INTRODUCTION AND PURPOSE
The ability to reach for and interact with objects is a skill that allows infants to explore, gather information, and learn about their environment.1,2 Reaching emerges as poorly controlled swiping movements from 1 to 3 months of age, followed by more controlled, visually-guided reaching and grasping of objects from 4 to 5 months of age.3,4 The ability to reach for objects has been shown to play a key role in advancing object exploration behaviors and learning in infancy.5,6
Arthrogryposis is a nonprogressive neuromuscular disorder emerging from limited mobility from 6 to 8 weeks' gestational age. Infants are born with significant muscle contractures, fibrosis, and weakness, limiting movement across multiple affected joints.7 They may have difficulty lifting their arms against gravity, which can impair reaching and object exploration. Rehabilitation devices have not been available to enhance movement, exploration, and learning for such young populations. Recently, a novel exoskeleton, the Wilmington Robotic Exoskeleton (WREX) became available to adolescents and adults with significant upper extremity weakness.8–10
The WREX used here is the Pediatric (P)-WREX. It consists of 3D-printed plastic supportive parts with elastic bands to provide torque about the shoulder and elbow joints to support flexion against gravity. The WREX is a passive exoskeleton that supports the arm in a new resting position based on the properties of the elastic bands. It does not allow for programming or feedback. It attaches to a custom trunk brace for use outside a seating device. The WREX has been shown to improve upper extremity function within 1 session for older children with arthrogryposis, muscular dystrophy, or spinal muscular atrophy.8–10 For children with arthrogryposis between 6 and 14 years of age, it has been shown to improve fine motor performance, feeding, participation in school and hobbies, self-esteem, motivation, and social interaction.8,9
This study is the first to evaluate the feasibility and effectiveness of the WREX device for an infant. The purpose of this study was to determine whether a pediatric version of the WREX (P-WREX; Figure 1) was feasible for use in daily intervention, and whether its use could improve reaching and object interaction behaviors for an infant with arthrogryposis. Our goal was to follow up the participant longitudinally to characterize his behavioral changes across time. On the basis of previous studies, we hypothesized our participant would show improved reaching and object interaction abilities when wearing the P-WREX.8–10 Because arthrogryposis is not a progressive disorder and literature suggests postnatal muscle growth is possible in this population, we also hypothesized that intervention using the P-WREX would improve reaching and object interaction abilities for the infant across time even when he was not wearing the device.11,12
An infant with amyoplasia, the most common type of arthrogryposis, and his family participated in this study. Parents provided informed consent. The infant was assessed every 2 weeks from 8 through 13 months of age. The infant had a history of muscle fibrosis, decreased muscle mass, and multiple joint contractures in more than one area of the body with the limbs affected in a symmetrical manner, patent ductus arteriosus, patent foramen ovale, bilateral Achilles tendon lengthening (age 4 months), and ear tube placement (age 12 months). The infant received physical therapy and occupational therapy each 1 hour per week since 3 months of age. These services continued throughout the study. At the initiation of the study, the infant had full functional passive range of motion at both shoulders and elbows. He sat independently without arm support and used a bilateral palmar grasp. No standardized assessment of cognition was performed for this study, but the child qualified for special education services on the basis of his early intervention assessments.
The participant's object interaction abilities with and without the P-WREX were assessed using a single-subject ABA (Baseline, Intervention, Postintervention) design once every 2 weeks throughout a (1) 1-month baseline (P-WREX only used during assessments), (2) 3-month intervention, and (3) 1-month postintervention phase.
Intervention. Parents were educated via a manual, discussion, and demonstration to perform intervention activities with the infant wearing the P-WREX 60 minutes daily. In addition, the P-WREX could be used as desired during unstructured free play, or typical daily activities. Parents were instructed to supervise the infant whenever the P-WREX was worn. Parents reported daily durations for intervention and free play wear.
