Teleyoga for Patients With Alzheimer’s Disease and Chronic Musculoskeletal Pain and Their Caregivers: A Feasibility Study

Abstract

Background

Chronic musculoskeletal pain is common in patients with Alzheimer’s disease (AD), and there is growing awareness that chronic pain has an impact on the progression of dementia. Yoga has shown promise in treating chronic pain. However, attending in-person yoga can be difficult for AD patients.

Objective

To assess the feasibility, acceptability and preliminary efficacy of an online yoga (teleyoga) protocol suitable for AD patients with chronic pain, and their caregivers.

Methods

Patients with comorbid mild AD and chronic musculoskeletal pain (n = 15, 57-95 y/o; 73% Female) and their caregivers (n = 15, 50-75 y/o; 67% Female) received 12-week of teleyoga individually (n = 5 dyads) or in groups (n = 10 dyads). Study measures included standard feasibility metrics, and secondary outcomes included the Brief Pain Inventory-Short Form (BPI-SF), Beck Depression Inventory-II (BDI-II), and cognitive function using the Cambridge Neuropsychological Test Automated Battery (CANTAB). Caregivers also completed measures of caregiver burden, and quality of life (Short Form Health Survey-36, SF-36).

Results

Feasibility measures showed adequate treatment adherence (85.1% in patients and 86.3% in caregivers), acceptability (mean acceptability rating = 3.0 for patients and 3.3 for caregivers, indicating positive approval), recruitment rate (n = 16 dyads within 1-year), retention rate (87%), missing data rate (.03%), and fidelity of treatment delivery (87%). Preliminary efficacy findings in the AD group showed significant reductions in pain severity (BPI-SF mean Δ = −.93, P = .045) and depression (BDI-II; mean Δ = −9.85, P = .005). %). Preliminary efficacy findings in the caregiver group showed significant reductions in depression (BDI-II mean Δ = −6.88, P = .036) and fatigue (SF-36 mean Δ = 9.81, P = .021).

Conclusion

Results show that teleyoga is a feasible treatment for patients with comorbid mild AD and chronic musculoskeletal pain. Results also provide preliminary evidence of health benefits of teleyoga for both AD patients and their caregivers.

Keywords

teleyoga Alzheimer’s disease chronic pain dementia yoga feasibility study

Introduction

The largest risk factor for Alzheimer’s disease (AD) is advanced age¹ and the prevalence of chronic musculoskeletal pain is associated with increasing age.^2-4 Almost half of AD patients report chronic musculoskeletal pain as a presenting concern.⁵ Pharmacological management of chronic pain includes opioids, which can be ineffective and dangerous when given long-term; and other pharmacological approaches such as NSAIDs, gabapentin, and muscle relaxants have been associated with an increased risk for adverse events in older adults.⁶ Consequently, there is a strong interest in non-pharmacological treatments for chronic pain. For example, based on moderate-quality evidence, the 2017 American College of Medicine Guidelines strongly recommends nonpharmacologic interventions as first-line treatments for low-back pain.⁷

Among non-pharmacological treatments, yoga has emerged as a popular and effective treatment for chronic pain.^8,9 A review of systematic reviews found that chronic pain was one of only three conditions that clearly benefitted from yoga in non-AD populations (anxiety and depression also benefited).¹⁰ The authors concluded that yoga had a consistently positive effect on pain, with a moderate effect size for acute pain that was slightly lower for fibromyalgia-like pain. Although these studies did not explicitly address AD-related pain, they suggest that yoga could also be effective for treating chronic pain in AD.

In addition to chronic pain and cognitive decline, AD patients often have comorbid sleep disorders, functional impairment, and depression.¹¹ Yoga has shown clear benefits for treating a range of disorders in non-AD populations, including reductions in anxiety¹² depression,¹³ and improvements in sleep.¹⁴ Of particular relevance is the finding that yoga-related improvements in sleep and mood may partially explain its beneficial effects on cognition in patients with mild cognitive impairment.¹⁵ Although promising, to date, there is only one study on the effects of yoga for comorbid dementia and chronic pain.¹⁶ This feasibility study met a priori defined feasibility metrics, retention (70%) and adherence (87.5%), and found no adverse events related to the intervention. It should be noted that chronic pain was not the focus of that study, and pain was not an inclusionary criterion.

