Abstract
Objectives:
Pharmacotherapy among children with attention-deficit/hyperactivity disorder (ADHD) is effective, but many patients suffer from secondary psychiatric problems even after improvement of ADHD core symptoms. Hippotherapy have been used as adjunct treatment options for physical and psychosocial rehabilitation as well as to ameliorate core symptoms. The aim of this study was to investigate the effects of Hippotherapy versus pharmacotherapy for children with ADHD.
Design:
Thirty-four participants with ADHD were randomly assigned at a 1:1 ratio to either 24 sessions of a twice-weekly hippotherapy or pharmacotherapy. To assess therapeutic effects, the ADHD Rating Scale (ARS) was used pretreatment and posttreatment as the primary outcome measure. Secondary outcomes included the Child Behavior Checklist (CBCL), Self-Esteem Scale (SES), Pediatric Quality of Life Inventory (PedsQL) child and parent report version, Developmental Coordination Disorder Questionnaire (DCDQ), Clinical Global Impressions-Severity (CGI-S), and quantitative electroencephalography.
Results:
Both groups showed marked improvements in ADHD symptoms, CGI-S. No significant differences between groups were detected regarding treatment outcome except thought problem subscales of CBCL. Twelve weeks of hippotherapy improved attention, impulsivity/hyperactivity, and quality of life.
Conclusion:
This trial is promising, but further studies are required to evaluate the long-term clinical effectiveness of hippotherapy. The study is registered with
Introduction
A
Hippotherapy is a psychosocial option for treating psychiatric disorders by facilitating motor skills, coordination, and self-regulation. 9 In particular, interacting with horses promotes social competence, trusting alliance, and self-confidence. 10 A recent systematic review involving treatment of psychiatric disorders demonstrated the beneficial effects of hippotherapy. 11 However, few attempts of hippotherapy specifically targeting ADHD have been made. Cuypers et al. found therapeutic effects on behavior, quality of life, and motor performance in five children with ADHD. 12 Hyun et al. 13 examined the impact of 4 weeks of hippotherapy in 12 participants with ADHD compared to healthy controls and found that the ADHD Rating Scale (ARS) significantly improved and showed increased brain connectivity. However, insufficient information exists to determine whether hippotherapy is an effective option in the treatment of ADHD.
Recently, the authors reported the effect of hippotherapy for children with ADHD. 14 Their study showed significant treatment effects on core ADHD symptoms and social problems. However, there was no control group. Therefore, they designed a randomized controlled trial (RCT) to investigate the efficacy of hippotherapy versus pharmacotherapy. The hypothesis was that hippotherapy would be effective for improving ADHD core symptoms, self-esteem, motor coordination, quality of life, and psychosocial functioning, and that it would change the theta/beta ratio in quantitative electroencephalography (QEEG) compared to conventional pharmacotherapy.
Materials and Methods
Participants
Children aged 6–12 years with ADHD were recruited from the Child and Adolescent Psychiatry Service. Diagnosis of ADHD was confirmed using the American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders, 4th Edition Text Revision (DSM-IV-TR). 15 The process to confirm ADHD and exclusion criteria are reported in a previous study. 14 Exclusion criteria were (1) a learning disorder or an intelligence quotient measured by the Korean Wechsler Intelligence Scale for Children-IV <70; (2) significant medical condition, schizophrenia or other psychotic disorder, bipolar disorder, a history of alcohol or drug dependence, neurologic disorders, epilepsy, and organic mental disorders; (3) a major depressive disorder that required pharmacotherapy; (4) significant suicidal ideation; (5) Tourette disorder or obsessive compulsive disorder that required pharmacotherapy; and (6) use of methylphenidate or atomoxetine within 90 days of baseline. A total of 34 children with ADHD were randomized to either hippotherapy or pharmacotherapy. Children who were taking methylphenidate or atomoxetine within 90 days of baseline were excluded. This study protocol was approved by the Institutional Review Board. Signed informed consent was obtained from all participants and their parents.
Measures
ADHD Rating Scale
The ARS is used to assess inattention and hyperactivity symptoms in children with ADHD. 16 It includes 18 items, 9 for inattention and 9 for hyperactivity and impulsivity. The Korean version of ARS 17 has been validated with internal consistency, with Cronbach's alpha of 0.77–0.89.
