Skip to main content
Top

Open Access 05-02-2024 | Diabetes-associated Diseases

Diabetic Sarcopenia. A proposed muscle screening protocol in people with diabetes

Expert document

Authors: Daniel de Luis Román, Juana Carretero Gómez, José Manuel García-Almeida, Fernando Garrachón Vallo, German Guzmán Rolo, Juan José López Gómez, Francisco José Tarazona-Santabalbina, Alejandro Sanz-Paris

Published in: Reviews in Endocrine and Metabolic Disorders

Login to get access

Abstract

Objectives

To propose the grounds for “diabetic sarcopenia” as a new comorbidity of diabetes, and to establish a muscle screening algorithm proposal to facilitate its diagnosis and staging in clinical practice. Method: A qualitative expert opinion study was carried out using the nominal technique. A literature search was performed with the terms “screening” or “diagnostic criteria” and “muscle loss” or “sarcopenia” and “diabetes” that was sent to a multidisciplinary group of 7 experts who, in a face-to-face meeting, discussed various aspects of the screening algorithm. Results: The hallmark of diabetic sarcopenia (DS) is muscle mass atrophy characteristic of people with diabetes mellitus (DM) in contrast to the histological and physiological normality of muscle mass. The target population to be screened was defined as patients with DM with a SARC-F questionnaire > 4, glycosylated haemoglobin (HbA1C) ≥ 8.0%, more than 5 years since onset of DM, taking sulfonylureas, glinides and sodium/glucose cotransporter inhibitors (SGLT2), as well as presence of chronic complications of diabetes or clinical suspicion of sarcopenia. Diagnosis was based on the presence of criteria of low muscle strength (probable sarcopenia) and low muscle mass (confirmed sarcopenia) using methods available in any clinical consultation room, such as dynamometry, the chair stand test, and Body Mass Index (BMI)-adjusted calf circumference. DS was classified into 4 stages: Stage I corresponds to sarcopenic patients with no other diabetes complication, and Stage II corresponds to patients with some type of involvement. Within Stage II are three sublevels (a, b and c). Stage IIa refers to individuals with sarcopenic diabetes and some diabetes-specific impairment, IIb to sarcopenia with functional impairment, and IIc to sarcopenia with diabetes complications and changes in function measured using standard tests Conclusion: Diabetic sarcopenia has a significant impact on function and quality of life in people with type 2 diabetes mellitus (T2DM), and it is important to give it the same attention as all other traditionally described complications of T2DM. This document aims to establish the foundation for protocolising the screening and diagnosis of diabetic sarcopenia in a manner that is simple and accessible for all levels of healthcare.
Literature
2.
go back to reference Donini LM, Busetto L, Bischoff SC, Cederholm T, Ballesteros-Pomar MD, Batsis JA, et al. Definition and diagnostic criteria for sarcopenic obesity: ESPEN and EASO Consensus Statement. Obes Facts. 2022;15(3):321–35.CrossRefPubMedPubMedCentral Donini LM, Busetto L, Bischoff SC, Cederholm T, Ballesteros-Pomar MD, Batsis JA, et al. Definition and diagnostic criteria for sarcopenic obesity: ESPEN and EASO Consensus Statement. Obes Facts. 2022;15(3):321–35.CrossRefPubMedPubMedCentral
3.
5.
go back to reference Seok WP, Goodpaster BH, Jung SL, Kuller LH, Boudreau R, De Rekeneire N, et al. Excessive loss of skeletal muscle mass in older adults with type 2 Diabetes. Diabetes Care. 2009;32(11):1993–7.CrossRef Seok WP, Goodpaster BH, Jung SL, Kuller LH, Boudreau R, De Rekeneire N, et al. Excessive loss of skeletal muscle mass in older adults with type 2 Diabetes. Diabetes Care. 2009;32(11):1993–7.CrossRef
6.
8.
go back to reference Viña J, Borras C, Gomez-Cabrera MC. A free radical theory of frailty. Free Radic Biol Med. 2018;124:358–63.CrossRefPubMed Viña J, Borras C, Gomez-Cabrera MC. A free radical theory of frailty. Free Radic Biol Med. 2018;124:358–63.CrossRefPubMed
10.
go back to reference Park SW, Goodpaster BH, Strotmeyer ES, De Rekeneire N, Harris TB, Schwartz AV, et al. Decreased muscle strength and quality in older adults with type 2 Diabetes: the health, aging, and body composition study. Diabetes. 2006;55(6):1813–8.CrossRefPubMed Park SW, Goodpaster BH, Strotmeyer ES, De Rekeneire N, Harris TB, Schwartz AV, et al. Decreased muscle strength and quality in older adults with type 2 Diabetes: the health, aging, and body composition study. Diabetes. 2006;55(6):1813–8.CrossRefPubMed
11.
go back to reference Alabadi B, Civera M, De la Rosa A, Martinez-Hervas S, Gomez-Cabrera MC, Real JT. Frailty is associated with oxidative stress in older patients with type 2 Diabetes. Nutrients. 2021;13(11):1–13.CrossRef Alabadi B, Civera M, De la Rosa A, Martinez-Hervas S, Gomez-Cabrera MC, Real JT. Frailty is associated with oxidative stress in older patients with type 2 Diabetes. Nutrients. 2021;13(11):1–13.CrossRef
12.