The COVID-19 pandemic had devastating consequences on the AD population with high rates of morbidity, mortality, and isolation-related mental health conditions.¹⁷ However, the recent rapid adoption of telehealth platforms by health care has increased access to complementary and integrative health services.¹⁸ Decreased physical mobility in AD patients,^19,20 coupled with travel and time demands of in-person yoga and COVID-19 concerns, makes teleyoga an attractive solution to solving the problem of inadequate access to health care services.²¹ Thus, further studies are needed to assess the feasibility of at-home teleyoga for AD patients.¹⁶

We conducted a study to test the feasibility of teleyoga for patients with comorbid mild AD and chronic musculoskeletal pain. The primary aim of this study was to test the feasibility of teleyoga for patients with comorbid mild AD and chronic musculoskeletal pain. The secondary aim was to test the preliminary efficacy of the intervention on pain, cognition, mood, sleep, and quality of life. We included caregivers in the treatment protocol because this population is known to experience elevated levels of depression and anxiety^22,23 which may benefit from yoga.^24-26 Indeed, the suggestion has been made that physical therapeutic recreation programs for dementia patients should be designed to serve both the patient and their caregiver.²⁷ The practice of yoga could help reduce caregiver depression and anxiety and help guide and motivate AD patients to practice during non-class days. Online delivery of yoga for patients with AD and their caregivers has not been studied before; therefore, we sought to determine whether group delivery of 10 participants per group was feasible, as this allowed the maximum number of participants to be virtually monitored by the yoga instructor.²⁸

Methods

Participants

Participants with chronic musculoskeletal pain and a diagnosis of probable Alzheimer’s disease, and their caregivers, were recruited via the Alzheimer’s Prevention Registry, which disbursed email and Facebook advertisements to members of the registry online, and via provider referrals from the Stanford/VA Alzheimer’s Center. Inclusion criteria for AD patients were (a) a diagnosis of probable Alzheimer’s disease, (b) baseline Telephone Mini-Mental State Examination (TMMSE) score 18-25 (indicative of mild dementia²⁹), (c) ≥ 18 years old, (d) a caregiver who was willing to enroll in the study and participate in the teleyoga classes, (e) a chronic musculoskeletal pain diagnosis during the last 6 months, (f) a pain intensity rating ≥4 on a 0-10 Likert-type scale, (g) not begun new pain treatments or medications in the past month, (h) if on a psychotropic medication regimen: stable regimen for at least 4 weeks prior to entry to the study and willingness to remain on a stable regimen during the 12-week acute treatment phase, (i) English literacy, and (j) wireless internet connection. Exclusion criteria for AD patients were (a) participation in another concurrent clinical trial, (b) back surgery within the last 12 months, (c) back pain potentially attributed to a specific underlying cause, disease, or condition, and (d) a baseline pain intensity rating <4 or ≥9 on a 0-10 Likert-type scale, (e) an unstable, serious coexisting medical illness, (f) an unstable, serious coexisting mental illness or psychiatric conditions, (g) attended a yoga class or practiced yoga more than once during the preceding 12 months, and (h) active current suicidal intent or plan. Inclusion criteria for the caregivers were (a) caring for a patient diagnosed with AD and (b) willingness to practice teleyoga alongside the patient. Exclusion criteria for the caregivers were (a) participation in another concurrent clinical trial, (b) back surgery within the last 12 months, (c) back pain potentially attributed to a specific underlying cause, disease, or condition, (d) an unstable, serious coexisting medical illness, (e) an unstable, serious coexisting mental illness or psychiatric conditions, (f) attended a yoga class or practiced yoga more than once during the preceding 12 months, and (g) active current suicidal intent or plan.

The intervention was advertised as an online intervention, and at-home Wi-Fi was an inclusion criterion, which possibly increased the likelihood of recruiting technologically proficient participants. However, anticipating technological difficulties, we provided participants with instructional YouTube videos on how to set up the iPad and connect to the Zoom platform. Additionally, we individually treated the first 5 patient/caregiver dyads to better address any technological challenges that arose.

A total of 16 dyads were enrolled in the study, and 15 dyads (n = 15 AD patients, n = 15 caregivers) received the teleyoga treatment. (Figure 1). All participants provided verbal informed consent. Demographic characteristics for patients and caregivers are shown in Table 1. Participants were between 50-95 years of age, were predominantly female Caucasian, and had at least a high school diploma or equivalent level of education (Table 1).

