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Published in: Diabetology International 4/2017

01-11-2017 | Original Article

Loss of skeletal muscle mass and its predictors in type 2 diabetes patients under a multifaceted treatment approach

Authors: Norihiko Ohara, Isao Minami, Ryotaro Bouchi, Hajime Izumiyama, Koshi Hashimoto, Takanobu Yoshimoto, Yoshihiro Ogawa

Published in: Diabetology International | Issue 4/2017

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Abstract

Background

Weight loss, which is an effective method for reducing visceral fat, may cause a concomitant loss of skeletal muscle mass. The aim of this study was to elucidate the changes in visceral fat and skeletal muscle mass in response to diabetes treatment including weight control.

Methods

For 6 months we observed the changes in the body compositions of 72 Japanese patients with type 2 diabetes who underwent multifaceted treatment including educational hospitalization. Visceral fat area (VFA) and appendicular skeletal muscle mass (ASM) were measured using a bioelectrical impedance method and dual-energy X-ray absorptiometry, respectively.

Results

During the follow-up period, VFA reduced significantly whereas the average ASM did not change. Changes in ASM were strongly positively associated with changes in body weight (r = 0.50). Additionally, in an analysis of covariance, an above-median BMI (27 kg/m2) and above-median VFA (110 cm2) at baseline were found to be independent predictors of ASM reduction prevention. Of the 55 patients who lost weight, those who had a baseline VFA of ≥110 cm2 had significantly greater reductions in VFA than those with a baseline VFA of <110 cm2 (p < 0.01). ASM reduced significantly in patients with a VFA of <110 cm2 (p < 0.01), but not in those with a VFA of ≥110 cm2 (p = 0.98).

