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Effects of whole-body cryotherapy on a total antioxidative status and activities of antioxidative enzymes in blood of depressive multiple sclerosis patients

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Oxidative stress (OS) plays an important role in the pathogenesis of multiple sclerosis (MS). In MS patients depression is often observed. Cryotherapy might have an effect on OS. The aim of this study was to compare the effects of whole body cryotherapy (WBCT) on changes in total antioxidative status (TAS) of plasma and activities of antioxidative enzymes in erythrocytes from depressive and non depressive MS patients. Twenty-two MS patients with secondary progressive disease course (12 depressive and 10 non depressive) were treated with 10 exposures in a cryochamber. Before and after WBCT the plasma TAS and the activities of superoxide dismutase (SOD) and catalase (CAT) in the erythrocytes were measured. The level of TAS in depressive MS group was significantly lower than in non depressive MS (P < 0.0003). WBCT increased the level of TAS in depressive (P < 0.002) more than in non depressive MS patients (P < 0.01). WBCT treatment of MS patients resulted in the significant increase of TAS level in plasma but had no effects on activities of SOD and CAT. Our results indicate that WBCT suppresses OS in MS patients, especially in depressive patients.
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Eur J Appl Physiol
DOI 10.1007/s00421-011-2122-x
123
ORIGINAL ARTICLE
EVect of short-term cryostimulation on antioxidative status
and its clinical applications in humans
Elrbieta Miller · Gukasz Markiewicz ·
Joanna Saluk · Ireneusz Majsterek
Received: 23 May 2011 / Accepted: 8 August 2011
© The Author(s) 2011. This article is published with open access at Springerlink.com
Abstract Whole body cryostimulation (WBCT) is
becoming popular in medicine and sport as an adjuvant
form of treatment since late 1970s. Only a few works con-
cerning antioxidant protection after WBCT have been pub-
lished. The aim of this study was to determine the eVect of
a ten 3-min-long exposures (one exposure per day) to cryo-
genic temperature (¡130°C) on the level of total antioxi-
dant status (TAS), activity of selected antioxidant enzyme
superoxide dismutase (SOD) and main non-enzymatic anti-
oxidant—uric acid (UA) in WBCT study group (man
n= 24; female n= 22) and non-WBCT control subjects
(man n=22; female n= 26). Moreover, we evaluated the
lipid peroxidation measured as thiobarbituric acid reactive
substances products. Their blood samples were collected
twice at an interval of 10 days in both study group and con-
trol subjects. The activity of antioxidant enzyme and lipid
peroxidation was assayed in erythrocytes, while the con-
centration of uric acid was measured in plasma. After com-
pleting a total of ten WBCT sessions a signiWcant increase
(p< 0.001) of TAS and UA levels in plasma (p< 0.001) in
comparison to non-WBCT was observed. Our data showed
that there was statistically signiWcant increase of the activi-
ties of SOD in erythrocytes obtained from WBCT study
group compared to non-WBCT controls after 10 days of
treatment (p< 0.001). It was concluded that expositions to
extremely low temperatures use in cryostimulation improve
the antioxidant capacity of organism.
Keywords Whole body cryostimulation · Antioxidant
therapy · Total antioxidant status · Lipid peroxidation
Introduction
Whole body cryostimulation (WBCT) is becoming popular
in medicine and sport as an adjuvant form of treatment. The
reported reasons for WBCT include improved general well-
being, and self-treatment or body hardening against respira-
tory tract infections and musculoskeletal pains. WBCT is
often used as an additional form of treatment for inXamma-
tion and pain in, for example, arthritis, osteoarthritis, and
Wbromyalgia (Duqué et al. 2005; Miller et al. 2010a, b, c).
WBCT has been found useful in neurological diseases
including multiple sclerosis (Miller et al. 2010a, b, c) and
psychiatric disorders such as anxiety–depressive syndrome
(Rymaszewska et al. 2008). Treatment with the total expo-
sure of the body at extremely low temperatures was Wrst
introduced in Japan towards the end of the 1970s by Yama-
uchi (1989) who constructed the Wrst cryogenic chamber
and successfully used cryotherapy to treat rheumatism. The
inXuence of extremely low temperatures on the human
Communicated by William J. Kraemer.
