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NEURO-REHABILITATION SUPPLEMENT
Year : 2023 | Volume
: 26
| Issue : 7 | Page : 15-25
Multi-modal rehabilitation therapy in Parkinson's disease and related disorders
Alvee Saluja1, Vinay Goyal2, Rajinder K Dhamija1
1 Department of Neurology, Lady Hardinge Medical College, New Delhi, India
2 Director-Neurology, Institute of Neurosciences, Medanta, Gurugram, Haryana, India
Correspondence Address:
Rajinder K Dhamija
Neurology Office, Room Number-1099, Old Building 1st Floor, Lady Hardinge, Medical College, New Delhi - 110 001
India
Source of Support: None, Conflict of Interest: None
CheckDOI: 10.4103/aian.aian_164_22
Abstract
Long-term use of dopaminergic therapy in Parkinson's disease (PD) is associated with reduction in efficacy and disabling dyskinesias. The current medical or surgical treatment modalities are ineffective for atypical parkinsonism syndromes. Hence, there is a need for holistic and cost-effective non-pharmacological interventions that act via multiple mechanisms to improve motor as well as non-motor symptoms among PD patients. Rehabilitation strategies focusing on multiple mechanisms can lead to improvement in certain symptoms among PD patients, which may be refractory to medical and surgical therapy. However, there is scanty literature available on the role of various rehabilitation strategies in patients with atypical parkinsonism patients. Multiple rehabilitation strategies such physiotherapy, aerobic exercises, strength/resistance exercises, treadmill training, cueing, dance and music, speech language therapy, occupational therapy, hydrotherapy, and martial arts have been found to improve motor as well as non-motor symptoms among PD patients. Newer modalities such as virtual-reality-based devices, exergaming, wearable sensors, and robotic prosthetic devices may be exciting future prospects in rehabilitation among patients with PD and atypical parkinsonian syndromes. This narrative review assessed and summarized the current evidence regarding the role of various rehabilitation strategies in PD and atypical parkinsonian syndromes. Furthermore, evidence regarding recent advancements in rehabilitation for patients with parkinsonism was highlighted. Despite the beneficial effect of rehabilitation in PD, there is still scanty literature available from India on rehabilitation strategies among PD patients. Larger prospective randomized control trials from India and other low- and middle-income countries, focusing on various rehabilitation strategies among PD patients, are an unmet need.
Keywords: Parkinson disease, physical therapy, rehabilitation
Introduction 
Parkinson's disease (PD) is a common neurodegenerative disorder afflicting the elderly and is second only to Alzheimer's disease in terms of prevalence.[1] The Global Burden of Disease Study for neurological disorders estimated Parkinson's disease (PD) prevalence at 6.06 million for the year 2016.[2] A recent study across various Indian states estimated the prevalence and mortality of PD for 2019 at 770,800 and 45,300, respectively.[3] Thus, the burden of PD is huge, both globally and in India.
The cardinal motor manifestations of PD are bradykinesia, tremors, rigidity, and postural instability. Additionally, PD has a multitude of non-motor manifestations, such as autonomic dysfunction, sleep disturbances, and cognitive and mood changes.[4],[5] Dopaminergic therapy remains the cornerstone of treatment in PD, with surgery (deep brain stimulation) being an option in a limited subgroup of PD patients. However, non-motor symptoms respond poorly to available therapies and significantly worsen the quality of life (QOL) among PD patients.[6] Long-term use of dopaminergic therapy in PD is associated with progressively decreasing efficacy along with the appearance of disabling dyskinesias, especially among advanced cases. Furthermore, balance dysfunction and gait freezing episodes respond poorly to dopaminergic therapy and deep brain stimulation (DBS) due to the involvement of non-dopaminergic pathways.[7] Hence, there is a need for holistic and cost-effective non-pharmacological interventions that act via multiple mechanisms to improve motor as well as non-motor symptoms among PD patients.
Multiple studies have shown the beneficial effects of various rehabilitation strategies in motor and non-motor symptoms among PD patients.[8],[9],[10],[11] The effect of exercise in neurodegenerative diseases such as PD could be explained via neuroplasticity of dopaminergic signaling and neurotransmission. Exercise also increases synaptic strength and brain connectivity and may improve behavior in PD patients.[12],[13],[14] Furthermore, studies have shown that physical exercise reduces chronic oxidative stress and stimulates synthesis neurotransmitters and trophic factors (particularly BDNF, FGF-2, and IGF1).[15],[16]
The majority of available literature has focused on the role of rehabilitation strategies in PD, and scanty literature is available on the role of rehabilitation in atypical parkinsonism. Because atypical parkinsonian syndromes respond poorly to currently available treatment options, rehabilitation strategies may be the only feasible options in such cases. However, studies that have assessed the role of different rehabilitation strategies among patients with advanced PD and atypical parkinsonism have included very few patients. Thus, evidence regarding the efficacy of different rehabilitation strategies (in isolation or delivered in combination) for patients with parkinsonism needs appraisal so that a safe, suitable, and effective rehabilitation program may be devised for a particular patient. Furthermore, virtual reality or robotic device-based strategies may be promising additions, especially among those with advanced PD and atypical parkinsonism where limited benefit is achieved with conventional rehabilitation.
