ANÁLISE COMPARATIVA DA HIPERTROFIA NEUROMUSCULAR EM IDOSOS SARCOPÊNICOS E IDOSOS SARCOPÊNICOS PÓS-COVID-19 SUBMETIDOS A UM PROGRAMA DE EXERCÍCIOS

Ciências da Saúde, Volume 27 - Edição 128/NOV 2023 / 06/12/2023

COMPARATIVE ANALYSIS OF NEUROMUSCULAR HYPERTROPHY IN SARCOPENIC OLDER ADULTS AND SARCOPENIC OLDER ADULTS POST-COVID-19 SUBMITTED TO AN EXERCISE PROGRAM

REGISTRO DOI: 10.5281/zenodo.10218966

Monique de Azevedo1; Bruno Hendriks Lobo2; Aline Teixeira Alves3; Serise Amaral Pequeno4; Patrícia Azevedo Garcia5; Daniela Mara de Oliveira.

Abstract 

Objective: Compare the gain of neuromuscular hypertrophy between sarcopenic older adults without COVID-19 and sarcopenic older adults post-COVID-19. Methods: This was a comparative study in which two control groups (G1 and G2) and two experimental groups (G3 and G4) were selected, all consisting of sarcopenic older adults, separated into negative and positive for COVID-19, and subjected to a muscle hypertrophy protocol applied for 8 weeks, with a 48-hour interval between sessions. The variables analyzed were body mass index, handgrip strength, and anthropometry of upper and lower limbs bilaterally in all groups, and in the experimental groups, data were collected before and after the final procedure. Results: A total of 37 older adults were selected. The study population consisted of 51% men, 51% institutionalized, and 42% sedentary individuals. Group 1 showed superiority in the variables, except for left and right handgrip strength and anthropometric measurement of the right arm, which were higher in G2. Individuals in groups G3 and G4 experienced strength and trophism gains in all aspects, except for a decrease in left leg measurement in group 4. Conclusion: Based on the findings of this research, it can be concluded that a physical exercise program can increase strength and trophism in sarcopenic older adults. However, post-COVID-19 older adults showed inferior gains in hypertrophy compared to the group without COVID-19, even when subjected to the same experimental protocol. 

Keywords: Aging. Skeletal muscle. Sarcopenia. Exercise. Hypertrophy. COVID-19

Resumo

Objetivo: Comparar o ganho de hipertrofia neuromuscular entre idosos sarcopênicos sem COVID-19 e idosos sarcopênicos pós-COVID-19. Métodos: Este foi um estudo comparativo no qual foram selecionados dois grupos controle (G1 e G2) e dois grupos experimentais (G3 e G4), todos constituídos por idosos sarcopênicos, separados em negativos e positivos para COVID-19, e submetidos a uma protocolo de hipertrofia muscular aplicado durante 8 semanas, com intervalo de 48 horas entre as sessões. As variáveis analisadas foram índice de massa corporal, força de preensão manual e antropometria de membros superiores e inferiores bilateralmente em todos os grupos, sendo que nos grupos experimentais os dados foram coletados antes e após o procedimento final. Resultados: Foram selecionados 37 idosos. A população do estudo foi composta por 51% de homens, 51% de institucionalizados e 42% de sedentários. O Grupo 1 apresentou superioridade nas variáveis, exceto para força de preensão palmar esquerda e direita e medida antropométrica do braço direito, que foram maiores no G2. Os indivíduos dos grupos G3 e G4 tiveram ganhos de força e trofismo em todos os aspectos, exceto pela diminuição da medida da perna esquerda no grupo 4. Conclusão: Com base nos achados desta pesquisa, pode-se concluir que um programa de exercícios físicos pode aumentar a força e trofismo em idosos sarcopênicos. No entanto, os idosos pós-COVID-19 apresentaram ganhos inferiores de hipertrofia em comparação ao grupo sem COVID-19, mesmo quando submetidos ao mesmo protocolo experimental.

Palavras-chave: Envelhecimento. Músculo esquelético. Sarcopenia. Exercício. Hipertrofia. COVID 19.

