The gender-specific associations between body composition, countermovement jump performance and bone quality in a young Chinese population

Background: Prophylactic interventions against osteoporosis require a determination of the factors that influence the bone status during adulthood. This study aimed to investigate the associations between body composition parameters (body height (BH), body weight (BW), fat free mass (FFM), fat mass (FM), lower limb muscle mass (LLMM), lower limb fat mass (LLFM)), countermovement jump (CMJ) performance, and calcaneal bone stiffness (SI) in a population of young adults. Methods: The study population included 560 Chinese adults (369 females), aged 20-40 years. Body composition was obtained by bioelectrical impedance analysis (BIA). The CMJ performance (CMJ height (CMJH), the impulse of CMJ phase (ICMJ) and potential energy in the CMJ phase (ECMJ)) was obtained by 3 maximal CMJ trials on ZTJ-II system. Bone quality was measured by quantitative ultrasound (QUS). Results: The present study found BW, FFM and LLMM had significant correlations with SI both in males (r=0.20-0.24, p<0.05) and females (r=0.12-0.20, p<0.05). However, FM and LLFM had positive correlations with SI only in females (p<0.05). CMJ performances, including CMJH, ICMJ and ECMJ, had significant positive correlations with SI in men (r=0.415, p<0.01; r=0.32, p<0.01; and r=0.39, p<0.01, respectively) and women (r=0.248, p<0.01; r=0.26, p<0.01; r=0.3, p<0.01, respectively). Conclusions: This provides evidence that local muscle mass have greater positive associations with calcaneal bone quality than total FFM, and local muscle mass and power are the determinations of region bone quality in young adults. The bone–muscle relationship is more prominent in males than in females.

3 largely on the peak bone quality achieved in young adulthood, and the subsequent ageand hormone -related bone loss. [10,18] Several risk factors, such as advanced age, low body weight (BW), sarcopenia and life-style factors as well as decreased mobility, have been reported to be the important determinants of bone quality in the general population.
Body composition is one of the important determinants of bone quality. [11] However, the importance of fat-free mass (FFM) and fat mass (FM) for bone quality has been somewhat controversial. Greater FFM and FM may imposed a greater mechanical stress on bone, and would be beneficial for bone health. [3] On the other hand, both adipocytes and osteoblasts are derived from a common multipotential mesenchymal stem cell, and the secretion of adipocyte-derived hormones (e.g., estrogens, insulin, leptin, adiponectin, and interleukin-6) may affect the activation of osteoblasts and osteoclasts. Several cross-sectional study studies had found that FFM and FM, as well as both of them were determinants of bone quality. [5,8,30] Contrasting studies, however, suggest that excessive FM may have detrimental effects on bone quality. Moreover, these relationships were difference between men and women according to the recent reports. [32] Some studies found that FM was a more important determinant of bone quality in women than men, [2] while reports to the contrary exist. [24] Meanwhile, regional muscle mass and strength has been shown to be related to local bone quality [14,23] [14,23]. 12,13 Muscle and bone form a functional unit, forces generated by muscle contraction induce changes in bone architecture. [6] However, recent reports found that the muscle-bone relationship is not necessarily site specific. [31,34] In addition, it is unknown whether gender alters the muscle-bone relationship. The correlation between muscle strength and bone characteristics has now been studied by previous studies using 4 isokinetic dynamometer. [4,9] In our study, the countermovement jump (CMJ) was chosen because it had been found to be the most reliable and valid field tests for assessing the explosive power output of the lower limbs in physically active subjects. [25] There is no large literature analyzing the association between body composition, muscle power and bone quality in the young adults, separately by gender. The objective of this cross-sectional study was (a) to determine the relationships among body composition parameters (body height (BH), BW, FFM, FM, lower limb muscle mass (LLMM), lower limb fat mass (LLFM)), CMJ performance and calcaneal bone stiffness (SI) in young Chinese adults, and (b) to assess the gender-specific contributions of regional muscle mass and power to local bone quality, so that if these are appropriately altered during adulthood, osteoporosis would be prevented.

