Effect of Equine-Assisted Activities on Cardiac Autonomic Function in Children with Cerebral Palsy: A Pilot Randomized-Controlled Trial

Abstract

Objective:

Children with cerebral palsy (CP) have an impaired cardiac autonomic function. Attenuated heart rate recovery (HRR), which is a valuable prognostic parameter for autonomic nervous system, is known to be associated with an increased risk of cardiovascular events and all-cause mortality. However, only few studies have observed the effects of exercise on the cardiac autonomic function in children with CP. The purpose of this pilot study was to examine the effects of equine-assisted activity (EAA) program on cardiac autonomic function in children with CP.

Design:

A single-blinded, parallel, two-arm pilot trial with 1:1 randomization to the EAA or control group.

Setting:

A tertiary university hospital and a local arena.

Subjects:

Twenty-six children with CP (Gross Motor Function Classification System Levels I–II).

Intervention:

Each lesson of the EAA program for the EAA group was conducted for 40 min twice a week, and the whole program duration was 16 weeks (a total of 32 sessions).

Outcome measures:

A graded exercise test was performed to measure the resting heart rate (RHR), HRR, and peak oxygen uptake (VO_2peak) on both groups before and after the 16-week period.

Results:

The autonomic nervous function measured by the response of HRR improved at 1 min (p < 0.009), 3 min (p < 0.001), and 5 min (p < 0.004) only in the EAA group. RHR significantly improved in the EAA group (p < 0.013), whereas the VO_2peak did not significantly differ between the two groups.

Conclusion:

The HRR and RHR of the children with CP improved after completing the 16-week EAA program. The results demonstrated that the program had a positive effect on the improvement of cardiac autonomic function in these patients.

Clinical Trial Registration Number: NCT03870893

Introduction

Cerebral palsy (CP) is a permanent disorder that causes nonprogressive damage to the developing fetal or infant brain, clinically resulting in limitations in movement and posture, and a decrease in physical activity. Disturbances in sensation, perception, cognition, communication, and behavior often occur with the motor disorders of CP.¹ It has been reported that adults with CP have a higher prevalence of many chronic conditions, including diabetes, asthma, hypertension, heart diseases, and stroke, than adults without CP.²

Movement and posture problems may lead to impairments in physical activity levels and physical fitness in patients with CP.³ Over the past three decades, cardiorespiratory fitness (CRF) has been considered a strong, independent predictor of all-cause mortality. Kodama et al. recently reported that better CRF was associated with a lower risk of all-cause mortality and cardiovascular events in healthy men and women.⁴ The peak oxygen uptake (VO_2peak) attained during a graded exercise test is considered the single best indicator of aerobic physical fitness.⁵ Furthermore, children with CP (aged 7–17 years) have been reported to have a 15%–28% lower maximum oxygen uptake than the normal children.⁶ There is a trend that children with CP have an impaired cardiac autonomic function,^7,8 and it may also be associated with the low CRF.^9,10

A recent meta-analysis found that children with CP showed significantly lower mean values in heart rate variability (HRV) parameters than the typically developed (TD) controls aged 1.5–18 years.⁷ Kholod et al. suggested that children with CP had a lesser efficient cardiac autonomic mechanism at rest and a lesser adaptive ability to exercise and activity than the TD children.⁸ The heart rate recovery (HRR) is known as an important predictor used to evaluate the function of the cardiac autonomic nervous system after exercise and to identify changes in training status.¹¹ Delayed HRR is known to be associated with increased cardiovascular events, sudden cardiac death, and overall mortality.^12,13 Furthermore, there is a strong evidence indicating the positive effects of exercise training on the cardiac autonomic function in patients with heart failure, established heart disease, chronic obstructive pulmonary disease, and type 2 diabetes, among others.^14

–17

The equine-assisted activity (EAA) is among the intervention methods used to improve the motor function in patients with CP. The EAA has a positive effect on the improvement of gross motor function, muscle asymmetry, posture, balance, and gait in children with CP.^18
–20 To date, EAA studies in children with CP have focused primarily on improving the motor function. To the best of knowledge, only two studies^21,22 have reported the effects of the EAA on cardiac autonomic function in medical literature. Cabiddu et al.²¹ reported that a single (15-min) session of hippotherapy could elicit an acute autonomic response during the recovery period in children with neurologic disorders aged 4–12 years. Nqwena and Naido²² reported that six sessions of therapeutic horseback riding demonstrated a change in HRV, showing significant increases in the interbeat (R-R) intervals average value (ms) before the therapeutic horseback riding over six sessions, in children with disabilities including autism spectrum disorder, CP, Down syndrome, spina bifida, and developmental delay (n = 29, mean age: 8.69 years). Further well-controlled trials are proposed to prove the effects of EAA on cardiac autonomic function, which is associated with cardiac morbidity and mortality in patients with CP.

