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Evidence-Based Complementary and Alternative Medicine
Volume 2011, Article ID 804321, 12 pages
doi:10.1093/ecam/nep171
Original Article
Connective Tissue Reflex Massage for Type 2 Diabetic Patients
with Peripheral Arterial Disease: Randomized Controlled Trial
Adelaida Mar´
ıa Castro-S´
anchez,1Carmen Moreno-Lorenzo,2
Guillermo A. Matar´
an-Pe˜
narrocha,3Belen Feriche-Fern´
andez-Castanys,4
Genoveva Granados-G´
amez,5and Jos´
e Manuel Quesada-Rubio6
1Department of Nursing and Physical Therapy, University of Almeria, 04120 Almer´ıa, Spain
2Department of Physiotherapy, University of Granada, Spain
3Health District of La Vega, Andalusian Health Service (M´alaga), Spain
4Department of Physical Education, University of Granada, Spain
5Department of Nursing and Physical Therapy, University of Almeria, Spain
6Department of Statistics, University of Granada, Spain
Correspondence should be addressed to Adelaida Mar´
ıa Castro-S´
anchez, adelaid@ual.es
Received 23 April 2009; Accepted 2 October 2009
Copyright © 2011 Adelaida Mar´
ıa Castro-S´
anchez et al. This is an open access article distributed under the Creative Commons
Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is
properly cited.
The objective of this study was to evaluate the efficacy of connective tissue massage to improve blood circulation and intermittent
claudication symptoms in type 2 diabetic patients. A randomized, placebo-controlled trial was undertaken. Ninety-eight type 2
diabetes patients with stage I or II-a peripheral arterial disease (PAD) (Leriche-Fontaine classification) were randomly assigned to
a massage group or to a placebo group treated using disconnected magnetotherapy equipment. Peripheral arterial circulation was
determined by measuring differential segmental arterial pressure, heart rate, skin temperature, oxygen saturation and skin blood
flow. Measurements were taken before and at 30 min, 6 months and 1 year after the 15-week treatment. After the 15-week program,
the groups differed (P<.05) in differential segmental arterial pressure in right lower limb (lower one-third of thigh, upper and
lower one-third of leg) and left lower limb (lower one-third of thigh and upper and lower one-third of leg). A significant difference
(P<.05) was also observed in skin blood flow in digits 1 and 4 of right foot and digits 2, 4 and 5 of left foot. ANOVA results were
significant (P<.05) for right and left foot oxygen saturation but not for heart rate and temperature. At 6 months and 1 year, the
groups differed in differential segmental arterial pressure in upper third of left and right legs. Connective tissue massage improves
blood circulation in the lower limbs of type 2 diabetic patients at stage I or II-a and may be useful to slow the progression of PAD.
1. Introduction
Peripheral arterial disease (PAD) is a common disease world-
wide and is associated with a high rate of disability [1,2].
Diabetes is one of the main causes of PAD. The development
of vascular complications in diabetics depends on the length
of time with the disease and their glycemia control [3]. At
endothelial level, diabetic vascular complications can lead to
luminal changes, affecting fibrinolysis, plasma coagulation,
platelet function, and to parietal changes in contractile and
secretory functions [4,5]. Diabetics also have a diminished
endothelium-dependent arterial relaxation capacity, due
to self-generating changes in the generation, release, and
association of self-produced vasodilatory substances [6].
Nitric oxide-mediated vasodilation is also affected, since
nitric oxide is deactivated by free radicals and advanced
glycation end products [7,8].
Intermittent claudication (IC) is a transient ischemia
caused by the inability of the vascular system to meet
muscle metabolic requirements. It usually clinically mani-
fests as a constrictive pain in the lower leg, although this
pain can also be reported in the thigh or foot in pre-
claudication conditions [9]. The pain can appear earlier
during steep or fast walks or at low temperatures. Other
symptoms associated with IC are cold feet and mottled
hairless skin with dryness or ulcerations. IC symptoms can
remain stable, heal spontaneously, or develop into chronic
ischemia of the lower limbs. It is well documented that
2 Evidence-Based Complementary and Alternative Medicine
around 5% of men and 2.5% of women aged >60 years
have IC symptoms [1]. Leriche-Fontaine established a four-
stage clinical classification of chronic lower limb ischemia.
Stage I is characterized by atheroma plaque symptoms, but
blood vessel obstruction is incomplete and compensatory
mechanisms have developed. In stage II, pain in lower limb
muscle groups, mainly calf muscles, is triggered by walking
and eases after rest: symptoms appear after a distance of
>150 m in stage II-a and after <150 m in stage II-b. In stage
III, the patient experiences pain while resting that worsens
when the limb is raised; the pain is mainly localized in the
feet, which become sensitive and cold and take on a pale
or red (erythematous) appearance. In stage IV, the patient
has ulcerations and limb necrosis and finds walking difficult
[10]. In stages III and IV, chronic lower limb ischemia is
mainly treated surgically by thrombectomy, embolectomy,
fasciotomy, thromboendarectomy, bypass or amputation
along with pre- and post-surgical drug treatments [11].
