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Journal of Human Kinetics volume 30/2011, 75 - 83DOI:10.2478/v10078-011-0075-075
Section II- Exercise Physiology & Sports Medicine
1 - Department of Physical Education and Physiotherapy, Technical University, Opole, Poland.
2 - Institute of Human Physiology, University School of Physical Education, Krakow, Poland.
3 - Department of Internal Diseases, VoivodshipHopsital, Opole, Poland.
Authors submitted their contribution of the article to the editorial board.
Accepted for printing in Journal of Human Kinetics vol. 30/2011 on December 2011.
Impact of 10 Sessions of Whole Body Cryostimulation on
Cutaneous Microcirculation Measured
by Laser Doppler Flowmetry
by
Szyguła Renata1, Dybek Tomasz1, Klimek Andrzej2, Tubek Sławomir3
The aim of the present study was to evaluate the basic and evoked blood flow in the skin microcirculation of the
hand, one day and ten days after a series of 10 whole body cryostimulation sessions, in healthy individuals.
The study group included 32 volunteers – 16 women and 16 men. The volunteers underwent 10 sessions of
cryotherapy in a cryogenic chamber. The variables were recorded before the series of 10 whole body cryostimulation
sessions (first measurement), one day after the last session (second measurement) and ten days later (third
measurement). Rest flow, post-occlusive hyperaemic reaction, reaction to temperature and arterio–venous reflex index
were evaluated by laser Doppler flowmetry.
The values recorded for rest flow, a post-occlusive hyperaemic reaction, a reaction to temperature and arterio –
venous reflex index were significantly higher both in the second and third measurement compared to the initial one.
Differences were recorded both in men and women. The values of frequency in the range of 0,01 Hz to 2 Hz (heart
frequency dependent) were significantly lower after whole-body cryostimulation in both men and women. In the range
of myogenic frequency significantly higher values were recorded in the second and third measurement compared to the
first one.
Recorded data suggest improved response of the cutaneous microcirculation to applied stimuli in both women
and men. Positive effects of cryostimulation persist in the tested group for 10 consecutive days.
Key words: cryotherapy, skin blood flow, rest flow, post-occlusive hyperaemic reaction, arterio–venous reflex index
Introduction
Whole body cryotherapy (WBCT) is more
and more frequently used to complete
pharmacotherapy and kinesiotherapy that are
applied in rheumatologic and neurological
diseases as well as in therapy of injuries of the
locomotor system or in overload syndromes. It is
also a modern, effective and safe procedure for
athletes’ recovery (Hubbard et al., 2004).
The procedure of whole body
cryostimulation is based on exposure of the
organism to extremely low temperature (-110°C to
-160°C) for a very short period (1 – 3 minutes)
without provoking hypothermia or congelation
(Westerlund et al., 2003). Cryogenic temperatures
trigger physiological thermoregulation
mechanisms, which results in analgesic (Long et
al., 2005; Brandner et al., 1996; Ingersoll et al.,
1991), anti-inflammatory (Banfi et al., 2010;
Knight, 1995), anti-oedematic (Meeusun et al.,
1998) and anti-oxidative effects (Akhalaya et al.,
2006; Dugue et al., 2005) and stimulate the
immune system (Lubkowska et al., 2010b). The
effect of low temperature is especially
pronounced in skin microcirculation of upper and
lower limbs. After exposure to extreme cold, in
the first phase constriction of skin vessels and
76 Impact of 10 sessions of whole body cryostimulation on cutaneous microcirculation measured
Journal of Human Kinetics volume 30/2011, http://www.johk.pl
opening of arterio-venous shunts occurs, due to
increased sympathetic stimulation, presynaptic
norepinephrine release and increased affinity of
the postsynaptic α2 receptors (Flouris and
Cheung, 2009; Charkoudian, 2003; Chotani et al.,
2000; Stephens et al., 2001; Koganezawa et al.,
2006). Most of the blood flows to the body cavities
in order to minimalize heat losses. The skin blood
flow is significantly decreased and may be
completely reduced (Charkoudian, 2003). Several
seconds after cessation of the stimulus, reflexive
hyperaemia of the tissues occurs due to decreased
sympathetic stimulation and local mechanisms –
mainly accumulation of metabolites in previously
hypoperfused areas as it was confirmed by
studies using thermovision (Bauer et al., 1997).
