Efeitos da crioterapia na recuperação das alterações na

performance física e de indicadores lesão muscular induzida

por um único jogo de futebol

Dissertação apresentada com vista à obtenção do 2º Ciclo em

Desporto de Alto Rendimento da Faculdade de Desporto da
Universidade do Porto (Decreto de Lei nº. 74/2006 de 24 de
Março)

Orientador. Prof. Doutor António Ascensão

Co-Orientador. Prof. Doutor José Magalhães

Autor. Marco Alexandre de Oliveira Santo Tirso Leite

Porto, Outubro 2009

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 FICHA DE CATALOGAÇÃO

Leite, M. A. (2009). Efeitos da crioterapia na recuperação das alterações na performance física e de

indicadores lesão muscular induzida por um único jogo de futebol. Porto: M. A. Leite. Dissertação de 2º
Ciclo apresentada à Faculdade de Desporto da Universidade do Porto.

PALAVRAS-CHAVE: FUTEBOL, EXERCÍCIO INTERMITENTE, CRIOTERAPIA, LESÃO MUSCULAR,

INFLAMAÇÃO, DOR.

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4
 AGRADECIMENTOS

A elaboração e consecução do presente trabalho foram realmente possíveis pela colaboração

de um conjunto de pessoas, instituições e entidades. Assim, gostaríamos de agradecer:

Aos Professores Doutores António Ascensão e José Magalhães, orientadores desta dissertação

pela forma como me ensinaram a estudar, a analisar a literatura com carácter científico e a

perceber os verdadeiros distanciamentos entre o conhecimento científico e a realidade prática.

Pelos ensinamentos e profundas correcções e sugestões na elaboração do trabalho e, em

particular, para o determinante auxílio na construção do artigo experimental.

Ao Professor Doutor António Natal pela colaboração na componente experimental do trabalho.

Por ao longo destes anos da minha vida, enquanto profissional de futebol, se ter constituído

como alguém a quem recorri com frequência, não só para me ajudar a esclarecer dúvidas

técnicas, mas também por me ajudar no campo pessoal a tomar determinadas decisões que,

em muito, foram determinantes para que hoje olhe para trás e não me arrependa nunca de as

ter tomado, e possa olhar para a frente com optimismo e seguro de daquilo que valho, bem

como daquilo que possa vir a fazer enquanto profissional desta riquíssima área. Conselheiro?

Referência? Fisicista? Chamem o que quiserem, muito obrigado Professor.

Ao Mestre Sérgio Rúben Magalhães pela sua preciosa colaboração na visualização das lâminas

para contagem de subpopulações de leucócitos.

Ao Manu pelo suporte prático que prestou ao nosso trabalho, sempre prestável e pronto a

ajudar. Grande enfermeiro e grande amigo que ali encontrei.

5
Ao Luis Pinto, pelo grande sentido prático com que encara todos os processos, pelo rigor, pelo

profissionalismo, pelo grande conhecimento que possui dentro da sua área, pelo contributo

que deu ao nosso trabalho. Grande Pinto, obrigado.

Ao Doutor Pedro Santos, por mostrar sempre e em qualquer situação disponível para ajudar.

À Naval 1º de Maio por ter disponibilizado, dentro das suas possibilidades, todas as condições

necessárias a que o trabalho decorresse sempre sem qualquer tipo de limitações ou

sobressaltos.

Aos jogadores que participaram de forma empenhada e responsável no estudo.

Ao treinador destes jovens jogadores, um homem de inegável qualidade e de grande sentido

entreajuda, muitas vezes sacrificando o próprio treino para que todo o nosso trabalho, em

nenhuma circunstância, fosse posto em causa. Obrigado Verdete.

À família:

Ao Tone: Eu tinha sem dúvida alguma, muito para escrever, outra tese por ventura para

elaborar, onde provavelmente o título seria qualquer coisa do género como; “O verdadeiro

Amigo”; ou, “Ser amigo é ser….”, ou ainda, “ Valemos amizade dos amigos?. Seria sobre este

tipo de personagem que, por manifesta sorte, encontro em 1993 nos corredores da faculdade,

onde desde logo, vi a pureza do olhar trazido das beiras, a simpatia de um sorriso

desinteressado, a amizade no estado mais puro.”Segundo Deschamps, “ Amigos são familiares

que cada uma escolhe sozinho”, eu escolhi este para sempre, julgo que ele também me

escolheu a mim. Havia muito para escrever, obrigado Amigo.

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À Lígia por toda a tua compreensão. A ausência do marido em fases cruciais no dia-a-dia, com

prejuízo próprio, fez e faz de ti uma grande amiga. Obrigado Liginha.

A todos meus amigos.

Aos meus Pais, aos meus pilares, por tudo o que vocês sempre por mim e pelos meus fizeram e

fazem. Tenho um grande orgulho em ser vosso filho. Obrigado por tudo.

À Maria João pelo constante apoio e compreensão pelos momentos que te privei da minha

companhia, pela paciência que tens para lidar comigo em muitas situações, pelos conselhos

prudentes e pertinentes que me dás, por seres mãe e pai ao mesmo tempo na minha ausência.

Segundo Schopenhauer “ A mulher é um efeito deslumbrante da natureza”, tu és o expoente

máximo. Adoro-te

Aos meus filhos, e que forças da natureza são estes meus meninos, são neles que de uma forma

geral encontro forças para levar avante aquilo que quero. Nada me da mais satisfação do que

vos ver felizes, obrigado pelo vosso carinho, pureza, ingenuidade, obrigado pelo vosso sorriso

quando chego a casa depois de dias difíceis, enchem-me o coração de esperança. Aos melhores

filhos do mundo.

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Resumo

O objectivo do presente estudo foi avaliar os efeitos de uma sessão de crioterapia (imersão em
água fria, IAF) ou imersão em água termoneutral (IAT) realizados imediatamente após um único
jogo de futebol na recuperação da funcionalidade neuromuscular, da lesão muscular e de
marcadores de inflamação em futebolistas juniores masculinos.

Dez futebolistas juniores masculinos completaram um jogo de futebol, previamente

demonstrado como indutor de disfunção neuromuscular, incrementando os níveis de lesão e
dor musculares, foram aleatoriamente divididos em grupo IAF (10 minutos de IAF a 10°C, n=10)
e grupo IAT (10 minutos de IAT a 35°C, n=10). Foram avaliadas alterações em marcadores de
lesão muscular (creatina quinase, CK; mioglobina, Mb), inflamação (proteína C reactiva, PCR e %
de subpopulações de leucócitos), na função neuromuscular (impulsão vertical, velocidade e
força máxima isométrica do quadriceps) e na sensação retardada de desconforto muscular
(SRDM) até aos 30 minutos, e às 24 e 48 horas após o jogo.

O jogo de futebol induziu um incremento na actividade plasmática da CK (30 minutos, 24 e

48h), nas concentrações de Mb (30 minutos) e de PCR (30 minutos e 24 horas) em ambos os
grupos. Resultou, igualmente, duma diminuição significativa da impulsão vertical e da força
máxima isométrica do quadriceps e no aumento da SRDM nos dois grupos. Contudo, foram
observadas diferenças significativas entre os grupos na actividade da CK (30 minutos, 24 e 48h),
Mb (30 minutos), PCR (30 minutos, 24 e 48h), força do quadriceps (24h, bem como na SRDM
(quadriceps 24h, gastrocnemius 24h, adutores 30 minutos).

Os resultados sugerem que a IAF imediatamente após um único jogo de futebol reduz os níveis
de lesão muscular e desconforto, contribuindo possivelmente para uma mais rápida
recuperação da funcionalidade neuromuscular em jogadores de futebol.

Palavras chave: Futebol, exercício intermitente, crioterapia, lesão muscular, inflamação, dor

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Abstract

The aim of the present study was to assess the effects of a single session of cryotherapy (cold
water immersion, CWI) or control thermoneutral water immersion (TWI) immediately following
one-off soccer game on the recovery of muscle function, muscle damage and inflammation
markers in junior male soccer players.

Twenty male soccer players completed a soccer match previously demonstrated to induce
neuromuscular dysfunction, increased muscle damage and soreness, and were randomly
divided into cryotherapy (10 minutes of CWI at 10°C, n=10) and control thermoneutral (10
minutes of TWI at 35°C, n=10) groups. Alterations in muscle damage (creatine kinase, CK;
myoglobin, Mb) and inflammatory (C-reactive protein, CRP and % leukocyte subpopulations)
markers, in neuromuscular function (jump and sprint abilities and maximal isometric
quadriceps strength) and in the delayed muscle soreness (DOMS) were evaluated before, within
30 minutes, and at 24 and 48 h after the soccer match.

