Diabetes & Metabolism Journal

Original Articles

Cardiovascular Risk/Epidemiology
Normalized Creatinine-to-Cystatin C Ratio and Risk of Cardiometabolic Multimorbidity in Middle-Aged and Older Adults: Insights from the China Health and Retirement Longitudinal Study: Honglin Sun, Zhenyu Wu, Guang Wang, Jia Liu; Received May 2, 2024 Accepted November 15, 2024 Published online January 20, 2025; DOI: https://doi.org/10.4093/dmj.2024.0100 [Epub ahead of print]

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Abstract PDF: Background
Normalized creatinine-to-cystatin C ratio (NCCR) was reported to approximate relative skeletal muscle mass and diabetes risk. However, the association between NCCR and cardiometabolic multimorbidity (CMM) remains elusive. This study aimed to explore their relationship in a large-scale prospective cohort.
Methods
This study included 5,849 middle-age and older participants from the China Health and Retirement Longitudinal Study (CHARLS) enrolled between 2011 and 2012. The baseline NCCR was determined as creatinine (mg/dL)/cystatin C (mg/L)×10/body mass (kg). CMM was defined as the simultaneous occurrence of two or more of the following conditions: heart disease, stroke, and type 2 diabetes mellitus. Logistic regression analysis and Cox regression analysis were employed to estimate the relationship between NCCR and CMM. The joint effect of body mass index and NCCR on the risk of CMM were further analyzed.
Results
During a median 4-year follow-up, 227 (3.9%) participants developed CMM. The risk of CMM was significantly decreased with per standard deviation increase of NCCR (odds ratio, 0.72; 95% confidence interval, 0.62 to 0.85) after adjustment for confounders (P<0.001). Further sex-specific analysis found significant negative associations between NCCR and CMM in female either without or with one CMM component at baseline, which was attenuated in males but remained statistically significant among those with one basal CMM component. Notably, non-obese individuals with high NCCR levels had the lowest CMM risk compared to obese counterparts with low NCCR levels in both genders.
Conclusion
High NCCR was independently associated with reduced risk of CMM in middle-aged and older adults in China, particularly females.

Cardiovascular Risk/Epidemiology
The Ratio of Estimated Glomerular Filtration Rate Based on Cystatin C and Creatinine Reflecting Cardiovascular Risk in Diabetic Patients: Ah Reum Khang, Min Jin Lee, Dongwon Yi, Yang Ho Kang; Diabetes Metab J. 2023;47(3):415-425. Published online March 6, 2023; DOI: https://doi.org/10.4093/dmj.2022.0177

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Background
The ratio of estimated glomerular filtration rate (eGFR) based on cystatin C and creatinine (eGFR_{cystatin C}/eGF_Rcreatinine ratio) is related to accumulating atherosclerosis-promoting proteins and increased mortality in several cohorts.
Methods
We assessed whether the eGFR_{cystatin C}/eGFR_creatinine ratio is a predictor of arterial stiffness and sub-clinical atherosclerosis in type 2 diabetes mellitus (T2DM) patients, who were followed up during 2008 to 2016. GFR was estimated using an equation based on cystatin C and creatinine.
Results
A total of 860 patients were stratified according to their eGFR_{cystatin C}/eGF_Rcreatinine ratio (i.e., <0.9, 0.9–1.1 [a reference group], and >1.1). Intima-media thickness was comparable among the groups; however, presence of carotid plaque was frequent in the <0.9 group (<0.9 group, 38.3%; 0.9–1.1 group, 21.6% vs. >1.1 group, 17.2%, P<0.001). Brachial-ankle pulse wave velocity (baPWV) was faster in the <0.9 group (<0.9 group, 1,656.3±333.0 cm/sec; 0.9–1.1 group, 1,550.5±294.8 cm/sec vs. >1.1 group, 1,494.0±252.2 cm/sec, P<0.001). On comparing the <0.9 group with the 0.9–1.1 group, the multivariate-adjusted odds ratios of prevalence of high baPWV and carotid plaque were 2.54 (P=0.007) and 1.95 (P=0.042), respectively. Cox regression analysis demonstrated near or over 3-fold higher risks of the prevalence of high baPWV and carotid plaque in the <0.9 group without chronic kidney disease (CKD).
Conclusion
We concluded that eGFR_{cystatin C}/eGFR_creatinine ratio <0.9 was related to an increased risk of high baPWV and carotid plaque in T2DM patients, especially, those without CKD. Careful monitoring of cardiovascular disease is needed for T2DM patients with low eGFR_{cystatin C}/eGFR_creatinine ratio.

