Effects of cryotherapy on muscle damage markers and perception ofdelayed onset muscle soreness after downhill running: A Pilot study

Effects   of   cryotherapy   on   muscle   damage   markers   and   perception   of delayed   onset   muscle   soreness   after   downhill   running:   A   Pilot   study

và thông tin bổ ích giúp sinh viên tham khảo, ôn luyện và phục vụ nhu cầu học tập của mình cụ thể là có định hướng, ôn tập, nắm vững kiến thức môn học và làm bài tốt trong những bài kiểm tra, bài tiểu luận, bài tập kết thúc học phần, từ đó học tập tốt và có kết quả cao cũng như có thể vận dụng tốt những kiến thức mình đã học.

RevAndal Med Deporte.
2015; :49–538(2)
w w w . e l s e v i e r . e s / r a m d
R e v i s t a A n d a l u z a d e
Medicina del Deporte
Original article
Effects of cryotherapy on muscle damage markers and perception of
delayed onset muscle soreness after downhill running: A Pilot study
M.
Rossato ,
a,
E. de Souza
Bezerra ,
a
D.A. de Ceselles Seixas da
Silva ,
a
T. Avila
Santana ,
b
W. Rafael
Malezam ,
c
F.P.
Carpes
d
a
Federal
University ofAmazonas, Manaus,Brazil
b
University
Center North,Manaus, Brazil
c
Federal
University ofSão Paulo, São Paulo, Brazil
d
Laboratory
of Neuromechanics, Federal University of Pampa,Uruguaiana, Brazil
a r t i c l e i n f o
Article history:
Received 8 November 2013
Accepted 29 July 2014
Keywords:
Inflammation
Post-exercise recovery
Fatigue
Muscle damage
a b s t r a c t
Objective: To investigate the effectsof cryotherapyon markers ofmuscle damage, as well as the perception
of muscle soreness caused by eccentricexercise after downhill running.
Methods: Ten participants (age= 26
±
5 year, height =173
±
8 cm and body mass = 70
±
4kg) performed
two running trials on a treadmill tilted –6.6%, separated byone-week period. Cryotherapy
(
15 C
for
30 minutes) was conducted after one of the trialsof exercise. Blood samples were analyzedfor markers
of muscle damage (creatine kinase CK; lactate dehydrogenase LDH; calcium
[Ca ]).
2+
Perception of
muscle soreness was quantified using an analogical scale ofpain. Data were collected before, 24and 48 h
after the trials with and without theuseof cryotherapy.
Results: Cryotherapy significantly reduced muscle soreness and was able to reestablish homeostasis in
CK, LDH and
[Ca ].
2+
Conclusion: Use of cryotherapy after exercise with eccentric contractions was effective to reestablish
the level of biochemical markers of muscle damage and reduce muscle soreness and pain perception in
subjects submittedto downhillrunning.
© 2013 Consejería de Educación, Cultura y Deporte dela Junta de Andalucía. Published by Elsevier
España, S.L.U.This isan open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Efectos de la crioterapia en los marcadores de
da ˜
no muscular y en la
percepción de mialgia de aparición tardía tras carrera en bajada
Palabras clave:
Inflamación
Recuperaciónpost-ejercicio
Fatiga
Da˜
nomuscular
r e s u m e n
Objetivo: Investigar los efectos de la crioterapia en los marcadores de
da˜
no muscular, así comola per-
cepción de mialgia causada por ejercicio excéntrico tras carrera en bajada.
Método: Diezparticipantes (edad= 26,0
±
5,0
a˜
nos, altura= 173,0
±
8,0 cm y masa corporal = 70,5
±
4,0 kg)
realizaron dosensayos de carrera entapiz rodantecon una inclinaciónde –6.6%, separadospor un periodo
de una semana. Se llevó a cabo una sesión de crioterapia
(
15 C,)
tras cada uno de los ensayos. Se
analizaron muestras de sangre para determinarlos marcadores de
da˜
no muscular (creatín kinasa–CK;
deshidrogenasa láctica–DHL; calcio- [Ca2+]). La percepción de dolormuscular fuecuantificada usando
una escala analógica dedolor. Los datos se tomaronantes, 24h y 48 h después delos ensayos con y sinel
uso de crioterapia.
Resultados: La crioterapia disminuyó significantemente el dolor muscular y fue capaz de reestablecer la
homeostasis en CK, DHLy [Ca2+].
Corresponding
author.
E-mailaddress: rossato.mateus@gmail.com (M.Rossato).
http://dx.doi.org/10.1016/j.ramd.2014.07.003
1888-7546/© 2013 Consejería de Educación, Cultura y Deporte de laJunta de Andalucía.Published by Elsevier España, S.L.U. This is an open access article under the CC
BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Document downloaded from http://www.elsevier.es, day 25/05/2015. This copy is for personal use. Any transmission of this document by any media or format is strictly prohibited.
50 M. Rossato et al. / Rev Andal Med Deporte. 2015; :49–538(2)
Conclusión: : Eluso de crioterapia tras ejercicio concontracciones excéntricas fue efectivo para reestable-
cer el nivel delos marcadores bioquímicos de
da˜
no muscular y reducir la mialgia y lapercepción dedolor
en sujetos sometidos a carrera en bajada.