E. Miller
Rehabilitation Ward, III General Hospital in Lodz,
Milionowa 14, Lodz, Poland
E. Miller (&)
Gyrwiarska 31, 94-124 Lodz, Poland
e-mail: betty.miller@interia.pl
J. Saluk
Department of General Biochemistry,
University of Lodz, Banacha 12/16, Lodz, Poland
e-mail: juszczak@biol.uni.lodz.pl
G. Markiewicz · I. Majsterek
Department of Chemistry and Clinical Biochemistry,
Medical University of Lodz, Pl. Hallera 1, Lodz, Poland
e-mail: lukasz.markiewicz@umed.lodz.pl
I. Majsterek
e-mail: ireneusz.majsterek@umed.lodz.pl
Eur J Appl Physiol
123
body and physiological reactions is not fully recognized
(Lange et al. 2008; Lubkowska et al. 2010; Miller et al.
2010a, b, c).
An imbalance between free radical generation and anti-
oxidant defense leads to oxidative stress which can damage
lipids, proteins, and nucleic acids in cells causing cell death
in various cell types. Oxidative stress is a hallmark of many
chronic diseases such as neurodegenerative and cardiovas-
cular disorders. The direct estimation of reactive oxygen
species (ROS) generation in vivo is diYcult. A common
approach to measure oxidative stress in vivo is to determi-
nate lipid peroxidation by means of commonly used assay
with thiobarbituric acid (expressed as thiobarbituric acid
reactive substances, TBARS). Lipid peroxidation is one of
the important phenomenon and has been implicated in a
number of deleterious eVects, such as increased osmotic
fragility, decreased membrane rigidity, and cellular defor-
mation (Miller et al. 2011).
The antioxidant system in the organism includes a vari-
ety of antioxidant enzymes such as superoxide dismutase
(SOD), catalase (CAT), glutathione peroxidase (GPx) and
non-enzymatic such as antioxidants glutathione, vitamins
A, C, D, coenzyme Q, uric acid, etc. In humans, over half
the antioxidant capacity of blood plasma comes from uric
acid. Uric acid like ascorbic acid is a strong reducing agent
and potent antioxidant responsible for total antioxidant sta-
tus (TAS) level in plasma (Miller et al. 2011).
Currently, a variety of antioxidative supplementary
therapy for the treatment of chronic diseases are used
worldwide. There is a need for developing new therapies
such as WBCT which can be used as adjuvant antioxida-
tive therapy. The mechanisms of action of hypothermic
protection are not entirely understood. It seems clear that
lower temperature protects tissues deprived of oxygen by
slowing the rate of cellular damage that occurs from the
formation of free radicals, chemical metabolites, and tissue
edema. According to increasing evidence, hypothermia
can signiWcantly improve outcomes of diseases with oxida-
tive stress background such as neonates hypoxic-ischemic
encephalopathy (Perrone et al. 2010), brain injury (Varon
et al. 2011), multiple sclerosis (Miller et al. 2010a, b, c),
depression (Miller et al. 2010a, b, c) and cerebral ischemia
(Varon et al. 2011). So, it seems important to know the
inXuence of repeated exposure to the stress induced by
cryogenic temperatures aVecting the whole body of
healthy people in order to use this knowledge eYciently in
clinical practice.
Only a few works concerning antioxidant protection
after ten sessions of WBCT (¡130°C) in healthy men have
been published (Duqué et al. 2005; Lubkowska et al. 2009).
Recent reports suggest a stimulating antioxidative eVect of
cryostimulation but there is no information regarding the
substances responsible for it (Miller et al. 2010a, b, c).
The antioxidants such as uric acid and the antioxidative
enzymes such as superoxide dismutase (CuZnSOD) protect
organisms (Lubkowska et al. 2009; Miller et al. 2010a, b, c)
against production of free radicals and diVerent reactive
oxygen and nitrogen species (ROS/RNS). The measure-
ment of TAS in plasma represents the body redox status
better than the measurement of the single circulating anti-
oxidant.
We hypothesized that the generation of ROS/RNS may
be partly inhibited by ten sessions of WBCT (Miller et al.
2010a, b, c). Therefore, the aim of this study was to deter-
mine the eVect of ten sessions of 3-min-long exposures
(one exposure per day) to cryogenic temperature (¡130°C)
on TAS, the activity of selected antioxidant enzyme super-
oxide dismutase (CuZnSOD) and main non-enzymatic anti-
oxidant—uric acid (UA) in the middle age healthy subjects.
Moreover, we evaluated the lipid peroxidation measured as
TBARS.
