Association of insufficient physical activity with sarcopenia and sarcopenic obesity in individuals aged 50 years or more

Objective To analyze the association of insufficient physical activity in different domains with sarcopenia or sarcopenic obesity in patients aged ≥50 years. Methods The sample consisted of 770 males and females. Sarcopenia was diagnosed when the individual had: (1) low muscle mass and muscle strength; or (2) low walking speed and low muscle mass; sarcopenic obesity was diagnosed when individuals were at risk of obesity and sarcopenia. Muscle mass was given by a predictive equation, and then the muscle mass index (in kg/m2) was given by muscle mass divided by height squared. 176 | VR SANTOS et al. Rev. Nutr., Campinas, 30(2):175-184, mar./abr., 2017 Revista de Nutrição https://doi.org/10.1590/1678-98652017000200003 Muscle strength, in kg, was given by measuring handgrip strength with a digital dynamometer. The 4m walk test evaluated walking sped. Low muscle mass, muscle strength, and walking speed were defined as the respective values below the 25th percentile, and risk of obesity was defined as body mass index ≥25kg/m2. Results Habitual physical activity was investigated by a questionnaire. Insufficient leisure-time physical activity was associated with sarcopenia (OR=2.55; 95%CI=1.10–5.88). In addition, insufficient leisure-time physical activity (OR=4.75; 95%CI=1.64–13.72), leisure-time and commuting physical activities (OR=2.49; 95%CI=1.02–6.11, and habitual physical activity (OR=3.55; 95%CI=1.0–11.79) were associated with sarcopenic obesity. Conclusion Insufficient physical activity is associated with sarcopenia or sarcopenic obesity in the study individuals aged ≥50years.


I N T R O D U C T I O N
Low muscle mass associated with low muscle strength or poor motor performance is defined as sarcopenia [1], and when it is associated with excess body fat, it is called sarcopenic obesity [2].Sarcopenia and sarcopenic obesity may reduce functional capacity, hindering the ability of older adults to perform Activities of Daily Living (ADL).Moreover, they are risk factors for cardiometabolic diseases [3,4], falls [5], frailty [6], and death [7,8].
Regular physical activity helps to maintain or even increase muscle mass and strength [9,10], and reduce body fat [9] and consequently, improve motor performance [11].In this sense, physical activity may contribute to the prevention and treatment of sarcopenia and sacorpenic obesity in older adults [12].
Recently, some studies have reported associations of insufficient physical activity with sarcopenia and sarcopenic obesity in older adults [13][14][15][16], but these studies did not investigate physical activity by domain and the relationship of said domains with sarcopenia and sarcopenic obesity, which would allow the adoption of preventive health measures, such as a knowingly beneficial physical activity of a specific domain.These aspects should be investigated in older adults, as their population is increasing rapidly and growing age reduces the level of physical activity and increases the risk of chronic diseases.Hence, the objective of this study was to analyze whether insufficient physical activity is associated with sarcopenia or sarcopenic obesity in individuals aged 50 years or more.

