Dhawale, Arjun A.a; Church, Chrisb; Henley, Johnb; Holmes, Laurens Jra; Thacker, Mihir M.a; Mackenzie, William G.a; Miller, Freemana
Morquio syndrome, also known as mucopolysaccharidosis IV (MPS IV) is a progressive, systemic lysosomal storage disorder with a prevalence ranging from 1/76 000 to 1/640 000 live births 1. Patients develop progressive genu valgum, hip dysplasia, ankle valgus, and difficulty in walking 2.
Standing weight-bearing lower extremity radiographs are used for assessment of the lower extremity deformities and preoperative planning; however, these films only provide information about the static alignment 3. Instrumented gait analysis provides information about the dynamic alignment of the lower extremities and has been shown to be helpful in decision making in various conditions 4. The kinetics and kinematics in children with MPS IV have not been previously described.
The purpose of this study was to describe the gait kinetics and kinematics in children with MPS IV who underwent instrumented gait analysis and had no previous lower extremity surgery. Our alternative hypothesis was that gait kinetics, kinematics, and foot pressures in patients with MPS IV were significantly different from the normal population. We also assessed the correlation of genu valgus measured on gait analysis, standing radiographs, and supine clinical examination.
Materials and methods
After obtaining IRB approval, we identified nine children (18 lower extremities) with a confirmed diagnosis of MPS IV who had no previous lower extremity surgery and underwent a three-dimensional gait analysis at our institution between March 2004 and April 2011. We retrospectively reviewed the charts, gait analysis reports (including physical examination, kinetics, kinematics, foot pressures), and standing weight-bearing lower extremity radiographs (done at the same time as the gait analysis). The mean age at gait analysis was 10.6±4 years, mean height was 105.2±15.6 cm (z=−4.5), and mean weight was 22.3±7.2 kg (z=−1.434). Measurements obtained on gait analysis were compared with data from 10 healthy young individuals with age ranging from 9.5 to 11.5 years, a mean height of 138±6.6 cm, and a mean weight of 32.5±7.1 kg.
Gait analysis was carried out using an eight-camera Motion Analysis System with kinetics and kinematics calculated using Cortex and Orthotrack software (Motion Analysis, Santa Rosa, California, USA). Motion was measured with the Cleveland Clinic marker set and ∼20 gait cycles were recorded for each patient. The mean of these cycles was used for analysis. AMTI force plates (Newton, Massachusetts, USA) were used to collect the kinetics data (during four to five steps), and a pedobarograph (F-scan, South Boston, Massachusetts, USA) was used to record the foot pressures during one to three steps 5.
We determined genu valgus using three methods. We measured genu valgus (minimum knee abduction in stance) using three-dimensional gait analysis. A physical therapist performed a complete physical examination during the gait analysis visit. Clinical genu valgus was measured using a goniometer with the patient lying supine on the examination table. A full-length standing weight-bearing radiograph of the lower extremities obtained within a month of the gait analysis was used to measure the radiographic genu valgus (anatomic tibiofemoral angle). Radiographic measurements were made by a single observer.
We performed a skewness/kurtosis test to determine normal distribution of the data. After confirming normal distribution, descriptive summary statistics were done for all the variables. To test the hypothesis, we compared the variables in our study population with means in normal individuals using the single-sample t-test (P<0.05, one tailed). Correlation of genu valgus measured on gait analysis, clinical examination, and standing radiographs was performed using Pearson’s correlation coefficient (r) as well as the coefficient of determination (r2). Post-hoc power and sample-size estimations were performed with type 1 error tolerance (α) of 0.05 [n=9 patients (18 lower extremities); mean knee abduction for study population: 21.9°; mean knee abduction for normal population: 1.47°] and a single-sample t-test (one sided). With these parameters, we obtained a power of 100%. We analyzed the data using STATA version 10 (STATA, College Station, Texas, USA).
Passive range of motion
Table 1 shows the passive range of motion at the hip, knee, ankle, and foot in the study population. The mean hip flexion was 122° (SD 4.9). The mean hip extension was reduced (0.3±8.6). Although knee flexion was normal, extension was restricted (−8.1±8.0°). The mean ankle dorsiflexion was reduced and measured 12.8° (SD 8.4).
Temporal spatial data
Children with MPS IV had a decreased forward velocity, cadence, and stride length compared with the normal population (P<0.05). Height-adjusted, normalized forward velocity, and stride length were also reduced (P<0.01; Table 2).
Trunk, pelvis, and hip
Forward tilt of the trunk and pelvis, hip flexion, hip adduction, and external hip rotation were increased compared with normal population (P<0.05; Table 2). Increased anterior pelvic tilt is consistent with high levels of lumbar lordosis.
There was increased knee flexion, genu valgus (abduction), and external tibial torsion compared with normal during stance (P<0.05, Table 2). Dynamic knee varus–valgus joint laxity showed a mean difference of 9.5° between the minimum and maximum genu valgus (abduction) recorded during stance, as compared with a difference of 0.9° in the normal population (P<0.05).
Ankle and foot
There was decreased ankle dorsiflexion at initial contact as compared with normal population (P=0.001; Table 2).
Pedobarograph found essentially normal foot pressures (P=0.24; Table 2). There was an increased mean external foot progression angle of 12.9° as compared with the normal population mean of 6.8°, although not statistically significant (P=0.06, Table 2).