Introduction 

Sarcopenia is a progressive and systemic process resulting from a disorder of skeletal muscle that leads to a rapid loss of muscle mass1,2. Sarcopenia has a close relationship with osteoporosis in the elderly, as both are deleterious effects of aging, such as muscle and bone mass deficit. The association of sarcopenia with osteoporosis, along with metabolic diseases often observed in aging, leads to a pronounced form of sarcopenia2. Sarcopenia in the elderly also leads to congestive heart failure (CHF) and chronic obstructive pulmonary disease (COPD) by impairing the functioning of muscles involved in respiratory activity3. Sarcopenia and osteoporosis share similar risk factors and metabolic pathways, posing a threat to independence, compromising the quality of life, and increasing the vulnerability of older individuals. The combination of osteoporosis and sarcopenia increases the propensity for falls, making elderly individuals more vulnerable4. Sarcopenia has a multifactorial etiology that is not yet fully elucidated; however, it is known that the decrease in anabolic hormones is involved in both the development and maintenance of sarcopenia5. 

The literature is consistent in describing the application of protocols for resistance exercise training to promote muscle hypertrophy. The hypertrophy of these muscles can be induced by mechanical stress, which affects different signaling pathways, such as kinase B, altering the balance of muscle proteins to favor synthesis over degradation6-8. Strength training can delay sarcopenia9,10. Power training also induces neuromuscular adaptations, increasing the recruitment and excitation of motor neurons of these fibers during voluntary muscle contraction11. 

Coronavirus is a group of viruses capable of causing respiratory infections, which can evolve with mild or severe repercussions. In December 2019, the first cases of coronavirus were detected in Wuhan, China, and were referred to as severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), causing the disease known as coronavirus (COVID-19)12,13. 

COVID-19 has been recognized to cause pneumonia, shortness of breath, and hypoxia, with the latter being difficult to reverse in certain cases, requiring supplemental oxygen with low saturation during exertion14,15. The clinical condition of severe COVID-19 patients can progress to multiorgan dysfunction, which, combined with immobility and low nutritional levels, becomes a risk factor for acute sarcopenia observed in acutely ill patients16. The deficits caused by COVID-19 can persist for periods that are still not fully understood and have a considerable impact on quality of life, return to work, and the ability to perform activities of daily living17. 

The present study aimed to compare the effects of the same muscle hypertrophy training protocol in sarcopenic elderly individuals and sarcopenic elderly individuals postCOVID-19, aiming to recover trophism in this population and compare it to that observed in sarcopenic patients who did not have COVID-1918,19. 

Methods 

This was a Quasi-Experimental study design that was conducted for six weeks, from October 18th until November 26th, 2023. The sample consisted of 40 sarcopenic older adults of both sexes residing in the Distrito Federal state, Brazil, aged 60 years or older. Some patients were institutionalized in Long-Term Care Facilities, while others were non-institutionalized. The participants were recruited through snowball sampling, a non-probabilistic sampling technique, in which initial participants invite new participants from their network of friends and acquaintances who fit the sample criteria.  This study was approved by the Ethics and Research Committee under CAAE: 48372921.0.0000.0023. 

All participants had preserved cognitive function, were functionally independent, did not participate in any physical training program, and had not experienced any fractures in the lower or upper limbs in the past six months. Individuals who had been hospitalized had a minimum hospital stay of 10 days. 

All participants completed and signed the Physical Activity Readiness Questionnaire (PAR-Q) and the Informed Consent Form according to the eligibility criteria and were distributed into four groups: GROUP 1: Control Group (CG), comprised of 10 sarcopenic older adults without a history of COVID-19 and without strength training intervention. GROUP 2: Post-COVID-19 Control Group (PCCG): comprised of 10 sarcopenic older adults who had recovered from COVID-19 without strength training intervention. GROUP 3: Non-COVID Sarcopenic Group with Strength Training Intervention (NCSG): comprised of sarcopenic older adults without COVID-19 who underwent strength training intervention; and GROUP 4: Post-COVID Sarcopenic Group with Strength Training Intervention (PCS): comprised of sarcopenic older adults who had recovered from COVID-19 and underwent strength training intervention. 

All participants underwent anthropometric assessment, which was performed by one of the researchers. The initial measurement was taken in the GROUP 1 (CG), and GROUP 2 (PCCG), while both initial and final measurements were taken in the GROUP 3 (NCSG) and GROUP 4 (PCS). Weight was measured in kilograms using a Serener® digital precision scale and an Omron® bioimpedance equipment. Height was measured using an anthropometer attached to the scale. The weight and height measurements were taken with the participants barefoot, wearing light clothing, in an orthostatic position, with their feet parallel and together, arms extended along the body, and the head positioned in the Frankfurt plane. The body mass index (BMI) was calculated by dividing the weight by the square of the height. The cutoff points proposed by the Pan American Health Organization (PAHO, 2002)19 were used: low weight: BMI ≤ 23 kg/m², eutrophics: BMI between 23 and 28 kg/m², and pre-obesity/obesity: BMI ≥ 28 kg/m² 20.  