In stage II, treatment largely consists of diabetic control
[12], non-pharmacological methods (physiotherapy, Yoga
programs, antioxidant plants) [13–18], genetic therapy,
and/or medication [19–21]. Patients with stage I disease
receive no therapy because they show no symptoms. It is
therefore important to implement measures to detect initial
stages of PAD and to control risk factors [22]. A review of
the literature on subclinical PAD diagnosis concluded that
individuals with risk factors (obesity, cholesterol, sedentary
lifestyle, smoking, dyslipemia) and positive family history
should undergo vascular Doppler examination (to calculate
ankle/brachial index (ABI)) and arterial plethysmographic
examinations (arterial neumoplethysmography and photo-
plethysmography) [23–27].
Connective tissue massage (CTM) may reduce symptoms
and improve IC by increasing blood circulation to the
musculature. This is achieved by massaging along reflex
lines on areas of the skin connected (at a distance) with
deep tissue and internal organs, known as Head zones
[28,29]. The hypertonic muscle region is known as the
McKenzie zone, while tissues linked to internal organs
via nerve connections are called Dicke’s connective zones.
Stimulation of these areas generates a neuro-vegetal balance
that produces a relaxed and analgesic state in the patient
and a regulation of vasomotricity in areas distantly linked
via nerve connections. CTM always begins in areas away
from hyperalgic points in affected methameric muscles to
avoid painful reactions. Loose connective tissue is stretched
and stimulated by the massage to produce a neurovegetal
balance, which skin-muscle reflex massage mainly achieves
via the autonomous or vegetal nervous system. The stimulus
produced at subcutaneous connective tissue level relaxes
contracted tissues and improves the circulation due to
vasodilation mediated by the vegetal nervous system [30,31].
To our best knowledge, however, no specific evaluation has
been published on the effects of CTM in patients with PAD.
With this background, the objective of this study was to
determine the efficacy of a CTM program to improve blood
circulation and IC symptoms in the lower limb and to serve
as a preventive measure against the progression of PAD in
type 2 diabetic patients. This approach may be of special
interest for patients unable to take part in physical exercise
programs.
2. Methods
2.1. Setting and Participants. This randomized, placebo-
controlled trial initially recruited all accessible patients with
medical records on the computer database of a Health-
care District in Southern Spain who were diagnosed with
and undergoing treatment for type 2 diabetes: a total of
146 patients. Study enrolment was from September 1 to
December 20, 2005. The 146 patients underwent an initial
examination (see below), and their consent was obtained
to review their clinical records to gather clinical data,
including medication history and date of type 2 diabetes
mellitus diagnosis, defined by oral glucose tolerance test of
>200 mg/dL or fasting blood glucose test of >126 mg/dL on
two separate occasions during the previous year.
The physical examination was conducted after >3h
without food intake and >4 h without medication [32],
measuring the ABI with the patient in supine position after
a Stradness test (10% gradient treadmill at 3 km h−1up
to maximum tolerated walking distance) [33]. An 8 MHz
Doppler probe (Hadeco Smartdop SD-20) and mercury
sphygmomanometer were used for this measurement, deter-
mining systolic blood pressure (SBP) first in the right and
left brachial arteries and then in the right and left posterior
tibial arteries. The ABI was obtained by dividing the SBP
of the posterior tibial artery in each extremity by the
SBP of the brachial artery [25,34]. The examination also
yielded glycosylated hemoglobin and BMI values, calculated
as weight (kg) divided by height squared (m2).
Study inclusion criteria were: diagnosis of type 2
diabetes; ABI of 0.6–0.9 on post-procedural Strandness
test (declared equivalent to stages I and II-a of Leriche-
Fontaine classification by the American Diabetes Association
and American College of Cardiology) [35]; glycosylated
hemoglobin of 7–10%; age of 18–65 years, and BMI of 27–35.
Exclusion criteria were: PAD stage II-b or higher; peripheral
venous insufficiency; cardiac, renal, or hepatic insufficiency;
uncontrolled hypertension (SBP >165/95 mmHg); central
or peripheral nervous system disorders; or myopathic or
neurologic damage that impaired mobility. These criteria
were satisfied by 98 patients (58 females and 40 males), who
gave their written consent to participation after being fully
informed about the study and told that they would be able
to choose the days and times of measurement and treatment
sessions. The study was approved by the ethics committees
of our university (University of Almeria) and hospital
(Andalusian Health Service). Patients were assigned to one
of two groups by using a randomized balanced (stratified)
selection process. The groups were balanced for type of
medication received and Leriche-Fontaine stage (I or II-a),
using a stratification system that generates a sequence of
letters (from table of correlatively ordered permutations) for
each category and combination of categories. The assessor,
massage and magnotherapy therapists, and patients were not
blinded to the treatment allocation of patients. The trial was
Evidence-Based Complementary and Alternative Medicine 3
conducted between January 15, 2005 and March 30, 2008.
The participants were asked to make no significant changes
in diet, therapy, or daily activities during the course of the
study [36].
2.2. Measurements. The data gathered for the selection
process were considered the baseline measurements. The
maximum interval between baseline data collection and start
of the program was one day. The same data were collected
at 30 min, 6 months, and one year after the program. At
these evaluation sessions, we always took the following
measurements in the order given below:
2.2.1. Walking Impairment. This was assessed by administer-
ing a validated Walking Impairment Questionnaire for PAD
patients that contains items on difficulties to walk a given
distance and at a given speed during the previous month and
on symptoms associated with walking impairment [32]. The
degree of difficulty was scored as none (3 points), some (2
points), great (1 point) or as no walking activity (0 point).
