Musculoskeletal and bone health characteristics in young men: A comparison of low and high bone mineral density

Abstract

BACKGROUND

Bone is a dynamic and metabolically active tissue, and reduced bone mineral density (BMD) is a significant risk factor for osteoporosis.

AIM

To compare differences in body composition, bone health parameters, and muscle strength across major joints between young men with low and high BMD.

METHODS

Twenty young men with a BMD Z score less than -1.6 and an age-matched reference group of twenty individuals with a Z score greater than 0.0 were selected. Body composition and BMD were evaluated via dual-energy X-ray absorptiometry (DXA). Muscle strength in six joints (shoulder, elbow, wrist, hip, knee, and ankle) was measured using a calibrated Biodex System 4 Pro isokinetic dynamometer.

RESULTS

Overall, young men with a high BMD (Z score: 0.73 ± 0.33) demonstrated significantly greater values across most body composition and bone health indices compared to those with a low BMD (Z score: -1.95 ± 0.98). These included regional (upper limb, lower limb, trunk) and whole-body measurements of fat mass (FM), lean mass (LM), fat-free mass, total mass, bone area, bone mineral content, and BMD (all P < 0.05). Conversely, no significant differences were found in whole-body fat percentage or fat area ratio between the groups (all P > 0.05). Similarly, while the high BMD group demonstrated elevated height-adjusted indices for FM, LM, and limb LM (all P < 0.01), their muscle-to-bone and soft tissue-to-bone ratios were significantly reduced (both P < 0.01). Furthermore, while muscle strength across most metrics for the shoulder, hip, and knee joints was significantly greater in the high BMD group (all P < 0.05), young men with high BMD demonstrated a significantly greater agonist-to-antagonist strength ratio specifically at the right knee (P < 0.01), while no such differences were observed at the left knee or any other joints (all P > 0.05).

CONCLUSION

These results suggest that LM and strength are key components of body composition associated with low BMD risk in young men with Z scores less than -1.6.

Key Words: Bone mineral density; Body composition; Muscle strength; Young men; Dual-energy X-ray absorptiometry; Lean mass

Core Tip: Young men exhibiting low bone mineral density (BMD) Z scores (Z < -1.6) are characterized by suboptimal body composition, notably reduced lean mass (LM) and diminished bone health. This physical disadvantage is mirrored by reduced muscle strength in major joints. Consequently, LM and muscular strength emerge as crucial determinants in mitigating low BMD risk during young adulthood, necessitating a holistic approach to bone health that extends beyond mere bone density measurements.

INTRODUCTION

Bone adapts to mechanical loading by altering its shape, size, microarchitecture, and density. Through a process of adaptive bone formation modeling, new bone is deposited on existing skeletal surfaces at sites of highest mechanical stress[1]. Notably, bone structure, size, and strength are dependent on-and responsive to-routine physiological and mechanical demands[2].

However, sedentary behaviors contribute to the simultaneous decline of both bone and muscle health. Excessive and prolonged sedentary behavior can lead to loss of lean mass (LM), strength, and bone mass, along with increased total body fat mass (FM)[3]. In adults and older adults, increased sedentary behavior results in significant reductions (1.3%-9%) in skeletal muscle or fat-FM (FFM)[4]. Increased bone resorption coupled with decreased bone formation is the primary mechanism behind immobilization-induced bone loss in weight-bearing bones[5]. Limb immobilization, for example, leads to substantial declines in bone mineral density (BMD) (1%), particularly in weight-bearing bones[6].

Peak bone mass (PBM), the maximal bone density attained prior to stabilization, is typically achieved in late adolescence or early adulthood, making this life stage crucial for skeletal health[7]. Inadequate bone accumulation during adolescence and early adulthood may lead to lifelong skeletal fragility, particularly in females[8]. Moreover, emerging evidence suggests that young male athletes may also face cumulative risk factors for low BMD, defined as Z scores less than -1.0[9].