This narrative review of literature assessed and summarized the current evidence regarding the role of various rehabilitation strategies in PD and atypical parkinsonian syndromes. In addition, this article reviewed the evidence regarding the role of recent advances and future prospects of rehabilitative strategies in these disorders.
Methods A literature search was conducted in MEDLINE (PubMed) and Cochrane databases using the following search terms: “Parkinson's Disease AND Rehabilitation,” “Parkinsonism AND Rehabilitation Therapy,” “Multimodal Rehabilitation therapy AND Parkinson's Disease,” “Physical Therapy AND Parkinson's Disease,” “Occupational Therapy AND Parkinson's Disease,” “Speech Language Therapy AND Parkinson's Disease,” “Tai Chi AND Parkinson's Disease,” “Yoga AND Parkinson's Disease,” “Dance therapy AND Parkinson's Disease,” “Music Therapy AND Parkinson's Disease,” “Hydrotherapy AND Parkinson's Disease.” In MEDLINE (PubMed), 23,895 results were obtained using the term “Parkinson's Disease AND Rehabilitation,” 6682 results obtained using “Parkinsonism AND Rehabilitation Therapy,” 608 results using “Multimodal Rehabilitation therapy AND Parkinson's Disease,” 42,438 results using “Physical Therapy AND Parkinson's Disease,” 7484 results using “Occupational Therapy AND Parkinson's Disease,” 8938 results using “Speech Language Therapy AND Parkinson's Disease,” 1650 results using “Tai chi AND Parkinson's Disease,” 1365 results using “Yoga and Parkinson's Disease,” 1373 results using “Dance therapy AND Parkinson's Disease,” 2336 results using “Music therapy AND Parkinson's Disease,” and 219 results using “Hydrotherapy AND Parkinson's Disease.” In the Cochrane database, the search term “Parkinson's Disease AND Rehabilitation” yielded 90 results, “Parkinsonism AND Rehabilitation Therapy” yielded 94 results, “Physical Therapy AND Parkinson's Disease” yielded 227 results, “Occupational Therapy AND Parkinson's Disease” yielded 89 results, “Speech Language Therapy AND Parkinson's Disease” yielded 76 results, “Tai chi AND Parkinson's Disease” yielded 10 results, “Yoga and Parkinson's Disease” yielded 15 results, “Dance Therapy and Parkinson's Disease” yielded 22 results, “Music Therapy AND Parkinson's Disease” yielded 28 results, and “Hydrotherapy AND Parkinson's Disease” yielded 1 result. We reviewed the relevant full text results and study abstracts. Furthermore, references of relevant studies were reviewed. We included randomized control trials (RCTs), trial protocols, consensus guidelines, cohort studies, systematic reviews, meta-analysis, review articles, pilot studies, case reports, observational studies, and pre-post studies until 2021 in this narrative review.
Role of Conventional Physiotherapy in PD Conventional physiotherapy in PD consists of both passive interventions administered by physiotherapists (massage, Bobath technique, and passive stretching) and active exercises (practicing daily functional activities) done by patients themselves.[17] The goals of conventional physiotherapy are as follows: (1) improvement in physical capacity of the individual, (2) improvement in transfers, (3) improvement in manual activities, upper limb function, and dexterity, (4) improvement in balance, gait, posture, and prevention of falls, and (5) reduction in pain.[18] Some of the active exercises that patients with PD can perform as part of conventional physiotherapy are climbing up and down the stairs, sitting down and rising from a chair, rolling over in bed, walking with large amplitude arm swing or steps, and walking and maintaining balance while dual tasking such as talking. The various active exercises which can be performed as part of conventional physiotherapy protocols among PD patient are enumerated in [Box 1].
Multiple studies have shown the beneficial effects of conventional physiotherapy on various symptoms in PD. A Cochrane review consisting of 39 randomized trials with 1827 PD patients (of any duration or severity) found that physiotherapy significantly improved gait speed [standard mean difference (SMD) 0.04 m/s, 95% confidence interval (CI) 0.02–0.06, P = 0.0002]; freezing of gait (−1.41, 95% CI −2.63 to −0.19, P = 0.02); functional mobility, and balance outcomes of Timed Up and Go test (TUG) (−0.63 s, 95% CI −1.05 to −0.21, P = 0.003), functional reach test (FRT) (2.16 cm, 95% CI 0.89–3.43, P = 0.0008), and Berg balance scale (BBS) (3.71 points, 95% CI 2.30–5.11, P < 0.00001); and clinician-rated disability using the unified PD rating scale (UPDRS) (total − 6.15 points, 95% CI −8.57 to −3.73, P < 0.00001; activities of daily living (ADLs): −1.36, 95% CI −2.41 to −0.30, P = 0.01; and motor: −5.01, 95% CI −6.30 to −3.72, P < 0.00001) when compared to no physiotherapy.[17] However, this review comprised all forms of physiotherapy (including conventional physiotherapy) with patients often receiving multiple rehabilitation interventions in addition to conventional physiotherapy.