The walking distance score was the sum of the following
points: 20 points for walking indoors, 50 points for walking
50, 150 for 150, 300 for 300, 600 for 600, 900 for 900,
and 1500 points for walking 1500. The walking speed score
was the sum of the following points: 1.5 for walking slowly,
2 for walking at average speed, 3 for walking quickly, and
5 for running or jogging. Each distance walked is used as a
weighting factor in the estimation of the walking difficulty.
Walking distance scores range from 0 to 34.5 and walking
speed scores from 0 to 6.60 [32].
2.2.2. Differential Segmental Arterial Blood Pressure. This
was estimated in both lower limbs using a plethysmograph
(MOD-PGV-20, Smart-V-Link, Quermed, Madrid) at the
proximal and distal thirds of thigh and leg; values were
expressed in mmHg. Briefly, a blood pressure cuffwas placed
on the corresponding lower limb segment, and a pressure
transducer in the plethysmograph was used to record BP
changes (for 60 s) after occlusion of the venous system at
75 mmHg. The differential segmental arterial pressure is the
difference between systolic and diastolic arterial pressures
[27]. Figure 1 shows the plethysmography results for the limb
segments.
2.2.3. Differential Voltage in Skin Blood Flow. Blood flow
changes were measured on each digit of both feet by photo-
plethysmography (MOD-PGV-20, Smart-V-Link, Quermed,
Madrid), with mV/V as the unit of measurement. Photo-
plethysmography is based on the principle that the infrared
range of light-emitting energy reflects the blood flow in
subcutaneous arteries. The source of infrared transmission
is the diode, which is placed next to the cadmium-selenium
photosensor receiver at a pressure of 5–40 mmHg. Most of
the light emitted by the diode is absorbed by the tissues,
and only 5–10% reaches the subcutaneous blood vessels. The
magnitude of light reflected by these blood vessels increases
with higher red blood cell density [37]. The reflected energy
is amplified and converted into a voltage differential. The
apparatus was calibrated such that a 1% increase in blood
flow corresponded to two squares on the plethysmograph
thermographic paper [38–41](Figure 2).
2.2.4. Heart Rate and Oxygen Saturation. These measure-
ments were taken with a pulseoxymeter (Megos 3300 Oxi-
pulso) placed on the second digit of right and left foot after
patients had rested (in supine) for 5 min. In connective tissue
reflex massage, changes in heart rate (bpm) and oxygen
saturation (%) are produced by the vasodilation produced.
2.2.5. Skin Temperature. Skin temperature (in ◦C) was
measured for 5 min in the inguinal region and right and
left popliteal spaces using a thermographic scan (Emergen
dermatempt).
2.3. Intervention. The massage group received a 1-h session
of CTM twice a week for 15 weeks. The placebo group
received a 30-min session of sham magnetotherapy in the
lower back and popliteal regions (15 min per zone) twice
a week for 15 weeks using disconnected equipment; these
patients were instructed on the use of the magnetotherapy
equipment and were unaware that it was switched off.
Because all patients were treated in prone position on a
massage bed with a face hole, placebo patients were unable to
see the equipment during sham treatment. The therapy room
was maintained at a temperature of 29.8–34.5◦C(Oregon
scientific model 299N) and relative humidity of 39–42%
(Oregon scientific model 299N).
2.3.1. Massage. The therapists applied standard therapeutic
CTM, using the Dicke approach 42. The massage protocol
consisted of reflex-massaging the skin with the third and
fourth fingertips to stretch the subcutaneous connective
tissue to the maximum. The massage must not cause pain
or enter deep into structures under the connective tissue,
avoiding overstimulation. The therapist flexes the elbow away
from the body, rotates the shoulder internally and applies a
light radial twist to the wrist. The patient should experience
the massage as a “switching-off” feeling.
Before the massage, patients remained in a relaxed prone
position for 30 min. At each therapy session, the full massage
protocol was applied as follows. After an initial “base build-
up” with lumbosacral and pelvic massage strokes [42,43],
alternate strokes from left to right were applied to the
spinal axis, always in the following order [44]: five short
curving movements from fifth to first lumbar vertebra, five
movements at angle of lumbosacral joint, five short curving
movements from intercostal proximal third to dorsal axis
and up to spinal apophysis, seven light strokes in intercostal
spaces, seven short curving movements from intercostal
proximal third to dorsal axis and up to spinal apophysis (DVI
to DVII), five transverse intercostal movements from spine
to inner edge of scapula, one deep upward movement along
inner edge of scapula, one light stroke along axillary edge of
scapula and a final movement along anterior side of scapular
spine. The following sequence of massage strokes was then
applied to the lower limbs: three strokes at origin and
4 Evidence-Based Complementary and Alternative Medicine
Derecha
Muslo superior
Izquierd Imprimir Volver
To b i l l o
Dedo grodo
Cambios (mmHg)
Cambios (mmHg)
Cambios (mmHg)
Cambios (mmHg)
Muslo superior
To b i l l o
Dedo grodo
Cambios (mmHg)
Cambios (mmHg)
Cambios (mmHg)
Cambios (mmHg)
Cambios (mmHg) Cambios (mmHg)
4.06 mmHg
4.37 mmHg
5.6 mmHg
3.24 mmHg
2.09 mmHg
4.62 mmHg
4.41 mmHg
2.93 mmHg
Smart-V-Link
HADECO
PV arterial
∗∗∗.∗mmHg ∗∗∗ .∗mmHg
1.6
0
−1.6
1.6
0
−1.6
1.6
0
−1.6
1.6
0
−1.6
1.6
0
−1.6
1.6
0
−1.6
1.6
0
−1.6
1.6
0
−1.6
PVPVPVPV
PVPVPVPV
Encima de la rodilla
Debaio de la rodilla
Encima de la rodilla
Debaio de la rodilla
Figure 1: Differential segmental arterial blood pressure in lower limbs is the difference between systolic and diastolic arterial pressures in
the segment under study. The wider the difference, the greater is the arterial blood flow.
