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PORTO ALEGRE – UFCSPA

PROGRAMA DE PÓS-GRADUAÇÃO EM CIÊNCIAS DA SAÚDE

Marlon Francys Vidmar

Efeito do exercício excêntrico nos músculos extensores de joelho em condições isotônicas e isocinéticas

após meniscectomia parcial ou reconstrução do ligamento cruzado

anterior.

Porto Alegre

2019

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Efeito do exercício excêntrico nos músculos extensores de joelho em condições isotônicas e isocinéticas

após meniscectomia parcial ou reconstrução do ligamento cruzado

anterior.

Tese submetida ao Programa de Pós- Graduação em Ciências da Saúde da Universidade Federal de Ciências da Saúde de Porto Alegre como requisito para a obtenção do grau de Doutor.

Orientador: Dr. Marcelo Faria Silva Coorientador: Dr. Bruno Manfredini Baroni

Porto Alegre

2019

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DEDICATÓRIA

Dedico esta dissertação à Deus, minha

família, namorada, orientadores e

amigos pelo apoio, força, incentivo,

companherismo e amizade. Sem vocês

nada disso seria possível.

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Agradeço a Deus por me amparar nos momentos difíceis, me dar força para superar as dificuldades, mostrar os caminhos nas horas incertas e me suprir em todas as minhas necessidades.

Aos meus pais e familiares, que sempre estiveram ao meu lado e me incentivaram a querer ser sempre melhor enquanto estudante, profissional e acima de tudo, enquanto ser humano.

À minha namorada, Vandressa, por ser tão importante na minha vida, devido a sua amizade, paciência, compreensão, dedicação e amor.

Ao meu orientador, Prof. Dr. Marcelo Faria Silva, e ao meu co- orientador Prof. Dr. Bruno Manfredini Baroni, pela confiança depositada em mim quando me aceitaram no Doutorado, por me mostrarem o caminho da ciência e pelas oportunidades oferecidas na busca de novos conhecimentos. Fazendo me enxergar, que existe mais que pesquisadores e resultados por trás de uma tese, mas vidas humanas.

Ao amigo, Prof. Me. Gilnei Lopes Pimentel, por terem me incentivado na busca do meu sonho, pelos encinamentos, pela competência e disposição em compartilhar experiências.

Aos amigos, Dr. Alexandre Fróes Michelin, Márcio Mezzomo e Ricardo Lugokenski pela confiança na execução do projeto e pela inestimável experiência em trabalhar com vocês.

Aos colegas do Laboratório de Biomecânica, Guilherme Bugança e Eduardo Favretto, pelo engajamento e empenho nas sessões de treinamento.

À todos os voluntários que participaram da pesquisa, pela sua disposinibilidade.

À Universidade de Passo Fundo, por disponibilizar a infraestrutura do Laboratório de Biomecânica e Clínica de Fisioterapia.

À CAPES, pelo apoio financeiro durante parte deste período.

A todos, reitero o meu apreço e a minha eterna gratidão.

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As lesões do ligamento cruzado anterior (LCA) e lesões meniscais são responsáveis por redução da força e massa muscular de extensores de joelho no período pós- operatório. Esses prejuízos podem promover instabilidade articular no joelho, gerando restrição a sua funcionalidade e, consequentemente, limitação das atividades de vida diárias e esportivas. O tema desta tese de Doutorado é comparar os efeitos do treinamento excêntrico convencional (carga constante) e excêntrico isocinético na massa muscular do quadríceps, força e desempenho funcional em atletas recreacionais após reconstrução do LCA ou meniscectomia parcial. Foram realizados dois ensaios clínicos randomizados, sendo as amostras compostas por 30 atletas recreacionais submetidos à reconstrução do LCA (Capítulo I) e 32 atletas recreacionais após meniscectomia parcial (Capítulo II). Os voluntários foram randomizados em: Grupo Convencional (GC), submetido a um programa de reabilitação muscular baseado no exercício excêntrico isotônico; e Grupo Isocinético (GI), submetido a um programa de reabilitação muscular baseado no exercício excêntrico isocinético. Anteriormente aos protocolos de reabilitação muscular, os indivíduos foram submetidos a um mesmo protocolo fisioterapêutico. Os programas de reabilitação muscular iniciaram aproximadamente 45 dias pós-reconstrução do LCA e 15 dias após meniscectomia parcial, o membro não operado foi utilizado como controle. Cada sessão de treinamento compreendeu a realização de 3 séries (semanas 1-3) ou 4 séries (semanas 4-6) de 10 repetições excêntricas máximas de extensores de joelho. Os programas tiveram duração de seis semanas, com frequência de treinamento de duas sessões por semana, separados por um intervalo mínimo de 72 horas. Foram realizadas avaliações da massa muscular por meio da área de secção transversa anatômica do quadríceps (ressonância nuclear magnética), força dos músculos extensores de joelho (dinamometria isocinética) e desempenho funcional do indivíduo (questionário e teste de salto) antes e após os programas de treinamento excêntrico. Nos indivíduos submetidos à reconstrução do LCA, o treinamento isocinético promoveu tamanhos de efeito grande para todos os desfechos de massa muscular (aumentos de 17-23%), bem como força extensora do joelho (25-66%) e desempenho de salto (20%). O treinamento convencional promoveu efeitos pequeno à moderado para desfechos de massa muscular (5-9%), tamanhos de efeitos moderado a grande para força extensora do joelho (16-0%) e tamanho de efeito grande para desempenho de salto (15%). Ambos os grupos apresentaram tamanhos de efeito grande no questionário Lysholm. O grupo IG apresentou maiores alterações que o GC para todos os desfechos de massa muscular (tamanho do efeito: 0,72-1,08), questionário Lysholm (tamanho do efeito:

0,7), força isométrica (tamanho do efeito: 0,71) e força excêntrica (tamanho do

efeito: 0,96). Já nos indivíduos após meniscectomia parcial, o treinamento

isocinético promoveu tamanhos de efeito grande para todos os desfechos de massa

muscular (aumentos de 9-10%), bem como força extensora do joelho (22-38%) e

desempenho de salto (15%). O treinamento convencional promoveu efeitos

pequenos para desfechos de massa muscular (3-8%), tamanhos de efeito pequeno

a moderado para força extensora do joelho (3-11%) e tamanho de efeito moderado

para desempenho de salto (11%). Ambos os grupos apresentaram tamanhos de

efeito grande no questionário Lysholm. O grupo IG apresentou maiores alterações

que o GC para todos os desfechos de massa muscular (tamanhos de efeito: 0,99-

1,41), bem como força (tamanhos de efeito: 1,48-2,35) e questionário Lysholm

(tamanho do efeito: 1,00). O treinamento isocinético excêntrico promoveu

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e força muscular extensora do joelho de atletas recreacionais submetidos à reconstrução do LCA ou meniscectomia parcial.