go back to reference Campins L, Camps M, Riera A, Pleguezuelos E, Yebenes JC, Serra-Prat M. Oral drugs related with muscle wasting and sarcopenia. A Review Pharmacology [Internet]. 2017 Jan 25 [cited 2023 Jun 15;99(1–2):1–8. https://doi.org/10.1159/000448247. Campins L, Camps M, Riera A, Pleguezuelos E, Yebenes JC, Serra-Prat M. Oral drugs related with muscle wasting and sarcopenia. A Review Pharmacology [Internet]. 2017 Jan 25 [cited 2023 Jun 15;99(1–2):1–8. https://​doi.​org/​10.​1159/​000448247.
13.
15.
go back to reference Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, et al. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol [Internet]. 2001 [cited 2023 Jun 15;3(11):1014–9. Available from https://pubmed.ncbi.nlm.nih.gov/11715023/. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, et al. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol [Internet]. 2001 [cited 2023 Jun 15;3(11):1014–9. Available from https://​pubmed.​ncbi.​nlm.​nih.​gov/​11715023/​.
18.
go back to reference Hiromine Y, Noso S, Rakugi H, Sugimoto K, Takata Y, Katsuya T, et al. Poor glycemic control rather than types of diabetes is a risk factor for sarcopenia in diabetes mellitus: The MUSCLES-DM study. J Diabetes Investig [Internet]. 2022 Nov 1 [cited 2023 May 29;13(11):1881–8. Available from: https://pubmed.ncbi.nlm.nih.gov/35796583/. Hiromine Y, Noso S, Rakugi H, Sugimoto K, Takata Y, Katsuya T, et al. Poor glycemic control rather than types of diabetes is a risk factor for sarcopenia in diabetes mellitus: The MUSCLES-DM study. J Diabetes Investig [Internet]. 2022 Nov 1 [cited 2023 May 29;13(11):1881–8. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​35796583/​.
19.
go back to reference de Luis D, Primo D, Izaola O, Gómez Hoyos E, López Gómez JJ. Relationship of circulating resistin levels with muscle mass determined by bioelectrical impedance in females with obesity. Endocrinol Diabetes Nutr [Internet]. 2023 Aug [cited 2023 Aug 30;70(7):468–75. Available from: https://pubmed.ncbi.nlm.nih.gov/37516610/. de Luis D, Primo D, Izaola O, Gómez Hoyos E, López Gómez JJ. Relationship of circulating resistin levels with muscle mass determined by bioelectrical impedance in females with obesity. Endocrinol Diabetes Nutr [Internet]. 2023 Aug [cited 2023 Aug 30;70(7):468–75. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​37516610/​.
20.
go back to reference Sugimoto K, Tabara Y, Ikegami H, Takata Y, Kamide K, Ikezoe T, et al. Hyperglycemia in non-obese patients with type 2 diabetes is associated with low muscle mass: The multicenter study for clarifying evidence for sarcopenia in patients with diabetes mellitus. J Diabetes Investig [Internet]. 2019 Nov 1 [cited 2023 Jun 13;10(6):1471–9. Available from: https://pubmed.ncbi.nlm.nih.gov/31074209/. Sugimoto K, Tabara Y, Ikegami H, Takata Y, Kamide K, Ikezoe T, et al. Hyperglycemia in non-obese patients with type 2 diabetes is associated with low muscle mass: The multicenter study for clarifying evidence for sarcopenia in patients with diabetes mellitus. J Diabetes Investig [Internet]. 2019 Nov 1 [cited 2023 Jun 13;10(6):1471–9. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​31074209/​.
22.
go back to reference Wu CN, Tien KJ. The impact of antidiabetic agents on sarcopenia in type 2 diabetes: a literature review. J Diabetes Res. 2020;2020. Wu CN, Tien KJ. The impact of antidiabetic agents on sarcopenia in type 2 diabetes: a literature review. J Diabetes Res. 2020;2020.
24.
go back to reference Zhang S, Qi Z, Wang Y, Song D, Zhu D. Effect of sodium-glucose transporter 2 inhibitors on sarcopenia in patients with type 2 diabetes mellitus: a systematic review and meta-analysis. Front Endocrinol (Lausanne) [Internet]. 2023 [cited 2023 Jul 27];14. Available from: https://pubmed.ncbi.nlm.nih.gov/37465122/. Zhang S, Qi Z, Wang Y, Song D, Zhu D. Effect of sodium-glucose transporter 2 inhibitors on sarcopenia in patients with type 2 diabetes mellitus: a systematic review and meta-analysis. Front Endocrinol (Lausanne) [Internet]. 2023 [cited 2023 Jul 27];14. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​37465122/​.