Figure 1.

Consolidated standards of reporting trials (CONSORT) flow diagram. Note. TMMSE, telephone mini-mental state examination; DVPRS, defense and veterans pain rating scale.

Table 1.

Demographic Characteristics of AD Patients and Their Caregivers.

Sample	Characteristic	Range	% or Mean	SD
AD patients (n = 15)
	Female		77.0%
	White		87.0%
	Hispanic or Latino		7.0%
	Age (years)	57-95	73.33	9.79
	Education (years)	12-22	16.14	2.77
	TMMSE	18-25	22.5	2.29
Caregivers (n = 15)
	Female		71.0%
	White		73.0%
	Hispanic or Latino		7.0%
	Age (years)	50-75	63.86	9.31
	Education (years)	12-18	16.13	2.20

Procedure

We developed a 12-week synchronous (i.e., real-time via Zoom) at-home teleyoga protocol for treating chronic musculoskeletal pain in AD patients, and their caregivers through a process of continuous modification. We started with an existing teleyoga protocol for treating veterans with musculoskeletal pain that had been developed for another study²⁸ and modified it for use in the current study. The prior protocol was developed for participants with a range of mobility, including those who were wheelchair-bound. For this population, we added a Kirtan Kriya meditation,³⁰ joint mobility sequences based on teachings from the Bihar school of yoga,³¹ seated self-massage, strength building, and contralateral movements. In modifying the yoga protocol for this population, we considered the possibility that we might encounter reduced mobility or a need to maintain mobility. Thus, we incorporated yoga tools that could be performed by all participants regardless of mobility constraints. Joint mobility and self-massage were two tools we expected to be accessible and beneficial for all participants. In light of a pilot study that showed improved cognition in self-reported memory, we used the Kirtan Kriya meditation as a non-movement yoga practice.²⁹ Additionally, based on the participants functional capacity to stand up from the floor and to return to the floor, as well as the time necessary to move props and audio/visual equipment, yoga teachers used their discretion whether to include prone and supine postures from the original pain protocol.

The first 5 patient/caregiver dyads were treated individually and the protocol was modified during these sessions. The remaining 10 dyads were treated in groups (Figure 1). The first two cohorts were used to refine and finalize the modified protocol for utilization in cohorts three and four. All study measures were completed online and participants were provided with Apple iPads (seventh and eighth Generation), yoga mats, yoga straps, and yoga blocks, yoga blankets, a TheraBand and a pinky ball. Participants completed baseline assessments within the week before the first session and completed end-of-treatment assessments within 1 week after completing session 12. For tests of cognition (TMMSE and CANTAB), caregivers were explicitly asked not to help participants with AD in completing the tasks. For other self-report measures, caregivers were not instructed either way with regard to assistance in completing the measures. Some participants had difficulty managing the iPad and used their own computers with web cameras. A HIPAA-compliant version of Zoom was used for treatment sessions. Participants were asked to open an email sent by the study coordinator and click on a Zoom link to join the weekly sessions. In the group yoga classes, privacy was not kept, and this was made clear to participants during consent. Participants kept their cameras and microphones on during sessions but the yoga instructor’s image was shown in full-screen during the class, and participants’ videos were shown in “gallery” view. Participants were not able to see each other during the yoga session, but before and during class the teacher was not shown in full-screen and participants could see each other and talk. Yoga teachers improved participant visibility by using a short throw, high lumen projector (ViewSonic Inc., DLP Projector, PS600X) to create a near life-sized image of the class, a webcam (Logitech Inc., BCC950 Conference Cam) with remote controlled zoom and positioning features, and an omni-directional desktop microphone system (Emeet Inc., Luna wireless), which provided optimal sound quality. For participants, we used an iPad stand to be adaptable to the position of the yoga postures (seated, standing, supine) to ensure that participants could always be seen. We also developed solutions to communication problems. For example, participants with poor vision were mailed a tablet with a larger screen (ChromeBook, 17” screen), and those with impaired hearing used Bluetooth speakers (Oontz Agile Speaker). Before starting the yoga treatment, all participants provided their location and two third-party emergency contacts to be used in case of an emergency. Safety was monitored by a second yoga instructor and an RA who were available to initiate an emergency response, if necessary; however, an emergency response was never needed.

