Abstract:

Sarcopenia (the loss of muscle mass, strength and skeletal muscle function) increases mortality and the risk of hospitalization in the older population. Although it is known that older adults with type 2 diabetes mellitus (T2DM) have a higher risk of dynapenia and sarcopenia, few studies have investigated these conditions in middle-aged populations. The objective of this study was to investigate whether T2DM, its duration, the presence of albuminuria, and glycemic control are associated with sarcopenia and its components in adults. The cross-sectional analysis was based on data from visit 2 of the Brazilian Longitudinal Study of Adult Health (2012-2014). The 2018 European Working Group on Sarcopenia in Older People criteria were used to define dynapenia, low appendicular muscle mass (LAMM), and sarcopenia (absent/probable/confirmed). The explanatory variables were: T2DM; duration of T2DM; T2DM according to the presence of albuminuria; and glycemic control (HbA1C < 7%) among people with T2DM. A total of 12,132 participants (mean age = 55.5, SD: 8.9 years) were included. The odds ratio for LAMM was greater among those with T2DM, T2DM duration from 5 to 10 years, and T2DM without albuminuria. Chances of dynapenia were higher among those with T2DM, T2DM duration > 10 years, and T2DM with and without albuminuria. The variables T2DM, T2DM ≥ 10 years, and T2DM with albuminuria increased the odds of probable sarcopenia, and T2DM duration from 5 to 10 years increased the odds of confirmed sarcopenia. The results support the importance of frequently monitoring the musculoskeletal mass and strength of individuals with T2DM to prevent sarcopenia and related outcomes.

Keywords:
Sarcopenia; Hand Grip Strength; Muscle Strength; Type 2 Diabetes Mellitus

Resumo:

A sarcopenia (perda de massa muscular, força e função muscular esquelética) aumenta a mortalidade e o risco de hospitalização em idosos. Idosos com diabetes mellitus tipo 2 (DMT2) apresentam risco elevado de desenvolver dinapenia e sarcopenia, mas poucos estudos investigaram populações de meia-idade. O objetivo foi investigar se DMT2, sua duração, a presença de albuminúria e o controle glicêmico estão associados à sarcopenia e seus componentes em adultos. Análise transversal baseada nos dados da segunda visita do Estudo Longitudinal de Saúde do Adulto (2012-2014). Os critérios do European Working Group on Sarcopenia in Older People [Grupo de Trabalho Europeu sobre Sarcopenia em Pessoas Idosas] de 2018 foram usados para definir dinapenia, baixa massa muscular apendicular e sarcopenia (ausente/provável/confirmada). As variáveis explicativas foram: DMT2; duração do DMT2; DMT2 de acordo com a presença de albuminúria; e controle glicêmico (HbA1c < 7%) entre pessoas com DMT2. Foram incluídos 12.132 participantes (idade média de 55,5; DP: 8,9 anos). A razão de chances para baixa massa muscular apendicular foi maior entre pessoas com DMT2, duração do DMT2 entre 5 e 10 anos e DMT2 sem albuminúria. As chances de dinapenia foram maiores entre pessoas com DMT2, duração do DMT2 > 10 anos e DMT2 com e sem albuminúria. DMT2, DMT2 ≥ 10 anos e DMT2 com albuminúria aumentaram as chances de sarcopenia provável e duração do DMT2 entre 5 e 10 anos aumentaram as chances de sarcopenia confirmada. Os resultados reforçam a importância do monitoramento frequente da massa e da força muscular em indivíduos com DMT2 para prevenir a sarcopenia e desfechos relacionados.

Palavras-chave:
Sarcopenia; Força da Mão; Força Muscular; Diabetes Mellitus Tipo 2

Resumen:

La sarcopenia (pérdida de masa muscular, fuerza y función muscular esquelética) aumenta la mortalidad y el riesgo de hospitalización en ancianos. Los ancianos con diabetes mellitus tipo 2 (DMT2) presentan un mayor riesgo de sufrir dinapenia y sarcopenia, pero pocos estudios han investigado poblaciones de mediana edad. El objetivo fue investigar si la DMT2, su duración, la presencia de albuminuria y el control glucémico están asociados con la sarcopenia y sus componentes en adultos. Análisis transversal basado en los datos de la visita 2 del Estudio Longitudinal de Salud del Adulto en Brasil (2012-2014). Se utilizaron los criterios del European Working Group on Sarcopenia in Older People [Grupo de Trabajo Europeo sobre Sarcopenia en Personas Mayores] del 2018 para definir dinapenia, baja masa muscular apendicular y sarcopenia (ausente/probable/confirmada). Las variables explicativas fueron las siguientes: DMT2; duración de la DMT2; DMT2 según la presencia de albuminuria; y control glucémico (HbA1c < 7%) entre personas con DMT2. Se incluyeron 12.132 participantes (edad media = 55,5, DE: 8,9 años). La razón de probabilidades de masa muscular apendicular baja fue mayor entre personas con DMT2, duración de la DMT2 entre 5 y 10 años y DMT2 sin albuminuria. Las probabilidades de dinapenia fueron mayores entre las personas con DMT2, duración de la DMT2 > 10 años y DMT2 con y sin albuminuria. Las condiciones de DMT2, DMT2 ≥ 10 años y DMT2 con albuminuria aumentaron las probabilidades de sarcopenia probable y la duración de la DMT2 entre 5 y 10 años las probabilidades de sarcopenia confirmada. Los resultados refuerzan la importancia del monitoreo frecuente de la masa y de la fuerza musculoesquelética en individuos con DMT2 para prevenir la sarcopenia y los desenlaces relacionados.

Palabras-clave:
Sarcopenia; Fuerza de la Mano; Fuerza Muscular; Diabetes Mellitus Tipo 2

Introduction

Sarcopenia is a multifactorial muscle disease characterized by loss of strength and muscle mass ¹1. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019; 48:16-31.^,22. Fuggle N, Shaw S, Dennison E, Cooper C. Sarcopenia. Best Pract Res Clin Rheumatol 2017; 31:218-42.. It is a major public health problem that causes loss of independence and high morbidity and mortality; in addition, it has high personal and social health care costs, due to frequent hospital admissions and increased institutionalization ³3. Peterson MD, McGrath R, Zhang P, Markides KS, Al Snih S, Wong R. Muscle weakness is associated with diabetes in older Mexicans: the Mexican Health and Aging Study. J Am Med Dir Assoc 2016; 17:933-8.. For a long time, sarcopenia was solely related to aging and was studied primarily in the older adults ⁴4. Epidemiologic and methodologic problems in determining nutritional status of older persons. Proceedings of a conference. Albuquerque, New Mexico, October 19-21, 1988. Am J Clin Nutr 1989; 50(5 Suppl):1121-235.. Its definition underwent successive changes until 2018, when the European Working Group on Sarcopenia in Older People (EWGSOP2) started to consider low muscle strength (dynapenia) the first parameter that should be assessed in individuals with suspected sarcopenia, as it is the most reliable measure of muscle function ¹1. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019; 48:16-31..