Palavras-chave: Joelho. Ligamento Cruzado anterior. Meniscos tibiais.

Dinamômetro de força muscular. Músculo quadríceps.

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Anterior cruciate ligament (ACL) injuries and meniscal injuries are responsible for reduction in knee extensor muscles mass and strength over the post-surgery period.

These deficits may contribute to promotion of joint instability, leading to functional restriction and limitation of daily and sport activities. The aim of this doctorate thesis was to compare the effects of conventional eccentric training (with constant load) and isokinetic eccentric training on quadriceps muscle mass, strength and functional performance of recreational athletes following either ACL reconstruction or partial meniscectomy. Two randomized clinical trails were conducted and their samples consisted of 30 athletes submitted to ACL reconstruction (Chapter I) and 32 athletes submitted to partial meniscectomy (Chapter II). Participants were randomized into:

Conventional Group (CG) composed by a muscular rehabilitation program based on isotonic eccentric exercise; or Isokinetic Group (IG) composed by a muscular rehabilitation program based on isokinetic eccentric exercise. Previously to the rehabilitation programs, individuals underwent a standard physiotherapy protocol.

Both rehabilitation programs commenced approximately 45 days after ACL reconstruction and 15 days after partial meniscectomy, so that the unaffected lower limb was used as control condition. Each training session consisted of 3 (1st to 3rd week) or 4 (4th to 6th week) series of 10 maximal eccentric contraction of the knee extensor muscles. Both programs were delivered during 6 weeks, with training frequency of 2 weekly sessions, and minimal interval of 72 hours. Assessments of quadriceps muscle mass (through magnetic resonance imaging), strength of the knee extensor muscles (through isokinetic dynamometry) and functionality (through Lysholm questionnaire and single leg hop test) were performed before and after eccentric training programs. In individuals submitted to ACL reconstruction, the isokinetic training led to large effect sizes for all muscle mass outcomes (increases of 17-23%), as well as quadriceps strength (25-66%) and jump performance (20%).

The conventional training promoted small to moderate effects for muscle mass outcomes (5-9%), moderate to large effect sizes for quadriceps strength (16-20%), and large effect size for jump performance (15%). Both groups presented large effect sizes in the Lysholm questionnaire. The IG group had higher changes than CG for all muscle mass outcomes (effect sizes: 0.72-1.08), Lysholm questionnaire (effect size:

0.7), isometric strength (effect size: 0.71), and eccentric strength (effect size: 0.96).

In individuals after partial meniscectomy, the isokinetic training led to large effect sizes for all muscle mass outcomes (increases of 9-10%), as well as for quadriceps strength (22-38%) and jump performance (15%). The conventional training promoted small effect sizes for muscle mass outcomes (3-8%), small to moderate effect sizes for quadriceps strength (3-11%) and moderate effect sizes for jump performance (11%). Both groups presented large effect sizes in the Lysholm questionnaire. The IG group had higher changes than CG for all muscle mass outcomes (effect sizes:

0.99-1.41), as well as strength (effect sizes: 1.48-2.35) and Lysholm questionnaire (effect size: 1.00). Isokinetic eccentric training promotes grater adaptations than conventional eccentric training on quadriceps muscle mass and strength of the recreational athletes after ACL reconstruction.

Key-words: Knee. Anterior Cruciate Ligament. Menisci, Tibial. Muscle Strength

Dynamometer. Quadriceps Muscle.

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Figura 1 – Flowchart of the study (Capítulo 1) ... 55

Figura 2 – Percent change pre- to post-training for conventional group (CG) and

isokinetic group (IG) (Capítulo 1)... 55

Figura 3 – Forest plot: standardized mean differences and 95%CI for conventional

group and isokinetic group (Capítulo 1).. ... 56

Figura 4 – Flowchart of the study (Capítulo 2) ... 87

Figura 5 – Percent change pre- to post-training for conventional group (CG) and

isokinetic group (IG) (Capítulo 2)... 87

Figura 6 – Forest plot: standardized mean differences and 95%CI for conventional

group and isokinetic group (Capítulo 2) ... 88

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Tabela 1 – Muscle mass, strength and functional performance pre-training and post-

training of the operated lower limb (Capítulo 1). ... 53

Tabela 2 – Muscle mass, strength and functional performance pre-training and post-

training of the non-operated lower limb (Capítulo 1)... 54

Tabela 3 – Muscle mass, strength and functional performance pre-training and post-

training of the operated lower limb(Capítulo 2) ... 85

Tabela 4 – Muscle mass, strength and functional performance pre-training and post-

training of the non-operated lower limb (Capítulo 2)... 86

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1 INTRODUÇÃO... 13

2 OBJETIVOS... 14

3 REVISÃO DE LITERATURA... 15

4 REFERÊNCIAS DA REVISÃO………. 18

5 CAPÍTULO I. Isokinetic eccentric training is better than constant load eccentric training on the quadriceps rehabilitation following anterior cruciate ligament reconstruction: a randomized clinical trial... 23 ABSTRACT... 25

INTRODUCTION... 26

METHODS... 28

Study design... 28

Participants... 29

Sample size... 29

Randomization and blinding... 29

ACL reconstruction surgery... 30

Post-surgery rehabilitation... 30

Eccentric training programs... 31

Muscle mass evaluation... 32

Muscle strength evaluation... 33

Functional performance evaluation... 33

Statistical analysis... 34

RESULTS... 35

DISCUSSION... 36

CONCLUSION... 42

KEY-POINTS... 42

REFERENCES... 43

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6 CAPÍTULO II. Isokinetic eccentric training is better than constant load eccentric training on the quadriceps rehabilitation following partial meniscectomy: a randomized clinical trial...