© 2013 Consejería de Educación, Cultura y Deporte de la Junta de Andalucía. Publicado por Elsevier
España, S.L.U. Este es un artículo OpenAccess bajo la licenciaCC BY-NC-ND
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Palavras-chave:
Inflamac¸ão
Recuperac¸ão pós-exercício
Fadiga
Dano muscular
Efeito da imersão em agua gelada no dano muscular e dor tardia após a corrida
de downhill: um estudo piloto
r e s u m o
Introduc¸ ão: Odano muscularé frequentementeobservado em indivíduosenvolvidos em atividades físicas
que envolvam contrac¸ õesexcêntricas. Nestas situac¸ ões, a crioterapia é utilizada para reduzir o dano
muscular e a sensac¸ ão de dor. No entanto, poucos estudos investigaram o efeito da imersão em agua
gelada em marcadores dedano muscular, bemcomo a percepc¸ ão de dor apósexercício excêntrico.
Método: Dez homens (26,0
±
5,0anosde idade, 173,0
±
8,0 cm de estatura, 70,5
±
4,0kg de massa corpo-
ral). Os voluntários completaram dois corridas (teste e controle)separadaspor sete dias, emumpercurso
declinado (–6,6%) em esteira. Em uma das tentativas realizou-se imersão em água gelada
(
15 C,
30
minutos). O dano muscular foi estimado mediante os níveis sanguíneos de (creatina quinase–CK; lac-
tato desidrogenase–LDH e cálcio–[Ca2+]). A percepc¸ ão dedor muscular foi estimada usandouma escala
analógica. Todas as medidas foram realizadas antes, 24 e 48 horas pós-exercício.
Resultados: A imersão em aguagelada diminuiu significativamente a dor muscular e auxiliou no reesta-
belecimento da homeostase da CH, LDH eCa2+.
Conclusão: A imersão em agua gelada após exercício excêntrico foi efetiva em reestabelecer os níveis
bioquímicos de marcadores musculares ediminuiu a percepcao de dor.
© 2013 Consejería de Educación, Cultura y Deporte de la Junta de Andalucía. Publicado por Elsevier
España, S.L.U. Este é um artigo Open Access soba licença de CC BY-NC-ND
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction
The physiological mechanism of thedelayed onset muscle sore-
ness (DOMS) after exercise is not well
elucidated. The
1
DOMS
is more frequent and of greater magnitude after exercises with
a predominance of eccentric
contractions. Among
1
the reasons
for this association between DOMS and eccentric exercise is the
fact that eccentric actions promote greater tension to the con-
tractile apparatus with greater accumulation of metabolites and
structural damage in
tissues. The
1–3
structural damage to the
sarcolemma and Z lines of sarcomeres are often measured by
markers such as creatine kinase (CK) and lactate dehydrogenase
(LDH).
4
DOMS is largely observed among sportsmen, and it may have
deleterious effects on human
performance. The
5
performance
degradation associated with DOMS results of mechanisms such
as the loss of homeostasis of calcium
(Ca and
2+
)
6
local ele-
vation of inflammatory substances like histamine, kinins and
prostaglandins.
7
These
inflammatory substances stimulate pain
receptors types III and
IV. Thus,
5,7,8
the effect of DOMS on per-
formance rely on an increased sensitivity to touch changing
characteristics of skinsensitivity, increased muscle stiffness and
reduced range of
motion.
3,9
Several strategies have been used in order to speed up recov-
ery after exercise reducing the period and magnitude of DOMS;
some examplesare laser
therapy, massage, contrast
10 11
(heat and
cold immersion) and immersion
cryotherapy; this
12
last one is
the most popular due to the low cost and easy use by sportsmen.
The vasoconstriction of blood vessels, capillaries, and lymphatics
supportedby
cryotherapy reduces
13
thespread of fluidin the inter-
stitial spaces, thereby minimizing inflammation, pain, edema,and
muscular
spasms.
14–16
Although cryotherapy is applied to reduce the DOMS, changes
in inflammatory markers show divergent
outcomes. Ingram
12,17
et
al., Bailey
12
et
al., Eston
17
and
Peters reported
15
no changein the
concentration of CK after cryotherapy, while Riseet al. observed
reduction in the concentration of CK, myoglobin and C-reactive
protein after immersion in cold water. Part of the incongruence
concerning these studiesresults from the variety of methods used,
such as different water temperatures, immersion time, intensity
and type of exercise
performed.
19
The influence of cryotherapy on DOMS is evaluated in real
sports
context, simulations, isokinetic
18 12,17,20,21
dynamom-
etry
evaluations, after
15
a series of maximum eccentric
contractions,
11,19,22
vertical
jumps from a higher
level and
24
plyometrics.
25
Regarding the use of runningprotocols, Hausswirth et
al. com-
20
pared the effects of the application of whole-body cryotherapy,
infrared and passive recovery in a well-trained runners group on
different grounds (flat, uphill and downhill). These authors con-
cluded that whole-body cryotherapy promotes faster recovery in
comparison to other methods. However, it is known that trained
people in modalities that require predominant eccentric contrac-
tions are more resistant to the damage caused by these types of
contractions,
26
which
leads us to question ifthe applicationof post-
eccentric exercise cryotherapy could significantly affect damage
markers and pain perception in physically active people. Never-
theless, few
studies have
27
sought a significant evaluation related
to the effects of application of cryotherapy on markers of muscle
damageand muscle sorenessafter downhillrunning inpeoplecon-
sidered to be physically active.As a result ofthe increasing number
of street racing fans and the diversity of ground characteristics,
studies with this perspective are necessary since the runners are
exposed to situations of greaterdemand for eccentric contractions.
Thus, the objective of this study was to investigate the effects of
application of cryotherapyon markers of muscledamage, as wellas
the perception of muscle soreness caused predominantlyby eccen-
tric exercise after downhill running.
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M. Rossato etal. / Rev Andal Med Deporte. 2015; :49–538(2) 51
Method
Subjects
This study included 10 male volunteer subjects, healthy and
sedentary (26
±
5 years of age,173
±
8 cmheight and 70
±
4 kg body
weight). This set of subjects is similar to the ones that underwent
cryotherapy in other studies (Eston and
Peters
15
n
= 8,Ascensão
et
al.