A recent randomized crossover trial comparing a 3 month group-based active balance exercise program versus usual care (inactivity) in 23 PD patients [Hoehn and Yahr (H&Y) stages 2 or 3] found a 37% reduction in rate of falls per month (95% CI 24–48%).[19] A recent meta-analysis which included 45 trials found a beneficial effect of conventional physiotherapy on UPDRS (n = 26; SMD 0.48, 95% CI 0.35–0.60, P < 0.001), 10 meter walk test (MWT) (n = 5; SMD 0.30, 95% CI 0.01–0.59, P < 0.04), cadence (n = 4; SMD 0.52, 95% CI 0.11–0.92, P = 0.01), and freezing of gait questionnaire (FOG-Q) scores (SMD 0.24, 95% CI 0.04–0.43, P = 0.02).[20]
Although conventional physiotherapy has been shown to improve motor symptoms of PD, the exercise regimen, frequency, duration, and intensity of exercises have not been clearly defined.[21],[22] The European guidelines on physiotherapy in PD recommend physiotherapy three times per week with a duration of 45 minutes at a time for a period of 12 weeks.[18] However, it is important to develop a personalized exercise regimen for a particular patient depending on individual goals, capacity, feasibility, and preferences. One must take a thorough history enquiring specifically regarding symptom duration, severity, activity limitations, barriers regarding exercise, and available support systems (at home or access to exercise groups). After a thorough history, examination focusing on UPDRS, H&Y staging, followed by risk stratification by using measurement tools is done. The measurement tools for risk stratification and monitoring treatment responses to physiotherapy among patients with PD are shown in [Table 1].
It is important to note that most of the physical therapy trials have included PD patients belonging to H&Y stages 1–3 (mild-to-moderate disease). Thus, the beneficial effects of exercise may be more pronounced during the early stages of the disease and this may be due to its neuroprotective effect on the remaining nigrostriatal dopaminergic neurons.[23]
Role of Aerobic, Strength, or Resistance Exercise Training in PD Various types of exercises have been shown to improve motor, non-motor symptoms, as well as the Quality of Life (QOL) among patients with PD. It is recommended that patients with PD strive toward achieving the WHO goals of physical activity for adults. According to these recommendations, adults between 18 and 64 years should engage in moderate-intensity aerobic physical activity for >150 minutes/week or vigorous intensity physical activity for >75 minutes/week or a combination thereof that are performed in bouts of 10 minutes duration. In adults >65 years, the same recommendations apply but balance exercise for ≥3 times/week is to be included in those with poor mobility. In addition, muscle-strengthening exercises of all major muscle groups for ≥2 days/week are recommended.[24] Examples of moderate and vigorous aerobic physical activities that can be advised in patients with PD are enumerated in [Table 2].
Multiple studies have shown the beneficial effect of different types of exercises in PD. A recent study found that a low-intensity 8 week cycling intervention (total of 16 training sessions) resulted in significant improvement of UPDRS-III [P-value (off): 0.001; P value (on state): 0.004] and TUG test scores (P-value: 0.003).[25] A RCT comparing aerobic endurance training (by cycle ergometer) and Tai chi found a significant improvement in UPDRS total scores, UPDRS III sub scores, and PD questionnaire 39 (PDQ-39) scores in the aerobic exercise group.[26] Kolk et al.[27] have reported a significant improvement in UPDRS-III scores and VO2 max with a remotely supervised aerobic exercise program (3 sessions/week for 6 months) when compared to stretching exercises alone.
