Background
Adolescent idiopathic scoliosis (AIS) is the most common spinal deformity occurred during puberty, with predominant curve progression in females [
1]. The anthropometric phenotypes of female AIS patients have been well-documented in studies. These patients are taller, have a longer arm spam, and have a lower body weight (BW) and body mass index (BMI) [
2‐
4]. In addition, female AIS patients have been found to have abnormal bone growth and metabolism, and the related pathogenesis has been widely studied, although the etiology is still unclear [
1,
5,
6]. In contrast, the anthropometric characteristic of male AIS patients have been only recently reported in two studies [
7,
8]. The male AIS patients were found to have significantly lower BW and BMI during and after the peak of pubertal growth than age- and gender-matched healthy controls, whereas their corrected standing height (SH) was comparable to [
8] or higher [
7] than that of the controls.
Because lower BW and BMI have been consistently found in both male and female AIS patients, examining body composition could help provide a better understanding of AIS pathogenesis. Less mesomorphism has been documented in female AIS patients by anthropometric methods [
9,
10] and was found to be a risk factor for curve progression [
10] Ramirez et al. [
11] reported lower fat mass and fat free mass in girls with AIS using bioelectrical impedance analysis. Dual-energy X-ray absorptiometry (DXA) is the preferred method for assessing whole body bone mineral density and body composition, especially in children and adolescents with higher accuracy [
12,
13] DXA could provide information for a three-compartment model of body composition that includes fat mass (FM), lean mass (LM), and bone mineral content (BMC). By assessing the body composition with DXA, Clark et al. [
14] found children with reduced FM and LM at 10 years (yrs) old had higher incidence to develop scoliosis before 15 years old. However, none of previous study has focused on the body composition of male AIS patients. Hence, a case–control study was conducted using DXA aimed at understanding whether male AIS patients have abnormalities in body composition and bone status.
Results
The AIS patients and controls showed comparable self-reported Tanner stage for pubic hair (3.9 ± 0.6 vs 4.0 ± 0.7,
p = 0.953). The anthropometric and body composition data of the patients and controls were summarized in Table
1. By adjusting for age, no significant difference was revealed between AIS and controls in SH. However, patients with AIS showed significantly lower BW and BMI than those of the controls.
Table 1
Logistic regression analysis on the measurements between male AIS patients and the controls
SH (cm) | 171.6 ± 8 | 168.6 ± 9.9 | 0.131 | 0.963 (0.810–1.146), P = 0.674 | |
BW (Kg) | 63.1 ± 15.8 | 52.6 ± 9 |
<0.001
|
0.517 (0.326–0.819),
P
= 0.005
| |
BMI (Kg/m2)ǂ
| 21.3 ± 4.3 | 18.5 ± 2.6 |
<0.001
|
0.621 (0.428–0.902),
P
= 0.012
| |
Fat Mass (Kg) | 12.8 ± 9.3 | 9.6 ± 5.3 | 0.049 | 0.671 (0.433–1.040), P = 0.074 | 1.652 (0.796–3.428), P = 0.178 |
Lean Mass (Kg) | 43.7 ± 7.6 | 36.2 ± 6.8 |
<0.001
|
0.420 (0.259–0.682),
P
< 0.001
|
0.117 (0.041–0.333),
P
< 0.001
|
BMC (Kg/cm) | 1.8 ± 0.3 | 1.5 ± 0.3 |
<0.001
|
0.397 (0.241–0.656),
P
< 0.001
| 0.373 (0.097–1.438), P = 0.152 |
BMD (g/cm2) | 0.93 ± 0.142 | 0.819 ± 0.069 |
<0.001
|
0.455 (0.288–0.719),
P
= 0.001
|
0.272 (0.093–0.801),
P
= 0.018
|
FMi (Kg/m2) | 4.29 ± 2.92 | 3.37 ± 1.82 | 0.078 | 0.868 (0.729–1.033), P = 0.111 | |
LMi (Kg/m2) | 14.78 ± 1.99 | 12.66 ± 1.94 |
<0.001
|
0.736 (0.610–0.888),
P
= 0.001
| |
For the body composition, the AIS patients had significantly lower LM, LMi and BMC than the controls by adjusting for age. In contrast, the FM and FMi were comparable between two groups. By further adjustment for SH, FM and LM, the BMC become comparable between two groups. In contrast, the BMD in patients with AIS was significantly lower than that in the controls, either adjusted for age only, or together with SH, LM and FM.