Therefore, this study aimed to elucidate the differences in body composition, bone health, and muscle strength between young men at risk for low BMD (BMD Z score < -1.0) and their age-matched controls. This investigation will quantify disparities in key areas, including lean and FM, regional and whole-body bone health, and strength across major joints, to provide evidence supporting the development of targeted prevention strategies for this population.

MATERIALS AND METHODS

Participants

From a cohort of 148 male students, 20 participants with the highest BMD (Z > 0.0) and 20 with the lowest BMD (Z < -1.6) were selected, based on a Z-score below -1.0 being defined as “at risk for low BMD”[9]. Students with a body mass index outside the normal range of 18.5 kg/m² to 24.0 kg/m² were excluded. The data are shown in Figure 1. Individual Z-scores were in fact derived from the manufacturer-provided normative reference data for young Asian males embedded in the Hologic dual-energy X-ray absorptiometry (DXA) system, rather than from internal standardization based on the present study cohort. These 40 age-matched individuals (mean age 18.13 ± 0.46 years) formed the final study cohort.

Figure 1 Distribution of bone mineral density and Z scores in the screened cohort (n = 148). Indicated selection thresholds (Z-scores are calculated based on the Hologic dual-energy X-ray absorptiometry manufacturer’s reference database for young Asian males, not on the mean/SD of the present cohort).

All subjects reported no significant medical history, contraindications to strenuous exercise, history of smoking, or alcohol abuse. Physical examinations, electrocardiograms, and other assessments revealed no evidence of organic heart disease.

DXA

Body composition was assessed using DXA, considered a reference method. A Hologic Horizon-Wi system (Hologic, Shanghai, China) with software version 5.6.0.5 was used for all whole-body scans. This system employs continuous sector-beam scanning acquisition technology with a switching pulsed dual-energy X-ray tube operating at 100 kV and 140 kV. Daily quality assurance was performed using the manufacturer’s spine phantom.

During scanning, subjects were positioned supine on the scanning table. Positioning was standardized by ensuring that the head, neck, and torso were centered and parallel to the long axis of the table, with arms positioned palms-down alongside the body and legs extended with slight internal rotation. Subjects were instructed to remain still and breathe normally throughout the procedure. All scans were acquired and analyzed by a single trained operator following standard manufacturer protocols. To ensure consistency, all scans were both acquired and analyzed by a single trained operator in accordance with the manufacturer’s standard protocols. The analysis encompassed six subregions: The head, torso, and both arms and legs. The primary whole-body composition outcomes derived were FFM, LM, FM, BMD, bone area (BA), bone mineral content (BMC), and percentage body fat. FFM, FM, LM, and BMC are expressed in grams (g); BMD is expressed in grams per square centimeter (g/cm²); and BA is expressed in square centimeters (cm²). The muscle-to-bone ratio (MBR) and soft tissue-to-bone ratio (SBR) were calculated by dividing LM/BMC and (LM + FM)/BMC[10].

Isokinetic strength test

All isokinetic tests were conducted using a calibrated Biodex System 4 Pro dynamometer (Biodex Medical Systems, Inc., Shirley, NY, United States). Participants performed abduction and adduction of both limbs, as well as flexion and extension movements, all in a concentric/concentric mode. Prior to testing, a 5-minute warm-up was administered to activate the relevant muscle groups. This was followed by a familiarization session consisting of five practice repetitions to acquaint the subjects with the equipment and ensure maximal effort during the actual test. To prevent fatigue, a 24-hour interval was maintained between tests of different joints.

During testing, subjects were securely positioned in the dynamometer chair according to standardized protocols. For shoulder assessment, participants were seated with the upper limb extended, performing abduction from 0° to maximum range. During elbow testing, the arm was placed in an elbow immobilizer and secured with a strap, moving from full extension to maximum flexion. Wrist testing was performed with the elbow flexed at 90° and fixed, starting from a fully supinated position. Hip testing involved a supine position with the distal thigh secured, the knee maintained at 90° flexion, and the lower limb moving from full extension to maximum flexion. Knee testing was conducted in a seated posture with straps stabilizing the distal thigh and shank, executing movements from flexion to full extension. Ankle testing was performed in a seated position with the knee flexed at 30°, the distal thigh strapped, and the foot secured on the footplate, moving through full dorsiflexion to plantar flexion.

