In children with lumbosacral myelomeningocele (MMC), an energy-expensive gait pattern during walking has been identified. 1,2 The excessive lateral movement of the trunk due to weakness of the hip abductor muscle is associated with increased range of pelvic rotation and obliquity coupled with rotation of the trunk. This gait pattern compensates for muscle weakness and facilitates forward progression. 3–5
Researchers have shown that gait pattern improves, oxygen cost decreases, and walking speed increases with the use of an ankle-foot orthosis (AFO) as compared with barefoot walking. 6–8 A knee-ankle-foot orthosis (KAFO) has also been studied in these patients, 9–11 but there are no reports of energy expenditure during walking with this orthosis.
It has been reported that children with MMC fatigue sooner than children without disabilities 12 and that in children with a disability, heart rate (HR) continues to climb during exercise. 13 We have observed children with low and midlumbar MMC who demonstrate functional walking with orthoses who perform only short walking distances in everyday life. These small breaks during walking might be interpreted as an attempt to keep HR at a “nonstrenuous” level. The aim of this study was to investigate HR and walking velocity during continuously independent walking with orthoses in children with low and midlumbar MMC, with special emphasis on a possible difference between AFOs and KAFOs.
Eight children (three boys, five girls) between the ages of five and 13 years (mean = 10.7, SD = 2.8) with a diagnosis of MMC participated in the study. All children habitually were using orthoses and walked without a walking aid. Seven of the children had participated in a gait study in which they had been tested with both an AFO and a KAFO of Ferrari type (FKAFO). 11 One child who switched from an AFO to a FKAFO at the time of the study was also included.
Muscle strength was assessed by manual muscle testing according to the guidelines of Hislop. 14 All eight children had muscle strength grades of four to five in hip flexion, hip adduction, and knee extension. Hip abduction strength was less than grade three in all children. Plantar flexion strength was grade zero in 13 of 16 limbs.
At the clinical examination, body mass and height were also documented. Prevalence of obesity was analyzed through the calculation of body mass index. Three children had a body mass index greater than the 97th percentile and were, therefore, classified as obese.
Four children were classified as community ambulators. 15 They had all hip extension and hip abduction muscle strength grades of two to four. Four children were classified as household ambulators; these children had hip extension and hip abduction strength grades of zero to two.
Five children, four community ambulators and one household ambulator, were able to walk to a limited degree without orthoses. Three children who were household ambulators could neither walk nor stand freely without orthoses. None of the children had medically diagnosed cardiac or respiratory problems. Patient data are shown in Table 1.
All children were tested during the same setting with AFOs and KAFOs that they had, in the presence of their parents, been instructed to alternate between during a two-week period before the test. The orthosis worn at the time the child arrived for testing was tested first; two children were tested first with KAFOs, and six were tested first with AFOs.
The KAFO used in this study has a thigh cuff with a freely articulating knee joint to align the thigh, shank, and foot in the frontal plane (FKAFO). 10 Both orthoses were identical in the ankle joint and sole. The ankle joint was restricted to prevent tibial advancement due to plantar flexor weakness. Five to seven degrees of dorsiflexion was permitted to create slight knee flexion that allowed the center of gravity to be positioned directly above the axis of the hip joint in the sagittal plane. The sole of the orthosis extended to the end of the toes with decreasing flexibility in the forefoot for children with weak hip extensor muscle strength. All shoes were adjusted for heel height to provide each individual optimal trunk alignment in the sagittal plane. The AFOs and FKAFOs weighed from 1.4 to 2.2 kg without shoes and from 1.8 to 2.9 kg with shoes.