57

ABSTRACT... 59

INTRODUCTION... 60

METHODS... 62

Study design... 62

Participants... 63

Sample size... 63

Randomization and blinding... 63

Partial meniscectomy surgery... 64

Post-surgery rehabilitation... 64

Eccentric training programs... 65

Muscle mass evaluation... 66

Muscle strength evaluation... 67

Functional performance evaluation... 67

Statistical analysis... 68

RESULTS... 69

DISCUSSION... 70

CONCLUSION... 75

KEY-POINTS... 75

REFERENCES... 76

7 CONCLUSÃO GERAL... 89

ANEXO A – Aprovação do Comitê de Ética... 91

ANEXO B – Normas da Revista... 94

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1 INTRODUÇÃO

O tema para a presente tese de Doutorado foi definido à partir da lacuna existente na literatura dentro da fisioterapia esportiva sobre o efeito do exercício excêntrico nos músculos extensores de joelho em condições isotônicas e isocinéticas após procedimento cirúrgico, de meniscectomia parcial ou reconstrução do ligamento cruzado anterior (LCA). Com o intuito de responder esta lacuna e aprofundar os conhecimentos a cerca desta temática, dois ensaios clínicos randomizados foram conduzidos durante o Doutorado de Marlon Francys Vidmar junto ao Grupo de Estudos em Fisioterapia Traumato-Ortopédica na Universidade Federal de Ciências da Saúde de Porto Alegra (UFCSPA).

O Capítulo I refere-se a um artigo original que tem por objetivo comparar os efeitos do treinamento excêntrico convencional (carga constante) e excêntrico isocinético na massa muscular do quadríceps, força e desempenho funcional em atletas recreacionais após reconstrução do LCA.

No Capítulo II apresenta-se outro artigo original para comparar os efeitos do treinamento excêntrico convencional (carga constante) e excêntrico isocinético na massa muscular do quadríceps, força e desempenho funcional em atletas recreacionais após meniscectomia parcial.

O final desta tese de Doutorado destina-se a apresentar as considerações

finais e as principais contribuições para a literatura científica, na área da Fisioterapia

Esportiva.

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2 OBJETIVOS

Objetivo Geral

Avaliar os efeitos de programas de reabilitação muscular baseados no treinamento excêntrico convencional (carga constante) e excêntrico isocinético na massa muscular do quadríceps, força e desempenho funcional em atletas recreacionais após reconstrução do LCA ou meniscectomia parcial.

Objetivos Específicos

 Avaliar a massa muscular do quadríceps femoral através de imagens de

ressonância nuclear magnética;

 Analisar a força muscular dos extensores do joelho por meio da dinamometria

computadorizada;

 Determinar o desempenho funcional dos indivíduos através de questionário e

teste específico;

 Comparar as variáveis analisadas entre os grupos reabilitados por meio dos

programas de exercício excêntrico em condições isotônicas e isocinéticas.

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3 REVISÃO DE LITERATURA

O joelho é a articulação mais solicitada do corpo humano, sendo formada pelos côndilos do fêmur e da tíbia, e entre a superfície posterior da patela e a superfície patelar do fêmur, (SAAVEDRA et al., 2012), acoplados pelos ligamentos, cápsula articular, meniscos e músculos que realizam a sua estabilização.

A estabilidade desta articulação depende da interação entre a sua geometria, da restrição dos tecidos moles, das cargas aplicadas pelo peso corporal e das ações musculares proximais e distais. Enquanto a arquitetura óssea e os meniscos geram pouca estabilidade ao joelho, os ligamentos, cápsula e tecidos moles contribuem significativamente para sua estabilidade. As forças compressivas, resultantes do peso corporal e da atividade muscular, propiciam forças adicionais que previnem uma sobrecarga dos ligamentos quando o joelho é submetido a cargas excessivas em atividades mais agressivas. (GLENN et al., 2001).

Além disso, qualquer dano aos componentes que integram essa complexa estrutura pode levar ao desequilíbrio de sua biomecânica e funcionalidade, com possível deterioração das demais estruturas articulares. (JUNIOR et al., 2008). A seguir serão relatadas duas estruturas importantes na homeostase (estabilidade e funcionalidade) desta articulação: o ligamento cruzado anterior (LCA) e os meniscos. (GIULIANI; KILCOYNE; RUE, 2009; SCOTTI et al., 2013; ENGLUND et al., 2008).

O ligamento cruzado anterior (LCA) possui um papel fundamental na estabilidade passiva do joelho, controlando o movimento rotacional e contendo a translação anterior da tíbia em relação ao fêmur (HOUGLUM & BERTOTI, 2014). Os meniscos, medial e lateral, são estruturas essenciais para a homeostase do joelho, tendo como principais funções a estabilidade articular, transferência de peso, absorção de choque durante os movimentos e proteção da cartilagem articular.

(SCOTTI et al., 2013; ENGLUND et al., 2008).

Nos Estados Unidos, cerca de 120.000 indivíduos sofrem ruptura do LCA por

ano (KIM et al., 2011), o que gera um custo anual aproximado de US$ 1,7 bilhão

(KIAPOUR & MURRAY, 2014). Essa lesão é mais frequente em adultos jovens e

fisicamente ativos (KIAPOUR & MURRAY, 2014), e está associada à prática

esportiva, seja em atletas profissionais ou amadores/recreacionais (NAGANO,

YAKO-SUKETOMO, NATSUI, 2018). Já as lesões meniscais podem ocorrem de

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forma traumática ou degenerativa. As lesões degenerativas do menisco desenvolvem-se lentamente e tipicamente ocorrem em indivíduos de meia-idade ou mais velhas. (BEAUFILS et al., 2017). Já as lesões traumáticas (giratório/pivô) ocorrem durante a prática esportiva (FERRY et al., 2014). Nos Estados Unidos, cerca de 500.000 indivíduos sofrem essa lesão por ano, o que gera um custo anual aproximado de US$ 4,0 bilhões (CULLEN; HALL; GOLOSINSKIY, 2009; KIM et al., 2011).

Atualmente, a cirurgia de reconstrução do LCA é o procedimento padrão em pacientes ativos com ruptura desse ligamento (KIAPOUR & MURRAY, 2014).

Apesar de a cirurgia de reconstrução do LCA restaurar a estabilidade e a homeostase articular do joelho (TIE et al., 2016), o paciente normalmente é acometido por considerável perda de massa muscular e inibição da ativação voluntária do quadríceps no período pós-operatório (OTZEL; CHOWA; TILLMAN, 2015). Como consequência, a capacidade de produção de força muscular se apresenta reduzida nos primeiros meses de pós-operatório (KRISHNAN &

WILLIAMS, 2011), havendo situações em que os déficits de força persistem por até 3 anos após a cirurgia (OTZEL; CHOW; TILLMAN, 2015), comprometendo a funcionalidade desses indivíduos (SCHMITT, PATERNO, HEWETT, 2012).

