EW, Handlery R, Beets MW, Fritz SL. Are aerobic programs similar in design to cardiac rehabilitation beneficial for survivors of stroke? A systematic review and meta-analysis. J Am Heart Assoc. 2019;8:e012761.
46. Prior PL, Hachinski V, Chan R, et al. Comprehensive cardiac rehabilitation for secondary prevention after transient ischemic attack or mild stroke. J Cardiopulm Rehabil Prev. 2017;37:428–436.
47. Marzolini S, Brooks D, Oh P, et al. Aerobic with resistance training or aerobic training alone poststroke: a secondary analysis from a randomized clinical trial. Neurorehabil Neural Repair. 2018;32:209–222.
48. Marzolini S, Oh PI, Thomas SG, Goodman JM. Aerobic and resistance training in coronary disease: single versus multiple sets. Med Sci Sports Exerc. 2008;40:1557–1564.
49. Spahillari A, Mukamal KJ, DeFilippi C, et al. The association of lean and fat mass with all-cause mortality in older adults: the Cardiovascular Health Study. Nutr Metab Cardiovasc Dis. 2016;26:1039–1047.
50. Srikanthan P, Horwich TB, Tseng CH. Relation of muscle mass and fat mass to cardiovascular disease mortality. Am J Cardiol. 2016;117:1355–1360.
51. Artero EG, Lee DC, Ruiz JR, et al. A prospective study of muscular strength and all-cause mortality in men with hypertension. J Am Coll Cardiol. 2011;57:1831–1837.
52. FitzGerald SJ, Barlow CE, Kampert JB, Morrow JR, Jackson AW, Blair SN. Muscular fitness and all-cause mortality: prospective observations. J Phys Act Health. 2004;1:7–18.
53. Winstein CJ, Stein J, Arena R, et al.; on behalf of the American Heart Association Stroke Council, Council on Cardiovascular and Stroke Nursing, Council on Clinical Cardiology, and Council on Quality of Care and Outcomes Research. Guidelines for adult stroke rehabilitation and recovery: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2016;47:e98–e169.
54. Brown C, Fraser JE, Inness EL, et al. Does participation in standardized aerobic fitness training during inpatient SR promote engagement in aerobic exercise after discharge? A cohort study. Top Stroke Rehabil. 2014;21:s42–s51.
55. Nathoo C, Buren S, El-Haddad R, et al. Aerobic training in Canadian stroke rehabilitation programs. J Neurol Phys Ther. 2018;42: 248–255.
56. Marzolini S, Robertson AD, Oh P, et al. Aerobic training and mobilization early post-stroke: cautions and considerations. Front Neurol. 2019;10:1187.
57. Krakauer JW, Carmichael ST, Corbett D, Wittenberg GF. Getting neurorehabilitation right: what can be learned from animal models? Neurorehabil Neural Repair. 2012;26:923–931.
58. Powers WJ, Rabinstein AA, Ackerson T, et al. 2018 Guidelines for the early management of patients with acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2018;49:e46–e99.
59. Stroke Foundation. Clinical Guidelines for Stroke Management 2017. v5.2. Melbourne, VIC, Australia: Stroke Foundation; 2017.
60. Hebert D, Lindsay MP, McIntyre A, et al. Canadian stroke best practice recommendations: stroke rehabilitation practice guidelines, update 2015. Int J Stroke. 2016;11:459–484.
61. Küçükdeveci AA, Sunnerhagen KS, Golyk V, et al. Evidence based position paper on Physical and Rehabilitation Medicine (PRM) professional practice for persons with stroke. The European PRM position (UEMS PRM Section). Eur J Phys Rehabil Med. 2018;54:957–970.
62. Bernhardt J, Langhorne P, Lindley RI, et al. Efficacy and safety of very early mobilisation within 24 h of stroke onset (AVERT): a randomised controlled trial. Lancet. 2015;386:46–55.
63. Tzeng Y-C, Ainslie PN. Blood pressure regulation IX: cerebral autoregulation under blood pressure challenges. Eur J Appl Physiol. 2014;114:545–459.
64. Mitchell GF, Vita JA, Larson MG, et al. Cross-sectional relations of peripheral microvascular function, cardiovascular disease risk factors, and aortic stiffness: the Framingham Heart Study. Circulation. 2005;112:3722–3728.
65. Latour LL, Kang D-W, Ezzeddine MA, Chalela JA, Warach S. Early blood-brain barrier disruption in human focal brain ischemia. Ann Neurol. 2004;56:468–477.
66. Keep RF, Zhou N, Xiang J, Andjelkovic AV, Hua Y, Xi G. Vascular disruption and blood-brain barrier dysfunction in intracerebral hemorrhage. Fluids Barriers CNS. 2014;11:18.
