Endurance muscular inspiratória em indivíduos obesos e eutróficos Inspiratory muscle endurance in obese and eutrophic individuals La resistencia muscular inspiratoria en individuos obesos y eutróficos

Endereço para correspondência: Carine Cristina Callegaro – Centro de Ciências da Saúde – Avenida Roraima, 1000, Cidade Universitária, Camobi – Santa Maria (RS), Brasil – CEP: 97105-900 – E-mail: ccallegaro84@gmail.com – Fonte de financiamento: Nada a declarar – Conflito de interesses: Nada a declarar – Apresentação: 25 fev. 2018 – Aceito para publicação: 27 jun. 2018 – Aprovado pelo Comitê de Ética da Universidade de Cruz Alta sob o parecer no 51573315.7.0000.5322. Laboratório de Fisiologia da Universidade de Cruz Alta (Unicruz) – Cruz Alta (RS), Brasil. 1 Programa de Pós-Graduação em Atenção Integral à Saúde pela Universidade de Cruz Alta (Unicruz) em rede com a Universidade Regional do Noroeste do Estado do Rio Grande Do Sul (Unijuí) – Cruz Alta (RS), Brasil. 2 Laboratório de Fisiologia da Universidade de Cruz Alta (Unicruz) – Cruz Alta (RS), Brasil. 3 Departamento de Fisioterapia e Reabilitação e Programa de Pós-Graduação em Reabilitação Funcional da Universidade Federal de Santa Maria (UFSM) – Santa Maria (RS), Brasil. 4 Universidade de Cruz Alta (Unicruz) – Cruz Alta (RS), Brasil. 5 Departamento de Fisioterapia e Reabilitação, Laboratório de Fisiologia e Reabilitação, Universidade Federal de Santa Maria (UFSM) – Santa Maria (RS), Brasil. Endurance muscular inspiratória em indivíduos obesos e eutróficos Inspiratory muscle endurance in obese and eutrophic individuals La resistencia muscular inspiratoria en individuos obesos y eutróficos Aline Dors Hoffmeister1, Katieli Santos de Lima2, Isabella Martins de Albuquerque3, Valderesa Binotto4, Carine Cristina Callegaro5


INTRODUCTION
Obesity may be related to reduced inspiratory muscle strength, leading to increased inspiratory effort, oxygen consumption, and energy expenditure 1 , which may contribute to high rates of diaphragmatic fatigue 2 .However, studies on respiratory muscle strength (RMS) of morbidly obese individuals have presented conflicting results 3 .A research indicated that excess body weight does not change the respiratory muscle mechanics 4 , while another described that no association exists between RMS and body mass index (BMI) 5 .In addition, the inspiratory and expiratory muscle strength of obese individuals was within the bounds of normality when compared to eutrophic individuals 5 .On the other hand, two studies indicate an increase of RMS in morbidly obese individuals 6,7 .
In addition to the lack of consensus about the influence of obesity on RMS, apparently, inspiratory muscle endurance has not yet been investigated in obese individuals.There is only one study, recently published, which showed a significant association between body weight and inspiratory muscle endurance, assessed by inspiratory resistance exercises in eutrophic children and adolescents 8 .
In healthy individuals, the inspiratory resistance exercise increases blood pressure and heart rate [9][10][11] .These hemodynamic responses to the inspiratory resistance exercise may vary according to clinical conditions, such as chronic heart failure (CHF) 12,13 and diabetes mellitus 14 .
The effects of obesity on inspiratory muscle endurance and hemodynamic responses to the inspiratory resistance exercise have not yet been studied in obese individuals.From the hypothesis that inspiratory muscle endurance and hemodynamic responses are altered in obese individuals, the objective of this research was to compare the reaction of obese and eutrophic individuals to inspiratory resistance exercises.

METHODOLOGY
This is a cross-sectional study, with a convenience sample composed of obese (n=20) and eutrophic (n=20) individuals recruited by disclosure of the inclusion and exclusion criteria in social networks, family health strategies, and clinics specializing in the treatment of obesity.All volunteers were sedentary, non-smokers, and free of cardiovascular, pulmonary, neuromuscular, and infectious diseases.The obese individuals included had a BMI>30kg/m², while eutrophic individuals presented BMI≥18.5 and <25kg/m 2 , aged between 18 and 46 years.Eutrophic individuals were matched for sex and age in relation to the obese individuals.We excluded individuals with acute health problems or complaints arising in the last month (viral or bacterial infections, accidents, allergic reactions), nervous system diseases or conditions that affected the understanding and participation in the study, pregnancy, diabetes mellitus type I, symptomatic coronary artery disease, left ventricular dysfunction, bronchial asthma, chronic obstructive pulmonary disease, chronic neuropathies, and use of drugs such as corticosteroids or bronchodilators.

