Step Types Produced
Both the younger and older age groups generated all 4 types of stepping patterns (Figures 4A and B). However, for younger infants, the predominant step type was single, followed by parallel, alternating, and double. With age, alternating steps more than doubled in percentage of all steps, as did parallel steps, while single steps reduced by half and double steps nearly disappeared.
Part 2: Context Effect on Step Frequency, Temporal Parameters, and LAR
Because there were, particularly for the younger infants, only a small number of steps in each of the 4 step categories for each of the conditions, we pooled the step types together to increase the power of subsequent statistical tests.
Absolute Step Rate
To examine the effect of age, lesion level, and conditions on total steps produced, we used a 2 (age) × 3 (lesion) × 6 (condition) ANOVA for repeated measures on condition. We found a significant age effect (F 1,23 = 6.76, P = .016), a significant lesion level effect (F 2,23 = 3.13, P = .063), a significant condition effect (F 5,115 = 2.38, P = .043), a significant age × condition interaction (F 5,115 = 3.13, P = .011), and a lesion × condition interaction (F 10,115 = 1.99, P = .040). Figure 5 plots step rate by age and condition, within each lesion level, A (low), B (middle), and C (high). These figures illustrate that the significant age × condition effect reflected that while conditions effectively increased step responses over baseline, the level of effect varied by age, showing a greater effect for older infants than younger ones. Furthermore, the effect of conditions presented was different across lesion levels, being greater for low than high lesion levels. For those in the middle-lesion group, no conditions showed clear improvement over baseline, though the age effect could not be examined because our sample included infants aged only 7 to 10 months.
First, to examine more closely the age × conditions interaction, we compared the most effective conditions for younger babies with those of older babies. For younger infants, friction produced the greatest increase in step rate (0.16 steps per second ± 0.18) compared with the baseline condition (0.11 steps per second ± 0.10), although the paired comparison post hoc did not reach statistical significance. For older babies, visual flow elicited the most steps (0.26 steps per second ± 0.23) compared with the baseline condition (0.19 steps per second ± 0.15), but both visual flow and friction achieved statistical significance: visual flow (df = 75, t = −2.37, P = .021) and friction (df = 75, t = −1.92, P = .058) compared with the baseline for the older group.
To examine the lesion level × condition interaction, we began by conducting a post hoc 2 (age) × 6 (condition) ANOVA with repeated measures on condition for the low-level lesion group. We did this because, as Figure 5A illustrates, this subgroup had both the most participants (and thus statistical power) and the largest overall step response. Results showed a significant condition effect (F 5,55 = 2.21, P = .066), age effect (F 1,11 = 5.87, P = .034), and an age × condition interaction (F 5,55 = 2.68, P = .031). Figure 5A suggests that whereas for older infants, all enhanced sensory conditions produced more steps than baseline, for younger infants, only friction seemed to elicit more steps. Post hoc–paired comparison tests among conditions showed statistically significant results for visual flow (df = 60, t = −1.71, P = .092) and friction (df = 60, t = −2.81, P = .007) compared with baseline.
Figure 5B suggests that for infants in the middle lesion level (L4), no enhanced sensory conditions improved their step frequency, though we observed a statistically significant decrease in responses for unloading (df = 25, t = 2.35, P = .027) and weights (df = 25, t = 2.16, P = .041) compared with baseline.
Infants with high-level lesions responded more to friction (0.10 steps per second ± 0.05) compared with the baseline (0.09 steps per second ± 0.05), though visual flow also showed a slightly higher mean response compared with the baseline for only the older infants. However, these changes did not achieve statistical significance.
Normalized Step Rate
The variability in mean step rate across infants was high, ranging from 0.03 to 0.67 steps per second. Therefore, we normalized step rates for each infant to his/her own mean (across conditions). Normalized responses (see Figure 6) show more clearly that, generally, visual flow and friction were the conditions most effective in eliciting steps when infants with MMC were supported on a pediatric treadmill. We plotted normalized responses as a function of age and lesion level. For the youngest infants, only friction increased step rate over baseline. For those with middle-level lesions, no conditions significantly increased step response compared with baseline; unloading and weights, in particular, significantly reduced step responses.