The testing velocity was 60°/second in the wrist, knee, ankle, shoulder, hip, and elbow. Outcome measures included absolute peak torque (APT, in N.m), relative peak torque (RPT, in N.m/kg), total work (TW, in J), and average power (AP, in W).

Statistical analysis

All statistical analyses were performed using Excel and SPSS version 27.0. Data are presented as mean ± SD. Differences in body composition, bone health, and joint muscle strength between the groups were assessed using independent samples t-tests. A P value of less than 0.05 was considered statistically significant.

RESULTS

Differences in regional and whole-body composition and bone health indices between young men with low and high BMD

Upper limb composition and bone health data are presented in Table 1. Compared with young men with a low BMD, those with a high BMD had significantly greater LM, FFM, overall mass, BA, BMC, BMD (all P < 0.001), and FM (P < 0.05) in both the left and right arms. However, no significant differences were observed in fat percentages of either arm (P > 0.05) (Supplementary Table 1).

Table 1 Comparison of upper limb composition and bone health between young men with low and high Bone mineral density, mean ± SD.

	Low BMD (n = 20)	High BMD (n = 20)	P value
Left arm fat mass (g)	775.52 ± 187.44	945.71 ± 204.81	P < 0.01
Left arm lean mass (g)	2437.27 ± 242.93	2799.55 ± 207.82	P < 0.001
Left arm fat-free mass (g)	2570.06 ± 254.90	2978.19 ± 214.54	P < 0.001
Left arm overall mass (g)	3345.57 ± 367.09	3923.88 ± 280.80	P < 0.001
Left arm fat percentage (%)	23.01 ± 3.82	24.00 ± 4.22	P > 0.05
Left arm bone area (cm2)	188.31 ± 19.68	215.56 ± 13.94	P < 0.001
Left arm bone mineral content (g)	132.78 ± 13.95	178.64 ± 11.57	P < 0.001
Left arm bone mineral density (g/cm2)	0.71 ± 0.02	0.83 ± 0.04	P < 0.001
Right arm fat mass (g)	809.96 ± 185.04	961.33 ± 206.73	P < 0.05
Right arm lean mass (g)	2626.84 ± 270.64	2943.33 ± 215.95	P < 0.001
Right arm fat-free mass (g)	2770.35 ± 289.09	3133.26 ± 225.25	P < 0.001
Right arm overall mass (g)	3580.31 ± 394.88	4094.58 ± 286.08	P < 0.001
Right arm fat percentage (%)	22.49 ± 3.74	23.39 ± 4.11	P > 0.05
Right arm bone area (cm2)	197.79 ± 23.06	222.01 ± 15.34	P < 0.001
Right arm bone mineral content (g)	143.50 ± 20.20	189.93 ± 15.05	P < 0.001
Right arm bone mineral density (g/cm2)	0.72 ± 0.03	0.86 ± 0.05	P < 0.001

BMD: Bone mineral density.

Lower limb composition and bone health data are presented in Table 2. Compared with young men with low BMD, those with high BMD had significantly greater LM, FFM, overall mass, BA, BMC, BMD (all P < 0.001), and FM (P < 0.05) in both the left and right legs. However, no significant differences were found in fat percentages of either leg (P > 0.05) (Supplementary Table 2).

Table 2 Comparison of lower limb composition and bone health between young men with low and high bone mineral density, mean ± SD.