Em pacientes que apresentem lesões meniscais instáveis, com bloqueio na articulação do joelho e dores constantes, (SCOTTI et al., 2013), o tratamento cirúrgico, por meio da meniscectomia parcial torna-se necessária, tendo em vista os bons resultados no alívio da dor, na melhora da função e satisfação dos pacientes.

(OSTERAS; OSTERAS; TORSTENSEN, 2012; YIM et al., 2013). No entanto, déficits musculares e neuromusculares do quadríceps podem ser apresentados pós meniscetomia, a curto (seis meses) e longo prazo (quatro anos). (GLATTHORN et al., 2010; ERICSSON, ROOS, DAHLBERG, 2006). Estes déficits afetam negativamente a mecânica de aterrissagem em testes funcionais (HSU; GEORGE;

CHMIELEWSKI, 2016), aumentam o risco de uma lesões futuras nesta articulação (PATERNO et al., 2010) e/ou o desenvolvimento de um quadro de osteoartrose no joelho operado (SEGAL & GLASS, 2011; HALL et al., 2013).

Diante dos aspectos supramencionados, o treinamento de força é um ponto

fundamental dos programas de reabilitação após cirurgia de reconstrução do LCA e

meniscectomia parcial (WILK & ARRIGO, 2017; COBIAN et al., 2017). Embora seja

comumente realizado com uma carga externa constante nas fases concêntrica e

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excêntrica do exercício, evidências sugerem que o treinamento puramente excêntrico ou com sobrecarga excêntrica seja capaz de otimizar as respostas musculares em relação ao ganho de força e massa muscular (DOUGLAS et al., 2017). Esse tipo de intervenção têm se mostrado eficaz no fortalecimento do quadríceps de atletas de elite (FRIEDMANN-BETTE et al., 2010), indivíduos jovens saudáveis (BARONI et al., 2013), idosos (ONAMBÉLÉ et al., 2008) e sujeitos acometidos por diferentes lesões musculoesqueléticas, como em lesões ligamentares do joelho (LCA), por meio de exercícios em cicloergômetro específico (GERBER et al., 2006; GERBER et al., 2007a; GERBER et al., 2007b; GERBER et al., 2009), exercícios convencionais com pesos livres (leg press) (LEPLEY;

WOJTYS; PALMIERI-SMITH, 2015a; LEPLEY; WOJTYS; PALMIERI-SMITH, 2015b) e exercícios isocinéticos em cadeia fechada (FRIEDMANN-BETTE et al., 2018) e aberta (BRASILEIRO et al., 2011). No entanto, de acordo com o nosso conhecimento, a literatura não apresenta relatos acerca do uso do treinamento excêntrico na reabilitação em indivíduos submetidos a meniscectomia parcial.

Até o presente momento os efeitos dos treinamentos excêntricos, isotônico e isocinético, ainda não foram comparados em estudos com metodologias padronizadas, (GHUILLEM; CORNU; GUÉVEL, 2010), como em ensaios clínicos randomizados, e, em populações submetidas a cirurgias ortopédicas. Identificando assim, uma lacuna na literatura em relação à comparação entre esses dois tipos de treinamento excêntrico em indivíduos submetidos à cirurgia no joelho, como reconstrução do LCA e meniscectomia parcial.

Assim os objetivos da presente Tese de Doutorado foram: (1) comparar os

efeitos do treinamento excêntrico convencional (carga constante) e excêntrico

isocinético na massa muscular do quadríceps, força e desempenho funcional em

atletas recreacionais após reconstrução do LCA; e (2) comparar os efeitos do

treinamento excêntrico convencional (carga constante) e excêntrico isocinético na

massa muscular do quadríceps, força e desempenho funcional em atletas

recreacionais após meniscectomia parcial.

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4 REFERÊNCIAS DA REVISÃO

BARONI, B. M.; et al. Time course of neuromuscular adaptations to knee extensor eccentric training. Int J Sports Med, v. 34, n. 10, p. 904-11. 2013.

BEAUFILS, P.; et al. Surgical Management of Degenerative Meniscus Lesions: The 2016 ESSKA Meniscus Consensus. Joints, v. 5, n. 2, p. 59-69. 2017.

BRASILEIRO, J. S.; et al. Functional and morphological changes in the quadriceps muscle induced by eccentric training after ACL reconstruction. Rev Bras Fisioter, v.

15, n. 4, p. 284-90. 2011.

COBIAN, D. G.; et al. Knee Extensor Rate of Torque Development Before and After Arthroscopic Partial Meniscectomy, With Analysis of Neuromuscular Mechanisms. J Orthop Sports Phys Ther, v. 47, n. 12, p. 945-956. 2017.

CULLEN, K. A.; HALL, M. J.; GOLOSINSKIY, A. Ambulatory surgery in the United States, 2006. Natl Health Stat Report, v. 28, n. 11, p. 1-25. 2009.

DOUGLAS, J.; et al. Chronic Adaptations to Eccentric Training: A Systematic Review. Sports Med, v. 47, n. 5, p. 917-941. 2017.

Englund, M.; et al. “Incidental meniscal findings on knee MRI in middle-aged and elderly persons”. The N Engl J Med, v. 359, n. 11, p. 1108-15. 2008.

ERICSSON, Y. B.; ROOS, E. M.; DAHLBERG, L. Muscle strength, functional performance, and self-reported outcomes four years after arthroscopic partial meniscectomy in middle-aged patients. Arthritis Rheum, v. 55, n. 6, p. 946-52.

2006.

FERRY, T.; et al. Epidemiology of acute knee injuries seen at the Emergency

Department at Umeå University Hospital, Sweden, during 15 years. Knee Surg

Sports Traumatol Arthrosc, v. 22, n. 5, p. 1149-55. 2014.

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FRIEDMANN-BETTE, B.; et al. Effects of strength training with eccentric overload on muscle adaptation in male athletes. Eur J Appl Physiol, v. 108, n. 4, p. 821-36.

2010.

FRIEDMANN-BETTE, B.; et al. Strength Training Effects on Muscular Regeneration after ACL Reconstruction. Med Sci Sports Exerc, v. 50, n. 6, p. 1152-1161. 2018.