Step Cycle Effects
To determine the effect of conditions on step cycle duration, we used a 2 (age) × 3 (lesion) × 6 (condition) ANOVA, with repeated measures on condition. Cycle duration, normalized to leg length, was the dependent variable. We found significant age (F 1,6 = 6.77, P = .041) and condition (F 5,15 = 4.83 P = .008) effects. Figure 7 shows that, with age, normalized cycle durations reduced across all conditions. The absolute cycle were higher in infants with longer legs, and they demonstrated increased strength; when normalized to leg length, the cycle duration decreased. The effect of condition was less clear-cut, though overall, Velcro tended to increase cycle duration, while unloading tended to decrease cycle duration. A 2 (age) × 3 (lesion) × 6 (condition) ANOVA with repeated measures on condition for swing- and stance-phase durations resulted in statistically significant effects for stance-phase durations for condition (F 5,15 = 3.65 P = .023).
Figure 8 illustrates the very-high variability across infants in LAR to all conditions and across age groups and lesion levels. When tested in a 2 (age) × 3 (lesion) × 6 (condition) ANOVA for repeated measures on condition with LAR as the dependent variable, we obtained only a significant age effect (F 1,23 = 4.35, P = .048). Older infants produced more leg activity when not stepping than younger infants. Nevertheless, the comparison to Figure 5 shows some parallels that may guide selection of conditions that elicit maximal action. For example, Figure 8A suggests that for older infants with low-level lesions, visual flow and friction seem to work better than baseline. For young infants, this effect is limited to friction. All conditions reduced the response compared with baseline for infants with middle-level lesions, with unloading and weights showing the most marked effects. For infants with high-level lesions, in both age groups, little improvement was evident across enhanced sensory conditions, though notably, none of these conditions appeared to reduce leg activity compared with baseline. We found for the infant group as a whole that the condition of unloading decreased LAR from 5.88 per seconds ± 6.40 at baseline to 3.65 per seconds ± 3.79. However, no condition produced a marked increase in LAR.
Our purpose in this experiment was to determine whether we could enable infants with MMC to increase their step rate when supported on a pediatric treadmill by enhancing the sensory input during test trials over that of typical treadmill belt conditions. Overall, our results show that we can do so, and that of the 5 sensory enhancements we created, friction and visual flow worked optimally to increase step frequency.
We chose to increase friction by covering the treadmill belt with Dycem to avoid a response observed in some infants with MMC in our previous work.31 That is, if they accepted minimal weight on their feet, or foot contact was on the side or ball of the foot, their feet moved backward with the belt only a small amount, and steps were less likely to result. We used Dycem to reduce slippage. In this context, it increased the opportunity for the treadmill dynamics to be effective. When the foot touched down, it created a more stable base for greater weight acceptance on the foot and kept the foot in contact longer. When leg joints and muscles are extended and then unloaded at the end of stance, passive pendular dynamics and viscoelastic muscle properties can assist with forward motion and joint flexion.
Visual flow has been shown by numerous researchers to elicit motor responses in infants.34,42,43 We chose this condition to access a sensory system that was not diminished by the neural tube defect and thus could, and did, facilitate infants' initiation of body movement. However, this condition was less effective for younger babies than for older babies. This might have been because younger babies failed either to “perceive” the motion implied or simply failed to attend to it. Although we did not specifically assess babies' looking time, Moerchen and Saeed44 showed that babies with TD who spent more time looking directly toward the belt in this context, rather than looking away or closing their eyes, stepped more frequently.
Like friction, Velcro also helped to maintain greater foot contact after touchdown, and this was the condition Ulrich et al32 found to be optimal for infants with Down syndrome. The difference here seemed to be the strength required to pull their feet off the belt, which was particularly reduced for young infants with MMC and those with high lesion levels. Similarly, adding weights might have increased proprioceptive input, but these infants simply did not have sufficient strength to overcome this added mass.