Active reperfusion of the skin
microcirculation persists for several hours after
single cryotherapy procedure. Although the effect
of a series of whole body cryotherapy sessions
remains unknown. Therefore the aim of the
present study was to evaluate the basic and
evoked blood flow in the skin microcirculation of
the hand one day and ten days after a series of 10
WBCT sessions in healthy individuals.
Material and methods
The study group included 32 healthy,
nonsmoking volunteers, students of physical
education at the Opole University of Technology -
16 women (F) and 16 men (M), who had never
experienced cryotherapy before. Prior to the test
they had a medical examination to rule out
contraindications for cryonic sessions.
Basic anthropometric measurements were
performed prior to the test. Body weight and
composition were evaluated with the use of
electric impedance (Tanita Body Composition
Analyzer, TBF-330). The results are shown in
Table 1.
The volunteers underwent 10 sessions of
WBCT in a cryogenic chamber of Pulmonology-
Rheumatology Hospital (Poland). The procedures
took place once a day in the morning from
Monday till Friday, for 3 minutes in the
temperature of -130°C. Each session was preceded
by adaptation in the temperature of -60°C for 30
seconds. Participants' dressing was consistent
with regulation for cryonic procedures
(swimsuits, covered feet, hands, ears and
airways).
The test of selected variables of skin
microcirculation.
The microcirculation was measured using
Doppler laser flowmeter Perifluks 4001 (Perimed,
Sweden). Laser-Doppler measurement of
cutaneous microvascular perfusion in humans has
many advantages: the measurement is
continuous, non-invasive and specific to the
cutaneous microcirculation. The technique
applied in the instrument uses the laser light of
wavelength 780 nm. With this technique the laser
light is used to transluminate approximately one
cubic millimeter of skin tissue and Doppler
principle is adopted to measure the velocity of red
blood cells in skin microvasculature.
Table 1
Somatic characteristics of the female and male study participants
Variables Male n=16 (x±SD) Female n=16 (x±SD)
AGE [years] 21.69±1.89 20.13±0.95
BODY HEIGHT [cm] 190.56±5.20 162.46±6.41
BODY MASS [kg] 84.87±8.74 53.65±7.94
BODY MASS INDEX [kg x cm-2] 23.38±2.31 20.21±1.98
FAT [%] 15.04±10.45 19.81±2.26
FAT MASS [kg] 11.26±4.14 10.83±2.57
FAT-FREE MASS [kg] 73.60±5.24 42.79±5.73
by Szyguła R. et al. 77
© Editorial Committee of Journal of Human Kinetics
The LDF signal is a stochastic
representation of the number of moving cells in
the tissue volume multiplied by their velocities.
The flow was measured in conventional Perfusion
Units score (PU), in proportion to the energy of
the Doppler signal. 1 PU corresponds to the
voltage of 10 mV at the outlet (Sundberg, 1984;
Cankar and Strucl, 2008). The test was performed
in horizontal position (on the back), in constant
surrounding temperature of 21C1,2 C, air
humidity 40-60%, after ca. 20 minutes of
adaptation (Beradesca et al., 2002; Fullerton et al.,
2002). The optode was placed on the skin of the
back of the hand between the first and second
metacarpal bones using special both sides
adhesive ring. The tested skin area was healthy
and shaved (Johnson and Kellogg, 2010). The
participants were asked not to take part in
physical activities and to avoid products that
influence the circulation (coffee, tea and Coca-
Cola) for at least 6 h prior to the study. Directly
before the start of the test the volunteers were
instructed to keep the lying position, not move
and keep a steady breathing pattern (Looga,
2005).
