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Visceral adiposity is associated with the discrepancy between glycated albumin and HbA1c in type 2 diabetes

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Abstract

Aim

We investigated the association of visceral adiposity with glycated albumin (GA) as well as GA/hemoglobin A1c (HbA1c) in type 2 diabetes.

Methods

One hundred twenty-three patients (68 males, 55 females) with type 2 diabetes were enrolled in this cross-sectional study. Visceral fat area (VFA) was determined using an abdominal dual bioelectrical impedance analysis (dual BIA) instrument. The relationship of VFA with GA and GA/HbA1c was analyzed.

Results

Simple regression analysis showed that BMI was inversely correlated with GA as well as GA/HbA1c, but not with HbA1c, while VFA had a significant correlation with GA and GA/HbA1c. Furthermore, multiple regression analysis revealed VFA as an independent contributor to GA/HbA1c. These results suggest that visceral adiposity is a primary factor associated with GA and HbA1c level discrepancy in patients with type 2 diabetes.

Conclusions

GA is a useful indicator for glycemic control, while visceral obesity should also be taken into consideration in type 2 diabetes cases.

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References

  1. Guthrow CE, Morris MA, Day JF, Thorpe SR, Baynes JW. Enhanced nonenzymatic glucosylation of human serum albumin in diabetes mellitus. Proc Natl Acad Sci USA. 1979;76:4258–61.

    Article  CAS  Google Scholar 

  2. Kohzuma T, Koga M. Lucica GA-L glycated albumin assay kit: a new diagnostic test for diabetes mellitus. Mol Diagn Ther. 2010;14:49–51.

    Article  CAS  Google Scholar 

  3. Koenig RJ, Peterson CM, Jones RL, Saudek C, Lehrman M, Cerami A. Correlation of glucose regulation and hemoglobin AIc in diabetes mellitus. N Engl J Med. 1976;295:417–20.

    Article  CAS  Google Scholar 

  4. Shima K, Ito N, Abe F, Hirota M, Yano M, Yamamoto Y, et al. High-performance liquid chromatographic assay of serum glycated albumin. Diabetologia. 1988;31:627–31.

    Article  CAS  Google Scholar 

  5. Jeffcoate SL. Diabetes control and complications: the role of glycated haemoglobin, 25 years on. Diabetes Med. 2004;21:657–65.

    Article  CAS  Google Scholar 

  6. Sakuma N. Converse contributions of fasting and postprandial glucose to HbA1c and glycated albumin. Diabetol Int. 2011;2:167–72.

    Article  Google Scholar 

  7. Hiramatsu Y, Shimizu I, Omori Y, Nakabayashi M, Group JGAS. Determination of reference intervals of glycated albumin and hemoglobin A1c in healthy pregnant Japanese women and analysis of their time courses and influencing factors during pregnancy. Endocr J. 2012;59:145–51.

    Article  CAS  Google Scholar 

  8. Inaba M, Okuno S, Kumeda Y, Yamada S, Imanishi Y, Tabata T, et al. Glycated albumin is a better glycemic indicator than glycated hemoglobin values in hemodialysis patients with diabetes: effect of anemia and erythropoietin injection. J Am Soc Nephrol. 2007;18:896–903.

    Article  CAS  Google Scholar 

  9. Austin GE, Mullins RH, Morin LG. Non-enzymic glycation of individual plasma proteins in normoglycemic and hyperglycemic patients. Clin Chem. 1987;33:2220–4.

    Article  CAS  Google Scholar 

  10. Schleicher ED, Olgemoller B, Wiedenmann E, Gerbitz KD. Specific glycation of albumin depends on its half-life. Clin Chem. 1993;39:625–8.

    Article  CAS  Google Scholar 

  11. Koga M, Murai J, Saito H, Matsumoto S, Kasayama S. Effects of thyroid hormone on serum glycated albumin levels: study on non-diabetic subjects. Diabetes Res Clin Pract. 2009;84:163–7.

    Article  CAS  Google Scholar 

  12. Okada T, Nakao T, Matsumoto H, Nagaoka Y, Tomaru R, Iwasawa H, et al. Influence of proteinuria on glycated albumin values in diabetic patients with chronic kidney disease. Intern Med. 2011;50:23–9.

    Article  CAS  Google Scholar 

  13. Koga M, Kasayama S, Kanehara H, Bando Y. CLD (chronic liver diseases)-HbA1C as a suitable indicator for estimation of mean plasma glucose in patients with chronic liver diseases. Diabetes Res Clin Pract. 2008;81:258–62.

    Article  CAS  Google Scholar 

  14. Nishimura R, Kanda A, Sano H, Matsudaira T, Miyashita Y, Morimoto A, et al. Glycated albumin is low in obese, non-diabetic children. Diabetes Res Clin Pract. 2006;71:334–8.

    Article  CAS  Google Scholar 

  15. Miyashita Y, Nishimura R, Morimoto A, Matsudaira T, Sano H, Tajima N. Glycated albumin is low in obese, type 2 diabetic patients. Diabetes Res Clin Pract. 2007;78:51–5.