Therefore, the purpose of this study was to evaluate the effects of a 16-week EAA program (40 min per lesson twice a week, totaling to 32 lessons) on HRR and cardiopulmonary fitness in children with CP.

Materials and Methods

Study design

The Institutional Review Board of the Samsung Medical Center (Seoul, Republic of Korea) approved this study protocol. Written informed consent was provided by the participants as well as parents or guardians before enrollment. The enrollment of participants began on August 1, 2017, and the data collection stopped on January 21, 2019. Children suitable for this study were identified using the institution's database. In the case of children whose parents agreed to participate in the study by telephone contact, screening was conducted by the primary investigator. All participants were evaluated before and after the EAA program by one pediatric physiatrist who has an experience in conducting EAA. Furthermore, the medical records of all patients were reviewed by the same physiatrist.

Participants

Inclusion criteria were (1) diagnosis of CP, (2) classified at Gross Motor Function Classification System (GMFCS) level I or II, (3) aged 6 and 12 years, and (4) body weight under 35 kg. Exclusion criteria were (1) injected a botulinum toxin within 3 months, (2) a selective dorsal rhizotomy or orthopedic surgery within 1 year, (3) poor visual acuity, (4) hearing impairment, (5) severe intellectual disability, (6) uncontrolled seizures, (7) hip dislocation, (8) scoliosis Cobb angle >30 degrees, and (9) unhealed fracture. The study and intervention protocols were drafted according to the Consolidated Standards of Reporting Trials (CONSORT) guidelines for randomized pilot and feasibility studies. After all of the inclusion and exclusion criteria were accounted for, the final study sample consisted of 26 patients; declined to participate (n = 1). Thus, 26 children were randomly assigned to two groups (EAA, n = 13; control, n = 13) (Fig. 1). The control group did not receive the intervention and continued their usual daily activities. The clinical characteristics of the children included in the analysis are shown in Table 1.

FIG. 1.

CONSORT study flow diagram. CONSORT, Consolidated Standards of Reporting Trials.

Table 1.

Characteristics of the Participants

Group	EAA (n = 13)	Control (n = 13)	p
Group	Mean (SD)	Mean (SD)	p
Age (years)	8.15 (1.91)	7.54 (1.56)	0.387
Height (cm)	126.04 (9.45)	127.65 (10.44)	0.383
Weight (kg)	25.01 (5.94)	26.41 (5.09)	0.522
Sex (boy/girl)	6/7	8/5	0.440
GMFCS (I/II)	7/6	7/6	1.00

EAA, equine-assisted activity; GMFCS, Gross Motor Function Classification System; SD, standard deviation.

Randomization

The eligible participants were randomized into one of the two groups (EAA or control). An independent statistician performed the randomization using computer algorithm (block size was 4).

Sample size calculation

Given that there had been no report on the changes in HRR in children with CP, the authors followed Julious's suggestion of the 12 per group rule of thumb.²³

Intervention

Children allocated in the EAA group participated in the EAA program provided by the Samsung's Riding for the Disabled Program (RD-SAMSUNG) in the indoor riding arena located in Gun-po, Republic of Korea. Thirteen children participated in the EAA program for 40 min per lesson, twice a week for 16 weeks (total of 32 sessions). The sessions were conducted by three therapeutic riding instructors. One leader and two side walkers walked with a horse, and all participants wore helmets. Three participants were grouped together for each session. The EAA program sessions consisted of exercises to facilitate correct posture and balance, including lower extremity strengthening, and basic riding skills while walking and trotting. The intensity of the exercises and degree of assistance were individualized according to the participants' ability to control their body and horse. The horse/ponies had a height of 110–125-cm and weight of 250–400 kg; all animals were very experienced in the EAA settings (Table 2).

Table 2.