Joint moments and powers
The hip extension and abduction and ankle plantarflexion joint moments were reduced compared with the normal population (P<0.001). An internal knee varus moment was recorded during gait in response to the genu valgus alignment (Fig. 1). The hip extension and ankle plantarflexion powers were also reduced when normalized to body weight compared with age-matched normals (P<0.0001).
The mean valgus was 24.7° (SD 9.6) on standing radiographs, 22° (SD 11.2) on gait analysis, and 19.5° (SD 7.6) on clinical examination. There was a strong correlation between genu valgus measured on gait analysis and standing radiographs (r=0.89) and a moderate correlation between genu valgus measured on gait analysis and on clinical examination (r=0.69). A strong correlation was also observed between genu valgus measured on radiographs and on clinical examination (r=0.73; Table 3).
The purpose of this paper was to characterize the baseline gait pattern in patients with MPS IV without intervention. There is common gait pattern that has not been described previously, and this can be the basis of defining treatment effects.
There were significant differences in the temporal spatial characteristics, kinetics, and kinematics in children with MPS IV as compared with the normal population on instrumented gait analysis. Children with MPS IV walk slowly with short stride lengths (even when normalized for their short stature). In the sagittal plane, there is an increased forward tilt of the trunk and pelvis with increased hip flexion, increased knee flexion, and decreased ankle dorsiflexion. In the coronal plane, there is increased hip adduction and genu valgus. In the axial plane, they have external hip rotation and external tibial torsion. Children with MPS IV also have knee joint laxity, as shown by the difference in the minimum and maximum genu valgus during the stance phase of gait. The hip and ankle joint moments and power generation were reduced. There was a consistently recorded knee varus moment during the gait cycle as a result of the genu valgus deformity. The overall gait pattern was consistent. These findings facilitate a better biomechanical understanding of the dynamic three-dimensional deformities and decreased walking ability in children with MPS IV and also help in planning treatment.
In this study, we found a strong correlation between the genu valgus recorded on gait analysis and standing radiographs. This is in contrast to a previous study in children with achondroplasia where the varus measured on radiographs did not correlate well with the gait analysis 6. This is an interesting finding, as the radiographs were taken with weight bearing on both lower extremities and the knee abduction was recorded on single limb support during gait analysis. The correlation between the genu valgus measured in the supine position and the genu valgus measured during gait analysis was moderate probably because of the effect of weight bearing and joint laxity. The strong correlation between the genu valgus recorded during radiograph and gait analysis was probably because both were obtained while weight bearing. Therefore, the full-length weight-bearing standing radiograph is more important in treatment planning than non-weight-bearing supine images. Many institutions do not have access to gait laboratories, and it is helpful to understand the correlation of these measures.
The radiographs cannot provide information about the rotational alignment of the lower extremities. Physical examination and CT version studies are helpful to evaluate static torsional alignment. Gait analysis provides information about rotational alignment in the dynamic weight-bearing state. From a clinical treatment perspective, it is important to recognize the external tibial torsion, which, combined with ligamentous knee laxity, contributes to the dynamic genu valgus deformity. This torsional malalignment needs to be considered when planning treatment. A weight-bearing measure of knee deformity is important because of joint laxity, which makes nonweight-bearing measurements less functionally relevant. It is important to remember that radiographs in weight bearing do not give much information on the torsional element and the joint laxity in weight bearing makes the torsional assessment with CT scan in the nonweight-bearing situation of less functional importance.
It has been shown that there is gradual progression of the lower extremity deformities with age and surgical intervention improves the radiological alignment and joint angles 7. This paper is an attempt to define the baseline physical examination and gait characteristics in MPS IV individuals before any lower extremity surgical intervention. It is difficult to say if this data would serve as a baseline for all patients with MPS IV as there is considerable phenotypic heterogeneity ranging from mild to severe. Patients should be evaluated at baseline and after treatment to make an objective valid comparison with regard to the effectiveness of enzyme replacement or surgical treatment. Instrumented three-dimensional gait analyses are especially helpful to assess the torsional and coronal plane malalignments due to joint laxity, which occur secondary to the forces of weight bearing during gait. This tends to be the primary physical loading these children place on the joints, therefore the goal is to reduce abnormal loading during this activity, which can only be measured with gait analysis.
This is a small series of nine children with MPS IV seen at a tertiary referral institution, and it may not be representative of the entire MPS IV population. Errors in measurement may occur in kinematics because of marker placement and in radiographs and clinical examination because of limb positioning. One observer made the radiographic measurements and no intraobserver reliability test was performed.
Children with MPS IV have a variable severity but consistent gait pattern with abnormal temporal spatial characteristics, kinetics, and kinematics as compared with the normal population on instrumented gait analysis. They walk slowly with an increased forward tilt of the trunk and pelvis with increased hip flexion, increased knee flexion, and decreased ankle dorsiflexion, there is an increased hip adduction and genu valgus, and they have external hip rotation and external tibial torsion. Children with MPS IV also have knee joint laxity, as shown by the difference in the minimum and maximum genu valgus during the stance phase of gait. We found a strong correlation between genu valgus recorded on gait analysis and weight-bearing standing radiographs.
Conflicts of interest
There are no conflicts of interest.
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