    Article  CAS  Google Scholar 

  16. Koga M, Matsumoto S, Saito H, Kasayama S. Body mass index negatively influences glycated albumin, but not glycated hemoglobin, in diabetic patients. Endocr J. 2006;53:387–91.

    Article  CAS  Google Scholar 

  17. Koga M, Otsuki M, Matsumoto S, Saito H, Mukai M, Kasayama S. Negative association of obesity and its related chronic inflammation with serum glycated albumin but not glycated hemoglobin levels. Clin Chim Acta. 2007;378:48–52.

    Article  CAS  Google Scholar 

  18. Smalley KJ, Knerr AN, Kendrick ZV, Colliver JA, Owen OE. Reassessment of body mass indices. Am J Clin Nutr. 1990;52:405–8.

    Article  CAS  Google Scholar 

  19. Frankenfield DC, Rowe WA, Cooney RN, Smith JS, Becker D. Limits of body mass index to detect obesity and predict body composition. Nutrition. 2001;17:26–30.

    Article  CAS  Google Scholar 

  20. Roubenoff R, Dallal GE, Wilson PW. Predicting body fatness: the body mass index vs estimation by bioelectrical impedance. Am J Public Health. 1995;85:726–8.

    Article  CAS  Google Scholar 

  21. Segal KR, Dunaif A, Gutin B, Albu J, Nyman A, Pi-Sunyer FX. Body composition, not body weight, is related to cardiovascular disease risk factors and sex hormone levels in men. J Clin Invest. 1987;80:1050–5.

    Article  CAS  Google Scholar 

  22. Kobayashi H, Nakamura T, Miyaoka K, Nishida M, Funahashi T, Yamashita S, et al. Visceral fat accumulation contributes to insulin resistance, small-sized low-density lipoprotein, and progression of coronary artery disease in middle-aged non-obese Japanese men. Jpn Circ J. 2001;65:193–9.

    Article  CAS  Google Scholar 

  23. Kim K, Valentine RJ, Shin Y, Gong K. Associations of visceral adiposity and exercise participation with C-reactive protein, insulin resistance, and endothelial dysfunction in Korean healthy adults. Metabolism. 2008;57:1181–9.

    Article  CAS  Google Scholar 

  24. Wang F, Ma X, Hao Y, Yang R, Ni J, Xiao Y, et al. Serum glycated albumin is inversely influenced by fat mass and visceral adipose tissue in Chinese with normal glucose tolerance. PLoS One. 2012;7:e51098.

    Article  CAS  Google Scholar 

  25. American Diabetes A. Standards of medical care in diabetes—2014. Diabetes Care. 2014;37(Suppl 1):S14–80.

    Article  Google Scholar 

  26. Yamazaki Y, Emoto M, Morioka T, Kawano N, Lee E, Urata H, et al. Clinical impact of the leptin to soluble leptin receptor ratio on subclinical carotid atherosclerosis in patients with type 2 diabetes. J Atheroscler Thromb. 2013;20:186–94.

    Article  CAS  Google Scholar 

  27. Matsuo S, Imai E, Horio M, Yasuda Y, Tomita K, Nitta K, et al. Revised equations for estimated GFR from serum creatinine in Japan. Am J Kidney Dis. 2009;53:982–92.

    Article  CAS  Google Scholar 

  28. Demura S, Sato S, Kitabayashi T. Percentage of total body fat as estimated by three automatic bioelectrical impedance analyzers. J Physiol Anthropol Appl Hum Sci. 2004;23:93–9.

    Article  Google Scholar 

  29. Ida M, Hirata M, Odori S, Mori E, Kondo E, Fujikura J, et al. Early changes of abdominal adiposity detected with weekly dual bioelectrical impedance analysis during calorie restriction. Obesity (Silver Spring). 2013;21:E350–3.

    Google Scholar 

  30. Yamakage H, Ito R, Tochiya M, Muranaka K, Tanaka M, Matsuo Y, et al. The utility of dual bioelectrical impedance analysis in detecting intra-abdominal fat area in obese patients during weight reduction therapy in comparison with waist circumference and abdominal CT. Endocr J. 2014;61:807–19.

    Article  CAS  Google Scholar 

  31. Morigami H, Morioka T, Yamazaki Y, Imamura S, Numaguchi R, Asada M, et al. Visceral adiposity is preferentially associated with vascular stiffness rather than thickness in men with type 2 diabetes. J Atheroscler Thromb. 2016;23:1067–79.

    Article  CAS  Google Scholar 

  32. Inoue K, Tsujimoto T, Yamamoto-Honda R, Goto A, Kishimoto M, Noto H, et al. A newer conversion equation for the correlation between HbA1c and glycated albumin. Endocr J. 2014;61:553–60.

    Article  CAS  Google Scholar 

  33. Salas-Salvado J, Bullo M, Garcia-Lorda P, Figueredo R, Del Castillo D, Bonada A, et al. Subcutaneous adipose tissue cytokine production is not responsible for the restoration of systemic inflammation markers during weight loss. Int J Obes (Lond). 2006;30:1714–20.