Materials and procedures
On different days, the individuals were submitted to blood collection for laboratory tests, assessment of inspiratory and expiratory muscle strength, and inspiratory muscle endurance test.

Laboratory tests
After 12 hours of fasting, approximately 8 ml of blood were collected from the individuals for laboratory analysis of blood glucose, triglycerides, and total cholesterol, HDL-C, LDL-C.The samples were processed on the same day of collection, with the serum being used to the analyses by the enzymatic method, by the device Biosystems Automatic Analyzer A-25 15 .

Respiratory muscle strength assessment
Inspiratory and expiratory muscle strength were determined by maximum inspiratory pressure (MIP) and maximum expiratory pressure (MEP), measured with an analogic manovacuometer (Famabras, Brazil), calibrated in cmH 2 O with an operating limit of +/-300cmH 2 O. Respiratory maneuvers were repeated until six measures with variation of less than 10% were obtained.The highest value obtained was used as MIP and as MEP 16 .The predicted values of MIP and MEP for the sex and age were calculated using the equation by Neder et al. 17 .

Anthropometric assessments
BMI was calculated by weight (kg) divided by the squared height (m²), as recommended by the World Health Organization (WHO) 18 .The weight was measured with a scale (Plenna Slim Digital, Brazil) and the height with a stadiometer (Compacto E210 -Wiso®, Brazil).
The waist and hip circumferences were measured with a measure tape with a scale from 0 to 250 cm.The waist-hip ratio was calculated by dividing the waist circumference by the hip circumference.The measurements were taken while the individuals were in the orthostatic posture 19 .

Inspiratory muscle endurance assessment
First, MIP was determined.After 15 minutes of rest, individuals sat for measurement of blood pressure, heart rate, and blood oxygen saturation.The inspiratory muscle endurance test was conducted with the participants using a nasal clip, while they breathed continuously through a nozzle connected to a linear inspiratory resistance (POWERbreathe, Southam, United Kingdom) of 50% of the MIP with a 10% increment of the MIP every three minutes, until the individual showed to be unable to continue the test.Individuals should maintain a respiratory rate of 15 breaths per minute, following a specific audio signal for inspiration and expiration from a metronome.We used as inspiratory muscle endurance measure the highest inspiratory pressure value sustained by at least 60 seconds (Pthmax), expressed as a percentage of MIP (Pthmax/MIP) 20,21 , as well as test duration expressed in seconds.
Hemodynamic variables were measured at rest and at the end of the inspiratory muscle endurance test.Blood pressure was measured in the non-dominant arm with a sphygmomanometer (Unilet®, Brazil).The cuff was positioned from 2 to 3 cm above the cubital fossa and without excessive compression of the stethoscope to the brachial artery.Systolic blood pressure was estimated by auscultation of the first sound (Korotkoff phase I) and diastolic blood pressure by the disappearance of sounds (Korotkoff phase V ) 22 .Heart rate and blood oxygen saturation was measured by a pulse oximetry (Fingertip Pulse Oximeter, China).
The data were analyzed, expressed as mean and standard deviation and distributed as determined by the Kolmogorov-Smirnov test.To analyze the results, the software SPSS 22.0 was used.The inspiratory muscle strength and endurance were compared between obese and eutrophic individuals by Student's t-test for independent samples.The analysis of variance for repeated measurements (ANOVA) was used to assess the effects of the inspiratory muscle endurance test on the hemodynamic variables in obese and eutrophic individuals.The association among variables was analyzed by Pearson correlation.A p-value<0.05 was considered significant.