Citations

Citations to this article as recorded by

Different ways of diagnosing selective glomerular hypofiltration syndromes such as shrunken pore syndrome and the associated increase in mortality
Anna Åkesson, Linnea Malmgren, Felicia Leion, Ulf Nyman, Anders Christensson, Jonas Björk, Anders Grubb
Journal of Internal Medicine.2025; 297(1): 79. CrossRef
Intraindividual difference in estimated GFR by creatinine and cystatin C, cognitive trajectories and motoric cognitive risk syndrome
Jinqi Wang, Yueruijing Liu, Rui Jin, Xiaoyu Zhao, Zhiyuan Wu, Ze Han, Zongkai Xu, Xiuhua Guo, Lixin Tao
Nephrology Dialysis Transplantation.2024; 39(5): 860. CrossRef
Research Progress of Creatinine, Cystatin C, and Their Ratio in Renal Diseases
广智杨
Advances in Clinical Medicine.2024; 14(04): 976. CrossRef
Muscle mass, creatinine, cystatin C and selective glomerular hypofiltration syndromes
Linnea Malmgren, Anders Grubb
Clinical Kidney Journal.2023; 16(8): 1206. CrossRef
Investigating kidney function changes in young adults with COVID-19: Serum creatinine level, glomerular filtration rate, and biochemical profile analysis
Nikita Matyushin, Dmitriy Ermakov, Inna Vasileva, Roza Vakolyuk, Anastasiya Spaska
Electronic Journal of General Medicine.2023; 20(6): em547. CrossRef

Metabolic Risk/Epidemiology
Normalized Creatinine-to-Cystatin C Ratio and Risk of Diabetes in Middle-Aged and Older Adults: The China Health and Retirement Longitudinal Study: Shanhu Qiu, Xue Cai, Bo Xie, Yang Yuan, Zilin Sun, Tongzhi Wu; Diabetes Metab J. 2022;46(3):476-485. Published online March 7, 2022; DOI: https://doi.org/10.4093/dmj.2021.0074

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Background
Creatinine-to-cystatin C ratio is recently suggested to be a surrogate marker for sarcopenia. However, little is known about its association with diabetes. This study aimed to fill in this gap based on a large-scale prospective cohort.
Methods
A population-based representative sample of 5,055 participants aged ≥45 years from the China Health and Retirement Longitudinal Study was enrolled between 2011 and 2012 and followed at least once during the subsequent surveys at 2013, 2015, or 2018. Creatinine-to-cystatin C ratio was calculated and normalized by body weight. Incident diabetes was ascertained by plasma glucose, glycosylated hemoglobin, self-reported history, or use of anti-diabetic drugs. Logistic regression analysis and mediation analysis were employed.
Results
During follow-up, 634 participants developed diabetes. The risk of diabetes was gradually and significantly decreased with increased normalized creatinine–cystatin C ratio. The multivariable-adjusted odds ratio for diabetes was 0.91 (95% confidence interval, 0.83 to 0.99) per 1 standard deviation higher of normalized creatinine-to-cystatin C ratio, and this relationship remained significant after controlling for muscle strength. The risk reduction in diabetes was significantly larger in participants with normal-weight and high normalized creatinine-to-cystatin C ratio compared with those with overweight/obesity and high normalized creatinine-to-cystatin C ratio (P_interaction=0.01). Insulin resistance and inflammation appeared to be key mediators accounting for the observed relationship between normalized creatinine-to-cystatin C ratio and risk of diabetes, with their mediating effect being 93.1% and 22.0%, respectively.
Conclusion
High normalized creatinine-to-cystatin C ratio is associated with reduced risk of diabetes in middle-aged and older adults.