The prevalence of sarcopenia varies greatly worldwide, ranging from 1%-29% in community-dwelling individuals aged over 50 years to 14%-33% among those living in long-term care facilities ⁵5. Cruz-Jentoft AJ, Landi F, Schneider SM, Zuniga C, Arai H, Boirie Y, et al. Prevalence of and interventions for sarcopenia in ageing adults: a systematic review. Report of the International Sarcopenia Initiative (EWGSOP and IWGS). Age Ageing 2014; 43:748-59.. A case-control study on chronic kidney disease based on the UK Biobank (United Kingdom) found a prevalence of 0.2% of confirmed sarcopenia in its control group, composed by adults (mean age = 56.1, standard deviation - SD: 8.1 years), using the EWGSOP2 criteria ⁶6. Wilkinson TJ, Miksza J, Yates T, Lightfoot CJ, Baker LA, Watson EL, et al. Association of sarcopenia with mortality and end-stage renal disease in those with chronic kidney disease: a UK Biobank study. J Cachexia Sarcopenia Muscle 2021; 12:586-98.. The large variation in sarcopenia prevalence may be caused by factors such as diagnostic criteria and the sociodemographic and health characteristics of the populations studied, especially age range and the prevalence of comorbidities ⁷7. 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 2010; 39:412-23.^,88. Santilli V, Bernetti A, Mangone M, Paoloni M. Clinical definition of sarcopenia. Clin Cases Miner Bone Metab 2014; 11:177-80.^,99. Wang T, Feng X, Zhou J, Gong H, Xia S, Wei Q, et al. Type 2 diabetes mellitus is associated with increased risks of sarcopenia and pre-sarcopenia in Chinese elderly. Sci Rep 2016; 6:38937.. In Brazil, which is a middle-income country with fast-ageing population, a systematic review of 31 studies identified that the prevalence of sarcopenia (defined as low muscle mass, low muscle function, or low muscle mass plus low muscle function) is 16% among individuals aged 60 years or older ¹⁰10. Diz JBM, Leopoldino AAO, Moreira BS, Henschke N, Dias RC, Pereira LSM, et al. Prevalence of sarcopenia in older Brazilians: a systematic review and meta-analysis. Geriatr Gerontol Int 2016; 17:5-16.. Low muscle mass levels were identified using magnetic resonance imaging, computed tomography, dual-energy X-ray absorptiometry (DEXA), and bioelectrical impedance or anthropometry; and low muscle function levels were defined by low hand grip and/or knee extension/flexion strength, or low physical performance according to components of the Short Physical Performance Battery and the Timed Up & Go test ¹⁰10. Diz JBM, Leopoldino AAO, Moreira BS, Henschke N, Dias RC, Pereira LSM, et al. Prevalence of sarcopenia in older Brazilians: a systematic review and meta-analysis. Geriatr Gerontol Int 2016; 17:5-16..

The prevalence of dynapenia also varies according to different definitions and scenarios (e.g., health conditions and characteristics of individuals), ranging from 17.8% in the European population aged 70 or over ¹¹11. Bertoni M, Maggi S, Manzato E, Veronese N, Weber G. Depressive symptoms and muscle weakness: a two-way relation? Exp Gerontol 2018; 108:87-91. to 71.2% in a Falls and Fractures Clinic in Colombia ¹²12. Benjumea AM, Curcio CL, Duque G, Gomez F. Dynapenia and sarcopenia as a risk factor for disability in a falls and fractures clinic in older persons. Open Access Maced J Med Sci 2018; 6:344-9.. The Brazilian Longitudinal Study of Aging (ELSI-Brazil) revealed a high prevalence of dynapenia (17.2%) in older adults ¹³13. Borges VS, Lima-Costa MFF, Andrade FB. A nationwide study on prevalence and factors associated with dynapenia in older adults: ELSI-Brazil. Cad Saúde Pública 2020; 36:e00107319..

Type 2 diabetes mellitus (T2DM) is a chronic noncommunicable metabolic disease with important systemic repercussions on the macro and microvasculature of individuals ¹⁴14. Sociedade Brasileira de Diabetes. Diretrizes da Sociedade Brasileira de Diabetes 2019-2020. http://www.saude.ba.gov.br/wp-content/uploads/2020/02/Diretrizes-Sociedade-Brasileira-de-Diabetes-2019-2020.pdf (accessed on 18/Sep/2022).
http://www.saude.ba.gov.br/wp-content/up... . Recent studies have shown that people with T2DM tend to have a significantly higher impairment of muscle function than individuals without the disease ¹1. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019; 48:16-31.^,33. Peterson MD, McGrath R, Zhang P, Markides KS, Al Snih S, Wong R. Muscle weakness is associated with diabetes in older Mexicans: the Mexican Health and Aging Study. J Am Med Dir Assoc 2016; 17:933-8.^,99. Wang T, Feng X, Zhou J, Gong H, Xia S, Wei Q, et al. Type 2 diabetes mellitus is associated with increased risks of sarcopenia and pre-sarcopenia in Chinese elderly. Sci Rep 2016; 6:38937.. Moreover, T2DM may also contribute to accelerating dynapenia progression and cause significant degradation of lean mass, alone or associated with low muscle strength, even in adults ¹1. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019; 48:16-31.^,1414. Sociedade Brasileira de Diabetes. Diretrizes da Sociedade Brasileira de Diabetes 2019-2020. http://www.saude.ba.gov.br/wp-content/uploads/2020/02/Diretrizes-Sociedade-Brasileira-de-Diabetes-2019-2020.pdf (accessed on 18/Sep/2022).
http://www.saude.ba.gov.br/wp-content/up... ^,1515. Trierweiler H, Kisielewicz G, Hoffmann Jonasson T, Rasmussen Petterle R, Aguiar Moreira C, Zeghbi Cochenski Borba V. Sarcopenia: a chronic complication of type 2 diabetes mellitus. Diabetol Metab Syndr 2018; 10:25.^,1616. Mesinovic J, Zengin A, De Courten B, Ebeling PR, Scott D. Sarcopenia and type 2 diabetes mellitus: a bidirectional relationship. Diabetes Metabol Syndr Obes 2019; 12:1057-72.^,1717. Guerrero N, Bunout D, Hirsch S, Barrera G, Leiva L, Henríquez S, et al. Premature loss of muscle mass and function in type 2 diabetes. Diabetes Res Clin Prac 2016; 117:32-8..

