Respiratory Muscle Strength as a Discriminator of Sarcopenia in Community-Dwelling Elderly: A Cross-Sectional Study

Abstract

Objectives

To compare the values obtained from maximum respiratory pressures (MRP) between sarcopenic and non-sarcopenic elderly; to verify the association of maximum respiratory pressures with sarcopenia and its indicators; and to establish cut-off points for MRP as a discriminator of sarcopenia.

Design

Cross-sectional study.

Location

Macapá, Brazil.

Participants

Community-dwelling elderly ≥ 60 years old, both sexes.

Measures

Evaluation of respiratory muscle strength (maximal inspiratory pressure - MIP and maximal expiratory pressure - MEP) and sarcopenia, according to the European Working Group on Sarcopenia in Older People (EWGSOP), in which the diagnosis of this condition considered the reduction of muscle mass (muscle mass index - MMI) associated with muscle strength reduction (hand grip strength - HGS) and / or impairment in physical performance (gait speed - GS).

Results

The sample consisted of 383 elderly individuals, with a mean age of 70.02 ± 7.3 years and a prevalence of sarcopenia of 12.53% (n = 48). Sarcopenic individuals presented significantly lower (obtained, obtained versus predicted) mean values for the maximal respiratory pressures compared to the non-sarcopenic elderly, and these were inversely associated with sarcopenia (an increase by 1 cmH2O in MIP and MEP reduced by 5% and 3%, respectively, the probability of sarcopenia). In relation to the association with the sarcopenia indicators, the increase by 1 cmH2O in MIP and MEP decreased, respectively, the probability of decreasing muscle strength (3% and 2%), GS (3% and 4%) and MMI (3 % - MIP). Cut-off points ≤60 cmH2O and ≤50 cmH2O for MEP and ≤55 cmH2O and ≤45 cmH2O for MEP, respectively for elderly men and women, served as a discriminant criterion for the presence of sarcopenia (area under the ROC curve superior to 0.70).

Conclusions

Elderly patients with sarcopenia had lower MIP and MEP values when compared to non-sarcopenic individuals, and respiratory muscle strength was inversely associated with the diagnosis of sarcopenia and its indicators (HGS, gait speed and MMI). Furthermore, cut-off points for MIP and MEP can be used in clinical practice as discriminators of sarcopenia in community-dwelling elderly.

Introduction

Population aging is a worldwide phenomenon, in which the increase in the elderly population has been expressive and accelerated over the years (1, 2). The consequences of the growth in the contingent of elderly people are many, in view of the greater susceptibility to the emergence of chronic and infectious diseases, which can result in several systemic problems, such as sarcopenia, reduced immunity, increased frailty, impairment of the respiratory system and of sensory and cognitive functions, factors that may generate functional disability in this population (3).

According to the European Working Group on Sarcopenia in Older People (EWGSOP) (4), sarcopenia is defined as progressive and generalized loss of skeletal muscle mass and strength with a risk of adverse outcomes, such as functional capacity impairment, dependence, falls and fractures, negative impact on quality of life, hospitalization and death (4, 5).

Not only the peripheral muscle strength can be affected though, but the respiratory muscles may present performance impairments in the elderly population. It is known that elderly individuals present increased elastic fiber proteolysis (elastin) and increased collagen in the pulmonary parenchyma, as well as increased chest wall stiffness, components that result in a mechanical disadvantage of the respiratory muscles and may cause weakness in the respiratory muscles over time (6).

There is a lack of studies to demonstrate the association between respiratory muscle weakness and sarcopenia in the elderly community-dwelling population. Izawa et al. (7) evaluated the relationship between maximal inspiratory pressure (MIP) and physical function variables assessed by sarcopenia, but in elderly patients with heart disease. MIP presented lower values in the sarcopenia group and also correlated positively with skeletal muscle mass index, hand grip strength and gait speed.

Hence, the objectives in this study were to compare the values obtained for maximal respiratory pressures among community-based sarcopenic and non-sarcopenic individuals; to verify the association of the maximum respiratory pressures with the diagnosis and indicators of sarcopenia; and establish cut-off points for maximal respiratory pressures to predict sarcopenia. The hypotheses for this study were that MIP and MEP values would be lower in sarcopenic individuals when compared to non-sarcopenic ones; and that these respiratory variables would be associated with the diagnosis and indicators of sarcopenia.