In addition, the responses that we observed to friction and visual flow were affected by age and lesion levels. Infants who were in the older group stepped more frequently, and responses increased as group lesion level lowered. In fact, those infants in the older age group with the lowest lesion levels responded more to all enhanced sensory conditions than to baseline. The question remains, why was the effect on younger infants and those with higher lesion levels so small? We propose 2 factors. First, these infants responded to baseline with a low number of steps, a finding that we had demonstrated in a previous study.31 These are the most fragile infants of this population, for whom lifting the legs and stepping may be a particularly difficult and energy-demanding response. Thus, expecting any real-time modification that does not reduce the muscle force demands may be unrealistic. First, more effective may be efforts to increase strength before expecting infants to use their muscles and step. Second, our design allowed infants only 30 seconds to adjust to each new test trial, and we moved fairly quickly from one trial to the next. We did this to avoid tiring infants and allow examination of several enhanced sensory conditions, since all data were collected on a single day. Unfortunately, by doing so, we may not have allowed this inherently unstable response to settle into each new sensory enhancement before the trial ended. Future studies should consider examining the most promising conditions by presenting them for longer periods of time and comparing responses of stronger infants, those who generate more extensor force when supported on the treadmill, with those less able to do so. In addition, more than 37% of our infants presented with bilateral clubfeet. These infants made initial contact with the lateral aspect of the foot in 47.2% of cases, which reduced during mid stance. However, even those infants without clubfeet made initial lateral foot contact in 19.6% of their steps, compared with about 8% lateral foot contact for infants with TD with structurally normal feet. The effect of clubfoot on the posture was to reduce the treadmill surface area in contact with the foot in addition to limiting weight bearing through the lower limbs, with the tester subsequently providing more body weight support. This decrease in sensory enhancement in infants with clubfeet may account for the reduction in number of steps elicited overall in infants with MMC.
Interestingly, in this study, we observed an age effect that was only minimally observed toward the end of the first year in our previous longitudinal study.31 We believe that this occurred because in the previous study, only the baseline condition was used. Here, by increasing the opportunities for sensory input to engage the motor system, greater overall stepping emerged with age.
As a group, infants with middle lesion levels differed in several respects from the pattern shown by the lower and higher lesion level groups. They did not increase step frequency in response to any enhanced sensory input conditions, and step frequency diminished during unloading and weight conditions. We do not have a definitive argument for this divergence, but 1 contributing factor may be the very-small subsample size, coupled with its very-high variability. The middle lesion level group was represented by half as many participants as the other 2 groups and comprised only 6 infants. Individual profiles showed that 3 of the infants in this group showed means for visual flow and friction that were equal to or higher than their baseline means. For only 2 infants in this group did the baseline condition produce the most steps, and for only 1 of them was that number more than 25% higher. Overall, in such a small sample, these less-common response patterns can overwhelm a group mean. A larger sample of infants with an L4 lesion level diagnosis will be needed to examine this subsample behavior more definitively.
We did not observe a significant increase in leg activity beyond steps as a function of enhanced sensory input, although the means for friction and visual flow were a bit higher than other conditions, paralleling the more significant outcomes that we found for step rate under these conditions. Previously, we showed that when infants with MMC were supported upright on a moving belt that was like our baseline belt in this study, infants moved their legs more even when not stepping than they did when supported upright on the treadmill and the belt did not move. The explanation for this lack of increase is not obvious; although perhaps when increased sensory flow reached a sufficient level to stimulate activity, this presented as a patterned motor response, a step, rather than random leg activity.
As we observed previously, the step patterns of infants with MMC produced at younger ages tended to be dominated by single steps and these decreased with age, while the proportion of alternating steps increased with age.31 The amount of increase in alternating steps was less than expected from previous work, to about 20% here and 40% previously. We propose that the increase in response frequency may first come in the form of the simplest patterns, single, or parallel steps and require greater control and practice to more consistently respond with alternating steps.
Our results also showed a negative correlation between PI and step rate for the low- and middle-level lesions. A higher PI indicates increased adipose tissue for body size. Luo et al45 also reported a negative correlation between the number of alternating steps and the percentage of total body fat, as determined by skinfold thickness. Our interpretation for our findings is that infants with increased adipose tissue per body size have more difficulty initiating step cycles, because of the relatively heavier lower limb without concomitantly greater muscle force. For infants with high lesion levels who stepped significantly less, we observed no effects of PI.