The soccer match induced an increase in plasma CK activity (30min, 24, 48h), myoglobin
(30min) and CRP (30min, 24h) concentrations in both treatment groups. It decreased peak jump
ability and maximal isometric quadriceps strength and increased DOMS in both groups.
However, differential alterations were observed between TWI and CWI groups in CK (30min, 24,
48h), Mb (30min), CRP (30min, 24, 48h), quadriceps strength (24h) and quadriceps (24h), calf
(24h) and adductor (30min) DOMS.

The present results suggest that CWI immediately after a one-off soccer match reduces the
levels of muscle damage and discomfort possibly contributing to a faster recovery of
neuromuscular function in soccer players.

Keywords: Soccer, intermittent exercise, cryotherapy, muscle damage, inflammation, soreness

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ÍNDICE

Agradecimentos

Resumo

Abstract

Introdução geral ------------------------------------------------------------------------------------- 13

Artigo experimental -------------------------------------------------------------------------------- 27

Referências Tese ------------------------------------------------------------------------------------- 59

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 INTRODUÇÃO GERAL

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O futebol é, indiscutivelmente, o desporto mais popular do mundo, o que pode ser ilustrado

pelas estimativas de cerca de 40 mil milhões de espectadores televisivos de finais dos

campeonatos do mundo da FIFA. O recente incremento rápido da indústria futebolística,

directa ou indirectamente implicada, tem aumentado a atractividade do desporto como

ocupação profissional para praticantes e não praticantes ao mais alto nível, nos quais o

investimento financeiro para o sucesso tem sido considerável. Por exemplo, a gestão e

orientação de equipas de alto nível contempla continuamente a prospecção de jogadores

emergentes, quer maturos desportivamente quer em desenvolvimento nos escalões mais

jovens tendo em vista o rendimento desportivo imediato e de médio prazo, mas também

perspectivando um benefício económico de futuro. Complementarmente, e em conjunto com

estas políticas, tem sido efectuado um investimento generalizado na melhoria de um conjunto

de condições que visam, em última instância, a sistematização de estratégias de melhoramento

da performance física dos jogadores.

As profundas e frequentes modificações na exigência imposta pelo futebol de hoje a diferentes

níveis levam-nos, à semelhança do que ocorre nas outras áreas de conhecimento das Ciências

do Desporto na especialidade do treino de atletas de alto rendimento, a uma série de

modificações, tanto nas suas bases e correntes teóricas, como nos seus procedimentos

metodológicos. Ainda assim, apesar dos inúmeros avanços no conhecimento apresentados nos

últimos anos, parece existir ainda um hiato entre o conhecimento teórico disponível, altamente

condicionado pelo necessário rigor metodológico nas abordagens experimentais, e a sua

aplicação prática.

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Esta modalidade tem sofrido alterações ao nível competitivo, devido ao constante aumento de

número de competições e subsequente número de jogos, encontrando-se os atletas

submetidos, invariavelmente, a um aumento da carga competitiva, com consequente

incremento da exigência física da modalidade.

As exigências do futebol dividem-se, habitualmente, em quatro componentes: Técnica, Táctica,

Social/Psicológica e Física. O futebolista ideal será aquele que consegue ter uma grande

compreensão táctica, boa habilidade técnica, ser mentalmente forte, e socialmente bem

integrado em equipa. A estas características soma-se, naturalmente, a importância da aptidão

física específica para cumprir os requisitos associados às acções para as quais os jogadores de

futebol são solicitados durante o treino e a competição. O futebol é uma modalidade

desportiva intermitente, com um perfil de actividade que contém constantes mudanças de

intensidade apresentando sem dúvida características particulares em cada movimento, sendo a

maioria das actividades composta de movimentos sem bola (Reilly, Bangsbo, & Franks, 2000). A

imprevisibilidade dos acontecimentos e acções durante uma partida exige que o atleta esteja

preparado para reagir aos mais diferentes estímulos, da maneira mais eficiente possível.

A capacidade física do futebolista de alto nível poderá dar uma indicação sobre as exigências

fisiológicas do jogo. Estas exigências são frequentemente quantificadas ou estimadas através da

avaliação da resposta fisiológica dos jogadores durante o jogo, representando de uma forma

indirecta, a intensidade geral a que o jogo é jogado. É contudo possível que o sucesso nas

acções das equipas seja alcançado, apesar do nível moderado de prontidão dos jogadores,

nomeadamente aqueles com um sentido táctico e níveis técnicos elevados que os ajudem a

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fornecer uma contribuição significativa para o sucesso da equipa durante o jogo. Se, por um

lado, este pressuposto poderá sugerir que a capacidade física individual do jogador de elite não

é o único factor determinante no rendimento das equipas, por outro lado, se um elevado

número de jogadores numa equipa apresentar níveis físicos baixos, as suas eventuais mais-

valias do ponto de vista táctico e técnico poderão não ser suficientes para compensar o nível

competitivo geral da equipa (Reilly, Bangsbo, & Franks, 2000).

Para uma melhor e mais profunda compreensão do impacto do jogo nos jogadores, tem sido

realizado um número considerável de estudos com o objectivo de avaliar as suas exigências

físicas e fisiológicas globais (Bangsbo, 1994; Bangsbo, 1997; Bangsbo, Iaia, & Krustrup, 2007;

Bangsbo, Mohr, & Krustrup, 2006; Krustrup et al., 2006; Mohr, Krustrup, & Bangsbo, 2005). Esta

análise tem sido efectuada através de estudos que recorrem à análise de tempo e movimento,

bem como à avaliação de diferentes parâmetros de performance e marcadores bioquímicos

musculares e sanguíneos, sendo que alguns deles se centraram na resposta física e fisiológica

ao longo do jogo, com especial atenção aos períodos e acções mais intensos e decisivos

(Andersson et al., 2008; Ascensao et al., 2008; Bangsbo, 1994; Bangsbo, Mohr, & Krustrup,

2006; Bradley et al., 2009; Caldwell & Peters, 2009; Carling & Bloomfield, 2008; Greig & Siegler,

2009; Ispirlidis et al., 2008; Krustrup et al., 2006; Lyons, Al-Nakeeb, & Nevill, 2006; Mohr,

Krustrup, & Bangsbo, 2003, 2005; Oliver, Armstrong, & Williams, 2008; Rahnama, Lees, & Reilly,

2006; Rahnama, Reilly, Lees, & Graham-Smith, 2003; Rampinini et al., 2008; Small,

McNaughton, Greig, & Lovell, 2009; Thorlund, Aagaard, & Madsen, 2009).

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Por exemplo, o dispêndio energético associado à competição tem sido estimado em cerca de

5700kJ num futebolista masculino de 75 kg de peso e um consumo máximo de oxigénio

(VO2máx) de 60 ml.kg-1.min-1. A taxa média de energia dispendida aproxima-se de um consumo

de oxigénio de cerca de 70% VO2máx pelo que tem sido repetidamente acentuado que a via

metabólica predominante durante a competição de futebol é a aeróbia (para refs ver Bangsbo,

Mohr, & Krustrup, 2006; Reilly, Bangsbo, & Franks, 2000). De facto, durante a maior parte do

jogo, as acções realizadas são sem bola e em média em regime fundamentalmente aeróbio,

sendo contudo as acções individuais com bola acentuadamente com predominância anaeróbia.

Tipicamente, o jogo exige em média a cada jogador um sprint all-out a cada 90 segundos e um

esforço de elevada intensidade em cada 30 segundos (Bangsbo, Mohr, & Krustrup, 2006). Assim

sendo, as actividades suportadas preferencialmente pelos sistemas anaeróbios de produção de

energia estão associadas aos momentos cruciais do jogo, contribuindo decisiva e directamente

para a garantia da posse de bola, de marcação e/ou concessão de golos.

A densidade dos compromissos competitivos ao longo de uma época de futebol é bastante

elevada, sendo o tempo de recuperação entre jogos reduzido, conduzindo habitual e

progressivamente os jogadores a condições que comprometem os seus níveis de performance

(Reilly & Ekblom, 2005). Assim sendo, o desenvolvimento de estratégias que visem recuperar o

mais rápido possível tem sido uma preocupação da comunidade desportiva e científica do

treino e fisiologia aplicada ao exercício em geral e ao futebol em particular (Reilly, 1997; Reilly

& Ekblom, 2005). De facto, o treino exaustivo e a competição sistemática induzem uma

condição genericamente denominada de fadiga muscular esquelética, nervosa e dos sistemas

metabólicos.