Even with the aforementioned data, critical gaps remain in the literature on the relationship between T2DM and sarcopenia. The use of different definitions and cut-off points to define sarcopenia, the recent changes in dynapenia and sarcopenia parameters, and the lack of studies including middle-aged adults limit conclusions about the relationship between T2DM and sarcopenia. The association of sarcopenia with T2DM-specific characteristics such as duration of diagnosis, disease complications, and glycemic control have been scarcely studied. Given this scenario, this study sought to investigate the association of T2DM and its factors, including the duration of diagnosis, presence of albuminuria, and glycemic control, with sarcopenia and each sarcopenia component in Brazilian middle-aged and older adults. We hypothesize that T2DM is associated with greater chances of sarcopenia and that the magnitude of the associations is greater among individuals with a longer duration of diagnosis, those with albuminuria, and those with inadequate glycemic control.

Materials and methods

Study design and population

This is a cross-sectional study that used data from the visit 2 of the Brazilian Longitudinal Study of Adult Health (ELSA-Brasil), a cohort consisting, at baseline (2008-2010), of 15,105 active and retired civil servants aged 35-74 years who worked in public higher education institutions and research centers in six Brazilian states: Minas Gerais, São Paulo, Rio de Janeiro, Rio Grande do Sul, Espírito Santo, and Bahia.

Muscle strength and body composition examinations began to be conducted in the visit 2 of the ELSA-Brasil cohort (2012-2014), which included 14,014 individuals. All participants with valid information regarding T2DM, handgrip strength (HGS), and bioelectrical impedance analysis (BIA) were included (n = 12,478). In order to avoid including individuals with type 1 diabetes mellitus, this study excluded participants who reported, at baseline of ELSA-Brasil, that they had been medically diagnosed with diabetes before 30 years of age (n = 45) and/or used insulin as the first medication for the treatment of diabetes (n = 32). In addition, this study excluded individuals with a self-reported medical diagnosis of stroke (n = 131), due to the well-defined association of this morbidity with sarcopenia, and those who, in visit 2, reported having undergone bariatric surgery (n = 138), due to the possibility of remission of the T2DM diagnosis during the study follow-up period. Considering these overlapping criteria, the final analytic sample consisted of 12,132 participants.

ELSA-Brasil was approved by the Research Ethics Committee of each participating institution under registries 669/06 (São Paulo University), 343/06 (Oswaldo Cruz Foundation), 041/06 (Espírito Santo Federal University), 186/06 (Minas Gerais Federal University), 194/06 (Rio Grande do Sul Federal University), and 027/06 (Bahia Federal University). All participants were informed about the objectives of the study and signed an informed consent form.

Procedures

In ELSA-Brasil, data collection was conducted via face-to-face interviews, clinical and laboratory examinations, and anthropometric measurements. Trained and certified professionals performed all measurements and evaluations according to pre-established protocols ¹⁸18. Aquino EML, Barreto SM, Bensenor IM, Carvalho MS, Chor D, Duncan BB, et al. Brazilian Longitudinal Study of Adult Health (ELSA-Brasil): objectives and design. Am J Epidemiol 2012; 175:315-24..

Investigation of sarcopenia and its components, and definition of the outcome variables

Muscle strength was investigated using HGS, which was obtained using a Jamar hydraulic hand dynamometer (Sammons Preston, https://www.performancehealth.com/products/brand/sammons-preston). Three measurements were made on each hand, with an interval of approximately one minute between them. The measure with the highest value in kilograms (kg) was used to define HGS.

Skeletal muscle mass was obtained using a vertical tetrapolar BIA device, which uses 8-point tactile electrodes (Inbody230; InBody Co., https://inbody.com). For the test, all participants were instructed not to exercise during the 24 hours prior to the test, not to drink caffeine or alcohol 12 hours before the test, and to empty their bladder just before the test. The BIA result is presented as a percentage of total, appendicular and trunk lean mass, adjusted for sex and age. The present study used appendicular muscle mass adjusted by height squared ¹1. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019; 48:16-31..

Sarcopenia and its components were defined according to the revised EWGSOP2 criteria ¹1. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019; 48:16-31., as follows: presence of low muscle strength (dynapenia), when HGS was < 27kg for men and < 16kg for women; low appendicular muscle mass (LAMM), when appendicular muscle mass corrected for squared height was < 7kg/m² for men and < 5.5kg/m² for women; and sarcopenia was determined by the simultaneous presence of dynapenia and LAMM.

Based on these criteria, three outcomes were analyzed separately: (a) LAMM (yes/no); (b) dynapenia (yes/no); and (c) sarcopenia, categorized as absent (reference), probable, when only dynapenia was present, and confirmed, when both LAMM and dynapenia were present. Individuals with isolated LAMM were considered to have no sarcopenia and included in the reference category, in accordance with the EWGSOP2.

T2DM and related variables

The presence of T2DM (yes/no) was investigated in all participants included in the present study with two means (questionnaire and laboratory measures), and defined by a self-reported diagnosis and/or the presence of at least one altered laboratory measurement, namely: fasting blood glucose ≥ 126mg/dL and/or blood glucose 2 hours after dextrosol ≥ 200mg/dL and/or glycated hemoglobin (HbA1c) ≥ 6.5 ¹⁹19. Schmidt MI, Hoffmann JF, de Fátima Sander Diniz M, Lotufo PA, Griep RH, Bensenor IM, et al. High prevalence of diabetes and intermediate hyperglycemia - The Brazilian Longitudinal Study of Adult Health (ELSA-Brasil). Diabetol Metab Syndr 2014; 6:123.^,2020. Barreto SM, Ladeira RM, Bastos MSCBO, Diniz MFHS, Jesus EA, Kelles SMB, et al. Estratégias de identificação, investigação e classificação de desfechos incidentes no ELSA-Brasil. Rev Saúde Pública 2013; 47:79-86.^,2121. Fedeli LG, Vidigal PG, Leite CM, Castilhos CD, Pimentel RA, Maniero VC, et al. Logística de coleta e transporte de material biológico e organização do laboratório central no ELSA-Brasil. Rev Saúde Pública 2013; 47 Suppl 2:63-71.. The self-reported diagnosis of T2DM was obtained by a positive response to one of the following questions: “Has a physician ever informed you that you have or had diabetes?” and “Have you used diabetes medication in the past two weeks?”, and self-reported T2DM criteria were met by 1,371 (61.9%) of the participants with diabetes.