18
n
= 10, and Santos et
al.
28
n
= 9). Subjects who have partici-
pated on this study wereinformed about the goals and methods of
the study and subsequently signed a consent form in accordance
with the local ethics committee. Subjects who reported muscu-
loskeletal problems were excluded.
Procedures
Thesubjects underwent two bouts of exercise with a predom-
inance of eccentric action (PEA) with one week interval between
bouts. In the end of one session, randomly, a treatment with
cryotherapy was applied. The perception of pain and markers of
muscle damage were measured immediately before, 24and 48 h
after the PEA.The subjects wereinstructed toavoidintense exercise
and maintainnormal diet during the previousdays to the testing.
All tests were performedin the afternoon,with a roomtemperature
of
24 C.
The PEA was performed on atreadmill, witha negative slope of
6.6%, similar to the one used by Malm et
al. The
29
protocol started
with a five-minutewarm upwalk (with noslope) at 5 km/h. After
warmingup, thetreadmill was declined andsubjects ran for25 min
at 8 km/h. After the PEA,the subjects walked for five min at 5 km/h
with no slope in orderto calm down.
The application of cryotherapy was immediately performed
after the end of one of the two sessions of PEA. Cryotherapy was
applied through theimmersion of the lower limbs into cold water
(15
±
1
C) for
25
30 min. During this period, the subjects remained
standing and hadboth legs submerged up tothe iliaccrest height.
A thermometer was used to check the temperature, which was
regulated by the addition ofice throughout the session.
Theperceptionof DOMS was assessedby a visual analogscale of
pain from 0 to 10
points, in
18
which zero indicates no pain and ten
indicates severe pain. Initially the subjects indicated the general
feelingof pain, and then reported the perceptionby muscle groups
of the lower limbs,which are ankle dorsal and plantar flexors and
knee flexors and extensors.
Samples of 10ml of venous blood were collected, centrifuged
and analyzed by spectrophotometry before exercise, 24and 48 h
after the application of cryotherapy.Blood testsallowed the analy-
sis oftheenzymes lactatedehydrogenase (LDH) and creatine kinase
(CK) using commercial kits (Labtest Diagnóstica, Lagoa Santa, MG,
Brazil). These enzymes are among thoseindicated for monitoring
muscle
injuries.
4
Analysisof data
The data were tested using Shapiro–Wilk for normality, fol-
lowed byMauchly’s test of sphericity. In order to check the effect of
350
300
250
200
150
100
50
0
0h 24h
48h
CK (IU/I)
Without cryotherapy
With cryotherapy
Fig. 1.
Concentrationof the creatinekinase (CK) in the pre-PEA (preconditions to
the exercise with predominance of eccentric action, 0 h), 24h and 48 h after PEA
conditions. * Indicates significant differences (p<0.05) for pre-PEA (0 h) and 48 h.
cryotherapyand time after treatment,as well as their interactions,
a linear mixed model of 2 factors (with and without cryotherapy;
0 h, 24 h or 48h) was usedwith Bonferroni adjustmentfor multiple
comparisons. When there was cryotherapy effect, the comparisons
were made employing Student’s
t
test for paired samples; when
there was effect on the different durations of the treatment, com-
parisons were made using the analysis of variance for repeated
measurements ANOVA. The significance level of 0.05 was used
for all analysis using a commercialstatistical package (SPSS version
13.0).
Results
The subjects reported no DOMS before starting the PEA proto-
cols. The culmination of theinduction protocol to DOMS without
the subsequent application of cryotherapy caused DOMS in 70% of
the subjects. The application of cryotherapy significantly reduced
(p
< 0.05) values of DOMS compared to the situation without
cryotherapy; no differences were observed concerning the previ-
ous situation (Table 1). In the situationwithout cryotherapy, DOMS
increased significantly after24and 48 h compared to the previous
situation; the highest valuesoccurred 24 hafter the PEA.
Reports of DOMS in different muscle groups showed a preva-
lence of the knee extensors of 71.4% opposite to the 57.1% of the
knee flexors; and a predominance of the ankle dorsal flexors of
57.1%, opposite to the28.5% ofthe ankleplantar flexors. The general
DOMS reports indicated only theknee extensor muscles.
Regarding markersof muscledamage, the plasmaconcentration
of CK in both situations was higher after 24 h, but it was onlya sig-
nificant changeinthe situationwithout cryotherapy (Fig. 1). Plasma
concentrations of LDH duringthe recovery period, regardlessof the
treatment, did not change significantly (Fig. 2). The concentrations
Table1
Scoresfor pain scale, expressed as mean
±
standard deviation for the group of subjects in the conditions with andwithout the application of cryotherapy.
Without cryotherapy Withcryotherapy
Pre 24h 48h Pre 24h 48 h
Painscale 0 6.2
±
2.4
*,#
5.3
±
2.6 0
*,#
2 0
*
Statistically
significant difference (p < 0.05) comparedto the group with cryotherapy.
#
Statistically
significant difference (p < 0.05) comparedto Pre.
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52 M. Rossato et al. / Rev Andal Med Deporte. 2015; :49–538(2)
350
300
250
200
150
100
50
0h 24h
48h
LDH (IU/I)
Without cryotherapy
With cryotherapy
0
Fig.2.
Concentration of the lactatedehydrogenase (LDH) inthe pre-PEA (precondi-
tions totheexercise with predominance of eccentric action, 0 h), 24 and 48 h after
exercise. There were nostatistically significant differences.
of blood calcium
[Ca ]
2+
were significantly higher in the situation
without cryotherapywhen compared 0 h and 48h(Fig. 3).