Equine-Assisted Activity Program

	Exercises	Supporters
Warm-up (5 min)	Stretching, breathing
Main exercise (30 min)
1–2 weeks	[Learning basic riding skills]	• One leader • Two side walkers
	• Getting up on the horse, getting off the horse
	• Rein control, transition from walk to halt
	[Balance training and walking]
	• Clapping with side walkers, raising hands over the head
	• Changing direction, making serpentines and circles
	• Balance at walk
3–6 weeks	[Balance training]	• Reduced assistance by the leader • One side walker
	• Raising hands over the head, throwing a ball
	• Changing direction, making serpentines, circles, and half circles
	[Trotting training]	• One leader • Two side walkers
	• Standing up and down with holding the rein
	• Sitting trot with holding the saddle
	• Posting trot with holding the saddle
7–10 weeks	[Balance training]	• Reduced assistance by the leader • No side walkers
	• Throwing a ball
	• Changing direction, making serpentines, circles, and half circles
	• Making figure eight
	[Trotting training]	• One leader • One side walker
	• Standing up and down with holding the rein
	• Sitting trot with holding the saddle
	• Posting trot with holding the saddle
11–16 weeks	[Balance training]	• No leader • No side walker
	• Throwing a ball
	• Changing direction, making serpentines, circles, and half circles
	• Making figure eight
	[Trotting training]	• One leader • No side walker
	• Standing up and down with holding the rein
	• Sitting trot with holding the rein
	• Posting trot with holding the rein
Cool down (5 min)	Stretching, breathing

To estimate the exercise intensity during EAA, the authors measured the heart rate (HR) once a month (3rd, 7th, 11th, and 15th week) using the HR monitors (H7; Polar Electro Oy, Kempele, Finland) connected to the accelerometers (GT3X; ActiGraph LCC, Pensacola, FL) and only in the EAA group (n = 13). The accelerometer was worn on the children's waist, and the HR monitor was worn on the chest. The data were downloaded and analyzed by using ActiLife software (version 6.13.3; ActiGraph LLC, Pensacola, FL).

Outcome measures

Resting HR and blood pressure (BP) were recorded after 5 min of resting. All patients performed a symptom-limited, treadmill exercise test using the Modified Naughton protocol (Table 3). The changes in the parameters, including HR, BP, and VO_2peak, were measured at every stage. The electrocardiogram (ECG) was also continuously monitored during the test to observe the abnormal heart rhythms. The ECG was checked by an exercise test device (Q-stress; Mortara Instrument, Inc.), and the cardiopulmonary fitness was estimated using TrueOne 2400 (Parvo Medics) to measure the VO_2peak. All children were verbally encouraged to continue the test until their exhaustion. The termination criteria for exercise testing included fatigue, leg discomfort, dyspnea, abnormal BP responses, or ischemic ECG changes. The exercise time and peak HR were recorded at a maximum exercise intensity. In the recovery period, the patients walked for 2 min at a speed of 1.9 km/h and a grade of 0% and then sat down in a chair for the last 3 min. The HRR was defined as the difference between peak HR during exercise testing and HR at 1 min (HRR1), 3 min (HRR3), and 5 min (HRR5) after exercise cessation. The authors quantified the % change in HRR at 1, 3, and 5 min after the baseline measurements between the two groups as effect sizes in this study. The % change of HRR was calculated by using the following formula:

Table 3.

The Modified Naughton Protocol

Stage (2 min/stage)	Speed (km/h)	Grade (%)
Stage 1	1.6	0
Stage 2	2.4	0
Stage 3	3.2	3.5
Stage 4	3.2	7.0
Stage 5	3.2	10.5
Stage 6	4.8	7.5
Stage 7	4.8	10.0
Stage 8	4.8	12.5
Recovery phase of 1–2 min	1.9	0
Recovery phase of 3 min	0	0
Recovery phase of 5 min	0	0

% change = [(post-pre) × 100/pre]

Statistical analysis

After certification of normality by the Shapiro–Wilks test, the independent t-tests or the Mann–Whitney U-test was performed to examine the differences between the groups. For multiple testing among the different time points of HRR, Bonferroni's correction (level = 3) was used. The p level was set at .05. Data were analyzed using SPSS for Windows, version 21.0 (SPSS, Inc., Chicago, IL). The Friedman test was used to evaluate the HR differences during EAA sessions across the study period.

Results

The baseline resting heart rate (RHR), HR peak, and HRR1, HRR3, and HRR5 were not statistically different between the EAA and control groups. Significant decreases in the RHR, HRR1, HRR3, and HRR5 were noted after the intervention in the EAA group only (Table 4). The %change in HRR1, HRR3, and HRR5 for the EAA group increased by 24.86%, 32.53%, and 19.89%, respectively, which was statistically different from those of the control group (p < 0.05).

Table 4.

