超声评估2型糖尿病患者骨骼肌状态的临床价值

Clinical value of ultrasonography in assessing skeletal muscle status in patients with type 2 diabetes mellitus

摘要

目的 探讨超声多参数评估2型糖尿病（T2DM）患者骨骼肌状态与弹性改变的临床价值，筛选糖尿病合并肌少症的有效诊断指标。方法 纳入2024年5月至2025年12月新疆维吾尔自治区人民医院收治的T2DM患者130例，依据亚洲肌少症工作组（AWGS）2019诊断标准分为单纯T2DM组（94例）、T2DM合并肌少症组（36例），同期纳入健康体检者79例为对照组。3组均完成一般资料采集、生化指标检测、骨骼肌质量指数（ASMI）测定及肱二头肌、股直肌、腓肠肌超声参数收集。比较3组临床与超声指标差异，绘制受试者操作特征（ROC）曲线评价超声指标的诊断效能。结果 3组BMI、空腹血糖（FBG）、ASMI、6 m步速、握力、3 m起立行走时间差异均有统计学意义（均 P＜0.05）；T2DM合并肌少症组BMI、ASMI、6 m步速、握力均减低、超声测量肱二头肌厚度、腓肠肌厚度、腓肠肌杨氏模量、腓肠肌羽状角背屈位、跖屈位与单纯T2DM组差异有统计学意义（均 P＜0.05）。ROC曲线分析显示，腓肠肌羽状角跖屈位诊断T2DM合并肌少症的AUC最高（0.845，95%CI 0.766～0.924），腓肠肌羽状角背屈位（0.762，95%CI 0.666～0.858）、腓肠肌杨氏模量（0.761，95%CI 0.689～0.834）、肱二头肌厚度（0.733，95%CI 0.642～0.824）依次降低。结论 T2DM患者早期即可出现骨骼肌状态与功能异常，合并肌少症者损害更为显著；超声多参数可定量骨骼肌，其中腓肠肌羽状角跖屈位、腓肠肌羽状角背屈位、腓肠肌杨氏模量、肱二头肌厚度对T2DM合并肌少症诊断效能良好。

Abstract

Objective To investigate the clinical value of multiparametric ultrasonography in assessing skeletal muscle morphological and elastic changes in patients with type 2 diabetes mellitus (T2DM), and to screen effective diagnostic indicators for diabetes complicated with sarcopenia. Methods The study enrolled 130 patients with T2DM who were admitted to Xinjiang Uygur Autonomous Region People’s Hospital from May 2024 to December 2025. According to the 2019 diagnostic criteria of the Asian Working Group for Sarcopenia (AWGS), they were divided into the T2DM-only group ( n = 94) and the T2DM with sarcopenia group ( n = 36). Seventy-nine healthy individuals who underwent physical examination during the same period were enrolled as the control group. General data collection, biochemical indicator testing, appendicular skeletal muscle mass index (ASMI) measurement, and ultrasound parameter collection of the biceps brachii, rectus femoris, and gastrocnemius were completed in all three groups. Differences in clinical and ultrasound indicators among the three groups were compared, and receiver operating characteristic (ROC) curves were plotted to evaluate the diagnostic efficacy of ultrasound indicators. Results There were statistically significant differences among the three groups in body mass index (BMI), fasting blood glucose (FBG), ASMI, 6-m gait speed, grip strength, and 3-m timed up-and-go test time (all P ＜ 0.05). Compared with the T2DM-only group, the T2DM with sarcopenia group had lower BMI, ASMI, 6-m gait speed, and grip strength, and statistically significant differences were observed in ultrasound-measured biceps brachii thickness, gastrocnemius thickness, gastrocnemius Young’s modulus, and gastrocnemius pennation angle in dorsiflexion and plantarflexion positions (all P ＜ 0.05). ROC curve analysis showed that gastrocnemius pennation angle in the plantarflexion position had the highest area under ROC curve (AUC) for diagnosing T2DM complicated with sarcopenia (0.845, 95%CI 0.766-0.924), followed by gastrocnemius pennation angle in the dorsiflexion position (0.762, 95%CI 0.666-0.858), gastrocnemius Young’s modulus (0.761, 95%CI 0.689-0.834), and biceps brachii thickness (0.733, 95%CI 0.642-0.824). Conclusions Skeletal muscle morphological and functional abnormalities may occur at an early stage in patients with T2DM, and the impairment is more pronounced in those complicated with sarcopenia. Multiparametric ultrasonography can quantitatively assess skeletal muscle, among which gastrocnemius pennation angle in the plantarflexion position, gastrocnemius pennation angle in the dorsiflexion position, gastrocnemius Young’s modulus, and biceps brachii thickness have good diagnostic efficacy for T2DM complicated with sarcopenia.