Discussion
This study has investigated the effects of cryotherapy on
markers of damage and muscle soreness caused by exercise pre-
dominantlyeccentric in downhill running. The results showedthat
the treatment with ice immediately after the PEAis able to reduce
and minimize DOMS effects caused by muscle damage and that
14
12
10
8
6
4
2
0
0h 24h
48h
Ca
++
(IU/I)
Without cryotherapy
With cryotherapy
Fig.3.
Concentration of calcium
[Ca ]
2+
in the pre-PEA (preconditions to theexercise
with predominance of eccentricaction, 0h), 24h and 48 h afterexercise. * Indicates
significant differences (p<0.05) compared to pre-PEA (0h).
some mechanisms associated with inflammation appear to be the
major determinants of DOMSin sedentary subjects.
The inflammatory process caused by damage to the muscle
tissue increases the concentration of pro-inflammatory chemical
mediators that stimulate pain
receptors. Although
5,7
the mech-
anisms are not yet fully elucidated, it is widely accepted that
cryotherapy has an analgesic effect. The ice seems to decrease
the ability of sensory transmission and thus reduces acetyl-
choline release influencing the pain
threshold. Yet,
19
according
to these authors, another possible benefit of cryotherapy would
be the change in hydrostatic pressure on the body, which could
be associated with a reduction in edema and pain in the mus-
cle.
When cryotherapy is used, the values found after 24 and 48 h
PEA did not differ from the preconditions. This demonstrates that
the application of cryotherapy maintains homeostasis in CK levels
after PEA. It is speculated that cryotherapy may reduce membrane
permeability and thus reduce theflow ofCK into the
interstitium.
15
However, the results found in the literature are not conclu-
sive regarding the effects of cryotherapy on CK. The differences
among the studies that concern the effectiveness of cryotherapy
on DOMS depend on the type of exercise and immersion time.
Ascensão et
al. observed
18
that,afterasoccer match,players treated
with cryotherapy
(10 C)
for 10 min decreased the concentrations
of CK after 24 and 48h compared to the control situation
(35 C).
Ingram et
al. using
12
the same temperature but with 2
×
5 min
immersions separated by 2.5 min, reported no significant differ-
ences in theconcentrations ofCK in a group of11 athletes. Goodall
and
Howatson induce
24
DOMS through jumps on downhill and
used cryotherapy
(10 C)
right after the exercise, 24 and 48h later.
The results indicated higher concentration of CKafter intervention
with cryotherapy. According to some researchers, CK shows great
variability among individuals, entailing considerableheterogeneity
between
subjects.
30,31
After PEA downhillrunning, LDH showed no significant changes
caused by cryotherapy. Although LDH is used to assess muscle
damage,
4
few
studies have evaluated the effects of cryother-
apy on its behavior. The effectsof acute intervention (first hour)
and subacute (24–168h) use of cryotherapy were analyzed and
reported that LDH was not affected significantly by the applica-
tion of cryotherapy, and that major changes were noticeable only
96 h after the harmful
stimulus. Vaile
22
et
al.
23
who
analyzed dif-
ferent hydrotherapy strategies for the recovery of muscle injuries,
also reported no differences in the concentrations of LDH, even
after 72 h. In the present study the concentrations of LDH were
checked 48h after the PEA, so we would expect that significant
increases were not noticeable and/or cryotherapy does not cause
many effects on thismarker. This suggests thatsome blood markers
can be used for evaluations of cryotherapy in acute post-exercise
recovery, while others seem to be more sensitive to medium and
long term changes.
Cryotherapy was effective in reducing the levels of calcium ion
48 hafter thePEA. This canbeexplained by the functionof cryother-
apy in reducing the plasma membrane
permeability. The
15
damage
caused byPEA results in anincreasing intracellular calciumconcen-
tration. It wouldbe associatedwith the stimulation of the autogenic
phase, increasing the actionof proteases and phospholipases, with
subsequent myofibrillar degradation especially desmine andcell,
thus triggering an inflammatory
process. This
5
increased pressure
also causes tissue edema, which activate pain receptors thereby
increasing the feeling of discomfort associated with
DOMS. The
19
ratio of intra- and extracellular calcium with the mechanism of
skeletal muscle apoptosis can lead to reduction in muscle power,
and the more releasing of inflammatory markers and DOMS, the
more muscle undergoes apoptosis thus reducing the number of
myocytes
chronically.
32
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M. Rossato etal. / Rev Andal Med Deporte. 2015; :49–538(2) 53
Ourmain conclusionis that cryotherapyafterexercise is a perti-
nent strategy to reduce DOMS andalso markers of muscle damage
for street racers who perform their training on slopes. Among the
limitationsof this study we canmention the small number of sub-
jects, and the fact that improvements in the perception of pain
reported by the subjects after treatment cannot be compared to
a placebo situation.
Our results suggest that the use of cryotherapy by immersion
for 30min at
15 C
immediatelyafter the practice of PEA reduces
the DOMS of the lower limbs, while maintaining the homeostasis
of some markers of muscle damage, such as CK and serumcalcium.
Conflict of interests
Theauthors agree that thereis no conflictof interests about this
study.
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strenuous exercise.Eur J Appl Physiol. 2003;89:53–62.
23. Vaile J, Halson S, Gill N, Dawson B. Effect of hydrotherapy on the signs and
symptoms of delayed onset muscle soreness. Eur J Appl Physiol. 2008;102:
447–55.
24. Goodall S, Howatson G. The effectsof multiple coldwaterimmersions onindices
of muscle damage. J Sports SciMed. 2008;7:235–41.
25. Howatson G, Good S, Van Someren KA.The influenceof cold water immersions
on adaptation following a single bout of damaging exercise.Eur JAppl Physiol.