Systolic peak
Diastolic peak
−1
0
1
2
(mV/V)
PPG
AC
PP: 0.5 mV/V HR: 80 BPM
(a)
Systolic peak
Diastolic peak
(mV/V)
−4
0
4
8PP: 9.5 mV/V HR: 89 BPM
PPG
(b)
Figure 2: Voltage differential in skin blood flow is the difference
between the voltage reached at systolic versus diastolic arterial
peaks.Thewiderthevoltagedifference, the greater is the supply of
arterial blood to the skin, as a consequence of vasodilation upper
panel (a) shows a lower skin blood flow than that observed in lower
panel (b).
insertion of ischiotibial muscles, three short strokes on both
sides of tensor fascia latae muscle, one lateral stroke from
distal region of iliotibial band to lateral side of knee, three
long strokes in triceps surae area towards each lateral side of
popliteal space, three long strokes on foot from lateral edge
of the calf muscles to lower edge of malleolus, three short
strokes upwards from lateral edges of vastus externus and
internus towards muscle fibers, two upward lateral strokes
on lateral outer side of vastus externus and lateral inner
side of vastus internus, four short strokes towards patella,
three transversal strokes from right to the left side under
tibial crest, one downward stroke from outer side of knee
to fibular malleolus, five short strokes in tibioastragalar area,
five short strokes on lateral outer edge of foot towards the
plantar cushion, four short strokes on interosseous muscles
and, finally, one long stroke from calcaneus to metatarsus-
phalanx joint in plantar area. After the massage, the patient
remained in a relaxed supine position for 30 min.
2.4. Statistical Analysis. SPSS statistics software (version
17.0) was used for statistical analyses. The reliability and
validity of the model was studied by analyzing residual inde-
pendence, normality, and variance homogeneity. Residual
independence was analyzed by plotting the values obtained
against residues, resulting in randomly distributed points
showing no specific trend and therefore verifying the residual
independence assumption. Residual normality was studied
by using a Q-Q graph, finding the dots to be located close
to the line and therefore confirming the residual normality
assumption. Variance homogeneity was tested with the
Levene test, obtaining a 95% confidence level and P-value
>.05, confirming variance equality. The normal distribution
of variables was determined by using the Kolmogorov-
Smirnof test, expressing continuous data as means with
standard deviation (SD) in the text and tables. Changes in
Evidence-Based Complementary and Alternative Medicine 5
Assessed for eligibility (n=146)
Randomized (n=98)
Allocated to intervention (n=49)
Perceived allocated intervention (n=48)
Did not receive allocated intervention (n=1)
Reason: Need for bed rest
Followed up at 30 min, 6 months and 1 year
Analyzed (n=48)
Allocated to intervention (n=49)
Received allocated intervention (n=46)
Did not receive allocated intervention (n=3)
Reasons: Need to care for severely ill or
disabled relatives
Followed up at 30 min, 6 months and 1 year
Analyzed (n=46)
Intervention
group Placebo
group
Excluded (n=48)
Didnotmeetinclusioncriteria(n=39)
Refused to participate (n=6)
Other reasons (n=3)
Figure 3: Flow chart of study participation None of the 98 randomized patients withdrew because of adverse events.
variables within each group were measured using the paired
t-test for independent samples. Temporal changes in the
scores were examined using a two-way repeated measures
ANOVA (group (massage group, placebo group) ×time
(baseline, 30 min, 6 months, 1 year)). Treatment efficacy was
analyzed by using a t-test for paired samples. Independent
t-tests were applied to baseline scores to determine whether
the random assignment to groups adequately controlled for
baseline demographic differences.
Relationships between variables at baseline and post-
treatment were assessed by calculating the Pearson correla-
tion coefficients, considering a 95% (α=0.05) confidence
level.
3. Results
3.1. Participants. The 98 patients (58 women and 40 men)
in the study group had a mean age of 53.57±11.69 years
(range 41–65 years). One patient dropped out of the massage
group and three from the placebo group (Figure 3) due to
mandatory bed rest (n=1) or the need to care for severely
ill relatives (n=3). No patient withdrew from the study due
to adverse effects of the intervention.
No significant differences in baseline characteristics
were observed between the massage and placebo groups
(Figure 4).