M E T H O D S
This cross-sectional study used the data obtained in the initial assessment of two distinct cohorts with similar characteristics (study variables, measurement instruments, and researchers).The first study, conducted from September 2013 to September 2015, aimed to investigate the association of physical activity with outpatient, secondary, and tertiary expenditures with the Unified Healthcare System (SUS) patients from Presidente Prudente (SP), a city located in the Southeast region of Brazil.The study included individuals aged 50 years or more registered and treated at two Primary Healthcare Units (PHU) referred by the Municipal Department of Health.The patients were invited to participate and assessed while they waited for their appointment or after the appointment.The assessments were performed in the morning in September and October of 2013, and the researchers remained in the PHUs during this period to invite all patients who met the inclusion criteria.Thus, 476 individuals aged 50 to 88 years were assessed.Body weight was measured by the electronic scale Filizola ® Antropométrica (São Paulo, SP, Brazil), with maximum capacity of 180kg and accuracy of 0.1kg, and height, by the wall-mounted stadiometer Sanny ® , Standard model (São Bernardo do Campo, SP, Brazil), with length of 2.20m and graduation of 0.1cm.The measurements were performed as recommended by Freitas Jr et al. [17].The Body Mass Index (BMI) was then calculated by dividing the body weight by the square of the height (kg/m 2 ).
The equation has been validated for the Brazilian population and presented high correlation with Dual-Energy X-Ray Absorptiometry (Dexa), (r=0.86 for men and r=0.90 for women, respectively, p<0.05).Agreement between Dexa and the predictive equation to find individuals with low muscle mass is strong (k=0.74;p<0.001) and has high specificity (89%) and sensitivity (86%) [20].
Later, the muscle mass index was calculated by dividing the muscle mass in kg by the square of the height in meters (kg/m²).
Muscle strength was estimated in kg by measuring the handgrip strength with a digital dynamometer of the brand Camry, model EH101 (Guangdong, China).The test was conducted twice while the individuals sat on an armless chair, shoulders adducted, and elbow of the dominant arm flexed 90º, with the forearm and wrist in neutral position.The older adults were instructed to press the dynamometer as hard as they could twice, at a one-minute interval.The highest value was recorded.
Walking speed was determined by the 4-meter walk test [21].The older adults were asked to walk naturally, as they were walking at home, and the highest speed (m/s) of two walks was recorded.
Low muscle mass, muscle strength, and walking speed were defined as those below the 25th percentile for each variable by gender (men=9.66kg/m 2 , 29.50kg, and 0.86m/s; women: 8.14kg/m 2 , 18.00kg, and 0.81m/s, respectively).Sarcopenia was diagnosed using the criteria recommended by Cruz-Jentoft et al. [1], namely (1) low muscle mass and muscle strength; or (2) low muscle mass and walking speed.
Individuals were considered at risk of obesity when they BMI ≥25kg/m 2 [22].Individuals with the two conditions (obesity and sarcopenia) were diagnosed with sarcopenic obesity [2].
Information related to Habitual Physical Activity (HPA) was collected by interview using the questionnaire developed by Baecke et al. [23].This instrument has been validated for Brazilians aged 50 years or more by Florindo et al. [24].
The instrument consists of 16 questions and investigates the level of HPA in three domains: occupational (type of occupation and activities performed during work); leisure-time physical activity (practice of regular physical exercises); and leisure-time and commuting activities (watch TV, walk, or bike during leisure time or when commuting).
The level of physical activity in each domain was calculated and the sum of the scores of each domain provide the HPA score.HPA was classified by the formula proposed by Baecke et al. [23].The level of physical activity of the sample was divided into quartiles for the three study domains: (1) occupational; (2) leisure-time physical activity; (3) leisure-time and commuting physical activity; and 4) total score (HPA).Individuals in the fourth quartile of each domain [occupational (3.00); leisure-time physical activity (2.50); leisure-time and commuting physical activity (2.50)] and HPA (7.37) were considered sufficiently active.Those in the first, second, and third quartiles of each domain were classified as insufficiently active.
Descriptive statistics was expressed as relative frequency.The association of the percentages of each variable with the presence or absence of sarcopenia or sarcopenic obesity was investigated by the Chi-square test.This same test also verified the association of the scores in the different physical activity domains with sarcopenia and sarcopenic obesity.All variables with p<0.20 in the Chi-square test were selected https://doi.org/10.1590/1678-98652017000200003for the forward stepwise binary multiple logistic regression models.The data were treated by the statistical software Statistical Package for the Social Sciences (SPSS Inc, Chicago, Illinois, United Srates), version 17.0, and the level of significance was established at 5%.This study used a confidence interval of 95%.
Table 1 shows the prevalence of sarcopenia and sarccopenic obsity for the total sample and by gender, and in each gender, by level of physical activity.The prevalences of sarcopenia and sarcopenic obesity did not differ significantly by gender.
The prevalences of both conditions was lower in sufficiently physically active women, especially sarcopenia (p<0.05).
Table 2 shows the general characteristics of the sample according to the presence of the two study conditions.Most individuals with sarcopenia were aged 70 years or more, had lower income, higher prevalence of hypertension (p<0.05), and low muscle mass and walking speed (p≤0.001).Most individuals with sarcopenic obesity were also aged 70 years or more, lower income, low muscle strength and walking speed (p≤0.001), and a higher prevalence of osteoporosis (p<0.05).
Figure 1 shows the percentage of physically active individuals in each of the study domains and HPA by gender.The percentage of women who were occupationally active was higher than that of men (p≤0.001).On the other hand, the percentage of physically active men during leisure time or commuting was higher than that of women (p≤0.001).Leisure-time physical activity and HPA did not differ by gender.
Table 3 shows the association of level of physical activity with sarcopenia and sarcopenic obesity.Insufficient leisure-time physical activity was associated with sarcopenia and sarcopenic obesity, and insufficient physical activity while commuting and in the sum of all physical activity domains was associated with sarcopenic obsity.
Table 4 shows the multiple logistic regression models of the association of physical activity with sarcopenia and sarcopenic obesity.Insufficient leisure-time physical activity was