Blood was drawn from the participants after they underwent a 12 hours fast. Plasma glucose was measured using the hexokinase enzyme method (ADVIA Chemistry; Siemens, https://www.siemens-healthineers.com); HbA1c was measured with high-pressure liquid chromatography (Bio-RadLaboratories, https://www.bio-rad.com/), using a method certified by the U.S. National Glycohemoglobin Standardization Program ¹⁸18. Aquino EML, Barreto SM, Bensenor IM, Carvalho MS, Chor D, Duncan BB, et al. Brazilian Longitudinal Study of Adult Health (ELSA-Brasil): objectives and design. Am J Epidemiol 2012; 175:315-24..

The duration of the T2DM diagnosis was obtained by subtracting the age of T2DM diagnosis from the age of the individual during visit 2 of the ELSA-Brasil, then divided into four categories: no T2DM (reference category), T2DM < 5 years, T2DM between 5 and 10 years, and T2DM ≥ 10 years.

The presence of albuminuria (yes/no) was defined by a urinary albumin/creatinine ratio (ACR) greater than or equal to 30mg/g in visit 2 ²²22. American Diabetes Association. Microvascular complications and foot care: standards of medical care in diabetes-2020. Diabetes Care 2019; 43 Suppl 1:S135-51.^,2323. Barreto SM, Ladeira RM, Duncan BB, Schmidt MI, Lopes AA, Benseñor IM, et al. Chronic kidney disease among adult participants of the ELSA-Brasil cohort: association with race and socioeconomic position. J Epidemiol Community Health 2015; 70:380-9.. Urinary creatinine was measured with the colorimetric enzymatic assay (Jaffé method, ADVIA Chemistry) and urinary albumin was measured using the immunochemical assay (nephelometry; Dade Behring, https://www.siemens.com/), both applied to 12-hour urine overnight samples ¹⁸18. Aquino EML, Barreto SM, Bensenor IM, Carvalho MS, Chor D, Duncan BB, et al. Brazilian Longitudinal Study of Adult Health (ELSA-Brasil): objectives and design. Am J Epidemiol 2012; 175:315-24.. The T2DM variable was categorized into three groups according to the presence of albuminuria: absence of T2DM (reference), T2DM without albuminuria (ACR < 30mg/g), and T2DM with albuminuria (ACR ≥ 30mg/g). Individuals with ACR ≥ 30mg/g and no T2DM remained in the reference category.

Lastly, the glycemic control analysis was restricted to participants who reported having already been diagnosed with T2DM (prevalent cases), i.e., individuals without T2DM or with T2DM identified only by laboratory findings during visit 2 of the ELSA-Brasil were not included in this analysis. The HbA1c test was used to identify T2DM glycemic control: individuals with HbA1c < 7% (reference category) were considered to have controlled T2DM and individuals with HbA1c ≥ 7% were considered to have uncontrolled T2DM ²⁴24. American Diabetes Association. Glycemic targets: standards of medical care in diabetes-2020. Diabetes Care 2019; 43 Supplement 1:S66-76..

Covariates

Sociodemographic, behavioral, and health indicators were included as covariate variables in the statistical models. The sociodemographic data were: sex; age (continuous scale); education level (university degree, high school, complete elementary school or incomplete elementary school); marital status (married/cohabiting, separated/divorced, widowed, single or other); and race/color (black, brown, white, yellow or Indigenous).

Health-related behaviors included leisure-time physical activity (low, moderate or vigorous), which was assessed using the International Physical Activity Questionnaire (IPAQ) ²⁵25. International Physical Activity Questionnaire. Guidelines for data processing and analysis of the International Physical Activity Questionnaire (IPAQ) - short form. https://www.physio-pedia.com/images/c/c7/Quidelines_for_interpreting_the_IPAQ.pdf (accessed on 15/Jul/2015).
https://www.physio-pedia.com/images/c/c7... , excessive alcohol consumption (yes/no), assessed with the semi-quantitative Food Frequency Questionnaire (SQ-FFQ) and defined as ≥ 210g of alcohol per week for men and ≥ 140g per week for women ²⁵25. International Physical Activity Questionnaire. Guidelines for data processing and analysis of the International Physical Activity Questionnaire (IPAQ) - short form. https://www.physio-pedia.com/images/c/c7/Quidelines_for_interpreting_the_IPAQ.pdf (accessed on 15/Jul/2015).
https://www.physio-pedia.com/images/c/c7... , and smoking (never smoked/ex-smoker/smoker). The body mass index (BMI) was calculated from body weight divided by height squared and used on a continuous scale.

Self-reported cardiovascular disease (CVD) (yes/no) included the following conditions: acute myocardial infarction; angina; congestive heart failure; and coronary artery bypass grafting. Renal dysfunction was defined by estimated glomerular filtration rate (eGFR) < 60mL/minute/1.73m², and eGFR was estimated with the Chronic Kidney Disease Epidemiology Collaboration (CKD-EPI) equation, without adjustment for race/color ²³23. Barreto SM, Ladeira RM, Duncan BB, Schmidt MI, Lopes AA, Benseñor IM, et al. Chronic kidney disease among adult participants of the ELSA-Brasil cohort: association with race and socioeconomic position. J Epidemiol Community Health 2015; 70:380-9..

The use of continuous medication in the last two weeks was assessed during an interview and by checking the packaging, package inserts, and/or cartridges of the medication used. The use of angiotensin-converting enzyme inhibitors (ACEI) and/or angiotensin receptor blockers (ARB) in visit 2 was considered for adjustment.

Finally, the self-reported medical diagnosis of rheumatic diseases and cancer in visit 1, the use of oral or parenteral corticosteroids, and the use of drugs for the treatment of rheumatoid arthritis and systemic lupus erythematosus (abatacepte, adalimumab, azathioprine, cyclosporine, hydroxychloroquine, leflunomide, methotrexate, sulfasalazine) were assessed.

