Independent walking and balance in children with CHARGE syndrome

Abstract

Children with CHARGE syndrome (CWCS) are born with multiple physical disabilities, several of which impair balance and the onset of motor milestones. Early motor development problems can include delayed independent walking, which has been found in CWCS. In addition, few studies have examined balance in CWCS and these studies have been limited in scope, necessitating a more comprehensive examination of balance in this population. Motor development occurs as a progression of stages as represented by Seefeldt’s conceptual model. As such, it is essential to examine the association of early development of foundational skills, such as balance, with the onset of motor milestones as they are building blocks to motor competence. The aims of this study are to (1) examine the differential effects of children with and without CHARGE syndrome on balance and (2) examine the association of age of walking to these balance measures. In this study, 27 CWCS and 22 children without CHARGE syndrome, aged 7 to 16 years, were assessed on four components of balance including anticipatory control, reactive postural control, sensory orientation, and dynamic gait using the shortened version of the Balance Evaluation Systems Test (mini-BESTest) and parental reported age of independent walking. Their balance and age of walking were compared to 22 typically developing peers of similar age and gender distribution. Results revealed that CWCS walked three times later than their peers without CHARGE syndrome and had significant deficits on all balance systems assessed with the largest difference occurring in anticipatory control. Anticipatory control is critically important in maintaining static and dynamic postural control. These results indicate a critical need for early functional balance training and compensatory strategies in CWCS.

Keywords

Deafblind motor development motor skills postural control motor milestones

CHARGE syndrome is a multifaceted syndrome of complex birth defects (Pagon et al., 1981). The unique nature of children with CHARGE syndrome (CWCS) brings a multitude of challenges that affect not only the overall motor development of the child but often result in developmental motor delays (Thelin et al., 2011). Therefore, it is very important to assess CWCS’s balance and gross motor skill development (Hartshorne et al., 2011; Salem-Hartshorne & Jacob, 2004). There are several components of CHARGE syndrome that can cause delays in motor development including sensory deficits (e.g. visual, auditory, and vestibular), musculoskeletal (e.g. muscle laxity, ataxia, and scoliosis), and neurological impairments (Donovan et al., 2017; Hartshorne et al., 2011). Environmental factors may also have a strong negative impact on motor development (Foster et al., 2019; Foster & French, 2018; Thelen & Fogel, 1989), particularly prolonged stays in the hospital (Hartshorne et al., 2011) and fewer opportunities at home, the community, and in schools to engage in physical activity, recreation, and sports (Lieberman et al., 2012).

Deficits in gross motor development begin at a very young age in infants with CHARGE syndrome as they go through motor milestones such as rolling, sitting, and independent walking much later than their typically developing peers (Hartshorne et al., 2011; Salem-Hartshorne & Jacob, 2004). Motor development occurs as a progression of stages as represented by Seefeldt’s conceptual model (Seefeldt, 1980). The first level of this model consists of reflexes and postural reactions during infancy, followed by a progression of motor milestones such as rolling, crawling, cruising, and walking. These early experiences are critical for subsequently developing fundamental motor skills during early childhood before reaching a critical proficiency barrier. For children who do not meet proficiency in these skills by the age of 7 years, their potential to develop transitional skills and sport-specific skills may be affected. A revised version of Seefeldt’s conceptual model is Clark and Metcalfe’s (2002) mountain of motor development which further breaks down the first stage, reflexes and reactions, into two periods, reflexive and the preadapted, indicating the critical importance of these basic skills that should be acquired at an early age (see Figure 1). As such, it is essential to examine early development of foundational skills, such as balance, as they are building blocks to motor competence, which is important for leading active and healthy lifestyles (Lima et al., 2017, 2019).

Figure 1.

Mountain of motor development with Seefeldt’s conceptual proficiency barrier.