The study protocol:
1. The procedure was started after 20 minutes
of stabilization of the circulatory system in
the horizontal position.
2. Blood pressure measurement (mmHg) was
performed on the brachial artery.
3. Registration of the rest flow (RF) in
horizontal position, on a dominating upper
limb, registration time 4 min.
4. Registration of the flow after occluding the
arm with the cuff of the manometer filled
with air up to pressure exceeding the
formerly measured systolic pressure by 50
mmHg, biological zero (BZ), registration
time 4 min.
5. Registration of the reactive hyperemia (RH)
after loosening the cuff, registration time 4
min.
6. Stabilization of the blood flow back to rest
values.
7. Rising the optode’s temperature up to 44C,
using the built-in heating module, 1 min.
8. Registration of thermal hyperemia (TH),
registration time 4 min.
9. Stabilization of the blood flow back to rest
values.
10. Changing the position from horizontal to
vertical.
11. Registration of the RF in a standing
position, after 2 minutes adaptation (ST).
Rest flow (RF), hyperaemic (RH),
hyperthermic (TH) reactivity of skin
microcirculation and arterio – venous reflex index
(VAR) were evaluated. The arterio–venous reflex
index calculated according to the formula RF –
ST/RF x 100%. The variables were recorded before
the series of 10 WBCT sessions (first
measurement- I), one day after the last session
(second measurement-II) and ten days later (third
measurement-III).
Frequency of signals (FS) received by
means of the laser Doppler fluximetry between
0.01 up to 2 Hz during basic flow was also
analyzed. In this range five groups were singled
out: I – frequency band between 0.01-0.02 Hz; II –
frequency band between 0.021-0.05 Hz; III –
frequency band between 0.051-0.145 Hz; IV –
frequency band between 0.15-0.5 Hz; V –
frequency band between 0.01-0.02 Hz. In each
band range there is a different factor which
determines blood flow oscillation. I – shows
vascular oscillations depending on the
endothelium metabolic activity (EF); II – shows
the effect of the sympathetic system on skin flow
(SF); III – illustrates oscillations resulting from the
arteriola basic systolic tonus which occurs due to
discharges of particular myocytes forming a
circular layer of the vessel muscle coat, this
response is often referred to as myogenic and it is
independent of the sympathetic system (MF); IV –
breath frequency (BF); V – heart frequency (HF).
Time of 0.03 s was selected, and every blood flow
signal was taken at the frequency of 32 Hz
(Kvernmo et al., 1999). Apart from frequency, the
signal power (SP) was also analyzed.
The distribution of dependent variables
was tested with the use of the Shapiro-Wilk test.
The differences between the tested variables in
specific periods (dependent variables), as well as
between men and women (independent variable),
were evaluated with the use of analysis of
variance (ANOVA) with repeated measurements.
In case of significant effects the differences among
the medians were evaluated with the post hoc
multiple comparisons test (Tukey test). The values
of the variables are shown as mean (x) ± standard
deviation (SD). The level of statistical significance
78 Impact of 10 sessions of whole body cryostimulation on cutaneous microcirculation measured
Journal of Human Kinetics volume 30/2011, http://www.johk.pl
was set at p<0,05.
All participants were informed about the
aim and course of the experiment and signed their
written consents. The experiment was accepted by
Bioethical Committee of the Regional Medical
Council in Opole (Resolution No 163/2009).
Results
After a series of WBCT the resting flow
(RF) increased significantly both in women
(p=0,0001) and in men (p=0,01). After subsequent
10 days the values of RF decreased insignificantly
compared to values recorded right after the
procedures. No interactions between men and
women were noticed.
Biological zero did not change
significantly at any stage.
A statistically significant increase of mean
values of post-occlusive hyperaemic reaction was
observed during the second measurement in both
groups: women (p=0,0001) and men (p=0,0001).