Clinical Global Impressions-Severity and Clinical Global Impressions-Improvement
The Clinical Global Impressions-Severity (CGI-S) is a widely used clinician administered scale for symptom severity (1 = not ill; 2 = very mild; 3 = mild; 4 = moderate; 5 = marked; 6 = severe; 7 = very severe). 18 The Clinical Global Impressions-Improvement (CGI-I) is a 7-point rating of treatment response (1 = very much improved; 2 = much improved; 3 = minimally improved; 4 = no change; 5 = minimally aggravated; 6 = much aggravated; 7 = very much aggravated).
Self-Esteem Scale
The Self-Esteem Scale (SES) comprises 10 items, and participants are instructed to rate each item from 1 to 4. Higher scores indicate higher levels of self-esteem. The authors used the Korean version of SES developed by Jeon. 19
Developmental Coordination Disorder Questionnaire
The Developmental Coordination Disorder Questionnaire (DCDQ) is a parent report form questionnaire used to screen for coordination disorders in children. 20 The questionnaire has shown good reliability, internal consistency (Cronbach's alpha = 0.94), and validity.
Child Behavior Checklist
The Child Behavior Checklist (CBCL) is a widely used standardized method of identifying childhood psychologic behavioral problems by parent report. 21 The CBCL includes 113 items divided into 8 syndrome scale scores (anxious/depressed, withdrawn/depressed, somatic complaint, social problems, thought problems, attention problems, rule-breaking behavior, aggressive behavior) and 2 broadband syndromes (internalizing and externalizing problems). Internalizing problems consist of withdrawal/depressed, anxious/depressed, and somatic complaints. Externalizing problems involve aggressive and rule-breaking behavior. Higher scores indicate worse symptoms.
Pediatric Quality of Life Inventory
The Pediatric Quality of Life Inventory (PedsQL) measures Health-Related Quality of Life (HRQOL) for the 1-month period before interview. 22 It consists of 4 domains and 23 items: Physical Functioning (8 items), Emotional Functioning (5 items), Social Functioning (5 items), School Functioning (5 items), and summary scores. A 5-point response scale is utilized (0 = never a problem; 1 = almost never a problem; 2 = sometimes a problem; 3 = often a problem; 4 = almost always a problem). Higher scores reflect better quality of life. Two forms of questionnaires were investigated: a form that parents reported about the quality of life of the child and a form that the child self reported.
Quantitative electroencephalography
The QEEG, which is a tool for measuring brain electrical activity, was recorded using a Neuroscan Synamp2 amplifier (Compumedics USA, El Paso, TX) provided by 32 Ag/AgCl electrodes positioned according to the 10/20 system. Input signals were referenced to the linked ears, filtered between 0.5 and 50 Hz, and digitized at a sampling rate of 250 Hz. Electrodes were placed according to the international 10–20 system. Electrode impedance was maintained below 5 kΩ. Artifact-free 300-sec periods were recorded and analyzed. Epochs of movement-related artifacts were excluded from analyses by direct visual inspection of the raw data. Participants were seated in a dimly lit, sound-attenuated room. EEG activity was recorded with eyes open during the go/no-go test for 5 min. The average power spectrum of EEG frequencies was calculated by the fast Fourier transform, a mathematical process that can be used to identify various frequency bands (delta, theta, alpha, and beta) on QEEG. Results are presented as absolute spectral power values (lV2) for individual segments of the EEG spectrum, including delta (0–4 Hz), theta (4–8 Hz), alpha (8–12 Hz), beta (12–20 Hz), and high beta (20–30 Hz). On the basis of previous literature, 23 the theta/beta ratio was considered a biological marker to evaluate the effect of intervention on cerebral functional changes in children with ADHD.