Citations

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Muscle Quality in Relation to Prediabetes Phenotypes: A Population-Based Study With Mediation Analysis
Shanhu Qiu, Xue Cai, Xiaoying Zhou, Jinshui Xu, Zilin Sun, Haijian Guo, Tongzhi Wu
The Journal of Clinical Endocrinology & Metabolism.2024; 109(3): e1151. CrossRef
Sex‐specific associations between skeletal muscle mass and incident diabetes: A population‐based cohort study
Dan Liu, Nan Li, Yiling Zhou, Miye Wang, Peige Song, Changzheng Yuan, Qingyang Shi, Hui Chen, Kaixin Zhou, Huan Wang, Tao Li, Xiong‐Fei Pan, Haoming Tian, Sheyu Li
Diabetes, Obesity and Metabolism.2024; 26(3): 820. CrossRef
Diabetes Mellitus Should Be Considered While Analysing Sarcopenia-Related Biomarkers
Justyna Rentflejsz, Zyta Beata Wojszel
Journal of Clinical Medicine.2024; 13(4): 1107. CrossRef
Associations of muscle mass and strength with new-onset diabetes among middle-aged and older adults: evidence from the China health and retirement longitudinal study (CHARLS)
Yun-Yun He, Mei-Ling Jin, Xiang-Yang Fang, Xiao-Juan Wang
Acta Diabetologica.2024; 61(7): 869. CrossRef
Lower serum creatinine to cystatin C ratio associated with increased incidence of frailty in community-dwelling elderly men but not in elderly women
Shixian Zhou, Peixia Wang, Linlin Sun, Xinxiu Zhao, Caixia Gong, Yichen Yang, Wen Ren, Yunmei Yang, Qin Zhang, JingJin Jiang
Aging Clinical and Experimental Research.2024;[Epub] CrossRef
Creatinine-to-cystatin C ratio and frailty in older adults: a longitudinal cohort study
Quhong Song, Taiping Lin, Rui Liang, Yanli Zhao, Ning Ge, Jirong Yue
BMC Geriatrics.2024;[Epub] CrossRef
Sex difference in the association between creatinine-to-cystatin C ratio and metabolic syndrome among Chinese adults
Jo-Hsuan Chen, Jau-Yuan Chen, Yi-Chuan Chen, Wen-Cheng Li
Frontiers in Endocrinology.2024;[Epub] CrossRef
Sex and Age Influence the Relationship Between Serum Creatinine/Cystatin C and Carotid Plaque in Patients With Type 2 Diabetes Mellitus
Dan Yang, Kexin Li, Qiujuan Zhang, Tian Yu, Ling Liu, You Wang, Shuyuan Kang, Shumiao Song, Baofeng Xu, Rui Liu
Angiology.2024;[Epub] CrossRef
The serum creatinine to cystatin C to waist circumference ratios predicts risk for type 2 diabetes: A Chinese cohort study
Yinfei Chen, Weiheng Wen, Zhiliang Mai, Ming Wang, Hong Chen, Jia Sun
Journal of Diabetes.2023; 15(10): 808. CrossRef
Associations of sarcopenia with peak expiratory flow among community-dwelling elderly population: based on the China Health and Retirement Longitudinal Study (CHARLS)
Yun-Yun He, Mei-Ling Jin, Jing Chang, Xiao-Juan Wang
European Geriatric Medicine.2023; 15(1): 95. CrossRef
Additive impact of diabetes and sarcopenia on all-cause and cardiovascular mortality: A longitudinal nationwide population-based study
Eyun Song, Soon Young Hwang, Min Jeong Park, Ahreum Jang, Kyeong Jin Kim, Ji Hee Yu, Nam Hoon Kim, Hye Jin Yoo, Ji A. Seo, Sin Gon Kim, Nan Hee Kim, Sei Hyun Baik, Kyung Mook Choi
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Clinical Usefulness of Serum Cystatin C as a Marker of Renal Function: Kwang-Sook Woo, Jae-Lim Choi, Bo-Ram Kim, Ji-Eun Kim, Jin-Yeong Han; Diabetes Metab J. 2014;38(4):278-284. Published online August 20, 2014; DOI: https://doi.org/10.4093/dmj.2014.38.4.278