Statistical analysis

Descriptive analyses were conducted using mean and SD (for continuous variables) and frequencies and percentages (for categorical variables). Differences between groups were investigated with the chi-square test. The association of T2DM, the variables related to T2DM, and the components of sarcopenia, LAMM (yes/no) and dynapenia (yes/no), was analyzed using a logistic regression model. The association of these variables with sarcopenia, which was identified according to the EWGSOP2 (absent/probable/confirmed), was assessed using multinomial logistic regression models.

All analyses followed the steps described as follows, and missing values were removed from the final models. We first investigated the association between the presence of T2DM and each response variable. When the final model showed a statistical association (p < 0.05) between T2DM and the response variable in question, the associations with the other T2DM-related explanatory variables (duration of diagnosis, presence of albuminuria, and glycemic control of T2DM) were investigated.

After the bivariate regression analyses (crude model) were conducted, sequential adjustments were made with the following covariates: BMI (model 1); sex, age, education level, marital status, and race/color (model 2); physical activity, excessive alcohol consumption, and smoking (model 3); CVD and chronic renal failure (model 4 - adjusted model). Additionally, the variable HbA1c (continuous) was added to the fully adjusted models with T2DM as an explanatory variable to evaluate if the association obtained was independent of the glycemic levels.

The variable use of ACEI and/or ARBs (yes/no) in visit 2 was added to the final models investigating the association between T2DM according to the presence of albuminuria and the outcome variables. Sensitivity analyses were also performed, excluding participants who reported using oral/parenteral corticosteroids, and those who had self-reported diagnoses of cancer and rheumatic diseases (with the concurrent use of specific medications). Lastly, interactions between T2DM and age were investigated (due to the already known association of these variables), and were not significant (data not shown).

The magnitude of the associations found was estimated using the odds ratio (OR), with a 95% confidence interval (95%CI). For all logistic regression models, the Hosmer-Lemeshow goodness-of-fit test was performed.

The data were analyzed using the Stata software, version 14.0 (https://www.stata.com), with a 95% confidence level.

Results

Most of the 12,132 participants were female (54.3%). The sample had a mean age of 55.5 (SD: 8.9) years (total age ranging from 38 to 79 years), and 18.3% of participants had T2DM. The overall prevalence of LAMM was 6.1% and that of dynapenia was 3.9%, with dynapenia being more frequent in women (4.5%). The prevalence of both LAMM and dynapenia rose in parallel with decreases in educational levels and with increases in age (Table 1). Regarding sarcopenia, defined according to the EWGSOP2, the frequency of probable sarcopenia was higher in women (3.8%) and rose in parallel with increases in age and with decreases in educational levels (Table 1).

Furthermore, the prevalences of probable and confirmed sarcopenia were higher among individuals with T2DM - especially those who had T2DM with albuminuria - and increased progressively with a longer duration of T2DM diagnosis (Table 1).

T2DM increased the odds of LAMM (OR = 1.51; IC95%: 1.12-2.04) after all adjustments for confounding factors (Table 2). For the duration of T2DM, a positive association with LAMM was identified only in individuals diagnosed between 5 and 10 years (OR = 2.14; 95%CI: 1.30-3.53) (Table 3). The presence of albuminuria and glycemic control in T2DM was not statistically associated with LAMM (Table 3).

T2DM also increased the odds of dynapenia (OR = 1.54; IC95%: 1.18-2.01) (Table 2). Regarding the duration of T2DM, only T2DM cases that lasted > 10 years remained statistically associated with dynapenia after adjustments (OR = 2.00; 95%CI: 1.38-2.92) (Table 4). In fully adjusted models, both T2DM without (OR = 1.31; 95%CI: 1.02-1.68) and with albuminuria (OR = 2.22; 95%CI: 1.44-3.43) were associated with higher odds of dynapenia, and the magnitude of association was greater in the latter (Table 4). In individuals with T2DM, glycemic control was not statistically associated with dynapenia (Table 4).

After all the adjustments, it was found that T2DM increased the chances of probable sarcopenia by about 40% (OR = 1.43; 95%CI: 1.07-1.93) and the chances of confirmed sarcopenia by more than double (OR = 2.50; 95%CI: 1.39-4.50) (Table 2). Regarding the duration of T2DM diagnosis, only a duration ≥ 10 years (OR = 1.75; 95%CI: 1.21-2.84) increased the odds of probable sarcopenia, while a duration of ≥ 5 to < 10 years increased the odds of confirmed sarcopenia by 3.30-fold (95%CI: 1.32-8,27) and a duration ≥ 10 years increased the odds by 3.74-fold (95%CI: 1.77-7.55) (Table 5). Both T2DM without and with albuminuria were associated with probable (OR = 1.27; 95%CI: 0.97-1.68 and OR = 2.04; 95%CI: 1.25-3.32, respectively) and confirmed sarcopenia (OR = 1.76; 95%CI: 0.96-3.22 and OR = 3.81; 95%CI: 1.50-9.67, respectively) (Table 5), even though the association of T2DM without albuminuria with confirmed sarcopenia was on the borderline of statistical significance. No statistical association was found between T2DM glycemic control and probable or confirmed sarcopenia among individuals with prevalent T2DM (Table 5).

Including the adjustment for ACEI and ARB use in the final models investigating the association between T2DM with and without albuminuria and response variables hardly changed the OR (Tables 6, 7, and 8). Sensitivity analyses excluding individuals with cancer, rheumatic diseases, and those who used oral/parenteral corticosteroid showed no changes in the directions of the associations between the presence of T2DM and the response variables and no major changes in the magnitude of the associations (Tables 9, 10, and 11).

The Hosmer-Lemeshow tests for goodness-of-fit showed an adequate fit of the models (p > 0.05).

Discussion

This study describes the prevalence of sarcopenia and its components, assessed according to the EWGSOP2, in a large cohort of Brazilian middle-aged and older adults living in the community. The findings support the initial hypotheses, as they show that T2DM increased the odds of LAMM, dynapenia, and probable and confirmed sarcopenia by 55%, 58%, 49%, and 153%, respectively, even after adjustments for several confounding factors were made. Regarding the duration of T2DM diagnosis, individuals with 5-9 years of diagnosis had higher odds of LAMM and confirmed sarcopenia, and those with a diagnosis duration ≥ 10 years had higher odds of dynapenia and sarcopenia (both probable and confirmed). T2DM without and especially with the presence of albuminuria was positively associated with dynapenia, whereas T2DM with albuminuria increased the odds of confirmed sarcopenia by more than 300%. Contrary to our initial expectations, glycemic control in subjects with a previous diagnosis of T2DM was not associated with any of the conditions analyzed. In addition, no interaction was observed between the explanatory variables and age.