Intervention consisted of activities in sitting to promote general arm movement, reaching, object exploration, and elbow flexion (See the Appendix, Supplemental Digital Content 1, available at http://links.lww.com/PPT/A108). The overall goal was for parents to provide opportunities for the infant to move and explore objects in a larger play space than was available to him without the P-WREX. To progressively challenge the infant, the level of assistance provided by the P-WREX was decreased every 2 weeks, while the intervention tasks and object placement remained stable. The assistance level was decreased by replacing the elastic bands across the shoulder with bands of lower stiffness so the resting shoulder flexion position changed from 90° to 80° and so forth across time.
Postintervention Phase. The family was instructed to discontinue the structured intervention but to continue use of the P-WREX for unstructured free play as desired. This phase provided us with information about intervention retention effects as well as how often the family might typically use the device outside of intervention. Parents reported duration of free play wear.
Visits were performed at Nemours/A. I. duPont Hospital for Children, the University of Delaware, or the home depending on the family's preference. Assessments were video recorded using 2 camcorders providing frontal and side views of the infant. Videos were synchronized and coded by 2 coders using OpenSHAPA software. Twenty percent of the files were recoded for intra- and interrater agreement (both >90% for all measures on the basis of the equation [Agreed/(Agreed + Disagreed)] × 100). Blind coding of P-WREX ON and OFF conditions was not possible. Random interrater reliability coding aimed to minimize bias related to knowledge of device condition.
The Alberta Infant Motor Scale, a reliable and validated norm-referenced comprehensive motor assessment tool, was administered at each visit to assess posture, weight-bearing, and movement in prone, supine, sitting, and standing positions.13,14
Strength was assessed monthly by measuring the maximum active shoulder flexion range of motion bilaterally in side-lying (gravity-eliminated), supine, and sitting positions, a common method for infants not yet able to follow instructions required for manual or mechanized muscle testing procedures.
To assess feasibility of the device, a perception questionnaire regarding ease of use, comfort, and appearance was provided to the parents.
At each visit, the infant was provided the Reaching Location Assessment and the Midline Reaching Assessment—both while seated with and without the P-WREX. Condition order was alternated at each visit to avoid familiarity or fatigue effects. Trials began when the infant was in a positive behavioral state and looking at the assessment object.
The Reaching Location Assessment measured ability to contact an object presented across the reaching space. The infant was provided 30-second opportunities to interact with an object (2 × 2″ block at all assessments) at eye, chest, and hip height. At each height, the object was presented at midline, right, and left, but for the current analyses, midline, right, and left data were combined within each height because no systematic differences were observed across these positions. We coded toy contacts on the basis of the start and end video frames for periods when any part of either hand was in contact with the toy. Data were converted to percentages of time by dividing by total assessment time.
The Midline Reaching Assessment measured ability to contact an object (2 × 12″ rod at all assessments) presented in midline at chest height for 3 consecutive minutes. We coded (1) right/left hand toy contact, when the left or right hand was in contact with the toy; (2) mouth reaching, when the infant opened his mouth and moved it toward the toy while looking at the toy, and (3) visual attention to the toy, when the infant's eyes were directed at the toy for more than 1 second. Data were converted to percentages of time, dividing by assessment time, and times of behavioral overlap were identified. This produced unimanual toy contact (when only either the left or right hand was in contact with the toy), bimanual toy contact (when left and right hand toy contact periods overlapped), and toy contact while looking (multimodal exploration when toy contact and visual attention periods overlapped). The types of behavioral analyses used in this study are well-established methods widely used in developmental research.5,15–17
Data Analysis. To test for changes within sessions with and without the P-WREX, Wilcoxon signed rank tests were used to analyze aggregated differences from all study visits because data were not normally distributed in some conditions due to the large number of zero values. Statistically significant differences between conditions occurred when P was ≤ .05 and trends occurred when P was ≤ .10.
To test for changes across time with and without the P-WREX, the 2-standard deviation (2SD) band method was applied.18,19 A statistically significant change during the intervention phase occurred when at least 2 consecutive data points during intervention fell outside the mean ± 2SD band calculated from baseline.20
For all analyses, PASW (Predictive Analytics Software) Statistics version 18.0.3 (IBM Corporation, Somers, New York) was used.