关键词

超声检查 / 2型糖尿病 / 骨骼肌 / 肌少症 / 剪切波弹性成像 / 羽状角

Key words

Ultrasonography / Type 2 diabetes mellitus / Skeletal muscle / Sarcopenia / Shear wave elastography / Pennation angle

参考文献

[1] Xu Y, Lu J, Li M, et al. Diabetes in China part 1: epidemiology and risk factors[J]. Lancet Public Health, 2024, 9(12): e1089-e1097. DOI: 10.1016/S2468-2667(24)00250-0.

[2] 任翔宇, 沈飞, 金玲, 等 . 运动促进骨骼肌健康的新视角: 基于Rac1/PAK1/p38 MAPK信号通路改善肌生成和糖代谢的研究进展与展望[J]. 中国体育科技, 2023, 59(5): 79-87. DOI: 10.16470/j.csst.2021096.

[3] Ren X Y, Shen F, Jin L, et al. A new perspective on exercise promoting skeletal muscle health: research progress and prospect of improving myogenesis and glucose metabolism based on Rac1/PAK1/p38 MAPK signaling pathway[J]. China Sport Sci Technol, 2023, 59(5): 79-87. DOI: 10.16470/j.csst.2021096.

[4] Lopez-Pedrosa J M, Camprubi-Robles M, Guzman-Rolo G, et al. The vicious cycle of type 2 diabetes mellitus and skeletal muscle atrophy: clinical, biochemical, and nutritional bases[J]. Nutrients, 2024, 16(1): 172. DOI: 10.3390/nu16010172.

[5] 孙清, 吴玉霄, 崔立敏. 中国2型糖尿病患者肌少-骨质疏松症患病率的Meta分析[J]. 中国全科医学, 2025, 28(12): 1520-1526. DOI: 10.12114/j.issn.1007-9572.2024.0449.

[6] Sun Q, Wu Y X, Cui L M. The prevalence of osteosarcopenia in Chinese patients with type 2 diabetes mellitus: a meta-analysis[J]. Chin Gen Pract, 2025, 28(12): 1520-1526. DOI: 10.12114/j.issn.1007-9572.2024.0449.

[7] Wu W, Liu M, Zeng Q, et al. Research progress on evaluation methods for skeletal muscle mass assessment in sarcopenia (Review)[J]. Oncol Lett, 2025, 30(3): 1-13. DOI: 10.3892/ol.2025.15169.

[8] 王译欧, 黄晨曦, 张晓东. 磁共振成像在肌少症评估中的研究进展[J]. 磁共振成像, 2025, 16(7): 209-214. DOI: 10.12015/issn.1674-8034.2025.07.033.

[9] Wang Y O, Huang C X, Zhang X D. Advances in magnetic resonance imaging for the assessment of sarcopenia[J]. Chin J Magn Reson Imaging, 2025, 16(7): 209-214. DOI: 10.12015/issn.1674-8034.2025.07.033.

[10] Ashir A, Jerban S, Barrère V, et al. Skeletal muscle assessment using quantitative ultrasound: a narrative review[J]. Sensors (Basel), 2023, 23(10): 4763. DOI: 10.3390/s23104763.

[11] 刘娟, 丁清清, 周白瑜, 等 . 中国老年人肌少症诊疗专家共识(2021)[J]. 中华老年医学杂志, 2021, 40(8): 943-952. DOI: 10.3760/cma.j.issn.0254-9026.2021.08.001.

[12] Liu J, Ding Q Q, Zhou B Y, et al. Chinese expert consensus on diagnosis and treatment for elderly with sarcopenia (2021)[J]. Chin J Geriatr, 2021, 40(8): 943-952. DOI: 10.3760/cma.j.issn.0254-9026.2021.08.001.

[13] Chen L K, Woo J, Assantachai P, et al. Asian working group for sarcopenia: 2019 consensus update on sarcopenia diagnosis and treatment[J]. J Am Med Dir Assoc, 2020, 21(3): 300-307.e2. DOI: 10.1016/j.jamda.2019.12.012.

[14] 中华医学会糖尿病学分会. 中国2型糖尿病防治指南(2020年版)[J]. 中华内分泌代谢杂志, 2021, 37(4): 311-398. DOI: 10.3760/cma.j.cn311282-20210304-00142.

[15] Chinese Diabetes Society. Guideline for the prevention and treatment of type 2 diabetes mellitus in China (2020 edition)[J]. Chin J Endocrinol Metab, 2021, 37(4): 311-398. DOI: 10.3760/cma.j.cn311282-20210304-00142.