Our results on the association of T2DM with dynapenia and sarcopenia (probable and confirmed) are consistent with previous studies conducted with different populations, regardless of the criteria employed to identify the presence of such muscle dysfunctions. For instance, in an English study on 5,290 older adults, the chance of dynapenia was found to be higher among individuals with T2DM than among those without it ²⁶26. Nebuloni CC, Máximo RO, de Oliveira C, Alexandre TS. Uncontrolled diabetes as an associated factor with dynapenia in adults aged 50 years or older: sex differences. J Gerontol A Biol Sci Med Sci 2020; 75:1191-7.. A Chinese study on 1,090 community-dwelling older adults also found a positive association of T2DM with sarcopenia ⁹9. Wang T, Feng X, Zhou J, Gong H, Xia S, Wei Q, et al. Type 2 diabetes mellitus is associated with increased risks of sarcopenia and pre-sarcopenia in Chinese elderly. Sci Rep 2016; 6:38937.. Positive associations between T2DM and sarcopenia, defined according to EWGSOP2 criteria, were also found in smaller studies conducted in Spain ²⁷27. Vergara Ruiz JC, Muñoz Triviño MP, Candelario Alcalá I, Sanz Sánchez M. Sarcopenia y dinapenia en pacientes con diabetes mellitus tipo 2 en un área rural de Castilla-La Mancha. Rev Clín Med Fam 2017; 10:86-95. and Japan ²⁸28. Su Y, Hirayama K, Han T, Izutsu M, Yuki M. Sarcopenia prevalence and risk factors among Japanese community dwelling older adults living in a snow-covered city according to EWGSOP2. J Clin Med 2019; 8:291..

The relationship between the duration of diabetes diagnosis and sarcopenia, shown in this study, suggests that the greater the duration of exposure to the disease, the greater the chances of developing muscle impairment and sarcopenia, which is in line with the literature ²⁹29. Mori H, Kuroda A, Ishizu M, Ohishi M, Takashi Y, Otsuka Y, et al. Association of accumulated advanced glycation end-products with a high prevalence of sarcopenia and dynapenia in patients with type 2 diabetes. J Diabetes Investig 2019; 10:1332-40.^,3030. Mori H, Kuroda A, Matsuhisa M. Clinical impact of sarcopenia and dynapenia on diabetes. Diabetol Int 2019; 10:183-7.^,3131. Zoungas S, Woodward M, Li Q, Cooper ME, Hamet P, Harrap S, et al. Impact of age, age at diagnosis and duration of diabetes on the risk of macrovascular and microvascular complications and death in type 2 diabetes. Diabetologia 2014; 57:2465-74.^,3232. Cui M, Gang X, Wang G, Xiao X, Li Z, Jiang Z, et al. A cross-sectional study: associations between sarcopenia and clinical characteristics of patients with type 2 diabetes. Medicine (Baltimore) 2020; 99:e18708.. Interestingly, in cases of confirmed sarcopenia, this relationship is observed when T2DM diagnosis has a duration of 5-10 years or ≥ 10 years, with no signs of a gradual relationship, but in cases of probable sarcopenia, this relationship is only present when T2DM diagnosis has a duration ≥ 10 years. Despite being preventable, micro and macrovascular complications are part of the T2DM pathway and are more frequent in individuals with a longer-lasting case of diabetes, a worse risk profile, and poor glycemic control ³³33. Girach A, Manner D, Porta M. Diabetic microvascular complications: can patients at risk be identified? A review. Int J Clin Pract 2006; 60:1471-83.. This study observed that T2DM accompanied by albuminuria doubled the chance of dynapenia and tripled the chance of confirmed sarcopenia (assessed according to the EWGSOP2), which corroborates previous results ³⁴34. Chung HS, Hwang SY, Choi JH, Lee HJ, Yoo HJ, Seo J-A, et al. Effects of low muscle mass on albuminuria and chronic kidney disease in patients with type 2 diabetes: the Korean Sarcopenic Obesity Study (KSOS). J Gerontol A Biol Sci Med Sci 2018; 73:386-92.^,3535. Bouchi R, Fukuda T, Takeuchi T, Minami I, Yoshimoto T, Ogawa Y. Sarcopenia is associated with incident albuminuria in patients with type 2 diabetes: a retrospective observational study. J Diabetes Investig 2017; 8:783-7.^,3636. Pechmann LM, Jonasson TH, Canossa VS, Trierweiler H, Kisielewicz G, Petterle RR, et al. Sarcopenia in type 2 diabetes mellitus: a cross-sectional observational study. Int J Endocrinol 2020; 2020:e7841390..

However, contrary to what was initially expected, we found that inadequate glycemic control (HbA1c ≥ 7%) was not associated with any of the response variables in the participants who reported having a diagnosis of T2DM. In addition, the inclusion of HbA1c as a continuous variable in the analysis that had T2DM as the explanatory variable had negligible effects on the magnitude of the associations. Some researchers have shown that poorer glycemic control, assessed with the HbA1c test, increases the long-term risk of muscle complications such as dynapenia and sarcopenia, microvascular complications, and mortality in individuals with T2DM ¹⁶16. Mesinovic J, Zengin A, De Courten B, Ebeling PR, Scott D. Sarcopenia and type 2 diabetes mellitus: a bidirectional relationship. Diabetes Metabol Syndr Obes 2019; 12:1057-72.^,3636. Pechmann LM, Jonasson TH, Canossa VS, Trierweiler H, Kisielewicz G, Petterle RR, et al. Sarcopenia in type 2 diabetes mellitus: a cross-sectional observational study. Int J Endocrinol 2020; 2020:e7841390.^,3737. Laiteerapong N, Ham SA, Gao Y, Moffet HH, Liu JY, Huang ES, et al. The legacy effect in type 2 diabetes: impact of early glycemic control on future complications (The Diabetes & Aging Study). Diabetes Care 2018; 42:416-26.. A cross-sectional study in Japan also demonstrated a dose-response relationship between HbA1c level and the chance of sarcopenia, regardless of anthropometric factors and the duration of diabetes ³⁸38. 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 2019; 10:1471-9.. In the literature, there is debate as to whether poor glycemic control decreases muscle function or worse muscle function primarily affects glycemic control ³⁹39. Morley JE, Anker SD, von Haehling S. Prevalence, incidence, and clinical impact of sarcopenia: facts, numbers, and epidemiology - update 2014. J Cachexia Sarcopenia Muscle 2014; 5:253-9.. The possibility of a bidirectional relationship is a challenging option that longitudinal studies can shed light on.