Balance is a foundational and critical component of much of the mountain of motor development including the preadapted period of acquiring motor milestones through skillfulness and is important for independent living. Adequate balance is not only necessary for involvement in sport skill development but also activities of daily living (e.g., showering, getting groceries, cleaning the house) and quality of life (e.g., participating in recreational physical activities as most require running and other locomotor skills; Rudd et al., 2015). Maintaining balance requires the sensory systems, specifically vision, vestibular, and somatosensory systems, to be integrated with the motor and cognitive systems (Shumway-Cook & Woollacott, 2012). Impairments in any of these systems can cause deficits in balance and postural control (Westcott & Burtner, 2004). A child who has an impairment in any one of these systems can likely compensate enough to limit adverse effects to their balance; however, when there are multiple impairments, in either sensory systems or a combination with the motor and/or cognitive systems, the child’s compensatory strategies become reduced (Sobsey & Wolf-Schein, 1996).

Limitations in balance can result in reduced physical activity participation (Westcott & Burtner, 2004). Early motor development problems can include delayed independent walking, which will likely negatively affect the child’s independence and interactions with the world (Dammeyer, 2012). Walking, the final motor milestone developed during the preadapted period (Clark & Metcalfe, 2002), is a complex balance task which requires coordination of the limbs while alternatively balancing on one foot while progressively moving forward. Walking also requires sufficient strength and the ability to solve problems such as stepping over or around objects and adjusting body positioning accordingly. The average ages of independent walking in CWCS are 23 to 48 months later than typically developing children, who independently walk between 12 and 14.5 months (Haibach & Lieberman, 2013; Karasik et al., 2011; Størvold et al., 2013). Age of independent walking has been found to be associated with a variety of other skills such as communication and language acquisition (Dammeyer, 2012; Thelin & Fussner, 2005), adaptive behavior (Salem-Hartshorne & Jacob, 2004), executive function, and self-monitored behavior (Hartshorne et al., 2007). In addition, age of walking was significantly correlated with age of crawling and walking ability which would fit the conceptual models of Seefeldt (1980) and Clark and Metcalfe (2002), indicating the significance of motor development occurring as a sequential and additive process. These findings also indicate that it is essential for researchers studying motor development to determine the potential effect of a child’s characteristics on motor development (Doralp & Bartlett, 2014).

Many populations have been found to have deficits in balance including children with cerebral palsy (Rosenbaum et al., 2007), developmental coordination disorder (Kane & Barden, 2012), visual impairments (Haibach et al., 2011; Nakata & Yabe, 2001; Ozdemir et al., 2013), and CHARGE syndrome (Haibach & Lieberman, 2013; Hartshorne et al., 2011). Although balance deficits have been found in CWCS, it is important to expand upon these findings through more comprehensive examinations as there are different systems which can affect balance including anticipatory control, reactive postural control, sensory orientation, and dynamic gait (Horak et al., 2009). Anticipatory control requires active movement in which the body systems must anticipate a change in the center of mass such as standing from a seated position or a transition from standing to rising onto toes. Reactive postural control, however, requires the ability to recover from an unexpected external perturbation such as a push from a therapist or positioning the individual in a leaning position and then releasing the individual. These tasks require the ability to make rapid postural changes to avoid a fall. Sensory orientation examines the influence of sensory input such as a change in visual or somatosensory information such as eliminating vision or standing on a compliant surface or incline. Dynamic gait examines balance during gait changes such as directional changes, stair climbing, or stepping over obstacles. Each of these systems play an important role in the maintenance of balance and are not exclusive of one another.

Currently, a differentiation in these systems has not been examined in CWCS. There is only one known study on balance in CWCS, which examined fall risk and self-efficacy of falls (Haibach & Lieberman, 2013). The purpose of this study was to expand upon this research to provide a comprehensive examination of balance to better understand the limitations that CWCS may have regarding anticipatory control, reactive control, sensory orientation, and dynamic gait by examining CWCS in comparison with their peers without CHARGE syndrome. CWCS have sensory and motor impairments that could negatively affect their balance and postural control; thus, it is important to examine balance and developmental needs in this population to be able to provide better interventions and education services. Specifically, the aims of this study are to (1) examine the differential effects of children with and without CHARGE syndrome on these balance systems and (2) examine the association of age of walking to these balance measures.