Materials and methods
Subjects presentation
Forty-six healthy subjects (man n= 24; female n= 22)
(mean age 37.5 §3.1 years; body mass index (BMI)
26.9 §4.2; height 171 §2.1 cm; weight 76.1 §9.7 kg;
body surface area (BSA) 1.77 §4.2 m2 (female),
1.98 §3.8 m2 (male); Table 1) were chosen for the study
group (WBCT). The subjects were matched pairwise, hav-
ing similar BMI, age, physical activity and use of hormonal
contraception (6 females as well as in the study and control
group). None of the subjects had practiced WBCT regularly
before the study. The subjects were moderately physically
active, and no outdoor workers were included. They were
asked to maintain their physical activity habits during the
study period. Non-WBCT group (man n= 22; female
n= 26) (mean age 37.9 §2.1 years; body mass index
(BMI) 27.1 §4.1; height 169.9 §9.2 cm; weight
78.1 §9.1 kg; body surface area (BSA) 1.76 §3.2 m2
(female), 1.97 §4.5 m2(male); p> 0.05) was also included
in the study as the control group to measure blood markers
before and 10 days later without any intervention to elimi-
nate the possibility of changes between days.
Their blood samples were collected twice at an interval
of 10 days similar to the study group but without WBCT
treatment. All examined subjects as well as controls
received no immunomodulators, immunostimulators, hor-
mones, vitamins, minerals or any other substitutions with
antioxidative properties. Prior to the study, all the subjects
had undergone medical checkups including a resting ECG.
Each participant gave his written consent before partici-
pation in the research, and the Bioethical Committee of the
Eur J Appl Physiol
123
Medical University of Lodz, Poland issued their formal
consent, according to the Declaration of Helsinki. The
study was performed in the Department of Biochemistry,
University of Lodz, Poland and Rehabilitation Division, III
General Hospital in Lodz, Poland.
Experimental design
An experimental trial with WBCT consisted of the 46 (man
n= 24; female n= 22) subjects exposed by ten sessions of
WBCT (one session per day) in a cryogenic chamber car-
ried out daily from Monday to Friday. The used cryogenic
chamber (KR2005N, liquid nitrogen as a coolant) had two
rooms: the vestibule, with the temperature of ¡60°C, and
the main chamber, with temperature ¡130°C. Sessions in
the chamber lasted 3 min according to the guidance of
Gregorowicz and Zagrobelny (2007) on the appropriated
duration of exposure and temperature for adult patients and
a list of medical conditions in which WBCT is unsuitable.
During WBCT, the whole subjects group wore the same
bathing suits, surgical masks, caps, gloves, socks, and
shoes. WBCT sessions were applied everyday between
10.30 and 11.30 a.m. The participants were exposed to ses-
sions of extremely low temperature (¡130°C) in a cryo-
genic chamber. Subjects entered the main chamber in
groups of Wve or four. In the cryogenic chamber, the sub-
jects were instructed to move slowly, walking in a circle,
one behind another, without verbal contact. Just before
each session of cryostimulation, systolic and diastolic blood
pressure was measured. In all 46 subjects completed the
WBCT treatment. No illnesses or side eVects occurred dur-
ing the study period.
The study was carried out from March to November
2010. Observations were examined at two stages: at the
beginning and at the end of the study.
In all the groups, blood samples (2.4 ml) were obtained
from an antecubital forearm vein using vacutainer system
tubes. Blood samples were collected into cooled EDTA and
centrifuged to isolate plasma and erythrocytes. Samples of
blood were taken just before the Wrst 10 days cycle of ther-
apy and directly after the last immersion.
Biochemical investigations
Measurement of uric acid
Blood samples were analyzed at the SYNEVO Laboratory
at III General Hospital in Lodz. The concentration of uric
acid was determined using a colorimetric enzyme assay on
the Cobas Integra 400 plus analyzer. Results are expressed
as mg/dl of uric acid. References range is 2.5–8.0 mg/dl.
Measurement of CuZnSOD activity
Superoxide dismutase activity in erythrocytes was mea-
sured according to Misra and Fridovich method (1972). The
absorbance of the examined samples was estimated at
380 nm (using Beckman spectrophotometer) at 37°C. The
activity was expressed as U/gHb. Superoxide dismutase
(CuZnSOD) is within the reference range. The body utilizes
this enzyme to rapidly convert the superoxide anion radical
to hydrogen peroxide, which is less toxic to cells. Refer-
ences range is 1334.34–2351.11 (U/g Hb) (Mrowicka et al.
2008).
Measurement of TAS
Determination of TAS in blood plasma was performed by
spectrophotometric method according to procedure no.
NX2332 by Randox (Randox Laboratories Ltd. Ardmore,
Diamond Road, Crumlin, Co Antrim, UK, BT29 4QY).