RESULTS
Regarding the clinical assessment, the groups did not differ as to age and sex.As for the anthropometric assessment, although the obese individuals, as expected, presented greater body weight, higher BMI, and higher waist and hip circumference measures than the eutrophic individuals, waist-hip ratio did not differ between the groups.The obese individuals were stratified in degrees of obesity: 6 of them were grade I, 9 grade II, and 5 were grade III obese.The laboratory assessment showed higher glycemia, triglycerides, and total cholesterol levels in obese individuals, compared to the eutrophic individuals (Table 1).Table 2 shows that inspiratory muscle strength, represented by the MIP, and expiratory muscle strength, represented by the MEP, presented no significant differences between obese and eutrophic individuals for both absolute and the predicted values for sex and age, according to the equation proposed by Neder et al. 17 .The duration of the inspiratory muscle endurance test for eutrophic individuals (651±215seg) was higher than among obese individuals (470±326seg, p=0.04).However, the MIP reached at the end of the test did not differ significantly between the groups (obese=77±24cmH 2 O; eutrophic=84±26cmH 2 O, p=0.88).At rest, the obese individuals showed systolic and diastolic blood pressure and heart rate higher than that of eutrophic individuals.However, the increase in systolic and diastolic blood pressure and heart rate was similar in both groups at the end of the inspiratory muscle endurance test.As for peripheral oxygen saturation, it did not undergo changes due to the test (Table 3).The duration of the inspiratory muscle endurance test was inversely associated with BMI (r=-0.37;p=0.020).However, there was no significant association between the percentage of MIP, reached at the inspiratory muscle endurance test, and BMI (r=-0.13;p=0.41).There was also no correlation between the MIP reached at progressive inspiratory muscle endurance test and BMI (r=-0.013;p=0.93).

DISCUSSION
This study showed that the inspiratory muscle endurance of obese individuals is less than that of eutrophic individuals.However, hemodynamic responses, induced by the inspiratory resistance exercise, were similar in both groups.
From the assumption that the inspiratory muscle endurance is important for the analysis of respiratory disorders and that its assessment is simple and of easy applicability, studying it in the obese population becomes relevant.It should be noted that so far we did not found in the literature any study that investigated if obesity changes the inspiratory muscle endurance, only one research with healthy children and adolescents, non-obese, which demonstrated the correlation between progressive inspiratory muscle endurance test performance and weight and height 8 .
Our study showed that inspiratory muscle endurance is inversely associated with BMI.Obesity did not alter the hemodynamic responses to inspiratory muscle resistance exercises, possibly due to the preservation of inspiratory muscle strength in obese individuals.Corroborating this finding, previous studies reported that obesity does not alter the strength of inspiratory muscles 23 , which can even be found within the range of normalcy 5 .In our research, workload during the inspiratory resistance exercise test was similar for obese and eutrophic individuals, however the duration of the exercise was greater in eutrophic individuals, suggesting greater work ability than obese individuals.Possibly, this reduced inspiratory muscle endurance is related to the type of muscle fiber and metabolic profile during muscular contraction 24 .
In fact, the inspiratory endurance test held until fatigue can accumulate metabolites that stimulate the metaboreceptors to activate the sympathetic nervous system and peripheral vasoconstriction, raising arterial pressure 25,26,11 .Despite the hemodynamic responses during the inspiratory resistance exercise being similar among obese and eutrophic individuals, the physiological mechanism may differ between the groups.In a preliminary study, the manual grasping exercise elevated the mean arterial pressure in obese and eutrophic children in a similar way, but the increase in blood pressure in eutrophic children was mediated by the increase of peripheral vascular resistance, while in obese children, it was induced by the increase in the systolic volume 27 .
Corroborating previous studies 28,29 , the obese individuals in this study showed cardiovascular adaptations such as high systolic, diastolic, and mean blood pressure, as well as heart rate at rest.These changes can be explained by the effects of visceral adipose tissue in the increasing of the activity of the sympathetic nervous system 30 and of angiotensin II, which, associated with endothelial dysfunction 31 , affects the elevation of the systemic vascular resistance and, therefore, blood pressure 29 .
The clinical relevance of this study is characterized by the applicability of the assessment of the inspiratory muscle endurance in the obese population, until then poorly studied.In addition to this aspect, the finding of decreased inspiratory muscle endurance in obese individuals can provide information about the limitations imposed by obesity on exercise capacity, suggesting that strength and inspiratory muscle endurance can be used to determine goals for physical training programs 32 .

CONCLUSION
This study showed that, compared to eutrophic individuals, obese individuals present reduced inspiratory muscle endurance, although the hemodynamic responses induced by inspiratory muscle endurance tests is similar in both groups.

Table 1 .
Clinical characteristics of obese and eutrophic individuals BMI: body mass index.*p=0.05

Table 2 .
Respiratory muscle force values in the sample MIP: maximum inspiratory pressure (p=0.814);% predicted MIP: percentage of the predicted maximum inspiratory pressure for sex and age (p=0.670);MEP: maximum expiratory pressure (p=0.496);% predicted MEP: percentage of the predicted maximum expiratory pressure for sex and age (p=0.395)

Table 3 .
Hemodynamic responses during the inspiratory muscle endurance test