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Published in: BMC Musculoskeletal Disorders 1/2022

Open Access 01-12-2022 | Sarcopenia | Research

Creatinine-to-cystatin C ratio as a marker of sarcopenia for identifying osteoporosis in male patients with type 2 diabetes mellitus

Authors: Huifang Dai, Jing Xu

Published in: BMC Musculoskeletal Disorders | Issue 1/2022

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Abstract

Background

Type 2 diabetes mellitus (T2DM) is associated with the increased incidence rate of sarcopenia and osteoporosis. Serum creatinine-to-cystatin C ratio (CCR) is a novel and simple tool which can be used as an index of sarcopenia. This study aims to investigate the association between CCR and osteoporosis as well as bone mineral density (BMD) in T2DM patients.

Methods

Four hundred eighteen T2DM patients were recruited, including 166 females and 252 males. General information, BMD data and laboratory data were collected. The correlation between CCR, BMD, bone metabolism markers and osteoporosis was explored by spearman correlation, receiver-operating characteristic (ROC) curve analysis and multiple regression analysis.

Results

Spearman correlation analysis showed that there was a positive correlation between CCR and BMD as well as serum calcium in male patients (r = 0.181–0.381, P < 0.01), but such correlation was not found in the female group. In multivariate regression analysis, it was found that there was a significant correlation between CCR and BMD of total lumbar spine, hip as well as femoral neck in male patients. ROC curve showed that the optimal cut-off value of CCR for predicting osteoporosis in male patients was 6.73 with the sensitivity of 88% and specificity of 63%.

