Angulo-Barroso, Rosa M. PhD; Tiernan, Chad W. MS; Chen, Li-Chiou PT, PhD; Ulrich, Dale PhD; Neary, Heather BS
Cerebral palsy (CP) has an incidence of 2 to 3 cases per 1000 live births in the United States, making it one of the leading causes of childhood disability.1–3 CP describes a group of permanent disorders of posture and movement development that hinder activity and result from nonprogressive brain disturbances of perinatal origin.1,4,5 These disorders are often associated with premature birth, low birth weight, and nonprogressive brain lesions, such as periventricular leukomalacia and intraventricular hemorrhages1–6 that may lead to activity limitation. With the exception of severe cases, a diagnosis of CP is usually not made before the child's first birthday.7 Infants with perinatal histories significant for prematurity, low birth weight, and certain brain abnormalities therefore, are commonly classified as being at risk for neuromotor delay (ND), some of whom may not receive a diagnosis of CP. Infants at risk for ND often experience problems with early motor behaviors due to brain abnormalities that result in reduced movement repertoires and difficulties selecting efficient neural activation patterns.8 These early movement abnormalities may affect functional motor skill development and overall activity.
Children with CP have deficits pertaining to walking and general physical activity (PA). For example, it is well documented that children with CP often demonstrate locomotor difficulties.9–14 Tremendous effort has been put forth by researchers to improve the quality of gait and functional ambulation in this population, using techniques such as partial body weight–supported treadmill (TM) training. Recent studies have been successful in demonstrating the feasibility of such training9 and improving ambulatory capability in children with CP using this intervention.10–14 Little is known, however, regarding the effect of such training in infants at risk for ND. In a case report, Bodkin et al15 trained an infant born preterm with a grade III intraventricular hemorrhage on the TM and concluded that such training may facilitate proper foot placement during stepping. However, before partial body weight–supported TM training can be widely implemented, we argue that it is important to first understand how infants at risk for ND respond to the TM up to the point of walking onset. Davis et al16 took an important first step toward addressing these concerns by examining on the TM what they considered to be infants at low risk who were born preterm at 1, 6, and 9 months of corrected age. In their study, only infants born preterm who were believed to have favorable developmental outcomes based on head circumference were included. Infants with various brain insults (ie, intraventricular hemorrhages) were excluded from the study. The authors found that infants at all ages were capable of producing alternating steps (AltStp).
We believe that additional research using the TM is warranted. To date, no study has looked at the development of TM stepping up to the point of walking onset in infants at risk for ND, including infants with varying degrees of prognosis for independent ambulation. Similarly, research is also needed to describe the general activity levels in this population. Evidence suggests that individuals with CP and infants born preterm with low birth weight are less active during childhood than peers who are unaffected.17,18 Little is known, however, regarding the activity levels of infants at risk for ND. Furthermore, research is also needed to examine the functional relevance of early TM stepping and PA. For example, is PA in infants at risk for ND related to their walking onset? Interestingly, research from our laboratory involving infants with Down syndrome suggests that higher levels of PA are associated with earlier walking onset.19
This study was conducted to provide a greater understanding of TM step performance and PA in infants at risk for ND without training manipulation. Our primary objective was to describe the developmental trajectories of both TM response and PA within this population. In addition, we explored whether stepping and PA profiles were related to age of walking onset. Finally, we assessed potential differences in stepping performance and PA patterns in infants with and without a CP diagnosis.
A convenience sample of 19 infants at risk for ND was recruited from the University of Michigan Hospital. Four participants were dropped from the study due to family relocation (2 infants) and parent voluntary withdrawal (2 infants), resulting in a final sample of 15 infants (8 males). Infants were referred to our study from pediatric physicians conducting a high-risk clinic. The physicians considered neuroimaging results and assessed neuromotor characteristics (eg, muscle tone, reflexes, and motor development) at 4 and/or 8 months of corrected age follow-up clinic visits to determine which infants were at risk for ND. Our inclusion criteria consisted of having risk for ND (as determined by a physician), being at least 6 months of corrected age, and possessing the ability to take 6 TM steps of any type within a minute. Previous evidence defines 6 months to be an age when infants with typical development (TD) or prematurity at low risk respond well to the TM.16 Exclusion criteria included other neuromotor or genetic abnormalities (eg, spina bifida, Down syndrome), severe hypotonia, musculoskeletal difficulties limiting participation (eg, developmental dysplasia of the hip), severe opisthotonic posturing, and uncontrolled seizure disorder (a controlled seizure was defined as one in which there had not been the need to change medication dose for at least 8 weeks).