We found no statistical relation between infants' step frequency and their scores on the BSID. This may be because the BSID is heavily weighted toward upper limb and trunk motor skills, and thus, may be insufficiently sensitive to neuromotor delays primarily occurring in the lower limbs. Perhaps, a scale such as the Alberta Infant Motor Scale46 would have identified a relation. Alternatively, the capacity for the dynamics of the treadmill to assist and elicit stepping patterns may occur before babies are able independently to create the functional motor patterns of sitting, crawling, and cruising. Previous studies provide limited insights. For example, Thelen and Ulrich47 found no relation between BSID scores and the onset of improved treadmill stepping in infants with TD, whereas Ulrich et al19 found for babies with Down syndrome that specific BSID items were associated with improved treadmill stepping but not an overall score. In future studies, we will investigate this issue further by employing a more sensitive set of items to reflect concurrent levels of lower limb function (skill).
Although our results show that enhancing sensory input can increase motor output and that infants with lower-level lesions and older infants responded to this input more than young infants and the ones with higher lesions; the variability among infants must also be emphasized. Scatterplots and standard deviations illustrate this, as does the very-high variability among infants in step rate. These reflect that behavioral outcomes are influenced by many factors, including other complications due to this neural tube defect, such as clubfeet (reduced contact area), hydrocephalus, or hip subluxation or dislocation, degree of damage to ascending and descending neural tracts, level of medical care and physical therapy, and family support networks.
It is important to note that in the future, the possible use of treadmill practice for early intervention for children with MMC would need to be paired with close monitoring of its effect on muscle imbalance around the hips and knees. Infants and children with MMC, especially those with lumbar lesions, are prone to show muscle imbalances in this region. Thus, careful attention to pelvis, hip, and spine alignment would be critical to avoid the potential development of muscle contracture and bony deformities.
In this study, we presented each enhanced sensory condition for only 30 seconds and moved infants quickly from one context to another. Future studies should examine the effect of longer exposure time to allow infants to adapt to each context. Furthermore, we enrolled only a small number of infants when sorted by age group and lesion levels; the mid-lesion level subgroup included only older infants and half as many in total as the lower and higher lesion level subgroups. Future studies of this nature should increase the sample within subgroups. We utilized the same sensory enhancements for the youngest and oldest infants. Future studies should test whether other modifications to the treadmill context can improve responses for younger infants and those with the highest lesion levels.
Our results showed that when supported upright on a pediatric treadmill, infants with MMC produced more steps when the context was modified to enhanced sensory input compared with the baseline condition of a typical smooth black belt. Generally, friction and visual flow elicited a greater number of steps than other conditions, producing increases of 47% and 20%, respectively, compared with baseline. We observed significant individual variability as well. Future studies should investigate the effect of enhancing sensory input by combining friction and visual flow, with opportunities to practice, thus allowing infants to adapt and, perhaps, settle into more stable response patterns.
We thank the participants and their families for taking part in this study. In addition, we thank the physicians and staff, especially of the University of Michigan Hospital and the Children's Hospital of Michigan Myelomeningocele Care Center at Detroit Medical Centre.
1. Bowman RM, Boshnjaku V, McLone DG. The changing incidence of myelomeningocele and its impact on pediatric neurosurgery: a review from the Children's Memorial Hospital. Child Nerv Syst. 2009;25(7):801–806.
2. Spina bifida fact sheet. In: National Institute of Neurological Disorders and Stroke, ed. NIH Publication No. 07-309. Bethesda, MD: NIH; 2007:886–894.
3. Buffart LM, van den Berg-Emonsrita JG, van Meeteren J, Stam JV, Roebroek M. Lifestyle, participation, and health-related quality of life in adolescents and young adults with myelomeningocele. Dev Med Child Neurol. 2009;51(11):886–894.
4. Sival DA, Begeer JH, Staal-Schreinemachers AL, Vos-Niel JM, Beekhuis JR, Prechtl HF. Perinatal motor behaviour and neurological outcome in spina bifida aperta. Early Hum Dev. 1997;50(1):27–37.
5. Reid GM. Sudden infant death syndrome (SIDS): microgravity and inadequate sensory stimulation. Med Hypotheses. 2006;66(5):920–924.
6. Sival DA, van Weerden TW, Vles JS, et al. Neonatal loss of motor function in human spina bifida aperta. Pediatrics. 2004;114(2):427–434.
7. Iborra J, Pages E, Cuxart A. Neurological abnormalities, major orthopaedic deformities and ambulation analysis in a myelomeningocele population in Catalonia (Spain). Spinal Cord. 1999;37(5):351–357.