25.
go back to reference Riddell MC, Gallen IW, Smart CE, Taplin CE, Adolfsson P, Lumb AN, et al. Exercise management in type 1 diabetes: A consensus statement. Lancet Diabetes Endocrinol. 2017;5(5):377–90.CrossRefPubMed Riddell MC, Gallen IW, Smart CE, Taplin CE, Adolfsson P, Lumb AN, et al. Exercise management in type 1 diabetes: A consensus statement. Lancet Diabetes Endocrinol. 2017;5(5):377–90.CrossRefPubMed
26.
go back to reference Carretero Gómez J, Galeano Fernández TF, Vidal Ríos AS, Pérez Palacios MR, García García GM, García Carrasco C, et al. Malnutrition and sarcopenia worsen short- and long-term outcomes in internal medicine inpatients. Postgrad Med J [Internet]. 2023 Mar 31 [cited 2023 Aug 30;99(1168):56–62. Available from: https://pubmed.ncbi.nlm.nih.gov/36828395/. Carretero Gómez J, Galeano Fernández TF, Vidal Ríos AS, Pérez Palacios MR, García García GM, García Carrasco C, et al. Malnutrition and sarcopenia worsen short- and long-term outcomes in internal medicine inpatients. Postgrad Med J [Internet]. 2023 Mar 31 [cited 2023 Aug 30;99(1168):56–62. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​36828395/​.
27.
28.
go back to reference Zugasti A, Riestra M, Petrina E. Sarcopenia otra complicación crónica a considerar en personas con diabetes. Endocrinol Diabetes Nutr. 2022;69:32–32. (Espec Cong 1). Zugasti A, Riestra M, Petrina E. Sarcopenia otra complicación crónica a considerar en personas con diabetes. Endocrinol Diabetes Nutr. 2022;69:32–32. (Espec Cong 1).
29.
go back to reference París AS, García JM, Gómez-Candela C, Burgos R, Martín Á, Matía P, et al. Malnutrition prevalence in hospitalized elderly diabetic patients. Nutr Hosp. 2013;28(3):592–9. París AS, García JM, Gómez-Candela C, Burgos R, Martín Á, Matía P, et al. Malnutrition prevalence in hospitalized elderly diabetic patients. Nutr Hosp. 2013;28(3):592–9.
30.
go back to reference Sanz-París A, Martín-Palmero A, Gomez-Candela C, García-Almeida JM, Burgos-Pelaez R, Sanz-Arque A, et al. GLIM criteria at hospital admission predict 8-year all-cause mortality in elderly patients with type 2 diabetes mellitus: results from VIDA Study. JPEN J Parenter Enteral Nutr [Internet]. 2020 Nov 1 [cited 2023 Aug 30;44(8):1492–500. Available from: https://pubmed.ncbi.nlm.nih.gov/32026501/. Sanz-París A, Martín-Palmero A, Gomez-Candela C, García-Almeida JM, Burgos-Pelaez R, Sanz-Arque A, et al. GLIM criteria at hospital admission predict 8-year all-cause mortality in elderly patients with type 2 diabetes mellitus: results from VIDA Study. JPEN J Parenter Enteral Nutr [Internet]. 2020 Nov 1 [cited 2023 Aug 30;44(8):1492–500. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​32026501/​.
31.
go back to reference Lardiés-Sánchez B, Sanz-París A, Pérez-Nogueras J, Serrano-Oliver A, Torres-Anoro ME, Cruz-Jentoft AJ. Influence of nutritional status in the diagnosis of sarcopenia in nursing home residents. Nutrition [Internet]. 2017 Sep 1 [cited 2023 Aug 30];41:51–7. Available from: https://pubmed.ncbi.nlm.nih.gov/28760428/. Lardiés-Sánchez B, Sanz-París A, Pérez-Nogueras J, Serrano-Oliver A, Torres-Anoro ME, Cruz-Jentoft AJ. Influence of nutritional status in the diagnosis of sarcopenia in nursing home residents. Nutrition [Internet]. 2017 Sep 1 [cited 2023 Aug 30];41:51–7. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​28760428/​.
32.
go back to reference Sanz-Paris A, González-Fernandez M, Hueso-Del Río LE, Ferrer-Lahuerta E, Monge-Vazquez A, Losfablos-Callau F, et al. Muscle thickness and echogenicity measured by ultrasound could detect local sarcopenia and malnutrition in older patients hospitalized for hip fracture. Nutrients [Internet]. 2021 Jul 1 [cited 2023 Aug 30];13(7). Available from: https://pubmed.ncbi.nlm.nih.gov/34371911/. Sanz-Paris A, González-Fernandez M, Hueso-Del Río LE, Ferrer-Lahuerta E, Monge-Vazquez A, Losfablos-Callau F, et al. Muscle thickness and echogenicity measured by ultrasound could detect local sarcopenia and malnutrition in older patients hospitalized for hip fracture. Nutrients [Internet]. 2021 Jul 1 [cited 2023 Aug 30];13(7). Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​34371911/​.