Methods

Study design and population

Cross-sectional study involving community-dwelling elderly in urban Macapá in 2017. Macapá (latitude - 0° 2'20» N; longitude - 51° 3' 59» W) is a Brazilian city in the Amazon region, capital of the state of Amapá, Northern Brazil. This is the only Brazilian state that has its capital cut by the imaginary line of the Equator and that is located on the banks of the Amazon river. The estimated population is 456,171 inhabitants, with a Human Development Index (HDI) of 0.733 and a life expectancy at birth of 74.2 years (8). According to data estimated by the Brazilian Institute of Geography and Statistics (IBGE), in the year 2010, the city of Macapá had a population of 20,743 (urban – 19,955 and rural - 788) aged 60 years or older, representing 5.21% of the total population (9).

The sample size calculation considered a prevalence of health problems in 50% of the elderly population, accuracy of 5%, and a 95% confidence interval for a finite population of 19,955 elderly, reaching a minimum required sample of 377 subjects. In order to define the population, a two-stage cluster sampling process was used, considering the census tracts with information from the districts and streets made available by the IBGE, which were drawn for subsequent identification of the elderly in the residences.

Elderly people aged 60 years or older, who lived in the urban area of Macapá, were able to walk and agreed to participate in the study, with the signing of the consent term, were included in this study. The elderly who were not located after three attempts by the interviewer, who had moved away from the city, who were hospitalized and/or suffered neurological sequelae and/or conditions that made evaluations impossible, were excluded. In addition, the study excluded elderly individuals who presented a cognitive decline that would make them unable to answer the interview questions and the tests, as identified through the Mini Mental State Examination (MMSE), in the version translated and validated in Brazil, which considers cut-off points according to educational level (10). Thus, a total of 383 elderly (Figure 1), of both genders, 60 years of age or older, participated in this study. This study received approval from the Research Ethics Committee of the Federal University of Amapá, opinion 1.738.671.

Figure 1.

Flow diagram representing the loss of the sample and final sample composition

Respiratory muscle strength (independent variable)

To assess the respiratory muscle strength, manovacuometry was used to obtain the maximal respiratory pressures, MIP and MEP, which reflect inspiratory and expiratory muscle strength, respectively. For these measures, the manovacuometer was used with scales from -150 to +150 cmH2O (duly calibrated), equipped with a plastic trachea, rigid plastic nozzle and leak hole (2mm diameter) to prevent pressure increase in the cavity oral due to contraction of the facial and oropharyngeal muscles (11).

The measures were taken in the seated position using the nasal clip. MIP was obtained by one maximal inspiration preceded by maximal expiration close to the residual volume (RV). For MEP, one maximal inspiration was performed close to total lung capacity (TLC) followed by maximal expiration (11). At least three and at most five maneuvers were performed, three of which were acceptible (sustain maneuver for at least one second) and two reproducible maneuvers (variation equal to or less than 10% of the highest value). The highest value obtained was considered for the analyses (12, 13, 14).

RSarcopenia (dependent variable)

Sarcopenia was defined based on the algorithm recommended by the European Working Group on Sarcopenia in Older People (EWGSOP) and the diagnosis considered the reduction of muscle mass associated with reduction of muscle strength and / or impairment in physical performance.

The muscle mass component was measured based on the total muscle mass (TMM) estimated by the equation proposed by Lee et al. (15), validated for use in Brazilian elderly (16) and used in previous population-based studies (17, 18):

MMT (kg) = (0.244 x body weight) + (7.8 x height) - (0.098 x age) + (6.6 x sex) + (ethnicity - 3.3)

The equation considers the parameters body mass, height, sex, age and race. For the sex variable, 0 = women and 1 = men; for ethnicity, 0 = white and indigenous, -1.2 = yellow and 1.4 = black and brown were adopted.

Based on the TMM, the muscle mass index (MMI = TMM / height2) was calculated. The cut-off point for muscle mass index (MMI) in the present study considered the 20th percentile of the sample studied, according to previous studies (19, 20) and represented values <9.61 kg/m2 for men and <6.92 kg/m2 for women.