Although the increase in women was significantly
higher than in men (p=0,0005). The mean values of
third measurement did not alter significantly
compared to the second measurement. The values
of HRmax were also significantly increased at the
second measurement in both groups (women-
p=0,0001, men -p=0,0001), whereas after 10 days
the values fell in women and rose in men. The
interaction between men and women was
statistically significant p=0,01.
After a series of WBCT, there was a
significant increase of mean and maximal values
of microcirculation’s reaction to temperature
(mean values:women- p=0,0001, men - p=0,0001).
The third measurement showed an insignificant
increase of the studied variable in men and
similarly insignificant decrease in women,
compared to values from the second
measurement. The interaction was not significant
(p=0,08). In turn, the maximal values increased in
women and decreased in men. Interaction was
significant (p=0,00005).
Table 2
Mean values (x) and standard deviation (SD) of the analyzed variables in succeeding
measurements for both sexes with statistical verification
Variables
[VU]
Sex I measurement
(x±SD)
II measurement
(x±SD)
III measurement
(x±SD)
RF F 10.32±2.56 10.89±2,31* 10.11±3.17
M 13.67±3.19 14.25±4.93* 13.83±4.68
BZ F 2.77±0.11 2.69±0.24 2.81±0.41
M 2.66±0.21 2.48±0.06 2.41±0.52
RH F 75.13±17.99 108.85±33.88* 110.84±30.02**
M 101.44±27.42 121.93±38.41* 123.94±40.42**
RHmax F 88.56±23.26 117.32±38.93* 119.43±41.44**
M 127.56±34.81 149.32±46.82* 148.77±39.88**
TH F 143.88±43.9 186.24±37.77* 180.38±40.81**
M 171.21±49.11 206.02±45.02* 209.01±30.86**
THmax F 169.42±49.11 194.82±44.91* 199.52±36.77**
M 196.34±58.11 229.02±51.72* 222.09±34.45**
VAR [%] F 38.44±4.97 49.38±5.99* 50.1±4.75**
M 42.33±5.08 55.42±6.12* 57.19±6.39**
* statistically significant differences between I and II measurement
** statistically significant differences between I and III measurement
RF – mean values of rest flow; BZ – mean values of biological zero
RH – mean values of reactive hyperemia
RHmax – maximal values of reactive hyperemia
TH - mean values of thermal hyperemia
THmax – maximal values of thermal hyperemia
VAR -arterio – venous reflex index
by Szyguła R. et al. 79
© Editorial Committee of Journal of Human Kinetics
Table 3
Mean values (x) and standard deviation (SD) of the variables analyzed in basal flow
in particular frequencies in succeeding measurements
for both sexes with statistical verification
I measurement I measurement I measurement
Frequency
of signals
[cycles/min]
Signal
power
Frequency
of signals
[cycles/min]
Signal
power
Frequency of
signals
[cycles/min]
Signal
power
HF F 71.87±3,19 0.64±0,22 65.22±3.44* 0.69±0.11 66.19±3.01** 0.68±2.89
M 68.83±5.12 0.7±0.31 62.6±4.66* 0.73±0.19 62.9±3.87** 0.71±1.37
BF F 12.81±0.87 0.51±0.19 13.03±2.12 0.51±0.17 13.01±1,01 0.49±0.1
M 12.02±0.59 0.49±0.2 12.73±0.72 0.47±0.11 12.71±0.91 0.5±0.09
MF F 5.95±0.49 1.64±1.02 6.76±0.77* 1.66±0.9 6.81±0.64** 1.54±0.91
M 6.11±0.71 1.73±0.99 6.81±0.56* 1.69±0.85 6.8±0.59** 1.69±0.75
SF F 1.9±0.46 0.52±0.31 2.04±0.62* 0.5±0.39 2.0±0.57 0.52±0.36
M 2.0±0.41 0.46±0.26 2.03±0.44 0.49±0,33 2.05±0.49 0.49±0.31
EF F 0.9±0.0 3.82±1.03 0.9±0.0 4.01±1.57 0.9±0.0 3.92±1.35
M 0.9±0.0 3.87±0.97 0.9±0.0 3.79±1.06 0.9±0.0 3.99±1.76
* statistically significant differences between I and II measurement
** statistically significant differences between I and III measurement
HF – mean values of heart frequency; BF – mean values of breath frequency
MF – mean values of myogenic frequency
SF – mean values of sympathetic frequency
EF – mean values of endothelium frequency
The arterio–venous reflex index
(microcirculation’s reaction to change of position)
was significantly higher after WBCT in both
groups (women- p=0,0001, men - p=0,0001). Ten
days later men showed further significant
increase compared to the second measurement
(p=0,01). In women the increase was insignificant.