2009;105:615–21.
26. Lieber RL, SameerS,Fridén J. Cytoskeletaldisruption after eccentric contraction-
induced muscle injury. Clin Orthop Relat Res. 2002;403 Suppl.:90–9.
27. Crystal NJ, Townson DH, CookSB, LaRocheDP. Effect of cryotherapy on muscle
recovery and inflammation following a bout of damaging exercise. Eur JAppl
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28. Santos WOC, Brito CJ, Júnior EAP, Valido CN, Mendes EL, Nunes MAP, et al.
Cryotherapy posttraining reduces muscle damage markers in jiu-jitsu fighters.
J Hum Sport Exerc. 2012;7:629–38.
29. Malm C,Sjodin TL,Sjoberg B,LenkeiR, Renström P, Lundberg IE,etal. Leukocytes,
cytokines, growth factors andhormones in human skeletal muscle and blood
after uphill or downhillrunning. J Physiol. 2004;556:983–1000.
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et al. The effect of an adventure race on lymphocyte and neutrophil death. Eur J
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Skeletal muscle apoptotic signaling predicts thigh muscle volume and gait
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Rev Andal Med Deporte. 2015;8(2):49–53 R e v i s t a A n d a l u z a d e Medicina del Deporte
w w w . e l s e v i e r . e s / r a m d Original article
Effects of cryotherapy on muscle damage markers and perception of
delayed onset muscle soreness after downhill running: A Pilot study M. Rossato a ∗ a a b ,
, E. de Souza Bezerra , D.A. de Ceselles Seixas da Silva , T. Avila Santana ,
W. Rafael Malezam c, F.P. Carpes d
a Federal University ofAmazonas, Manaus,Brazil
b University Center North,Manaus, Brazil
c Federal University ofSão Paulo, São Paulo, Brazil
d Laboratory of Neuromechanics, Federal University of Pampa,Uruguaiana, Brazil a r t i c l e i n f o a b s t r a c t Article history:
Objective: To investigate the effectsof cryotherapyon markers ofmuscle damage, as well as the perception Received 8 November 2013
of muscle soreness caused by eccentric exercise after downhill running. Accepted 29 July 2014
Methods: Ten participants (age= 26 ±5 year, height = 173 ±8 cm and body mass = 70 ±4kg) performed
two running trials on a treadmill tilted –6.6%, separated byone-week period. Cryotherapy (∼15 ◦C for Keywords:
30 minutes) was conducted after one of the trialsof exercise. Blood samples were analyzedfor markers Inflammation
of muscle damage (creatine kinase – CK; lactate dehydrogenase – LDH; calcium – [Ca2+]). Perception of Post-exercise recovery
muscle soreness was quantified using an analogical scale ofpain. Data were collected before, 24and 48 h Fatigue
after the trials with and without the useof cryotherapy. Muscle damage
Results: Cryotherapy significantly reduced muscle soreness and was able to reestablish homeostasis in CK, LDH and [Ca2+].
Conclusion: Use of cryotherapy after exercise with eccentric contractions was effective to reestablish
the level of biochemical markers of muscle damage and reduce muscle soreness and pain perception in
subjects submittedto downhillrunning.
© 2013 Consejería de Educación, Cultura y Deporte dela Junta de Andalucía. Published by Elsevier
España, S.L.U.This isan open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Efectos de la crioterapia en los marcadores de da ˜ no muscular y en la
percepción de mialgia de aparición tardía tras carrera en bajada r e s u m e n Palabras clave:
Objetivo: Investigar los efectosde la crioterapia en los marcadores de da ˜no muscular, así como la per- Inflamación
cepción de mialgia causada por ejercicio excéntrico tras carrera en bajada. Recuperación post-ejercicio
Método: Diez participantes (edad= 26,0± 5,0 a ˜nos, altura= 173,0 ± 8,0 cm y masa corporal = 70,5 ± 4,0 kg) Fatiga
realizaron dosensayos de carrera entapiz rodantecon una inclinaciónde –6.6%, separadospor un periodo Da˜nomuscular
de una semana. Se llevó a cabo una sesión de crioterapia (∼15 ◦C,) tras cada uno de los ensayos. Se
analizaron muestras de sangre para determinarlos marcadores de da ˜no muscular (creatín kinasa–CK;
deshidrogenasa láctica–DHL; calcio- [Ca2+]). La percepción de dolor muscular fue cuantificada usando
una escala analógica dedolor. Los datos se tomaronantes, 24h y 48 h después delos ensayos con y sin el uso de crioterapia.
Resultados: La crioterapia disminuyó significantemente el dolor muscular y fue capaz dereestablecer la
homeostasis en CK, DHLy [Ca2+]. ∗ Corresponding author.
E-mail address: rossato.mateus@gmail.com (M. Rossato).
http://dx.doi.org/10.1016/j.ramd.2014.07.003
1888-7546/© 2013 Consejería de Educación, Cultura y Deporte de laJunta de Andalucía.Published by Elsevier España, S.L.U. This is an open access article under the CC
BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Document downloaded from http://www.elsevier.es, day 25/05/2015. This copy is for personal use. Any transmission of this document by any media or format is strictly prohibited. 50
M. Rossato et al. / Rev Andal Med Deporte. 2015;8(2):49–53
Conclusión: : Eluso de crioterapiatras ejercicio concontracciones excéntricas fue efectivo parareestable-
cer el nivel delos marcadores bioquímicos de da ˜no muscular y reducir la mialgia y lapercepción dedolor
en sujetos sometidos a carrera en bajada.
