Body Weight and Range of Motion as Predictors of Trunk Asymmetry in Children With Spinal Muscular Atrophy: A Prospective Functional Assessment

Introduction

Spinal muscular atrophy (SMA) is a lower motor neuron disease with autosomal recessive inheritance that results in progressive proximal muscle weakness and skeletal muscle atrophy [1,2]. This disorder leads to the degeneration of α-motor neurons in the spinal cord and brainstem. Traditionally, before the advent of disease-modifying therapies, SMA was categorized into types 0 to 4 [3]. The disease was first described in 1891 by the Austrian neurologist Guido Werdnig, who showed 2 cases of SMA with common features. The next year, John Thomson reported similar cases, offering a report that was clinically and pathologically better illustrated and of better quality than that of Werdnig [4]. In 1893, Johann Hoffmann described patients with similar symptoms, and he was the first to introduce the term spinale muskelatrophie (spinal muscular atrophy) [5]. There are isolated reports on the influence of body mass index (BMI) on motor development, but there is no information on the influence of BMI on structural disorders. Today, due to early disease screening and treatment introduction, patients with SMA are classified according to functional status into non-sitters, sitters, and walkers. Children and parents cite 3 areas as burdens associated with the disease: physical, mental, and social. Patients and their families often identify the physical challenges as not only motor function impairment, the main challenge, but also as the development of contractures and scoliosis [6]. Contractures in the major joints of the lower extremities, such as the hips, knees, and ankles, can hinder weight-bearing activities and limit the preventive use of range of motion (ROM) exercises in patients with SMA. Contractures are common due to decreased ROM, prolonged static positioning, and agonist-antagonist muscle imbalance. Functionally and symptomatically, contractures can lead to pain and inhibit function in patients [7]. Authors indicate that physiotherapy exercises are necessary even when a contracture has not yet developed [8,9].

The 2018 recommendations for the diagnosis, rehabilitation, and orthopedic and nutritional care of patients with SMA [7] indicate the need to evaluate postural control, scoliosis, hip dislocation, and contractures, including ROM and goniometry measurements, in non-sitter patients. In the sitter patients, the same elements plus additional parameters, such as foot and chest deformities and pelvic obliquity, are evaluated. In the strongest patients, walkers, contractures (ROM, goniometry), postural control, scoliosis, and hip dislocation are assessed [7].

Another problem arising in patients with SMA is nutritional status. Most studies report BMI as an indicator of the nutritional status of children and adolescents because it is easy to assess and can be determined through routine examinations [10,11]. One more argument that accounts for its widespread use is its predictive power [12–14]; however, when analyzing patients with SMA, it is necessary to be aware that their reduced body weight is mainly due to reduced muscle mass, which can affect the calculation of BMI [15]. In patients with SMA, the BMI z-score allows BMI to be interpreted in reference to age- and sex-specific norms, especially in children and adolescents, helping assess how a person compares with others of the same age and sex. Negative values indicate that the BMI is lower than average, while positive values indicate the BMI is higher than average.

Ferrantini et al [10] conducted a study in a group of children with type 2 SMA (SMA2), in which children with a BMI-for-age z-score less than −2 standard deviations (SD) were classified as underweight, whereas those with a BMI-for-age z-score greater than +2SD were classified as overweight. They showed that a low BMI-for-age z-score was a common feature in patients with SMA2; baseline BMI-for-age z-score and sex were significant contributors to eventual changes in BMI-for-age z-score, and patients with a low BMI-for-age z-score were at a greater risk of developing further reductions in those parameters.

BMI does not consider body composition (muscle mass, body fat), so it may not be appropriate for people with SMA who have reduced muscle mass. Still, it can reveal important clinical data and encourage a more thorough medical evaluation. In the literature, although structural changes, contractures, or scoliosis are inherent in the disease in most patients with SMA, there are few publications on this issue, and it is even more challenging to find information on the effect of BMI on structural changes and contractures. Based on previous findings and a comprehensive review of the literature, we hypothesize that low body mass may coexist with structural alterations in some patients with SMA. Therefore, we aimed to assess the relationship between these 2 parameters. The objective of this study was to determine whether changes in BMI and BMI z-scores are associated with structural parameters in patients with SMA.

Material and Methods

STRUCTURAL ASSESSMENT:

The measurement of structural elements was performed in accordance with previous studies by Stępień et al [17]. Previous studies have confirmed the reliability of measurements of trunk position with the use of a scoliometer [17–19] and the measurements of ROM with the use of a plurimeter [20,21].