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O elevado número de contracções excêntricas associadas a uma forte exigência tensional e

contráctil de inúmeras acções durante o jogo, as quais resultam das permanentes travagens

para mudanças de direcção e sentido, dos saltos e recepções, remates, carrinhos e

desacelerações com alterações morfológicas, bioquímicas e funcionais que se manifestam

durante, imediatamente e no período de recuperação são demonstrativas da elevada exigência

metabólica e funcional do futebol. Este quadro parece agravado, em particular no futebol, por

este ser realizado em relva e os jogadores utilizarem um calçado bastante abrasivo e de elevada

capacidade de tracção por acção dos pitões. Estas alterações caracterizam um fenómeno

habitualmente designado por agressão-lesão muscular esquelética, o qual se encontra

associado à perda de funcionalidade neuromuscular, à ocorrência de alterações imunológicas,

alterações na homeostasia do ião cálcio, perda de integridade de membranas com consequente

libertação de proteínas citoplasmáticas, stress oxidativo, lesão muscular e sensação retardada

de desconforto ou dor musculares (Clarkson, 1992; Clarkson & Hubal, 2002; Clarkson & Sayers,

1999; Proske & Allen, 2005; Proske & Morgan, 2001). Efectivamente, as actividades com

predominância de contracções excêntricas promovem, pelos níveis de tensão a que estão

associados, micro lesões musculares com grande frequência (Armstrong, 1984, 1990;

Armstrong, Warren, & Warren, 1991). A sensação de desconforto muscular originada por este

tipo de actividades varia muito em função da intensidade e duração, podendo variar entre uma

fraqueza muscular que vai desaparecendo ao longo do dia com o desenrolar da nossa

actividade e uma severa dor que limita movimentos (Clarkson, 1992; Clarkson & Hubal, 2002).

As alterações do padrão, na sequência e recrutamento muscular podem também ocorrer,

causando stress nos tendões e ligamentos, levando a mecanismos compensatórios que estão

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associados ao aumento do risco de lesão em caso de um regresso prematuro à actividade. Esta

sensação aparece com grande incidência no inicio de época, quando os jogadores voltam de um

período de menor actividade. De salientar que, de entre os factores causadores de

comprometimento da performance física nos dias subsequentes à realização de exercício-

indutor de lesão muscular esquelética, a diminuição da amplitude articular do movimento, a

dificuldade de amortecimento do impacto no solo e a redução da força muscular têm sido os

mais considerados (Cheung, Hume, & Maxwell, 2003).

Algumas manifestações deste fenómeno, embora com uma exuberância menor

comparativamente com os exercícios de um só grupo muscular indutores de lesão muscular,

têm sido recentemente reportadas durante e após um jogo de futebol (Andersson et al., 2008;

Ascensao et al., 2008; Ispirlidis et al., 2008; Magalhaes et al., 2009; Malm, Ekblom, & Ekblom,

2004).

Assim, torna-se muito importante o período pós treino e competição, onde as estratégias e

métodos de recuperação assumem cada vez um papel mais imperativo. Uma vez que as

competições se sucedem, existe a necessidade ter todos os atletas bem recuperados para que

possam abordar os jogos/treinos seguintes o mais disponíveis possível.

Efectivamente, a maioria dos órgãos e sistemas apresentam alterações na homeostasia durante

e após o jogo de futebol. Estes incluem os sistemas de produção de energia (por exemplo,

diminuições significativas das concentrações de glicogénio muscular e hepático), no sistema

neuro-muscular esquelético, endócrino e nervoso.

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Existe, de facto, um considerável número de estratégias e mecanismos que tem vindo a ser

utilizados e estudados de forma a aliviar a severidade do desconforto muscular, bem como

restabelecer as funções musculares de uma forma rápida e eficaz. A recuperação activa, os anti-

inflamatórios não esteróides, a massagem, ultra-sons, alongamentos, dietas alimentares,

hidratação, banhos de imersão, como banhos de contraste e crioterapia são algumas técnicas

de recuperação pós exercício a que, treinadores e jogadores recorrem com alguma frequência

para atenuar o desconforto e restabelecer a performance de forma a, consequentemente,

reduzir o tempo de recuperação (Barnett, 2006; Cheung, Hume, & Maxwell, 2003; Reilly &

Ekblom, 2005; Wilcock, Cronin, & Hing, 2006).

Os métodos de recuperação activa, utilizando normalmente exercício de baixa intensidade

imediatamente após o exercício intenso, permitem remover o lactato do sangue de forma mais

rápida que os métodos de recuperação passiva (Reilly, 2005). Facilitam, também, o declínio da

temperatura corporal e da corrente sanguínea de uma forma gradual. A recuperação activa

promove uma diminuição significativa da actividade do sistema nervoso central atenuando

possíveis distúrbios no sono pós exercício (Smith & Reilly, 2004). Existe, contudo, uma sugestão

de que a recuperação activa pode beneficiar o sistema imunitário, pois a seguir a um exercício

extenuante o nosso organismo pode ficar sujeito a qualquer tipo de infecções menores, se a

temperatura corporal baixar de uma forma abrupta (Reilly,2005).

Os alongamentos são habitualmente uma modalidade utilizada durante, no pré e pós treino,

bem como durante os habituais períodos de recuperação. Tem sido recomendada como

medida preventiva do desconforto muscular, ajudando assim no alívio do espasmo muscular

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(Cheung, Hume, & Maxwell, 2003). A proposta de que os alongamentos pós exercício dos

músculos com desconforto e/ou dor podem conduzir à dispersão do edema que se encontra

acumulado junto do tecido lesionado.

Milhões de pessoas no mundo utilizam compostos anti-inflamatórios devido às suas

propriedades analgésicas na redução da dor bem como à acção anti-inflamatória, propriedades

que fizeram deles uma ferramenta atractiva no tratamento de atletas e na possível melhoria da

recuperação entre sessões de treino e competição. O seu efeito anti-inflamatório deve-se à

inibição da ciclo-oxigenase (COX), uma enzima envolvida na síntese de prostaglandinas,

potentes modeladores inflamatórios (Barnett, 2006; Cheung, Hume, & Maxwell, 2003). Apesar

de alguns trabalhos sugerirem benefícios da utilização de anti-inflamatórios na recuperação de

curto-termo da função muscular, parece não existir consenso relativamente aos seus efeitos na

força muscular e na taxa de recuperação da função muscular após exercício. O efeito analgésico

dos anti-inflamatórios na sensação dolorosa perece associado com o grau de desconforto. De

facto, a severidade do desconforto muscular encontra-se tipicamente associada ao grau de

habituação ao exercício, sendo que quanto mais inabitual, intenso e com uma incidência de

contracções excêntricas é o exercício para os sujeitos, mais elevado é o nível de desconforto.

Deste modo, parece ser sugerido que os benefícios analgésicos da utilização de anti-

inflamatórios em atletas de elite, altamente treinados e adaptados à intensidade e tipo de

contracções típicas da sua modalidade, poderão ser mínimos durante os períodos normais de

treino (Barnett, 2006).

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Uma outra modalidade de recuperação utilizada é o banho de imersão. Os banhos de imersão,

têm sido utilizados durante séculos em algumas culturas, como meio tratamento e recuperação

do bem-estar físico. Recentemente, os banhos de imersão têm ganho popularidade como meio

de recuperação após exercício. Algumas entidades médico-desportivas neozelandesas

recomendam que durante torneios com competições consecutivas em poucos dias, os

jogadores devem realizar um banho de contraste durante 5 minutos de forma diminuir o tempo

de recuperação e manter a performance (Barnett, 2006; Cheung, Hume, & Maxwell, 2003). As

alterações fisiológicas associadas aos banhos de imersão são atribuídas essencialmente aos

efeitos da pressão hidrostática e de temperatura (Wilcock, Cronin, & Hing, 2006). A pressão

hidrostática é a pressão que a água exerce no corpo quando este esta submergido. Esta pressão

leva a uma migração de fluidos das extremidades para a cavidade central. A migração destes

fluidos aumenta a movimentação de alguns substratos dos músculos, aumenta o débito

cardíaco, reduz as resistências periféricas e aumenta a habilidade de o corpo para transportar

substratos e remover produtos do metabolismo. Adicionalmente, a ausência de gravidade pode

reduzir a percepção de fadiga, bem como manter o nível de energia corporal (Wilcock, Cronin,

& Hing, 2006). Os pequenos e frequentes ciclos de acção muscular conducentes ao desconforto

muscular são tratados, frequentemente, com a utilização de deslocamentos subaquáticos

promovidos em programas de treino físico, particularmente durante reabilitação de lesões e

durante leves sessões de recuperação imediatamente após ou no dia seguinte à competição.