The study was conducted between February 2021 and January 2022 and was approved by the Stanford University Institutional Review Board. The primary outcome measures were treatment adherence, treatment satisfaction, recruitment rate, and retention rate. The secondary outcome measures were cognitive function (AD patients only), depression (AD patients and caregivers), pain (AD patients only), sleep quality (AD patients and caregivers), caregiver burden (caregivers only), and health-related quality of life (caregivers only).

Yoga Intervention

The study protocol was developed by a certified yoga therapist (LM), and study yoga instructors (KF, AK, KP-B, HM). All study instructors were Registered Yoga teachers with at least 200 hours of training. The 12-week protocol consisted of one session per week for 75 minutes, and completing 15-20 minutes of daily homework on 5 non-class days (see Appendix 1 for protocol details). Classes incorporated seated warm-up with joint mobility and self-massage, standing, prone and supine yoga postures as well as yoga breathing, hand gestures, vocalization (humming and Kirtan Kriya), and meditation practices. Therabands and pinky balls were incorporated into the practice to aid with joint mobility and strength. One example of contralateral and counting movement included an 8-count “choreographed” stretch where one arm stretched up as the opposite foot pressed down into the floor – alternating sides before bringing both arms back down together. Quotes and poetry were incorporated into the meditative practices chosen to enhance a theme. If participants missed a session, they were not offered a make-up session in another cohort. Homework materials were provided as printed instructions and online videos created for the project. Homework practice was monitored with a participant daily practice log, where participants logged their total daily practice time in minutes (average weekly practice time = 76 minutes, average weekly practice days = 3.7).

Measures

Primary (Feasibility) Outcomes

Treatment Adherence

We operationalized treatment adherence as the total number of classes attended during the 12-week intervention, as assessed by weekly attendance logs. We used a benchmark adherence rate of ≥65% (i.e., attending at least 8 of the 12 sessions) for adequate feasibility. This rate is based on previous full-scale RCTs of yoga for cLBP, which used the same yoga dose as in the present study,^32,33 reported 60%-67% adherence based on class attendance.

Treatment Satisfaction

Satisfaction of treatment was measured using the Multi-Dimensional Treatment Satisfaction Measure (MDTSM),³⁴ which is composed of 33 questions that assess treatment process and outcome attributes. Each of the 33 questions was scored on a zero to 4 Likert rating scale with a score of zero indicating “not at all satisfied” and a score of 4 indicating “very satisfied”. For each participant the mean score across all 33 ratings was calculated, which produced a MDTSM score ranging from zero (not at all satisfied) to 4 (very satisfied). For the assessment of feasibility, we set the group mean target score on the MDTSM to ≥2, representing neutral or positive satisfaction.

Recruitment Rate

We set recruitment rate as the ability to recruit n = 15 dyads into the study within the 1-year project timeline.

Retention Rate

Retention rate was operationalized as the percentage of consented participants who remained in the study at end-of-treatment. We used a benchmark retention rate of ≥65% for adequate feasibility. Larger studies involving yoga treatment for veterans with chronic musculoskeletal pain have typically reported retention rates of approximately 60%-74% by the end of treatment.^35-37

Treatment Fidelity

Video recordings of the yoga teachers were made for all yoga sessions. As the yoga protocol was modified across cohorts 1 and 2 (Figure 1), we only measured treatment fidelity in cohorts 3 and 4. Accordingly, a certified yoga instructor (who was not the teacher) scored a randomly selected session from weeks 1-4, weeks 5-8, and weeks 9-12 from cohort 3 and cohort 4, representing 25% of the treatment sessions of these cohorts. We used a binary yes/no checklist to rate instructor adherence to each yoga component in the protocol. We set an a priori benchmark for minimum competency at ≥95% of treatment components.³⁸

Missing Data Rate

We calculated the aggregated missing data rate across all items at both timepoints for all participants. We used a benchmark missing data rate of ≤15% for adequate feasibility.

Adverse Events

Data Safety Monitoring Board was convened for this project who reviewed safety concerns every 6 calendar months.