Muscle strength was measured using a manual dynamometer (CROWN®) with a capacity of 90 kg. The participant was seated with their feet flat on the ground, elbows flexed at 90º, and forearms close to the body. The dynamometer was adjusted to fit the size of the participant’s hand, and they were instructed to exert maximum palmar grip strength for about three seconds, in triplicate, with a 30-second interval between measurements. The average of the three measurements was considered. The cutoff point for low muscle strength was FPP < 30 kg for men and FPP < 16 kg for womem21. All grip strength measurements were expressed in kilograms of strength. The reliability of the applied tests was previously determined as an appropriate indicator of test-retest reliability (Vincent, 2005)22. 

The participants were instructed to maintain an orthostatic position, barefoot, remove any metallic adornments, fast for at least two hours, and empty their bladder before the assessment. Sarcopenia was confirmed by the combination of low muscle strength and low skeletal muscle mass (SMM), following the definition established by the European Working Group on Sarcopenia in Older People (EWGSOP2)23. The assessment protocol was carried out by trained and blinded researchers in relation to the patients’ data and groups. They were provided with the participant’s name, the location where the intervention would take place, and confirmation that the individual was eligible to receive the training, ensuring blinding in the study. 

Before and after the exercise sessions, the following measurements were taken blood pressure using a calibrated Omron® 7421 device, oxygen saturation using an Omron® finger pulse oximeter, and temperature using a functioning digital thermometer. The exercise sessions began with three sets of 15 repetitions for each of the proposed exercises targeting major muscle groups. In an orthostatic position, the exercises included elbow flexion and extension (biceps and triceps brachii), lateral raises (deltoids), and chest flies (pectoralis, back, and latissimus dorsi). For the lower limbs, exercises included hip flexion in an orthostatic position, leg abduction and adduction in lateral decubitus, and gastrocnemius exercises in an orthostatic position using weights ranging from 1 to 2 kilograms, with a 30-second rest between sets24. The exercise protocol was conducted over a period of 6 weeks, with a 48-hour interval between sessions, as suggested in the literature. 

After the six weeks of the intervention protocol, the initial measurements were collected again by the primary researcher. The measurements were identified as follows: Wei: weight, BMI: body mass index (calculated by dividing the weight by the square of the height), LH: left hand strength (measured by dynamometry), RH: right hand strength (measured by dynamometry), CRA: circumference of the right upper arm in centimeters, CLA: circumference of the left upper arm in centimeters, CRL: circumference of the right upper leg in centimeters, and CLL: circumference of the left upper leg in centimeters.  

Initially, a descriptive analysis was performed to describe the observed data. Analysis of variance (ANOVA) was adopted to compare the means of the groups, based on the variance of the sample groups22. 

Results and Discussion 

Initially, a total of 53 individuals were approached and distributed as follows: 

  • GROUP 1 (CG) with 14 individuals, of which 3 were excluded for being outside the specified age range and 1 due to withdrawal. 
  • Group 2 (PCCG) with 13 individuals, of which 3 were excluded for not meeting the eligibility criteria. 
  • Group 3 (NCSG) with 15 individuals, of which 6 were excluded for having attendance below 75%, and 1 at the request of a family member. 
  • Group 4 (PCS) with 11 individuals, of which 2 were excluded for having attendance below 75%. 

In the analysis of the sociodemographic profile, as shown in Table 1, regarding gender, the presence of males in groups 1, 2, 3, and 4 was 40%, 50%, 64%, and 56%, respectively. Regarding institutionalization, group 1 consisted solely of noninstitutionalized older adults, while in groups 2, 3, and 4, the proportion of institutionalized individuals was 50%, 90%, and 80%, respectively.

Tables 2 and 3 display the information on the variables for groups 1 and 2, where group 1 showed higher numbers than group 2, except for the items: RH, LH and CRA, which had greater gains in individuals in group 2. 

Tables 4 and 5 show the variables of experimental groups 3 and 4, where there was slight bilateral gain in strength in hand dynamometry, in both groups. In the anthropometric measurement of arms bilaterally, hypertrophy was also noted in both groups. In group 3, hypertrophy was perceived bilaterally in leg anthropometry. In group 4, there was a decrease in measurement in the left leg. 