8. Williams EN, Broughton NS, Menelaus MB. Age-related walking in children with spina bifida. Dev Med Child Neurol. 1999;41(7):446–449.
9. Bartonek Á, Gutierrez EM, Haglund-Ákerlind Y, Saraste H. The influence of spasticity in the lower limb muscles on gait pattern in children with sacral to mid-lumbar myelomeningocele: a gait analysis study. Gait Posture. 2005;22(1):10–25.
10. Bartonek A, Saraste H. Factors influencing ambulation in myelomeningocele: a cross-sectional study. Dev Med Child Neurol. 2001;43(4):253–260.
11. Gutierrez EM, Bartonek Á, Haglund-Ákerlind Y, Saraste H. Characteristic gait kinematics in persons with lumbosacral myelomeningocele. Gait Posture. 2003;18(3):170–177.
12. Schoenmakers MA, de Groot JF, Gorter JW, Hillaert JL, Helders PJ, Takken T. Muscle strength, aerobic capacity and physical activity in independent ambulating children with lumbosacral spina bifida. Disabil Rehabil. 2009;31(4):259–266.
13. Moore CABS, Nejad BBA, Novak RAMS, Dias LSMD. Energy cost of walking in low lumbar myelomeningocele. J Pediatr Orthoped. 2001;21(3):388–391.
14. Asher M, Olson J. Factors affecting the ambulatory status of patients with spina bifida cystica. J Bone Joint Surg. 1983;65(3):533–539.
15. Morrison KM, Atkinson SA, Yusuf S, et al. The Family Atherosclerosis Monitoring in Early Life (FAMILY) study: rationale, design, and baseline data of a study examining the early determinants of atherosclerosis. Am Heart J. 2009;158(4):533–539.
16. Buffart LM, van den Berg-Emons RJ, Burdorf A, Janssen WG, Stam HJ, Roebroeck ME. Cardiovascular disease risk factors and the relationships with physical activity, aerobic fitness, and body fat in adolescents and young adults with myelomeningocele. Arch Phys Med Rehabil. 2008;89(11):2167–2173.
17. Dobkin B, Barbeau H, Deforge D, et al. The evolution of walking-related outcomes over the first 12 weeks of rehabilitation for incomplete traumatic spinal cord injury: the multicenter randomized Spinal Cord Injury Locomotor Trial. Neurorehabil Neural Re. 2007;21(1):25–35.
18. Ulrich B. Opportunities for early intervention based on theory, basic neuroscience, and clinical science. Phys Ther. 2010;90:839–845.
19. Ulrich DA, Ulrich BD, Angulo-Kinzler RM, Yun J. Treadmill training of infants with Down syndrome: evidence-based developmental outcomes. Pediatrics. 2001;108(5):E84.
20. Wu J, Looper J, Ulrich BD, Ulrich DA, Angulo-Barroso RM. Exploring effects of different treadmill interventions on walking onset and gait patterns in infants with Down syndrome. Dev Med Child Neurol. 2007;49(11):839–845.
21. Ulrich BD, Ulrich DA. Spontaneous leg movements of infants with Down syndrome and nondisabled infants. Child Dev. 1995;66(6):1844–1855.
22. Macias M, Nowicka D, Czupryn A, et al. Exercise-induced motor improvement after complete spinal cord transection and its relation to expression of brain-derived neurotrophic factor and presynaptic markers. BMC Neurosci. 2009;10(1):130–145.
23. Scott ALM, Ramer MS. Differential regulation of dendritic plasticity by neurotrophins following deafferentation of the adult spinal cord is independent of p75NTR. Brain Res. 2010;1323:48–58.
24. Gazula V-R, Roberts M, Luzzio C, Jawad AF, Kalb RG. Effects of limb exercise after spinal cord injury on motor neuron dendrite structure. J Compar Neurol. 2004;476(2):130–145.
25. Karmiloff-Smith A, Thomas M. What can developmental disorders tell us about the neurocomputational constraints that shape development? The case of Williams syndrome. Dev Psychopathol. 2003;15(4):969–990.
26. Chiaretti A, Ausili E, Di Rocco C, et al. Neurotrophic factor expression in newborns with myelomeningocele: preliminary data. Eur J Paediatr Neurol. 2008;12(2):113–118.