3.2. 30-Min Outcomes. At 30 min after the 15-week program,
mean differential segmental arterial pressure values (by
plethysmography) were significantly (P<.05) improved
versus baseline values (right and left leg) in the massage
group, with the greatest improvements in upper third of
the right thigh (1.69 (0.83) mmHg; P<.035), lower third
of right thigh (2.09 (0.64) mmHg; P<.031), upper third
of right leg (3.22 (1.15) mmHg; P<.029), upper third of
left thigh (1.54 (0.47) mmHg; P<.004), lower third of left
thigh (1.62 (0.94) mmHg; P<.021), and upper third of left
leg ( 2.57 (1.08) mmHg; P<.024). No significant pressure
changes were observed in the placebo group. Significant
differences were found between massage and placebo group
in differential arterial pressure values in the lower third of
right thigh, upper third of right leg, lower third of right
leg, lower third of left thigh, and upper third of left leg
(Tab l e 1). Repeated-measures ANOVA showed a significant
time ×groups interaction for differential arterial pressure
values in lower third of right third (F=8.289; P<.03),
upper third of right leg (F=7.321; P<.03), lower third
of right leg (F=11.201; P<.04), lower third of left thigh
(F=7.323; P<.05), and upper third of left leg (F=9.321;
P<.01).
A similar pattern was observed for the differential voltage
in digits. Significant (P<.05) improvement from baseline
in the massage group was observed in differential voltage in
right first digit (3.10 (3.37) mV/V; P<.014), right second
6 Evidence-Based Complementary and Alternative Medicine
47.88
49.25
47
47.5
48
48.5
49
49.5
Age
Mean
(a)
Mean
25.96
26.16
25.85
25.9
25.95
26
26.05
26.1
26.15
26.2
Body mass index
(b)
159
155
153
154
155
156
157
158
159
160
Systolic blood pressure (mmHg)
Intervention group
Placebo group
(c)
Intervention group
Placebo group
88
87
87.5
90
88
88.5
89
89.5
90
90.5
Dyastolic blood pressure (mmHg)
(d)
Figure 4: P<.05 between intervention and placebo groups.
digit (3.93 (2.77) mV/V; P<.024), right fourth digit (6.50
(2.82) mV/V; P<.017), right fifth digit (6.30 (3.77) mV/V;
P<.014), left second digit (6.27 (2.54) mV/V; P<.022),
left fourth digit (5.36 (4.81) mV/V; P<.003) and left fifth
digit (6.58 (6.13) mV/V; P<.001). In the placebo group,
no significant change in differential voltage was observed
in any digit (Ta b le 2). ANOVA showed a significant time ×
groups interaction for differential voltage in right first digit
(F=7.984; P<.03), right fourth digit (F=8.321; P<.01),
left second digit (F=7.224; P<.04), left fourth digit
(F=6.932; P<.05), and left fifth digit (F=8.846; P<.01).
No significant changes in heart rate values were observed
in either group between baseline and post-treatment
(Figure 5). In the massage group, skin temperature signifi-
cantly (P<.05) differed between baseline and the end of
the 15-week treatment in right inguinal fold (35.52 (0.78)◦C;
P<.037), left inguinal fold (35.99 (0.47)◦C; P<.048), right
popliteal space (35.82 (0.39)◦C; P<.039), and left popliteal
space (35.13 (0.75)◦C; P<.042). Significant differences
were also found (baseline versus 15 wks) in oxygen saturation
values in right foot (97.92 (2.93)◦C; P<.026) and left
foot (98.09 (2.64)◦C; P<.008). The placebo group showed
Evidence-Based Complementary and Alternative Medicine 7
Tab le 1: Differences between groups in differential segmental arterial pressure in lower limbs.
Variable
(mmHg)
Baseline M(SD) Pvalue
Pre-T
30 min post-program
M(SD) Pvalue
1st-PT
6monthsM(SD) Pvalue
2nd-PT
1yearM(SD) Pvalue
3rd-PT
IG PG IG PG IG PG IG PG
UTRT 1.09
(0.44)
1.17
(0.32) .32 1.69
(0.83)
1.21
(0.76) .07 1.50
(0.49)
1.24
(0.29) .09 1.48
(0.33)
1.19
(0.41) .11
LTRT 1.49
(0.06)
1.22
(0.12) .10 2.09
(0.64)
1.15
(0.51) .03∗1.87
(0.55)
0.89
(0.83) .04∗1.56
(0.94)
1.06
(0.36) .07
UTRL 2.31
(0.97)
1.79
(0.72) .07 3.22
(1.15)
1.88
(0.67) .03∗2.91
(1.05)
1.87
(0.58) .04∗2.49
(0.61)
1.86
(0.90) .04∗
LTRL 0.90
(0.06)
0.60
(0.97) .99 1.21
(0.11)
0.57
(0.06) .05∗1.18
(0.99)
0.69
(0.64) .08 1.03
(0.43)
0.64
(0.96) .09
UTLT 1.05
(0.34)
1.12
(0.82) .35 1.54
(0.47)
1.09
(0.71) .08 1.31
(0.58)
1.11
(0.45) .15 1.26
(0.23)
1.08
(0.55) .23
LTLT 1.39
(0.73)
1.13
(0.79) .10 1.62
(0.94)
0.99
(1.01) .05∗1.54
(0.88)
0.86
(0.72) .05∗1.41
(0.62)
0.98
(0.34) .08
UTLL 1.66
(2.57)
1.32
(0.99) .98 2.57
(1.08)
1.33
(0.92) .01∗2.21
(0.83)
1.35
(0.64) .04∗1.98
(0.51)
1.29
(0.63) .04∗
LTLL 0.89
(0.31)
0.92
(0.87) .67 1.12
(0.57)
0.97
(0.56) .18 1.07
(0.46)
0.94
(0.38) .25 0.99
(0.712)
0.90
(0.57) .36
Values are presented as mean (SD). RMG, reflex massage group; PG, placebo group; 1st PT, post-treatment (30 min after 15-week treatment ends); 2nd PT,
6 months post-treatment; 3rd PT, 1 year post-treatment; UTRT, upper third of right thigh; LTRT, lower third of right thigh; UTRL, upper third of right leg;
LTRL, lower third of right leg; UTLT, upper third of left thigh; LTLT, lower third of left thigh; UTLL, upper third of left leg; LTLL, lower third of left leg.