Change in the Heart Rate, Exercise Time, and VO_2peak

	Group	Pre	Post	%Change	p-Value
	Group	Mean (SD)	Mean (SD)	%Change	p-Value
RHR (bpm)	EAA	87.38 (8.19)	77.31 (4.92)	−11.01	0.013^*
RHR (bpm)	Control	90.46 (16.71)	90.08 (13.07)	0.75	0.013^*
HRpeak (bpm)	EAA	165.62 (13.22)	169.23 (10.89)	2.63	0.616
HRpeak (bpm)	Control	164.23 (14.87)	165.54 (14.06)	1.1	0.616
HRR1 (bpm)	EAA	31.00 (6.54)	37.54 (5.30)	24.86	0.009^*
HRR1 (bpm)	Control	31.23 (6.80)	29.08 (8.85)	−7.46	0.009^*
HRR3 (bpm)	EAA	48.31 (10.05)	61.69 (10.26)	32.53	0.001^*
HRR3 (bpm)	Control	51.46 (14.85)	45.92 (12.89)	−10.51	0.001^*
HRR5 (bpm)	EAA	64.67 (10.00)	73.38 (12.26)	19.89	0.004^*
HRR5 (bpm)	Control	62.23 (10.78)	59.62 (9.31)	−3.88	0.004^*
Exercise time (seconds)	EAA	748.38 (108.43)	814.15 (135.35)	8.92	0.503
Exercise time (seconds)	Control	706.08 (270.94)	751.15 (293.72)	5.79	0.503
VO_2peak (mL/kg/min)	EAA	25.25 (2.69)	26.85 (2.92)	10.89	0.055
VO_2peak (mL/kg/min)	Control	26.62 (5.10)	25.72 (4.19)	−2.21	0.055

p < 0.05.

bpm, beats per minute; EAA, equine-assisted activity; HRpeak, heart rate peak; HRR1, heart rate recovery at 1 min; HRR3, heart rate recovery at 3 min; HRR5, heart rate recovery at 5 min; RHR, resting heart rate; SD, standard deviation; VO_2peak, peak oxygen uptake.

The baseline exercise time and VO_2peak were not statistically different between the two groups. Furthermore, there were no differences in the exercise time and VO_2peak between the two groups after the intervention (Table 4).

The average HRs during the EAA programs across the study period are shown in Table 5. There was no change in the HRs across the study period (p = 0.421, Friedman's test).

Table 5.

Change in the Heart Rate of the Equine-Assisted Activity Group During Riding

	3rd week	7th week	11th week	15th week
	Mean (SD)	Mean (SD)	Mean (SD)	Mean (SD)
Heart rate during riding (bpm)	100.69 (7.51)	99.37 (7.22)	98.39 (9.01)	101.80 (7.90)

bpm, beats per minute.

Discussion

To the best of knowledge, this study is the first randomized-controlled trial that evaluated the positive effect of the 16-week EAA program on cardiac autonomic function in children with CP. The RHR and HRR improved at the end of the 16-week EAA program (40 min per lesson twice a week; a total of 32 lessons) in these patients.

The cardiac autonomic nervous system can be evaluated by several methods, including measurements of HRR, HRV, and baroreflex sensitivity.^24,25 The HRR is a readily obtainable, relatively inexpensive, and very simple diagnostic and prognostic parameter that reflects the cardiac autonomic functions. It is checked up to 5 min after the graded exercise test. The HRR can be divided into two phases. The first phase is the fast phase, and the HR decreases rapidly up to the first minute, which is mainly adjusted via the parasympathetic reactivation. The second phase is defined as the slow phase, and the HR decreases relatively slowly under the influence of sympathetic withdrawal and parasympathetic reactivation.²⁶ Considering that the HRR improved at 1, 3, and 5 min in this study, the EAA program has a positive effect on both the fast and slow phases via parasympathetic reactivation and sympathetic withdrawal.

A regular aerobic exercise has been reported to have a positive effect on HRR in adults.^14

–17 Several studies also reported the effect of exercise on HRR in children.^27,28 Wilks et al.²⁷ reported an improvement in HRR at 1, 3, and 5 min by 32%, 18%, and 11%, respectively, in overweight and obese children through the inpatient lifestyle-change program. The program consisted of ∼11 h of structured and supervised moderate-intensity physical activity per week (4–6 weeks). Singh et al.²⁸ also reported that the HRR following the peak exercise improved at 1 min (27 ± 15 at baseline vs. 40 ± 23 after rehabilitation) in children with CHD after the participation in a 12-week cardiac rehabilitation program (1 h per session twice a week). The authors also observed significant improvements at 1, 3, and 5 min with 19%, 27%, and 14% increases in HRR, respectively, after the 16-week EAA program (40 min per session twice a week; for a total of 21.3 h).