27. Geerdink N, Pasman JW, Roeleveld N, Rotteveel JJ, Mullaart RA. Responses to lumbar magnetic stimulation in newborns with spina bifida. Pediatr Neurol. 2006;34(2):101–105.
28. Stark GD, Baker GCW. The neurological involvement of the lower limbs in myelomeningocele. Dev Med Child Neurol. 1967;9:359–374.
29. Maltin C, Delday M, Sinclair K, Steven J, Sneddon A. Impact of manipulations of myogenesis in utero on the performance of adult skeletal muscle. Reproduction. 2001;122(3):359–374.
30. Rademacher N, Black DP, Ulrich BD. Early spontaneous leg movements in infants born with and without myelomeningocele. Pediatr Phys Ther. 2008;20(2):137–145.
31. Teulier C, Smith BA, Kubo M, et al. Stepping responses of infants with myelomeningocele when supported on a motorized treadmill. Phys Ther. 2009;89(1):60–72.
32. Ulrich BD, Ulrich DA, Angulo-Kinzler RM. The impact of context manipulations on movement patterns during a transition period. Hum Mov Sci. 1998;17:8–14.
33. World Health Organization Multicentre Growth Reference Study Group. WHO motor development study: windows of achievement for six gross motor development milestones. Acta Paediatr Suppl. 2006;450:8–14.
34. Barbu-Roth M, Anderson DI, Despres A, Provasi J, Cabrol D, Campos JJ. Neonatal stepping in relation to terrestrial optic flow. Child Dev. 2009;80(1):8–14.
35. Ivanenko YP, Grasso R, Macellari V, Lacquaniti F. Control of foot trajectory in human locomotion: role of ground contact forces in simulated reduced gravity. J Neurophysiol. 2002;87(6):3070–3089.
36. Conway BA, Hultborn H, Kiehn O. Proprioceptive input resets central locomotor rhythm in the spinal cat. Exp Brain Res. 1987;68(3):643–656.
37. Yang JF, Gorassini M. Spinal and brain control of human walking: implications for retraining of walking. Neuroscientist. 2006;12(5):379–389.
38. Bayley N. Bayley Scales of Infant and Toddler Development. 3rd ed. San Antonio, TX: Pearson; 2005.
39. Hof AL. Scaling gait data to body size. Gait Posture. 1996;4:480–493.
40. Lehingue L, Remontet L, Munoz MJ, Faber-Krol MC, Mamelle N. Birth Ponderal Index and body mass index reference curves in a large population. Am J Hum Biol. 1998;10:327–340.
41. Forssberg H. Ontogeny of human locomotor control. I. Infant stepping, supported locomotion and transition to independent locomotion. Exp Brain Res. 1985;57(3):480–493.
42. Barbu-Roth M, Trujillo M, Desprès A, et al. 1.1 The coupling between optical flow and neonatal stepping. Gait Posture. 2005;21(Suppl 1):S1.
43. Lejeune L, Anderson DI, Campos JJ, Witherington DC, Uchiyama I, Barbu-Roth M. Responsiveness to terrestrial optic flow in infancy: does locomotor experience play a role? Hum Mov Sci. 2006;25(1):4–17.
44. Moerchen VA, Saeed ME. Visual attention and step responsiveness to visual flow during treadmill stepping in infants with typical development. Infant Beh Dev. In submission.
45. Luo HJ, Chen PS, Hsieh WS, et al. Associations of supported treadmill stepping with walking attainment in preterm and full-term infants. Phys Ther. 2009;89(11):1215–1225.
46. Barbosa VM, Campbell SK, Sheftel D, Singh J, Beligere N. Longitudinal performance of infants with cerebral palsy on the test of infant motor performance and on the Alberta Infant Motor Scale. Phys Occup Ther Pediatr. 2003;23(3):7–29.
47. Thelen E, Ulrich BD. Hidden skills: a dynamic systems analysis of treadmill stepping during the first year. Monogr Soc Res Child. 1991;56(1):1–98.
Keywords:Copyright © 2011 Academy of Pediatric Physical Therapy of the American Physical Therapy Association
age factors; ambulation; body weight; child development/physiology; early ambulation; gait disorders/neurologic; infants; lumbar vertebrae; meningomyelocele; motion perception; motor activity; proprioception; treadmill test; weight bearing