    Article  CAS  Google Scholar 

  34. Alexopoulos N, Katritsis D, Raggi P. Visceral adipose tissue as a source of inflammation and promoter of atherosclerosis. Atherosclerosis. 2014;233:104–12.

    Article  CAS  Google Scholar 

  35. Bertin E, Nguyen P, Guenounou M, Durlach V, Potron G, Leutenegger M. Plasma levels of tumor necrosis factor-alpha (TNF-alpha) are essentially dependent on visceral fat amount in type 2 diabetic patients. Diabetes Metab. 2000;26:178–82.

    CAS  PubMed  Google Scholar 

  36. Kumagai S, Kishimoto H, Zou B. The leptin to adiponectin ratio is a good biomarker for the prevalence of metabolic syndrome, dependent on visceral fat accumulation and endurance fitness in obese patients with diabetes mellitus. Metab Syndr Relat Disord. 2005;3:85–94.

    Article  CAS  Google Scholar 

  37. Tessari P, Kiwanuka E, Millioni R, Vettore M, Puricelli L, Zanetti M, et al. Albumin and fibrinogen synthesis and insulin effect in type 2 diabetic patients with normoalbuminuria. Diabetes Care. 2006;29:323–8.

    Article  CAS  Google Scholar 

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Acknowledgements

We thank the patients for their participation in this study. Additionally, we are grateful for the staff of Osaka City University Hospital for their help with recruiting the patients, and collecting and recording clinical information.

Author information

Authors and Affiliations

  1. Department of Metabolism, Endocrinology and Molecular Medicine, Osaka City University Graduate School of Medicine, 1-4-3, Asahi-machi, Abeno-ku, Osaka, 545-8585, Japan

    Saori Maruo, Koka Motoyama, Tomoe Hirota, Yoshinori Kakutani, Yuko Yamazaki, Tomoaki Morioka, Masaaki Inaba & Masanori Emoto

  2. Department of Nephrology, Osaka City University Graduate School of Medicine, 1-4-3, Asahi-machi, Abeno-ku, Osaka, 545-8585, Japan

    Katsuhito Mori

  3. Department of Premier Preventive Medicine, Osaka City University Graduate School of Medicine, 1-4-3, Asahi-machi, Abeno-ku, Osaka, 545-8585, Japan

    Shinya Fukumoto

  4. Department of Vascular Medicine, Osaka City University Graduate School of Medicine, 1-4-3, Asahi-machi, Abeno-ku, Osaka, 545-8585, Japan

    Atsushi Shioi & Tetsuo Shoji

Authors
  1. Saori Maruo
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  2. Koka Motoyama
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  3. Tomoe Hirota
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  4. Yoshinori Kakutani
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  5. Yuko Yamazaki
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  6. Tomoaki Morioka
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  9. Atsushi Shioi
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  11. Masaaki Inaba
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  12. Masanori Emoto
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Contributions

SM performed all of the processes involved in this study. KM managed all of the processes involved in this study, and wrote and edited the drafts of the manuscript. MI, ME, and KM conceived the study, and participated in its design and coordination. TH, YK, YY, TM, KM, SF, AS, TS, and ME recruited the patients. All co-authors contributed to discussions related to and were involved in drafting or critically revising the manuscript. Each author has read the final version of the manuscript and approved its submission for publishing.

Corresponding author

Correspondence to Koka Motoyama.

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Conflict of interest

The authors have no conflicts of interest to declare.

Ethical approval

All procedures employed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national), and with the Helsinki Declaration of 1964 and later versions.

Informed consent

Written informed consent was obtained from all subjects. The ethical review board of Osaka City University Graduate School of Medicine approved the study protocol (Approval date: not applicable. no. 308).

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Electronic supplementary material

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13340_2020_431_MOESM1_ESM.pptx

Correlation between VFA and, GA (a)(b) or GA/HbAb1c (c)(d) separately in males and females. Correlation of VFA with (a) GA in male, (b) GA in female, (c) GA/HbA1c in male, and (d) GA/HbA1c in female (PPTX 72 kb)

13340_2020_431_MOESM2_ESM.pptx

Comparison analysis between actual measured HbA1c and that calculated with a formula using GA. Non-obese (a) BMI <25 kg/m2, (c) VFA <100 cm2, and obese (b) BMI ≥25 kg/m2, (d) VFA ≥100 cm2, patients. Data are presented as mean with SD (PPTX 60 kb)

13340_2020_431_MOESM3_ESM.pptx

Cumulative response curve of VFA. A cut-off value for prediction of a -2SD of calculated HbA1c to measured HbA1c was shown to be 121 cm2 (PPTX 64 kb)

Supplementary material 4 (DOC 44 kb)

Supplementary material 5 (DOC 44 kb)

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Maruo, S., Motoyama, K., Hirota, T. et al. Visceral adiposity is associated with the discrepancy between glycated albumin and HbA1c in type 2 diabetes. Diabetol Int 11, 368–375 (2020). https://doi.org/10.1007/s13340-020-00431-z

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  • DOI: https://doi.org/10.1007/s13340-020-00431-z

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