Thus far, there have been few studies showing the effects of EAA on the cardiac autonomic function. Cabiddu et al.²¹ reported that a single (15 min) session of hippotherapy could elicit an acute positive response in the cardiac autonomic system in children with neurologic disorders aged 4–12 years, with a significant increase in the standard deviation of R-R intervals (p < 0.05) in HRV during the recovery period. Nqwena and Naido²² reported that six sessions of therapeutic horseback riding demonstrated a change in HRV in children with disabilities, including those with autism spectrum disorder, CP, Down syndrome, spina bifida, and developmental delay (n = 29, a mean age of 8.69 years). The children participated in the horseback riding sessions weekly, which included basic riding skills, and they also performed various activities, such as using a ball and extending arms, during the session. These reports including this study suggest that EAA might be an option for children with CP to optimize their cardiac autonomic function.

The physiological mechanisms that exercise contributes to improved autonomic nervous system are not yet fully understood. However, exercise training is considered to increase nitric oxide and decrease angiotensin II, which lead to an improved cardiac vagal tone and reduced sympathetic activity.²⁹ More studies are needed to explore this issue.

Most studies that observed the effects of exercise on the HRR have been conducted at moderate or high intensity. A review article that was conducted in adult heart failure patients³⁰ reported that most aerobic exercise programs were conducted for 20 to 60 min at moderate or high intensity, with the patients reaching 50%–80% of their HR reserve or peak oxygen consumption, and concluded that participation in exercise training was effective in improving the HRR in the patients with CHF. The intensity of this EAA program was considered relatively low, which was not consistent with the exercise intensity in the previous review article. The possible mechanisms of the improvement of cardiac autonomic function by EAA with a low-intensity exercise can be due to the relaxation effect of the rhythmical movements associated with horseback riding. One study showed that low-intensity activities, such as breathing, relaxation exercises, or meditation, can positively affect the parasympathetic and sympathetic activities.³¹ Considering that it is difficult for children with CP to exercise at a high intensity, this study seems meaningful. Further research is needed to identify the optimal type and intensity of exercise to improve the cardiac autonomic function in children with CP during EAA.

The authors also found a decrease in the RHR after the 16-week EAA program. The RHR is also an important factor that predicts the function of the cardiac autonomic nervous system, and the increased RHR is associated with an increased risk of coronary heart disease, sudden cardiac death, atrial fibrillation, stroke, cardiovascular disease, and all-cause mortality in adults.³² It has been also reported that children with an increased RHR also have a higher total cholesterol and triglyceride level,³³ higher BP,³⁴ and an increased risk of total mortality.³⁵ Furthermore, they rarely engage in physical activity³⁶ and showed a positive association between RHR and sedentary behavior (high media use). Children with CP are known to have a higher RHR than the normal children due to the dysfunction of the cardiac autonomic nervous system and owing to their relatively sedentary lifestyle.^7,8 The children with CP have higher RHR of 15–17 beats/min than that of normal children.^8,37 Reimers reported that exercise, especially endurance training and yoga, decreases RHR.³⁸ In this context, EAA may be another option for endurance training or activity itself to decrease RHR in children with CP.

VO_2peak, defined as a CRF, is one of the predictive factors in estimating exercise tolerance or exercise capacity. As previously stated, children with CP (aged 7–17 years) have been reported to have a 15%–28% lower maximum oxygen uptake than the normal children.⁶ There was no significant difference in the maximal oxygen uptake between the groups in this study. The authors consider that the reason for this could be the low exercise intensity of the program (∼18%–22% of the HRR; Karvonen method: Target HR = [(HRmax − HRrest) × intensity % + HRrest]. In general, moderate (>40% of HRR) or high exercise intensity is recommended to increase the maximal oxygen uptake. A further study is needed to demonstrate the effect of EAA with a high intensity on VO_2peak in children with CP.

The sample size for this study was small; therefore, the effects of EAA on cardiac autonomic function should be verified in a larger population to generalize results in the future. Moreover, this study did not show the positive effect of the EAA program on VO_2peak in children with CP. Further studies are needed to investigate the effect of EAA with a high intensity on VO_2peak.

Conclusions

This study showed improved cardiac autonomic function in children with CP after completing the 16-week EAA program. In this study, The authors suggest that EAA may be one of the important exercises that can be provided to CP patients to improve their cardiac autonomic function.

Footnotes

Author Disclosure Statement

No competing financial interests exist.

Funding Information

This research was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (2017R1A2B4004615).

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