Conclusion

In male T2DM patients, CCR was negatively correlated with osteoporosis and positively correlated with BMD.
Literature
1.
go back to reference Lin X, Xiong D, Peng YQ, Sheng ZF, Wu XY, Wu XP, Wu F, Yuan LQ, Liao EY. Epidemiology and management of osteoporosis in the People’s Republic of China: current perspectives. Clin Interv Aging. 2015;10:1017–33.PubMedPubMedCentral Lin X, Xiong D, Peng YQ, Sheng ZF, Wu XY, Wu XP, Wu F, Yuan LQ, Liao EY. Epidemiology and management of osteoporosis in the People’s Republic of China: current perspectives. Clin Interv Aging. 2015;10:1017–33.PubMedPubMedCentral
2.
go back to reference Janghorbani M, Van Dam RM, Willett WC, Hu FB. Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol. 2007;166(5):495–505.CrossRef Janghorbani M, Van Dam RM, Willett WC, Hu FB. Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol. 2007;166(5):495–505.CrossRef
3.
go back to reference Vestergaard P. Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes–a meta-analysis. Osteoporos Int. 2007;18(4):427–44.CrossRef Vestergaard P. Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes–a meta-analysis. Osteoporos Int. 2007;18(4):427–44.CrossRef
4.
go back to reference Holm JP, Hyldstrup L, Jensen JB. Time trends in osteoporosis risk factor profiles: a comparative analysis of risk factors, comorbidities, and medications over twelve years. Endocrine. 2016;54(1):241–55.CrossRef Holm JP, Hyldstrup L, Jensen JB. Time trends in osteoporosis risk factor profiles: a comparative analysis of risk factors, comorbidities, and medications over twelve years. Endocrine. 2016;54(1):241–55.CrossRef
5.
go back to reference Chua JR, Tee ML. Association of sarcopenia with osteoporosis in patients with chronic obstructive pulmonary disease. Osteoporos Sarcopenia. 2020;6(3):129–32.CrossRef Chua JR, Tee ML. Association of sarcopenia with osteoporosis in patients with chronic obstructive pulmonary disease. Osteoporos Sarcopenia. 2020;6(3):129–32.CrossRef
6.
go back to reference Kim JE, Lee YH, Huh JH, Kang DR, Rhee Y, Lim SK. Early-stage chronic kidney disease, insulin resistance, and osteoporosis as risk factors of sarcopenia in aged population: the fourth Korea National Health and Nutrition Examination Survey (KNHANES IV), 2008–2009. Osteoporos Int. 2014;25(9):2189–98.CrossRef Kim JE, Lee YH, Huh JH, Kang DR, Rhee Y, Lim SK. Early-stage chronic kidney disease, insulin resistance, and osteoporosis as risk factors of sarcopenia in aged population: the fourth Korea National Health and Nutrition Examination Survey (KNHANES IV), 2008–2009. Osteoporos Int. 2014;25(9):2189–98.CrossRef
7.
go back to reference Saeki C, Oikawa T, Kanai T, Nakano M, Torisu Y, Sasaki N, Abo M, Saruta M, Tsubota A. Relationship between osteoporosis, sarcopenia, vertebral fracture, and osteosarcopenia in patients with primary biliary cholangitis. Eur J Gastroenterol Hepatol. 2021;33(5):731–7.CrossRef Saeki C, Oikawa T, Kanai T, Nakano M, Torisu Y, Sasaki N, Abo M, Saruta M, Tsubota A. Relationship between osteoporosis, sarcopenia, vertebral fracture, and osteosarcopenia in patients with primary biliary cholangitis. Eur J Gastroenterol Hepatol. 2021;33(5):731–7.CrossRef
8.
go back to reference Pan Y, Xu J. Association between muscle mass, bone mineral density and osteoporosis in type 2 diabetes. J Diabetes Investig. 2022;13(2):351–8.CrossRef Pan Y, Xu J. Association between muscle mass, bone mineral density and osteoporosis in type 2 diabetes. J Diabetes Investig. 2022;13(2):351–8.CrossRef
9.
go back to reference Osaka T, Hamaguchi M, Hashimoto Y, Ushigome E, Tanaka M, Yamazaki M, Fukui M. Decreased the creatinine to cystatin C ratio is a surrogate marker of sarcopenia in patients with type 2 diabetes. Diabetes Res Clin Pract. 2018;139:52–8.CrossRef Osaka T, Hamaguchi M, Hashimoto Y, Ushigome E, Tanaka M, Yamazaki M, Fukui M. Decreased the creatinine to cystatin C ratio is a surrogate marker of sarcopenia in patients with type 2 diabetes. Diabetes Res Clin Pract. 2018;139:52–8.CrossRef
10.