The interaction between men and women was
significant (p=0,00018).The recorded results
(values recorded for post-occlusive hyperaemic
reaction, reaction to temperature and the arterio–
venous reflex index) are shown in Table 2.
The myogenic frequency (MF)
significantly rose in the second measurement
compared to the first one in both men and women
(p=0,0001) and on the third measurement did not
change significantly with values close to those
obtained during the second measurement.
Heart frequency (HF) decreased
remarkably after cryostimulation (F, M p=0,0001)
and remained stable after ten days in both groups.
Neurogenic rhythm (SF) increased
significantly after cryostimulation in women
(p=0,016).
Other variables did not alter significantly.
The recorded results (the values of frequency in
the range of 0,01 Hz to 2 Hz) are shown in Table 3.
Discussion
Despite the fact that WBCT has become an
accepted physiotherapy method, it remains
unclear how the extremely low temperatures
work, what is the optimal number of sessions and
how long the positive therapeutic effects for the
cutaneous microcirculation last. In healthy
individuals the analgesic and relaxing effects
persist for several months after a series of
cryotherapy sessions (Zagrobelny and Zimmer,
1999; Wojtecka-Lukasik et al., 2010). In this study
10 cryogenic sessions were applied during 10
consecutive days as this is the most frequently
applied procedure, recommended by the
producers of cryogenic chambers, which does not
mean it is optimal. Lubkowska et al. (2010a)
proved that best therapeutic effect was observed
after 20 sessions. The flows in the cutaneous
80 Impact of 10 sessions of whole body cryostimulation on cutaneous microcirculation measured
Journal of Human Kinetics volume 30/2011, http://www.johk.pl
microcirculation were measured with the use of
laser Doppler flowmeter. It is a safe, non-invasive
and reproducible method and it records data from
thermoregulation area of the vessel bed excluding
the tissues underneath (Rousti et al., 2010;
Sokolnicki et al., 2009). No reference values have
been determined for this method, therefore the
status of the skin vessel bed is defined with the
use of provoked reactions to heat, occlusive or
orthostatic stimulus. Many authors studied
changes in skin microcirculation after local
cooling but there are no data regarding the impact
of extreme low temperature (WBCT) in this area.
The results obtained by the authors
showed that a series of 10 WBCT sessions did not
lead to significant changes in basal blood flow
measured one and ten days after the sessions. The
values were in the range of 10 – 20 PU, presumed
by Oimomi et al. (1985) as normal. In women the
values of baseline RF were lower than in men,
which was previously reported by other authors
(Pollock et al., 1993; Maurel et al., 1991).
Authors’ own research showed
significantly increased values of post-occlusive
hyperaemic reaction after a series of WBCT in the
second and third measurement that was similar in
both female and male group. The mechanism of a
hyperaemic reaction to occlusion is similar to the
response to extremely low temperatures. Initially,
hypoperfusion of the tissues occurs, leading to a
decrease in pO2 and accumulation of the
metabolites that results in active hyperaemia after
cessation of the stimulus (Strucl et al., 1994).