Multiple mechanisms have been proposed to explain the association of T2DM with dynapenia and sarcopenia, namely: the reduction in muscle synthesis or sensitivity to anabolic hormones such as testosterone; mitochondrial dysfunction caused by chronic hyperglycemia inducing apoptosis and atrophy or loss of muscle fibers; and the increased secretion of inflammatory cytokines (e.g., tumor necrosis factor-α and interleukin-6) decreasing the action of glucose transporters and generating impairment in energy metabolism ⁸8. Santilli V, Bernetti A, Mangone M, Paoloni M. Clinical definition of sarcopenia. Clin Cases Miner Bone Metab 2014; 11:177-80.^,99. Wang T, Feng X, Zhou J, Gong H, Xia S, Wei Q, et al. Type 2 diabetes mellitus is associated with increased risks of sarcopenia and pre-sarcopenia in Chinese elderly. Sci Rep 2016; 6:38937.^,1616. Mesinovic J, Zengin A, De Courten B, Ebeling PR, Scott D. Sarcopenia and type 2 diabetes mellitus: a bidirectional relationship. Diabetes Metabol Syndr Obes 2019; 12:1057-72.^,3030. Mori H, Kuroda A, Matsuhisa M. Clinical impact of sarcopenia and dynapenia on diabetes. Diabetol Int 2019; 10:183-7.^,3131. Zoungas S, Woodward M, Li Q, Cooper ME, Hamet P, Harrap S, et al. Impact of age, age at diagnosis and duration of diabetes on the risk of macrovascular and microvascular complications and death in type 2 diabetes. Diabetologia 2014; 57:2465-74.^,3232. Cui M, Gang X, Wang G, Xiao X, Li Z, Jiang Z, et al. A cross-sectional study: associations between sarcopenia and clinical characteristics of patients with type 2 diabetes. Medicine (Baltimore) 2020; 99:e18708.^,3333. Girach A, Manner D, Porta M. Diabetic microvascular complications: can patients at risk be identified? A review. Int J Clin Pract 2006; 60:1471-83.^,3434. Chung HS, Hwang SY, Choi JH, Lee HJ, Yoo HJ, Seo J-A, et al. Effects of low muscle mass on albuminuria and chronic kidney disease in patients with type 2 diabetes: the Korean Sarcopenic Obesity Study (KSOS). J Gerontol A Biol Sci Med Sci 2018; 73:386-92.^,3535. Bouchi R, Fukuda T, Takeuchi T, Minami I, Yoshimoto T, Ogawa Y. Sarcopenia is associated with incident albuminuria in patients with type 2 diabetes: a retrospective observational study. J Diabetes Investig 2017; 8:783-7.^,4040. 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; 55:1813-8.. Peripheral insulin resistance is one of the main mechanisms leading to diabetes-related impairments in muscle function. It is known that skeletal muscle is responsible for much of the postprandial glucose uptake ⁴⁰40. 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; 55:1813-8. and that insulin acts on muscle function by facilitating and increasing the transport of glucose and amino acid to muscle cells, increasing cellular protein synthesis and storage, as well as glycogen in the muscles and triglycerides in fat cells, stimulating protein synthesis in muscles, and decreasing protein catabolism ³²32. Cui M, Gang X, Wang G, Xiao X, Li Z, Jiang Z, et al. A cross-sectional study: associations between sarcopenia and clinical characteristics of patients with type 2 diabetes. Medicine (Baltimore) 2020; 99:e18708.. Insulin resistance, which is characteristic of T2DM, alters glucose utilization by skeletal muscle, thus negatively affecting protein synthesis, causing proteolytic activity, and consequently leading to the loss of muscle mass and/or strength ³²32. Cui M, Gang X, Wang G, Xiao X, Li Z, Jiang Z, et al. A cross-sectional study: associations between sarcopenia and clinical characteristics of patients with type 2 diabetes. Medicine (Baltimore) 2020; 99:e18708.^,3333. Girach A, Manner D, Porta M. Diabetic microvascular complications: can patients at risk be identified? A review. Int J Clin Pract 2006; 60:1471-83.. Insulin resistance can increase the gene expression of myostatin, an inhibitor of skeletal muscle growth ³²32. Cui M, Gang X, Wang G, Xiao X, Li Z, Jiang Z, et al. A cross-sectional study: associations between sarcopenia and clinical characteristics of patients with type 2 diabetes. Medicine (Baltimore) 2020; 99:e18708.^,3333. Girach A, Manner D, Porta M. Diabetic microvascular complications: can patients at risk be identified? A review. Int J Clin Pract 2006; 60:1471-83.. Nevertheless, the loss of muscle mass and strength leads to decreases in glucose transport, which may worsen insulin resistance - this process results in a negative vicious cycle between insulin resistance and muscle dysfunction ³³33. Girach A, Manner D, Porta M. Diabetic microvascular complications: can patients at risk be identified? A review. Int J Clin Pract 2006; 60:1471-83.. Lastly, fat infiltration in skeletal muscle due to obesity, which happens more commonly in individuals with diabetes than in those without it, aggravates insulin resistance and deteriorates glucose metabolism, consequently compromising muscle function ³⁶36. Pechmann LM, Jonasson TH, Canossa VS, Trierweiler H, Kisielewicz G, Petterle RR, et al. Sarcopenia in type 2 diabetes mellitus: a cross-sectional observational study. Int J Endocrinol 2020; 2020:e7841390..