Developmental and Strength Assessments
The infant consistently scored below the fifth percentile on the Alberta Infant Motor Scale, suggesting considerably delayed motor development.13 The infant's active shoulder flexion range of motion (Table 1) did not change during baseline, but improved both against gravity (sitting and supine) and with gravity eliminated (side-lying) throughout the intervention and postintervention phases, more for the right arm than left.
During the intervention phase, intervention occurred 37.3 ± 11.9 min/d (general arm movement 2.5 ± 5.9 min, reaching 18.3 ± 4.7 min, object exploration 8.1 ± 4.0 min, and elbow flexion 8.5 ± 3.6 min) and unstructured free play wear occurred 44.6 ± 32.8 min/d. During the postintervention phase, free play wear occurred 61.4 ± 15.2 min/d.
Parents rated ease of donning as a 3 (1 = very difficult, through 5 = very easy) and ease of doffing as a 4. They rated the infant's comfort as a 3 (1 = very uncomfortable, through 5 = very comfortable) after 1 hour of wear. They rated ease of use outside the home as a 2 (1 = very difficult, through 5 = very easy), reporting it did not fit in the car seat or stroller, was “cumbersome” to carry alone, and was “difficult to carry (the infant) with it on.” They rated restrictiveness on daily activities as a 3 (1 = extremely restricted, through 5 = no restrictions), reporting it did not assist elbow flexion well and limited floor play. They rated restrictions on mobility as a 1 (1 = extremely restricted, through 5 = no restrictions) because it restricted floor mobility (transitions and rolling). They rated appearance as a 2 (1 = very unattractive, through 5 = very attractive), noting the unattractive elastic bands and device bulk.
Reaching Location Assessment
Within sessions, the P-WREX was most effective at improving reaching ability when the infant reached for objects at hip and chest level (Figure 2A). The infant contacted objects at hip level more with the P-WREX (median = 34.78% of time) than without (median = 17.86%), z = -1.960, P = .050, medium effect size r = -0.46. He contacted objects at chest level more with the P-WREX (median = 35.42%) than without (median = 0%), z = -2.521, P = .012, large effect size r = -0.59. The infant never contacted objects at eye level without the P-WREX (median = 0%), and rarely contacted objects at eye level with it (median = 0%), z = -1.604, P = .109, medium effect size r = -0.38. The infant had increased contact with objects at hip and chest levels when wearing the P-WREX at most visits during the baseline, intervention, and postintervention phases (Figures 2B and 2C). He contacted objects at eye level at only a few visits during the baseline and intervention phases while wearing the P-WREX (Figure 2D).
Across time with the P-WREX ON, the infant spent significantly more time contacting objects at hip (2SD band 0%-56.8%) and chest (2SD band 0%-29.9%) level during intervention than during baseline, whereas contact at eye level did not significantly change (2SD band 0%-12.85%). Across time when not wearing the P-WREX, the infant spent significantly more time contacting objects at hip level (2SD band 0%-25.5%), whereas change in contacts at chest (2SD band at 0%) and hip level (2SD band at 0%) was not significant.
Midline Reaching Assessment
Within sessions, the infant showed improved unimanual and bimanual contact with objects presented in midline at chest level when wearing the P-WREX (Figure 3A). The infant spent more time contacting objects unimanually with the P-WREX (median = 25.49% of time) than without (median = 1.67%), z = -2.547, P = .011, large effect size r = -0.58 (Figures 3A and 3B).
Across time, there was a significant increase in unimanual contacts between the baseline and intervention phases without the P-WREX (2SD band at 0%), but not with the P-WREX (2SD band 0%-92.83%). Around 6 weeks into the intervention, the infant showed independent reaching for the first time and his percent time contacting objects unimanually while not wearing the P-WREX steadily increased from this point through the end of the study (Figure 3B). In contrast, while wearing the device, his unimanual contacts increased during intervention but decreased during the postintervention phase.