Discussion
The anthropometry and body composition of 47 male AIS patients were studied and compared to those of 40 age- and gender- matched healthy controls. The patients showed significant lower BW and BMI values. After adjusting for height loss using Bjure’s equation, the standing height of the AIS patients was comparable to that of the controls. The AIS patients had significantly lower subcranial LM, LMi and BMC than the healthy controls. These findings suggested that male AIS patients have abnormal body composition. In addition, the comparable BMC but significantly lower subcranial BMD observed in the males with AIS than those of healthy controls by adjustment for SH, FM and LM indicated that they may be abnormal bone metabolism in these patients.
Curve progression in AIS patients mainly occurs during puberty and is highly correlated with the velocity of longitudinal growth [
2,
4,
18‐
20]. Abnormal pubertal growth has been documented in both female and male AIS patients. Female AIS patients showed significantly greater corrected standing height and longer arm spans after the onset of puberty than their age- and gender-matched healthy peers [
4]. In addition, they showed significantly lower BW and BMI and a higher incidence of underweight than healthy control [
21]. In contrast, only two studies have focused on the anthropometry of males who have AIS [
7,
8]. Our previous cross-sectional study, which included 332 male AIS patients and 356 controls between the ages of 11 and 19 years, found that the AIS patients had comparable SH and arm span to the controls at each age group [
8]. Another study, conducted by Oh et al. [
7], compared 420 male AIS patients, who were 19 years of age, with 409 age-matched controls, showed greater SH in the AIS patients than that of the controls (176.1 cm vs. 174.7 cm) although the difference was small. Our previous study [
8] also showed that compared to the controls, the male AIS patients who were older than 14 years had significantly lower BW and that the patients between the ages of 15 and 17 years had significantly lower BMI. In contrast, Oh et al. [
7] found that the male AIS patients had significantly lower BW and BMI than the controls. In the present study, the subjects in both groups were newly recruited, and the results are consistent with previous findings; the male AIS patients showed comparable corrected SH to that of the controls, whereas their BW and BMI were significantly lower than those of the controls.
Since lower BW and BMI have been commonly observed in patients with AIS, we thought it would be interesting to examine their body composition. The morphologic somatotypes of the human body can be classified as endomorphic, mesomorphic and ectomorphic [
22]. By analyzing the morphologic somatotypes through the measurement of skinfold thickness, LeBlanc et al. [
10] found that the girls with progressive AIS were less mesomorphic than the age- and gender-matched controls. Mesomorphism results from the development of bone, cartilage, ligament and muscle; hence, the finding by LeBlanc et al. [
10] suggested that bone and muscle mass are less developed in patients with progressive AIS. By comparing the body composition profiles of 52 female AIS patients to those of 92 age-matched healthy female controls, Barrios et al. [
9] also found that the female AIS patients had a lower mesomorphic component. Moreover, their results showed a significantly higher ectomorphic component and a marginally lower endomorphic component in the AIS patients than in the controls. Because lower endomorphism is related to delayed maturation and higher ectomorphism is related to delayed onset of puberty, the observed somatotypes in girls with AIS might be related to their delay in puberty onset and physical maturation in terms of skeletal development [
9,
23]. In addition to analyzing the somatotypes of AIS patients, Ramirez et al. [
11] used bioelectrical impedance analysis to examine the body composition of 27 female AIS patients who were candidates for corrective spinal surgery. They compared their results with data from a study of 488 age- and gender-matched healthy controls and found that the AIS patients had significantly lower BW, BMI, FM and FFM (fat free mass, same as LM in the present study). In addition, the AIS patients showed significantly lower FMi and FFMi than 25 locally recruited healthy girls. The application of DXA on body composition assessment has been found more accurately than other methods, such as skinfold thickness measurements and impedance analysis [
12]. Recently significant association between altered body composition assessed by DXA and the occurrence of scoliosis during puberty was reported by Clark et al. [
14] with a population-based prospective longitudinal study. They found that the lower FM and LM at 10 years suggested higher incidence of scoliosis before 15 years, and per standard deviation increase in FM at 10 years would result in 14 % reduced risk of scoliosis at 15 years by adjusting for age and gender, while per standard deviation increase in LM could result in 20 % reduced risk of scoliosis at 15 years by adjusting for age, gender, FM and leg length. In the study by Clarks et al. [
14], the etiology of scoliosis occurred during puberty was not clarified although most of them should be idiopathic, and the severity of scoliosis was unknown. With the great interest in body composition of male with AIS, whole body scans by DXA were conducted. After adjustment for age, we observed significantly lower BW, BMI, LM and LMi in the male AIS patients than in the controls. These findings were in agreeing to those reported in female AIS patients [
10,
11], although lower FM was not retrieved. Our results support the hypothesis that male AIS patients have an altered body composition compared to that of healthy controls. Moreover, the abnormalities in body composition that have been consistently observed in male and female AIS patients support that lower BW, BMI and LM were a general phenotype of AIS. In addition, this phenotype might be existed before the occurrence of scoliosis during puberty [
14].