Secondary Outcomes

Completed by Participants Eith AD Only

Cognitive Impairment

During the telephone screening interview for eligibility, the 26-point Telephone Mini-Mental State Examination (TMMSE) was used for the assessment of cognitive impairment.³⁹ The MMSE has been used extensively in clinical and research settings and is commonly used to screen for dementia.

Cognitive Function

Measured using Cambridge Neuropsychological Test Automated Battery (CANTAB)^40,41 (Cambridge Cognition; https://www.cambridgecognition.com) at baseline and end-of-treatment. The CANTAB is a computerized neuropsychological assessment system. It is a well-validated and widely used cognitive research software.^40-44 Tasks assessed sustained attention [Rapid Visual Information Processing (RVP)], spatial working memory [Spatial Working Memory (SWM)], and learning and visual memory [Paired Associates Learning (PAL)], with alternate versions used at the second assessment to control for practice effects.

Pain

Patient pain was measured with the Pain, Enjoyment and General Activity Scale (PEG) at screening, baseline and end-of-treatment.⁴⁵ The PEG is a 3-item self-report measure that assesses pain severity and pain interference. Patients also completed the Brief Pain Inventory-Short Form (BPI-SF) at baseline and end-of-treatment, a 9-item self-report measure that assesses pain severity and pain interference.⁴⁶ The Defense and Veterans Pain Rating Scale (DVPRS), a well-validated behaviorally anchored 10-point Likert-type scale, was used during screening to assess pain severity for inclusion.⁴⁷

Completed by Caregivers Participants Only

Caregiver Burden

Caregivers completed the Revised Memory and Behavior Problems Checklist (RMBPC) at baseline and end-of-treatment.⁴⁸ The RMBPC contains 24 caregiver-rated items that assess memory-related problems, affective distress, and disruptive behaviors of AD patients as well as the degree to which these problems cause caregiver distress. Two scores are derived from the RMBPC; frequency, which quantifies the number of times that memory and behavior problems arose during the preceding week, and reaction, which measures how much caregivers were bothered by the reported memory and behavior problems.

Quality of Life

The Short Form Health Survey-36 was given at baseline and end-of-treatment.⁴⁹ The SF-36 consists of eight scales that assess physical functioning, role limitations due to physical problems, role limitations due to emotional problems, energy/fatigue, emotional wellbeing, social functioning, pain, general health, and health change.

Completed by Patients and Caregivers

Depression

Depression was measured at baseline and end-of-treatment using the Beck Depression Inventory (BDI-II), a 21-item self-report questionnaire.⁵⁰

Sleep Quality

Sleep quality for both patients and caregivers was measured at baseline and end-of-treatment using the Pittsburg Sleep Quality Index (PSQI).⁵¹ This 19-item self-report questionnaire assesses sleep quality, sleep duration, sleep latency, sleep efficiency, sleep disturbances, use of sleep medication, and difficulties with activities of daily living during the preceding month.

Data Analysis

Due to the small sample size (n = 15 patients, n = 15 caregivers), we used descriptive statistics to evaluate treatment adherence (≥65%), treatment satisfaction (mean ≥2 indicating neutral or positive satisfaction), recruitment rate, retention rate (≥65%), missing data rate (≤15%), and treatment fidelity. For depression, pain, sleep quality, caregiver burden, and quality of life, we estimated changes over time with Wilcoxon rank-sum tests. For cognitive function, we estimated changes over time with linear mixed models.⁵² Given the small sample size and the auxiliary status of the secondary outcome measures in this feasibility study, we aggregated data from secondary outcome measures to improve statistical power.

We estimated results for secondary outcomes separately for patients and caregivers. Accordingly, in terms of secondary outcomes for AD patients, we estimated changes over time in cognitive function (CANTAB, Paired Associates Learning; Rapid Visual Information Processing; Spatial Working Memory), depression (BDI-II), pain (PEG, BPI-SF), and sleep quality (PSQI). For caregiver secondary outcomes, we estimated changes over time in caregiver burden (RMBPC), quality of life (SF-36), depression (BDI-II), and sleep quality (PSQI).