Method

Participants

We tested balance in 28 CWCS (age: M = 11.00 years, SD = 2.94 years) and 22 typically developing children (age: M = 11.09 years, SD = 2.27 years). Based on parental reports, 17 of the CWCS had profound hearing loss and the other 11 had mild-to-moderate hearing loss in one or both ears. With respect to visual impairment, 3 of the CWCS were classified as B1, 1 was classified as B2, 10 were classified as B3, and 14 were classified as B4 in one or both eyes. In addition, 20 of the CWCS were missing their semicircular canals and 18 had malformed semicircular canals. CWCS mean height was 50.59 in (SD = 7.22 in) and weight was 66.44 lbs (SD = 22.99 lbs); 14 were male and 14 were female. The typically developing children mean height was 59.95 in (SD = 5.65 in) and mean weight was 107.25 lbs (SD = 36.49 lbs); 14 were male and 7 were female. To participate in the study, the CWCS had to meet the following inclusion criteria: have CHARGE syndrome, be between 7 and 17 years of age, and be able to ambulate independently (i.e., without any supportive devices, such as walkers).

Procedure

Participants with CHARGE syndrome were tested in a large conference hall at an international CHARGE syndrome conference, and typically developing children were assessed at the lead investigator’s institution following the assessments of CWCS to age and gender match the groups.

Prior to conducting research, all participants signed assent forms and parents signed informed consent forms, which were approved by the lead investigator’s Institutional Review Board committee. Participants were informed prior to beginning the assessments that they had the option to withdraw at any time. One participant dropped out of the study following consent due to their inability to complete the study. Due to the fact that many CWCS are hard-of-hearing or deaf, the four researchers involved had to have unique qualifications including specialties in adapted physical education, motor development, and postural control assessments. It was also important that the researchers had experience working with children who are deafblind and CWCS as well as the ability to sign.

Before any data were collected, the researchers had some time to get to know the communication, level of vision, and attention span of each participant. An interpreter was provided for participants who used sign language and support from parents was provided when necessary in receptive and expressive communication for participants who used gestures and body language. This protocol was undertaken with communication guidelines from the early work of Salem-Hartshorne and Jacobs (2004). In cases where the child had a very short attention span or had any behavioral needs, the parents were available for questions or to help with motivation. Every child was tested in their preferred mode of communication. In any instance where it was not clear if the child understood the directions, they were given another opportunity to execute the test item.

Assessment

A parent of each child completed a demographic survey, which included a parental report of their child’s age (years), height (inches), weight (pounds), and age at independent walking (months). Parents of CWCS also answered additional questions regarding their child’s CHARGE syndrome characteristics, which included information pertaining to their child’s visual impairment (open-ended), visual acuity (B1–B4), hearing loss (normal, slight, mild, moderate, moderately severe, severe, profound), semicircular canals (fully developed, partially formed, missing), choanal atresia (yes/no, open-ended description), heart defects (open-ended), and growth/development restrictions (open-ended).

To assess balance, the shortened version of the Balance Evaluation Systems Test was used. The balance assessments were live coded by a trained researcher in the BESTest who also has 20 years of experience in postural assessments. The test includes 14 assessment measures. The assessments are categorized into four categories including anticipatory control (sit to stand, rise to toes, and stand on one leg), reactive postural control (compensatory stepping correction- forward, backward, and lateral), sensory orientation (standing feet together, eyes open and eyes closed, and incline eyes closed), and dynamic gait (change in gait speed, walk with head turns, walk with pivot turns, step over obstacles, and time up and go with dual task). To complete the mini-BESTest, the following equipments were needed: a 4-in-thick foam mat, chair without armrest or wheels, an incline ramp, a 9-in box, and a stopwatch. Scoring was conducted as described in the protocol by Franchignoni and colleagues (2010). Each assessment was scored between 0 and 2 points with a maximum total score of 28 points. A score of “0” indicates lowest level of function for each assessment and a score of “2” would indicate the highest level of function. The mini-BESTest has been found to have high internal consistency with Cronbach’s alpha coefficient values above .85. It also has high sensitivity and specificity for people without a history of falls (Padgett et al., 2012). The mini-BESTest has been found to have excellent reliability for real-time scores in children aged 7 to 17 years (interclass correlation [ICC] = .84, 95% CI = [0.72, 0.93]; Dewar et al., 2017).