Exit criteria included walking onset or reaching 24 months of corrected age (whichever occurred first). Walking onset was defined as the ability to take 3 independent steps over ground. Six of the 15 infants received a CP diagnosis during the course of the study or within 1 year of study completion. Procedures of the study were approved by the Internal Review Board at the University of Michigan. All participating families were required to sign informed consent forms before initiation of the study.
Infants needed to take 6 TM steps within a 1-minute trial before they were able to enter the study. In some cases, it took multiple pre-testing sessions for the infant to reach the entry stepping criterion. If the entry criterion was not reached at the pretest visit, we went back to the infants' homes once a month until the infant took the required number of steps. After entry conditions were satisfied, we went to the infants' homes once every 2 months until an exit criterion was met. Each testing session consisted of 5 minutes of partial body weight–supported stepping on a small motorized TM. Infants were held on the TM by one of the trained researchers. The belt speed was set at 0.20 m/sec for each of the sessions. Researchers determined how many consecutive minutes the infant stepped before taking a break. This decision was based primarily on the infant's status and temperament. The breaks lasted 1 to 2 minutes. Participants generally stepped for 1- or 2-minute intervals during the 5-minute sessions, depending on how quickly they tired or became fussy. Stepping was videotaped during each session and subsequently coded on a frame-by-frame basis (60 frames per second) to determine foot placement and alternating step frequencies. In addition to TM performance, we also monitored the infants' activity levels. An activity monitor (Actiwatch, Respironics/Mini Mitter Company, Bend, OR) was used to measure PA at each visit. The activity monitor was placed on the right side of the trunk, just above the iliac crest, to assess overall body movement. The device was programmed to record movement for 24 hours.
At study entry and exit, we assessed motor development using the Gross Motor Function Measure (GMFM)-8820 and spasticity via the Modified Ashworth Scale (MAS).21 Because we were not interested in examining any movement asymmetries in this study, global spasticity scores were used. Total body Ashworth scores were computed by summing the bilateral upper and lower extremity scores. A single, trained researcher administered both the GMFM and MAS as these assessments were only used to describe the population at entry into and exit from the study. We acknowledge that one must be cautious in interpreting our GMFM and MAS data, because these measures have not been validated specifically for the population in this study as far as we know. Finally, we recorded the age of independent walking onset. Participants' families were called at 12 months post-study (up to 36 months of corrected age in some cases) to update walking and diagnostic status. All infants continued to receive any therapies prescribed by their physician throughout the duration of the study.
TM variables of interest were the frequency of AltStp and percentage of toe contacts (TCs). The total number of steps for each of the 5-minute sessions was recorded. Steps were coded as alternating (step of one leg followed by step of the other leg), single (step of one leg not followed by another of the other leg), and parallel (both legs move forward together). AltStp per minute was calculated for each session per infant. For every step, we determined the foot placement during the stance phase. Foot placement was coded as either toe or flat from a frame-by-frame analysis of the videotapes. Flat contact was defined as having a minimum of half of the foot remaining in contact with the TM surface for a minimum duration of 180 msec (ie, 6 frames). If contact was less than this duration, foot placement was scored as a TC (ie, the forefoot was predominantly in contact, with more than half of the posterior of the foot being off the ground). Percentage of TC per minute was calculated per session for each participant. Interrater and intrarater codings were calculated to be 96.5% and 100% for foot placement and 92.3% and 91.7% for alternating stepping frequency, respectively. Two trained research personnel were responsible for all the step coding.
The PA variables were outcomes of 24 hours of data collection using an Actiwatch, an omnidirectional accelerometer with frequency sampling of 32-Hz and 15-second epoch length. Activity data were downloaded onto a computer and coded to separate day/night and awake/sleep. Only data obtained during the day when the child was awake were considered in analysis. For details determining day and awake categories, see Angulo-Barroso et al.22 For each bimonthly assessment, a single frequency distribution of day/awake data including all available participants was generated to classify intensity of movement. The lower 70% of data was considered to be low activity, whereas the upper 30% was classified as high activity, resulting in a bimonthly movement threshold. The average of the bimonthly thresholds yielded a value of 66.19 movement units/15 sec, and it was used to separate low versus high activity across all time points and participants. This 70/30 intensity ratio has been used in similar studies with infants with and without Down syndrome.19,22 Duration (Durhigh and Durlow), amplitude (Amphigh and Amplow), and product (Prodhigh and Prodlow) were calculated separately for the high and low activity categories. Product was determined by multiplying the time spent in high or low activity (duration) by the amount of activity (amplitude).