Procedures
The children were evaluated at entry by the Kiddie Schedule for Affective Disorders and Schizophrenia (K-SADS) for School-aged Children. K-SADS was administered by a trained psychologist with a master's degree. The Principal Investigator reviewed the diagnostic information and only individuals meeting criteria for a full DSM-IV ADHD diagnosis were included. At visit 1, participants received an initial comprehensive evaluation to determine study eligibility. Child psychiatrists performed a baseline physical examination, and participants then completed the study measures. Laboratory studies included complete blood cell count, electrolyte profile, comprehensive metabolic panel, and electrocardiogram. Eligible participants were given a 30-day period before visit 2. During visit 2, the psychologist administered ARS-Korean Version and CGI-S. Participants and their parents completed the self-rating scale measures SES, DCDQ, CBCL, and PedsQL. Hippotherapy or medication was started within 2 weeks after visit 2 and continued for 12 weeks. Within 2 weeks after the 24th hippotherapy session or medication for 12 weeks, all study scales were readministered (visit 3). Medications for ADHD were not permitted during hippotherapy to reduce the effect of confounding factors.
Randomization
Eligible participants were randomized into 1 of 2 groups (hippotherapy or pharmacotherapy). Random group assignment study numbers were generated by the statistician on this project.
Hippotherapy
Hippotherapy was based on a psycho-exercise program to enhance attention and inhibit impulsivity. Hippotherapy is conducted in groups of two participants. Participants received hippotherapy sessions over 12 weeks. Each session was held twice per week (total of 24 sessions) and lasted ∼1 h. The hippotherapy program consists of unmounted activities and mounted activities. Participants learn to focus and enhance their attention, awareness, and self-control by hippotherapy. Details of the 12-week EAT program are described in Table 1. 24 Children were accompanied by their parents to each session, wore protective equipment (helmet, boots, stirrups, safety vest, and gloves), and were accompanied by two trained side walkers and a leader for safety. The program was delivered by experienced physical therapists who are trained in hippotherapy by the American Hippotherapy Association and had obtained Professional Association of Therapeutic Horsemanship (PATH) International registered riding instructor.
Pharmacotherapy
The participants assigned to pharmacotherapy received a medication prescription from a child and adolescent psychiatrist. After the psychiatric interview, psychiatrists selected either methylphenidate or atomoxetine according to clinical decision. To optimize the drug effects, doses were titrated to target (1.2 mg/kg of methylphenidate or 1.2 mg/kg of atomoxetine) in the first 8 weeks and maintained for at least 4 weeks after complete dose titration. Participants were free to discontinue medication use on request. When medication was not effective or intolerable side effects emerged, changes in dose or medication type were made after a face-to-face interview with the child psychiatrist.
Statistical analyses
Baseline demographic data were analyzed using χ2 tests for categorical variables. Baseline and follow-up comparisons of clinical characteristics between hippotherapy group and pharmacotherapy were examined using independent t tests or Wilcoxon signed rank sum test for continuous variables. The changes from baseline to follow-up within groups were compared using paired t test or Mann–Whitney tests. Changes from baseline to follow-up between groups were examined using independent t test or Wilcoxon signed rank sum test. The rate of responders between groups was assessed using χ2 tests. Pearson correlation analysis was performed to estimate the association between change of theta/beta ratio and treatment response. To correct multiplicity, Bonferroni correction was applied. Analyses were executed using SAS version 9.4 (SAS Institute, Cary, NC) with the alpha value set at 0.05.
Results
A total of 34 children were referred from a child and adolescent psychiatry unit. Parents completed screening questionnaires and children were randomized to 2 groups (17 in hippotherapy group and 17 in pharmacotherapy group). Of 34 parents willing to participate in the RCT, 2 parents in the pharmacotherapy group declined to participate in the RCT. Seventeen participants in the hippotherapy group and 15 participants in the pharmacotherapy group had 12 weeks of follow-up.
Of randomized children, 31 (91.18%) were male. Table 2 gives the demographic characteristics of the hippotherapy group and pharmacotherapy group. A total of 1 (5.88) of 14 participants in the hippotherapy group and no participants in the pharmacotherapy group had received medication before the study. Hippotherapy and pharmacotherapy groups were comparable on all measures at baseline (Tables 2 and 3). One participant in the pharmacotherapy group did not complete follow-up assessment. In the pharmacotherapy group, 2 participants were treated with atomoxetine and 13 participants were treated with methylphenidate. Mean atomoxetine dose was 34 mg (0.83 mg/kg) and mean methylphenidate dose was 18.31 mg (0.63 mg/kg).