© 2013 Consejería de Educación, Cultura y Deporte de la Junta de Andalucía. Publicado por Elsevier
España, S.L.U. Este es un artículo OpenAccess bajo la licencia CC BY-NC-ND
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Efeito da imersão em agua gelada no dano muscular e dor tardia após a corrida de downhill: um estudo piloto r e s u m o Palavras-chave: Inflamac¸ão
Introduc¸ ão: Odano muscularé frequentementeobservado em indivíduosenvolvidos em atividades físicas Recuperac¸ão pós-exercício
que envolvam contrac¸ õesexcêntricas. Nestas situac¸ões, a crioterapia é utilizada para reduzir o dano Fadiga
muscular e a sensac¸ão de dor. No entanto, poucos estudos investigaram o efeito da imersão em agua Dano muscular
gelada em marcadores dedano muscular, bemcomo a percepc¸ ão de dor após exercício excêntrico.
Método: Dez homens (26,0 ± 5,0anos de idade, 173,0 ±8,0 cm de estatura, 70,5 ±4,0kg de massa corpo-
ral). Os voluntários completaram dois corridas (teste e controle)separadas por sete dias, em umpercurso
declinado (–6,6%) em esteira. Em uma das tentativas realizou-se imersão em água gelada (∼15 ◦C, 30
minutos). O dano muscular foi estimado mediante os níveis sanguíneos de (creatina quinase–CK; lac-
tato desidrogenase–LDH e cálcio–[Ca2+]). A percepc¸ão dedor muscular foi estimada usando uma escala
analógica. Todas as medidas foram realizadas antes, 24 e 48 horas pós-exercício.
Resultados: A imersão em aguagelada diminuiu significativamente a dor muscular e auxiliou no reesta-
belecimento da homeostase da CH, LDH eCa2+.
Conclusão: A imersão em agua gelada após exercício excêntrico foi efetiva em reestabelecer os níveis
bioquímicos de marcadores musculares ediminuiu a percepcao de dor.
© 2013 Consejería de Educación, Cultura y Deporte de la Junta de Andalucía. Publicado por Elsevier
España, S.L.U. Este é um artigo OpenAccess sob a licença de CC BY-NC-ND
(http://creativecommons.org/licenses/by-nc-nd/4.0/). Introduction
et al.,12 Bailey etal., 17 Eston andPeters15 reported no changein the
concentration of CK after cryotherapy, while Riseet al. observed
The physiological mechanism of thedelayed onset muscle sore-
reduction in the concentration of CK, myoglobin and C-reactive
ness (DOMS) after exercise is not well elucidated.1 The DOMS
protein after immersion in cold water. Part of the incongruence
is more frequent and of greater magnitude after exercises with
concerning these studiesresults from the variety of methods used,
a predominance of eccentric contractions.1 Among the reasons
such as different water temperatures, immersion time, intensity
for this association between DOMS and eccentric exercise is the
and type of exercise performed.19
fact that eccentric actions promote greater tension to the con-
The influence of cryotherapy on DOMS is evaluated in real
tractile apparatus with greater accumulation of metabolites and
sports context,18 simulations,12,17,20,21 isokinetic dynamom-
structural damage in tissues.1–3 The structural damage to the etry evaluations,15 after a series of maximum eccentric
sarcolemma and Z lines of sarcomeres are often measured by
contractions,11,19,22 vertical jumps from a higher level24 and
markers such as creatine kinase (CK) and lactate dehydrogenase plyometrics.25 (LDH).4
Regarding the use of runningprotocols, Hausswirth et al.20 com-
DOMS is largely observed among sportsmen, and it may have
pared the effects of the application of whole-body cryotherapy,
deleterious effects on human performance.5 The performance
infrared and passive recovery in a well-trained runners group on
degradation associated with DOMS results of mechanisms such
different grounds (flat, uphill and downhill). These authors con-
as the loss of homeostasis of calcium (Ca2+)6 and local ele-
cluded that whole-body cryotherapy promotes faster recovery in
vation of inflammatory substances like histamine, kinins and
comparison to other methods. However, it is known that trained
prostaglandins.7 These inflammatory substances stimulate pain
people in modalities that require predominant eccentric contrac-
receptors types III and IV.5,7,8 Thus, the effect of DOMS on per-
tions are more resistant to the damage caused by these types of
formance rely on an increased sensitivity to touch changing
contractions,26 which leads us to question ifthe applicationof post-
characteristics of skin sensitivity, increased muscle stiffness and
eccentric exercise cryotherapy could significantly affect damage reduced range of motion.3,9
markers and pain perception in physically active people. Never-
Several strategies have been used in order to speed up recov-
theless, few studies27 have sought a significant evaluation related
ery after exercise reducing the period and magnitude of DOMS;
to the effects of application of cryotherapy on markers of muscle
some examplesare laser therapy,10 massage,11 contrast (heat and
damage and muscle sorenessafter downhillrunning inpeople con-
cold immersion) and immersion cryotherapy;12 this last one is
sidered to be physically active.As a result ofthe increasingnumber
the most popular due to the low cost and easy use by sportsmen.
of street racing fans and the diversity of ground characteristics,
The vasoconstriction of blood vessels, capillaries, and lymphatics
studies with this perspective are necessary since the runners are
supported by cryotherapy13 reduces thespread of fluidin the inter-
exposed to situations of greaterdemand for eccentric contractions.
stitial spaces, thereby minimizing inflammation, pain, edema,and
Thus, the objective of this study was to investigate the effects of muscular spasms.14–16
application of cryotherapyon markers of muscledamage, as wellas
Although cryotherapy is applied to reduce the DOMS, changes
the perception of muscle soreness caused predominantlyby eccen-
in inflammatory markers show divergent outcomes.12,17 Ingram
tric exercise after downhill running.