Within sessions, the infant showed bimanual object contacts only when wearing the P-WREX (Figures 3A and 3C). Although never observed without the P-WREX (median = 0%), this challenging behavior was observed infrequently, but significantly more, while using the P-WREX (median = 1.95%), z = -2.366, P = .018, large effect size r = -0.53.
Across time, the ability to contact objects bimanually emerged midway through the intervention phase and persisted thereafter. There were no significant differences in bimanual contacts between the baseline and intervention phases with (2SD band 0%-10.34%) or without (2SD band at 0%) the P-WREX.
Within sessions, the infant spent less time reaching for objects with his mouth with the P-WREX (median = 0%) than without (median = 2.15%), z = -2.100, P = .036, medium effect size r = -0.47 (Figures 3A and 3D).
Across time, mouth reaching without the P-WREX significantly decreased throughout the study (2SD band 4.82%-32.35%) completely disappearing in the middle of intervention. Interestingly, this decrease in mouth reaching without the P-WREX coincided with the emergence and steady increase in hand-reaching ability also observed without the device (Figure 3E). Thus, as the infant's manual abilities improved across time, he decreased his attempts to reach for and explore objects using his mouth, a less adaptive strategy.
Within sessions, the infant showed improved visual attention for objects when wearing the P-WREX. The infant's visual attention to presented objects was higher with the P-WREX (median = 48.86%) than without (median = 23.51%), z = -2.191, P = .028, medium effect size r = -0.49 (Figures 4A and 4B). Across time, there were no significant differences in visual attention from baseline through intervention with (2SD band 0%-97.83%) or without (2SD band 0%-79.94%) the P-WREX.
Within sessions, percent time looking at objects while contacting them, or multimodal exploration, was significantly greater with the P-WREX (median = 24.58%) than without (median = 6.09%), z = -2.803, P = .005, large effect size r = -0.63 (Figures 4A and 4C). Across time, multimodal exploration did not significantly change with (2SD band 0%-62.98%) or without (2SD band 0%-32.87%) the P-WREX. Interestingly, both visual attention to objects and multimodal exploration seemed to increase during the intervention then decrease during the postintervention phase of the study with the P-WREX ON (Figures 4B and 4C).
Moreover, Figures 4D and 4E suggest that time looking at objects was associated with the time reaching for and contacting objects with either hand. This association was much stronger with the P-WREX than without (Pearson correlation, 2-tailed: r(7) = 0.99, P < .0001 with the P-WREX; r(8) = 0.004, P = .992 without the P-WREX). Thus, the P-WREX may have facilitated not only object contacts but also interest in objects.
Exoskeletons May Be Feasible for Daily Intervention in the Natural Environment
This study suggests that exoskeletons like the P-WREX may be feasible for use in daily home-based intervention with infants. Throughout the study, the P-WREX device was used daily for up to 1 hour. The device was reasonably comfortable and did not present significant difficulties for donning and doffing. However, parents reported concerns that it restricted floor mobility, poorly assisted elbow flexion, was unattractive, and bulky (difficult to carry and incompatible with devices like car seats and strollers).
Other key challenges relate to accessibility and affordability. Versions of the device can be purchased through JAECO Orthopedic, A. I. DuPont Hospital for Children, or Magic Arms for about $10 000 per pair. There is typically an extended waiting period to receive the device, and young children require replacements regularly because of growth. There is a need to continue to improve existing exoskeletons and to develop more affordable, accessible exoskeletal devices that address the limitations identified in this study (recently developed alternatives are Angel Arms open source 3D-printed exoskeleton, http://3dprint.com/tag/angel-arms/; Playskin Lift open source exoskeletal garment, http://www.ncbi.nlm.nih.gov/pubmed/26316534).
Exoskeletons May Be Effective Assistive Devices
The findings suggest that exoskeletons may serve as effective assistive devices to improve function when worn. Within a session, the P-WREX significantly improved reaching ability at hip and chest level, increased unimanual and bimanual object contact, decreased less adaptive mouth reaching, increased attention to objects, and increased multimodal exploration. Reaching and visual attention were significantly correlated only while wearing the P-WREX, further suggesting that the P-WREX facilitated both object interaction and attention.