GERBER, J. P.; et al. Early application of negative work via eccentric ergometry following anterior cruciate ligament reconstruction: a case report. J Orthop Sports Phys Ther, v. 36, n. 5, p. 298-307. 2006.

GERBER, J. P.; et al. Effects of early progressive eccentric exercise on muscle structure after anterior cruciate ligament reconstruction. J Bone Joint Surg Am, v.

89, n. 3, p. 559-570. 2007. A

GERBER, J. P.; et al. Safety, feasibility, and efficacy of negative work exercise via eccentric muscle activity following anterior cruciate ligament reconstruction. J Orthop Sports Phys Ther, v. 37, n. 1, p. 10-18. 2007. B

GERBER, J. P.; et al. Effects of early progressive eccentric exercise on muscle size and function after anterior cruciate ligament reconstruction: a 1-year follow-up study of a randomized clinical trial. Phys Ther, v. 89, n. 1, p. 51-59. 2009.

GIULIANI, J. R.; KILCOYNE, K. G.; RUE, J. P. H. Anterior cruciate ligament anatomy: a review of the anteromedial and posterolateral bundles. J Knee Surg, v.

22, n. 2, p. 148–154. 2009.

GLATTHORN, J. F.; et al. Neuromuscular function after arthroscopic partial meniscectomy. Clin Orthop Relat Res, v. 468, n. 5, p. 1336-43. 2010.

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5 CAPÍTULO I – Isokinetic eccentric training is better than constant load eccentric training on the quadriceps rehabilitation following anterior cruciate ligament reconstruction: a randomized clinical trial

(Journal of Orthopaedic & Sports Physical Therapy; Qualis: A1; Fator de impacto: 3,090)

Authors

Marlon Francys Vidmar (PT, MSc)

1,2

, Bruno Manfredini Baroni (PT, PhD)

1

, Alexandre Fróes Michelin (MD)

2

; Márcio Mezzomo (MD)

2

; Ricardo Lugokenski (MD)

2

; Gilnei Lopes Pimentel (PT, MSc)

3

; Marcelo Faria Silva (PT, PhD)

1

1

Physical Therapy Department, Graduate rogram in Reha ilitation ciences niversidade Federal de i ncias da a de de orto legre F orto Alegre, Rio grande do Sul, Brazil

2

Hospital Ortopédico (HO), Passo Fundo, Rio grande do Sul, Brazil

3

Physical Therapy Department, Universidade de Passo Fundo (UPF), Passo Fundo, Rio grande do Sul, Brazil

Ethics committee

Ethics Committee approval of the study protocol (protocol number 1.461.842).

PublicTrials Registry

Registered at Clinical Trials website (NCT02961543).

Corresponding Author:

Dr Marlon Francys Vidmar

Hospital Ortopédico, Setor Fisioterapia, Av Sete de Setembro, n 817, Centro, 99.010-121, Passo Fundo, Rio Grande do Sul, Brasil.

Email: marlonfrancys@msn.com

Ph: +55 (54) 9 9907 1273 Fax: +55 (54) 2104 4333

(24)

Title

Isokinetic eccentric training is better than constant load eccentric training on the quadriceps rehabilitation following anterior cruciate ligament reconstruction: a randomized clinical trial

Financial Disclosure and Conflict of Interest

The authors have no financial affiliation (including research funding) or involvement

with any commercial organization that has a direct financial interest in any matter

included in this manuscript.

(25)

ABSTRACT 1

STUDY DESIGN: Randomized controlled trial.

2

BACKGROUND: Eccentric training is an effective strategy after anterior cruciate 3

ligament (ACL) reconstruction, but the advantages of using isokinetic dynamometry 4

during rehabilitation remain unclear.

5

OBJECTIVES: To compare the effects of conventional (constant load) eccentric 6

training and isokinetic eccentric training on quadriceps muscle mass, strength and 7

functional performance in recreational athletes following ACL reconstruction.

8

METHODS: Thirty recreational male athletes (~25 years old) undergoing ACL 9

reconstruction received a standard rehabilitation program. Volunteers were 10

randomized to conventional group (CG; n=15) or isokinetic group (IG; n=15) to be 11

engaged in a 6-week (2 sessions/week) quadriceps eccentric training program at the 12

extensor chair or at the isokinetic dynamometer, respectively. Assessments of 13

quadriceps muscle mass, strength and functionality were performed before and after 14

training programs.

15

RESULTS: The isokinetic training led to large effect sizes for all muscle mass 16

outcomes (increases of 17-23%), as well as quadriceps strength (25-66%) and jump 17

performance (20%). The conventional training promoted small to moderate effects 18

for muscle mass outcomes (5-9%), moderate to large effect sizes for quadriceps 19

strength (16-20%), and large effect size for jump performance (15%). Both groups 20

presented large effect sizes in the Lysholm questionnaire. IG group had higher 21

changes than CG for all muscle mass outcomes (effect sizes: 0.72-1.08), Lysholm 22

questionnaire (effect size: 0.7), isometric strength (effect size: 0.71), and eccentric 23

strength (effect size: 0.96).

24

(26)

CONCLUSION: Isokinetic eccentric training promotes grater adaptations than 25

conventional eccentric training on quadriceps muscle mass and strength after ACL 26

reconstruction.

27

KEYWORDS: Knee, Anterior cruciate ligament, Quadriceps, Isokinetics, Eccentric 28

training.

29

INTRODUCTION 30

The anterior cruciate ligament (ACL) plays a fundamental role in the passive stability 31

of the knee joint by controlling rotational motion and restraining anterior translation of 32

the tibia relative to the femur.

26

Every year, over 120,000 individuals are victimized 33

by this injury in the United States,

30

which results in annual costs of approximately 34

1.7 billion dollars.

31

The ACL rupture occurs more frequently in younger more 35

physically active adults,

31

mainly professional, amateur and recreational athletes.

38

36

Despite the growing knowledge over the risk factors and strategies for prevention of 37

ACL rupture,

37

the incidence within professional athletes has not decreased in the 38

past two decades.

54

The average time to return to sport is 244 days (about eight 39

months),

48

so ACL injuries compromise team performance and club finances.

14

40

The current standard procedure to treat physically active patients with ACL rupture is 41

the ligament reconstruction surgery.

31

Although this surgery restores the knee 42

mechanical stability,

51

patients are often affected by considerable loss of muscle 43

mass and by inhibition of the voluntary activation of the quadriceps muscle during 44

post-operative period.

41

Consequently, a marked quadriceps muscle weakness is 45

expected in the initial rehabilitation phase.