go back to reference Dai H, Xu J. Preoperative geriatric nutritional risk index is an independent prognostic factor for postoperative survival after gallbladder cancer radical surgery. BMC Surg. 2022;22(1):133.CrossRef Dai H, Xu J. Preoperative geriatric nutritional risk index is an independent prognostic factor for postoperative survival after gallbladder cancer radical surgery. BMC Surg. 2022;22(1):133.CrossRef
11.
go back to reference Sjostrom P, Tidman M, Jones I. Determination of the production rate and non-renal clearance of cystatin C and estimation of the glomerular filtration rate from the serum concentration of cystatin C in humans. Scand J Clin Lab Invest. 2005;65(2):111–24.CrossRef Sjostrom P, Tidman M, Jones I. Determination of the production rate and non-renal clearance of cystatin C and estimation of the glomerular filtration rate from the serum concentration of cystatin C in humans. Scand J Clin Lab Invest. 2005;65(2):111–24.CrossRef
12.
go back to reference Gojanovic M, Holloway-Kew KL, Hyde NK, Mohebbi M, Shivappa N, Hebert JR, O’Neil A, Pasco JA. The dietary inflammatory index is associated with low muscle mass and low muscle function in older Australians. Nutrients. 2021;13(4):1166.CrossRef Gojanovic M, Holloway-Kew KL, Hyde NK, Mohebbi M, Shivappa N, Hebert JR, O’Neil A, Pasco JA. The dietary inflammatory index is associated with low muscle mass and low muscle function in older Australians. Nutrients. 2021;13(4):1166.CrossRef
13.
go back to reference Kanis JA. Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: synopsis of a WHO report. WHO Study Group. Osteoporos Int. 1994;4(6):368–81.CrossRef Kanis JA. Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: synopsis of a WHO report. WHO Study Group. Osteoporos Int. 1994;4(6):368–81.CrossRef
14.
go back to reference Liu-Ambrose T, Eng JJ, Khan KM, Carter ND, McKay HA. Older women with osteoporosis have increased postural sway and weaker quadriceps strength than counterparts with normal bone mass: overlooked determinants of fracture risk? J Gerontol A Biol Sci Med Sci. 2003;58(9):M862–6.CrossRef Liu-Ambrose T, Eng JJ, Khan KM, Carter ND, McKay HA. Older women with osteoporosis have increased postural sway and weaker quadriceps strength than counterparts with normal bone mass: overlooked determinants of fracture risk? J Gerontol A Biol Sci Med Sci. 2003;58(9):M862–6.CrossRef
15.
go back to reference Bonewald LF, Kiel DP, Clemens TL, Esser K, Orwoll ES, O’Keefe RJ, Fielding RA. Forum on bone and skeletal muscle interactions: summary of the proceedings of an ASBMR workshop. J Bone Miner Res. 2013;28(9):1857–65.CrossRef Bonewald LF, Kiel DP, Clemens TL, Esser K, Orwoll ES, O’Keefe RJ, Fielding RA. Forum on bone and skeletal muscle interactions: summary of the proceedings of an ASBMR workshop. J Bone Miner Res. 2013;28(9):1857–65.CrossRef
16.
go back to reference Binkley N, Krueger D, Buehring B. What’s in a name revisited: should osteoporosis and sarcopenia be considered components of “dysmobility syndrome?” Osteoporos Int. 2013;24(12):2955–9.CrossRef Binkley N, Krueger D, Buehring B. What’s in a name revisited: should osteoporosis and sarcopenia be considered components of “dysmobility syndrome?” Osteoporos Int. 2013;24(12):2955–9.CrossRef
17.
go back to reference Cooper C, Dere W, Evans W, Kanis JA, et al. Frailty and sarcopenia: definitions and outcome parameters. Osteoporos Int. 2012;23(7):1839–48.CrossRef Cooper C, Dere W, Evans W, Kanis JA, et al. Frailty and sarcopenia: definitions and outcome parameters. Osteoporos Int. 2012;23(7):1839–48.CrossRef
18.
go back to reference Haderslev KV, Haderslev PH, Staun M. Accuracy of body composition measurements by dual energy x-ray absorptiometry in underweight patients with chronic intestinal disease and in lean subjects. Dyn Med. 2005;4(1):1.CrossRef Haderslev KV, Haderslev PH, Staun M. Accuracy of body composition measurements by dual energy x-ray absorptiometry in underweight patients with chronic intestinal disease and in lean subjects. Dyn Med. 2005;4(1):1.CrossRef
19.