Tools like the P-WREX are important to assist movement and play in early development. The way children interact with and gather information about objects impacts their perceptual-motor, language, social, and cognitive development.21–24 Children typically learn about objects by interacting with them a large amount of the time via a variety of behavioral combinations.16 The amount and variability of behavioral performance, and consequent information uptake and learning, is often diminished for children with disabilities.17,25–27 Devices like the P-WREX may allow young children to explore, gather information, play, and learn when it is critical in early development despite their existing movement limitations.
Exoskeletons May Be Effective Rehabilitative Devices
The findings also suggest that exoskeletons like the P-WREX may serve as effective rehabilitative devices to improve function even when they are not donned. Across time, the infant's active range of shoulder flexion improved during the intervention and postintervention phases, but not during baseline, suggesting intervention with the P-WREX increased muscle strength. While wearing the device, the infant spent more time contacting objects at hip and chest height during the intervention phase compared with baseline.
Without the device donned, the infant showed improved object interaction during the intervention phase, spending more time contacting objects at hip and chest height and less time mouth reaching compared with baseline. At the first visit, the infant was unable to contact objects at chest height although he was 8 months old and reaching typically emerges by 5 months. This ability to contact objects emerged for the infant without the device about 6 weeks into the intervention, a period long enough to allow for changes in muscle strength, and improved throughout the remainder of the study.
This steady increase in hand-reaching ability without the P-WREX donned was temporally associated with a significant decrease in mouth reaching, which was no longer observed after the middle of the intervention. Individuals who cannot yet control their arm movement for reaching often employ mouth or feet reaching strategies. These strategies provide limited object exploration and manipulation possibilities and typically dissipate as manual abilities improve.
The limited number of baseline visits in this study likely reduced power to detect other effects. For future studies, more data points in baseline are recommended. Because the device cost was high and this was the first time a device like this has been used for an infant, only 1 participant was studied. Future studies would benefit from a larger participant pool. Also, because these devices are novel, we did not have subject-specific criteria for adjusting the level of assistance. Future research should evaluate criteria for determining optimal levels of assistance to promote skill development. Furthermore, the nature of this study did not allow us to separate the effects of the device and intervention from one another or potential maturational effects, especially considering that the course of early development has not been well documented for children with arthrogryposis. Studies with larger subject pools from a variety of populations must be conducted to verify these findings and rule out other potential causes of change, such as maturation, experience, and ongoing interventions.
Exoskeletons May Be Most Effective as Part of a Targeted Intervention Program
An important finding was that when wearing the device, the infant showed improved unimanual reaching ability, visual attention, and multimodal exploration across time only during periods when device wear was paired with targeted daily intervention. Performance of these behaviors while wearing the P-WREX increased during the intervention phase, but then decreased during the postintervention phase when the family continued using the P-WREX about 1 h/d for free play but ceased performing the targeted intervention activities. These results suggest that devices like the P-WREX may be most effective at maximizing function across time when combined with targeted interventions. Isolated use of such devices may not facilitate long-term improvements in behavioral performance longitudinally.
Exoskeletons may serve as feasible and effective assistive devices for immediate improvements in infants' reaching and visual attention abilities when they are worn. They may also have potential as rehabilitative devices to improve object interaction abilities across time, even when they are not donned. It is likely that exoskeletons need to be paired with targeted intervention activities for optimal rehabilitative benefits to be observed across time. Early intervention could be greatly enhanced by these innovative tools that allow children to learn to move, explore, and play in spaces otherwise unavailable to them. Future research incorporating measures of cognition and larger samples of children representing a wider spectrum of diagnoses is needed to further explore the effectiveness of novel exoskeletons like the P-WREX.
We acknowledge the infant and his parents for their participation, time, and patience in making the current longitudinal study possible. Also, we thank the research assistants who helped with the coding of data.