Significantly lower BMC and BMD were found in the male AIS patients than that of the controls by adjusting for age in the present study. The bone mineral status of female AIS patients has been widely studied, and the most comprehensive data have been reported by a research group in Hong Kong [
24‐
31]. In their studies, female AIS patients showed a significantly lower percentage (28–33 %) of bone mass and this was found to be a systemic phenomenon that could persist into skeletal maturity [
24‐
27]. They also found that the patients suffered from diminished bone quality [
28]. Moreover, osteopenia, which was detected by DXA and the bone stiffness index, which was assessed by quantitative ultrasound, were found to be prognostic factors of curve progression in females with AIS [
29,
30]. In contrast, none of the previous studies have focused on the bone status of male AIS patients [
31]. The present study showed that the male AIS patients had significantly lower BMC and BMD when compared with age- and gender- matched healthy male controls. However, due to the small size in the control group, the reference Z-score could not be calculated. Hence, the incidence of osteopenia and osteoporosis in the male AIS patients could not be determined in the present study. Weight-bearing is highly associated with bone mineral accrual during adolescence due to the additional mechanical loading during physical exercise and the resulting muscle-mediated effects [
32]. In children, total and areal BMD values have been reported to be highly related to body mass, FM, FFM and BMI [
33]. In studying the bone mineral status of AIS patients, Szalay et al. [
34] suggested that the decreased BMD in scoliosis patients might due to lower BMI and that patients with normal or heavy weight were much less likely to have lower BMD than controls. In the present study, the BMC in patients with AIS was no longer different from that of controls by adjusting for the age, SH, FM and LM. This finding was in agree with previous studies and supported that lower weight might play an important role in the lower bone mineral content of male AIS patients. Several studies have demonstrated that LM was more important than FM in contributing to bone mineral accumulation [
13,
35,
36] and that the contribution of FM was not consistent [
37]. Our results also showed significantly lower LM in male AIS patients than the controls when adjusted for age and FM. After when further adjusted for age, SH, LM and FM, the difference in BMD between male AIS patients and controls was still significant, suggesting there may be abnormal bone metabolism in the male AIS. Thus, it could be interest to carry out further study focusing on the bone metabolism in male AIS.
Several limitations cannot be neglected in the present study. Both body weight and bone mineral status could be affected by several factors, such as nutritional status, eating habits, physical activity level and weight-bearing. These confounders were neither quantified nor controlled for in our study. In addition, the application of Adams forward bending test to rule out spinal deformity may have bias since small spinal curvature could be missed without X-ray films examination, although this test was done by experienced senior consultant spine surgeon. Moreover, this study had a relatively small sample size when compared with the previous studies on the bone mineral status of AIS patients; this was partially due to the fact that the prevalence of AIS is rarer in males.
Competing interest
The authors stated that there are no conflicts of interest regarding the publication of this article. The manuscript has not been submitted or published elsewhere.
Authors’ contributions
WJW and YQ designed the study. ZZZ, FZ and YQ recruited the AIS patients and documented the clinical data, while WJW and ZWW recruited the healthy control from local school. The DXA assessment was carried out by WJW and ZWW. WJW analyzed the data and drafted the manuscript, while all the other authors involved in results interpretation and paper discussion. All authors read and approved the final manuscript.