BrieXy, ABTS (2,2-Azino-di-[3ethylbenzthiazoline sul-
phonate]) was incubated with peroxide (metmyoglobin)
and H2O2 to produce the radical cation ABTS with a rela-
tively stable blue-green colour. Antioxidants when added in
examined sample caused suppression of this color production
measured as decrease of absorbance with a spectrometer
(UV/VIS Spectrometer Lambda 14P, Perkin Elmer, USA)
at 600 nm. TAS was calculated as concentration of antioxi-
dants (mmol/l). References range is 8.30–1.77 mmol/l
plasma. This range was measured in a European working
population. It is recommended that each laboratory estab-
lish its own reference range to reXect the age, sex, diet, and
geographical location of the population.
Measurement of TBARS
For TBARS estimation in plasm, samples of plasma were
transferred to an equal volume of 20% (v/v) cold trichloro-
acetic acid in 0.6 M HCl and centrifuged at 1200£gfor 15
min. One volume of clear supernatant was mixed with 0.2
vol. of 0.12 M thiobarbituric acid in 0.26 M Tris, pH 7.0
and immersed in a boiling water bath for 15 min. Absor-
bance at 532 nm was measured and the results are
Table 1 Characteristics of study subjects
BMI body mass index, BSA body surface area
Females (n= 22) Males (n=24)
Mean age (years) 38§337§5
BMI (kg/m2)24§4 27.7 §4
Height (cm) 165 §8172§8
Weight (kg) 68 §10 82 §12
BSA (m2)1.77§4.2 1.98 §3.8
Eur J Appl Physiol
123
expressed as mol of TBARS. Normal human plasma has
lipid peroxide level of range 1.86–3.94 mol.
Statistical analysis
The results were statistically elaborated. An enzyme activ-
ity as well as plasma uric acid level was expressed as mean
value §SD. 10% of the samples were blinded and repli-
cated for quality control (QC). If no signiWcant diVerences
between variations were found, as assessed by the Snede-
cor–Fisher test, the diVerences between the two groups
were evaluated by applying the Student’s t-test. Otherwise,
the Cochran–Cox test was used. The data were analyzed
using the STATISTICA (StatSoft, Tulsa, OK) statistical
package. DiVerences were considered signiWcant, when the
signiWcance was p< 0.05.
Results
Firstly, our study showed a statistically signiWcant increase
of 10% of the level of UA in plasma obtained from WBCT
study group compared to non-WBCT controls after 10 days
of treatment (p < 0.001) (Fig. 1; Table 3). We also showed
that there was statistically signiWcant increase of 13% of the
UA level in WBCT study group after 10 days of treatment
compared to the initially taken sample in this group
(p<0.001) (Fig.1; Table 3). Moreover, after WBCT the
increase of UA was about 14% in women and 10% in men
(p< 0.0001) (Table 2). There were no statistically signiW-
cant increase of UA levels in the non-WBCT control group
after 10 days when compared to the initially taken sample
in this group (p> 0.05) (Fig. 1; Table 3).
Secondly, data obtained showed that there was statistically
signiWcant increase of 15% of the activities of CuZnSOD in
erythrocytes obtained from WBCT study group compared to
non-WBCT controls after 10 days of treatment (p< 0.001)
(Fig. 1; Table 3). There was also statistically signiWcant
increase of 6% of the activities of CuZnSOD in erythrocytes
obtained from WBCT study group after 10 days of treatment,
compared to the initially taken sample in this group
(p<0.001) (Fig.1; Table 3). The activities of CuZnSOD in
erythrocytes after cryostimulation were also increased by
about 6% in both sexes (p< 0.0001) (Table 2). Moreover,
there were no statistically signiWcant increase of the activities
of CuZnSOD in erythrocytes obtained from non-WBCT con-
trol group after 10 days when compared to the initially taken
sample in this group (p> 0.05) (Fig. 1; Table 3).
Fig. 1 The eVect of whole body cryostimulation (WBCT) on the level
of uric acid (UA), total antioxidant status (TAS), thiobarbituric acid
reactive substances (TBARS) in plasma and superoxide dismutase
(SOD) activity in erythrocytes of WBCT study group before (WBCT-0)
and after 10 days of cryostimulation (WBCT-10) as well as non-
WBCT control subjects before (Cont.-0) and 10 days after (Cont.-10);
Error bars denote standard deviation (SD). (*p<0.05, **p< 0.01,
***p<0.001)
WBCT-0 WBCT-10 Cont.-0 Cont.-10
TBARS [nmolMDA/gHb]
0,1
0,2
0,3
0,4
WBCT-0 WBCT-10 Cont.-0 Cont.-10
SOD [U/g Hb]
500
1000
1500
2000
2500
WBCT-0 WBCT-10 Cont.-0 Cont.-10
Uric Acid [mg/dl]
2
4
6
WBCT-0 WBCT-10 Cont.-0 Cont.-10
TAS [mmol/l]
0,2
0,4
0,6
0,8
1,0
*** *** *** ***
*** *** ***
Eur J Appl Physiol
123
We also showed that there was statistically signiWcant
increase of 8% of the TAS in plasma obtained from WBCT
study group compared to non-WBCT controls after 10 days
(p< 0.001) (Fig. 1; Table 3). There was also statistically
signiWcant increase of 19% of TAS in plasma obtained
from WBCT study group after 10 days of treatment com-
pared to the initially taken sample in this group (p< 0.001)
(Fig. 1; Table 2). It is important that no statistically signiW-
cant increase of the total antioxidant status in plasma
obtained from non-WBCT control group after 10 days
when compared to the initially taken sample in this group
was observed (p> 0.05) (Fig. 1).