Bonferroni-adjusted p-value.
Wilcoxon rank sum test was used.
Fisher's exact test was conducted.
ADHD, attention-deficit hyperactivity/disorder; NOS, not otherwise specified; SD, standard deviation.
There were no significant differences between groups for any variable.
Bonferroni-adjusted p-value.
Independent t test was used.
Wilcoxon rank sum test was used.
ARS, Attention-Deficit Hyperactivity/Disorder Rating Scale; CGI-I, Clinical Global Impressions-Improvement; CGI-S, Clinical Global Impressions-Severity; DCDQ, Developmental Coordination Disorder Questionnaire; PedsQL, Pediatric Quality of Life Inventory; PedsQL_child, PedsQL reported by child; PedsQL_parent, PedsQL reported by parent; SD, standard deviation; SES, Self-Esteem Scale.
Clinical outcomes
ADHD core symptoms
ADHD core symptoms significantly improved in both groups over time (hippotherapy group: t = 8.50, p < 0.001, pharmacotherapy group: t = 5.86, p < 0.001). However, there was no significant difference between groups regarding ADHD core symptoms (Table 3).
Secondary outcomes
Baseline and 12 week follow-up scores of all clinical outcome measures are presented in Tables 3 and 4. In the hippotherapy group, the quality of life reported by the children (t = −2.14, p = 0.048), the quality of life of the children reported by the parents (t = −3.21, p = 0.006), and the CGI-S improved significantly over time (t = 5.34, p < 0.001). In the pharmacotherapy group, CGI-S significantly improved (t = 6.09, p < 0.001) and the total problems (t = 2.64, p = 0.022), externalizing problems (t = 2.66, p = 0.21), and aggressive behaviors (t = 2.64, p = 0.022) in CBCL subscale were statistically significantly improved. There were no significant differences between groups on the other secondary outcomes, including self-esteem, DCDQ, and PedsQL. The thought problem subscales of CBCL at follow-up were 58.06 ± 7.04 (mean ± standard deviation) for the hippotherapy group and 65.93 ± 7.47 for the pharmacotherapy group, showing a statistically significant difference between the two groups. However, the CBCL score changes before and after intervention in each group were not significantly different between the two groups.
Higher values denote more severe symptoms.
Bonferroni-adjusted p-value.
Wilcoxon rank sum test was used.
Independent t test was used.
SD, standard deviation.
Quantitative electroencephalography
Changes in the theta/beta ratio at baseline and postintervention were not significantly different between groups (Table 5). Although the changes were not significant, after 12 weeks of intervention, the theta/beta ratio decreased at Fz, Pz, and Oz in both groups, apart from the increased theta/beta ratio at Cz in the hippotherapy group (p = 0.05). Pearson correlation analyses revealed no significant association between changes of theta/beta ratios and treatment response.
Bonferroni-adjusted p-value.
Wilcoxon rank sum test was used.
Independent t test was used.
SD, standard deviation.
Response rate
Thirteen participants (76.47%) in hippotherapy group and 11 participants (73.33%) in the pharmacotherapy group demonstrated response to intervention (Table 6), as measured by a 30% reduction on the ARS score across treatment (p = 1.00).
Bonferroni-adjusted p-value.
Rating of 30% baseline ARS total score reduced was used to classify treatment response status.
ARS, Attention-Deficit Hyperactivity/Disorder Rating Scale.
Discussion
To the best of the authors' knowledge, this study is the first RCT of hippotherapy in children with ADHD. Both hippotherapy and pharmacotherapy groups showed significant improvement in ADHD core symptoms and CGI-S over time. The results indicate that hippotherapy is not inferior to pharmacotherapy in treating ADHD among children. However, there are several important issues to consider when interpreting the results. First, the trial does not deliver with the same intensity. In the current study, most children and their parents were willing to participate in the hippotherapy group although they understand the random assignment of intervention. After randomization, some participants and parents assigned to pharmacotherapy were disappointed and two participants dropped out. This suggests that the adherence and compliance rates for the hippotherapy group could be significantly different from those in the pharmacotherapy group. However, since the authors did not evaluate exact drug compliance by drug level checks, they cannot compare rates of adherence and compliance between the two groups. Second, there were no differences between the groups in demographic information. However, the pharmacotherapy group tended to have a severe psychopathology profile and low quality of life compared to the hippotherapy group at baseline, indicating that the pharmacotherapy group may be more complicated or resistant to intervention. Thus, they might have underestimated the efficacy of pharmacotherapy and overestimated the efficacy of hippotherapy.