Conclusions

Baseline accumulation of visceral fat may predict a preferential reduction of visceral fat rather than skeletal muscle during weight control programs in type 2 diabetes patients.
Literature
1.
go back to reference UK Prospective Diabetes Study 7. Response of fasting plasma glucose to diet therapy in newly presenting type II diabetic patients, UKPDS Group. Metabolism. 1990;39:905–12. UK Prospective Diabetes Study 7. Response of fasting plasma glucose to diet therapy in newly presenting type II diabetic patients, UKPDS Group. Metabolism. 1990;39:905–12.
2.
go back to reference Goldstein DJ. Beneficial health effects of modest weight loss. Int J Obes Relat Metab Disord. 1992;16:397–415.PubMed Goldstein DJ. Beneficial health effects of modest weight loss. Int J Obes Relat Metab Disord. 1992;16:397–415.PubMed
3.
go back to reference Pastors JG, Warshaw H, Daly A, Franz M, Kulkarni K. The evidence for the effectiveness of medical nutrition therapy in diabetes management. Diabetes Care. 2002;25:608–13.CrossRefPubMed Pastors JG, Warshaw H, Daly A, Franz M, Kulkarni K. The evidence for the effectiveness of medical nutrition therapy in diabetes management. Diabetes Care. 2002;25:608–13.CrossRefPubMed
4.
go back to reference American Diabetes Association. 6. Obesity management for the treatment of type 2 diabetes. Diabetes Care. 2016;39(Suppl 1):S47–51. American Diabetes Association. 6. Obesity management for the treatment of type 2 diabetes. Diabetes Care. 2016;39(Suppl 1):S47–51.
5.
go back to reference Pownall HJ, Bray GA, Wagenknecht LE, Walkup MP, Heshka S, Hubbard VS, Hill J, Kahn SE, Nathan DM, Schwartz AV, Johnson KC. Changes in body composition over 8 years in a randomized trial of a lifestyle intervention: the Look AHEAD study. Obesity (Silver Spring). 2015;23:565–72. Pownall HJ, Bray GA, Wagenknecht LE, Walkup MP, Heshka S, Hubbard VS, Hill J, Kahn SE, Nathan DM, Schwartz AV, Johnson KC. Changes in body composition over 8 years in a randomized trial of a lifestyle intervention: the Look AHEAD study. Obesity (Silver Spring). 2015;23:565–72.
6.
go back to reference Jendle J, Nauck MA, Matthews DR, Frid A, Hermansen K, During M, Zdravkovic M, Strauss BJ, Garber AJ. Weight loss with liraglutide, a once-daily human glucagon-like peptide-1 analogue for type 2 diabetes treatment as monotherapy or added to metformin, is primarily as a result of a reduction in fat tissue. Diabetes Obes Metab. 2009;11:1163–72.CrossRefPubMed Jendle J, Nauck MA, Matthews DR, Frid A, Hermansen K, During M, Zdravkovic M, Strauss BJ, Garber AJ. Weight loss with liraglutide, a once-daily human glucagon-like peptide-1 analogue for type 2 diabetes treatment as monotherapy or added to metformin, is primarily as a result of a reduction in fat tissue. Diabetes Obes Metab. 2009;11:1163–72.CrossRefPubMed
7.
go back to reference Cefalu WT, Leiter LA, Yoon KH, Arias P, Niskanen L, Xie J, Balis DA, Canovatchel W, Meininger G. Efficacy and safety of canagliflozin versus glimepiride in patients with type 2 diabetes inadequately controlled with metformin (CANTATA-SU): 52 week results from a randomised, double-blind, phase 3 non-inferiority trial. Lancet. 2013;382:941–50.CrossRefPubMed Cefalu WT, Leiter LA, Yoon KH, Arias P, Niskanen L, Xie J, Balis DA, Canovatchel W, Meininger G. Efficacy and safety of canagliflozin versus glimepiride in patients with type 2 diabetes inadequately controlled with metformin (CANTATA-SU): 52 week results from a randomised, double-blind, phase 3 non-inferiority trial. Lancet. 2013;382:941–50.CrossRefPubMed
8.
go back to reference Bolinder J, Ljunggren O, Kullberg J, Johansson L, Wilding J, Langkilde AM, Sugg J, Parikh S. Effects of dapagliflozin on body weight, total fat mass, and regional adipose tissue distribution in patients with type 2 diabetes mellitus with inadequate glycemic control on metformin. J Clin Endocrinol Metab. 2012;97:1020–31.CrossRefPubMed Bolinder J, Ljunggren O, Kullberg J, Johansson L, Wilding J, Langkilde AM, Sugg J, Parikh S. Effects of dapagliflozin on body weight, total fat mass, and regional adipose tissue distribution in patients with type 2 diabetes mellitus with inadequate glycemic control on metformin. J Clin Endocrinol Metab. 2012;97:1020–31.CrossRefPubMed