Results

Primary Outcomes

Table 2 shows descriptive statistics of feasibility measures for both patients and their caregivers. With regard to treatment adherence (% attendance), we achieved an average of 85.1% for AD patients and 86.3% for caregivers, both exceeding our goal of 65% attendance. In terms of treatment satisfaction, the mean score was 3.0 for the AD patients and 3.3 for caregivers, indicating a generally positive satisfaction with the intervention. We also achieved our recruitment goal, as indicated by our ability to recruit 16 dyads into the study within the 1-year project timeline. The first participant was enrolled in February of 2021 and the last participant was enrolled in January of 2022. The retention rate at end of treatment was 87%, which exceeded our feasibility benchmark of 65% retention. The average treatment fidelity rating was 87%, which was below our 95% benchmark target for fidelity. The aggregated missing data rate was .03%. No unanticipated problems involving risks to participants or others occurred, and there was no incidence of injury.

Table 2.

Feasibility Outcomes for Patients and Caregivers.

		n	Range	Mean	SD
Patients
	Treatment adherence	15	58.3-100.0	85.12	15.75
	MDTSM	13	1.6-4.0	3.01	.69
	Retention rate	13/15		87%
Caregivers
	Treatment adherence	15	58.3-100.0	86.31	15.19
	MDTSM	13	2.3-4.0	3.30	.63
	Retention rate	13/15		87%

Note. MDTSM, multi-dimensional treatment satisfaction measure; EOT, end-of-treatment; treatment adherence is the average number of classes attended per participant.

Secondary Outcomes

Table 3 shows change in secondary outcome measures from pre-to-post treatment. We found a statistically significant reduction in depression as measured by the BDI-II in both patients and caregivers. On average, patients demonstrated a reduction of 9.85 points on the BDI-II, which is considered a clinically significant improvement in depression.^53,54 Patients also showed statistically significant and clinically significant reductions in pain severity, with clinical significance demonstrated by a reduction greater than 15% (% reduction [pain severity] = 21.85%).⁵⁵ Our analyses did not reveal any statistically significant improvements in cognitive functioning as measured by the CANTAB (Table 4).

Table 3.

Secondary Outcome Measures for AD Patients and Their Caregivers.

	Measure	Baseline			EOT			Change (EOT - Baseline)
	Measure	n	Mean	SD	n	Mean	SD	Mean	Cohen’s d	P-value*
Patients	BDI-II	15	18.40	9.96	13	9.15	7.94	−9.85	−1.14	.005**
	PSQI	15	7.53	4.19	13	6.92	4.13	−.85	−.22	.653
	BPI pain severity	15	4.21	1.89	13	3.29	1.83	−.93	−.59	.045*
	BPI pain interference	15	4.11	2.22	13	2.92	2.52	−1.10	−.40	.116
	PEG average	15	5.00	2.26	13	3.56	2.36	−1.23	−.51	.100
Caregivers	BDI-II	15	12.80	14.31	13	5.92	6.36	−6.88	−.65	.036*
	PSQI	15	7.40	3.72	13	6.38	3.04	−1.02	−.33	.264
	SF-36 physical functioning	15	60.33	33.03	13	68.08	29.12	7.74	.42	.205
	SF-36 physical limitations	15	61.67	39.94	13	67.31	43.76	5.64	.14	.763
	SF-36 emotional limitations	15	80.00	32.90	13	74.31	41.23	−5.69	−.06	.785
	SF-36 energy/fatigue	15	47.73	17.75	13	57.54	15.48	9.81	.79	.021*
	SF-36 emotional wellbeing	15	73.40	16.08	13	74.15	16.22	.75	.20	.440
	SF-36 social functioning	15	76.80	28.16	13	74.15	32.08	−2.65	−.18	.667
	SF-36 pain	15	62.13	22.71	13	65.31	19.41	3.17	.23	.310
	SF-36 general health	15	58.67	16.74	13	59.62	16.52	.95	.11	.589
	SF-36 health change	15	59.93	24.74	15	46.67	31.15	−13.27	−.45	.119
	RMBPC frequency	15	6.93	6.01	15	5.20	5.39	−1.73	−.33	.116
	RMBPC reaction	12	13.00	13.34	10	12.30	16.06	−.70	−.12	.102

Note. EOT, end-of-treatment; BDI-II, beck depression inventory; PSQI, Pittsburg sleep quality index; BPI, brief pain inventory-short form; PEG, pain enjoyment and general activity scale; SF-36, short form health survey-36; RMBPC, revised memory and behavior problems checklist; Approximate P-values based on nonparametric Wilcoxon signed rank test; *P < .05, **P < .01, ***P < .001.