33.
go back to reference Ahmed N, Choe Y, Mustad VA, Chakraborty S, Goates S, Luo M, et al. Impact of malnutrition on survival and healthcare utilization in Medicare beneficiaries with diabetes: A retrospective cohort analysis. BMJ Open Diabetes Res Care. 2018;6(1):1–9.CrossRef Ahmed N, Choe Y, Mustad VA, Chakraborty S, Goates S, Luo M, et al. Impact of malnutrition on survival and healthcare utilization in Medicare beneficiaries with diabetes: A retrospective cohort analysis. BMJ Open Diabetes Res Care. 2018;6(1):1–9.CrossRef
36.
go back to reference Fukuda T, Bouchi R, Takeuchi T, Nakano Y, Murakami M, Minami, I et al. Association of diabetic retinopathy with both sarcopenia and muscle quality in patients with type 2 diabetes: A cross-sectional study. BMJ Open Diabetes Res Care [Internet]. 2017 May 1 [cited 2023 May 30];5(1):e000404. Available from: https://drc.bmj.com/content/5/1/e000404. Fukuda T, Bouchi R, Takeuchi T, Nakano Y, Murakami M, Minami, I et al. Association of diabetic retinopathy with both sarcopenia and muscle quality in patients with type 2 diabetes: A cross-sectional study. BMJ Open Diabetes Res Care [Internet]. 2017 May 1 [cited 2023 May 30];5(1):e000404. Available from: https://​drc.​bmj.​com/​content/​5/​1/​e000404.
37.
go back to reference Malmstrom TK, Miller DK, Simonsick EM, Ferrucci L, Morley JE. SARC-F: A symptom score to predict persons with sarcopenia at risk for poor functional outcomes. J Cachexia Sarcopenia Muscle [Internet]. 2016 Mar 1 [cited 2023 Jun 14];7(1):28–36. Available from: https://pubmed.ncbi.nlm.nih.gov/27066316/. Malmstrom TK, Miller DK, Simonsick EM, Ferrucci L, Morley JE. SARC-F: A symptom score to predict persons with sarcopenia at risk for poor functional outcomes. J Cachexia Sarcopenia Muscle [Internet]. 2016 Mar 1 [cited 2023 Jun 14];7(1):28–36. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​27066316/​.
38.
go back to reference Parra-Rodríguez L, Szlejf C, García-González AI, Malmstrom TK, Cruz-Arenas E, Rosas-Carrasco O. Cross-cultural adaptation and validation of the spanish-language version of the SARC-F to assess sarcopenia in mexican community-dwelling older adults. J Am Med Dir Assoc [Internet]. 2016 Dec 1 [cited 2022 Jul 22;17(12):1142–6. Available from: http://www.jamda.com/article/S1525861016304236/fulltext. Parra-Rodríguez L, Szlejf C, García-González AI, Malmstrom TK, Cruz-Arenas E, Rosas-Carrasco O. Cross-cultural adaptation and validation of the spanish-language version of the SARC-F to assess sarcopenia in mexican community-dwelling older adults. J Am Med Dir Assoc [Internet]. 2016 Dec 1 [cited 2022 Jul 22;17(12):1142–6. Available from: http://​www.​jamda.​com/​article/​S152586101630423​6/​fulltext.
39.
42.
go back to reference Oviedo-Briones M, Laso ÁR, Carnicero JA, Cesari M, Grodzicki T, Gryglewska B, et al. A comparison of frailty assessment instruments in different clinical and social care settings: The frailtools project. J Am Med Dir Assoc [Internet]. 2021 Mar 1 [cited 2023 Jul 20;22(3):607.e7–607.e12. Available from: http://www.jamda.com/article/S1525861020308215/fulltext. Oviedo-Briones M, Laso ÁR, Carnicero JA, Cesari M, Grodzicki T, Gryglewska B, et al. A comparison of frailty assessment instruments in different clinical and social care settings: The frailtools project. J Am Med Dir Assoc [Internet]. 2021 Mar 1 [cited 2023 Jul 20;22(3):607.e7–607.e12. Available from: http://​www.​jamda.​com/​article/​S152586102030821​5/​fulltext.
43.
go back to reference Kaiser MJ, Bauer JM, Ramsch C, Uter W, Guigoz Y, Cederholm T, et al. Validation of the Mini Nutritional Assessment short-form (MNA-SF): A practical tool for identification of nutritional status. J Nutr Health Aging [Internet]. 2009[cited 2023 Jul 28;13(9):782–8. Available from: https://pubmed.ncbi.nlm.nih.gov/19812868/. Kaiser MJ, Bauer JM, Ramsch C, Uter W, Guigoz Y, Cederholm T, et al. Validation of the Mini Nutritional Assessment short-form (MNA-SF): A practical tool for identification of nutritional status. J Nutr Health Aging [Internet]. 2009[cited 2023 Jul 28;13(9):782–8. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​19812868/​.
44.
go back to reference De Ulíbarri JI, González-Madroño A, De Villar NG, González P, González B, Mancha A, et al. CONUT: A tool for controlling nutritional status. First validation in a hospital population. Nutr Hosp. 2005;20(1):38–45. De Ulíbarri JI, González-Madroño A, De Villar NG, González P, González B, Mancha A, et al. CONUT: A tool for controlling nutritional status. First validation in a hospital population. Nutr Hosp. 2005;20(1):38–45.