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Background

Accurate renal function measurements are important in the diagnosis and treatment of kidney diseases. In contrast to creatinine, the production of serum cystatin C has been extensively reported to be unaffected by body muscle mass, age, gender, and nutritional status.

Methods

Our study included 37 samples from diabetic chronic kidney disease (CKD) patients for whom serum creatinine tests had been requested and 40 samples from a healthy populations in Dong-A University Hospital between May 2010 and June 2010. The assay precision (i.e., the coefficient of variation) and the reference range of the serum cystatin C test were evaluated. We compared the estimated glomerular filtration rates (GFRs) based on cystatin C with those based on creatinine. Moreover, we investigated the influences of age, gender, weight, and muscle mass on serum creatinine and serum cystatin C.

Results

There was a positive correlation between GFR based on creatinine and that based on cystatin C (r=0.79, P<0.0001) among the diabetic CKD patients. Serum creatinine and cystatin C were significantly correlated with body weight and muscle mass, but the strengths of these correlations were greater for serum creatinine. The precision study revealed excellent results for both the high and low controls. The 95% reference interval of cystatin C in the healthy population was 0.371 to 1.236 mg/L.

Conclusion

Based on these results, we conclude that, despite the strong correlation between serum creatinine and cystatin C, cystatin C is less affected by weight and muscle mass and might represent a better alternative for the assessment of renal function.

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Serum Cystatin C Reflects the Progress of Albuminuria: Jeong Seon Yoo, Young Mi Lee, Eun Hae Lee, Ji Woon Kim, Shin Young Lee, Ki-Cheon Jeong, Shin Ae Kang, Jong Suk Park, Joo Young Nam, Chul Woo Ahn, Young Duk Song, Kyung Rae Kim; Diabetes Metab J. 2011;35(6):602-609. Published online December 26, 2011; DOI: https://doi.org/10.4093/dmj.2011.35.6.602

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Abstract PDF PubReader

Background

Research on the relationship between urinary albumin excretion and serum cystatin C in diabetes is restricted to cross-sectional studies. In this study, we investigated how well serial measurements of serum cystatin C level reflect changes in the urinary albumin excretion rate.

Methods

We enrolled and retrospectively collected data on 1,058 participants with type 2 diabetes who were older than 18 years and who had more than 3 years of follow-up with serial measurements of albuminuria and serum cystatin C at an outpatient clinic.

Results

With the use of a linear mixed model, we found that the albuminuria level for each patient over time corresponded with the annual change in serum cystatin C-based estimated glomerular filtration rate (cysC-eGFR) but did not correspond with the creatinine-based eGFR calculated by the modification of diet in renal disease formula (MDRD-eGFR). The discrepancy in the direction of the trend was smaller with cysC-eGFR than with MDRD-eGFR.

Conclusion

Serum cystatin C level reflects the trend in albuminuria level more accurately than serum creatinine level in Korean type 2 diabetes mellitus patients.

Citations

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Diabetes & Metabolism Journal.2019; 43(4): 461. CrossRef
Evaluation of creatinine-based and cystatin C-based equations for estimation of glomerular filtration rate in type 1 diabetic patients
Caroline Pereira Domingueti, Rodrigo Bastos Fóscolo, Ana Cristina Simões e Silva, Luci Maria S. Dusse, Janice Sepúlveda Reis, Maria das Graças Carvalho, Ana Paula Fernandes, Karina Braga Gomes
Archives of Endocrinology and Metabolism.2016; 60(2): 108. CrossRef

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