In a systematic review and meta-analysis of 8 controlled trials and strength or resistance exercise training (whole body, lower body, and core strengthening using weights or machines) resulted in improvement in the upper as well as lower limb muscle strength. Furthermore, strength or resistance exercise resulted in significant improvement in movement speed, UPDRS III scores, balance, and mobility. However, there was no significant improvement in mood, falls, fatigue, functional capacity, and QOL.[28] In a review of 8 studies (6 systematic reviews with meta-analysis and 2 systematic reviews) by Paolucci et al.,[29] it has been suggested that progressive resistance training conducted 2–3 times/week for a duration of 10 weeks should be a part of PD rehabilitation programs for improving muscle strength, endurance, and improvement of motor symptoms in PD. A RCT has shown that adapted resistance training with instability (ARTI) using devices (such as a foam pad, dynamic discs, or a bionic oscillatory stabilization unit device), when compared to traditional motor rehabilitation, resulted in the reduction of new freezing of gait scores (NFOGQ) scores [P < 0.0001, Effect Size (ES) = 0.80], UPDRS III motor scores (P < 0.0001, ES = 0.66), Stroop III test values (P < 0.0001, ES = 0.35), and PDQ39 scores (P = 0.0001, ES = 0.54).[30] A recent systematic review and meta-analysis including 41 studies with 1838 participants found a moderate effect for all forms of exercise/training on freezing of gait (Z = 4.91, ES= −0.37, P < 0.00001, 95% CI −0.51 to −0.22). However, the statistical heterogeneity across studies in this review was marked.[31]
The benefits of exercises are not just limited to motor symptoms. A single center, prospective, parallel-group, RCT comprising 51 non-demented patients with mild–moderate PD showed that progressive resistance exercise training (PRET) or modified fitness count program (stretching, balance, breathing, and non-progressive strengthening exercises) delivered twice a week for 24 months resulted in improvement from baseline in digit span, Stroop, and brief test of attention scores.[32] Passive cycling interventions and moderate aerobic exercise activities have been found to improve executive function among patients with PD.[33] Two small RCTs have found an improvement in sleep quality among PD patients using multimodal exercise regimens or resistance training.[34],[35] A large RCT involving 231 PD patients demonstrated that strengthening exercises (40–60 minutes, 3 times/week for a duration of 6 months) resulted in improvement of positive effects compared to usual care.[36] Aerobic exercises (2 times/week for 12 weeks) too have been found to improve mood among 13 patients with early PD compared to those who did not exercise.[37] In a large longitudinal cohort study of 3408 participants with at least 3 clinic visits over 2 years, consistent exercises (>2.5 hours/week) or early start of exercise resulted in improvement of health-related QOL as well as mobility.[38]
Treadmill Training in Pd Gait disturbances are one of the most debilitating motor symptoms in PD.[39] Treadmill training may be an effective and promising tool for gait rehabilitation among patients with PD. Once trained, patients may continue exercises independently with minimal to no supervision. Multiple studies have shown the beneficial effects of treadmill training in PD. In a single-blinded, prospective, parallel-group trial, 67 patients with PD (H&Y stages 1–3) were randomly assigned to either (1) high-intensity treadmill training (30 minutes; 70–80% heart rate reserve), (2) low-intensity treadmill training (50 minutes; 40–50% heart rate reserve), or (3) stretching and resistance exercises (2 sets; 10 repetitions on each leg; 3 resistance machines). The lower-intensity treadmill group and the stretching/resistance exercises group showed a statistically significant improvement on 6MWT [12% increase, P (low-intensity treadmill): 0.001 and 9% increase, P (stretching) < 0.02]. Both treadmill protocols significantly improved peak V̇O2 (7–8% increase; P < 0.05).[40] In a Cochrane review of 18 trials (633 participants), treadmill training resulted in an improvement in gait speed (MD = 0.09 m/s; 95% CI 0.03–0.14; P = 0.001, I2 = 24%; moderate-quality evidence) and stride length (MD = 0.05 meters; 95% CI 0.01–0.09; P = 0.01, I2 = 0%; low-quality evidence).[41] A recent single blinded randomized pilot study consisting of 30 randomized PD patients found that low-frequency (2 days/week) and intermediate-frequency (3 days/week) treadmill training sessions resulted in significant improvement in TUG, 10MWT, Falls Efficacy Scale (FES), and Falls diary scores.[42] Another randomized single blinded clinical trial including 20 PD patients showed that moderate-intensity treadmill intervention (60% heart rate reserve) resulted in significant improvement at 2 and 4 months after the baseline analysis in TUG [P (2 months): 0.003, P (4 months): 0.001], 6MWT [P (2 months): 0.003, P (4 months): 0.004]. Treadmill training also resulted in significant improvement in SF-8 scores 4 months post the baseline analysis. Thus, treadmill training resulted in short-term as well as long-term benefits.[43] A systematic review and meta-analysis of 16 trials found that treadmill training resulted in significant improvement in walking velocity (MD 0.21 m/s, 95% CI 0.15–0.27), stride length (MD 0.12 m, 95% CI 0.02–0.23), and step length (MD 0.12 m, 95% CI 0.01–0.23) in patients with PD. However, there was no improvement in cadence or walking endurance.[44] Body weight-supported treadmill training (BWSTT) may provide even greater symptomatic benefit among PD patients. In a recent double-blinded RCT, 10% BWSTT and 20% BWSTT resulted in greater improvements in 6MWD (P = 0.004 and P < 0.001, respectively), UPDRS motor score (P = 0.012 and P = 0.005, respectively), Nottingham Health Profile pain subscore (P = 0.003 and P = 0.002, respectively), and fatigue (P = 0.005 for both) compared to unsupported treadmill training.[45]