For infants' characteristics including birth weight, gestational age, entry and exit GMFM, and Ashworth scores, t tests and nonparametric tests were used to examine group differences between infants with and without CP. To assess developmental change, repeated-measures analysis of variance was used to examine the effect of corrected age on stepping and PA variables in all infants from 8 to 24 months. Statistically, a sample of 2 in a developmental trajectory analysis does not add any information, especially when such a small sample belongs to one subgroup. Therefore, the 2 infants at 6 months of corrected age were removed from these analyses. To determine whether group differences (CP versus no CP) existed for these variables, 2-way (age × group) repeated-measures analysis of variance was used. In the latter analyses, only data from 10 to 18 months were used because insufficient sample existed outside this range. Appropriate post hoc comparisons with Bonferroni adjustment were performed on any significant age effect or age × group interactions. Finally, Pearson correlation was applied to examine the relationship of walking onset age with infants' PA and their stepping performance on the TM from 10 to 18 months. All statistical analyses were performed with the Statistical Analysis Software (SAS) program (Release version 9.1, SAS Institute Inc, Cary, NC). A p value <0.05 was defined as statistically significant.
Although the group of infants with CP compared with infants without CP had comparable birth body weights and gestational ages (both p > 0.05), they showed significant differences in the GMFM and Ashworth scores at entry and exit of the study (all p < 0.05). Infants with CP demonstrated lower GMFM and higher Ashworth scores than those with no CP. All 9 infants without CP achieved independent walking by 18 months. Only 1 of 6 infants with CP, however, was able to walk (onset 22 months) by the end of the follow-up period, ie, 36 months of age (Table 1).
TM Performance and PA
All Infants (8–24 Months).
Examining the developmental changes of stepping performance in all infants from 8 to 24 months of corrected age, our results revealed significant increases in AltStp and decreases in percent TC with increasing age. Post hoc comparison revealed that TM performance was significantly different between the earlier and later months. That is, between 8 to 10 months and 14 to 24 months AltStp increased and between 8 to 14 and 22 to 24 months percent TC decreased (all adjusted p < 0.05).
For those with high-level PA, our results showed significant age effects in Prodhigh and Amphigh (both p < 0.05) but no age-related changes in Durhigh (p > 0.05). For the measures of low-level PA, significant age effect was only found in Amplow (p < 0.05) but not in Prodlow or Durlow (both p > 0.05). Post hoc comparisons revealed that infants showed higher Prodhigh and Amphigh but lower Amplow at 18 months than they did at 8 to 12 months (all adjusted p < 0.05).
Infants with and without CP (10–18 Months).
Figures 1 and 2 present the developmental profiles of stepping performance on the TM and PA in infants with or without CP. When comparing the 2 groups of infants (CP versus no CP) from 10 to 18 months, our results revealed significant main effects of group and age with no age × group interactions in their stepping performance. Infants with CP showed fewer AltStp and higher percent TC than those without CP (both p < 0.05). For their PA, infants without CP showed higher level PA, as revealed by higher Prodhigh, Amphigh, and Durhigh, than those with CP (all p < 0.05). A significant age × group interaction was also found for Amphigh, and post hoc comparisons revealed that infants without CP, but not those with CP, showed higher Amphigh as they became older (adjusted p < 0.05). For low PA, Amplow became significantly lower with increasing age (p < 0.05), although this is not shown clearly in Figure 2e. Meanwhile Prodlow and Durlow showed significant group effect and age by group interactions (both p < 0.05). Although not shown clearly in Figure 2d, further analysis revealed that Prodlow was higher at 18 months than at 12 months only in infants without CP but not those with CP. From 10 to 14 months of corrected age, infants without CP spent more time in low PA than those with CP (all adjusted p < 0.05).