67. Attwell D, Buchan AM, Charpak S, Lauritzen M, MacVicar BA, Newman EA. Glial and neuronal control of brain blood flow. Nature. 2010;468:232.
68. Marzolini S, Oh PI, McIlroy W, Brooks D. The feasibility of cardiopulmonary exercise testing for prescribing exercise to people after stroke. Stroke. 2012;43:1075–1081.
69. Olson TP, Tracy J, Dengel DR. Relationship between ventilatory threshold and cerebral blood flow during maximal exercise in humans. Open Sports Med J. 2009;3:9–13.
70. Smith KJ, Ainslie PN. Regulation of cerebral blood flow and metabolism during exercise. Exp Physiol. 2017;102:1356–1371.
71. Ballweg J, Foster C, Porcari J, Haible S, Aminaka N, Mikat RP. Reliability of the talk test as a surrogate of ventilatory and respiratory compensation thresholds. J Sport Sci Med. 2013;12:610.
72. Kernan WN, Ovbiagele B, Black HR, et al. Guidelines for the prevention of stroke in patients with stroke and transient ischemic attack: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2014;45:2160–2236.
73. Gelfand D, Acker JE Jr, Hellerstein HK. Rehabilitation of patients with cardiovascular disease other than stroke—community services. Listing Res Cardiovasc Field. 1964;10:820–826.
74. Suaya JA, Shepard DS, Normand S-LT, Ades PA, Prottas J, Stason WB. Use of cardiac rehabilitation by Medicare beneficiaries after myocardial infarction or coronary bypass surgery. Circulation. 2007;116:1653–1662.
75. Howes T, Mahenderan N, Freene N. Cardiac rehabilitation: are people with stroke or transient ischaemic attack being included? A cross-sectional survey. Heart Lung Circ. 2020;29(3):483–490.
76. Harrison AS, Gaskins NJ, Connell L, Doherty P. Factors influencing the uptake of cardiac rehabilitation by cardiac patients with a comorbidity of stroke. IJC Heart Vasculature. 2020;27:100471.
77. Grace SL, Russell K, Reid R, et al. Effect of cardiac rehabilitation referral strategies on utilization rates: a prospective, controlled study. Arch Intern Med. 2011;117:235–241.
78. Cortés O, Arthur HM. Determinants of referral to cardiac rehabilitation programs in patients with coronary artery disease: a systematic review. Am Heart J. 2006;151:249–256.
79. Oosenbrug E, Pedercini Marinho R, Zhang J, et al. Sex differences in cardiac rehabilitation adherence: a meta-analysis. Can J Cardiol. 2016;32:1316–1324.
80. Ades PA, Keteyian SJ, Wright JS, et al. Increasing cardiac rehabilitation participation from 20% to 70%: a road map from the Million Hearts Cardiac Rehabilitation Collaborative. Mayo Clin Proc. 2017;92:234–242.
81. MacKay-Lyons MJ, Makrides L. Exercise capacity early after stroke. Arch Phys Med Rehabil. 2002;83:1697–1702.
82. Macko RF, Ivey FM, Forrester LW, et al. Treadmill exercise rehabilitation improves ambulatory function and cardiovascular fitness in patients with chronic stroke: a randomized, controlled trial. Stroke. 2005;36:2206–2211.
83. Lennon O, Denis RS, Grace N, Blake C. Feasibility, criterion validity and retest reliability of exercise testing using the Astrand-rhyming test protocol with an adaptive ergometer in stroke patients. Disabil Rehabil. 2012;34:1149–1156.
84. Samayoa L, Grace SL, Gravely S, Scott L, Marzolini S, Colella TJF. Sex differences in cardiac rehabilitation enrollment: a meta-analysis. Can J Cardiol. 2014;30:793–780.
85. Colella TJF, Gravely S, Marzolini S, et al. Sex bias in referral of women to outpatient cardiac rehabilitation? A meta-analysis. Eur J Prev Cardiol. 2015;22:423–441.
86. Marzolini S, Brooks D, Oh PI. Sex differences in completion of a 12-month cardiac rehabilitation programme: an analysis of 5,922 women and men. Eur J Cardiovasc Prev Rehabil. 2008;15:698–703.
87. Marzolini S, Balitsky B, Jagroop D, et al. Factors affecting attendance at an adapted cardiac rehabilitation exercise program for individuals with mobility deficits poststroke. J Stroke Cerbrovasc Dis. 2016;25:87–94.
88. Gabelhouse J, Eves N, Grace SL, Reid RC, Caperchione CM. Traditional versus hybrid outpatient cardiac rehabilitation: a comparison of patient outcomes. J Cardiopulm Rehabil Prev. 2018;38:231–238.