Data analyses

All participant data were transferred from the protocol sheets to SPSS Version 24. The data were stored anonymously and the protocol sheets were destroyed. The participant who dropped out of the study was excluded from the analysis. Descriptive statistics were conducted for all of the balance measures in the mini-BESTest and age of independent walking. Correlation analyses were then conducted using Pearson’s partial correlations for each variable, controlling for age and gender. Correlations of less than .3 signify low associations, .3 to .5 moderate associations, and more than .6 strong associations (Hahs-Vaughn & Lomax, 2013). Finally, Mann–Whitney’s U-test and an independent samples t-test were used to examine the differences in balance measures and age of independent walking, respectively, between the CWCS and the typically developing children. All statistical tests were set at an alpha level of .05.

Results

Results from the correlation analysis are located in Table 1. All balance measures had strong positive relationships with each other (r = .66 to .83, p < .001) and strong negative relationships with age of independent walking (r = −.60 to −.71, p < .001). Descriptive statistics and results from Mann–Whitney’s U-test can be found in Table 2. The analysis revealed significant group differences for all balance measures (p < .001), wherein the typically developing children outperformed the CWCS on all balance measures with the largest difference occurring in anticipatory control. A significant group difference was also found for age of independent walking, F(46) = 13.71, p = .001, with the typically developing children walking significantly earlier than the CWCS. On average, the CWCS were able to walk independently at 44.4 months (SD = 23.6 months), while the typically developing children were able to walk independently at 12.8 months (SD = 3.3 months).

Table 1.

Correlations between balance measures and age at walking.

	WalkAge	Anticipatory	Reactive	Sensory	Dynamic
WalkAge	1.00	−.69*	−.69*	−.71*	−.60*
Anticipatory		1.00	.69*	.75*	.83*
Reactive			1.00	.68*	.66*
Sensory				1.00	.73*
Dynamic					1.00

p < .001.

Table 2.

Comparison of balance scores between children with and without CHARGE syndrome.

	CHARGE (N = 27)		Controls (N = 22)		Z	p	R
	Median	Range	Median	Range	Z	p	R
Anticipatory control	4.00	1.00–6.00	6.00	5.00–6.00	−5.96	<.000	.85
Reactive postural control	4.00	0.00–6.00	6.00	2.00–6.00	−3.89	<.000	.56
Sensory orientation	5.00	0.00–6.00	6.00	6.00–6.00	−4.07	<.000	.58
Dynamic gait	8.00	1.00–10.00	10.00	8.00–10.00	−3.94	<.000	.56

Discussion

The results of this study provided further support that CWCS develop significantly behind their typically developing peers in age of independent walking and balance (Dammeyer, 2012; Haibach et al., 2011; Hartshorne et al., 2011). This study extended these studies by examining balance systems, anticipatory control, reactive postural control, sensory orientation, and dynamic gait, finding significant delays in each balance system. It is important to note that there was variation across scores in each balance system assessed and overall balance scores. Perhaps, most importantly, the balance scores were associated with age of independent walking indicating the developmental progression illustrated in Seefeldt’s conceptual model (Seefeldt, 1980). CWCS walked more than three times later than their typically developing peers. Children who walked earlier performed better on balance assessments than children who walked later.

Although CWCS performed significantly poorer on all balance systems, it should be noted that the most significant difference from their typically developing peers was with anticipatory control. Anticipatory control requires active body movements in anticipation of balance-related adjustments that happen in preparation for the expected changes of forces during motion (Rabbani et al., 2014). Possessing adequate anticipatory control will thus minimize the danger of losing equilibrium (Horak et al., 2009). Everyday movements such as standing from a seated position and locomotion require adequate anticipatory control. When there is a lack of anticipatory control, it is further difficult to move up the mountain of motor development (Clark & Metcalfe, 2002) to more challenging skills such as fundamental motor skills and sport-specific skills.