De entre as várias variantes dos banhos de imersão, compressão ou massagem, a imersão em

água fria, habitualmente designada por crioterapia, tem assumido um papel de destaque pela

sua utilização frequente como estratégia de recuperação pós exercício. A crioterapia, tem sido

25
largamente utilizada no tratamento imediato de lesões traumáticas e pode ser apropriada

como modalidade de recuperação após treino e competição que promovam lesão muscular

(Banfi, Melegati, & Valentini, 2007; Barnett, 2006; Cheung, Hume, & Maxwell, 2003; Eston &

Peters, 1999; Fu, Cen, & Eston, 1997; Halson et al., 2008; Howatson, Gaze, & van Someren,

2005; Ingram, Dawson, Goodman, Wallman, & Beilby, 2009; Isabell, Durrant, Myrer, &

Anderson, 1992; Meeusen & Lievens, 1986; Merrick, Rankin, Andres, & Hinman, 1999;

Montgomery et al., 2008; Sellwood, Brukner, Williams, Nicol, & Hinman, 2007; Swenson, Sward,

& Karlsson, 1996; Vaile, Halson, Gill, & Dawson, 2008a, 2008b; Wilcock, Cronin, & Hing, 2006;

Yanagisawa et al., 2003a, 2003b). No terreno, esta consiste em colocar sacos de gelo numa tina

cheia de água, onde os atletas vão imergir os membros inferiores até à bacia. O tempo de

duração que cada atleta deve permanecer dentro da tina varia no terreno entre períodos de 30

segundos, até ao tempo em que o atleta aguentar (Wilcock, Cronin, & Hing, 2006). A sensação

de dor à água fria começa aos 15°C, sendo certo que em alguns estudos a temperatura da água

é <15°C. Esta modalidade de tratamento tem sido bem aceite durante a fase aguda, bem como

durante a reabilitação. No entanto, a efectividade e as linhas de orientação desta modalidade

de recuperação são ainda limitadas visto serem obtidas através de estudos clínicos e de

investigação básica ou aplicada com modelos laboratoriais de exercício e os estudos de carácter

experimental e com valor ecológico serem de facto muito escassos. Estudos de revisão

relacionados com estratégias de combate ao desconforto muscular após exercício físico tem

sido sugerido que a investigação não suporta de forma conclusiva a eficácia da crioterapia, com

excepção do seu efeito analgésico (Barnett, 2006; Cheung, Hume, & Maxwell, 2003). Contudo,

26
importa salientar que o efeito analgésico pode permitir uma evolução na mobilização geral,

embora possa mascarar os sinais de alerta dados pela lesão muscular (Fu, Cen, & Eston, 1997).

No que diz respeito ao futebol em particular, e como foi referido anteriormente, a

predominância de contracções excêntricas em muitos dos seus movimentos, a crescente

densidade de treinos e competições bem como a intensidade dos jogos cada vez mais elevada,

justificam um investimento no estudo de estratégias adicionais de recuperação da

funcionalidade muscular, nas quais se inclui a crioterapia. Apesar das contradições na literatura

associadas a razões de carácter metodológico, nomeadamente aos indicadores e aos modelos

de exercício utilizados nos diferentes estudos, são escassos os estudos que analisam o efeito da

crioterapia na recuperação da função muscular e em indicadores de lesão muscular e

inflamação, utilizando como modelos de exercício o jogo de futebol. Alguns trabalhos recentes

têm utilizado modelos que pretendem simular o padrão de exercício típico de modalidades

intermitentes de equipa (Bailey et al., 2007; Ingram, Dawson, Goodman, Wallman, & Beilby,

2009) e muito recentemente, o efeito da imersão em água fria em marcadores de lesão

muscular, inflamação e parâmetros de percepção generalizada de fadiga foi estudado durante

um torneio de 4 jogos em 4 dias, em jogadores juniores australianos (Rowsell, Coutts, Reaburn,

& Hill-Haas, 2009). Contudo, pelo menos no contexto do futebol internacional, e na lógica

competitiva das principais competições na Europa e América do Sul, este modelo competitivo

de torneio não apresenta tanta validade ecológica, dada a “exagerada” densidade competitiva

que o caracteriza com um jogo por dia em 4 dias consecutivos. Deste modo, o efeito da

crioterapia, através de uma única imersão em água fria imediatamente após um único jogo de

futebol, na recuperação da função neuromuscular (força, velocidade e impulsão vertical), em

27
marcadores de lesão muscular (actividade plasmática da enzima creatina quinase e conteúdo

de mioglobina) e inflamação (proteína C reactiva), bem como da sensação dolorosa, avaliados

até às 48 horas de recuperação, não foi ainda estudado, pelo que se constitui como o objectivo

do presente trabalho. Este será apresentado no formato de um artigo experimental que se

segue.

28
 ARTIGO EXPERIMENTAL

29
30
Effects of cold-water immersion on the recovery from alterations in physical performance and muscle
damage induced by one-off soccer match in male players

Author: Marco Leite

Collaborators: António Natal2, Sérgio Magalhães1

Supervisors: António Ascensão1  , José Magalhães1

1
Research Centre in Physical Activity, Health and Leisure, Faculty of Sport, University of Porto,
Portugal
2
Department of Soccer, Faculty of Sport, University of Porto

 Corresponding author:
António Ascensão
Research Centre in Physical Activity, Health and Leisure
Faculty of Sport Sciences, University of Porto
Rua Dr. Plácido Costa, 91, 4200-450 Porto, Portugal
Phone: +351 225074774, Fax: +351 225500689
e-mail: aascensao@fade.up.pt

Running head: Cryotherapy and soccer-induced muscle damage

31
Abstract

The aim of the present study was to assess the effects of a single session of cryotherapy (cold water

immersion, CWI) or control thermoneutral water immersion (TWI) immediately following one-off soccer

game on the recovery of muscle function, muscle damage and inflammation markers in junior male

soccer players.

Twenty male soccer players completed a soccer match previously demonstrated to induce

neuromuscular dysfunction, increased muscle damage and soreness, and were randomly divided into

cryotherapy (10 minutes of CWI at 10°C, n=10) and control thermoneutral (10 minutes of TWI at 35°C,

n=10) groups. Alterations in muscle damage (creatine kinase, CK; myoglobin, Mb) and inflammatory (C-

reactive protein, CRP and % leukocyte subpopulations) markers, in neuromuscular function (jump and

sprint abilities and maximal isometric quadriceps strength) and in the delayed muscle soreness (DOMS)

were evaluated before, within 30 minutes, and at 24 and 48 h after the soccer match.

The soccer match induced an increase in plasma CK activity (30min, 24, 48h), myoglobin (30min) and

CRP (30min, 24h) concentrations in both treatment groups. It decreased peak jump ability and maximal

isometric quadriceps strength and increased DOMS in both groups. However, differential alterations

were observed between TWI and CWI groups in CK (30min, 24, 48h), Mb (30min), CRP (30min, 24, 48h),

quadriceps strength (24h) and quadriceps (24h), calf (24h) and adductor (30min) DOMS.

The present results suggest that CWI immediately after a one-off soccer match reduces the levels of

muscle damage and discomfort possibly contributing to a faster recovery of neuromuscular function in

soccer players.

Keywords: Soccer, intermittent exercise, cryotherapy, muscle damage, inflammation, soreness

32
Introduction

The activity of soccer players during the competitive season entails one week cycles of training,

taper, competition and recovery. At top level, this cycle is altered by several irregularities in the

competitive fixture list, being match day not necessarily the same from one week to another.