Heart Rate and Walking Velocity
HR was monitored using a commercially available chest electrode monitor equipped with a transmitter (Polar Sport Tester, Polar Electro Oy, Kempele, Finland). The monitor is placed on the chest wall to detect heartbeats. The child was instructed to walk as far as possible along a straight corridor 102 meters long at a self-selected velocity, three times with each orthosis. The child was also told that she or he would be taken back in a wheelchair to the starting point after each trial. During the walking period, the HR and walking time were collected from a watch receiver, which was carried by an examiner positioned close to the child. An assistant walked alongside to register the time and HR values at each six-meter interval. Before the walking trial began, the child sat quietly for five minutes to reach a resting steady state at which the lowest HR was documented. The HR was also registered at the start of each new walking trial. During the walking trials there were no breaks other than the time required to roll back in the wheelchair and to change to the second orthosis after three walking trials.
The Wilcoxon signed rank test was used to compare results between the AFO and FKAFO trials. The Mann-Whitney U test was used to compare results between the two groups of children (community ambulation and household ambulation groups). Statistical significance was determined at p ≤ 0.05. All statistical analyses were performed using commercially available software (SPSS, Cary, NC).
Forty-eight trials were performed. In two children, one walking trial could not be used for analysis because of an interruption in the middle of their walking distance. In one child, one trial with each type of orthosis was interrupted shortly after initiation, and the subject was not motivated to repeat the trials.
Two children walked the entire distance in one or more trials, whereas six of the eight children quit before the end of the 102 meters because of a lack of energy. The distance walked by each subject with both orthoses is shown in Table 2.
Resting Heart Rate
Resting HR, defined as the lowest HR measured before the start of the initial gait trial, ranged from 73 to 100 beats/min (Table 2). The HR after the first six-meter interval of each trial is shown in Figure 1 for subjects one through four and in Figure 2 for subjects five through eight.
Heart Rate During Walking
Mean HR during walking for each subject was calculated after excluding the first six-meter interval. Among subjects in the study group, mean HR ranged from 112 to 168 beats/min when analyzed as the mean of all available trials for each orthosis. The highest HRs were observed in the two children classified as obese (subjects one and eight). Mean HR during walking with both orthoses is given for each child in Table 2.
When calculating walking velocity, the first six-meter interval was excluded as in the HR calculations. Mean walking velocity of the available trials for each orthosis ranged from 29 to 74 meters/min. Mean walking velocities for each child with both orthoses are given in Table 2.
During the last 30 meters of the walking distance, a steady-state plateau could be identified in six children with an increase of HR between zero and eight beats/min. One child (Table 1, subject eight) had an increase of 12 and 13 heartbeats with the two orthoses. For one child (Table 1, subject seven), HR continuously increased throughout all trials by 26 and 25 beats/min or more.
Concerning the short steady-state and walking periods, no physiological cost index 16 based on steady-state HR was calculated. HR during all walking trials in all subjects who were classified as community ambulators is shown in Figure 1, and HR in those who were classified as household ambulators is shown in Figure 2.
Comparison Between Groups of Functional Ambulation
Resting HR did not differ between the household or community ambulation groups (p = 0.686). Mean HR during walking was slightly higher in the children who were community ambulators with both orthoses, but these differences did not reach statistical significance (Table 3).
Children in the household ambulation group had less muscle strength in hip extension and abduction (strength grades ranging from zero to two) than children in the community ambulation group (strength grades ranging from two to four), and walking distance was significantly shorter in the household ambulation group than in the community ambulation group. Walking velocity was apparently slower in the household ambulation group with both orthoses, although this difference was statistically significant only with the FKAFO (Table 3).
Comparison Between Orthoses
In each subject, HR during walking was somewhat higher when wearing the FKAFO as compared with the AFO (p = 0.018) with correspondingly increased walking velocity in seven subjects (p = 0.401). Distance walked showed no difference with respect to orthoses (Table 2).
The main finding of the study was that children with low and midlumbar neurological lesions who walk independently did not walk sufficiently long uninterrupted distances necessary to achieve steady-state walking. The results confirm the finding of Bailey and Radcliffe 17 that walking for a sufficient time to measure HR under steady-state conditions in persons with locomotor disability is not always possible. In a recent study, Boyd et al 13 noted that in children with a disability, HR continues to climb during exercise, so calculation of the physiological cost index, which assumes that HR during testing rises to a steady-state plateau, is invalid. Because of the short steady-state plateau that was achieved in our study group, we also found calculation of the physiological cost index to be invalid.