The board below shows the general average and standard deviation of the variables of all groups. 

Graph 1 shows the average and standard deviation of the body mass index (BMI)for all groups. Graph 2 shows the average and standard deviation of right handle (RH)for all groups. Graph 3 shows the average and standard deviation of left handle (LH) for all groups. Graph 4 shows the average and standard deviation of circumference of right upper arm (CRA) for all groups. Graph 5 shows the average and standard deviation of circumference of left upper arm (CRA) for all groups. Graph 6 shows the average and standard deviation of circumference of right upper leg (CRL) for all groups. Graph 7 shows the average and standard deviation of circumference of left upper leg (CLL) for all groups. 

The coronavirus, responsible for the infectious condition COVID-19, has significantly affected and continues to impact the lives and routines of the global population. The elderly population has shown growth in recent decades, and with increased longevity, certain chronic diseases tend to worsen due to the deleterious effects of aging. One common issue in this population is sarcopenia, which leads to musculoskeletal limitations and compromises the individual’s quality of life. 

The average educational level of the groups was considered high, which is not common according to some authors who claim that low education is prevalent among the elderly population, as they lived in a context where education was not a priority, especially for females19,20. Our sample was recruited in the capital city of the country, in affluent neighborhoods, and not all individuals were institutionalized, which may account for this difference. An important finding from another study emphasizes that higher education tends to reduce the number of diseases by providing access to information that improves overall quality of life21,22,23. 

In our study, in the control groups, older adults post-COVID showed greater muscle strength compared to those who did not have COVID. This result somewhat contradicts the literature, which states that post-COVID patients demonstrate musculoskeletal limitations even after hospital discharge or the late phase of the disease24,25,26,27. Several factors can explain our results: in the control groups, the age of the older adults who had COVID was 8 years younger. This aligns with some authors who describe musculoskeletal limitations as an event that worsens with advancing age28. The result in the experimental groups was like the control group, meaning that older adults post-COVID had greater muscle strength compared to the group without COVID. The age of Group 4 (G4) was younger, and despite the smaller age difference in these groups compared to Groups 1 and 2, a contributing factor to this result may be that in the group without COVID, 90% were sedentary, while in the group with COVID, 60% were sedentary. Another interesting finding is that 90% of G3 were institutionalized, while 18% of G4 were institutionalized, indicating that institutionalized older adults commonly experience greater health issues, making them more fragile29,30. Without exception, there was an increase in strength and muscle mass in the experimental groups. G4 showed more significant gains, which can be explained by the age difference or the factor of institutionalization31,32. Many of these older adults engaged in some form of physical exercise, compared to most sedentary individuals in G3, which may have created a memory of exercise adaptation, resulting in a more effective response to the protocol. The gains in G4 were surprising since all of them spent more than 10 days in hospitalization, which, according to other authors32,33. can lead to a loss of up to 2% of muscle mass per day, and the length of hospital stay negatively influences muscle mass loss due to immobility33,34,35. 

The benefits of physical exercise are well-known and consensus in the literature35,36. During times of social isolation, this practice has become challenging, especially for the elderly, as they are considered a high-risk group. Sarcopenia is a frequently present condition in the lives of older adults due to the deleterious effects of aging, which includes low muscle mass, low physical performance, and low muscle strength27. All these criteria were observed in the population of this study, reinforcing conformity with the literature studied. This pattern is eminent among the elderly, estimated to have an average annual skeletal muscle mass loss of 1% to 2% and muscle strength loss of 1.5% to 5% 28. 

One of the analyzed studies reported that 5-13% of individuals aged 60 to 70 years and up to 50% of individuals over 80 years of age are affected by sarcopenia [29]. In our sample, all older adults were sarcopenic due to it being one of the inclusion criteria for the study, and the literature categorically states that sarcopenia has a negative influence on functionality, leading to partial or complete loss of autonomy. Authors are emphatic in stating that strength training can reduce the process of sarcopenia and even delay it30,37. 