Walking Onset (Before 36 Months) Versus Early Motor Activities (10–18 Months)
Analysis of the relationships between walking onset and early motor activities from 10 to18 months included all infants without a diagnosis of CP and one infant with CP (none of the others walked by the end of our follow-up period at 36 months). Our results revealed significant correlations between infants' ages at walking onset and AltStp at 14 and 16 months (both p < 0.05), and the same trend was observed at 10 and 12 months (both p < 0.07). The more AltStp that infants performed during 10 to 16 months of age, the earlier they achieved independent walking. Although higher Amphigh at 10 and 14 months significantly correlated with earlier walking onset, higher Amplow at 18 months showed correlations to later walking onset (all p < 0.05). Across the investigated period, infants' early motor activities at 10 months of corrected age seemed to best correlate with their ages at walking onset as significant correlations or trends were found in AltStp, Amphigh, Prodhigh, Durlow, and Prodlow (Table 2).
The data presented in this article describe the developmental trajectories of preindependent locomotion TM stepping responses and levels of PA of infants at risk for ND. In addition, relationships between early motor performance and walking onset were explored. When examining the sample as a whole, the frequency of TM AltStp and higher intensity PA increased, whereas the percent TC decreased with developmental time. However, the developmental trajectories for TM stepping and PA were delayed and diminished in the group of infants who received a diagnosis of CP compared with those infants who started with an at risk status but ended up without a diagnosis of CP. The group differences in trajectories may be important given our observation that aspects of TM stepping and PA are possibly associated with the onset of independent walking. Although group differences in both Ashworth and GMFM scores at entry and exit were found, these results should be interpreted with caution given the concerns regarding validity, reliability of the Ashworth, and GMFM assessments in this population.
It is well known that infants with TD increase the number of steps taken on a TM as they develop.23 Previous research has also demonstrated the natural progression in TM stepping from 1 to 9 months of age in infants born preterm but at low risk for ND.16 Our results support a similar stepping progression in older infants and those at higher risk for ND. A more interesting question from a clinical standpoint is the performance of those infants with a transient ND versus those who receive a diagnosis of CP. The results of this study showed significant group differences in both frequency of AltStp and percent TCs, with the infants who received a diagnosis of CP producing less AltStp and higher percent TCs. Despite these discrepancies, the developmental trajectories of both groups for both stepping variables showed similar ascending or descending patterns. We argue that this may suggest a developmental delay as opposed to a developmental incapacity regarding TM stepping in those infants with CP, given the infants' abilities to both increase steps and improve foot placement over developmental time without training.
Although the preceding results are encouraging, we recognize that TM stepping represents a very small portion of overall motor performance. It was also important to examine PA in all infants (8–24 months of age) at risk for ND. Our results demonstrated that levels of high PA increased with developmental time, whereas low PA was maintained at the same level. After closer examination, we were able to determine that improvements in high activity were primarily due to increases in the amplitude of high activity as opposed to the amount of time spent in high activity. In fact, the durations of time spent in both high and low activity did not change within the developmental window studied (8–24 months). These results are consistent with those of Tennefors et al,24 who found that at both 9 and 14 months, the amount of time that infants with TD were active remained fairly constant. The amplitude and duration findings suggest that infants at risk for ND produce more movements in a given unit of time as they develop (ie, increases in amplitude of high PA), allowing them more potential opportunities to explore their own actions and surrounding environment as they develop.
When we examined PA levels by group from 10 to 18 months, we found that activity between the 2 groups differed and largely favored the group without CP. For instance, the infants with CP demonstrated less high activity and showed flatter activity profiles from 10 to 18 months relative to their peers without a diagnosis of CP. The collective and group results for TM stepping and PA have 2 important implications. First, the observed stepping and PA deficiencies in the CP group suggest the need for a focused intervention that could improve both task-specific performance relevant to functional motor skills (ie, TM stepping) and overall PA. Second, the TM stepping and activity profiles during 10 to 18 months may provide some insights into future delays in walking onset in infants at risk for ND, if indeed the association that we observed between TM stepping/activity and onset of independent locomotion can be replicated with a larger sample in future studies.
TM responses may have a functional relevance due to the suggestive relationship found between the frequency of AltStp and the onset of independent walking at 10 to 16 months of age. In other words, it seems that the capacity of an infant to produce AltStp in a partial body weight– supported TM condition is related to how early the infant will start to walk independently. However, this result should be interpreted with caution because the sample is small (N = 10) and all but one of the infants in this analysis did not receive a diagnosis of CP. Despite this limited generalization, previous research in a population of infants with Down syndrome suggests the benefit of a TM intervention for onset and quality of independent walking25–28 as well a significant relationship between frequency of alternating TM steps and onset of walking. Whether these relationships would hold in a population of infants with CP is not known and warrants further investigation.