To determine the muscle strength, hand grip strength (HGS) was evaluated using the SAEHAN® Hydraulic Hand Dynamometer model SH5001. The test procedure followed the recommendations of the American Society of Hand Therapists (21). Three measures were obtained at one-minute intervals and the mean value of the measures was considered. Values lower than 30 kilograms / force (Kgf) for men and 20kgf for women were considered as reduced muscle strength (22).

Physical performance was assessed by means of the gait speed test, an integral part of the Short Physical Performance Battery - SPPB (time to walk 4 meters) (23, 24) according to EWGSOP recommendations (4). Values inferior than or equal to 0.8 m/s were considered as impaired physical performance (4).

Adjustment variables

The variables age, sex, number of diseases and medications were measured using a structured instrument, based on the Older Americans Resources and Services (OARS) questionnaire, developed by Duke University (1978), and adapted to the Brazilian reality (25), being called the Brazilian Functional and Multidimensional Evaluation Questionnaire (BOMFAQ). The elderly were asked about the consumption and time (in years) of tobacco (yes/no). The level of physical activity was measured based on the long version of the International Physical Activity Questionnaire (IPAQ), adapted for the elderly by Benedetti et al. (26) and considered elderly subject as active enough if they spent 150 minutes or more of weekly physical activity at vigorous and moderate intensity; and as inactive if they spent from 0 to 149 minutes of weekly physical activity at vigorous and moderate intensity.

Statistical analysis

Descriptive analysis was performed using means, standard deviations, absolute numbers and percentages. To compare the obtained, obtained vs. predicted values between sarcopenic, non-sarcopenic and total sample, Student's t-test and paired t-test were used and the chi-square test for categorical variables. To verify the association between the maximal respiratory pressures (independent variable) and sarcopenia and sarcopenia indicators (dependent variable), we performed the crude and adjusted analyses using the logistic regression model with the odds ratio estimates, considering a level of significance of 5% (p <0.05) and 95% confidence interval (CI). The Hosmer and Lemeshow test was used to analyze the degree of fit of the models (p> 0.05). The data were analyzed in the program Statistical Package for Social Sciences (SPSS) version 21.0.

To determine the cut-off points of the maximal respiratory pressures as discriminators of sarcopenia, the Receiver Operating Characteristic (ROC) curves were constructed, with the area parameters under the ROC curve (AUC), sensitivity and specificity using MedCalc 11.4.4., a 95% CI and 5% significance level (p<0.05).

Results

The final sample consisted of 383 elderly individuals, according to the inclusion and exclusion criteria. The sample loss is described in Figure 1. The mean age of the evaluated elderly was 70.02 ± 7.3 years, 132 males (34.5%) and 251 females (65.5%). The prevalence of sarcopenia was 12.53% (n = 48). Sarcopenic elderly individuals had lower mean values for age, anthropometric variables, MMI, muscle strength and gait speed when compared to non-sarcopenic individuals (Table 1).

Table 1.

Characteristics of elderly according to sarcopenia. Macapá, AP, Brazil, 2017 (n=383)

Variables	Sarcopenic	Non-sarcopenic	P-value	Total sample
	(n=48)	(n=335)		(n=383)
Age (in years)	77.31±7.95	68.9±6.58	<0.001	70.02±7.3
Sex
Male	14 (29.2)	118 (35.2)	0.409*	132 (34.5)
Female	34 (70.8)	217 (64.8)		251 (65.5)
Height (m)	1.51±0.86	1.54±0.08	0.006	1.54±0.09
Weight (Kg)	50.69±7.66	68.99±12.34	<0.001	66.7±13.31
BMI (kg/m2)	22.23±2.31	28.90±4.65	<0.001	28.07±4.94
MMI (kg/m2)	6.99±1.42	9.19±1.63	<0.001	8.92±1.76
HGS (Kgf)	18.84±5.26	25.48±9.17	<0.001	24.65±9.05
Gait speed (0.8 m/s)	0.79±0.30	1.03±0.29	<0.001	0.98±0.31
Number of illnesses	5.5±0.86	5.34±2.93	0.725	5.36±2.86
Number of drugs	1.71±1.66	1.63±1.77	0.787	1.64±1.76
Smoking
Yes	5 (10.4)	28 (8.4)	0.586*	33 (8.6)
No	43 (89.6)	307 (91.6)		350 (91.4)
Physical activity
Sufficiently active	20 (41.7)	185 (55.2)	0.078*	205 (53.5)
Insufficiently active	28 (58.3)	150 (44.8)		178 (46.5)