TRUNK:

Evaluation of trunk parameters included measurements of cervical rotation and the supine angle of trunk rotation (SATR). Cervical rotation was assessed by measuring the passive ROM with stabilization of the ribs on the opposite side. A plurimeter was used for the assessment.

The SATR parameter was assessed at 2 levels: the first at the sternum level and second rib (SATR-U) and the second in the lower torso at the xiphoid process level (SATR-L). A scoliometer was used for the evaluation.

UPPER AND LOWER LIMBS:

The neutral positions and passive ROM were assessed for the following parameters: arm flexion (AF), arm abduction (AB), elbow flexion (EF), forearm supination (FS), hip flexion (HF), knee flexion (KF), and ankle dorsiflexion (ADF). Joint contractures were diagnosed if the value of the neutral position varied from 0 (ie, the patient could not reach the correct initial position). The severity of contracture increased with the value of the neutral position. Evaluation of the upper and lower extremities was conducted using a goniometer. In the goniometer test, a 5-degree measurement error was adopted [22].

ANTHROPOMETRIC MEASUREMENTS:

The anthropometric measurements of weight and height/length were made according to World Health Organization standards, with a precision of 0.1 kg and 0.1 cm, respectively. In non-sitter patients, body weight was measured using an electronic wheelchair scale, with the caregiver as the tare value. In sitters, the patient’s weight was obtained using a chair scale, while walkers could be evaluated in the standing position. Supine length (SL), an equivalent of body length/height in non-standing patients, was measured using a tape on the child’s right side on an examination table. The patient had shoulders and buttocks resting on the table, arms along the torso, palms facing up, legs as straight as possible, and in contact with the table. In cases of scoliosis and contractures, segmental lengths were measured 3 times: from the apex of the head to the greater trochanter of the femur, successively from the greater trochanter of the femur to the lateral epicondyle of the femur (knee), and from the knee to the distal point of the heel bone. Then, the total average measurement was summed and recorded. The BMI was calculated using the following equation: body weight (kg)/SL (height)² (m²).

The nutritional status of the patients was determined by calculating the BMI-for-age z-Score [17]. The BMI z-score value less than -1 was considered underweight, a value between −1 and +1 was considered a healthy weight, a value between +1 and +2 was considered overweight, and a value greater than +2 was considered obese [17] (Figure 1).

STATISTICAL ANALYSIS:

Interval variables are presented by the mean value with standard deviation, and ordinal variables are presented by median, quartile range, and min–max values. Only min–max values are given for the underrepresented group of walkers. Binary variables are shown as numbers. A paired t test or the Wilcoxon signed rank test was used to assess differences over time. Pearson correlation coefficients (r) were calculated to assess relationships between continuous variables. Spearman rank correlation coefficients (ρ) were used to evaluate associations between ordinal variables or between ordinal and continuous variables. A significance level of P<0.05 was assumed for all calculations.

Results

CORRELATION FOR ALL PATIENTS:

The first measurement showed a significant correlation between BMI value and SATR-L (r=−0.327). As body weight increased, the risk of trunk asymmetry increased. In the second measurement, a significant correlation was found between BMI value and SATR-U (r=−0.419), again indicating the same relationship. A significance level of P<0.05 was assumed.

Significant differences in the change in ROM between the non-sitters and sitters groups were noted for the following joints: KF-R (t=2.57; P=0.015), ADF-R (t=−3.36; P=0.002), ADF-L (t=−2.18; P=0.037), EF-R (t=2.21; P=0.035), and FS-R (t=2.51; P=0.018). These differences indicated a significantly greater motor impairment in children in the non-sitters group, consistent with the course of the disease. A detailed analysis of the BMI category in this group was impossible, as 7 out of 9 children were underweight (see Table 2). At the same time, this shows that problems with muscle mass and nutrition translate into poorer structure and function of the musculoskeletal system.

CORRELATION IN THE SITTERS’ GROUP:

Significant differences in trunk parameters between underweight and healthy weight did not occur in the first measurement. However, in the second measurement, only SATR-U increased trunk asymmetry more in underweight children (t=2.84; P=0.011). There were no differences between the groups in either the first or second study for the neutral position or ROM. There were no differences regarding the changes in trunk parameters, in a neutral position for any joint tested or ROM for comparisons within the sitter’s group divided by BMI categories (healthy weight vs underweight). Notably, most of the patients in this group also fell into the underweight category and did not change it during the year of follow-up (although the mean BMI increased slightly, the z-score decreased), indicating worsening underweight relative to healthy peers. However, this did not translate into deterioration of structural parameters: there was no significant increase in contractures or decrease in ROM.