Strategy Training (Cueing)-Based Rehabilitation and Pd Striatal dopamine loss results in defective sensorimotor integration. This leads to a reduced ability to detect internal sensory or movement cues. Over time, PD patients become overdependent on environmental stimuli for automatically initiating and/or maintaining movements.[46],[47],[48] Cueing applies a spatial or temporal stimulus that facilitates initiation or maintenance of a motor activity.[49] Cueing bypasses the defective basal ganglia (BG) and may result in neuroplasticity of the cortico-BG-cerebellar circuitry.[50] Cueing may involve visual, auditory, or somatosensory modalities and is of two types: (1) open-loop cueing and (2) closed-loop cueing. In open-loop cueing, stimuli are provided in a preset manner independent of the patient's performance, whereas in the closed-loop type, there is real-time feedback of the patient's performance, which can facilitate movements to achieve the optimum response.[51],[52]
Nordic walking involves walking with long poles (similar to skiing poles) held in the upper limbs. Nordic walking has been found to significantly improve motor symptoms, gait, freezing, and balance parameters among PD patients when compared to sham or no exercise.[53],[54] In a case-control study involving 19 PD patients and 17 controls, visual cueing by means of white transverse stripes (25 cm and 50 cm apart) on a medical treadmill resulted in significantly better stride length (P < 0.001), stride time (P < 0.001), and cadence [P (narrow strips): 0.002; P (wide strips) < 0.001] among PD patients compared to controls.[55] Rhythmic auditory stimulation (RAS) by means of an auditory pacer device delivering beats at a fixed rate while walking has been shown to significantly improve gait speed and stride length after 1 week when compared to walking at usual speed without cues in 21 PD patients.[56] Combined auditory and visual cueing by a virtual reality cycling system (V-cycle) has been found to improve pedaling speeds in PD patients.[57] In a prospective single blinded RCT, adults 60–90 years of age (including PD patients; H&Y stages 2–3) were randomized to treadmill training with virtual reality (VR) motion capture visual feedback system versus treadmill training alone. Treadmill training plus VR (3 sessions for 6 weeks) resulted in significant reduction in fall rates (P: 0.01) at the end of 6 months of follow-up among patients with PD.[58] A recent parallel-group assessor blinded RCT compared RAS (musical song) along with treadmill training versus treadmill training alone in 50 PD patients. The trial concluded that RAS plus treadmill training was superior to treadmill training alone in improving FES (P < 0.001), functional gait assessment (FGA) (P < 0.001), TUG (P < 0.001), and UPDRS (P < 0.001).[59] A recent systematic review involving 18 studies found that RAS improved gait velocity, cadence, and stride length among PD patients.[60] A recent randomized crossover trial in 12 PD patients compared somatosensory cueing via a wireless wrist-based vibratory cueing device (ArmSense) and visual cueing (via stripes on ground). The ArmSense device was found to significantly improve the step length during comfortable walking (P: 0.002) and cadence (P < 0.001) when compared to visual cueing.[61] Furthermore, a single blinded multicentric phase II RCT of smartphone-based on-demand auditory cueing in freezing of gait among PD patients is ongoing (DeFOG trial).[62]
Occupational Therapy and Pd Occupational therapy (OT) helps patients in maintaining usual levels of selfcare, work, and leisure activities as far as possible. During advanced stages of the disease, an occupational therapist may help PD patients in adapting to the environment by developing new activities and roles. In a Cochrane review of two RCTs, a small improvement was noted with occupational therapy in PD.[63] The PD REHAB trial was a large, multi-center, open-label RCT that included 762 patients with mild to moderate PD. Patients were randomized to receive physiotherapy plus occupational therapy versus no therapy, and the effect on the ADL and health-related QOL was assessed. At the end of 3 months, there was no significant difference in the Nottingham Extended Activities of Daily Living (NEADL) scores nor the PDQ-39 scores [P (NEADL): 0.41; P (PDQ39): 0.99].[64] A recent systematic review including 10 studies (1343 PD patients) found that a few studies showed an improvement in perceived occupational performance and upper limb function with OT. Majority of the studies in this review did not find a significant improvement with OT in ADL, QOL, mobility, and global function among PD patients.[65] Thus, there are limited studies with conflicting results on the role of occupational physiotherapy in PD rehabilitation. However, according to the National Institute for Health and Clinical Excellence guidelines, an occupational physiotherapist should assist PD patients in maintaining work, family roles, improvement in transfers/mobility, selfcare activities, environmental safety strategies, improvement of balance, and cognitive rehabilitation.[66]