50.
go back to reference Porta M, Curletto G, Cipullo D, de la Longrais RR, Trento M, Passera P, et al. Estimating the delay between onset and diagnosis of type 2 diabetes from the time course of retinopathy prevalence. Diabetes Care [Internet]. 2014 Jun 1 [cited 2023 Jun 15];37(6):1668–74. https://doi.org/10.2337/dc13-2101. Porta M, Curletto G, Cipullo D, de la Longrais RR, Trento M, Passera P, et al. Estimating the delay between onset and diagnosis of type 2 diabetes from the time course of retinopathy prevalence. Diabetes Care [Internet]. 2014 Jun 1 [cited 2023 Jun 15];37(6):1668–74. https://​doi.​org/​10.​2337/​dc13-2101.
51.
go back to reference Fukuda T, Bouchi R, Takeuchi T, Nakano Y, Murakami M, Minami I, et al. Association of diabetic retinopathy with both sarcopenia and muscle quality in patients with type 2 diabetes: A cross-sectional study. BMJ open diabetes Res care [Internet]. 2017 May 1 [cited 2023 May 29];5(1). Available from: https://pubmed.ncbi.nlm.nih.gov/28761661/. Fukuda T, Bouchi R, Takeuchi T, Nakano Y, Murakami M, Minami I, et al. Association of diabetic retinopathy with both sarcopenia and muscle quality in patients with type 2 diabetes: A cross-sectional study. BMJ open diabetes Res care [Internet]. 2017 May 1 [cited 2023 May 29];5(1). Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​28761661/​.
53.
go back to reference Andreassen CS, Jakobsen J, Ringgaard S, Ejskjaer N, Andersen H. Accelerated atrophy of lower leg and foot muscles–a follow-up study of long-term diabetic polyneuropathy using magnetic resonance imaging (MRI). Diabetologia [Internet]. 2009[cited 2023 Jun 15;52(6):1182–91. Available from: https://pubmed.ncbi.nlm.nih.gov/19280173/. Andreassen CS, Jakobsen J, Ringgaard S, Ejskjaer N, Andersen H. Accelerated atrophy of lower leg and foot muscles–a follow-up study of long-term diabetic polyneuropathy using magnetic resonance imaging (MRI). Diabetologia [Internet]. 2009[cited 2023 Jun 15;52(6):1182–91. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​19280173/​.
54.
go back to reference Sundar VV, Ong SH, Easaw MEPM, Chee WSS. Sarcopenia with co-existent type 2 diabetes mellitus is associated with worse clinical outcomes among hospitalised cardiac patients. Clin Nutr ESPEN [Internet]. 2021 Dec 1 [cited 2023 May 29];46:380–5. Available from: https://pubmed.ncbi.nlm.nih.gov/34857224/. Sundar VV, Ong SH, Easaw MEPM, Chee WSS. Sarcopenia with co-existent type 2 diabetes mellitus is associated with worse clinical outcomes among hospitalised cardiac patients. Clin Nutr ESPEN [Internet]. 2021 Dec 1 [cited 2023 May 29];46:380–5. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​34857224/​.
55.
go back to reference Yabe D, Nishikino R, Kaneko M, Iwasaki M, Seino Y. Short-term impacts of sodium/glucose co-transporter 2 inhibitors in Japanese clinical practice: considerations for their appropriate use to avoid serious adverse events. Expert Opin Drug Saf [Internet]. 2015 Jun 1 [cited 2023 Jun 15;14(6):795–800. Available from: https://pubmed.ncbi.nlm.nih.gov/25851664/. Yabe D, Nishikino R, Kaneko M, Iwasaki M, Seino Y. Short-term impacts of sodium/glucose co-transporter 2 inhibitors in Japanese clinical practice: considerations for their appropriate use to avoid serious adverse events. Expert Opin Drug Saf [Internet]. 2015 Jun 1 [cited 2023 Jun 15;14(6):795–800. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​25851664/​.
57.
go back to reference Perna S, Guido D, Bologna C, Solerte SB, Guerriero F, Isu A, et al. Liraglutide and obesity in elderly: Efficacy in fat loss and safety in order to prevent sarcopenia. A perspective case series study. Aging Clin Exp Res [Internet]. 2016 Dec 1 [cited 2023 Jun 15;28(6):1251–7. Available from: https://pubmed.ncbi.nlm.nih.gov/26749118/. Perna S, Guido D, Bologna C, Solerte SB, Guerriero F, Isu A, et al. Liraglutide and obesity in elderly: Efficacy in fat loss and safety in order to prevent sarcopenia. A perspective case series study. Aging Clin Exp Res [Internet]. 2016 Dec 1 [cited 2023 Jun 15;28(6):1251–7. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​26749118/​.
58.
59.
go back to reference Ishii S, Nagai Y, Kato H, Fukuda H, Tanaka Y. Effect of the dipeptidyl peptidase-4 inhibitor sitagliptin on muscle mass and the muscle/fat ratio in patients with type 2 diabetes. J Clin Med Res [Internet]. 2020 [cited 2023 Jul 27;12(2):122–6. Available from: https://pubmed.ncbi.nlm.nih.gov/32095182/. Ishii S, Nagai Y, Kato H, Fukuda H, Tanaka Y. Effect of the dipeptidyl peptidase-4 inhibitor sitagliptin on muscle mass and the muscle/fat ratio in patients with type 2 diabetes. J Clin Med Res [Internet]. 2020 [cited 2023 Jul 27;12(2):122–6. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​32095182/​.