Finally, our results showed that there was statistically
signiWcant increase of 13% of the level of TBARS in
plasma obtained from WBCT study group compared to
non-WBCT controls after 10 days (p< 0.001) (Fig. 1;
Table 3). What must be emphasized there was no statisti-
cally signiWcant changes of the level of TBARS in plasma
obtained from WBCT study group after 10 days of treat-
ment compared to the initially taken sample in this group
(Table 2). We have observed that the level of TBARS in
both groups (male and women) after WBCT was higher (by
about 2.7%) than before WBCT (p<0.05, p>0.05 in men
and women, respectively) (Table 2). There was no statisti-
cally signiWcant increase of the level of TBARS levels in
the non-WBCT control group after 10 days in compare to
the initially taken sample in this group (p>0.05) (Fig.1;
Table 3).
Discussion
The response of the human body to cold occurs through
changes in the endocrine, circulatory, nervous–muscular,
and immunological systems (Kellogg 2006). The cutaneous
circulation is a major eVecter of human thermoregulation.
There are tenfold more cold receptors in dermis compared
to heat receptors. Experimental evidence indicates that the
early phase of vasoconstriction due to cooling is mainly
dependent on neural regulation and that late phase vasocon-
striction relies more on non-neural mechanisms (Hampl
et al. 2006).
Shivering is the earliest and most primitive response to
increase in heat production. This form of thermogenesis
consumes large amounts of energy, which is not eVective
during severe cold (Silva 2006) such as WBCT. Humans
have evolved a more eYcient and long-lasting form of non-
shivering facultative thermogenesis that uses pure meta-
bolic mechanisms to generate heat. The non-shivering ther-
mogenesis has two categories: obligatory and facultative
(Kellogg 2006). The facultative thermogenesis is regulated
mainly by catecholamines released from adrenals and the
Table 2 EVect of whole body cryostimulation (WBCT) on TBARS (thiobarbituric acid reactive substances), superoxide dismutase (SOD), total
antioxidant status (TAS), and uric acid in men and women
pvalue refers to diVerence before WBCT and after WBCT subjects (females and males)
Females (n=22) pMales (n=24) p
Before WBCT After WBCT Before WBCT After WBCT
TBARS (nmolMDA/gHb) 0.308 §0.98 0.317 §0.86 >0.05 0.365 §0.75 0.375 §0.83 <0.05
CuZnSOD (U/g Hb) 1898.1 §165.7 2003.3 §198.7 <0.001 2102.18 §213.1 2244.8 §2546 <0.001
Uric Acid (mg/dl) 4.8 §0.85 5.52 §0.78 <0.0001 5,5 §0.9 6.0 §0.65 <0.0001
TAS (mM) 0.76 §0.24 0.93 §0.36 <0.001 0.78 §0.34 0.91 §0.35 <0.001
Table 3 The eVect of whole body cryostimulation (WBCT) on the
level of uric acid (UA), total antioxidant status (TAS), thiobarbituric
acid reactive substances (TBARS) in plasma and superoxide dismutase
(SOD), activity in erythrocytes of WBCT study group before (WBCT-
0) and after 10 days of cryostimulation (WBCT-10) as well as non-
WBCT control subjects before (Cont.-0) and 10 days after (Cont.-10)
aSEM standard error of the mean
Study subjects (n=46) pControls (n= 48) p
WBCT-0 WBCT-10 Cont.-0 Cont.-10
TBARS
(nmolMDA/gHb)
0.344 §0.78 (0.03)a0.352 §0.82 (0.04)a>0.05 0.303 §0.52 (0.03)a0.309 §0.43 (0.025)a>0.05
CuZnSOD (U/g Hb) 2060.7 §171.2 (123.46)a2202.4 §186.7 (134.23)a<0.001 1922.12 §235.1 (56.63)a1991.5 §234.4 (76.82)a>0.05
Uric acid (mg/dl) 4.9 §0.82 (0.26)a5.59 §0.68 (0.22)a<0.0001 5.09 §0.9 (0.29)a5.09 §0.75 (0.3)a>0.05
TAS (mM) 0.78 §0.27 (0.06)a0.92 §0.32 (0.09)a<0.001 0.86 §0.32 (0.06)a0.87 §0.34 (0.07)a>0.05
Eur J Appl Physiol
123
sympathetic nervous system (Hampl et al. 2006). Obliga-
tory thermogenesis proceeds continuously in all organs and
tissues of the body. The most important endocrine factors
modulating obligatory thermogenesis are thyroid hormones
which increases metabolic rate and thermogenesis (Silva
2006).