The group of walkers could not be divided by weight category, as most of the children fell within the healthy weight range. They did not have structural abnormalities.

CORRELATION OF CHANGES IN CONTRACTURES WITH CHANGES IN BMI FOR THE ENTIRE STUDY GROUP:

An increase in BMI meant a rise in hip contracture but an improvement in KF-L, ADF-L, and ADF-R, with only ADF-L showing a significant correlation (r=0.339; P<0.05).

When categorized by BMI, there was a reduction in HF-R contracture for non-sitters, and reductions in KF-R, KF-L, ADF-R, and ADF-L contractures with increasing BMI, although these were not significant. In the sitters group, a significant improvement was observed in ADF-R contracture (r=−0.423; P<0.05), while the change in ADF-L was not significant. In the walkers group, there was an unclear improvement in ADF-R and ADF-L contractures.

In analyzing changes in trunk parameters in children divided by functional level (non-sitter, sitter, walker) and BMI category, only those subgroups with at least 3 children were included. It is also worth noting that there were no children with overweight in the non-sitters group, while there are no children with underweight in the walkers group (Figure 4).

In the non-sitter group, cervical rotation parameters deteriorated among children classified as underweight or of normal weight. The SATR parameter remained unchanged in most children. In the sitter group, more unfavorable changes were noted in the children classified as underweight, but when considering the entire group, some showed improvement in the trunk parameters. In the walkers group, we would expect the parameters to remain the same or improve, but deterioration of both parameters was noted mainly in the group classified as having healthy weight.

The following step of the analysis examined whether there were changes in joint contractures depending on the weight category. Figure 5 shows those joints with contractures in the study group.

In the non-sitters group, there was an increase in hip and knee contractures regardless of BMI category. In contrast, foot contractures subsided slightly, more often in children with underweight. A similar trend was noted in the sitters’ group, with foot contractures remaining at the same level. In walkers, the neutral position of the hips, which had been normal from the start, did not change; knee contractures increased, and ankle contractures decreased in most. There were no differences based on weight category.

Subsequently, ROM was analyzed according to functional level (non-sitter, sitter, walker) and BMI category. Measurements were taken of all joints studied (Figure 6). The most noticeable finding was more deterioration of ROM in children in the non-sitters group, regardless of BMI category. Improvements were noted for AB, HF, and KF on the right side, which can indicate the presence of asymmetry (scoliosis). In the sitter’s group, the most common changes or improvements were noted for upper limb measurements, and there was no clear trend in lower limb joints, regardless of the BMI category. The minor changes were pointed out for the walker’s group, with ranges usually not deviating from normal values. Deterioration was seen in the joints of the feet, which is associated with the widely described course of the disease.

Discussion

CLINICAL IMPLICATIONS:

Measuring the neutral position and passive ROM of the lower and upper limbs is of great clinical importance. Systematic measurements allow physiotherapists to design therapy/exercise programs focused on specific goals. This can affect gross and fine motor skills, and consequently, the patient’s independence. Preventing pain, which often occurs during the development of contractures, is an important aspect. Physiotherapy interventions can improve quality of life. Measuring BMI and BMI z-score is crucial in preventing malnutrition (especially in patients with SMA1) and weight gain, which often results from limited movement due to the disease.

STUDY LIMITATIONS:

This article presents a limited group of patients to illustrate the transitional period in SMA therapy – specifically, the time before the implementation of newborn screening and the initiation of treatment immediately after diagnosis. Due to the nature of the medications used, the start of the study did not completely coincide with the initiation of treatment and differed between the 2 groups.

Another limitation was the high heterogeneity of the group, which is a common issue in rare diseases such as SMA. Additionally, the use of objective measurement tools was challenging due to specific structural abnormalities. However, all measurements were performed by 2 experienced physiotherapists in accordance with best clinical practice.

The study was conducted at a single clinical center. Furthermore, due to the specific clinical course of SMA, there were very few patients who were walking at the time of late diagnosis, which is certainly a limitation of the study. Nevertheless, we decided to present the results because of the clinical specificity of this subgroup, particularly regarding structural alterations.

Conclusions

In this study group, there was no deterioration of trunk parameters or reduction in the ROM of limbs over 1 year of observation, which can already be considered favorable. Non-sitters and sitters showed an increase in lower limb contractures measured at all 3 joints, and non-sitters showed a deterioration in ROM. As body weight increased, the risk of trunk asymmetry increased. Measurement of contractures and ROM should be introduced as standard practice in the evaluation of children with SMA, alongside parallel measurements of forearm length and body length.