60.
go back to reference Rondanelli M, Perna S, Astrone P, Grugnetti A, Solerte SB, Guido D. Twenty-four-week effects of liraglutide on body composition, adherence to appetite, and lipid profile in overweight and obese patients with type 2 diabetes mellitus. Patient Prefer Adherence [Internet]. 2016 Mar 24 [cited 2023 Jul 27];10:407–13. Available from: https://pubmed.ncbi.nlm.nih.gov/27069358/. Rondanelli M, Perna S, Astrone P, Grugnetti A, Solerte SB, Guido D. Twenty-four-week effects of liraglutide on body composition, adherence to appetite, and lipid profile in overweight and obese patients with type 2 diabetes mellitus. Patient Prefer Adherence [Internet]. 2016 Mar 24 [cited 2023 Jul 27];10:407–13. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​27069358/​.
62.
go back to reference Ozeki Y, Masaki T, Kamata A, Miyamoto S, Yoshida Y, Okamoto M, et al. The effectiveness of GLP-1 receptor agonist semaglutide on body composition in elderly obese diabetic patients: A pilot study. Med (Basel, Switzerland) [Internet]. 2022 Sep 16 [cited 2023 Jul 27];9(9):47. Available from: https://pubmed.ncbi.nlm.nih.gov/36135828/. Ozeki Y, Masaki T, Kamata A, Miyamoto S, Yoshida Y, Okamoto M, et al. The effectiveness of GLP-1 receptor agonist semaglutide on body composition in elderly obese diabetic patients: A pilot study. Med (Basel, Switzerland) [Internet]. 2022 Sep 16 [cited 2023 Jul 27];9(9):47. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​36135828/​.
63.
go back to reference Osaka T, Hamaguchi M, Fukui M. Favorable appendicular skeletal muscle mass changes in older patients with type 2 diabetes receiving GLP-1 receptor agonist and basal insulin co-therapy. Clin Med Insights Endocrinol Diabetes [Internet]. 2023 Jan 1 [cited 2023 Jul 27];16. Available from: https://pubmed.ncbi.nlm.nih.gov/37025567/. Osaka T, Hamaguchi M, Fukui M. Favorable appendicular skeletal muscle mass changes in older patients with type 2 diabetes receiving GLP-1 receptor agonist and basal insulin co-therapy. Clin Med Insights Endocrinol Diabetes [Internet]. 2023 Jan 1 [cited 2023 Jul 27];16. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​37025567/​.
64.
65.
go back to reference Massimino E, Izzo A, Riccardi G, Della Pepa G. The impact of glucose-lowering drugs on sarcopenia in type 2 diabetes: Current evidence and underlying mechanisms. Cells. 2021;10(8). Massimino E, Izzo A, Riccardi G, Della Pepa G. The impact of glucose-lowering drugs on sarcopenia in type 2 diabetes: Current evidence and underlying mechanisms. Cells. 2021;10(8).
67.
go back to reference Lee CG, Boyko EJ, Barrett-Connor E, Miljkovic I, Hoffman AR, Everson-Rose SA, et al. Insulin sensitizers may attenuate lean mass loss in older men with diabetes. Diabetes Care [Internet]. 2011 Nov 1 [cited 2023 Jun 15;34(11):2381–6. https://doi.org/10.2337/dc11-1032. Lee CG, Boyko EJ, Barrett-Connor E, Miljkovic I, Hoffman AR, Everson-Rose SA, et al. Insulin sensitizers may attenuate lean mass loss in older men with diabetes. Diabetes Care [Internet]. 2011 Nov 1 [cited 2023 Jun 15;34(11):2381–6. https://​doi.​org/​10.​2337/​dc11-1032.
68.
go back to reference Laksmi PW, Setiati S, Tamin TZ, Soewondo P, Rochmah W, Nafrialdi N, et al. Effect of metformin on handgrip strength, gait speed, myostatin serum level, and health-related quality of life: A double blind randomized controlled trial among non-diabetic pre-frail elderly patients. Acta Med Indones [Internet]. 2017 Aug 8 [cited 2023 Jun 15];49(2):118. Available from: https://www.actamedindones.org/index.php/ijim/article/view/330. Laksmi PW, Setiati S, Tamin TZ, Soewondo P, Rochmah W, Nafrialdi N, et al. Effect of metformin on handgrip strength, gait speed, myostatin serum level, and health-related quality of life: A double blind randomized controlled trial among non-diabetic pre-frail elderly patients. Acta Med Indones [Internet]. 2017 Aug 8 [cited 2023 Jun 15];49(2):118. Available from: https://​www.​actamedindones.​org/​index.​php/​ijim/​article/​view/​330.