32

Since strength deficits can persist for up 46

to three years after reconstruction,

41

some athletes may return to sport with strength 47

imbalances between the operated and the unaffected limb, and/or between the 48

extensor and flexor muscle groups.

33

Strength deficits have been associated to

49

(27)

alterations in knee mechanics,

12

reduction in functional performance,

49

delayed 50

return to preinjury competitive level,

1

increased risk of ligament re-injury

21

and 51

development of knee osteoarthritis.

39

52

Strength training is a fundamental stage within the rehabilitation programs following 53

ACL reconstruction.

57

Although traditional strength training is performed with the 54

same external load during the exercises‟ concentric and eccentric phases evidence 55

suggests that eccentric overload exercises optimize the muscle hypertrophy and 56

strengthening.

13

Studies that recruited healthy elderly,

40

young adults

55

and 57

athletes

15

have demonstrated higher increments in muscle mass, strength and 58

functional performance through eccentric training compared to traditional strength 59

training. Similarly, eccentric training appears to be more effective to restore 60

quadriceps muscle mass,

18,20,16

strength

19,20

and functional performance

19,20

in 61

individuals submitted to ACL reconstruction. This body of evidence supports the 62

implementation of eccentric training in rehabilitation programs of patients undergoing 63

ACL reconstruction.

17, 18, 19,20,7,34,35,16

64

The implementation of eccentric loading during ACL rehabilitation has been 65

conducted through exercises with specific cycle ergometers,

17, 18, 19,20

conventional 66

(constant load) gym machine (e.g. leg press)

34,35

and isokinetic dynamometers 67

(either in open

7

or closed

16

kinetic chain). The isokinetic dynamometer enables the 68

performance of exercises with maximal intensity and constant angular velocity along 69

the full range of motion.

56

It means the equipment allows the exercise to be 70

performed at the individual maximal muscle strength level at each joint angle, and 71

minimizes the risk of loading a ove the patient‟s tolerance.

29

Therefore, isokinetic 72

exercise has been included in rehabilitation programs in order to optimize muscle 73

strengthening, especially when treating elite athletes.

46

Nevertheless, a question

74

(28)

remains to be answered in sports physical therapy: does isokinetic exercise produce 75

larger and/or faster muscle strength gains than conventional exercise (i.e. constant 76

load) in patients following ACL reconstruction?

77

The aim of the present study was to compare the effects of conventional eccentric 78

training and isokinetic eccentric training on quadriceps muscle mass, strength and 79

functional performance in recreational athletes following ACL reconstruction. Our 80

hypothesis was that isokinetic eccentric training would lead to greater increments on 81

quadriceps muscle mass, strength and functional performance compared to 82

conventional eccentric training.

83

METHODS 84

Study design 85

The current study was a prospective randomized clinical trial and blinded for 86

assessors. All participants underwent ACL reconstruction surgery. Next, they were 87

randomized to Conventional Group (CG) or Isokinetic Group (IG). All participants 88

were engaged in a standard rehabilitation program. Approximately 45 days post- 89

surgery, they initiated either the conventional eccentric training or the isokinetic 90

eccentric training for a period of 6 weeks. Assessments of quadriceps muscle mass 91

(through magnetic resonance imaging), strength (through isokinetic dynamometry) 92

and functionality (through questionnaire and hop test) were performed one week 93

prior to eccentric training commencement and one week after conclusion. Figure 1 94

shows the study‟s flowchart. This study was approved y the institutional ethics 95

committee (protocol number 1.461.842) and previously registered at Clinical Trials 96

website. The Consolidated Standards of Reporting Trials (CONSORT) was 97

respected during the writing process of this article.

98

(29)

INSERT FIGURE 1 HERE 99

Participants 100

During the period from January to November of 2017, male subjects submitted to 101

ACL reconstruction surgery at the XXXX Hospital (XXXX, XXXX) were invited to the 102

study. To be included, participants should be 18 to 40 years old recreational athletes 103

(i.e. sports practice at least once a week), with body mass index between 18.5 and 104

24.9 Kg/m², and unilateral ACL rupture diagnosed through clinical evaluation and 105

magnetic resonance imaging. Participants were excluded in the following cases: re- 106

injury; injury event longer than 90 days; associated ligament and/or meniscal injury;

107

associated patellofemoral pain syndrome; muscle injury in the previous 6 months;

108

respiratory or cardiovascular limiting condition; consumers of ergogenic supplements 109

or anabolic steroids. All eligible participants received instructions relative to the aims 110

and procedures of the study and signed a consent form.

111

Sample size 112

The number of participants was estimated using the free-access software WinPepi 113

(Copyright JH Abramson, 2012). The knee extension peak torque is considered a 114

primary outcome in the current study, so results reported by Brasileiro et al.

7

were 115

used in the sample size estimation. Power was set as 80%, with an alpha level of 116

5%, resulting in a sample size of 15 subjects per group.

117

Randomization and blinding 118

Participants were randomly allocated in one of two groups by flipping a coin (heads - 119

CG, tails - IG). This procedure was performed by an independent researcher not 120

involved in the outcome measures. The surgeons and researchers responsible for

121

(30)

the pre and post assessments were linded for participants‟ allocation. The clinicians 122

who applied the rehabilitation protocols did not participate in the assessments.

123

ACL reconstruction surgery 124

The technique performed was ACL anatomical reconstruction through simple band 125

with autologous graft from ipsilateral knee flexor tendons (semitendinosus and 126

gracilis muscles). All surgeries were performed by the same two knee surgeons who 127

had at least 15 years of technical experience with ACL reconstruction.

58

128

Post-surgery rehabilitation 129

Following surgery, participants received a standard physical therapy protocol

53

with 130

60-minute daily sessions, from the 2

nd

to the 30

th

day after ACL reconstruction. This 131

is a post-surgery routine protocol adopted in the hospital where surgeries were 132

performed. In the present study, participant adherence was of 100% and no adverse 133

effects were reported. A synthesis of this early stage of the rehabilitation protocol is 134

presented next:

135

- Increase of knee range of motion: passive, active-assisted and active exercises of 136

knee flexion and extension, performed in three series of 10 repetitions, with 20- 137

second intervals;

138

- Increase of flexibility: static stretching for knee flexor and extensor muscles, hip 139

adductor, abductor, extensor and flexor muscles, and ankle dorsal and plantar 140

flexors, performed twice for 30 seconds each, with 30-second intervals;

141

- Neuromuscular and proprioceptive reeducation: closed kinetic chain exercises 142

progressing from bipedal to unipedal, initiating on the ground and progressing to 143

unstable devices, performed twice for 30 seconds each, with 30-second intervals;

144

- Gait retraining: exercises of lateral, anterior and posterior displacement between 145

parallel bars, performed in two series of 10 repetitions, with 60-second intervals.