	Low BMD (n = 20)	High BMD (n = 20)	P value
Left leg fat mass (g)	2825.66 ± 625.64	3346.23 ± 627.28	P < 0.05
Left leg lean mass (g)	7619.47 ± 828.71	8884.63 ± 820.32	P < 0.001
Left leg fat-free mass (g)	8002.67 ± 855.97	9427.94 ± 849.47	P < 0.001
Left leg overall mass (g)	10828.33 ± 1318.75	12774.16 ± 1239.72	P < 0.001
Left leg fat percentage (%)	25.89 ± 3.57	26.08 ± 3.26	P > 0.05
Left leg bone area (cm2)	352.07 ± 29.48	391.29 ± 23.73	P < 0.001
Left leg bone mineral content (g)	383.19 ± 34.93	543.32 ± 41.48	P < 0.001
Left leg bone mineral density (g/cm2)	1.09 ± 0.04	1.39 ± 0.06	P < 0.001
Right leg fat mass (g)	2859.92 ± 595.83	3435.14 ± 708.40	P < 0.01
Right leg lean mass (g)	7871.40 ± 846.44	9016.27 ± 896.31	P < 0.001
Right leg fat-free mass (g)	8257.29 ± 879.05	9553.59 ± 929.81	P < 0.001
Right leg overall mass (g)	11117.22 ± 1309.92	12988.73 ± 1414.73	P < 0.001
Right leg fat percentage (%)	25.57 ± 3.27	26.29 ± 3.32	P > 0.05
Right leg bone area (cm2)	351.01 ± 34.09	388.82 ± 24.78	P < 0.001
Right leg bone mineral content (g)	385.90 ± 41.86	537.32 ± 45.80	P < 0.001
Right leg bone mineral density (g/cm2)	1.10 ± 0.04	1.38 ± 0.06	P < 0.001

BMD: Bone mineral density.

Trunk composition and bone health data are presented in Table 3. Young men with high BMD had significantly greater LM, FFM, and total trunk mass than those with low BMD (all P < 0.001), along with a larger FM (P < 0.01).

Table 3 Comparison of trunk composition and bone health between young men with low and high bone mineral density, mean ± SD.

	Low BMD (n = 20)	High BMD (n = 20)	P value
Trunk fat mass (g)	6652.34 ± 1486.67	7915.93 ± 1333.12	P < 0.01
Trunk lean mass (g)	21137.79 ± 1743.09	24192.21 ± 1778.35	P < 0.001
Trunk bone mineral content (g)	558.32 ± 43.96	828.76 ± 49.82	P < 0.001
Trunk fat-free mass (g)	21696.12 ± 1773.10	25020.98 ± 1789.99	P < 0.001
Trunk overall mass (g)	28348.46 ± 2740.03	32936.90 ± 2463.52	P < 0.001
Trunk fat percentage (%)	23.31 ± 3.44	24.55 ± 3.09	P > 0.05
Left subcostal bone area (cm2)	129.31 ± 12.73	138.28 ± 12.35	P < 0.05
Left subcostal bone mineral content (g)	80.73 ± 8.93	108.37 ± 13.76	P < 0.001
Left subcostal bone mineral density (g/cm2)	0.62 ± 0.03	0.78 ± 0.04	P < 0.001
Right subcostal bone area (cm2)	133.21 ± 15.68	142.44 ± 12.28	P < 0.05
Right subcostal bone mineral content (g)	81.04 ± 10.62	110.69 ± 11.10	P < 0.001
Right subcostal bone mineral density (g/cm2)	0.61 ± 0.04	0.78 ± 0.04	P < 0.001
Thoracic vertebral bone area (cm2)	126.90 ± 9.92	138.77 ± 11.72	P < 0.01
Thoracic vertebral bone mineral content (g)	97.53 ± 10.83	138.70 ± 13.19	P < 0.001
Thoracic vertebral bone mineral density (g/cm2)	0.77 ± 0.05	1.00 ± 0.06	P < 0.001
Lumbar vertebral bone area (cm2)	60.09 ± 5.75	65.47 ± 8.49	P < 0.05
Lumbar vertebral bone mineral content (g)	58.20 ± 7.41	78.39 ± 10.03	P < 0.001
Lumbar vertebral bone mineral density (g/cm2)	0.97 ± 0.08	1.20 ± 0.09	P < 0.001
Pelvic bone area (cm2)	235.37 ± 23.82	286.78 ± 18.20	P < 0.001
Pelvic bone mineral content (g)	240.84 ± 22.26	392.60 ± 32.14	P < 0.001
Pelvic bone mineral density (g/cm2)	1.03 ± 0.06	1.37 ± 0.10	P < 0.001

BMD: Bone mineral density.