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M. Rossato etal. / Rev Andal Med Deporte. 2015;8(2):49–53 51 Method 350 Subjects 300
This study included 10 male volunteer subjects, healthy and
sedentary (26± 5 yearsof age, 173± 8 cmheight and70 ±4 kg body 250
weight). This set of subjects is similar to the ones that underwent
cryotherapy in other studies (Eston and Peters15 n= 8, Ascensão 200
et al.18 n = 10, andSantos et al.28 n = 9). Subjects who have partici- /I)
pated on this study wereinformed about the goals and methods of (IU K
the study and subsequently signed a consent form in accordance C 150
with the local ethics committee. Subjects who reported muscu-
loskeletal problems were excluded. 100 Procedures 50
The subjects underwent two bouts of exercise with a predom-
inance of eccentric action (PEA) with one week interval between 0
bouts. In the end of one session, randomly, a treatment with 0h 24h 48h
cryotherapy was applied. The perception of pain and markers of Without cryotherapy With cryotherapy
muscle damage were measured immediately before, 24and 48 h
Fig. 1. Concentration of the creatinekinase (CK) in the pre-PEA (preconditions to
after the PEA.The subjects wereinstructed toavoid intense exercise
the exercise with predominance of eccentric action, 0 h), 24h and 48 h after PEA
and maintainnormal diet during the previousdays to the testing.
conditions. * Indicates significant differences (p<0.05) for pre-PEA (0 h) and 48 h.
All tests were performedin the afternoon,with a roomtemperature of 24 ◦C.
cryotherapyand time after treatment,as well as their interactions,
The PEA was performed on atreadmill, witha negative slope of
a linear mixed model of 2 factors (with and without cryotherapy;
6.6%, similar to the one used by Malm etal.29 The protocol started
0 h, 24 h or 48h) was usedwith Bonferroni adjustmentfor multiple
with a five-minute warm up walk (with no slope) at 5 km/h. After
comparisons. When there was cryotherapyeffect, the comparisons
warmingup, thetreadmill was declined andsubjects ran for25 min
were made employing Student’s t test for paired samples; when
at 8 km/h. After the PEA,the subjects walked for five min at 5 km/h
there was effect on the different durations of the treatment, com-
with no slope in orderto calm down.
parisons were made using the analysis of variance for repeated
The application of cryotherapy was immediately performed
measurements – ANOVA. The significance level of 0.05 was used
after the end of one of the two sessions of PEA. Cryotherapy was
for all analysis using a commercial statistical package (SPSS version
applied through theimmersion of the lower limbs into cold water 13.0).
(15 ± 1 ◦C)25 for 30 min. During this period, the subjects remained
standing and hadboth legs submerged up to the iliac crest height. Results
A thermometer was used to check the temperature, which was
regulated by the addition ofice throughout the session.
The subjects reportedno DOMS before starting the PEA proto-
The perceptionof DOMS was assessedby a visual analogscale of
cols. The culmination of theinduction protocol to DOMS without
pain from 0 to 10 points,18 in which zero indicates no pain and ten
the subsequent application of cryotherapy caused DOMS in 70% of
indicates severe pain. Initially the subjects indicated the general
the subjects. The application of cryotherapy significantly reduced
feeling of pain, and then reported the perceptionby muscle groups
(p< 0.05) values of DOMS compared to the situation without
of the lower limbs, which are ankle dorsal and plantar flexors and
cryotherapy; no differences were observed concerning the previ- knee flexors and extensors.
ous situation (Table 1). In the situationwithout cryotherapy, DOMS
Samples of 10ml of venous blood were collected, centrifuged
increased significantly after 24and 48 h compared to the previous
and analyzed by spectrophotometry before exercise, 24and 48 h
situation; the highest valuesoccurred 24 h after the PEA.
after the application of cryotherapy.Blood testsallowed the analy-
Reports of DOMS in different muscle groups showed a preva-
sis oftheenzymes lactatedehydrogenase (LDH) andcreatine kinase
lence of the knee extensors of 71.4% opposite to the 57.1% of the
(CK) using commercial kits (Labtest Diagnóstica, Lagoa Santa, MG,
knee flexors; and a predominance of the ankle dorsal flexors of
Brazil). These enzymes are among those indicated for monitoring
57.1%, opposite to the28.5% ofthe ankleplantar flexors. The general muscle injuries.4
DOMS reports indicated only theknee extensor muscles.
Regarding markersof muscledamage, the plasmaconcentration Analysis of data
of CK in both situations was higher after 24 h, but it was onlya sig-
nificant changeinthe situation without cryotherapy(Fig. 1). Plasma
The data were tested using Shapiro–Wilk for normality, fol-
concentrations of LDH duringthe recovery period, regardlessof the
lowed byMauchly’s testof sphericity. In order to check the effect of
treatment, did not change significantly (Fig. 2). The concentrations Table 1
Scoresfor pain scale, expressed asmean ±standard deviation for the group of subjects in the conditions with andwithout the application of cryotherapy. Without cryotherapy Withcryotherapy Pre 24h 48h Pre 24h 48 h Painscale 0 6.2 ± 2.4*,# 5.3 ± 2.6*,# 0 2 0
* Statistically significant difference (p < 0.05) comparedto the group with cryotherapy.
# Statistically significant difference (p < 0.05) comparedto Pre.
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M. Rossato et al. / Rev Andal Med Deporte. 2015;8(2):49–53 350
some mechanisms associated with inflammation appear to be the
major determinants of DOMS in sedentary subjects.
The inflammatory process caused by damage to the muscle 300
tissue increases the concentration of pro-inflammatory chemical
mediators that stimulate pain receptors.5,7 Although the mech-
anisms are not yet fully elucidated, it is widely accepted that 250
cryotherapy has an analgesic effect. The ice seems to decrease
the ability of sensory transmission and thus reduces acetyl-
choline release influencing the pain threshold.19 Yet, according 200 /I)
to these authors, another possible benefit of cryotherapy would (IU H
be the change in hydrostatic pressure on the body, which could D L
be associated with a reduction in edema and pain in the mus- 150 cle.