Table 4.

Cognitive Function Outcome Measures for AD Patients in the CANTAB Tests of Neuropsychological Function.

Measure	Baseline Mean	End-of-Treatment Mean	Mean Difference	P-value*
Paired associates learning total error	28.00	18.50	−9.50	.059
Rapid visual information processing false alarms	12.50	2.88	−9.62	.102
Rapid visual information processing mean latency	657.11	552.32	−104.79	.181
Spatial working memory between errors	18.50	21.00	2.50	.722
Spatial working memory strategy	9.25	10.38	1.12	.127

Note. Higher scores on all 5 measures indicate worse performance; *P < .05, **P < .01, ***P < .001.

Discussion

The primary aims of this study were to develop an online yoga protocol for patients with comorbid mild AD and chronic musculoskeletal pain, and their caregivers, and to evaluate its feasibility. Using an iterative approach, we modified an existing teleyoga protocol for chronic musculoskeletal pain for non-AD patients. Our results demonstrated adequate feasibility in terms of treatment adherence, satisfaction, retention, recruitment rate, and missing data. However, the treatment fidelity rating of 87%, was below our goal of ≥95%. We based the fidelity rating benchmark on results from a previous study with younger participants and the difference in fidelity may be explained by the yoga teachers’ choice not to offer the prone and/or supine poses. This decision was based on their judgment that doing so would be costly with regard to class time (e.g., the need to adjust the camera and the time to get down to the floor) and would disrupt the flow of class. Prone and supine poses were kept in the protocol as an option for current and future studies. Although not powered to show efficacy, the study secondary outcomes demonstrated a statistically significant reduction in depression among AD patients and caregivers. In addition, AD patients showed a statistically significant reduction in pain severity, and caregivers showed a statistically significant reduction in fatigue.

Although a number of studies have evaluated the effects of yoga on symptoms of AD,¹⁵ to our knowledge this is the first study to assess the feasibility of teleyoga as a treatment for pain in patients with comorbid AD and chronic pain. Moreover, to our knowledge this is the first AD teleyoga study to include caregivers directly into the protocol and to examine the effects of the intervention on caregiver distress. To date, only one prior study included caregivers into the teleyoga protocol but did not report the impact of the intervention on measures of caregiver distress.¹⁶

The physical vulnerabilities of the AD population during the COVID-19 pandemic made it extremely difficult for AD patients to socialize, and resulted in increased levels of isolation and depression.^56,57 Anecdotally, we noted that caregivers enjoyed the yoga sessions with their partners and some reported better relationships with their spouse. Retrospectively, yoga instructors anecdotally reported that visual demonstration of yoga poses was more effective than verbal instruction, possibly due to hearing loss. Yoga instructors also reported that participants expressed gratitude for the treatment and were eager to join sessions, as indicated by frequently logging into the platform 15 minutes prior to the start of the session. One of the participants wrote a poem about their experience with the intervention and reflected on their feelings of loosening, releasing, letting go, and spiritual emergence (Appendix 2). None of the participants reported technological barriers. These results demonstrate that our teleyoga protocol is safe, feasible, and was positively received by patients and caregivers. This suggests that our protocol has the potential to treat comorbid AD and chronic pain.

Our findings are consistent with previous studies on yoga in AD patients that have shown improvements in cognitive function,^58-61 mood,⁶² quality of life,⁵⁸ and physical health.⁶² Our results revealed significant pre-to post-treatment reductions in pain among patients, providing preliminary support for teleyoga as a treatment for chronic musculoskeletal pain in AD. While promising, future studies with larger sample sizes are needed to evaluate the efficacy of the teleyoga protocol in AD patients and caregivers. Teleyoga is an accessible nonpharmacological approach for pain management, and has the potential to supplant high-risk pharmacological pain management approaches in AD patients.

A small but growing body of literature has established a possible link between chronic musculoskeletal pain and dementia,^63-65 with chronic pain-related hippocampal atrophy possibly driving this association.⁶⁶ Prior studies have demonstrated improvements in cognitive functioning in older adults with mild cognitive impairment¹⁵ following yoga. Our findings indicate that yoga may help to minimize the association between chronic pain and dementia possibly by decreasing pain-related atrophy in the hippocampus. However, further studies are needed to address the association between chronic pain, hippocampal atrophy, and cognition in this population.