go back to reference Patel SS, Molnar MZ, Tayek JA, Ix JH, Noori N, Benner D, Heymsfield S, Kopple JD, Kovesdy CP, Kalantar-Zadeh K. Serum creatinine as a marker of muscle mass in chronic kidney disease: results of a cross-sectional study and review of literature. J Cachexia Sarcopenia Muscle. 2013;4(1):19–29.CrossRef Patel SS, Molnar MZ, Tayek JA, Ix JH, Noori N, Benner D, Heymsfield S, Kopple JD, Kovesdy CP, Kalantar-Zadeh K. Serum creatinine as a marker of muscle mass in chronic kidney disease: results of a cross-sectional study and review of literature. J Cachexia Sarcopenia Muscle. 2013;4(1):19–29.CrossRef
20.
go back to reference Baxmann AC, Ahmed MS, Marques NC, Menon VB, Pereira AB, Kirsztajn GM, Heilberg IP. Influence of muscle mass and physical activity on serum and urinary creatinine and serum cystatin C. Clin J Am Soc Nephrol. 2008;3(2):348–54.CrossRef Baxmann AC, Ahmed MS, Marques NC, Menon VB, Pereira AB, Kirsztajn GM, Heilberg IP. Influence of muscle mass and physical activity on serum and urinary creatinine and serum cystatin C. Clin J Am Soc Nephrol. 2008;3(2):348–54.CrossRef
21.
go back to reference Wyss M, Kaddurah-Daouk R. Creatine and creatinine metabolism. Physiol Rev. 2000;80(3):1107–213.CrossRef Wyss M, Kaddurah-Daouk R. Creatine and creatinine metabolism. Physiol Rev. 2000;80(3):1107–213.CrossRef
22.
go back to reference Francis RM, Peacock M, Barkworth SA. Renal impairment and its effects on calcium metabolism in elderly women. Age Ageing. 1984;13(1):14–20.CrossRef Francis RM, Peacock M, Barkworth SA. Renal impairment and its effects on calcium metabolism in elderly women. Age Ageing. 1984;13(1):14–20.CrossRef
23.
go back to reference Vieth R, Ladak Y, Walfish PG. Age-related changes in the 25-hydroxyvitamin D versus parathyroid hormone relationship suggest a different reason why older adults require more vitamin D. J Clin Endocrinol Metab. 2003;88(1):185–91.CrossRef Vieth R, Ladak Y, Walfish PG. Age-related changes in the 25-hydroxyvitamin D versus parathyroid hormone relationship suggest a different reason why older adults require more vitamin D. J Clin Endocrinol Metab. 2003;88(1):185–91.CrossRef
24.
go back to reference Hirai K, Tanaka A, Homma T, Goto Y, Akimoto K, Uno T, Yoshitaka U, Miyata Y, Inoue H, Ohta S, et al. Serum creatinine/cystatin C ratio as a surrogate marker for sarcopenia in patients with chronic obstructive pulmonary disease. Clin Nutr. 2021;40(3):1274–80.CrossRef Hirai K, Tanaka A, Homma T, Goto Y, Akimoto K, Uno T, Yoshitaka U, Miyata Y, Inoue H, Ohta S, et al. Serum creatinine/cystatin C ratio as a surrogate marker for sarcopenia in patients with chronic obstructive pulmonary disease. Clin Nutr. 2021;40(3):1274–80.CrossRef
25.
go back to reference Fu X, Tian Z, Wen S, Sun H, Thapa S, Xiong H, Liu H, Li L, Yu S. A new index based on serum creatinine and cystatin C is useful for assessing sarcopenia in patients with advanced cancer. Nutrition. 2021;82:111032.CrossRef Fu X, Tian Z, Wen S, Sun H, Thapa S, Xiong H, Liu H, Li L, Yu S. A new index based on serum creatinine and cystatin C is useful for assessing sarcopenia in patients with advanced cancer. Nutrition. 2021;82:111032.CrossRef
26.
go back to reference Lu YW, Tsai YL, Chou RH, Kuo CS, Chang CC, Huang PH, Lin SJ. Serum creatinine to cystatin C ratio is associated with major adverse cardiovascular events in patients with obstructive coronary artery disease. Nutr Metab Cardiovasc Dis. 2021;31(5):1509–15.CrossRef Lu YW, Tsai YL, Chou RH, Kuo CS, Chang CC, Huang PH, Lin SJ. Serum creatinine to cystatin C ratio is associated with major adverse cardiovascular events in patients with obstructive coronary artery disease. Nutr Metab Cardiovasc Dis. 2021;31(5):1509–15.CrossRef
27.
go back to reference Tabara Y, Okada Y, Ochi M, Ohyagi Y, Igase M. Association of creatinine-to-cystatin c ratio with myosteatosis and physical performance in older adults: the Japan shimanami health promoting program. J Am Med Dir Assoc. 2021;22(11):2366-2372.e3.CrossRef Tabara Y, Okada Y, Ochi M, Ohyagi Y, Igase M. Association of creatinine-to-cystatin c ratio with myosteatosis and physical performance in older adults: the Japan shimanami health promoting program. J Am Med Dir Assoc. 2021;22(11):2366-2372.e3.CrossRef