The deficits in the all systems of balance, which were all associated with delayed independent walking, places CWCS at potential risk for limited involvement in fundamental motor skills such as running, jumping, throwing, and kicking as proposed by Seefeldt’s (1980) conceptual model of a proficiency barrier for the development of fundamental motor skills. In order to attain independent walking, the body must be developed to support the body in an upright position through the use of posture, balance, and strength (Thelen, 1986). Children without physical or cognitive impairments are able to make continuous subconscious body adjustments to maintain upright posture while moving (Delorme et al., 1989). This ability to make adjustments is particularly important when learning new motor skills which is likely why deficits in motor skill performance have been found in children who are blind (Wagner et al., 2013) and CWCS (Haibach-Beach et al., 2019).

Limitations

Despite these clear findings, there were several limitations to this study. CWCS often have challenges with clear communication. We tried to minimize communication barriers using three researchers who were fluent in sign language and utilizing parent input when necessary. Another limitation was that our participants only came from the pool of CWCS who participated in the international CHARGE syndrome conference. This may have biased the pool to children who come from families who have higher incomes and/or who are resourceful. In addition, only participants who could independently walk were able to participate. This limits 20% of the CHARGE population, and therefore, cannot generalize to all CWCS. It should also be noted that age of walking was parental report which potentially limits the accuracy of the age of independent walking data. Finally, some CWCS have difficulty maintaining focus for prolonged periods of time. The balance test included 14 assessments, some of which require maintaining a static position for up to 30 s. Keeping the participants’ attention and motivation for the entire testing period was often difficult with breaks in between to ensure valid results.

Implications for early intervention professionals and parents

Balance is foundational for motor milestones as well as fundamental motor skills. This study found an association of age of walking with balance revealing the sequential and progressive importance of acquiring motor milestones early as illustrated in the Seefeldt’s (1980) conceptual model and Clark and Metcalfe’s (2002) mountain of motor development. These models indicate that a lack of balance and postural control can have a profound effect in later development of fundamental motor skills and beyond. Lower motor competence can have a detrimental effect on children’s involvement in recess, physical education, and community sports and recreation (Stodden et al., 2008) which can continue throughout adolescence and adulthood (Babic et al., 2014; Westcott & Burtner, 2004) and may also affect their socialization, recreation, and self-determination (Lieberman et al., 2013).

The findings of this study revealed the critical need for early intervention services focusing on balance with the goal of improving motor skill development such as developing independent walking at an earlier age in CWCS. Although deficits were found in all balance systems assessed within this current research investigation, it is important to assess each CWCS on balance and focus early intervention on assessment results and the unique needs of the child as determined by the Individual Education Program team. Because many balance difficulties in CWCS are due to missing semicircular canals and anomalies in the cerebellum, practitioners should also focus on developing compensatory strategies.

Early intervention should promote early development of motor milestones such as walking and once independent walking has been established, CWCS should challenge their walking capabilities on various terrains and surfaces, running, climbing, swinging, and engaging in physical activities with same-age peers (Lieberman & MacVicar, 2003). Balance activities can be modified to allow for sensory adaptations as well as varying levels of complexity such as using exercise balls, stepping stones, sound sources, or bright colored tape. This will provide CWCS opportunities for success and continual challenge. For more specific balance-related skills, please see Foster et al. (in press).

Conclusion

Age of independent walking was associated with balance in CWCS, indicating the foundational importance of motor milestones with subsequent motor development. The CWCS performed significantly behind on all balance systems assessed and walked significantly later than their typically developing peers. The largest differences between the two groups were found in anticipatory control. These deficits can put these children in danger of a lifetime of limited physical activity which can compromise quality of life. Future research should be conducted on the benefits of early intervention programs on compensatory strategies and the development of motor milestones in CWCS. With intentional early intervention programs targeting balance and fundamental motor skills with their typically developing peers, CWCS may be able to reach their full potential in balance and in life.

Footnotes

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) received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Pamela Haibach-Beach

Lauren Lieberman

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