Additionally, compared with young men with low BMD, those with high BMD had significantly greater BMC and BMD in both the left and right ribs (both P < 0.001). The BA of the left and right rib was also larger in the high BMD (P < 0.05).

Similarly, the thoracic vertebral and lumbar region showed significantly greater BMC and BMD in the high BMD group (both P < 0.001), along with a larger BA (P < 0.05). Furthermore, BA, BMC, and BMD in the pelvic region were significantly greater in the high BMD group than in the low BMD group (all P < 0.001) (Supplementary Table 3).

Whole-body composition and bone health data are presented in Table 4. Compared with young men with low BMD, those with high BMD had significantly greater age-matched Z scores, LM, FFM, overall mass, BMC, and BMD (all P < 0.001), as well as FM and BA (P < 0.01). However, no significant differences were observed in whole-body fat percentage or height between the two groups (P > 0.05) (Supplementary Table 4).

Table 4 Comparison of total body composition and bone health between young men with low and high bone mineral density, mean ± SD.

	Low BMD (n = 20)	High BMD (n = 20)	P value
Height (cm)	176.15 ± 5.16	178.60 ± 5.17	P > 0.05
Age-matched Z scores	-1.95 ± 0.98	0.73 ± 0.33	P < 0.001
Fat mass (g)	15138.68 ± 2934.44	17934.59 ± 2931.64	P < 0.01
Lean mass (g)	44836.51 ± 3899.54	51262.15 ± 3581.27	P < 0.001
Fat-free mass (g)	46847.82 ± 4038.82	54071.30 ± 3655.75	P < 0.001
Overall mass (g)	61986.49 ± 6120.16	72005.89 ± 5350.26	P < 0.001
Fat percentage (%)	24.28 ± 2.95	24.84 ± 2.91	P > 0.05
Bone area (cm2)	2030.02 ± 146.48	2161.97 ± 140.96	P < 0.01
Bone mineral content (g)	2011.32 ± 169.17	2602.51 ± 233.95	P < 0.001
Bone mineral density (g/cm2)	0.99 ± 0.02	1.20 ± 0.05	P < 0.001

BMD: Bone mineral density.

LM distribution data are presented in Table 5. Young men with the high BMD group had significantly greater LM/height², limb LM/height² (both P < 0.001), and FM/height² (P < 0.01) than the low BMD group. The high BMD group demonstrated significantly lower MBR and SBR (both P < 0.001). However, no significant differences were observed in whole-body fat percentage or fat area ratio between the two groups (P > 0.05) (Supplementary Table 5).

Table 5 Comparison of lean mass distribution between young men with low and high bone mineral density, mean ± SD.

	Low BMD (n = 20)	High BMD (n = 20)	P value
Fat mass/height2 (kg/m2)	4.85 ± 1.01	5.70 ± 0.88	P < 0.01
Lean mass/height2 (kg/m2)	14.41 ± 0.91	16.19 ± 0.55	P < 0.001
Limb lean mass/height2 (kg/m2)	6.62 ± 0.48	7.46 ± 0.33	P < 0.001
Muscle-to-bone ratio	22.32 ± 1.18	19.82 ± 2.01	P < 0.001
Soft tissue-to-bone ratio	29.85 ± 2.12	26.79 ± 3.15	P < 0.001

BMD: Bone mineral density.

As shown in Table 6, there were no significant differences in any of the measured limb symmetry metrics (bilateral FFM differences or upper-to-lower limb ratios for FFM, LM, overall mass, or FM) between the high- and low-BMD groups (all P > 0.05) (Supplementary Table 6).