9.
go back to reference Garciacaballero M, Reyes-Ortiz A, Garcia M, Martinez-Moreno JM, Toval JA, Garcia A, Minguez A, Osorio D, Mata JM, Miralles F. Changes of body composition in patients with BMI 23–50 after tailored one anastomosis gastric bypass (BAGUA): influence of diabetes and metabolic syndrome. Obes Surg. 2014;24:2040–7.CrossRefPubMed Garciacaballero M, Reyes-Ortiz A, Garcia M, Martinez-Moreno JM, Toval JA, Garcia A, Minguez A, Osorio D, Mata JM, Miralles F. Changes of body composition in patients with BMI 23–50 after tailored one anastomosis gastric bypass (BAGUA): influence of diabetes and metabolic syndrome. Obes Surg. 2014;24:2040–7.CrossRefPubMed
10.
go back to reference Park SW, Goodpaster BH, Lee JS, Kuller LH, Boudreau R, de Rekeneire N, Harris TB, Kritchevsky S, Tylavsky FA, Nevitt M, Cho YW, Newman AB. Excessive loss of skeletal muscle mass in older adults with type 2 diabetes. Diabetes Care. 2009;32:1993–7.CrossRefPubMedPubMedCentral Park SW, Goodpaster BH, Lee JS, Kuller LH, Boudreau R, de Rekeneire N, Harris TB, Kritchevsky S, Tylavsky FA, Nevitt M, Cho YW, Newman AB. Excessive loss of skeletal muscle mass in older adults with type 2 diabetes. Diabetes Care. 2009;32:1993–7.CrossRefPubMedPubMedCentral
11.
go back to reference Wannamethee SG, Shaper AG, Lennon L, Whincup PH. Decreased muscle mass and increased central adiposity are independently related to mortality in older men. Am J Clin Nutr. 2007;86:1339–46.PubMed Wannamethee SG, Shaper AG, Lennon L, Whincup PH. Decreased muscle mass and increased central adiposity are independently related to mortality in older men. Am J Clin Nutr. 2007;86:1339–46.PubMed
12.
go back to reference Lee CG, Boyko EJ, Barrett-Connor E, Miljkovic I, Hoffman AR, Everson-Rose SA, Lewis CE, Cawthon PM, Strotmeyer ES, Orwoll ES. Insulin sensitizers may attenuate lean mass loss in older men with diabetes. Diabetes Care. 2011;34:2381–6.CrossRefPubMedPubMedCentral Lee CG, Boyko EJ, Barrett-Connor E, Miljkovic I, Hoffman AR, Everson-Rose SA, Lewis CE, Cawthon PM, Strotmeyer ES, Orwoll ES. Insulin sensitizers may attenuate lean mass loss in older men with diabetes. Diabetes Care. 2011;34:2381–6.CrossRefPubMedPubMedCentral
13.
go back to reference Yamada M, Moriguch Y, Mitani T, Aoyama T, Arai H. Age-dependent changes in skeletal muscle mass and visceral fat area in Japanese adults from 40 to 79 years-of-age. Geriatr Gerontol Int. 2014;14(Suppl 1):8–14.CrossRefPubMed Yamada M, Moriguch Y, Mitani T, Aoyama T, Arai H. Age-dependent changes in skeletal muscle mass and visceral fat area in Japanese adults from 40 to 79 years-of-age. Geriatr Gerontol Int. 2014;14(Suppl 1):8–14.CrossRefPubMed
14.
go back to reference Seino Y, Nanjo K, Tajima N, Kadowaki T, Kashiwagi A, Araki E, Ito C, Inagaki N, Iwamoto Y, Kasuga M, Hanafusa T, Haneda M, Ueki K. Report of the Committee on the Classification and Diagnostic Criteria of Diabetes Mellitus. J Diabetes Investig. 2010;1:212–28. Seino Y, Nanjo K, Tajima N, Kadowaki T, Kashiwagi A, Araki E, Ito C, Inagaki N, Iwamoto Y, Kasuga M, Hanafusa T, Haneda M, Ueki K. Report of the Committee on the Classification and Diagnostic Criteria of Diabetes Mellitus. J Diabetes Investig. 2010;1:212–28.
15.
go back to reference Matsuo S, Imai E, Horio M, Yasuda Y, Tomita K, Nitta K, Yamagata K, Tomino Y, Yokoyama H, Hishida A. Revised equations for estimated GFR from serum creatinine in Japan. Am J Kidney Dis. 2009;53:982–92.CrossRefPubMed Matsuo S, Imai E, Horio M, Yasuda Y, Tomita K, Nitta K, Yamagata K, Tomino Y, Yokoyama H, Hishida A. Revised equations for estimated GFR from serum creatinine in Japan. Am J Kidney Dis. 2009;53:982–92.CrossRefPubMed
16.