Even though the dose-response association between the duration of T2DM and increased prevalence of sarcopenia, which was found in this study, suggests a longitudinal association, the cross-sectional design of our analysis hampers any causal evaluation between T2DM and sarcopenia. In addition, a self-reported diagnosis of T2DM, which may be less accurate than objective laboratorial parameters, was one of the criteria used to ascertain the exposure of interest. However, the presence of non-differential misclassifications would contribute to bias the estimated OR towards the null in this study. The cut-off points for dynapenia and LAMM used in this study were validated in older populations of North American and European countries, which means we might have under- or super-estimated the presence of muscle dysfunction in younger populations from different regions of the world, such as ours. Longitudinal studies with outcomes known to be associated with sarcopenia in younger and older Brazilians are needed to validate the proposed EWGSOP2 cut-off points. Furthermore, although BIA is an accepted and accessible method for estimating body composition, it has limitations for assessing skeletal muscle mass, especially in individuals with obesity ³⁷37. Laiteerapong N, Ham SA, Gao Y, Moffet HH, Liu JY, Huang ES, et al. The legacy effect in type 2 diabetes: impact of early glycemic control on future complications (The Diabetes & Aging Study). Diabetes Care 2018; 42:416-26.. The estimation of body composition made by BIA is based on the values of resistance and inductive reactance derived from the electric current generated by the equipment that travels through the body during the analysis ⁴¹41. Yoon JW, Ha Y-C, Kim KM, Moon JH, Choi SH, Lim S, et al. Hyperglycemia is associated with impaired muscle quality in older men with diabetes: the Korean Longitudinal Study on Health and Aging. Diabetes Metab J 2016; 40:140.. However, while body fat is estimated directly by BIA, muscle mass is estimated by prediction equations ⁴²42. Sousa-Santos AR, Amaral TF. Differences in handgrip strength protocols to identify sarcopenia and frailty - a systematic review. BMC Geriatr 2017; 17:238.. Such equations are calibrated based on the lean mass obtained by DEXA in a specific population chosen according to the device used and the population studied ³⁷37. Laiteerapong N, Ham SA, Gao Y, Moffet HH, Liu JY, Huang ES, et al. The legacy effect in type 2 diabetes: impact of early glycemic control on future complications (The Diabetes & Aging Study). Diabetes Care 2018; 42:416-26.^,4343. He Q, Wang X, Yang C, Zhuang X, Yue Y, Jing H, et al. Metabolic and nutritional characteristics in middle-aged and elderly sarcopenia patients with type 2 diabetes. J Diabetes Res 2020; 2020:6973469.^,4444. Buckinx F, Landi F, Cesari M, Fielding RA, Visser M, Engelke K, et al. Pitfalls in the measurement of muscle mass: a need for a reference standard. J Cachexia Sarcopenia Muscle 2018; 9:269-78.^,4545. Kim M, Shinkai S, Murayama H, Mori S. Comparison of segmental multifrequency bioelectrical impedance analysis with dual-energy X-ray absorptiometry for the assessment of body composition in a community-dwelling older population. Geriatr Gerontol Int 2015; 15:1013-22.. Lastly, although HGS is a good indicator of overall muscle strength, it shows a moderate correlation with strength in other body parts ⁷7. 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 2010; 39:412-23.^,4646. Yu S, Powell A, Khow K, Visvanathan R. The performance of five bioelectrical impedance analysis prediction equations against dual X-ray absorptiometry in estimating appendicular skeletal muscle mass in an adult Australian population. Nutrients 2016; 8:189.. A three-year follow-up study with 1,840 subjects aged 70-79 showed that the 50% faster decline in knee extensor strength in older adults with T2DM was not explained by a greater loss of leg muscle mass ⁴⁷47. Fang W-H, Yang J-R, Lin C-Y, Hsiao P-J, Tu M-Y, Chen C-F, et al. Accuracy augmentation of body composition measurement by bioelectrical impedance analyzer in elderly population. Medicine (Baltimore) 2020; 99:e19103.. Nonetheless, in the study, the changes in arm strength and muscle quality did not differ between those with and without diabetes ⁴⁷47. Fang W-H, Yang J-R, Lin C-Y, Hsiao P-J, Tu M-Y, Chen C-F, et al. Accuracy augmentation of body composition measurement by bioelectrical impedance analyzer in elderly population. Medicine (Baltimore) 2020; 99:e19103..

Progress in clinical research shows that the force generated by a muscle is not directly proportional to its size and to the amount of muscle fiber, and that the decline in muscle strength happens at a faster rate than the loss of muscle mass - which corroborates the change in the algorithm proposed by the EWGSOP2 ¹1. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019; 48:16-31.^,4848. Coppini LZ, Waitzberg DL, Campos ACL. Limitations and validation of bioelectrical impedance analysis in morbidly obese patients. Curr Opin Clin Nutr Metab Care 2005; 8:329-32.^,4949. 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 2009; 57:251-9.. Among the strengths of the present work, we highlight the use of EWGSOP2 definitions of sarcopenia and its components, the large sample size, and the inclusion of middle-aged and older adults from three regions of Brazil. In addition, the present analysis considered the influence of numerous potential confounders, and our results remained the same even in sensitivity analyses that excluded comorbidities strongly associated with sarcopenia (e.g., cancer and rheumatic diseases).

It is noteworthy that the presence of dynapenia and sarcopenia in individuals with T2DM is associated with a significant increase in adverse events that negatively impact quality of life ³⁶36. Pechmann LM, Jonasson TH, Canossa VS, Trierweiler H, Kisielewicz G, Petterle RR, et al. Sarcopenia in type 2 diabetes mellitus: a cross-sectional observational study. Int J Endocrinol 2020; 2020:e7841390.^,5050. Ai Y, Xu R, Liu L. The prevalence and risk factors of sarcopenia in patients with type 2 diabetes mellitus: a systematic review and meta-analysis. Diabetol Metab Syndr 2021; 13:93.. This emphasizes the importance of monitoring musculoskeletal functions in individuals with the disease in order to detect early changes. Furthermore, the use of different operational definitions of the components of sarcopenia obscures our understanding of these relationships. In order to promote early diagnosis, it is necessary to standardize and validate the definition and cut-off points of dynapenia and sarcopenia in different and younger populations. The early screening of muscle strength and mass has been identified as an effective strategy for minimizing this deterioration and promoting the maintenance of quality of life. Thus, further research with longitudinal follow-up and evaluation of outcomes associated with muscle dysfunction is important to better understand the relationship between T2DM and sarcopenia and its components, and would allow for the planning of earlier interventions and for the prevention of potential negative outcomes of the disease.

Acknowledgments

ELSA-Brasil is funded by the Brazilian Ministry of Health (Department of Science and Technology) and the Brazilian Ministry of Science and Technology - Brazilian Funding Authority for Studies and Projects (FINEP) and Brazilian National Research Council (CNPq) (Rio Grande do Sul: 01060010.00, Bahia: 01060212.00, Espírito Santo: 01060300.00, Minas Gerais: 01060278.00, São Paulo: 010600115.00, and Rio de Janeiro: 01060071.00). The ELSA-Brasil Musculoskeletal Study receives support from the Brazilian Coordination for the Improvement of Higher Education Personnel (CAPES; SUS 054/2010), Minas Gerais State Research Foundation (FAPEMIG; APQ-00921-16, APQ-00549-22) and CNPq (423585/2016-9 and 404728/2021-9).

References

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