Table 6 Comparison of interlimb symmetry between young men with low and high bone mineral density, mean ± SD.

	Low BMD (n = 20)	High BMD (n = 20)	P value
Left-right upper limb fat-free mass difference (g)	200.82 ± 124.93	190.89 ± 96.91	P > 0.05
Left-right lower limb fat-free mass difference (g)	322.61 ± 255.12	313.35 ± 222.26	P > 0.05
Upper-to-lower limb fat-free mass ratio	0.33 ± 0.02	0.32 ± 0.03	P > 0.05
Upper-to-lower limb lean mass ratio	0.33 ± 0.02	0.32 ± 0.03	P > 0.05
Upper-to-lower limb overall mass ratio	0.32 ± 0.02	0.31 ± 0.02	P > 0.05
Upper-to-lower limb fat mass ratio	0.28 ± 0.03	0.28 ± 0.03	P > 0.05

BMD: Bone mineral density.

Differences in muscle strength indices between young men with low and high BMD

Shoulder muscle strength outcomes are summarized in Figure 2. Young men with high BMD demonstrated significantly greater strength in most metrics than those with low BMD.

Figure 2 Shoulder muscle strength. A: Absolute peak torque of shoulder adduction and abduction on both sides between the two groups; B: Relative peak torque of shoulder adduction and abduction on both sides between the two groups; C: Total work of shoulder adduction and abduction on both sides between the two groups; D: Average power of shoulder adduction and abduction on both sides between the two groups. BMD: Bone mineral density.

In the left shoulder abductors, the high BMD group demonstrated significantly greater APT, TW, AP (all P < 0.001), and RPT (P < 0.05). Similar significant differences were observed in the right shoulder abductors for APT, RPT, TW (all P < 0.001), and AP (P < 0.01).

With respect to left and right shoulder adduction, significant increases in APT, TW, AP (all P < 0.01) were detected in the high BMD group, whereas no significant difference was observed in RPT (P > 0.05) (Supplementary Table 7).

Muscle strength measurements of the elbow joint are presented in Figure 3. Compared with young men with low BMD, those with high BMD showed no significant differences in APT, RPT, TW, or AP in the elbow extension muscle groups on either side (all P > 0.05).

Figure 3 Elbow muscle strength. A: Absolute peak torque of elbow flexion and elbow extension on both sides between the two groups; B: Relative peak torques of elbow flexion and elbow extension on both sides between the two groups; C: Total work of elbow flexion and extension on both sides between the two groups; D: Average power of elbow flexion and extension on both sides between the two groups. BMD: Bone mineral density.

For the left elbow flexion, the high BMD group exhibited significantly greater APT and AP (both P < 0.05). However, no significant difference was observed in the RPT or TW of the left flexion (both P > 0.05). In contrast, for the right elbow flexion, the low BMD group exhibited significantly greater RPT (P < 0.05). However, no significant difference was observed in APT, TW, or AP of the right flexion (all P > 0.05) (Supplementary Table 8).

Wrist muscle strength data are presented in Figure 4. Compared with young men with low BMD, those with high BMD showed no significant differences in APT, RPT, TW, or AP in wrist flexion muscle groups on either side (all P > 0.05).

Figure 4 Wrist muscle strength. A: Absolute peak torque of wrist flexion and extension on both sides between the two groups; B: Relative peak torques of wrist flexion and extension on both sides between the two groups; C: Total work of wrist flexion and extension on both sides between the two groups; D: Average power of wrist flexion and extension on both sides between the two groups. BMD: Bone mineral density.

For the right wrist extension, the high BMD group demonstrated significantly greater APT (P < 0.05). However, no significant difference was observed in the RPT or TW of the left extension (both P > 0.05). Similarly, no significant difference was observed in APT, RPT, TW, or AP of the left extension (all P > 0.05) (Supplementary Table 9).

Comparisons of hip muscle strength are summarized in Figure 5. Young men with high BMD demonstrated significantly greater strength across most hip muscle metrics compared to those with low BMD.