We interpret the lack of significant relationships between TCs and onset of independent walking by suggesting that foot placement on the TM may be more relevant to the quality of gait rather than the onset of walking. If this were to be true, it may be important to gradually implement a TM intervention that would initially focus on the frequency of stepping but later incorporate proper foot placement to promote both walking onset and efficient gait patterns. In fact, rehabilitation protocols for stroke recovery often use TM training with the aid of functional stimulation to facilitate proper foot placement during the step cycle.29,30 Similarly, robot-assisted locomotor training in children with central gait impairments was been used to ensure better gait patterns, including foot placement.31
This study also offers a first glance at the possible associations between PA levels and onset of walking in a population of infants at risk for ND. Our results support negative correlations between high levels of PA and onset of independent walking, and positive correlations between low PA and independent walking; that is, the onset of walking tends to occur earlier if low PA is less and high PA is greater early in development. Our results are only consistent at 10 months of age when our sample is the largest and all but one of the infants included in the analysis were at risk for ND but did not receive a diagnosis of CP. Therefore, one must be cautious about the generalization of these results to those infants with CP. Nevertheless, it is reasonable to believe that early PA may be important to subsequent motor milestone development. We recently found that levels of PA in infants with Down syndrome are related to the onset of walking in such a way that, early in development, more time in low activity correlates with later walking onset, whereas more high activity is associated with earlier onset of walking.19,32 Furthermore, recent studies in children with CP point to significant functional implications (ie, biomechanical efficiency) for levels of PA in the economy of gait.33
Collectively, results from this study suggest that infants at risk for ND spontaneously improve their TM response during a prewalking developmental window. In addition, it seems that their stepping frequency may be related to the onset of walking. This study, however, did not examine the effect of individual risk factors such as prematurity, low birth weight, or specific brain injuries on our outcomes. Despite the existing evidence relating prematurity and low birth weight to increased risk for CP,5 neither of these 2 factors seemed to be associated with poor TM responses or the diagnosis of CP in our study. For example, 2 infants without a CP diagnosis having similar birth weights, and both being born preterm, showed very different TM responses. In a second case, 2 infants were both born approximately 3 months early with similar low birth weights (<1000 g). Although their TM responses were analogous, one was diagnosed of CP, whereas the other was not.
In our sample, some infants received a diagnosis of CP and TM responses differed by group. However, we believe that the results are encouraging for 2 reasons. First, even those infants considered at risk for ND who received a diagnosis of CP were able to increase their AltStp during the course of the study. Second, their percent TCs decreased with time, providing a naturally occurring window of intervention. Therefore, it would be reasonable to propose that the developmental stepping profiles in infants at risk for ND could be shifted toward typical patterns through task-specific practice via a TM training intervention. Although we consider this work to be an important first step in the consideration of TM training in this population, it remains unclear what effect such an intervention might have on infants at risk for ND. Richards et al9 demonstrated that TM training is in fact feasible in a population of slightly older and more severely involved children. In addition, previous research demonstrated that TM training benefits in older children with CP10–12,14 and in a case report involving an infant at risk for ND.15 Unfortunately, in the case report, the TM intervention was stopped before the onset of independent walking. The authors reported that the number of TCs increased with the cessation of TM practice.15 Indirectly, this suggests to us that the TM intervention, if nothing else, may have the positive effect of reducing TCs in TM stepping in infants at risk for ND. However, further research is necessary to support this claim.
We believe that the results from this study in conjunction with previous findings warrants future research examining the effects of TM training in infants at risk for ND. However, we propose that researchers proceed cautiously and start with a moderately affected group using a moderate level of TM intensity because there are still many unknowns regarding the implementation of this type of therapy in young infants with high levels of risk for ND. Future studies should explore the effect of TM training on task-relevant variables, such as step response, walking onset, and quality of gait, in addition to generalized activity. Although it remains unclear whether TM training in this population would directly affect PA, our Down syndrome studies suggest the importance of high-intensity activity in infancy for motor milestone achievement. In addition to locomotor-related benefits, TM training may be a plausible means to achieve more intense activity early in development.
The authors thank the participants and their families, the local hospitals, Drs Gahagan, Carlson, Ayyangar, Solomon, and all the people who helped with participant recruitment, data collection, and data analysis.
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