According to our clinical observations, children with extensive paresis in hip extensor and hip abductor muscles who walk independently with orthoses but without walking aids seem to walk short distances to keep ambulation functional. This became apparent in a child in the present study. Subject five was known to ambulate functionally indoors during the whole day in her daycare surroundings but became fatigued during the trial after walking a distance of 36 meters. Walking short distances with small breaks combined with use of an electric wheelchair outdoors seems to be necessary to keep energy expenditure at a comfortable level. This was confirmed by Williams et al, 12 who found that children with myelodysplasia fatigue sooner than their peers without disabilities because of the energy-demanding walking pattern, and they adopt a comfortable, energy-efficient walking speed. 18 Furthermore, our findings indicated a faster walking velocity at a similar walking HR in the group with stronger hip abductor and extensor muscles as compared with the group with less hip muscle strength. This is in accordance with the findings of Duffy et al, 2 who reported that oxygen cost increased significantly above normal when there was weakness or paralysis of the hip abductors. According to Waters et al, 19 the average walking velocity was 70 meters/min for children without disabilities, and no gender-related differences were found. In our study, the mean walking velocity in two children was normal according to the definition of Waters et al, 19 but their mean HR ranged from 156 to 168 beats/min as compared with 111 to 118 beats/min for children who are not disabled and walking at normal speed (six to 12 years). 19 This was in accordance with Williams et al, 12 who found an increased rate of oxygen consumption above normal values among children with MMC when walking at the same velocity as children who are not disabled, indicating that the children with MMC would fatigue sooner during this activity than their peers who are not disabled. The role of obesity was not analyzed further in this study.
The orthosis worn when the child arrived was tested first; two children were tested initially with the FKAFO and six children with the AFO. In all children, motivation decreased to some degree before testing was done, and this might have been a disadvantage for the later-tested orthosis. Furthermore, the FKAFO weighed more than the AFO, which might have influenced the results. In addition, this study design, comparing the different orthosis trials when the first set of trials was from a resting state and the second set was started after the subjects had already walked three trials, does not allow a valid comparison between the two orthoses. Note, however, that a comparison of upper body movements wearing the same orthoses did not show any difference. 11 Nevertheless, no conclusions can be made about differences between the orthoses with respect to energy expenditure, and further studies are recommended to better address this question.
For the HR to reach a steady state during walking, a minimum of three minutes is required. 7,12 Moreover, the children studied by Duffy et al 1 were able to walk at least 50 meters comfortably and were all classified as community ambulators. None of our subjects walked for longer than two minutes, although two subjects (community ambulators who used a wheelchair outdoors) may have been able if more motivated. This conclusion might be supported by the fact that in subject two (Fig. 1B), the initial HR was lower for the last trial than for the first trial. This indicates that a longer walkway might have enabled the faster subjects in this study to reach a steady state. Children with low and midlumbar paresis who are able to walk independently, however, particularly those classified as household ambulators, seem to compensate for their energy-demanding gait pattern by maintaining the HR at a comfortable level. Besides the physiological limitations to achieving a steady-state HR, walking behavior is also dependent on psychological factors; together these factors determine perceived fatigue.
Children with low and midlumbar MMC have higher HRs during walking than their peers who are not disabled. All children in our household ambulation group had weaker hip abductors and hip extensors and walked at a slower velocity than the children in the community ambulation group. The children in the household ambulation group also walked significantly shorter distances than children in the community ambulation group, but HRs were similar between the two groups. This might be interpreted as a solution to maintain walking as functional as possible by keeping the HR and thus energy expenditure at a perceived comfortable level.
We thank the children and their families for participating in this study.