146

(31)

At the end of each session, cryotherapy was applied on the affected knee for 20 147

minutes to alleviate pain and reduce edema.

148

Eccentric training programs 149

Participants allocated to the IG were engaged in an isokinetic eccentric training 150

program for the knee extensor muscles using a Biodex™ Multi Joint ystem 3 ro 151

computerized dynamometer (Biodex Medical System, United States of America).

152

They were positioned according to manufacturer‟s recommendations for knee 153

flexion-extension tests. The isokinetic eccentric training program was applied by 6 154

weeks, twice a week, with a minimal interval of 72h between sessions. Training 155

sessions were preceded by a warming protocol with 10 submaximal eccentric 156

contractions performed on the dynamometer at an angular velocity of 90°/s. In each 157

training session, participants performed three (weeks 1 to 3) or four sets (weeks 4 to 158

6) of 10 maximal intensity knee extensor eccentric contractions. A one-minute 159

resting interval was given between sets. The isokinetic eccentric contractions were 160

performed according to the protocol described by Baroni et al

2

as follows: after the 161

researcher passively positioned the participant‟s knee in 30° of flexion 0° = full knee 162

extension), the participant was encouraged to perform a maximal eccentric 163

contraction of the knee extensor muscles in order to resist against the movement of 164

knee flexion exerted by the dynamometer until 90° of knee flexion, at a 60°/s 165

constant angular velocity.

166

Participants allocated in the CG were engaged in a conventional eccentric training 167

program for the knee extensor muscles using an extensor chair (Kenkorp, Brazil).

168

Training duration, weekly frequency and volume (number of sets and repetitions) 169

were the same adopted for IG. During the eccentric exercise on the extensor chair, 170

the concentric phase (from 90° to 30° of knee flexion) was performed by a

171

(32)

researcher. From this position, participants were instructed to perform a knee 172

extensor eccentric contraction to return their legs to 90° of knee flexion in a 173

controlled manner. An electronic metronome was used to maintain a standard 174

cadence of 2 seconds for each movement phase. The load for the first training 175

session was estimated at 80% of the knee extensor eccentric torque peak using the 176

following calculation: m = 0.8T/gr (m=mass, T=torque, g=gravitational acceleration 177

and r=lever arm). The exercise load was increased progressively throughout the 178

training program according to the individual patient feedback (i.e. self-perception of 179

ability) and his muscle strength response (i.e. once the patient could perform an 11

th

180

repetition into a set, the load was increased in the next set or training session).

181

Muscle mass evaluation 182

The anatomical cross-sectional area (ACSA) of the quadriceps femoris muscle was 183

measured using images taken from participants‟ thigh through T2-weighted magnetic 184

resonance imaging (MRI) (3.0 T Magnetom, Siemens, Berlim, Germany; repetition 185

time 4,260ms, echo time 95ms, means: 3, vision field of 200 x 200, cutting thickness 186

of 4mm). Cross-sectional images were taken at 50% of the distance between the 187

minor trochanter and the lateral femoral condyle. All assessment were taken by the 188

same investigator with 12 years of experience in this evaluation. Participants were 189

instructed to avoid joining any vigorous physical activity during the 48h prior to MRI.

190

After a 10-minute resting period, participants were positioned in supine, with their 191

lower limbs fully extended and relaxed while the MRI images were obtained.

192

MRI images were analyzed using the Image-J software (National Institute of Health, 193

USA). The perimeter of each muscle (rectus femoris, vastus intermedius, vastus 194

lateralis and vastus medialis) was assessed manually by a single researcher blinded 195

to the groups allocation. The average of three measures was used for analysis.

6

The

196

(33)

quadriceps femoris‟ was estimated y summing the perimeters of these 197

muscles.

198

Muscle strength evaluation 199

The strength of the knee extensor muscles was measured using a Biodex™ Multi 200

Joint System 3 Pro computerized dynamometer (Biodex Medical System, United 201

States of America). Prior to each assessment, the equipment was calibrated and 202

participants were positioned according to manufacturer‟s recommendations.

5

All 203

participants performed a familiarization session two days before the pre-training 204

evaluation in order to minimize learning effects.

205

Each participant was warmed-up with a single set of 10 submaximal concentric 206

repetitions at 90°/s. The assessment followed the protocol adopted by Baroni et al

3

. 207

Isometric peak torque was assessed though three 5-s maximal isometric 208

contractions of the knee extensor muscles at 60° of knee flexion (0° = full extension).

209

Concentric and eccentric peak torques were measured through three maximal 210

contractions at 60°/s with ranges of motion between 90

o

to 10° and 30° to 90°, 211

respectively. Participants rested for 2 minutes between tests. A single researcher 212

with experience in isokinetic evaluation and blinded to groups allocation was 213

responsible for all assessments. He provided standard instructions, feedback and 214

encouragement during tests.

215

Functional performance evaluation 216

Functional performance was assessed using the Lysholm Score version translated to 217

Brazilian Portuguese and validated for patients with ligament injury.

42

The Lysholm 218

Score comprises eight questions that subjectively evaluate functional status in terms 219

of limp, need for cane or crutches, locking sensation, instability, pain, swelling and 220

difficulties for climbing stairs or squatting. The final score is expressed in both

221

(34)

categorical and numerical results: “excellent” for 95 to 100 points; “good” for 84 to 94 222

points; “regular” for 65 to 83 points; and “poor” for less than 64 points. single 223

evaluator was previously trained to use this tool in order to minimize gauging bias.

224

The single leg hop test was also used to asses functional performance and has 225

previously demonstrated excellent reliability for patients following ACL reconstruction 226

(CCI = 0.96).

52

For this test, participants started from a single-legged and semi-squat 227

standing position and were instructed to hop forward as far as possible, landing on 228

the same foot from which they took off. The distance between the initial and final foot 229

position was measured and the test was performed three times for each participant 230

with one-minute intervals. The longest distance of the three repetitions was taken for 231

analysis. For all participants the non-operated limb was tested first.