When cryotherapy is used, the values found after 24 and 48 h 100
PEA did not differ from the preconditions. This demonstrates that
the application of cryotherapy maintains homeostasis in CK levels
after PEA. It is speculated that cryotherapy may reduce membrane 50
permeability and thus reduce theflow ofCK into the interstitium.15
However, the results found in the literature are not conclu-
sive regarding the effects of cryotherapy on CK. The differences 0
among the studies that concern the effectiveness of cryotherapy 0h 24h 48h
on DOMS depend on the type of exercise and immersion time. Without cryotherapy With cryotherapy
Ascensão etal.18 observed that,after asoccer match, players treated ◦
Fig. 2. Concentration of the lactatedehydrogenase (LDH) inthe pre-PEA (precondi-
with cryotherapy (10 C) for 10 min decreased the concentrations
tions to the exercise with predominance of eccentric action, 0 h), 24 and 48 h after
of CK after 24 and 48h compared to the control situation (35 ◦C).
exercise. There were nostatistically significant differences.
Ingram et al.12 using the same temperature but with 2 × 5 min
immersions separated by 2.5 min, reported no significant differ-
ences in theconcentrations ofCK in a group of11 athletes. Goodall
of blood calcium [Ca2+] were significantly higher in the situation
and Howatson24 induce DOMS through jumps on downhill and
without cryotherapywhen compared 0 h and 48h (Fig. 3).
used cryotherapy (10 ◦C) right after the exercise, 24 and 48h later.
The results indicated higher concentration of CKafter intervention Discussion
with cryotherapy. According to some researchers, CK shows great
variability among individuals,entailing considerableheterogeneity
This study has investigated the effects of cryotherapy on between subjects.30,31
markers of damage and muscle soreness caused by exercise pre-
After PEA downhillrunning, LDH showed no significant changes
dominantlyeccentric in downhill running. The results showedthat
caused by cryotherapy. Although LDH is used to assess muscle
the treatment with ice immediately after the PEAis able to reduce
damage,4 few studies have evaluated the effects of cryother-
and minimize DOMS effects caused by muscle damage and that
apy on its behavior. The effects of acute intervention (first hour)
and subacute (24–168h) use of cryotherapy were analyzed and
reported that LDH was not affected significantly by the applica- 14
tion of cryotherapy, and that major changes were noticeable only
96 h after the harmful stimulus.22 Vaile et al.23 who analyzed dif-
ferent hydrotherapy strategies for the recovery of muscle injuries, 12
also reported no differences in the concentrations of LDH, even
after 72 h. In the present study the concentrations of LDH were
checked 48h after the PEA, so we would expect that significant 10
increases were not noticeable and/or cryotherapy does not cause
many effects on thismarker. This suggests thatsome blood markers
can be used for evaluations of cryotherapy in acute post-exercise 8 /I)
recovery, while others seem to be more sensitive to medium and (IU+ long term changes. + aC
Cryotherapy was effective in reducing the levels of calcium ion 6
48 h after thePEA. This canbeexplained by the function of cryother-
apy in reducing the plasma membrane permeability.15 The damage
caused byPEA results in anincreasing intracellular calciumconcen- 4
tration. It wouldbe associatedwith the stimulation of the autogenic
phase, increasing the actionof proteases and phospholipases, with 2
subsequent myofibrillar degradation – especially desmine andcell,
thus triggering an inflammatory process.5 This increased pressure
also causes tissue edema, which activate pain receptors thereby 0
increasing the feeling of discomfort associated with DOMS.19 The 0h 24h 48h
ratio of intra- and extracellular calcium with the mechanism of Without cryotherapy With cryotherapy
skeletal muscle apoptosis can lead to reduction in muscle power,
and the more releasing of inflammatory markers and DOMS, the
Fig. 3. Concentration of calcium [Ca2+]in the pre-PEA (preconditions to theexercise
with predominance of eccentricaction, 0h), 24h and 48 h after exercise. * Indicates
more muscle undergoes apoptosis – thus reducing the number of
significant differences (p<0.05) compared to pre-PEA (0 h). myocytes chronically.32
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M. Rossato etal. / Rev Andal Med Deporte. 2015;8(2):49–53 53
Ourmain conclusionis that cryotherapyafterexercise is a perti-
14. Eston RG, Mickleborough J, Baltzopoulos V. Eccentric activation and muscle
nent strategy to reduce DOMS andalso markers of muscle damage
damage: biomechanical andphysiological considerations during downhillrun-
for street racers who perform their training on slopes. Among the
ning. Br J Sports Med. 1995;29(2):89–94.
15. Eston R,Peters D. Effects of cold water immersion on the symptoms of exercise-
limitationsof this study we canmention the small number of sub-
induced muscle damage.J SportsSci. 1999;17(3):231–8.
jects, and the fact that improvements in the perception of pain
16. Sellwood KL, Brukner P, Williams D, Nicol A, Hinman R. Ice-water immersion
and delayed-onset muscle soreness:a randomised controlled trial. Br J Sports
reported by the subjects after treatment cannot be compared to Med. 2007;41(6):392–7. a placebo situation.
17. Bailey DM, Erith SJ, Griffin PJ, Dowson A, Brewer DS, Gant N, et al. Influence
Our results suggest that the use of cryotherapy by immersion
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intermittent shuttle running. J Sports Sci. 2007;25:1163–70.
15 ◦C immediatelyafter the practice of PEA reduces
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