Speech and Language Rehabilitation in Pd Eighty nine percent of PD patients may develop speech disturbances, which can be disorders of voice (reduced loudness, monotonous voice, and breathy quality), articulation (imprecise consonants and vowel centralization), and rate (increased, decreased, and variable).[67],[68] Defects in central sensory processing and internal cueing may be responsible for these speech errors and may be a possible explanation for poor responsiveness to dopamine replacement therapy.[69],[70] A Cochrane review in 2012 that included only three trials concluded that there was insufficient evidence to prove or disprove the benefit of speech language (SPL) therapy in PD.[71] However, recent literature has found SPL therapy to be beneficial in PD rehabilitation. In a recent RCT, the benefit of the Lee Silverman Speech Therapy LOUD (LVST LOUD) was compared with a protocol targeting articulation (LVST ARTIC) and with untreated PD patients (UNTXPD). At the end of 1 and 7 months, participant-reported Modified Communication Effectiveness Index (CETI-M) was assessed. Both LVST LOUD and LVST ARTIC improved the CETI-M scores at the end of 1 month compared to UNTXPD [P (LVST LOUD): 0.02; P (LVST ARTIC): 0.02]. However, only LVST LOUD protocol improved CETI-M at the end of 7 months.[72] A recent meta-analysis that included 10 studies (230 treatment groups and 205 control groups) found that SPL therapy improved sound pressure levels during sustained phonation, reduced voice handicap index scores, and improved reading of the rainbow passage and monologue (an objective speaking skill test) at 6 and 12 months after treatment.[73]
Dance, Music, and Singing Therapy in Pd Rehabilitation Dancing may improve speed of movement, balance, wellbeing, and QOL in patients with PD.[74],[75] Multiple dancing interventions and their impact on symptomatology of PD patients have been assessed. In a systematic review of 38 articles that studied the role of various dancing interventions (tango, waltz/foxtrot, Sardinian folk dancing, Irish set dancing, Brazilian samba, Zumba, mixed dance forms, and home-based dance interventions), there was a moderate-to-large beneficial effect of dancing interventions in mild-to-moderate PD. Dancing sessions (once/week to daily for 30 minutes to 2 hours) significantly improved balance, total UPDRS, mobility, endurance, gait freezing, and depression among PD patients.[76]
Music and rhythmic auditory stimulation can improve gait parameters in PD.[77] BEATWALK is a smartphone-based application that initially assesses cadence in PD patients and then progressively increases musical tempo in order to reach the desired speed. A recent study found that BEATWALK significantly improved gait velocity (P < 0.01), cadence (P: 0.01), stride length (P: 0.04), and distance (P: 0.01) among 39 PD patients who could walk unaided and had no gait freezing.[78] The ParkinSong trial studied the effect of singing intervention (at weekly and monthly intervals) in PD and found significant improvements in vocal intensity (P = 0.018), maximum expiratory pressure (P = 0.032), and voice-related QOL (P = 0.043) among PD patients when compared to controls.[79] A recent systematic review and meta-analysis including 67 publications found that tango resulted in significantly improved UPDRS-III scores (Z = 2.87, P = 0.004) and TUG scores (Z = 11.25, P < 0.00001), whereas PD-specific dance resulted in improvement in PDQ-39 scores (Z = 3.77, P = 0.0002) when compared to usual care.[80]
Hydrotherapy in Pd Rehabilitation An aquatic environment allows PD patients to undergo balance training safely and reduces the risk of falls. In a single blinded pilot RCT, 34 PD patients were randomized for hydrotherapy (60 minutes, 5 days/week for 2 months) versus land-based therapy (cardiovascular, stretching, and balance exercises). Hydrotherapy resulted in significant improvement in the center of pressure sway with closed eyes (P: 0.05), BBS scores (P: 0.005), FES (P: 0.003), Activities-Specific Balance Confidence Scale (P: 0.0001), Falls diary (P: 0.001), and PDQ39 scores (P: 0.006).[81] Halliwick aquatic therapy exercises specifically focus on complex rotational movements, balance, trunk mobility, core stabilization, walking, and stretching exercises. In a recent study, Halliwick aquatic therapy was compared with traditional aquatic physiotherapy and land-based exercises. Halliwick aquatic therapy was safe and showed a significant improvement in Mini-BESTest scores for balance.[82] A recent meta-analysis including 8 trials on hydrotherapy also showed a beneficial effect on TUG, BBS, and FES scores in PD.[20]
Yoga, Boxing Therapy, and Whole-Body Vibration in Pd Rehabilitation Multiple studies have shown the safety and efficacy of yoga in PD. Mindfulness programs over 8 weeks have been shown to significantly improve non-motor symptoms (particularly anxiety and depression) and QOL compared to stretching/resistance exercises among PD patients.[83],[84]
A recent double-blinded RCT found that boxing sessions (60 minute session, 3 times/week for 10 weeks) resulted in significant improvement in motor symptoms among PD patients compared to sensory exercises alone.[85]
A Cochrane review that included 6 trials on PD concluded that there was insufficient evidence regarding the role of whole-body vibration in PD rehabilitation.[86]
Martial Arts (Tai Chi and Qigong) in Pd Rehabilitation Tai chi and Qigong are Chinese martial art forms that incorporate flexibility, neuromuscular conditioning, balance training along with body awareness, focused mental attention, imagery, and multi-tasking.[87] A systematic review of 21 studies (15 RCTs and 755 subjects) showed that Tai Chi Qigong was associated with significant improvements in UPDRS III scores (ES = −0.444, P < 0.001), balance (ES = 0.544, P < 0.001), TUG (ES = −0.341, P = 0.005), falls (ES = −0.403, P = 0.004), depression (ES = −0.457, P = 0.008), QOL (ES = −0.393, P < 0.001) among PD patients.[88]