Moreover, players from top level teams may be involved in additional commitments such as

national cups and other knock-out matches, or representing their countries in international

championships. These competitive demands may impose strains to various physiological

systems, including musculoskeletal, nervous and immune, to a point where recovery strategies

post-exercise became influential in preparing the next match. In fact, when competitive

schedules are congested and/or there is a need of consecutively train both with high intensity

and volume as usually occur during more intense training camps and some pre-seasons, the

recovery process should be optimized for performance capabilities to be restored to normal as

soon as possible (Reilly and Ekblom 2005).

Despite some controversy on its effectiveness and the lack of evidence regarding the underlying

mechanisms, numerous recovery strategies have been proposed. These include, among others,

nutritional care pre, during and post-exercise, warm-down active recovery, deep-water running

and rehydration to recover body physiological homeostasis previously disturbed at various

levels by intense exercise (Reilly and Ekblom 2005). Moreover, as muscle damage is an

important limiting factor for muscle performance during the subsequent days after intense

exercise (Clarkson and Hubal 2002), different single and/or combination methods of alleviating

DOMS and associated muscle damage symptoms have been discussed, including stretching,

33
massage, compression, anti-inflammatory drugs, antioxidants, exercise and cold-water

immersion (Cheung et al. 2003; Barnett 2006).

Post-exercise cold-water immersion (cryotherapy) is widely used to treat acute traumatic injury and may

be appropriate as a recovery strategy after training and competition that cause some level of traumatic

injury, although definitive support for its successful application against exercise-induced muscle damage

remains scarce. As cold is widely accepted as an effective treatment for direct contact-induced muscle

trauma (Swenson et al. 1996), it is possible that it might have some value as a recovery strategy in field

settings where players experience acute soft-tissue injury as well as contraction-induced muscle

disarrangements that typically result in delayed onset muscle damage (DOMS) (Eston and Peters 1999;

Yanagisawa et al. 2003a; Bailey et al. 2007). Cryotherapy-induced decreased cellular, lymphatic and

capillary permeability due to vasoconstriction is also thought to reduce inflammatory response of

damaged muscle, oedema and pain perception. Actually, cold immersion has been shown to reduce cell

necrosis, neutrophil migration, as well as slow cell metabolism and nerve conduction velocity, which in

turn reduces secondary damage (Wilcock et al. 2006). There is little evidence about its effectiveness in

counteracting symptoms of muscle damage and neuromuscular dysfunction particularly that resulting

from severe eccentric exercise models used to induce DOMS (see Cheung et al. 2003; Barnett 2006).

However, there are reasons to suspect that cryotherapy may be somewhat advantageous against

muscle damage symptoms and biochemical markers when more ecological whole-body exercise models

are used (Yanagisawa et al. 2003a, b; Bailey et al. 2007; Montgomery et al. 2008). Bailey et al., (2007)

reported that a single session of cold-water immersion after the prolonged Loughborough Intermittent

Shuttle Test (LIST), a field exercise that has been suggested to simulate the activity pattern and the

workload imposed by soccer, i.e., was designed to mimic the activities performed and the distance

covered in a typical soccer match (Bishop et al. 1999; Nicholas et al. 2000), reduced some indexes of

exercise-induced muscle damage, including perceived soreness, maximal isometric voluntary

34
contraction of knee flexor muscles and muscle myoglobin release to the plasma in healthy active male

individuals. However, previous results from our group suggest some differential alterations in physical

performance indices and in markers of muscle damage and inflammation between soccer and LIST

(Magalhaes et al. 2009) and thus, an extrapolation for a more ecological approach should be carefully

done. Very recently, Rowsell et al., (2009) analyzed the effect of cold-water immersion on physical test

performance and perception of fatigue during a 4-day simulated soccer tournament in which the players

performed 4 games in 4 days, suggesting that cryotherapy had only reduced the perception of general

fatigue and muscle soreness, although no positive outcomes on neuromuscular parameters and on

indices of muscle damage and inflammation were observed. However, no data analyzing the effect of a

single session of cryotherapy treatment on the alterations of neuromuscular function, indices of muscle

damage and inflammation during the recovery from a one-off soccer match have yet been published in

soccer players, thus providing more ecologically valid information regarding the practical value of this

therapy during the recovery period from a one-off soccer match.

Therefore, the aim of the present study was to assess the effects of a single bout of cryotherapy applied

immediately following a one-off soccer game on the recovery of biochemical, neuromuscular and

perceptual markers of muscle damage.

Methods

Subjects

Twenty male junior soccer players from two national level teams participated in this study after being

informed about the aims, experimental protocol, procedures and after delivering writing consents. The

experimental protocol was approved by the local Institutional Review Board and followed the

Declaration of Helsinki of the World Medical Association for research with humans.

35
Experimental design and procedures

The general picture of the protocol is summarized in figure 1. Briefly, the participants were randomly

allocated in either thermoneutral (TWI) or cold water immersion (CWI) groups before the match. As

detailed below, biochemical, neuromuscular performance and perceived measurements were obtained

at baseline and at 30 min, 24 and 48 hours after one-off friendly soccer match.

For 2 weeks prior to data collection and during the protocol period, soccer players were instructed not

to change their normal eating habits and to refrain from additional vitamin or antioxidant dietary

supplementation. One week prior the beginning of experiments, the players, previously familiarized with

the test, performed an intermittent endurance test to evaluate their endurance intermittent

performance, the level 2 of the Yo-Yo Endurance Intermittent Test (Bangsbo 1994). Subjects were also

instructed to abstain from exhaustive exercise during the 48-h pre- and post-match, with exception of

the functional tests.

Blood samples, perceived muscle soreness and functional data (jump and 20 m sprint abilities, and

muscle strength) were assessed pre-match and 30 min, 24, 48 h of the recovery period in response to a

2x45min soccer match. On the day of the game, players arrived at the club after an overnight fast of

between 10 and 12 h. A resting blood sample was taken after subjects had been standing for at least 15

min, after which subjects consumed a light standardized meal and drink and rested for 2 h. The meal

consisted of 1.7 g white bread and 0.3 g of low-fat spread; both values are per kilogram of body mass

(Thompson et al. 2003a). Pre-match jump and sprint abilities, and muscle strength were assessed during

the 2 h period between the consumption of pre-exercise meal and the start of the soccer match. Players

were required to ingest water in a bolus equal to 5 ml. kg-1 immediately before the match and were

allowed to ingest water ad libitum during the game when possible (match interruptions).

36
For 2 days after the match, subjects returned to the club after an overnight fast and at approximately

the same time of the morning (within 1 h). A blood sample was taken from the forearm vein after the

subjects had been at complete rest for at least 15 min. Subsequently, perceived muscle soreness was

assessed and the players performed the physical performance tests as outlined below.

Figure 1. Test schedule for the whole test period. Triangle denotes the time point (immediately
after the match) where cold-water or thermoneutral immersions occurred. Downward arrows
denote the time points when sprint and jump performance, maximal isometric strength were
measured. Drop marks denote the time points when blood samples were taken. DOMS –
delayed onset muscle soreness, Yo-Yo IE2 – Yo-Yo Endurance Intermittent Test, Level 2.

Endurance intermittent exercise performance (Yo-Yo test)

One week prior to data collection, the players undertook an incremental and intermittent shuttle

running field test until exhaustion, the so-called Yo-Yo Endurance Intermittent Test - level 2 (Yo-Yo IE2),

following the instructions of the test (Bangsbo 1994). The test was preceded by a 10 min warm-up. The

Yo-Yo IE2 consisted of repeated 2x20 m runs with a progressively increased speed until exhaustion. The

speed running is low in the beginning and progressively increases as dictated by an audible cue played

37
from a CD. Subjects must be at one end of a 20-m base every time a cue is played. The test allows 5 s of

recovery after every 20-m shuttle run. The second time that subjects are unable to maintain the speed

running under the given signals the test is over, and the Yo-Yo IE2 test performance is considered as the

total distance covered. The test was performed in running lanes 2 m wide and 20 m long, marked by

cones.

Match time-motion analysis

For time motion analysis each player was video-filmed close up during the entire match in order to

evaluate possible differences in the distance covered by the players from the different groups in each

time motion category. The VHS-format movie cameras (NV-M50, Panasonic, Germany) were positioned

at the side of the pitch at the level of the halfway line, at a height of about 15 m and at an approximate

distance of 30-40 m of the touching line. The videotapes were later replayed for computerized time-

motion analyses according to the procedures described by Mohr et al. (2003). The used motor pattern

categories included standing (0 km.h-1), walking (6 km.h-1), jogging (8 km.h-1), low-speed running (12

km.h-1), moderate-speed running (15 km.h-1), high-speed running (18 km.h-1), sprinting (30 km.h-1),

sideways, and backwards (10 km.h-1) running. The match activities were later analysed considering

standing, walking, jogging, cruising, sprinting, backwards running and sideways running.