∗P<.05 was considered significant.
Tab le 2: Differences between groups in differential voltage in skin blood flow.
Variable
(Digits)
(mV/V)
Baseline M(SD) Pvalue
Pre-T
30 min post-program
M(SD) Pvalue
1a-PT
6monthsM(SD) Pvalue
2a-PT
1yearM(SD) Pvalue
3a-PT
IG PG IG PG IG PG IG PG
Right first 2.19
(2.60)
2.23
(4.23) .35 3.10
(3.37)
2.18
(3.89) .03∗3.04
(6.55)
2.29
(5.60) .04∗2.59
(4.13)
2.24
(4.97) .06
Right second 3.10
(1.94)
3.42
(2.35) .07 3.93
(2.77)
3.56
(2.27) .06 3.41
(4.73)
3.48
(2.11) .30 3.21
(5.03)
3.33
(3.01) .27
Right third 2.63
(0.12)
2.87
(1.45) .10 2.96
(3.19)
2.76
(2.03) .14 2.24
(5.24)
2.80
(1.63) .05 2.38
(6.04)
2.71
(1.98) .08
Right fourth 4.73
(1.08)
4.67
(2.13) .29 6.50
(2.82)
4.62
(1.99) .01∗5.73
(4.46)
4.58
(4.32) .03∗5.02
(3.12)
4.52
(3.12) .05
Right fifth 5.57
(2.69)
6.01
(2.56) .06 6.30
(3.77)
6.15
(3.11) .08 6.59
(4.80)
6.23
(2.88) .06 6.01
(5.32)
6.08
(2.97) .29
Left first 3.84
(0.37)
4.12
(1.35) .07 4.17
(2.53)
4.09
(1.41) .31 4.55
(4.32)
4.21
(1.57) .08 4.11
(5.32)
4.01
(1.22) .22
Left second 5.20
(1.50)
5.39
(3.78) .16 6.27
(2.54)
5.55
(3.88) .04∗6.12
(4.17)
5.45
(3.92) .04∗5.88
(4.01)
5.39
(3.61) .05
Left third 4.06
(2.89)
4.23
(2.57) .21 4.44
(2.31)
4.17
(2.78) .09 4.52
(2.95)
4.29
(2.65) .09 4.48
(1.12)
4.25
(2.82) .10
Left fourth 4.88
(4.03)
4.92
(4.99) .35 5.36
(4.81)
4.89
(4.83) .05∗5.44
(3.73)
4.98
(5.32) .04∗5.24
(2.39)
4.96
(5.05) .09
Left fifth 4.72
(5.01)
4.51
(4.57) .12 6.58
(6.13)
4.49
(4.68) .01∗5.04
(4.13)
4.57
(4.08) .04∗4.69
(3.13)
4.52
(4.14) .13
Values are presented as mean (SD). RMG, reflex massage group; PG, placebo group; 1aPT, post-treatment (30min after 15-week treatment ends); 2aPT, 6
months post-treatment; 3aPT, 1 year post-treatment).
∗P<.05 was considered significant.
8 Evidence-Based Complementary and Alternative Medicine
Heartrate(bpm)
68.39
70.36
71.03 71.12
70.76
70.73
70.66
70.76
67
67.5
68
68.5
69
69.5
70
70.5
71
71.5
Baseline 25 weeks 6 months 1year
Time point
Mean
Intervention group
Placebo group
Figure 5: Comparisons between study groups in levels of depres-
sion, anxiety and pain. ∗P<.05 (95% confidence interval). Values
are presented as means.
no significant difference in any variable between baseline
and 15 weeks. The massage group showed a significantly
(P<.05) greater improvement versus the placebo group
in temperature at right and left popliteal spaces (Figure 6).
ANOVA showed a significant time ×groups interaction for
skin temperature at right popliteal space (F=5.825; P<.04)
and left popliteal space (F=4.139; P<.05) and for oxygen
saturation in right foot (F=20.034; P<.03) and left foot
(F=21.938; P<.01).