Exergaming and Rehabilitation in Pd Exergames (exercise + games) are videogame-based strategies that may improve PD symptoms as patients are involved in cognitive activities along with physical movements. These gaming strategies can also stimulate cueing mechanisms when combined with virtual reality tools. A recent systematic review of 16 studies showed that virtual-reality based rehabilitation can significantly improve balance, gait speed, mobility, QOL, and level of confidence.[89] Studies using platforms such as Nintendo Wii (example Wii Balance Board) and Microsoft Kinect have been shown to improve motor symptoms (especially gait and balance) among PD patients. In a systematic review of 64 studies (including Kinect, Wii Balance Board, and WiiMote modalities), exergaming platforms significantly improved motor (TUG and BBS) and cognitive domains (attention, alertness, working memory, and executive function). Exergames were a safe alternative to traditional rehabilitation in home settings as well.[90] Pooled data of 9 trials on exergaming (303 participants) has shown a moderately large beneficial effect on TUG, BBS, and PDQ39 scores compared to sham or no intervention.[20]
Neurocognitive Strategies and Non-Invasive Neurostimulation in PD Rehabilitation Motor imagery (MI) is a cognitive process in which a person imagines that he is performing a movement/task without actual muscle involvement. Action observation (AO) is a technique of motor learning by observing tasks performed by others. These techniques act by somatosensory integration, multisensory processing, neuroplasticity by long-term potentiation, and by involving the mirror neuron systems.[91],[92] Action observation therapy in addition to physiotherapy has been found to significantly improve UPDRS and Functional Independence Measure (FIM) scale scores compared to physiotherapy alone among PD patients.[93] In a RCT, autogenic training in addition to physiotherapy resulted in significant improvement in UPDRS motor scores (MD: 4.3; 95% CI 2.5–6; P: 0.00) at the end of 12 weeks among PD patients (H&Y stages 2–3) compared to physiotherapy alone.[94] Transcranial direct stimulation (tDCS) along with visual cueing has been recently shown to significantly improve UPDRS, FGA, and cadence compared to visual cueing with sham tDCS.[95] Application of repetitive transcranial magnetic stimulation (rTMS) at 1 Hz and 25 Hz to treadmill training was found to significantly improve walking speed at 3 months post-intervention. Furthermore, rTMS with the treadmill training group had significant and sustained improvement in TUG and UPDRS part III motor scores.[96]
Multidisciplinary Intensive Rehabilitation Therapy in PD Multidisciplinary intensive rehabilitation therapy (MIRT) is a multidisciplinary, aerobic, motor-cognitive goal-directed rehabilitation strategy.[97] It consists of a 4 week program having 4 daily sessions (each session is of 1 hour) for 5 days and 1 hour of physical exercise on the sixth day. The components of the MIRT program include cardiovascular warm-up, active and passive exercises, balance training using a stabilometric platform, treadmill training with cueing strategies (treadmill plus strategy as described previously), occupational therapy, and SPL therapy session for 1 hour. Other components which may be added are virtual-reality devices, hydrotherapy, and robotic assistive devices.[98] Prior RCTs have shown the efficacy of a multidisciplinary rehabilitation strategy in improving motor symptoms, balance dyskinesias, and sleep quality among PD patients.[99],[100],[101] In a prospective, single-center, single-blinded RCT with 250 participants and employment of MIRT resulted in significant improvement in PDQ39 scores among PD patients.[98] Similarly, a prospective cohort pilot study found that MIRT was associated with significant improvements in UPDRS III scores, balance, posture, and walking ability among PD patients at discharge with benefits persisting up to 3 months.[102]
Effect of Rehabilitation Strategies on Atypical Parkinsonism There is scanty literature on the role of rehabilitation strategies in atypical parkinsonian syndromes. Most of the studies on the role of exercise in progressive supranuclear palsy (PSP) have been small. In a RCT including 24 PSP patients, MIRT along with a robotic gait orthosis (Lokomat) was compared to MIRT with a treadmill-plus program. Both the Lokomat-MIRT group and the MIRT group resulted in significant improvement in the total PSP rating scale (PSPRS), PSPRS-gait sub-score, BBS, number of falls (P < 0.003 for all in both groups), and 6MWT (P = 0.032 and P = 0.018 in MIRT-Lokomat and MIRT group, respectively).[103] Musical auditory cueing using a portable digital music player has been found to improve gait speed and variability in two out five PSP patients.[104] A dynamic antigravity postural system (SPAD) along with a vibration sound system (VISS) conducted as 3 sessions/week schedule for 2 months resulted in improvement of the PSP rating scale and PD36 QOL scale scores at the end of treatment.[105] In a systematic review of 11 studies (three RCTs, two quasi-experimental studies, one cohort study, four case studies, and one case series), various interventions such as balance exercises, treadmill training, auditory cueing, robot-assisted walking, and virtual gaming among patients with PSP were assessed. The interventions were usually applied for 4–8 weeks across various studies with session frequencies ranging from 2–5/week. The review concluded that a meta-analysis could not be performed due to a large degree of statistical heterogeneity in the studies. In addition, various exercise interventions such as strength/resistance training and aerobic activities have not been assessed.[106] Thus, larger controlled studies or prospective longitudinal studies comparing various physiotherapy modalities are still required before making definite recommendations on the beneficial effects of rehabilitation strategies in PSP.