go back to reference Hind K, Oldroyd B, Truscott JG. In vivo precision of the GE Lunar iDXA densitometer for the measurement of total body composition and fat distribution in adults. Eur J Clin Nutr. 2011;65:140–2.CrossRefPubMed Hind K, Oldroyd B, Truscott JG. In vivo precision of the GE Lunar iDXA densitometer for the measurement of total body composition and fat distribution in adults. Eur J Clin Nutr. 2011;65:140–2.CrossRefPubMed
17.
go back to reference Heymsfield SB, Smith R, Aulet M, Bensen B, Lichtman S, Wang J, Pierson RN Jr. Appendicular skeletal muscle mass: measurement by dual-photon absorptiometry. Am J Clin Nutr. 1990;52:214–8.PubMed Heymsfield SB, Smith R, Aulet M, Bensen B, Lichtman S, Wang J, Pierson RN Jr. Appendicular skeletal muscle mass: measurement by dual-photon absorptiometry. Am J Clin Nutr. 1990;52:214–8.PubMed
18.
go back to reference Chen LK, Liu LK, Woo J, Assantachai P, Auyeung TW, Bahyah KS, Chou MY, Chen LY, Hsu PS, Krairit O, Lee JS, Lee WJ, Lee Y, Liang CK, Limpawattana P, Lin CS, Peng LN, Satake S, Suzuki T, Won CW, Wu CH, Wu SN, Zhang T, Zeng P, Akishita M, Arai H. Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc. 2014;15:95–101.CrossRefPubMed Chen LK, Liu LK, Woo J, Assantachai P, Auyeung TW, Bahyah KS, Chou MY, Chen LY, Hsu PS, Krairit O, Lee JS, Lee WJ, Lee Y, Liang CK, Limpawattana P, Lin CS, Peng LN, Satake S, Suzuki T, Won CW, Wu CH, Wu SN, Zhang T, Zeng P, Akishita M, Arai H. Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc. 2014;15:95–101.CrossRefPubMed
19.
go back to reference Ryo M, Maeda K, Onda T, Katashima M, Okumiya A, Nishida M, Yamaguchi T, Funahashi T, Matsuzawa Y, Nakamura T, Shimomura I. A new simple method for the measurement of visceral fat accumulation by bioelectrical impedance. Diabetes Care. 2005;28:451–3.CrossRefPubMed Ryo M, Maeda K, Onda T, Katashima M, Okumiya A, Nishida M, Yamaguchi T, Funahashi T, Matsuzawa Y, Nakamura T, Shimomura I. A new simple method for the measurement of visceral fat accumulation by bioelectrical impedance. Diabetes Care. 2005;28:451–3.CrossRefPubMed
20.
go back to reference Yamakage H, Ito R, Tochiya M, Muranaka K, Tanaka M, Matsuo Y, Odori S, Kono S, Shimatsu A, Satoh-Asahara N. 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.CrossRefPubMed Yamakage H, Ito R, Tochiya M, Muranaka K, Tanaka M, Matsuo Y, Odori S, Kono S, Shimatsu A, Satoh-Asahara N. 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.CrossRefPubMed
21.
go back to reference Li Y, Bujo H, Takahashi K, Shibasaki M, Zhu Y, Yoshida Y, Otsuka Y, Hashimoto N, Saito Y. Visceral fat: higher responsiveness of fat mass and gene expression to calorie restriction than subcutaneous fat. Exp Biol Med (Maywood). 2003;228:1118–23.CrossRefPubMed Li Y, Bujo H, Takahashi K, Shibasaki M, Zhu Y, Yoshida Y, Otsuka Y, Hashimoto N, Saito Y. Visceral fat: higher responsiveness of fat mass and gene expression to calorie restriction than subcutaneous fat. Exp Biol Med (Maywood). 2003;228:1118–23.CrossRefPubMed
22.
go back to reference Kim TN, Park MS, Ryu JY, Choi HY, Hong HC, Yoo HJ, Kang HJ, Song W, Park SW, Baik SH, Newman AB, Choi KM. Impact of visceral fat on skeletal muscle mass and vice versa in a prospective cohort study: the Korean Sarcopenic Obesity Study (KSOS). PLoS One. 2014;9:e115407.CrossRefPubMedPubMedCentral Kim TN, Park MS, Ryu JY, Choi HY, Hong HC, Yoo HJ, Kang HJ, Song W, Park SW, Baik SH, Newman AB, Choi KM. Impact of visceral fat on skeletal muscle mass and vice versa in a prospective cohort study: the Korean Sarcopenic Obesity Study (KSOS). PLoS One. 2014;9:e115407.CrossRefPubMedPubMedCentral
23.
go back to reference Koster A, Ding J, Stenholm S, Caserotti P, Houston DK, Nicklas BJ, You T, Lee JS, Visser M, Newman AB, Schwartz AV, Cauley JA, Tylavsky FA, Goodpaster BH, Kritchevsky SB, Harris TB. Does the amount of fat mass predict age-related loss of lean mass, muscle strength, and muscle quality in older adults? J Gerontol A Biol Sci Med Sci. 2011;66:888–95.CrossRefPubMed Koster A, Ding J, Stenholm S, Caserotti P, Houston DK, Nicklas BJ, You T, Lee JS, Visser M, Newman AB, Schwartz AV, Cauley JA, Tylavsky FA, Goodpaster BH, Kritchevsky SB, Harris TB. Does the amount of fat mass predict age-related loss of lean mass, muscle strength, and muscle quality in older adults? J Gerontol A Biol Sci Med Sci. 2011;66:888–95.CrossRefPubMed