Strengths of our study include the inclusion of caregivers into the experimental design, the development of a protocol suitable for AD populations, and the fully online methods which expand the reach of the intervention. Weaknesses include a small sample size and the lack of a control group. The generalizability of our results are also weakened by a predominantly White and female sample. Future fully-powered randomized controlled trials are needed to draw more definitive conclusions about the generalizability of the findings reported here.

Footnotes

Acknowledgments

The authors would like to thank members of the Data Safety and Monitoring Board (Dr Erik Groessl, Dr Jane Pak, and Dr Margaret Chesney), as well as Dr Steven Z. Chao, Dr Jauhtai Cheng, and Pauline Lu from the Alzheimer’s Stanford/VA Center for assistance with recruitment.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the National Center for Complementary and Integrative Health (NCCIH; NCT04512040, Peter J. Bayley, PhD, Principal Investigator).

Trial Registration

ClinicalTrials.gov NCT04512040.

ORCID iD

Santiago Allende

Appendix 1

Details of the yoga protocol that was given to participants with mild Alzheimer’s disease and their caregivers

Target	Yoga Tool	Weekly Class Themes
Breath and sensation awareness	Natural breath, body scan, pelvic and thoracic diaphragm breathing	1. Breath
Balancing, calming, activating breath practices	Even (Sama Vritti), cooling (Sheetkari), alternate nostril (Nadi shodhana), ocean (Ujayii), lion’s (Simha), humming (Brahmari), skull shining (Kapalabhati), Breath of Joy, soft Belly breath	2. Self compassion and self love
Posture and alignment	Seated or standing mountain (Tadasana)	3. Starting where you are
Joint mobility	Jelly ball rolling (hands and feet), hand rubbing, joint lubrication series adapted from the Bihar school, shoulder mobility with strap	4. Start small and move slowly - with comfort
Cognition	Kirtan Kriya, contralateral movement, skull shining breath (Kapalabhati), counting with movement, root chakra bind (Mula Bandha)	5. Linking movement with breath
Musculoskeletal strength, balance and flexibility, posture, alignment, moving with the pace of the breath	Warrior (Virabhadrasana) I & II, 5 pointed start (Utthita Tadasana), chair (Utkatasana), horse (Vatayanasana), upward salute (Urdhva Hastasana) with lateral bend, wide leg forward fold (Prasarita Padottanasana), pyramid (Parvostanasana), tree (Vrikshasana), Heel rise in mountain balance, modified reclining bound angle (Supta Padangusthasana), figure 4 stretch (Ardha Matsyendrasana), side plank (Vasisthasana), modified locust (Salabhasana), child’s pose (Balasana), Bent Knee/Tabletop internal oblique strengthen, modified, bridge (Setu Bandha Sarvangasana)	6. Focus on the positive – what is going right for us in this moment
Calming	Crocodile (Makarasana), bent knee spinal twist (Jathara Parivartanasana), legs up the wall (on a chair) (Viparita Karani), corpse (Savasana)	7. Notice how pain has become familiar - like a protective shell - but you don’t need it, let it go
Hand gestures	Prayer (Anjali), sun (Surya), water (Varun), deer (Mrigi) Mudras	8. Focus on slow breath - in and out - throughout the yoga practice
		9. Have fun, laugh at yourself and your teacher - love who you are right now
		10. Breath and movement as one
		11. Yoga is the ability to direct attention to a chosen object without wavering - yoga sutra 1.2 - reemphasize living with compassion towards yourself and others
		12. Review how to bring what we’ve learned in class into daily living and options for yoga in the community

Yoga Online

Out of the tiny screen

Sprays an invisible shower

Of photons and soundwaves

Across the room where we wait.

It’s our wonderful weekly workout.

Something so good for ourselves.

As the shower washes over our bodies,

And into our eyes and ears.

We move with their flow,

Into asanas and positions.

Bending and folding,

Stretching and twisting.

All loosened up and released,

From the tightness and aches,

Both physical and spiritual,

Some carried for years.

In our arms and legs,

Backs, necks, and joints,

Brain, nerves, and soul,

But now shaken loose.

This done by a soft gentle voice,

Spoken from miles far away,

Teaching us how to let go of this,

Pain we’ve carried much too long.

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