There have been very few studies focusing on rehabilitation strategies in multiple system atrophy (MSA). Gait, balance, aerobic exercises, conventional physiotherapy, and occupational therapy may be provided to MSA patients; however, the benefit is limited.[107],[108] Thus, non-invasive stimulation has been increasingly studied for improvement in MSA. In a recent systematic review (9 studies with 3 RCTs, 2 controlled trials, 2 non-controlled trials, and 2 case reports), tDCS and rTMS were found to significantly improve motor symptoms and cerebellar activation among both MSA-p and MSA-c subtypes.[109]
Telerehabilitation for Pd in the Era of Covid-19 Multiple studies have shown the efficacy of telerehabilitation in improving gait, balance, voice/speech, and upper limb dexterity in PD.[110],[111],[112] ParkPro Train is a quasi-randomized prospective longitudinal study which has shown that physiotherapy delivered via a tablet-based approach (videos of exercises, assessments, advice, time schedules, notifications, etc.) can be an effective supportive tool for improving QOL and ensuring long-term adherence to exercise programs for 9 months after an inpatient Parkinson's complex rehabilitation treatment.[113] LVST LOUD therapy delivered via group telerehabilitation improved acoustic parameters of voice and speech among 8 PD patients with good satisfaction rates.[114] A recent trial studied the barriers to the implementation of tele-neurorehabilitation among Indian patients. The study found that shared phones, lack of good internet facilities, lack of rapport building/communication, fear of fall, and lack of confidence were major hindrances in implementing telerehabilitation programs among PD patients.[115]
Limitations and Future Considerations This narrative review brings forth current evidence regarding the role of various rehabilitation strategies in Parkinson's Disease and atypical parkinsonism. However, most of the studies have included a small number of patients. There have been multiple studies that have assessed the role of combined interventions. Thus, the effect of individual rehabilitation strategies may have been overestimated. Furthermore, most of the literature has focused on mild–moderate PD with very few studies being available on advanced stages of PD. Hence, the benefit portended by rehabilitative strategies in advanced PD is not certain. There is still dearth of literature on the role and efficacy of rehabilitation strategies in atypical parkinsonism with multiple studies having small sample sizes. There have been very few studies from India, focusing on the role of different rehabilitation strategies in PD and atypical parkinsonism. Thus, larger prospective RCTs from India and other low- and middle-income countries (LMICs) might help to shed further light on the efficacy, feasibility, challenges, and roadblocks to various rehabilitation strategies among PD patients that may be encountered in LMICs. Some exciting future prospects for rehabilitation in PD and atypical parkinsonism may be the increased use of closed loop brain–machine–body interfaces,[116] virtual reality-based exercise strategies,[117] sensor-based videogaming strategies (e.g., leap motion controllers),[118] wearable sensor technology (Opal, SENSE-PARK, GAITrite, Dynaport Minimod Hybrid, and Stepwatch 3),[119] robotic-based technologies (especially as gait prosthesis),[120],[121] and home-based telerehabilitation programs.
Conclusions and Author's Opinion There is robust evidence of benefit in both motor as well as non-motor symptoms for certain rehabilitation strategies such as conventional physiotherapy, aerobic exercises, resistance training, treadmill training, balance exercises, cueing-based strategies, and SPL therapy in mild-to-moderate PD patients. Thus, these strategies may routinely form a part of exercise programs for PD patients. However, the efficacy of rehabilitation in advanced PD and atypical parkinsonism is difficult to ascertain as prior studies have included only a small number of such patients. Furthermore, very few studies have investigated the beneficial role of rehabilitation strategies in atypical parkinsonism, albeit with encouraging results. There are very few studies focusing on different rehabilitation strategies among PD patients from India and other LMICs. This may partly be due to the overall lack of emphasis on rehabilitation in busy settings and may be an area of further improvement and research. To conclude, incorporation of rehabilitation strategies, particularly early in the disease course, may improve motor as well as non-motor symptoms along with the QOL in PD patients. In addition, these strategies may be the only feasible options that can be offered to atypical parkinsonism syndromes.
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