The data are expressed as n: number of subjects; mean±standard deviation; m: meters; Kg: kilogram; BMI: body mass index; MMI: muscle mass index; HGS: hand grip strength; Kgf: kilogram-force; *χ2 test; † t-test.

Elderly sarcopenic individuals had significantly lower (obtained, obtained vs. predicted) values for maximal respiratory pressures compared to non-sarcopenic patients. The comparison also indicated differences (values obtained vs. predicted) for the non-sarcopenic elderly group and total sample for the maximal respiratory pressures (Table 2).

Table 2.

Association of obtained, obtained vs. predicted values of maximal respiratory pressures between elderly with and without sarcopenia and total sample. Macapá, AP, Brazil, 2017 (n=383)

Maximal Respiratory	Sarcopenic	Non-sarcopenic	Total sample
Pressures	(n=48)	(n=335)	(n=383)
MIP (cmH2O) obtained	40.10±19.28	61.27±25.23	58.61±25.53
p<0.001*
MIP (cmH2O) predicted	78.64±10.78	84.92±12.11	84.13±12.12
	p<0.001	p<0.001	p<0.001
MEP (cmH2O) obtained	53.75±18.61	73.39±28.98	70.92±28.63
p<0.001*
MEP (cmH2O) predicted	78.44±16.71	86.19±17.93	85.22±17.94
	p<0.001	p<0.001	p<0.001

The data are expressed as n: number of subjects; mean±standard deviation; MIP: maximal inspiratory pressure; MEP: maximal expiratory pressure; p<0.05; * t-test; † paired t-test.

The adjusted analysis of the logistic regression model showed that the maximal respiratory pressures were inversely related with sarcopenia, indicating that a 1 cmH2O increase in MIP and MEP reduces the probability of sarcopenia in the elderly by 5% and 3%, respectively (Table 3).

Table 3.

Association between maximal respiratory pressures and sarcopenia in the elderly. Macapá, AP, Brazil, 2017 (n=383)

MaximalRespiratory Pressures	Sarcopenia
	Gross Analysis		Adjusted Analysis
	OR	95% CI	p*	OR	95% CI	p*
MIP (cmH2O)	0.95	0.93-0.97	<0.001	0.95	0.93-0.98	<0.001
MEP (cmH2O)	0.96	0.94-0.98	<0.001	0.97	0.95-0.99	0.004

CI: Confidence Interval; OR: Odds Ratio; MIP: maximal inspiratory pressure; MEP: maximal expiratory pressure; *p<0.05; Adjusted for age, sex, number of drugs and illnesses, smoking and physical activity level; Hosmer–Lemeshow test (p>0.05).

The adjusted analysis of the logistic regression model showed that maximal respiratory pressures were inversely associated with the indicators muscle strength and gait speed; while muscle mass was associated only with MIP. The results indicate that a 1 cmH2O increase in MIP and MEP reduces, respectively, the probability of decreasing muscle strength (3% and 2%), gait speed (3% and 4%) and muscle mass (3% - MIP) among the elderly (Table 4).

Table 4.