The mechanism of action of hippotherapy in children with ADHD is uncertain. There are several possible explanations for improving ADHD core symptoms. First, physical activity may positively affect inattention and impulsivity. 25 Recent meta-analysis of the efficacy of exercise interventions indicates that exercise intervention has specific beneficial effects on inhibitory, cognitive, and memory function. 26 A second hypothesis is that the repetitive symmetric and rhythmic motion of horse riding stimulates a range of vestibulo-cerebellar system processes. Almost half of children with ADHD exhibit poor balance and coordination. 27 Researchers reported that the cerebellum, right prefrontal cortex, and striatum are significantly smaller in children with ADHD 28 and suggested that dysfunction of the ventral tegmental-limbic dopaminergic system could be involved in the pathophysiology of ADHD. 29 Arnold et al. also proposed that vestibular stimulation may lead to improved ADHD symptoms in patients with ADHD. 30 A third hypothesis is that hippotherapy contributes to improved self-regulation and behavioral problems. Previous studies demonstrated that riding a horse enables the rider to promote a sense of autonomy, problem solving skills, and control by experiencing complete control of direction and speed. 31 There is some evidence to suggest that improvements in anxiety, irritability, inattention, and hyperactivity could be achieved by reciprocal interaction with horses. 32 In addition, interaction with horses may be an enjoyable experience that leads to higher motivation to facilitate learning and alter behavior. 33
In this study, although there were no statistically significant differences, the scale of social problems improved after 12 weeks of hippotherapy. This result is consistent with previous studies that have reported significant improvement in social competence and communication skills after therapeutic horse riding. 34 The previous meta-analysis of animal-assisted therapy found a moderate effect for improving social skills. 35 A recent RCT of therapeutic horse riding targeting individuals with autism spectrum disorder also demonstrated improved social interaction, communication skills, and behavior. 36 Children with ADHD commonly have difficulties in social problems, including social withdrawal, peer rejection, and bullying. 37 The promotion of nonverbal communication and joint attention in these children would be achieved by interaction with horses. Therefore, hippotherapy may be a new psychosocial option to enhance social incompetence in children with ADHD.
QEEG has been proposed as a useful tool to investigate the pathophysiology of ADHD. 38 Theta/beta ratio has been reported as an inattention index in children with ADHD. 39 Monastra et al. found increased theta band power and decreased beta band power in children with ADHD. 40 Jang et al. reported that the theta/beta ratio changes at Pz after hippotherapy in children with ADHD. 14 After 12 weeks of intervention in this study, the theta/beta ratio of pharmacotherapy and the hippotherapy group tended to decrease in Fz, Pz, and Oz, although there was a greater reduction in the pharmacotherapy group. In Cz, the theta/beta ratio of the hippotherapy group tended to increase compared to that of the pharmacotherapy group. In this study, QEEG was the only rater-blinded biological measure that could block halo effect and rater bias. Thus, the results indicate that hippotherapy may affect cerebral function less than pharmacotherapy in children with ADHD.
The limitations of this study include lack of long-term follow-up assessment and small sample size. Thus, these results are limited in generalizability and should be cautiously interpreted. Replication with a large randomized clinical trial to confirm the effects of hippotherapy over time is needed. Measurement outcomes (CBCL, PedsQL parent report form, CGI-S) were assessed by nonblinded estimator, which may increase the bias due to expected benefits of hippotherapy or pharmacotherapy.
Conclusions
The current study found beneficial effects of hippotherapy on ADHD core symptoms and quality of life in children with ADHD.
Footnotes
Acknowledgments
This study was conducted by the Special Reserve Fund of the Korea Racing Authority. The findings and conclusions in this study are those of authors and do not necessarily represent the views of the funding agency. The results of the present study do not constitute endorsement by the “Journal of Alternative and Complementary Medicine.”
Author Disclosure Statement
No competing financial interests exist.