D I S C U S S I O N
The main findings of this study was that after assessing the level of physical activity in different domains (occupational, leisure-time, and commuting) and globally, insufficient physical prevalences of sarcopenia.Moreover, the prevalences of sarcopenic obesity in males and females were similar, also differing from other reports [27,28], which found a higher prevalence of sarcopenic obesity in women.In fact, the prevalences and intergender differences may vary according to diagnostic criteria and cut-off points.
Sufficiently active women had lower prevalences of sarcopenia and sarcopenic obesity (p<0.05).Ryu et al. [16] also found an inverse activity, especially during leisure time, is associated with sarcopenia or sarcopenic obesity.
The prevalence of sarcopenia in the study sample was similar for males and females, but it differed from the prevalences reported by other studies, which found differences by gender, with higher prevalences in men [25,26].The prevalence of sarcopenic obesity was similar to that of sarcopenia, contrary to what has been reported by other studies [3,16], which found higher Rev. Nutr., Campinas, 30(2):175-184, mar./abr., 2017 Revista de Nutrição https://doi.org/10.1590/1678-98652017000200003association between level of physical activity and sarcopenic obesity, not between level of physical activity and sarcopenia in women.Unlike Ryu et al. [16], the present study did not find an association between insufficient physical activity and sarcopenia in men.It was also not possible to investigate whether insufficient physical activity was associated with sarcopenie obesity because none of the sufficiently active men had sarcopenic obesity.
Women perform more household chores confirmed by the present study, and men are more active in other domains.Men also tend to get more involved in sports [29][30][31].The study men were significantly more active in the domain 'leisure time and commuting, Nevertheless, neither leisure-time physical activity nor HPA differed by gender.Intergender differences may vary according to the characteristics of the sample (income, education level, and access to areas appropriate for physical activities) [29].
Insufficient leisure-time physical activity was associated with sarcopenia in the study sample.One of the possible explanations is the fact that leisure-time physical activities are related to sports, supervised training in gyms, and anaerobic exercises, which more effectively prevent and treat sarcopenia [12].Such observation reinforces the importance of also investigating whether the sarcopenia is associated with physical activity in different domains.Thus, the study findings may complement the results of other studies [13][14][15][16] that did not investigate this association.
Physical activity may minimize the effects of muscle apoptosis, which reduces the number and size of muscle fibers [12,32], and helps the musculoskeletal function, improving motor function [11], ability to carry out activities of daily living, and consequently, the quality of life of older adults [33].
Insufficient physical activity was associated with sarcopenic obsity in two domains, leisuretime physical activity and leisure-time physical activity & commuting, and in the total score, which represents the total habitual physical activity.Similar results were found by Ryu et al. [16] in older South Koreans of both genders.Regular physical activity, especially aerobic activity, reduces body fat, which inhibits the synthesis of pro-inflammatory cytokines, such as Tumor Necrosis Factor-α (TNF-α) and Interleukin 6 (IL-6), which may decrease physical functioning because of their catabolic effect on muscles as these substances increase myofibrillar protein degradation and reduce protein synthesis [32].
Muscle also has endocrine function and produces cytokines, like IL-6, during physical activity.These substances are called myokines and may influence metabolism in other organs and tissues, but in this case they have antiinflammatory action [34].This evidence reinforces the importance of physical activity for the prevention of sarcopenia and sacopenie obesity.
The study limitations include the sample, which is not representative of the population, so the results should not be generalized, the study cross-sectional design does not allow the establishment of a cause and effect relationship, the use of BMI and the cut-off point of 25kg/m 2 to diagnose obesity, and the use of percentilebased cut-off points to classify muscle mass, muscle strength, and walking speed status.However, the literature has a gab regarding studies that aimed to verify these aspects in the Brazilian population.Another factor would be the subjective analysis of physical activity, but the use of more accurate instruments for measuring physical activity, such as accelerometer, is difficult in epidemiological studies.The study strengths include the assessment of people treated by primary healthcare units and the search for information that will allow an assiduous development of strategies to enable the primary prevention of sarcopenia, epidemiological investigation of sarcopenic obesity, and the association between sarcopenic obesity and different physical activity domains.https://doi.org/10.1590/1678-98652017000200003 In conclusion, insufficient physical activity was associated with sarcopenia and sarcopenic obesity in the study sample of individuals aged 50 years or more.Preventive measures, such as lifelong practice of physical activity, may contribute to the maintenance of muscle mass and strength, and to reduce the occurrence of sarcopenia and sarcopenic obesity in older adults.

C O N T R I B U T O R S
VR SANTOS obtained the subjects and data, analyzed and interpreted the results, and prepared, wrote, and reviewed the manuscript.MYC ARAUJO, MR CARDOSO, VC BATISTA and DGD CHRISTOFARO, LA GOBBO conceived and designed the study, obtained the subjects and data, analyzed and interpreted the data, and prepared and reviewed the manuscript.

Table 1 .
Prevalence of the study conditions by gender and Habitual Physical Activity.

Table 2 .
General characteristics of the study sample by the presence of the study conditions.
Figure 1.Percentage of physically active individuals according to physical activity domains and gender.Note: HPA: Habitual Physical Activity.

Table 3 .
Association of physical activity with sarcopenia and sarcopenic obesity in individuals aged 50 years or more.

Table 4 .
Multiple regression models for the association of physical activity in each domain and total score with sarcopenia and sarcopenic obesity in individuals aged 50 years or more.