Figure 5 Hip muscle strength. A: Absolute peak torque of hip flexion and extension on both sides between the two groups; B: Relative peak torques of hip flexion and extension on both sides between the two groups; C: Total work of hip flexion and extension on both sides between the two groups; D: Average power of hip flexion and extension on both sides between the two groups. BMD: Bone mineral density.

For the left hip extension, the high BMD group presented significantly greater APT, TW, AP (all P < 0.001), and RPT (P < 0.05). For the right hip extension, significant increases were observed in APT, TW, AP (all P < 0.001), and RPT (P < 0.01).

With respect to hip flexion, the high BMD group had significantly greater APT, TW, AP (all P < 0.001), and RPT (P < 0.05) in both the left and right hip flexion (Supplementary Table 10).

Knee muscle strength data are presented in Figure 6. For the left knee flexion, young men in the high BMD group demonstrated significantly greater APT, TW, and AP (all P < 0.01), whereas no significant difference was observed in RPT (P > 0.05). For the right knee flexion, the high BMD group demonstrated significantly greater APT and RPT (both P < 0.001), as well as greater TW and AP (both P < 0.01).

Figure 6 Knee muscle strength. A: Absolute peak torque of knee flexion and extension on both sides between the two groups; B: Relative peak torques of knee flexion and extension on both sides between the two groups; C: Total work of knee flexion and extension on both sides between the two groups; D: Average power of knee flexion and extension between the two groups. BMD: Bone mineral density.

With respect to the left knee extension, the high BMD group showed significant increases in TW, AP (both P < 0.01), and APT (P < 0.001), whereas no significant difference was observed in RPT (P > 0.05). Similarly, for the right knee extension, there were significant increases in APT, AP (both P < 0.01), and TW (P < 0.001), whereas no significant difference was observed in RPT (P > 0.05) (Supplementary Table 11).

Ankle muscle strength data are presented in Figure 7. Compared with young men with low BMD, those with high BMD showed no significant differences in APT, RPT, TW, or AP in the dorsiflexion and plantar flexion muscle groups on either side (all P > 0.05).

Figure 7 Ankle muscle strength. A: Absolute peak torque of ankle dorsiflexion and plantar flexion on both sides between the two groups; B: Relative peak torques of ankle dorsiflexion and plantar flexion on both sides between the two groups; C: Total work of ankle dorsiflexion and plantar flexion on both sides between the two groups; D: Average power of ankle dorsiflexion and plantar flexion on both sides between the two groups. BMD: Bone mineral density.

Agonist-to-antagonist muscle ratio data are presented in Figure 8. Compared with the low BMD group, young men with high BMD demonstrated a significantly higher agonist-to-antagonist ratio at the right knee (P < 0.01), while no significant between-group difference was observed at the left knee (P > 0.05). Similarly, no significant differences in agonist-to-antagonist ratios were found at the wrist, elbow, shoulder, hip, or ankle joints on either side (all P > 0.05) (Supplementary Table 12).

Figure 8 Results of the absolute peak torque ratio of active muscle to antagonist muscle in each joint. A: Absolute peak torque ratio of the agonist to antagonist of the wrist; B: Absolute peak torque ratio of the agonist to antagonist of the elbow; C: Absolute peak torque ratio of the agonist to antagonist of the shoulder; D: Absolute peak torque ratio of hip agonist to antagonist; E: Absolute peak torque ratio of agonist to antagonist of the knee; F: Absolute peak torque ratio of ankle agonist to antagonist muscle. BMD: Bone mineral density.

DISCUSSION

BMD at specific skeletal sites is primarily determined by the intensity and magnitude of mechanical loading rather than physical activity alone[11]. This principle aligns with Wolff’s law, which states that bone adapts its mass and architecture in response to mechanical demands[12]. Importantly, the degree of bone mass accumulation during growth periods significantly influences the risk of osteoporosis in adulthood[13].