232

Statistical analysis 233

The Shapiro-Wilk test was used for assumption of data normality. Data were 234

expressed by mean and standard deviation. Independent t-test with a significance 235

level set as 5% α <0.05 was used to compare groups for age ody mass and 236

height.

237

Within-group analysis to verify training effects were performed with the following 238

calculations: paired sample t-test with a significance level set as 5% α <0.05 ; and 239

effect size E through the ohen‟s d [E = M

post

− M

pre

)/SD

pooled

, where M

post

is 240

the mean post-training measure, M

pre

is the mean pre-training measure, and SD

pooled

241

is the pooled standard deviation of the pre- and post-measurement], and training 242

effects were considered as “trivial” E <0.2 “small” E >0.2 “moderate” E >0.5 243

or “large” E >0.8 .

10

244

Longitudinal percent changes (pre- to post-training) were used for between-group 245

analysis. CG and IG were compared through an independent t-test, with a

246

(35)

significance level set as 5% α <0.05 . Data were also analyzed for practical 247

significance using magnitude-based inferences because traditional statistical 248

approaches often do not indicate the magnitude of an effect, which is typically more 249

relevant to sports medicine than statistical significance.

25

The chances of a possible 250

substantial effect favorable to CG or IG were calculated [ie, greater that the smallest 251

worthwhile change (0.2 multiplied by the between-subject standard deviation).

252

Quantitative chances of trivial effects and substantial effects for each group were 253

assessed qualitatively as follows: <1%, almost certainly not; 1-5%, very unlikely; 5- 254

25%, unlikely; 25-75% = possibly; 75-95% = likely; 95-99% = very likely; >99% = 255

almost certain.

4

When the CG and IG values were both >5 %, the inference was 256

classified as unclear.

4

257

RESULTS 258

There were no significant differences between CG and IG in terms of age (24.3±4.6 259

vs. 26.9±5.8 years; p=0.17), body mass (78.7±6.0 vs. 78.2±8.7 kg; p=0.84), height 260

(178.4±8.9 vs. 178.5±8.6 cm; p=0.96), or body mass index (23.7±1.2 vs. 23.4±1.0 261

kg/m

2

; p=0.670).

262

Within-group analysis of the operated limb is shown in Table 1. Significant 263

increments and large effect sizes were observed in all muscle mass outcomes, 264

muscle strength and functional performance of the operated side when comparing 265

pre and post intervention in the IG. In the CG, no significant changes were found for 266

measures of rectus femoris ACSA. The conventional training promoted moderate 267

effects for most outcomes (vastus lateralis and quadriceps ACSA, concentric and 268

eccentric peak torque, and single leg hop test), as well as small effects for vastus 269

medialis and vastus intermedius ACSA, and large effects for isometric peak torque.

270

Both groups showed significant improvements (p<0.001) with large effect sizes

271

(36)

(CG=1.78;IG=4.3) in the Lysholm questionnaire. Table 2 shows the within-group 272

analysis for the non-operated limb.

273

INSERT TABLE 1 HERE 274

INSERT TABLE 2 HERE 275

Between-groups analysis is shown in Figure 2 (null-hypothesis test) and Figure 3 276

(magnitude-based inference). IG had significant higher improvements (p<0.05) for all 277

muscle mass outcomes, as well as isometric and eccentric peak torques. The 278

magnitude-based inference supports that results „likely‟ or „very likely‟ favour IG 279

compared to CG for all outcomes, with exception of single leg hop test and 280

concentric peak torque.

281

INSERT FIGURE 2 HERE 282

INSERT FIGURE 3 HERE 283

DISCUSSION 284

This randomized clinical trial used rehabilitation programs based on eccentric 285

exercises, either in conventional (constant load) or in isokinetic conditions, to 286

improve quadriceps muscle mass, strength and functional performance of 287

recreational athletes undergoing ACL reconstruction. Both training programs 288

promoted improvements in the three analyzed domains; however, the effect 289

magnitudes were greater in IG compared to CG for most of the outcomes. Our initial

290

(37)

hypothesis was confirmed by the fact that participants trained with isokinetic 291

eccentric exercise demonstrated greater increments in quadriceps muscle mass and 292

strength in comparison to those who were trained at the extensor chair.

293

Evidence suggests that exclusively eccentric training programs or those containing 294

eccentric overloading optimize the muscle responses to strength training.

13

Although 295

the underlying mechanics remain unclear, the maximal force production capacity of 296

the skeletal muscle is higher during eccentric compared to concentric contraction.

11

297

Therefore, using the same load during both the concentric and the eccentric phases 298

leads the muscle to work in a lower relative intensity (percentage of maximal 299

capacity) during the eccentric phase than during the concentric phase.

300

Consequently, traditional strength training favours gains in concentric compared to 301

eccentric strength.

45

Moreover, the greater mechanic tension exerted on muscle 302

tissue during eccentric exercise promotes a larger exercise-induced muscle damage, 303

which is one of the key mechanisms to muscle hypertrophy.

50

The superiority of 304

eccentric training over traditional strength training has been endorsed by other 305

studies involving patients submitted to ACL reconstruction.

18,19,20

In Gerber et al

18,19

, 306

greater changes in quadriceps cross-sectional area (24% vs 9%), knee extension 307

concentric peak torque (28% vs 3%) and single leg hop distance (41% vs 9%) were 308

found in the participants trained with eccentric loading in relation to those who 309

followed traditional protocols. In contrast, a recent trial by Friedmann-Bette et al

16

310

reported no differences on muscle strengthening between eccentric training and 311

traditional strength training, despite the greater improvements in quadriceps cross- 312

sectional area following eccentric training.

313

Studies that engaged patients submitted to ACL reconstruction in eccentric training 314

programs found increases of 9-28% in quadriceps cross-sectional area,

7,17,18,16

20-

315

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Raso et al. showed that the strength produced by isometric muscle actions, concentric, eccentric, isotonic and isokinetic decreases after stopping a training program,

Na perspectiva do ensino interprofissional, da complexidade e dos desafios para reorientação da formação de estudantes na área de saúde, este trabalho pretende

Abstract – he aim of this study was to propose a mechanical device that could increase the mechanical load during the entire eccentric (ECC) action on a knee lexor machine and

Effects of isokinetic eccentric training on knee extensor and lexor torque and on gait of individuals with long term ACL reconstruction:.. A controlled

Objective: The aim of the present study was to evaluate the effects that inspiratory muscle training (IMT) and respiratory exercises have on muscle strength, peak expiratory