[16] Zhu S, Lin W, Chen S, et al. The correlation of muscle thickness and pennation angle assessed by ultrasound with sarcopenia in elderly Chinese community dwellers[J]. Clin Interv Aging, 2019, 14: 987-996. DOI: 10.2147/CIA.S201777.

[17] 穆晶晶, 徐莉力, 张巧莹, 等 . 剪切波弹性成像技术在骨骼肌及周围神经系统的应用研究进展[J/OL]. 中华医学超声杂志(电子版), 2018, 15(7): 494-496. DOI: 10.3877/cma.j.issn.1672-6448.2018.07.004.

[18] Mu J J, Xu L L, Zhang Q Y, et al. Application of shear wave elastic elastography in skeletal muscle and nervous system[J/OL]. Chin J Med Ultrasound (Electron Ed), 2018, 15(7): 494-496. DOI: 10.3877/cma.j.issn.1672-6448.2018.07.004.

[19] Jaiswal N, Gavin M G, Quinn W J, et al. The role of skeletal muscle Akt in the regulation of muscle mass and glucose homeostasis[J]. Mol Metab, 2019, 28: 1-13. DOI: 10.1016/j.molmet.2019.08.001.

[20] 梁眉黛, 杨秀颖, 杜冠华. 2型糖尿病诱导骨骼肌萎缩机制及常用降糖药影响研究进展[J]. 药学学报, 2022, 57(3): 568-575. DOI: 10.16438/j.0513-4870.2021-1217.

[21] Liang M D, Yang X Y, Du G H. The mechanisms of type 2 diabetic skeletal muscle atrophy and the effects of commonly used hypoglycemic drugs: a review[J]. Acta Pharm Sin, 2022, 57(3): 568-575. DOI: 10.16438/j.0513-4870.2021-1217.

[22] Hayashi K, Sato K, Ochi S, et al. Inhibitory effects of Saururus chinensis extract on receptor for advanced glycation end-products-dependent inflammation and diabetes-induced dysregulation of vasodilation [J]. Int J Mol Sci, 2022, 23(10): 5757. DOI: 10.3390/ijms23105757.

[23] Papachristou S, Rizzo M, Papanas N . Advanced glycation end products: do they impair bone health in Diabetes[J]. Exp Clin Endocrinol Diabetes, 2022, 130(10): 636-637. DOI: 10.1055/a-1903-1752.

[24] Kang J H, Kim D H, Yoo J, et al. Sinapine suppresses ROS-induced C2C12 myoblast cell death through MAPK and autophagy pathways[J]. Food Sci Biotechnol, 2024, 33(15): 3629-3637. DOI: 10.1007/s10068-024-01718-6.

[25] Agrawal S, Chakole S, Shetty N, et al. Exploring the role of oxidative stress in skeletal muscle atrophy: mechanisms and implications[J]. Cureus, 2023, 15(7): e42178. DOI: 10.7759/cureus.42178.

[26] 罗雅雯, 李俊, 付艳芹. 住院2型糖尿病合并肌少症患者的影响因素分析[J]. 中国医药导报, 2025, 22(12): 14-18. DOI: 10.20047/j.issn1673-7210.2025.12.03.

[27] Luo Y W, Li J, Fu Y Q. Analysis of influencing factors in elderly inpatients with diabetes mellitus type 2 combined with sarcopenia[J]. China Med Her, 2025, 22(12): 14-18. DOI: 10.20047/j.issn1673-7210.2025.12.03.

[28] 钟文霞, 杨娜, 赵浩, 等 . 高频超声在糖尿病足部肌及小腿腓肠肌早期病变诊断中的应用[J]. 影像研究与医学应用, 2021, 5(20): 201-202.

[29] Zhong W X, Yang N, Zhao H, et al. Application of high-frequency ultrasound in early diagnosis of diabetic foot muscle and gastrocnemius muscle[J]. J Imaging Res Med Appl, 2021, 5(20): 201-202.

[30] 鲁亚玲, 罗定强, 彭海旭, 等 . 常规超声联合超声弹性成像在评估2型糖尿病肌少症中的应用[J]. 实用医学影像杂志, 2022, 23(6): 553-556. DOI: 10.16106/j.cnki.cn14-1281/r.2022.06.003.

[31] Lu Y L, Luo D Q, Peng H X, et al. Application of conventional ultrasound combined with ultrasound elastography in the evaluation of type 2diabetic sarcopenia[J]. J Pract Med Imaging, 2022, 23(6): 553-556. DOI: 10.16106/j.cnki.cn14-1281/r.2022.06.003.