Our experimental groups, when subjected to the hypertrophy protocol, showed an increase in both strength and anthropometric value. The increase was discreet in all individuals of the group, with no significance between the groups but with a slight increase among men. In our search, a study reveals that sedentary behavior enhances the onset of sarcopenia, especially related to aging. Sedentary older adults with low mobility have lower muscle mass, leading to increased physical disability31. The main question of this study was to verify if there is a significant difference in muscle mass gain between sarcopenic older adults who had COVID-19 and those who did not. A minimum of 10 days of hospitalization was included in this study based on the reinforcement of the literature, which states that the musculoskeletal consequences of COVID-19 are still not elucidated, but it is known that hospitalized patients are more likely to develop muscle atrophy and weakness due to immobility and prolonged mechanical ventilation32. These results conform to other studies stating that not only long periods of immobility but also situations of social isolation affect muscle homeostasis, leading to physical inactivity and disuse33.

In this sample, we found no significant difference between the groups in terms of strength and muscle mass gains. Although this difference was not significant, it was possible to observe more precise movements, agility in the proposed exercises, and increased disposition in all subjects of the experimental groups. Our perception of these facts is based on the analyzed literature, which states that physical exercise, when performed regularly with moderate to vigorous intensity, can improve health conditions and have a direct relationship with the pathophysiological mechanisms of COVID-19, reducing the severity of the disease’s effects by mobilizing immune system cells and reducing systemic inflammation, thereby increasing pre- and post-infection immunity34,38,39. 

It is worth noting that other types of influenza can also weaken older individuals and leave them with a more vulnerable immune system. In this sense, the WHO reports the occurrence of influenza worldwide, affecting 5% to 15% of the population, causing 3 to 5 million severe cases and 250,000 to 650,000 deaths every year35. This virus is responsible for flu cases that occur with seasonal variation and can progress from mild symptoms to more severe conditions, resulting in a significant impact on hospitalizations and mortality39,40,41. Although our work focuses on the sequelae of COVID-19, it is important to mention influenza cases that inflate the morbidity and mortality rates in the elderly population, including muscle weakness and the difficult return to the overall pre-flu health state, as it predominantly affects the respiratory system. While not always leading to death, it can cause complications that directly interfere with the quality of life. Therefore, the identification and understanding of this phenomenon and its repercussions, particularly in the elderly organism, are of utmost importance42,43. 

In a 2015 study on factors related to the adherence of non-institutionalized elderly individuals to influenza vaccination campaigns in a municipality in São Paulo, Brazil, the most frequent response for non-adherence was the lack of confidence in the vaccine’s efficacy. The variables used in that study included demographic characteristics, gender, nationality, age, marital status, living alone, skin color, socioeconomic conditions, education, current work, alcohol consumption, smoking, health conditions, falls in the last year, and use and access to health services. These variables align with the parameters used in our work, although with different objectives, demonstrating the importance of these combinations to obtain more accurate information for data collection in this population37-39,42,44

Conclusion 

The present study allowed us to conclude that a physical exercise program is capable of increasing strength and trophism in sarcopenic older adults; however, post-COVID19 older adults showed inferiority in hypertrophy gains when compared to the group without COVID-19, even though they were submitted to the same experimental protocol. Further studies in the area with a larger and more varied sample are suggested. 

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Financiamento da pesquisa: Fundação Universidade de Brasília – DPI/DPG

1Programa de Pós-Graduação em Biologia Animal, Universidade de Brasília – UnB,Brasília, DF. Brasil. Doutoranda em Biologia Animal- PPGBioAni-UnB. E-mail: moniazewedo2@gmail.com;
2Centro Universitário de Brasília- CEUB. Brasília, Brasil. Graduado em. Educação Física.E-mail: Brunohendrikslobo@gmail.com;
3Programa de Pós-Graduação em Ciências da Reabilitação da Faculdade de Ceilândia, Universidade de Brasília – PPGCR- UnB.  Brasília, Brasil. Doutora em Ciências da Saúde – UnB. Email: alinealves@unb.br;
4Programa de Pós-Graduação em Ciências da Reabilitação da Faculdade de Ceilândia, Universidade de Brasília – PPGCR- UnB. Brasília, Brasil. Mestranda em Ciências da Reabilitação – PPGCR-UnB. Email: serise.amaral@gmail.com;
5Programa de Pós-Graduação em Ciências da Reabilitação da Faculdade de Ceilândia, Universidade de Brasília – PPGCR- UnB. Brasília, Brasil. Doutora em Ciências da Reabilitação – UFMG. Email: patriciaagarcia@unb.br;
6Departamento de Genética e Morfologia, Instituto de Ciências Biológicas, Universidade de Brasília – UnB. Brasília, Brasil. Doutora em Bioquímica – Instituto de Química da Universidade de São Paulo- Brasil. Email: dmoliveira@unb.br