WBCT provokes active reperfusion of the skin
microcirculation of the whole body of much more
profound intensity than in case of local occlusive
stimulation. It can be presumed that a better
reaction of the skin microcirculation to occlusion
in the second and third measurement resulted
from increased reactivity of the smooth muscles of
the vessels that adapted their function to
cryogenic temperatures applied. Increased
frequency in the range of 0,051 – 0,145 Hz
suggests that extremely low temperature impacts
the myogenic control of the blood flow, although
the mechanism of the adaptation requires further
studies.
Authors’ own research used heat stimulus
of 44°C as this temperature warrants maximal
response of the skin vessel bed (Charkoudian,
2003). In the first phase a rapid vasodilation
occurs due to heat dependent decreased
sympathetic stimulation, later hyperaemia is
sustained by increased NO secretion (Brothers et
al., 2010; Rousti et al., 2010; Minson et al., 2001).
Significantly higher values of hyperaemic reaction
to heat were recorded after a series of WBCT
compared to initial values. It can be explained by
a more efficient response of the cutaneous
microcirculation to decreased sympathetic
stimulation. Better reactivity of the
microcirculation may also explain a 50% decrease
in blood flow in the arterio–venous reflex index.
Change of the position from horizontal to vertical
is a strong stimulus provoking vasoconstriction in
order to avoid a rapid and excessive increase of
hydrostatic pressure.
There is a remarkable decrease in
frequency in the range of 0,01 – 0,02 Hz. Most
probably it results from a move of the autonomic
balance towards parasympathetic component.
Such a reaction to extremely low temperature was
reported by Lee et al. (2011).
The cryostimulation–related increase in
neurogenic rhythm noted only in women can be
explained by higher levels of estrogens. The
estrogens induce increased susceptibility of the α2
adrenergic receptorsby increasing the oscillation
neurogenic (Colucci et al., 1982).
The variations between men and women
are most likely related to the hormonal
differences. Over the last decade, the impact of
sex hormones on skin microcirculation in women
and men have been analyzed. Most studies were
concentrated on estrogens, which decrease the
number of angiotensin type 1 receptors (AT1) and
the concentration of angiotensin convertase
inhibitors (ACE) that results in vasodilation.
Estrogens modulate the function of the
baroreceptors and ion channels (K+, Ca2+) as well
as increase endothelium-dependent vaso-dilating
mechanisms by regulating the expression of genes
of nitric oxide synthase (eNOS) or endothelin-1.
They also stimulate the synthesis of
prostaglandins (PG) and increase the
susceptibility of the vessels to acetylcholine (Ach).
Progesterone and testosterone also influence sex-
related regulation of the vessel bed but their role
remains controversial. Some authors report their
vasodilating function whereas other suggest their
vasoconstrictive effects (Mercuro et al., 1999;
Sudhir et al., 1996; Huang and Kaley, 2004;
by Szyguła R. et al. 81
© Editorial Committee of Journal of Human Kinetics
Gonzales et al., 2008).
There is no doubt that the activity of sex
hormones has an impact on flows in the skin
microcirculation and on reactivity of the skin
vessel bed and that the differences in their
concentration are probably responsible for the
interaction between the groups of men and
women. Although the impact of hormones on
circulation in women and men still remains
unclear and warrants further studies.
The values recorded in the second and
third measurement were very similar and
significantly higher compared to the first
measurement, which suggests positive impact of
10 sessions of WBC on skin microcirculation and
persistence of the effect for the following 10 days.
Lack of similar studies makes a comparison
difficult and shows the need for further studies.
Conclusions
A series of 10 procedures of whole body
cryostimulation resulting in a significant increase
of post-occlusive hyperemic reaction, hyperemic
reaction to temperature and orthostatic reaction in
both women and men suggests positive effects of
extremely low temperatures on reactivity of the
skin microcirculation in healthy persons,
persisting during whole cryostimulation period.
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Corresponding author:
Dr Renata Szyguła
Department of Physical Education and Physiotherapy, Technical University, Opole, Poland.
Prószkowska 76
45-758 Opole
Poland
Phone: 697310368
Email: r.szygula@po.opole.pl