[32] Granic A, Simoes D C M, Bowen T S, et al. Ageing of human myofibres in the Vastus Lateralis muscle: a narrative review[J]. Ageing Res Rev, 2026, 115: 103022. DOI: 10.1016/j.arr.2026.103022.

[33] Alraddadi A S . The morphometric parameters of the biceps brachii: cadaveric study[J]. Surg Radiologic Anat, 2024, 46(4): 463-472. DOI: 10.1007/s00276-024-03328-7.

[34] Schoenfeld B J, Vigotsky A D, Grgic J, et al. Do the anatomical and physiological properties of a muscle determine its adaptive response to different loading protocols[J]. Physiol Rep, 2020, 8(9): e14427. DOI: 10.14814/phy2.14427.

[35] Albers P H, Pedersen A J, Birk J B, et al. Human muscle fiber type-specific insulin signaling: impact of obesity and type 2 diabetes[J]. Diabetes, 2015, 64(2): 485-497. DOI: 10.2337/db14-0590.

[36] Eid S A, Rumora A E, Beirowski B, et al. New perspectives in diabetic neuropathy[J]. Neuron, 2023, 111(17): 2623-2641. DOI: 10.1016/j.neuron.2023.05.003.

[37] Yang X, Xue P, Liu Z, et al. SESN2 prevents the slow-to-fast myofiber shift in denervated atrophy via AMPK/PGC-1α pathway [J]. Cell Mol Biol Lett, 2022, 27(1): 66. DOI: 10.1186/s11658-022-00367-z.

[38] Chen K, Hu S, Liao R, et al. Application of conventional ultrasound coupled with shear wave elastography in the assessment of muscle strength in patients with type 2 diabetes[J]. Quant Imaging Med Surg, 2024, 14(2): 1716-1728. DOI: 10.21037/qims-23-1152.

[39] Aluganti Narasimhulu C A, Singla D K . Abstract 14193: bmp-7 ameliorates lipid accumulation induced, Hmgb1 initiated pyroptosis leading to sarcopenia, muscle deterioration and adverse muscle remodeling in diabetes[J]. Circulation, 2021, 144(suppl_1): 14193. DOI: 10.1161/circ.144.suppl_1.14193.

[40] 宋宝娜, 林萍, 王琴. 钠-葡萄糖共转运蛋白2抑制剂对老年2型糖尿病患者发生肌肉减少症的影响[J]. 中华全科医学, 2023, 21(6): 1016-1020. DOI: 10.16766/j.cnki.issn.1674-4152.003039.

[41] Song B N, Lin P, Wang Q. Effect of sodium-glucose cotransporter 2 inhibitor on sarcopenia in elderly patients with type 2 diabetes[J]. Chin J Gen Pract, 2023, 21(6): 1016-1020. DOI: 10.16766/j.cnki.issn.1674-4152.003039.

[42] 李倩, 李振兴, 乔鹏燕, 等 . 剪切波弹性成像在骨骼肌研究领域应用的可视化分析[J]. 中国组织工程研究, 2026, 30(23): 6021-6029. DOI: 10.12307/2026.364.

[43] Li Q, Li Z X, Qiao P Y, et al. Visual analysis of shear wave elastography in skeletal muscle research[J]. Chin J Tissue Eng Res, 2026, 30(23): 6021-6029. DOI: 10.12307/2026.364.

[44] Figueira A C C, Pereira A, Leitão L, et al. Effects of Moderate Exercise Training on Cancer-Induced Muscle Wasting[J]. Healthcare (Basel), 2023, 11(19).

[45] Cardaci T D, VanderVeen B N, Huss A R, et al. Decreased skeletal muscle intramyocellular lipid droplet-mitochondrial contact contributes to myosteatosis in cancer cachexia[J]. Am J Physiol Cell Physiol, 2024, 327(3): C684-C697. DOI: 10.1152/ajpcell.00345.2024.

[46] Galasso L, Vitale F, Pietramale M, et al. Echoes of muscle aging: the emerging role of shear wave elastography in sarcopenia diagnosis[J]. Diagnostics (Basel), 2025, 15(19): 2495. DOI: 10.3390/diagnostics15192495.

[47] Giovannini S, Brau F, Forino R, et al. Sarcopenia: diagnosis and management, state of the art and contribution of ultrasound[J]. J Clin Med, 2021, 10(23): 5552. DOI: 10.3390/jcm10235552.

[48] Csiernik B, Edgar M, DeGraauw C, et al. The utility of bioelectrical impedance analysis in the diagnosis of sarcopenia: a systematic review[J]. J Can Chiropr Assoc, 2022, 66(2): 118-129.

基金资助

新疆维吾尔自治区卫生健康保健科研专项项目(BL202407)

新疆维吾尔自治区自然科学基金(2022D01C149)