24.
go back to reference Yagi S, Kadota M, Aihara K, Nishikawa K, Hara T, Ise T, Ueda Y, Iwase T, Akaike M, Shimabukuro M, Katoh S, Sata M. Association of lower limb muscle mass and energy expenditure with visceral fat mass in healthy men. Diabetol Metab Syndr. 2014;6:27.CrossRefPubMedPubMedCentral Yagi S, Kadota M, Aihara K, Nishikawa K, Hara T, Ise T, Ueda Y, Iwase T, Akaike M, Shimabukuro M, Katoh S, Sata M. Association of lower limb muscle mass and energy expenditure with visceral fat mass in healthy men. Diabetol Metab Syndr. 2014;6:27.CrossRefPubMedPubMedCentral
25.
go back to reference Schaap LA, Pluijm SM, Deeg DJ, Harris TB, Kritchevsky SB, Newman AB, Colbert LH, Pahor M, Rubin SM, Tylavsky FA, Visser M. Higher inflammatory marker levels in older persons: associations with 5-year change in muscle mass and muscle strength. J Gerontol A Biol Sci Med Sci. 2009;64:1183–9.CrossRefPubMed Schaap LA, Pluijm SM, Deeg DJ, Harris TB, Kritchevsky SB, Newman AB, Colbert LH, Pahor M, Rubin SM, Tylavsky FA, Visser M. Higher inflammatory marker levels in older persons: associations with 5-year change in muscle mass and muscle strength. J Gerontol A Biol Sci Med Sci. 2009;64:1183–9.CrossRefPubMed
26.
27.
go back to reference Abdelhafiz AH, Koay L, Sinclair AJ. The effect of frailty should be considered in the management plan of older people with type 2 diabetes. Future Sci OA. 2016;2:FSO102. Abdelhafiz AH, Koay L, Sinclair AJ. The effect of frailty should be considered in the management plan of older people with type 2 diabetes. Future Sci OA. 2016;2:FSO102.
28.
go back to reference Castaneda C, Layne JE, Munoz-Orians L, Gordon PL, Walsmith J, Foldvari M, Roubenoff R, Tucker KL, Nelson ME. A randomized controlled trial of resistance exercise training to improve glycemic control in older adults with type 2 diabetes. Diabetes Care. 2002;25:2335–41.CrossRefPubMed Castaneda C, Layne JE, Munoz-Orians L, Gordon PL, Walsmith J, Foldvari M, Roubenoff R, Tucker KL, Nelson ME. A randomized controlled trial of resistance exercise training to improve glycemic control in older adults with type 2 diabetes. Diabetes Care. 2002;25:2335–41.CrossRefPubMed
29.
go back to reference Ito S, Harada A, Kasai T, Sakai Y, Takemura M, Matsui Y, Hida T, Ishiguro N. Use of alfacalcidol in osteoporotic patients with low muscle mass might increase muscle mass: an investigation using a patient database. Geriatr Gerontol Int. 2014;14(Suppl 1):122–8.CrossRefPubMed Ito S, Harada A, Kasai T, Sakai Y, Takemura M, Matsui Y, Hida T, Ishiguro N. Use of alfacalcidol in osteoporotic patients with low muscle mass might increase muscle mass: an investigation using a patient database. Geriatr Gerontol Int. 2014;14(Suppl 1):122–8.CrossRefPubMed
30.
go back to reference Kim HK, Suzuki T, Saito K, Yoshida H, Kobayashi H, Kato H, Katayama M. Effects of exercise and amino acid supplementation on body composition and physical function in community-dwelling elderly Japanese sarcopenic women: a randomized controlled trial. J Am Geriatr Soc. 2012;60:16–23.CrossRefPubMed Kim HK, Suzuki T, Saito K, Yoshida H, Kobayashi H, Kato H, Katayama M. Effects of exercise and amino acid supplementation on body composition and physical function in community-dwelling elderly Japanese sarcopenic women: a randomized controlled trial. J Am Geriatr Soc. 2012;60:16–23.CrossRefPubMed
Metadata
Title
Loss of skeletal muscle mass and its predictors in type 2 diabetes patients under a multifaceted treatment approach
Authors
Norihiko Ohara
Isao Minami
Ryotaro Bouchi
Hajime Izumiyama
Koshi Hashimoto
Takanobu Yoshimoto
Yoshihiro Ogawa
Publication date
01-11-2017
Publisher
Springer Japan
Published in
Diabetology International / Issue 4/2017
Print ISSN: 2190-1678
Electronic ISSN: 2190-1686
DOI
https://doi.org/10.1007/s13340-017-0325-z

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