Cryogenic temperatures induced vasoconstriction fol-
lowed by vasodilation after 4 min which is connected with
increasing blood Xow seen as skin hyperemia and return to
normal skin temperatures (after about 14 min). Vasodilata-
tion appears about 4 min after WBCT and achieves four
times higher value than before cryostimulation and can
maintain for some hours (Bauer and Skrzek 1999) increasing
blood Xow and stimulating the elimination of metabolic
products. There is a large variation in the individual
responses to cold due to factors such as body size, Wtness
level, amount of subcutaneous fat and sex (Gordon 2001;
Gordon et al. 2003). The lowest local skin temperatures after
WBCT were recorded in the forearm, 11°C and in the calf
12°C (Westerlund et al. 2003). In our study, after cryostimu-
lation skin temperature dropped below 13.6°C in the back,
upper arm, forearm, thigh, and calf. The eVects of cryostimu-
lation on rectal temperature were minimal, probably due to
the short duration of cryostimulation. Cooling the skin below
20°C causes a marked reduction in the production of acetyl-
choline and in the rate of conduction along cooling nerves,
which varies according to the size of Wbres, thus producing
asynchrony of impulses (Wozniak et al. 2007).
Females have a reduced cold temperature tolerance com-
pared to men because of their lower aerobic capacity. On
the other hand, they have more subcutaneous fat, which
serves as a thermal insulator (Gordon 2010).
Some authors observe that cryostimulation leads to an
increase in plasma ACTH and cortisol, epinephrine and
norepinephrine (Leppäluoto et al. 2008), while others have
not reported any changes in stress hormones (Zagrobelny
et al. 1993). WBCT resulted in decreased hemoglobin and
iron in erythrocytes (BanW et al. 2009) which probably
cause decreased testosterone. Iron activates xanthine oxi-
dase while copper deactivates it. Man accumulates iron
with age, which decreases testosterone level in blood (ferri-
tin levels rise above 45 ng/dl). WBCT resulted in decreased
levels of testosterone and estradiol in football players,
although there were no changes in the concentration of
luteinizing hormone and dehydroepiandrosterone (DHEA-
S) (Korzonek-Szlacheta et al. 2007). Smolander et al.
(2009) showed that ten sessions of WBCT in healthy
females did not lead to disorders related to altered secre-
tions of the growth hormone, prolactin, thyrotropin, or thy-
roid hormone. Thermoregulation induced by low
temperatures is associated with an increase in lipid metabo-
lism. The human body uses energy derived mainly from the
conversions of carbohydrates and lipids (Vallerand and
Jacobs 1989). The release of norepinephrine from the ter-
minal endings of sympathetic neurons during non-shivering
thermogenesis leads to the mobilization of fatty acids from
intracellular stores of triacylglycerides and their oxidation
in the mitochondria (Florez-Duquet and McDonald 1998).
The mechanisms of action of hypothermic protection are
not entirely understood. It seems clear that lower tempera-
ture protects tissues deprived of oxygen by slowing the rate
of cellular damage that occurs due to the formation of free
radicals, chemical metabolites, and tissue edema (Miller
et al. 2010a, b, c).