Our study revealed that young men with low BMD demonstrated significantly poorer body composition (Supplementary Figure 1) and bone health (Supplementary Figure 2), both in total and regional terms (e.g., arms, legs, trunk), compared to their high BMD counterparts. Key LM distribution indices such as FM/weight, LM/height², and limb LM/height² were also markedly lower in the low BMD group. Interestingly, however, the high BMD group had significantly lower MBR and SBR. In terms of muscular strength across six major joints, those with low BMD demonstrated significantly reduced extensor and flexor strength in the shoulder, hip, and knee joints. Collectively, these findings suggest that young men with low BMD are characterized primarily by a relative deficit in muscular fitness.

Osteoporosis is defined by low bone mass and the deterioration of bone microarchitecture, conditions that collectively heighten susceptibility to fractures. It is therefore regarded as a serious public health concern[13]. Since childhood and adolescence are critical for skeletal development, low PBM during these stages is a significant risk factor for osteoporosis later in life[13]. Body composition, particularly LM and FM, is crucial for determining the BMD in young individuals. While LM has a well-established positive association with BMD due to mechanical loading, the relationship with FM is more complex and debated[13]. In this context, our study revealed that young men with low BMD had a lower LM distribution, which was reflected in their elevated MBR and SBR. Despite the theoretical link between a higher FM percentage and lower bone mass suggested by some studies[14], we did not observe this relationship in our cohort. Therefore, our findings strengthen the established evidence supporting a positive association between LM and BMD[15].

Beyond LM, muscular strength itself plays a crucial and independent role in maintaining BMD. This finding is supported by research demonstrating that high levels of muscular fitness are beneficial for bone health, especially among overweight and obese children[16]. Moreover, the type of strength is relevant; notably, isometric strength has been shown to correlate more strongly with positive bone health outcomes than dynamic strength[17]. Our findings align with and extend this understanding, reinforcing the view that muscular strength is a key marker of skeletal health in young adults. The significantly lower APT observed in the low-BMD group was markedly attenuated when normalized to body weight (RPT). This indicates that their reduced strength is primarily explained by smaller body size and LM, rather than impaired muscle quality or neuromuscular efficiency.

The development of low BMD in young adults is a multifactorial process influenced by an interplay of genetic, biological, environmental, and lifestyle factors. Key modifiable risks include low body weight, delayed puberty, and insufficient weight-bearing physical activity, all of which are associated with reduced areal or volumetric BMD[18]. Furthermore, the close relationship between bone and LM is largely governed by mechanical stimuli[18]. Increased loading, such as that from resistance exercise, promotes muscle hypertrophy and concurrent bone adaptation; conversely, reduced loading leads to declines in both muscle and bone integrity[19]. This relationship is clearly demonstrated in experimental models of prolonged bed rest[20] and limb immobilization[3], which result in significant detrimental effects on both tissues.

While the assessment of physical capacity and asymmetry should be context-specific and guided by the demands of the given exercise[21], our study found no significant differences in either interlimb asymmetry or agonist/antagonist ratios across the five movements tested between young men with high and low BMD. This pattern suggests that the musculoskeletal alterations associated with low BMD may reflect systemic adaptation rather than localized asymmetries.

Current evidence strongly supports the use of exercise interventions, particularly supervised progressive resistance training combined with weight-bearing activities, as a cornerstone management strategy for young men with low BMD[22]. Such regimens have been proven to slow the progression of bone and muscle loss, improve mobility and balance, and enhance quality of life[23]. In light of our study’s findings of lower LM and weaker muscle strength in young men with low BMD, targeted interventions to address these deficits are strongly indicated and align perfectly with established clinical guidelines[8].

There is currently no consensus on the BMD criteria for diagnosing osteoporosis in younger adults. This lack of consensus directly impacts clinical practice, as the optimal methods for investigating and monitoring low BMD remain unclear. Therefore, significant research efforts are urgently needed to establish clear guidelines.

CONCLUSION

These findings indicate that young men at risk for low BMD (Z score < -1.6) are characterized primarily by reduced muscular fitness.