Subjects
The study is a cross-sectional study in 963 independently living people, aged 20-40 years, who were randomly selected from Anhui, Hubei and Hunan province in the middle areas of China. They were initially selected to participate in this study carried out in Anhui National

Measurements of CMJ performance
Compared with squat jump (SJ) test, the CMJ test showed higher relationship with the explosive power factor. [25] In our study, CMJ was performed for the measurement of  [15] and there was a high correlation between dual-energy X-ray absorptiometry (DXA) and Tanita MC-180. [26] Measurements of bone quality Quantitative ultrasound (QUS) measurements have been found to reflect strength and architecture of bone [16,33] [16,33]. 22,23 In this study, QUS device (Achilles express; LUNAR, USA) was used to assess SI of the right calcaneus, which is a combination of speed of sound (m/s) (SOS) and broadband ultrasound attenuation(BUA) (dB/MHz) (SI=0.67×BUA+0.28×SOS-420). [27] This measurement was calibrated daily in accordance with the manufacturer's recommendations and before measurement. To examine the reliability of Achilles devices, short-term precision expressed as CV and standardized CV

Participant characteristics and age-related differences
The participant characteristics are summarized in and SI were significantly (p<0.001) higher in men than in women. However, FM, LLLFM and RLLFM were higher in women than in men. Moreover, the CMJ performances (CMJH, I CMJ , and E CMJ ) were higher in women than in men. Meanwhile, the calcaneal QUS parameters (SI) was also higher in men than in women.
The distributions of age-related difference in anthropometric characteristics, CMJH and SI are shown in TABLE 2. BH, BW, FFM, LLMM, CMJH and SI were higher in men than in women in all age groups. CMJH and SI reduced with age both in men and women.

Influences of anthropometric parameters to QUS parameters
The bivariate correlation analysis of SI against age, anthropometric characteristics and CMJH is shown in TABLE 3. In both genders, age was a negative predictor of SI, and there were significant positive correlations between BW, FFM, LLLMM, RLLMM and SI in males and females, but the correlations were weaker in females than in males. Meanwhile, FM, LLLFM, RLLFM showed positive correlations with SI in females, which were not found in 8 males. Moreover, CMJH had positive correlations with SI in males and females, but correlations were stronger in males than in females.

Bone-Muscle Relationships
The correlations between I CMJ , E CMJ and LLMM in males and females were showed in

Discussion
This study was conducted to assess age, body composition, muscle power to bone quality in young men and women, and to assess the gender-specific contributions of regional muscle mass and power to local bone quality. We found that CMJ performances (CMJH, I CMJ , and E CMJ ) and bone quality decreased with increasing age in men as well as in women. BW and FFM had positive associations with calcaneal bone quality, while FM had a positive correlation with bone quality only in women. Local muscle mass and power was the determinations of region bone quality in young adults. However, the bone-muscle 9 relationship was more prominent in males than in females.
In our previous research, we have found that BW and FFM positively correlate with bone quality in young adults [7]. In this research, we have further discover that local muscle mass (RLLMM) have a stronger relationship with region bone quality (right calcaneus) comparing with LLLMM and FFM. Our study suggests that the greater local muscle mass may be an important factor in achieving peak bone density. We also observed that FM and LLFM had positive correlations with bone quality only in women. IR Reid et al. found that bone density was closely related to FM in premenopausal women, but less so in men, [29] and similar results were found by others studies. 4,8 In contrast, other studies used QUS to study the effect of body composition on bone quality with differing results. Our finding supports the point of view that FM has a positive relationship with bone quality in young women. FM contributes to skeletal load in the same way as lean mass, so this simple mechanical effect may contribute to the fat-bone relationship to some extent. In our study, female samples had less BW and more FM and LLFM than male samples, and this would contributes to the gender discrepancy. A further possible link between the two tissues is the common stromal cell origin of both osteoblasts and adipocytes, and a number of hormones may link the two tissues. The secretion of estrogens from the adipocyte in women may be involved in bone metabolism. This may probably contribute to this gender discrepancy.
CMJ performance depends on the muscle power (muscle force and muscle velocity), [13] and CMJ test had been found to be the most reliable and valid field tests for assessing the explosive power output of the lower limbs in physically active subjects. 15 In our study, we found LLMM and CMJ performance showed positive relationships with SI in males and females. This indicated that local muscle mass and muscle strength were the determinations of region bone quality in young adults. Our results were consistent with those findings by others, which human regional muscle mass was related with bone mass [8] and bone mineral density (BMD). [19] Zudin Puthucheary et al. found that trainingrelated increases in rectus femoris volumes and bone volumes were related (R 2 =0.21-0.31). [28] Regional muscle plays a vital role in bone biomechanics, especially with exercise, which is most likely producing osteocyte viability factors that protect osteocytes against glucocorticoid induced apoptosis. [17,20] Muscle strength is associated with total osteocalcin levels which was reported by Fernandez-Real JM et al., [12] and osteocalcin levels have a direct effect on bone formation. [22] In addition, we observed that bone-muscle relationship was more prominent in males than in females. A cross-sectional study in including 2264 older men and women in Korea, found that the positive correlations between muscle and BMD were stronger in older men than in older women. 34 Our results further proves this point of view in a young adult population by measuring the local body composition and muscle performance. To our knowledge, testosterone in men increases both muscle mass muscle strength and bone quality, while estrogen in women only affects the bone through inhibiting bone resorption by binding to its estrogen receptor. [21]5 This may partly explain this gender discrepancy.