In the course of normal human activity, energy produc-
tion, detoxiWcation of pollutants, and immunologic defense
mechanisms, free radicals are produced. Dietary antioxi-
dants (such as proanthocyanidins found in blueberries and
bioXavonoids found in citrus fruits), as well as the human
antioxidant enzymes (CuZnSOD) and non-enzymatic (UA)
provide critical protection against free radical damage. Oxi-
dative stress results when this delicate pro-oxidant/antioxi-
dant equilibrium is disrupted in favor of the pro-oxidant
(free radical) state. The enzymatic antioxidant system
includes a variety of antioxidant enzymes such as CuZn-
SOD, catalase (CAT), and glutathione peroxidase. Antioxi-
dants, whether synthesized endogenously or exogenously
administered, are reducing agents that neutralize the oxida-
tive compounds (ROS) before they can cause damage to
diVerent biomolecules (Miller et al. 2010a, b, c). There is a
need for developing new therapies such as WBCT which
can be used as adjuvant antioxidative therapy. In our pres-
ent study, we determinated TAS in plasma which was dis-
tinctly higher (p< 0.001) after ten sessions of
cryostimulation compared to non-WBCT group. Our obser-
vations of suppression of oxidative stress by WBCT are
consistent with other reports (Duqué et al. 2005; Siems
et al. 1999; Miller et al. 2010a, b, c). Wosniak et al. (2007)
shows that cryostimulation induced an increase in the activ-
ity of superoxide dismutase (SOD) by 36% (p< 0.001) and
glutathione peroxidase (GPx) by 68% (p< 0.01) in the
human erythrocytes.
It has been suspected that an adaptation to cold stimuli
and the improvement in the body hardening could be
related to an increase in the protection against oxidative
stress (Duqué et al. 2005). Simes et al. (1999) reported a
higher enzymatic protection (i.e., in the increased activity
of red blood cells CAT, glutathione peroxidase, SOD) for
those who regularly practice winter swimming activities or
after heavy endurance physical exercise in comparison with
control. This activation can be viewed as an adaptive defen-
sive mechanism to cope with increased oxidative stress.
Our results indicate for the Wrst time that cryostimulation
stimulates the antioxidative response of organism via aug-
mentation of SOD activities (p< 0.001) and increase of UA
level (p< 0.001) compared to non-WBCT subjects. UA is a
Eur J Appl Physiol
123
natural antioxidant, accounting for upto 60% of the free
radical scavenging activity in human blood. UA can scavenge
superoxide, the hydroxyl radical, and singlet oxygen. UA may
assist in the removal of superoxide by preventing against the
degradation of SOD, the enzyme that is responsible for clear-
ing superoxide from the cell (Kutzing and Firestein 2008).
In our study, we showed that cryostimulation may
reduce oxidative stress via a signiWcant increase not only in
the level of TAS but also UA in plasma and activity of SOD
in erythrocytes. In the present study, lipid peroxidation in
erythrocytes measured as TBARS was not statistically
increased after WBCT. Other important antioxidants such
as glutathione peroxidase should be examined by further
research on cryostimulation.
It seems that WBCT may be used as adjuvant therapy in
the treatment of diseases with oxidative stress background,
since it improves the antioxidant capacity of organism.
Further studies are required to explain the antioxidative
mechanisms in humans and determine the short term or
long term eVects of cryochamber exposure.
Open Access This article is distributed under the terms of the Crea-
tive Commons Attribution Noncommercial License which permits any
noncommercial use, distribution, and reproduction in any medium,
provided the original author(s) and source are credited.
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... Since the 70 s, several forms of WBC have been applied in people suffering from autoimmune diseases such as multiple sclerosis, 22,23 ankylosing spondylitis 24,5,7 and rheumatoid arthritis. 25 Autoimmune diseases are diseases in which the immune system is overactive and causes increased inflammatory reactions, which in their turn cause tissue damage. ...
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... In studies regarding the influence of WBC on pro-oxidative-antioxidant balance, it is shown that obtaining beneficial antioxidant effects requires repeated application of these treatments [19][20][21][22][23]47]. ...
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... There are a number of studies that demonstrate the benefits of its use in the course of various diseases, including patients with MS. Studies describing the positive effect of WBC on MS patients focus, among others, on changes in the physicochemical parameters of the blood, or reductions in oxidative stress [12,13,14,15,16]. When analysing available literature, a number of studies can be found that indicate the beneficial effects of frequent WBC in biological renewal -improving muscle strength, faster muscle recovery after exercise, improved cardiovascular and hormonal systems, better lipid changes in the body, and many others factors showing an improved functional status of the body [22,23,24,25]. ...
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... Single studies indicate that treatment with cold may have positive effects for both the body and the psyche, and that the improvement in well-being can be particularly observed in people suffering from depression [60]. It is worth paying attention to the possibility of using whole-body cryostimulation (WBC) to reduce fatigue. ...