Cold-water and thermoneutral immersions

Immediately after the match, soccer players from the cryotherapy group fully submerged their lower

limbs until iliac crest in a stirred cold-water bath for 10 min. The water was maintained at a mean

temperature of 10°C by the addition of crushed ice. This cryotherapy treatment protocol was similar to

38
that used by Bailey et al., (2007). During the time of cold-water immersion, soccer players from the

control group remained at rest in the same long seated position as their cryotherapy counterparts, fully

immersing their lower limbs in a water bath at a mean temperature of 35°C. Core body temperature was

followed at regular intervals throughout the cryotherapy period. According to the same authors, ratings

of perceived coldness were assessed during treatment using a visual scale that ranged from 0 (‘‘not

cold’’) to 10 (‘‘very, very cold’’).

Delayed Onset muscle soreness (DOMS)

After the match (within 30 min after immersion) and at 24 and 48h recovery, each subject was asked to

complete a muscle soreness questionnaire, in which they rated their perceived muscle soreness on a

scale from 0 (normal absence of soreness) to 10 (very intense sore) previously used (Ascensao et al.

2008). They were instructed to rate the general soreness of the entire muscle area and were

encouraged to palpate the muscle groups during assessment. The muscle groups included on the

questionnaire were the quadriceps, harmstrings, calf and hip adductor muscles.

Blood sampling and preparations

All the venous blood samples were taken by conventional clinical procedures using EDTA as

anticoagulant. An aliquot of the whole blood was used to perform relative counts of leukocyte

subpopulations. The remaining freshly withdrawn blood was immediately centrifuged at 3000

rpm during 10 minutes for careful removal of the plasma. Plasma was separated into several

aliquots and rapidly frozen at –80°C for later biochemical analysis of myoglobin (Mb), creatine

kinase (CK) and C-reactive protein (CRP).

39
Biochemical Assays

Plasma creatine kinase (CK) activity was determined spectrophotometrically using a commercial test kit

(ABX A11A01632, Mompelier, FR). Plasma myoglobin concentration was assessed using a commercial

test kit (myoglobin bioMerieux 30446, Carnaxide, PT). CRP was spectrophotometrically measured

according to the instructions of the manufacturer (Roche Diagnostics).

Samples were analysed in duplicate and the mean of the two values was used for statistical analysis.

Whole blood smears on glass slides (VBS 655/A Microscope - Biosigma) were used for white blood cell

differential analysis. Smears were stained using Wright coloring (Merck) and air-dried. Cell differentials

were performed using an Olympus microscope equipped with 1000X oil immersion lens.

Jumping performance

Conventional squat and counter-movement vertical jumps were evaluated on a Bosco’s jumping mat

(Ergojump, Globus, Italy). The depth of the counter-movement was self-selected and represented each

players’ optimal depth for maximal jump. Each athlete performed three jumps and the best result

expressed as jump height was recorded.

20m sprint ability

Sprint ability measurements were carried out using telemetric photoelectric cells placed at 0 and 20m

(Brower Timing System, IRD-T175, Utah, USA). The players stood 1m behind the starting line, started on

a verbal signal being time activated when players cross the first pair of photocells, and then ran as fast as

40
they could to complete the 20m distance. Players completed two runs interspersed by 1 min recovery

period and the best time at each distance was registered.

Strength assessment

In order to evaluate muscle function, maximal voluntary isometric torque of quadriceps

muscles was measured using an isometric loading cell (Tempo Technologies, Globus

Ergometer). Soccer players were familiarized with the device and protocol on at least two

separate occasions before the match. They were seated on the chair at 85º inclination (external

angle from the horizontal) with stabilization straps at the trunk, abdomen and thigh to prevent

inaccurate joint movements. The knees were positioned at 90º of flexion and the axis of the

strength machine lever arm was aligned with the distal point of the lateral femoral condyle.

Subjects were also instructed to hold their arms comfortably across their chest to further

isolate knee joint flexion and extension movements. After a warm-up set of 5 sub-maximal

repetitions of knee extension at the referred angle, players completed two maximal isometric

repetitions for 5 s. Maximal voluntary contractions were separated by 60-s rest periods.

Participants were verbally encouraged and the highest performed value of both repetitions was

recorded.

Fluid loss and intake

To determine sweat loss during the soccer match, the players were weighted wearing dry

shorts immediately before and after the match using a digital weight (Tanita Scale InnerScan

41
Model BC533). The subjects were allowed to drink water ad libitum during the match, and their

water intake was recorded.

Statistics

Mean, standard deviation and standard error mean were calculated for all variables in each of the

experimental groups. A two-way repeated measure (ANOVA) was used to establish if differences exist

between treatment conditions over time. When significant F values were observed the Bonfferoni

adjustment was used for post-hoc comparisons. When there were only single comparisons, a paired

sample t-test was used to determine whether any differences between groups existed. The Statistical

Package for the Social Sciences (SPSS Inc, version 17.0) was used for all analysis. The significance level

was set at 5%.

Results

The main anthropometric and physical performance characteristics of soccer players from the

two groups are presented in table 1. No significant differences were found between groups

regarding the observed variables.

42
 Table 1. Anthropometric and physical performance characteristics of soccer players
from the two groups

TWI CWI

Age (years) 18.3±0.8 18.1±1.8

Height (cm) 180.2±0.03 181.6±0.4

Weight (kg) 70.6±5.2 68.4±3.8

Fat mass (%) 9.6±2.5 8.9±1.8

Training sessions per week (n) 6 6

Yo-Yo IE2(m) 1217.1±409.1 1321.3±224.8

Note: Values are mean and SD; TWI (thermoneutral water immersion) group, CWI (cold
water immersion) group.

In order to ascertain whether differences between groups exist regarding motor pattern categories,

time motion analysis was performed for each player. As seen in table 2, there were no significant

differences between TWI and CWI groups either with respect to low or high intensity activities analysed

by the frequency, duration and the percentage of match covered in each category.

43
Table 2. Frequency, mean duration and percent of match time spent on the considered motor
categories for each treatment group.

Backwards Sideways
Standing Walking Jogging Cruising Sprinting
running running

TWI

Frequency (n) 100.2 32.8 245.6 75.2 162.7 50.4 77.6 14.1 79.7 15.0 83.5 18.6 80.5 16.8

Mean duration
4.5 3.2 31.5 3.6 39.8 9.4 3.2 1.5 3.8 1.7 5.3 2.4 1.8 0.7
(min)

% total time 5.0 2.3 35.0 8.9 44.2 6.1 3.5 1.3 4.2 1.9 5.8 1.7 2.0 0.8

CWI

Frequency (n) 130.1 24.8 262.4 76.1 148.9 66.2 69.7 13.4 68.7 18.0 98.1 16.6 79.9 7.8

Mean duration
5.0 2.5 32.1 3.6 40.8 7.4 2.9 2.5 3.6 1.5 4.3 1.3 1.6 0.2
(min)

% total time 5.5 3.4 35.6 9.9 45.3 7.6 3.2 2.3 4.0 2.4 4.7 1.9 1.7 1.2

Note: Values are mean and SD; TWI (thermoneutral water immersion) group, CWI (cold water
immersion) group.

During immersions, perception of coldness was higher during CWI (mean 7) than during TWI (mean 0.5)

and remained elevated during the 30 minutes recovery (p<0.05).

As can be depicted from figure 2, the soccer match caused a significant increase in the plasma activity of

CK at 30 min, 24 and 48 h for both groups (p<0.05). However, the increases at 24 and 48 h were higher

in TWI than in the CWI group (2A). The levels of Mb in plasma increased in both treatment groups at 30

min, although higher in TWI than in CWI (2B). CRP levels also increased in both groups in response to

soccer match at 30 min and 24 h, and the increase was higher in TWI than in CWI (p<0.05) (2C).

44
Figure 2. Plasma creatine kinase (CK) activity (A) myoglobin (Mb) (B) and C-reactive protein (CRP)
contents (C) following one-off soccer match for thermoneutral water immersion (TWI, broken line) and
cold water immersion (CWI, solid line) groups. Values are mean and SD. * vs. baseline for both groups
(p<0.05); # vs. TWI group (p<0.05).