The mean (SD) maximum walking distance score sig-
nificantly improved between baseline and 10-min post-
treatment (20.03 (4.32) versus 26.85 (4.26); P<.029) in
the massage group. There were also significant differences
between groups in this score at the end of the 15-week
treatment (baseline: 20.03 (4.32) versus 21.19 (3.94), P<
.063; 15 weeks: 26.85 (4.26) versus 21.77 (3.67), P<.034).
However, no significant change was observed versus baseline
or between groups in relation to the maximum walking speed
score (baseline: 3.97 (1.10) versus 3.89 (1.25), P<.319; 15
weeks: 4.46 (0.97) versus 3.99 (1.08), P<.087) (Figure 7).
ANOVA showed differences in maximum walking distance
score (F=19.347; P<.03).
Although both differential segmental arterial pressure
and heart rate responded significantly to CTM therapy, there
were no statistically significant correlations (Pearson corre-
lation coefficient) between the increase in skin temperature
values and the decrease in heart rate values in the massage
group (r=0.334; P=.188) or the placebo group (r=0.319;
P=.721). However, there were significant correlations in
the massage group between the increase in skin temperature
and oxygen saturation values (r=0.346, P=.045) and
between the increase in skin temperature and differential
segmental arterial pressure values in the upper third of the
thigh (r=0.496; P=.031), lower third of thigh (r=0.511;
P=.027), upper third of leg (r=0.436; P=.025), and lower
third of leg (r=0.392; P=.046).
3.3. Six-Month Outcomes. At 6 months post-treatment,
differential arterial pressure remained high in the CTM in
segments with larger muscular mass, that is, lower third of
the right thigh (P<.048), upper third of right leg (P<
.045), and upper third of left leg (P<.039). No significant
change (versus baseline) was observed in the placebo group.
At 6 months, the groups significantly (P<.05) differed in
differential pressure in lower third of right thigh, upper third
of right leg, lower third of left thigh, and upper third of left
leg (Tab l e 1). There were also statistically significant (P<
.05) differences between the groups in differential voltage
in right first digit, right fourth digit, left second digit, left
fourth digit, and left fifth digit (Tab l e 2). Repeated-measures
ANOVA showed a significant time ×groups interaction for
differential arterial pressure values in lower third of right
third (F=7.321; P<.04), upper third of right leg (F=
7.146; P<.04), lower third of left thigh (F=6.852; P<.05),
and upper third of left leg (F=7.049; P<.04) and for
differential voltage in right first digit (F=8.129; P<.04),
right fourth digit (F=7.646; P<.03), left second digit
(F=8.731; P<.04), left fourth digit (F=8.427; P<.04),
and left fifth digit (F=8.633; P<.04).
In the massage group, significant differences were found
between baseline and six months post-treatment in skin
temperature of right inguinal fold (P<.046) and in oxygen
saturation of right (P<.045) and left foot (.043). The
placebo group showed no significant difference between
baseline and two months in any variable. The massage group
showed a significantly greater improvement versus placebo
group in maximum walking distance (P<.049) but not
in maximum walking speed (P<.073) (Figure 7). ANOVA
analysis showed significant differences for oxygen saturation
in right foot (F=3.821; P<.04) and left foot (F=4.053;
P<.03) and for maximum walking distance (F=17.721;
P<.04).
3.4. One-Year Outcomes. At the 1-year follow-up, the
improvements observed in the massage group at 6 months
largely persisted, with significant differences versus baseline
in: differential pressure in upper third of right leg (P<.041)
and upper third of left leg (P<.039); differential voltage in
right first digit (P<.045) and left second digit (P<.046);
and oxygen saturation in right (P<.047) and left (P<.049)
feet. The placebo group again showed no differences with
baseline values. The massage group showed a significantly
greater improvement versus placebo group (P>.05) in
differential pressure in upper third of right leg and upper
third of left leg and in oxygen saturation in both feet (Ta b le 1
and Figure 6). No significant changes were observed versus
baseline or between groups in maximum walking distance or
maximum speed scores (Figure 7). ANOVA analysis showed
significant interaction for differential arterial pressure values
in upper third of right leg (F=7.124; P<.04) and upper
third of left leg (F=6.993; P<.04) and for oxygen
saturation in right foot (F=3.747; P<.04) and left foot
(F=4.236; P<.03).
4. Discussion
In a group of type 2 diabetes patients with stage I or II-a
PAD, the application of a CTM protocol (Dicke approach)
Evidence-Based Complementary and Alternative Medicine 9
Baseline 30 min
post-
program
6months 1year
34.7
34.8
34.9
35
35.1
35.2
35.3
35.4
35.5
35.6
Skin temperature (right inguinal fold)
Mean
35.11
35.23
35.01
35.52
35.4
35.16
35.09
35.46
(a)
34.6
34.8
35
35.2
35.4
35.6
35.8
36
36.2
Baseline 30 min
post-
program
6months 1year
Skin temperature (left inguinal fold)
Mean
35.33
35.48
35.29
35.99 35.9
35.14
35.12
35.97
(b)
Baseline 30 min
post-
program
6 months 1 year
92
93
94
95
96
97
98
99
∗
∗
∗
Mean
Oxygen saturation (%) right foot
95.9
96.5
94.56
97.92
94.67 94.67
94.56
95.04
(c)
Intervention group
Placebo group
Baseline 30 min
post-
program
6months 1year
∗
Mean
33
33.5
34
34.5
35
35.5
36
Skin temperature (right popliteal space)
34.36
34.32
34.26
35.82
34.67
34.91
34.26
34.98
(d)
Intervention group
Placebo group
Baseline 30 min
post-
program
6 months 1 year
∗
Mean
0
5
10
15
20
25
30
Skin temperature (left popliteal space)
22.89
21.17
25.96
20.53
22.4
22.42
24.43
26.16
(e)
Intervention group
Placebo group
Baseline 30 min
post-
program
6 months 1 year
∗
∗
∗
Oxygen saturation (%) left foot
Mean
92
93
94
95
96
97
98
99
91
95.79
96.56
94.53
98.09
94.93 94.93
94.53
93.98
(f)
Figure 6: Comparisons between study groups in skin temperature and oxygen saturation. ∗P<.05 (95% confidence interval). Values are
presented as means.