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Multiple sclerosis (MS) is the most common autoimmune disease of the central nervous system (CNS), with an inflammatory demyelinating basis and a progressive course. The course of the disease is very diverse and unpredictable. Patients face many problems on a daily basis, such as problems with vision; sensory, balance, and gait disturbances; pain; muscle weakness; spasticity; tremor; urinary and fecal disorders; depression; and rapidly growing fatigue, which significantly influences quality of life among MS patients. Excessive fatigue occurs in most MS patients in all stages of this disease and is named MS-related fatigue. The crucial issue is the lack of effective treatment; therefore, this review focuses not only on the most common treatment methods, but also on additional novel therapies such as whole-body cryotherapy (WBC), functional electrical stimulation (FES), and non-invasive brain stimulation (NIBS). We also highlight the advantages and disadvantages of the most popular clinical scales used to measure fatigue. The entire understanding of the origins of MS-related fatigue may lead to the development of more effective strategies that can improve quality of life among MS patients. A literature search was performed using MEDLINE, EMBASE, and PEDro databases.
... Recently published reports suggested the increase of the activity of antioxidant enzymes (64) and the beneficial effect on other oxidative stress markers in rats (65). The decrease of parameters of oxidative stress or increase of total antioxidative status in healthy men and depressive multiple sclerosis patients (66,67) were also observed. These encouraged us to explore the level of NO and total antioxidative status. ...
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IntroductionAccumulating evidence indicates the effectiveness of cryogenic temperature interventions in rheumatoid arthritis, ankylosing spondylitis, fibromyalgia, multiple sclerosis, and chronic low back pain. The application of whole-body cryotherapy (WBC) in psychiatric aspects of medicine was also noted. Nevertheless, the exact mechanisms explaining the beneficial effect of WBC on mood disorders remain unclear. The study aimed to assess the efficacy of repetitive short exposure to extremely low temperatures (WBC) on mood, quality of life as well as on biochemical measures among people diagnosed with depressive episode undergoing pharmacological treatment.Materials and Methods Prospective randomized, double-blind sham-controlled protocol was used. The study enrolled 92 medically stable adults (aged 20–73 years) with a diagnosis of a depressive episode. The participants were randomly allocated and exposed to 10 whole-body cryotherapy (WBC) sessions (−110°C till −160°C [the experimental group (EG)] or to low, but not cryogenic temperatures −50°C [the control group (CG)]. Thirty participants in the EG and 26 in CG completed the whole study. The primary outcome measures were depressive symptoms evaluated with the Beck Depression Inventory-II (BDI-II) as well as the Hamilton Depression Rating Scale (HAM-D 17). The quality of life, quality of sexual life, acceptance of the disease and self-reported mood, vitality, and sleep quality were assessed as secondary outcome measures. The study was registered at Australian New Zealand Clinical Trials Registry (ACTRN12619001600134).ResultsThe results show evidence for a statistically significant difference in the clinical assessment of depressive symptoms according to HAM-D 17 scale (T4 by group interaction p=0.02), BDI-II (T2 time by group interaction p=0.01), cognitive-affective BDI dimension (T4 by group interaction p=0.00), and somatic BDI dimension (T4 by group interaction p=0.028). Significant improvement was also noticed in life quality (p < 0.05), self-assessed mood (p=0.035), and disease acceptance (p=0.007). There were no statistically significant changes related to sexual satisfaction, self-assessed vitality, and sleep (p > 0.05).Conclusions Whole-body cryotherapy is a useful method to improve standard pharmacological treatment. The WBC intervention reduces mental health deterioration, especially in mood disorders, such as depression, and can be beneficial for well-being and quality of life.
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There is strong evidence that multiple sclerosis (MS) is characterized not only by immune mediated inflammatory reactions but also by neurodegenerative processes. Accumulated data indicate that oxidative stress (OS) plays a major role in this process. Generated in excess, reactive oxygen species (ROS) lead to oxidative stress and are involved in demyelination and axonal damage in MS. ROS generation may be inhibited partly by hypothermia, which is known as a potent putative neuroprotectant and may inhibit generating free radicals and oxidative stress. Whole-body cryotherapy (WBCT) treatment may improve both survival and neurological outcome in MS patients.The aim of the study was to determine the effects of WBCT on oxidative stress by the level of total antioxidative status (TAS) in plasma and the activity of antioxidative enzymes: superoxide dismutase (SOD) and catalase (CAT) in the erythrocytes from MS patients. Moreover, we measured the combined effects of WBCT and melatonin on TAS and activity of antioxidative enzymes in MS patients. Sixteen MS patients were treated with 3 cycles of 10 exposures in a cryogenic chamber. The last cycle was accompanied by a 14-day-long supplementation of melatonin (10 mg daily). Healthy subjects as a control group had 1 cycle of WBCT.Our preliminary results for the first time showed that WBCT treatment of MS patients resulted in the increase of TAS but had no effects on activity of antioxidative enzymes: SOD and CAT. Supplementation of melatonin and the treatment along with WBCT significantly increased the activity of SOD and CAT in erythrocytes of MS patients.