The relative counts of leukocyte subpopulations were also evaluated. As seen in figure 3, a significant

reduction of the % neutrophils occurred in the CWI group from 30 min to 24 and 48 h post-match (3A).

Cryotherapy induced a significant increase in the % of lymphocytes from 30 min to 24 and 48 h. A

significant reduction was observed in the % of lymphocytes of the CWI when compared to TWI at 30 min

recovery (p<0.05) (3C). No differences were observed in % monocytes between moments and groups

(3B).

45
Figure 3. Percentage of whole blood neutrophils (A), monocytes (B) and lymphocytes (C) following one-
off soccer match for thermoneutral water immersion (TWI, black squares) and cold water immersion
(CWI, white squares) groups. Values are mean and SD. * vs. baseline (p<0.05); † vs. 30 min (p<0.05); #
vs. TWI group (p<0.05).

Neuromuscular function during the recovery of soccer match was assessed in both groups through the

ability to jump and sprint as well as through the maximal isometric strength of the quadriceps muscle

group at 90º knee flexion (Figure 4). Significant decrease in squat jump was observed at 24h (4A) and in

countermovement jump performance at 24 and 48h in the TWI group (p<0.05) (4B). Only a significant

decrease was found in countermovement jump at 24 h in the CWI group (p<0.05) (4B). No significant

differences were observed between groups regarding jump ability in each analysed time point. Also,

46
soccer match did not alter sprint ability during the recovery and no differences were found between

treatment groups (4C).

The soccer game induced significant decrease in the peak quadriceps isometric strength in the TWI

group at 24 and 48 h and at 48 h in the CWI group (4D). However, strength levels at 24 h were

significantly higher in the CWI than in the TWI group (p<0.05).

Figure 4. Maximal squat (A) and countermovement (B) jump performance, sprint ability (C) and
isometric voluntary contraction (D) following one-off soccer match for thermoneutral water immersion
(TWI, broken line) and cold water immersion (CWI, solid line) groups. Values are mean and SD. * vs.
baseline for both groups (p<0.05); # vs. TWI group (p<0.05).

47
As can be observed in figure 5, the soccer match resulted in increased muscle soreness that peaked at

30 min and again at 24 h for some muscle groups such as quadriceps, hamstrings and calf. Cryotherapy

only reduced the ratings of perceived soreness at 24 h in the quadriceps and calf, and at 30 min in the

adductor muscle groups.

Figure 5. Perceived muscle soreness in quadriceps (A), hamstrings (B), calf (C) and hip adductor (D)
muscle groups following one-off soccer match for thermoneutral water immersion (TWI, black squares)
and cold water immersion (CWI, white squares) groups. Values are mean and SD. * vs. baseline for both
groups (p<0.05); † vs. 24 h (p<0.05); # vs. TWI group (p<0.05).

48
The fluid loss during the game was 0.89 ± 0.18 L vs. 0.92 ± 0.3 L, or 1.3 ± 0.4 % vs. 1.3 ± 0.3 % of the body

mass for TWI and CWI groups, respectively. The fluid intake was 0.75 ± 0.2 L vs. 0.67 ± 0.3 L. Thus, the

total fluid loss was similar between the two group treatments, respectively 1.64 ± 0.3 L vs. 1.59 ± 0.3 L,

corresponding to 2.3 ± 0.3 % vs. 2.3 ± 0.4 % of the body mass.

Discussion

Overview of principal findings

The present study was designed to examine the effect of immediate post-exercise CWI (using TWI as

control) on biomarkers of muscle damage, neuromuscular performance and on perceptual measures of

muscle soreness during the recovery period until 48 h after a one-off soccer match. The main findings of

this work were that the soccer players who underwent CWI immediately after the match reported lower

perception of quadriceps and calf DOMS at 24h, hip adductor at 30 minutes, demonstrated a temporary

recovery of MIVC at 24 h and a diminished increase in plasma CK activity up to 48 h, Mb at 30 minutes

and CRP levels up to 24 h than soccer players who were submitted to TWI. Despite the large controversy

concerning the efficacy of cryotherapy treatment against neuromuscular disturbances caused by

exercise, particularly eccentric-based exercise, these results are in the same line of similar studies using

this method to attenuate the neuromuscular and biochemical signs of muscle damage in exercise

models that are close to the specific demands of intermittent team sports such as basketball or soccer

(Bailey et al. 2007; Montgomery et al. 2008; Ingram et al. 2009; Rowsell et al. 2009). Of much consensus

is the effect of immediate cooling in the reduction of the levels of perceived soreness and general

49
fatigue after and throughout recovery from exercise (Bailey et al. 2007; Rowsell et al. 2009), which

corroborates the present data.

The compressive effects of hydrostatic pressure exerted on body during water immersion are thought to

create a displacement of fluids from periphery to the central cavity, resulting in multiple physiological

changes (Wilcock et al. 2006). These include increased central blood volume and extracellular fluid

volume via intracellular-intravascular osmotic gradients, and decreased peripheral resistance,

contributing to increase the removal of metabolic by-products with the potential of enhancing recovery

from exercise (Wilcock et al. 2006). However, the recovery benefits from cold observed here are most

likely due to water temperature rather than hydrostatic pressure, given that a group of TWI was used as

control.

Specific endurance of the players and match intensity

Two important factors that could influence the results in these kind of studies might be associated with

(i) the possible distinct specific physical endurance ability of the players to intermittently exercise and

the also, (ii) potentially different distance covered by the players from the two groups in the different

locomotive categories during the match. In fact, it is well described that the ability to perform high

intensity activities during soccer match is significantly correlated with the endurance intermittent

performance, evaluated for instance by Yo-Yo tests, being the differences in the response to this test

sensitive to playing positions, i.e., defenders and forwards vs. fullbacks and midfielders (Krustrup et al.

2003). Moreover, the players’ level is also known to determine the match performance with respect to

the different locomotive categories of analysis. Top-class players cover higher total distance as well as

higher distances in elevated intensity activities (sprinting, backwards and high speed running) known to

be closely related to muscle damage, than moderate soccer players and thus, are less susceptible to

50
fatigue (Mohr et al. 2003). In the present study, we therefore determined the endurance intermittent

capacity of the players from the two groups through the Yo-Yo Endurance Intermittent Test and also

analyzed the activity profile of the players during the game using time motion methodology. As there

were no significant differences between groups regarding both Yo-Yo performance and locomotive

categories during the match, it is likely that these two factors did not contribute to the observed

differences during the recovery from one-off soccer match, being the effects attributed to a great extent

to the cryotherapy treatment.

Apart from some physical performance indices such as sprint ability that did not reach statistical

significance, the present match induced a decline in physical performance that was accompanied by

increased levels of muscle damage and perceived soreness. These data are consistent with those

reported in recent studies that analyzed the response of performance indices, muscle damage,

inflammation as well as oxidative stress and damage markers of male and female soccer players during

the recovery from a match (Andersson et al. 2008; Ascensao et al. 2008; Ispirlidis et al. 2008; Magalhaes

et al. 2009).

Biochemical markers

The levels of both CK and Mb in plasma have been reported to characterize muscle membrane

disruption and have also been extensively used within the literature as biomarkers of myofibrillar

damage (Clarkson and Sayers 1999; Clarkson and Hubal 2002). The effectiveness of cold water therapies

on the appearance of intracellular proteins in plasma during the recovery from exercise-induced muscle

damage are still a matter of controversy with data evidencing beneficial and no effect of these

treatments when both conventional severe single muscle groups or overall body are used as exercise

models (Isabell et al. 1992; Eston and Peters 1999; Howatson et al. 2005; Bailey et al. 2007; Banfi et al.

51
2007; Sellwood et al. 2007; Halson et al. 2008; Montgomery et al. 2008; Vaile et al. 2008a, b; Ingram et

al. 2009; Rowsell et al. 2009).

Probably due to the different blood kinetics and to inter-individual variability of some of these proteins,

it is suggested that the release in response to exercise is protein-specific (Lee and Clarkson 2003; Bailey

et al. 2007). Moreover, due to its referred inter-subjects variation, caution in the interpretation of

plasma CK activity as a marker of muscle damage is advised. For instance, Lee and Clarkson (2003)

reported an association between the plasma glutathione content of the subjects and the variation of CK

activity in response to eccentric exercise. It is however worth noting that this widely described inter-

individual variation in response of CK activity was not observed in the players of the present study

during the recovery following the match.