twice a week for 15 weeks increased differential segmental
pressure in leg as measured by plethysmography, improved
skin blood flow as determined by photoplethysmography,
and increased pulse volume according to Doppler studies.
The improvement observed in the massage group after CTM
was in line with the results obtained by Castro et al. [43]
applying a massage protocol to healthy subjects. Massage of
the connective tissue reduces peripheral vascular resistance
at microcirculation level [28–30]. The vascular structure
facilitates the work of increasing the blood flow from ter-
minal arterioles until it progressively reaches the large blood
vessels. A contribution to this ascending vasodilatation may
be made by the endothelium from flattened squamous cells
on the contact surface between vessel wall and circulating
blood. These cells respond to changes in humoral conditions
in the cardiovascular system, translating these changes into
vasoactive signals that regulate the blood flow [44,45].
We measured variations in skin blood flow by photo-
plethysmography based on techniques studied by Didier et al.
[46], Allen et al. [27]andBertinoetal.[47], who all stressed
the usefulness of digital photoplethysmographic evaluation
at the different Leriche-Fontaine stages of the disease. This
method allows qualitative variations in wave morphology
(differences between systolic and diastolic peaks) to be
measured before and after therapy. The presence of arterial
ischemia produces qualitative changes in curve morphology
recorded by the photoplethysmograph as a differential
voltage decrease versus the contralateral foot.
At the first post-therapeutic evaluation (at 30min), a
slight temperature increase due to skin vasodilation was
detected, likely due to a combination of both neuronal and
localized processes [48]. Previous studies [49–51] found no
difference between high- and normal-blood pressure groups
in the internal body temperature at which vasodilation
begins.
Oxygen saturation (by pulseoxymetry) and digit ABI are
good screening tools for diagnosing and monitoring PAD in
type 2 diabetic patients [52]. One study found no significant
improvements in oxygen saturation values in these patients
after 5 min of foot massage, which may be too brief to achieve
benefits; the massage produced a downward trend in the
heart rate due to vasodilation [53]. In the present study,
10 Evidence-Based Complementary and Alternative Medicine
Instantly
1 year
2 months15 weeksBaseline
95% IC variable
26.00
25.50
25.00
24.50
24.00
23.50
23.00
Maximum walking distance score RMG
∗
∗
(a)
Instantly
1 year2 months15 weeksBaseline
25.50
24.50
95% IC variable
26.00
25.00
Maximum walking distance score PG
(b)
Instantly
1 year
2 months15 weeksBaseline
95% IC variable
24.50
24.00
23.50
23.00
22.50
Maximum walking speed score RMG
(c)
Instantly
1 year2 months15 weeksBaseline
95% IC variable
23.75
23.50
23.25
23.00
22.75
Maximum walking speed score PG
(d)
Figure 7: Error bars in Walking Impairment Questionnaire. RMG, reflex massage groups, PG, placebo group. ∗P<.05.
heart rate values were significantly lower versus baseline in
the massage group but not in the placebo group.
It has been reported in general terms that CTM may
causepatientssomediscomfort[54]. None of our patients
described any such feelings during our application of the
Dicke method. Patients were instructed to tell the therapist
immediately pain was felt, and this never proved necessary.
Nevertheless, discomfort may have gone unreported by some
patients, and it would be useful to explore this aspect in
greater depth in future studies.
4.1. Study Limitations. Among study limitations, the patients
with type II-a PAD continued to receive their usual medi-
cation during the massage program, for ethical reasons. A
further limitation is that the therapists were not blinded to
the group to which the patients belonged, which may have
influenced outcomes.
5. Conclusion
CTM increases blood circulation in the lower limbs of type
2 diabetic patients at stage I and II-a (Leriche-Fontaine)
of the disease, with improvements in differential segmental
pressure in leg and greater skin blood flow. At 30 min
after this massage, the heart rate lowered and oxygen
saturation and temperature values rose, confirming the role
of the parasympathetic nervous system in the effects of this
treatment. CTM is a treatment option for asymptomatic
patients suspected of being in Leriche-Fontaine stage I,
that is, having the main risk factors for developing the
disease. This type of massage may also be useful to improve
Evidence-Based Complementary and Alternative Medicine 11
symptoms and perhaps slow the progression of the disease in
stage II-a PAD patients who have difficulties in taking part in
any kind of exercise, including walking programs.
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