Association of maximal respiratory pressures with sarcopenia indicators in the elderly. Macapá, AP, Brazil, 2017 (n=383)

Maximal Respiratory Pressures	Sarcopenia indicators
	OR	Muscle mass 95%CI	p*	OR	Muscle strength95%CI	p*	OR	Gait speed95%CI	p*
MIP (cmH2O)
Not adjusted	0.97	0.96-0.98	<0.001	0.97	0.96-0.98	<0.001	0.96	0.95-0.97	<0.001
Adjusted	0.97	0.96-0.99	0.003	0.97	0.96-0.98	<0.001	0.97	0.96-0.98	<0.001
MEP (cmH2O)
Not adjusted	0.98	0.97-0.99	0.007	0.98	0.97-0.98	<0.001	0.93	0.95-0.97	<0.001
Adjusted	0.99	0.98-1.00	0.156	0.98	0.97-0.99	0.001	0.96	0.95-0.98	<0.001

CI: Confidence Interval; OR: Odds Ratio; MIP: maximal inspiratory pressure; MEP: maximal expiratory pressure; *p<0.05; Adjusted for age, sex, number of drugs and illnesses, smoking and physical activity level; Hosmer–Lemeshow test (p>0.05).

The results of the area under the ROC curve indicated coefficients superior to 0.70, representing moderate accuracy (Figure 1). Cut-off points ≤60 cmH2O and ≤50 cmH2O for MEP and ≤55 cmH2O and ≤45 cmH2O for MIP, respectively for elderly men and women, constituted a discriminant criterion for the presence of sarcopenia (Figure 2).

Figure 2.

Areas under the ROC curve for maximal respiratory pressures as discriminators for the presence of sarcopenia among elderly men (A) and women (B). Macapá, AP, Brazil, 2017 (n=383). AUC: area under the ROC curve; CI: confidence interval; MEP: Maximal expiratory pressures; MIP: Maximal inspiratory pressures

Discussion

These study results showed the association between respiratory muscle strength and sarcopenia, because MIP and MEP were associated with the diagnosis of sarcopenia and its respective indicators.

In individuals with sarcopenia, both inspiratory (MIP) and expiratory (MEP) muscle strength were lower when compared to non-sarcopenic elderly. The inspiratory muscle weakness in this population may occur as a consequence of the changes in the chest wall compliance, which is reduced and becomes more rigid as a result of the decrease in the number of chondrocytes, thickening of the collagen fibers and greater calcium deposits in the synovial joints between the sternum and costal cartilages. In addition to this condition, there is a loss of the intrinsic elastic recoil of the pulmonary parenchyma, which causes an increase in residual volume and functional residual capacity, resulting in pulmonary hyperinflation. Reduction of chest compliance and pulmonary hyperinflation alter respiratory mechanics, which leaves the diaphragm flatter and at a disadvantage in generating strength while contracting (6, 27, 28).

Additionally, researchers have argued that the diaphragm muscle may also present sarcopenia. Greising et al. (29) identified the occurrence of reduced diaphragmatic muscle strength and mass in an experiment with rats, components that characterize sarcopenia and which, according to these authors, confirm the presence of diaphragmatic sarcopenia. In the same study, a 27% reduction in the cross-sectional area (AST) of type IIx and/or IIb diaphragmatic fibers was identified in older mice compared to young mice.

In 2015, the same group of investigators (30) developed a study involving a group of 79 male and female mice, aged six (young mice) and 24 months (elderly mice) (100% and 70-75% survival, respectively). They examined the transdiaphragmatic pressure (Pdi) generated during motor behavior in the specific strength of the diaphragm. Among the main findings, a significant effect of age on maximal Pdi (20-41% reduction) and generation of specific strength of the diaphragm muscle (30% decline) was identified, which demonstrates the occurrence of diaphragmatic sarcopenia, as suggested by the authors.

In addition, in this study, we also demonstrated the reduction of expiratory muscle strength in sarcopenic elderly patients, which shows that they may present damage of the bronchial hygiene mechanism (31), as in coughing, for example, and increases the risk of developing respiratory diseases with high incidence, morbidity and mortality rates in the elderly, such as pneumonia (32).

Shin et al. (33) verified the relation between inspiratory (MIP) and expiratory (MEP) muscle strength and the sarcopenia indicators (skeletal muscle mass index, HGS, gait speed and SPPB) among 65 elderly (30 males and 35 females) with a mean age of 69.90 ± 7.63 years. Both MIP and MEP were positively correlated with skeletal muscle mass index and HGS, and only MEP was correlated with SPPB, results that demonstrate the existing relationship between respiratory muscle strength and the indicators of sarcopenia.