70.
go back to reference Rajaobelina K, Helmer C, Vélayoudom-Céphise FL, Nov S, Farges B, Pupier E, et al. Progression of skin autofluorescence of AGEs over 4 years in patients with type 1 diabetes. Diabetes Metab Res Rev [Internet]. 2017 Oct 1 [cited 2023 Jun 15];33(7). Available from: https://pubmed.ncbi.nlm.nih.gov/28719154/. Rajaobelina K, Helmer C, Vélayoudom-Céphise FL, Nov S, Farges B, Pupier E, et al. Progression of skin autofluorescence of AGEs over 4 years in patients with type 1 diabetes. Diabetes Metab Res Rev [Internet]. 2017 Oct 1 [cited 2023 Jun 15];33(7). Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​28719154/​.
71.
go back to reference Sencan C, Dost FS, Ates Bulut E, Isik AT. DPP4 inhibitors as a potential therapeutic option for sarcopenia: A 6-month follow-up study in diabetic older patients. Exp Gerontol [Internet]. 2022 Jul 1 [cited 2023 Jul 27];164. Available from: https://pubmed.ncbi.nlm.nih.gov/35526704/. Sencan C, Dost FS, Ates Bulut E, Isik AT. DPP4 inhibitors as a potential therapeutic option for sarcopenia: A 6-month follow-up study in diabetic older patients. Exp Gerontol [Internet]. 2022 Jul 1 [cited 2023 Jul 27];164. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​35526704/.
72.
go back to reference Solomon SD, Chew E, Duh EJ, Sobrin L, Sun JK, VanderBeek BL, et al. Diabetic retinopathy: A position statement by the American Diabetes Association. Diabetes Care. 2017;40(3):412–8.CrossRefPubMedPubMedCentral Solomon SD, Chew E, Duh EJ, Sobrin L, Sun JK, VanderBeek BL, et al. Diabetic retinopathy: A position statement by the American Diabetes Association. Diabetes Care. 2017;40(3):412–8.CrossRefPubMedPubMedCentral
76.
go back to reference Ibrahim K, May C, Patel HP, Baxter M, Sayer AA, Roberts H. A feasibility study of implementing grip strength measurement into routine hospital practice (GRImP): Study protocol. Pilot Feasibility Stud [Internet]. 2016 Sep 23 [cited 2023 Jun 16];2(1). Available from: https://pubmed.ncbi.nlm.nih.gov/27965846/. Ibrahim K, May C, Patel HP, Baxter M, Sayer AA, Roberts H. A feasibility study of implementing grip strength measurement into routine hospital practice (GRImP): Study protocol. Pilot Feasibility Stud [Internet]. 2016 Sep 23 [cited 2023 Jun 16];2(1). Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​27965846/​.
77.
go back to reference Leong DP, Teo KK, Rangarajan S, Lopez-Jaramillo P, Avezum A, Orlandini A, et al. Prognostic value of grip strength: findings from the Prospective Urban Rural Epidemiology (PURE) study. Lancet (London, England) [Internet]. 2015 Jul 18 [cited 2023 Jun 16];386(9990):266–73. Available from: https://pubmed.ncbi.nlm.nih.gov/25982160/. Leong DP, Teo KK, Rangarajan S, Lopez-Jaramillo P, Avezum A, Orlandini A, et al. Prognostic value of grip strength: findings from the Prospective Urban Rural Epidemiology (PURE) study. Lancet (London, England) [Internet]. 2015 Jul 18 [cited 2023 Jun 16];386(9990):266–73. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​25982160/​.
78.
80.
go back to reference Chen S, Yan S, Aiheti N, Kuribanjiang K, Yao X, Wang Q, et al. A bi-directional Mendelian randomization study of sarcopenia-related traits and type 2 diabetes mellitus. Front Endocrinol (Lausanne) [Internet]. 2023 Mar 8 [cited 2023 May 29];14. Available from: https://pubmed.ncbi.nlm.nih.gov/36967750/. Chen S, Yan S, Aiheti N, Kuribanjiang K, Yao X, Wang Q, et al. A bi-directional Mendelian randomization study of sarcopenia-related traits and type 2 diabetes mellitus. Front Endocrinol (Lausanne) [Internet]. 2023 Mar 8 [cited 2023 May 29];14. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​36967750/​.
81.
go back to reference Roberts HC, Denison HJ, Martin HJ, Patel HP, Syddall H, Cooper C, et al. A review of the measurement of grip strength in clinical and epidemiological studies: Towards a standardised approach. Age Ageing [Internet]. 2011 Jul [cited 2023 Aug 30;40(4):423–9. Available from: https://pubmed.ncbi.nlm.nih.gov/21624928/. Roberts HC, Denison HJ, Martin HJ, Patel HP, Syddall H, Cooper C, et al. A review of the measurement of grip strength in clinical and epidemiological studies: Towards a standardised approach. Age Ageing [Internet]. 2011 Jul [cited 2023 Aug 30;40(4):423–9. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​21624928/​.