28.
go back to reference Srikanthan P, Hevener AL, Karlamangla AS. Sarcopenia exacerbates obesity-associated insulin resistance and dysglycemia: findings from the national health and nutrition examination survey III. PLoS One. 2010;5(5):e10805.CrossRef Srikanthan P, Hevener AL, Karlamangla AS. Sarcopenia exacerbates obesity-associated insulin resistance and dysglycemia: findings from the national health and nutrition examination survey III. PLoS One. 2010;5(5):e10805.CrossRef
29.
go back to reference Landi F, Cruz-Jentoft AJ, Liperoti R, Russo A, Giovannini S, Tosato M, Capoluongo E, Bernabei R, Onder G. Sarcopenia and mortality risk in frail older persons aged 80 years and older: results from ilSIRENTE study. Age Ageing. 2013;42(2):203–9.CrossRef Landi F, Cruz-Jentoft AJ, Liperoti R, Russo A, Giovannini S, Tosato M, Capoluongo E, Bernabei R, Onder G. Sarcopenia and mortality risk in frail older persons aged 80 years and older: results from ilSIRENTE study. Age Ageing. 2013;42(2):203–9.CrossRef
30.
go back to reference Liu W, Zhu X, Tan X, Yang L, Wang Y, Diao S, Huang S, Zhang X, Yang Y, Ni J. Predictive Value of Serum Creatinine/Cystatin C in Acute Ischemic Stroke Patients under Nutritional Intervention. J Nutr Health Aging. 2021;25(3):335–9.CrossRef Liu W, Zhu X, Tan X, Yang L, Wang Y, Diao S, Huang S, Zhang X, Yang Y, Ni J. Predictive Value of Serum Creatinine/Cystatin C in Acute Ischemic Stroke Patients under Nutritional Intervention. J Nutr Health Aging. 2021;25(3):335–9.CrossRef
31.
go back to reference Qiu S, Cai X, Yuan Y, Xie B, Sun Z, Wu T. Changes in creatinine-to-cystatin C ratio over 4 years, risk of diabetes, and cardiometabolic control: the China health and retirement longitudinal study. J Diabetes. 2021;13(12):1025–33.CrossRef Qiu S, Cai X, Yuan Y, Xie B, Sun Z, Wu T. Changes in creatinine-to-cystatin C ratio over 4 years, risk of diabetes, and cardiometabolic control: the China health and retirement longitudinal study. J Diabetes. 2021;13(12):1025–33.CrossRef
32.
go back to reference Zofkova I. Hormonal aspects of the muscle-bone unit. Physiol Res. 2008;57(Suppl 1):S159-169.CrossRef Zofkova I. Hormonal aspects of the muscle-bone unit. Physiol Res. 2008;57(Suppl 1):S159-169.CrossRef
33.
go back to reference Macdonald H, Kontulainen S, Petit M, Janssen P, McKay H. Bone strength and its determinants in pre- and early pubertal boys and girls. Bone. 2006;39(3):598–608.CrossRef Macdonald H, Kontulainen S, Petit M, Janssen P, McKay H. Bone strength and its determinants in pre- and early pubertal boys and girls. Bone. 2006;39(3):598–608.CrossRef
34.
go back to reference Lang TF. The bone-muscle relationship in men and women. J Osteoporos. 2011;2011:702735.CrossRef Lang TF. The bone-muscle relationship in men and women. J Osteoporos. 2011;2011:702735.CrossRef
35.
go back to reference Thomas T, Burguera B. Is leptin the link between fat and bone mass? J Bone Miner Res. 2002;17(9):1563–9.CrossRef Thomas T, Burguera B. Is leptin the link between fat and bone mass? J Bone Miner Res. 2002;17(9):1563–9.CrossRef
36.
go back to reference Mudali S, Dobs AS. Effects of testosterone on body composition of the aging male. Mech Ageing Dev. 2004;125(4):297–304.CrossRef Mudali S, Dobs AS. Effects of testosterone on body composition of the aging male. Mech Ageing Dev. 2004;125(4):297–304.CrossRef
37.
go back to reference Hsu CY, Chen LR, Chen KH. Osteoporosis in patients with chronic kidney diseases: a systemic review. Int J Mol Sci. 2020;21(18):6846.CrossRef Hsu CY, Chen LR, Chen KH. Osteoporosis in patients with chronic kidney diseases: a systemic review. Int J Mol Sci. 2020;21(18):6846.CrossRef
Metadata
Title
Creatinine-to-cystatin C ratio as a marker of sarcopenia for identifying osteoporosis in male patients with type 2 diabetes mellitus
Authors
Huifang Dai
Jing Xu
Publication date
01-12-2022
Publisher
BioMed Central
Published in
BMC Musculoskeletal Disorders / Issue 1/2022
Electronic ISSN: 1471-2474
DOI
https://doi.org/10.1186/s12891-022-05636-8

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