Likewise, our results showed that both MIP and MEP, even after adjustment, were associated with the sarcopenia diagnosis and with the gait indicators, HGS and muscle mass index (MMI), except MEP in relation to MMI, in which this relationship was not maintained.

These findings may indicate that respiratory muscle strength interferes further in the physical performance (HGS and gait speed) of the elderly. As previously mentioned, due to the changes that may affect the respiratory system of the elderly, the muscles responsible for breathing, especially the diaphragm, will present a mechanical disadvantage, resulting in increased respiratory work and early symptoms of dyspnea and fatigue in case of physical exertion. In this sense, elderly individuals with inspiratory muscle weakness will be less able to tolerate certain physical exercises because activities will be limited by symptoms that may occur early, which may result in sedentary behavior and promote physical deconditioning and sarcopenia (34, 35).

The fact that only MIP is associated with MMI may have occurred because the diaphragm muscle may be more influenced by muscle mass as a consequence of diaphragmatic sarcopenia, as researchers have demonstrated in their studies (29, 36). And these changes in diaphragmatic muscle mass impact the contraction capacity of this muscle, which can result in muscle weakness (reduction of MIP). According to scientific literature findings, in case of diaphragmatic sarcopenia, denervation of the phrenic nerve may occur, which results in atrophy and reduction in the more pronounced specific strength of diaphragmatic type IIx and/or IIb muscle fibers. Even so, the mechanisms involved in the process of diaphragmatic sarcopenia still require further investigation (36).

In the study by Izawa et al. (7), the relationship between MIP and physical function variables in sarcopenic individuals was evaluated; and the differences and cut-off values for MIP were determined according to the sarcopenia diagnosis in elderly patients with heart disease. MIP presented lower values in the sarcopenia group and also correlated positively with MMI, HGS and gait speed. The cut-off point for MIP as a discriminator of sarcopenia was 55.6 cmH2O, with 0.76 sensitivity, 0.37 specificity and area under the curve of 0.70.

These results support the present study results, in which the MIP cut-off points to discriminate sarcopenia were ≤55 cmH2O and ≤45 cmH2O, respectively, for elderly men and women. Furthermore, a cut-off point for MEP as a sarcopenia discriminator was established as ≤60 cmH2O for men and ≤50 cmH2O for women, values that could contribute as screening markers for the identification and diagnosis of sarcopenia.

Some limitations of our study should be considered. The maximum respiratory pressure values may have been lower because the sample was mostly female, although this fact was minimized by the adjustment of the analysis by sex. The use of Lee's equation offers an estimated calculation, but the method is easy to apply and does not require expensive equipment, is validated and widely used. The schedule and the environment in which the measures were collected were not controlled. As the participants were community-dwelling elderly, the evaluations were carried out at the elderly's homes in accordance with their availability, being executed in a way that promoted greater comfort and offered less risk to the elderly. Finally, the causal relationship between respiratory muscle strength and sarcopenia still needs to be better clarified, because the cross-sectional design of this study is also a limiting factor.

On the other hand, our study presents a representative sample of the community-dwelling elderly population in a city in the Amazon region. Based on our findings, it could be demonstrated that respiratory muscle strength is a relevant component in the clinical evaluation of the elderly, due to its association with sarcopenia. Furthermore, our study presents cut-off points for MIP and MEP as discriminators of sarcopenia, measures that are easily accessible and performed in clinical practice and that may be useful in providing additional information about the health condition of the elderly population.

Conclusion

Elderly patients with sarcopenia presented inspiratory and expiratory muscle weakness when compared to non-sarcopenic individuals, and respiratory muscle strength was inversely associated with the diagnosis of sarcopenia and its indicators (HGS, gait speed and MMI). Finally, cut-off points ≤55 cmH2O and ≤45 cmH2O for MIP and ≤60 cmH2O and ≤50 cmH2O for MEP were determined in men and women, respectively, as sarcopenia discriminators in community-dwelling elderly.

Ethicals declaration

This study received approval from the Research Ethics Committee of the Federal University of Amapá, number 1.738.671.

Conflict of interest disclosure

There was no conflict of interest. This research was financed by the Foundation for Research Support of the State of Amapá (FAPEAP, Concession nº 250.203.029/2016).