Our data demonstrated that CWI was able to significantly attenuate the increased levels of plasma CK

and Mb observed after a one-off soccer match (Fig 2A and 2B). These results are in agreement with

those from Bailey et al., (2007) for Mb but not for CK after a prolonged shuttle test designed to simulate

a soccer game. On the other hand, Banfi et al., (2007) suggested that CWI accompanied by active

recovery stabilises CK activity in top-level rugby players and can be effective for improving recovery.

Very recently, others have reported no effect of CWI in the response of muscle damage and

inflammation markers throughout a simulated tournament composed of 4 competitive soccer matches

in 4 consecutive days or during the recovery following exhaustive simulated team sports exercise

(Ingram et al. 2009; Rowsell et al. 2009).

It is still unclear what is/are the mechanism(s) responsible for the lower exercise-induced intracellular

protein release to the plasma following CWI treatment. It has been suggested that cryotherapy might

reduce the post-exercise protein efflux from the muscle into the lymphatic system or a reduction in the

amount of post-exercise damage. It is likely that this indirect indication of lower muscle damage could

52
be associated with a decreased vessels permeability probably due to an effect of cryotherapy on the

attenuation of the inflammatory response (Eston and Peters 1999). Accordingly, in the present study, an

attenuated CRP response after soccer match in CWI compared with TWI treated group was observed

(Fig 2C). In fact, one of the major characteristics of the inflammatory response resulting from exercise-

induced muscle injury is the increase in the permeability of vessel walls. Given that CK diffuses into the

lymph vessels, it is possible that a reduced permeability of these vessel walls induced by CWI reduced

the rate of CK efflux from the muscle. However, other factors in addition to slower CK efflux from the

muscle might be involved as increased Mb content was also attenuated following the match in CWI

group. Further analysis of direct histological markers of muscle damage resulting from this type of

therapies should be of interest as they would provide direct evidence of cryotherapy effects against

muscle damage.

Despite the mechanisms are still unidentified, the prolonged intramuscular cooling effect after CWI on

the reduction of muscle damage is also suggested to have a role (Meeusen and Lievens 1986). It is

known the importance of inflammation-dependent secondary damage in the subsequent periods after

eccentric exercise (Lapointe et al. 2002a; Lapointe et al. 2002b) and cryotherapy retardation effect on

this damage (Merrick et al. 1999). However, besides the decreased percentage of lymphocytes at 30

minutes recovery in CWI compared with TWI group, no other significant differences between treatment

groups were observed with respect to percentage of blood neutrophils and monocytes at any recovery

time points (Fig 3).

The relationship between immune response, inflammation and muscle adaptation should be analysed

with caution and further dose-response studies are needed to clarify this particular physiological issue

(Malm 2001; Lapointe et al. 2002a; Lapointe et al. 2002b; Malm et al. 2004).

53
Neuromusclular function

The impairment of neuromuscular function after exercise in general, and particularly following soccer

match, evaluated through jump and sprint abilities and through maximal voluntary generated strength,

are frequently used as reliable measurement tools for quantifying exercise-induced muscle damage

(Warren et al. 1999). This is supported by the consistent decrease in the performance of neuromuscular

parameters considered in the present study in response to soccer match, and is accordance with other

previous studies (Andersson et al. 2008; Ascensao et al. 2008; Ispirlidis et al. 2008; Magalhaes et al.

2009; Rowsell et al. 2009).

Cold water immersion treatment following soccer match resulted in a transient attenuation observed at

24h of MIVC, but not of sprint and jump abilities (Fig 4). These findings seem to corroborate the specific

sensitivity of a more contractile-dependent muscular performance test such as MIVC compared with

sprint and vertical jump assessments (Warren et al. 1999; Bailey et al. 2007). Accordingly, Rowsell et al.,

(2009) did not find any significant treatment effect of CWI against the decrements in the repeated sprint

and countermovement jump abilities caused by successive soccer matches, supporting together with

our data, the increased sensitivity of MIVC. However, this lack of treatment efficacy against sprint

abilities conflicted with the facilitated return of repeated sprint performance to baseline of CWI group

vs. controls and hot/cold contrast water immersion recently reported during the recovery from

exhaustive simulated team sports exercise (Ingram et al. 2009). Of note is the reported value of

repeated sprint ability performance as a highly valid measure of soccer match-related physical

performance (Rampinini et al. 2007).

54
Perceived soreness

In the present study, we evaluated the perceived soreness reported by the players from four different

lower limb muscle groups implicated in soccer motor activities, namely quadriceps, hamstrings, calf and

hip adductors. Our results show that CWI group reported less DOMS in hip adductors at 30 min, and in

calf and quadriceps at 24h compared with TWI at the same time points (Fig 5).

The increase in muscle soreness observed following exercise is known to have a biphasic pattern: (i)

immediately after exercise due to tissue oedema and/or accumulation of metabolic and contraction-

related by-products and (ii) delayed soreness associated with inflammatory response and muscle

damage (Cheung et al. 2003). With the exception of hip adductors, no treatment effect against acute

onset muscle soreness was observed with respect to the other assessed muscle groups.

The precise mechanisms of cooling effects on the reported perception of muscle soreness and pain are

still unclear. The most consensual mechanism associated with cooling-induced reduction of pain

perception is attributed to its analgesic effect. In fact, muscle tissue temperatures around 10-15°C

reduced nerve conduction velocity, mechanoreceptor activity including muscle spindles with consequent

blunted stretch-reflex response and inhibition of pain-spasm cycle (Meeusen and Lievens 1986).

However, as the duration of these analgesic-related neural mechanisms is limited to 1-3 h, it is likely that

this might only account for the attenuated DOMS observed at 30 min after the end of the match. Other

potential benefit of muscle cooling in combination with immersion-related changes in hydrostatic

pressure could be associated with the decrease in tissue oedema (Wilcock et al. 2006).

In general, our data are in the same line of others showing beneficial effects of CWI against the

increased DOMS and general fatigue perception observed after several models of intermittent field

exercise-induced muscle damage, including soccer match (Bailey et al. 2007; Montgomery et al. 2008;

Ingram et al. 2009; Rowsell et al. 2009). In fact, subjective reports of faster recovery are commonly

55
observed following CWI. It is however important to note that this type of studies does not incorporate a

placebo control for cooling conditions and thus a treatment effect cannot be dismissed, with athletes

commonly reporting enhanced feelings of alertness following CWI. There are evidences that athletes

perform better when they believe they are involved in beneficial treatments (Beedie and Foad 2009),

being likely that the enhanced perceptions of recovery from increased DOMS after soccer match

observed in the current study might have occurred.

Concluding remarks

From a practical point of view, it is of note that, in addition to the beneficial outcomes on the recovery

of muscle performance and perceptual measurements of muscle discomfort, some disadvantageous

results regarding immediate post-exercise forearm and leg cooling against endurance and resistance

training effects on muscle performance and circulatory adaptation were recently described (Yamane et

al. 2006). The possible effects of cooling on the modulation of immune response, hyperthermia and

vasodilatation-induced capillary permeability and variations in oxygen tension with consequent

regulation of endothelial nitric oxide synthase expression and subsequent release of the endothelium-

derived relaxing factor nitric oxide, cytokine release, vascular endothelial growth factor and heat-related

heat shock protein over expression (Liu et al. 1999; Malm 2001; Harris et al. 2003; Thompson et al.

2003b) as a consequent of exercise should be balanced. Consequently, further research is needed to

analyse both advantages and disadvantages of cooling effects after exercise, targeting the molecular

mechanisms associated with muscle repair.

Regardless the caution and the non definitive clues on the effectiveness with respect to molecular

mechanisms behind muscle adaptation and regeneration after exercise, the present results suggest that

cryotherapy applied as an immediate single bout of CWI post- soccer match is effective in reducing some

56
biochemical, functional and perceptual signs of muscle damage. Further research with ecological value

for intermittent-based team sports such as soccer is needed to better clarify the mechanisms associated

with this possible benefit.

Acknowledgments

We would like to thank to soccer players involved in the study for their committed participation. The

authors are thankful to the excellent technical and practical assistance and skilful involvement of

Emanuel Alves and Luis Pinto. The authors are also grateful to the Labmed for the determination of

biochemical markers and to Naval 1º de Maio for providing the pitch and facilities where soccer match

and evaluations were carried out. António Ascensão is supported by a grant from the Portuguese

Foundation for Science and Technology (SFRH/BPD/42525/2007).

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