Strength and limitations
Compared with previous studies, the strengths of our study are that body composition, CMJ performance and calcaneal bone quality were simultaneously measured in the subjects, which included different genders and ages within a single group in certain areas in a certain age range, and these people were not receiving medication or suffering from diseases affecting bone metabolism. There are several limitations to our studies. First, we did not consider further variables that might impact bone quality, such as physical activity, dietary calcium and vitamin D intake, genetic, serum hormone levels in our study.
Second, we did not include measurements of bone quality at other sites or use additional techniques such as DXA. But as we know, QUS measurement has become an important modality for the assessment of osteoporosis status and the estimate of osteoporotic fracture risk, and the general consensus is that QUS seems to provide structural information in addition to density. [27] Conclusion In conclusion, we observed that local muscle mass have greater positive associations with calcaneal bone quality than total FFM, and local muscle mass and strength are the determinations of region bone quality in young adults, with the bone-muscle relationship being more prominent in males than in females. To increase or preserve the bone quality of specific site, maintaining or increasing regional muscle mass and muscle power would appear to be an appropriate strategy, especially in men.

Availability of data and materials
The raw data is available upon reasonable request from the corresponding authors.

Author contributions
Zenghui Ding was responsible study concept and design and drafting of the manuscript.
Yubing Xu led on the statistical analyses and manuscript revise. Yanyan Chen contributed to data collection. Yue Xia played a key role in service user engagement. Yining Sun wrote sections of the paper, with input from Xianjun Yang. All authors contributed to the design of the study and approved the final draft of the manuscript.

Ethics approval and consent to participate
The study was approved by the local Institutional Review Board. All study participants were given written informed consent after the study was explained to them.

Consent for publication
Not applicable  Relationship between the impulse of CMJ phase (Icmj) (Icmj= BW×√(2g×CMJH)) and lower limb muscle mass (LLMM) in males (A) and in females (B); Relationship between the potential energy in the CMJ phase (Ecmj) (Ecmj=BW*g*CMJH) and lower limb muscle mass (LLMM) in males (C) and in females (D), BW indicates body weight, g = acceleration due to gravity.
22 Figure 2 Relationship between the impulse of CMJ phase (Icmj) (Icmj= BW×√(2g×CMJH)) and calcaneal bone stiffness index (SI) in males (A) and in females (B); Relationship between the potential energy in the CMJ phase (Ecmj) (Ecmj=BW*g*CMJH) and SI in males (C) and in females (D); BW indicates body weight, g = acceleration due to gravity.

Supplementary Files
This is a list of supplementary files associated with the primary manuscript. Click to download. Equations.pdf