82.
go back to reference Mateo Lázaro ML, Penacho Lázaro MA, Berisa Losantos F, Plaza Bayo A. Nuevas tablas de fuerza de la mano para población adulta de Teruel. Nutr Hosp. 2008;23(1):35–40.PubMed Mateo Lázaro ML, Penacho Lázaro MA, Berisa Losantos F, Plaza Bayo A. Nuevas tablas de fuerza de la mano para población adulta de Teruel. Nutr Hosp. 2008;23(1):35–40.PubMed
83.
go back to reference Sánchez Torralvo FJ, Porras N, Abuín Fernández J, García Torres F, Tapia MJ, Lima F, et al. Valores de normalidad de dinamometría de mano en España. Relación con la masa magra. Nutr Hosp. 2018;35(1):98–103.PubMed Sánchez Torralvo FJ, Porras N, Abuín Fernández J, García Torres F, Tapia MJ, Lima F, et al. Valores de normalidad de dinamometría de mano en España. Relación con la masa magra. Nutr Hosp. 2018;35(1):98–103.PubMed
84.
go back to reference Sipers WMWH, Verdijk LB, Sipers SJE, Schols JMGA, van Loon LJC. The Martin vigorimeter represents a reliable and more practical tool than the jamar dynamometer to assess handgrip strength in the geriatric patient. J Am Med Dir Assoc [Internet]. 2016 May 1 [cited 2023 Jun 16];17(5):466.e1–466.e7. Available from: https://pubmed.ncbi.nlm.nih.gov/27107163/. Sipers WMWH, Verdijk LB, Sipers SJE, Schols JMGA, van Loon LJC. The Martin vigorimeter represents a reliable and more practical tool than the jamar dynamometer to assess handgrip strength in the geriatric patient. J Am Med Dir Assoc [Internet]. 2016 May 1 [cited 2023 Jun 16];17(5):466.e1–466.e7. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​27107163/​.
87.
go back to reference Cesari M, Kritchevsky SB, Newman AB, Simonsick EM, Harris TB, Penninx BW, et al. Added value of physical performance measures in predicting adverse health-related events: Results from the Health, Aging, and Body Composition Study. J Am Geriatr Soc [Internet]. 2009 Feb [cited 2023 Jun 16];57(2):251. Available from: https://pubmed.ncbi.nlm.nih.gov/19207142/. Cesari M, Kritchevsky SB, Newman AB, Simonsick EM, Harris TB, Penninx BW, et al. Added value of physical performance measures in predicting adverse health-related events: Results from the Health, Aging, and Body Composition Study. J Am Geriatr Soc [Internet]. 2009 Feb [cited 2023 Jun 16];57(2):251. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​19207142/​.
88.
go back to reference Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing [Internet]. 2010 Apr 13 [cited 2023 Jul 28;39(4):412–23. Available from: https://pubmed.ncbi.nlm.nih.gov/20392703/. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing [Internet]. 2010 Apr 13 [cited 2023 Jul 28;39(4):412–23. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​20392703/​.
90.
go back to reference Newman AB, Simonsick EM, Naydeck BL, Boudreau RM, Kritchevsky SB, Nevitt MC, et al. Association of long-distance corridor walk performance with mortality, cardiovascular disease, mobility limitation, and disability. JAMA [Internet]. 2006[cited 2023 Jul 28,;295(17):2018–26. Available from: https://pubmed.ncbi.nlm.nih.gov/16670410/. Newman AB, Simonsick EM, Naydeck BL, Boudreau RM, Kritchevsky SB, Nevitt MC, et al. Association of long-distance corridor walk performance with mortality, cardiovascular disease, mobility limitation, and disability. JAMA [Internet]. 2006[cited 2023 Jul 28,;295(17):2018–26. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​16670410/​.
91.
go back to reference Pavasini R, Guralnik J, Brown JC, di Bari M, Cesari M, Landi F, et al (1995) Short physical performance battery and all-cause mortality: systematic review and meta-analysis. BMC Med [Internet]. 2016 Dec 22 [cited 2023 Jul 28];14(1). Available from:https://pubmed.ncbi.nlm.nih.gov/28003033/. Pavasini R, Guralnik J, Brown JC, di Bari M, Cesari M, Landi F, et al (1995) Short physical performance battery and all-cause mortality: systematic review and meta-analysis. BMC Med [Internet]. 2016 Dec 22 [cited 2023 Jul 28];14(1). Available from:https://​pubmed.​ncbi.​nlm.​nih.​gov/​28003033/​.
92.
go back to reference Guralnik JM, Ferrucci L, Simonsick EM, Salive ME, Wallace RB. Lower-extremity function in persons over the age of 70 years as a predictor of subsequent disability. N Engl J Med [Internet]. 1995 Mar 2 [cited 2023 Jul 28];332(9):556–62. Available from: https://pubmed.ncbi.nlm.nih.gov/7838189/. Guralnik JM, Ferrucci L, Simonsick EM, Salive ME, Wallace RB. Lower-extremity function in persons over the age of 70 years as a predictor of subsequent disability. N Engl J Med [Internet]. 1995 Mar 2 [cited 2023 Jul 28];332(9):556–62. Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​7838189/​.
93.
Metadata
Title
Diabetic Sarcopenia. A proposed muscle screening protocol in people with diabetes
Expert document
Authors
Daniel de Luis Román
Juana Carretero Gómez
José Manuel García-Almeida
Fernando Garrachón Vallo
German Guzmán Rolo
Juan José López Gómez
Francisco José Tarazona-Santabalbina
Alejandro Sanz-Paris
Publication date
05-02-2024