1. Duffy CM, Hill AE, Cosgrove AP, et al. Energy consumption in children with spina bifida and cerebral palsy: a comparative study. Dev Med Child Neurol. 1996; 38: 238–243.
2. Duffy CM, Hill AE, Cosgrove AP, et al. The influence of abductor weakness on gait in spina bifida. Gait Posture. 1996; 4: 34–38.
3. Vankoski S, Sarwack JF, Moore C, et al. Characteristic pelvic, hip, and knee kinematic patterns in children with lumbosacral myelomeningocele. Gait Posture. 1995; 3: 51–57.
4. Duffy CM, Hill AE, Cosgrove AP, et al. Three-dimensional gait analysis in spina bifida. J Pediatr Orthop. 1996; 16: 786–791.
5. Vankoski S, Moore C, Statler KD, et al. The influence of forearm crutches on pelvic and hip kinematics in children with myelomeningocele: don't throw away the crutches. Dev Med Child Neurol. 1997; 39: 614–619.
6. Thomson JD, Ounpuu S, Davis RB, et al. The effects of ankle-foot orthoses on the ankle and knee in persons with myelomeningocele: an evaluation using three-dimensional gait analysis. J Pediatr Orthop. 1999; 19: 27–33.
7. Duffy CM, Graham HK, Cosgrove AP. The influence of ankle-foot orthoses on gait and energy expenditure in spina bifida. J Pediatr Orthop. 2000; 20: 356–361.
8. Galli M, Crivellini M, Fazzi E, et al. Energy consumption and gait analysis in children with myelomeningocele. Funct Neurol. 2000; 15: 171–175.
9. Schiltenwolf M, Carstens C, Rohwedder J. Results of orthotic treatment in children with myelomeningocele. Eur J Pediatr Surg. 1991; 1 (Suppl 1): 50–52.
10. Bartonek Å, Saraste H, Knutson L, et al. Orthotic treatment with Ferrari knee-ankle-foot orthoses: case report. Pediatr Phys Ther. 1999; 1: 33–38.
11. Bartonek Å, Saraste H, Eriksson M, et al. Upper body movements during walking in children with lumbo-sacral myelomeningocele. Gait Posture. 2002; 15: 120–129.
12. Williams LO, Anderson AD, Campell J, et al. Energy cost of walking and wheelchair propulsion by children with myelodysplasia: comparison with normal children. Dev Med Child Neurol. 1983; 25: 617–624.
13. Boyd R, Fatone S, Rodda J, et al. “High-tech” or “low-tech” measurements of energy expenditure in clinical gait analysis? Dev Med Child Neurol. 1999; 41: 676–682.
14. Hislop HJ. Daniel's and Worthingham's Muscle Testing: Techniques of Manual Testing. Philadelphia: Saunders Co; 1995.
15. Hoffer M, Feiwell E, Perry J, et al. Functional ambulation in patients with myelomeningocele. J Bone Joint Surg Am. 1973; 55: 137–148.
16. Butler P, Engelbrecht M, Major RE, et al. Physiological cost index of walking for normal children and its use as an indicator of physical handicap. Dev Med Child Neurol. 1984; 26: 607–12.
17. Bailey M, Radcliffe CM. Reliability of physiological cost index measurements in walking normal subjects using steady-state, non-steady-stare and post-exercise heart rate recording. Physiotherapy. 1995; 81: 618–623.
18. Vankoski S, Bare A, Dias L, et al. Energy expenditure in myelomeningocele: what's the cost of walking? Dev Med Child Neurol. 1997; 75 (Suppl): 18–19.
19. Waters RL, Lunsford BR, Perry J, et al. Energy-speed relationship of walking: standard tables. J Orthop Res. 1988; 6: 215–222.
Keywords:© 2002 Lippincott Williams & Wilkins, Inc.
spinal dysraphism; child; gait physiology; heart rate; walking physiology; orthotic devices