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Accepted Manuscript

Title: Venous flow during manual lymphatic drainage applied


to different regions of the lower extremity in people with and
without chronic venous insufficiency: a cross-sectional study
Author: R.S. dos Santos Crisostomo M.S. Candeias P.A.S.
Armada-da-Silva
PII:
DOI:
Reference:

S0031-9406(16)00023-7
http://dx.doi.org/doi:10.1016/j.physio.2015.12.005
PHYST 889

To appear in:

Physiotherapy

Received date:
Accepted date:

19-3-2014
3-12-2015

Please cite this article as: Crisostomo RSS, Candeias MS, Armada-da-Silva PAS,
Venous flow during manual lymphatic drainage applied to different regions of the lower
extremity in people with and without chronic venous insufficiency: a cross-sectional
study, Physiotherapy (2016), http://dx.doi.org/10.1016/j.physio.2015.12.005
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*Title Page (with authors and addresses)

Venous flow during manual lymphatic drainage applied to


different regions of the lower extremity in people with and

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without chronic venous insufficiency: a cross-sectional study

Laboratrio de Biomecnica e Morfologia Funcional, Faculdade de Motricidade

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R.S. dos Santos Crisstomoa,b,c,*, M.S. Candeiasd, P.A.S. Armada-da-Silvaa,b

Humana, Universidade de Lisboa, Lisboa, Portugal

Centro Interdisciplinar para o Estudo da Performance Humana, Faculdade de

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Motricidade Humana, Universidade de Lisboa, Lisboa, Portugal


Instituto Politcnico de Castelo Branco, Escola Superior de Sade Dr. Lopes Dias,

Cardiotime Lda., Elvas, Portugal

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Castelo Branco, Portugal

Corresponding author. Address: Escola Superior de Sade Dr. Lopes Dias, Instituto Politcnico de

Castelo Branco, Avenida do Empresrio, Campus da Talagueira, 6000-767 Castelo Branco, Portugal.
Tel.: +351 272340560/+351 968584992; fax: +351 272 340 568.
E-mail address: crisostomo.rute@ipcb.pt (R.S. dos Santos Crisstomo).

Page 1 of 35

*Abstract

Abstract
Objectives To evaluate the effect of manual lymphatic drainage (MLD) on venous flow
when applied to the medial and lateral aspects of the thigh and leg in patients with
chronic venous insufficiency (CVI) and healthy subjects.

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Design Cross-sectional study.

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Setting Participants were assessed in a school-based health community attendant


service.

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Participants Fifty-seven subjects participated in this study {mean age: 43 [standard


deviation (SD) 14] years, 38 women and 19 men}. Of these, 28 subjects had CVI [mean

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age 47 (SD 12) years] and 29 subjects did not have CVI [mean age 39 (14) years].

lateral aspects of the thigh and leg.

Intervention MLD was applied by a certificated physical therapist to the medial and

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Main outcome measurements Cross-sectional area; blood flow velocities in the


femoral vein, great saphenous vein, popliteal vein and small saphenous vein at baseline

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and during MLD, measured by duplex ultrasound.


Results Flow volume in the femoral vein increased from baseline [5.19 (SD 3.25)
cm3/second] when MLD was applied to the medial [7.03 (SD 3.65) cm3/second;

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P0.001; mean difference -1.69; 95% confidence interval (CI) -2.418 to -0.968] and
lateral [6.16 (SD 3.35) cm3/second; P0.001; mean difference -1.04; 95% CI -1.699 to 0.389] aspects of the thigh. Venous flow augmentation in the femoral vein and great
saphenous vein was higher when MLD was applied to the medial aspect of the thigh
(P<0.001), while MLD had a similar effect on venous blood flow regardless of whether
it was applied to the medial or the lateral aspect of the leg (P=0.731).

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Conclusions MLD increases blood flow in deep and superficial veins. MLD should be
applied along the route of the venous vessels for improved venous return.

Keywords: Manual lymphatic drainage; Duplex ultrasonography; Venous flow velocity;

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Venous insufficiency

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*Manuscript (without Author details)

<A>Introduction
Manual lymphatic drainage (MLD) is used as a conservative treatment for
chronic venous insufficiency (CVI) [1]. When applied along the course of the great

haemodynamics, clinical severity and quality of life [4,5]

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saphenous vein [2] and before surgery [3,4], MLD appears to improve venous

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MLD is also a well-known conservative treatment for lymphoedema [6]. It


consists of a skin-stretching form of massage that is performed along the anatomical

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distribution of the superficial lymphatic vessels and ganglions [7], and exerts mild
pressure (<40 mmHg) over the underlying soft tissues to stimulate lymph flow and re-

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absorption of interstitial fluid and macromolecules by the lymphatic system [8,9].

The real impact of MLD on venous blood flow is unclear, but it has been
suggested to be minor [8]. Improving venous return in patients with CVI is important in

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order to avoid peripheral venous hypertension and consequent luminal hypoxaemia and
vein wall distension, which, in turn, impair blood perfusion and cause endothelial

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hypoxia, leukocyte invasion of the vessel wall, oedema [10] and ongoing damage of
skin and subcutaneous tissues (i.e. lipodermosclerosis and skin ulceration) [11].
Although scarce, data show that MLD enhances venous blood flow in distinct

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deep and superficial veins of the lower extremities in healthy subjects and patients with
chronic venous disease [2]. These are important observations given that MLD can be
performed not only by therapists, but also by patients and caregivers, if offered proper
advice and training [12]. Therefore, MLD may be an interesting alternative for the
conservative treatment of CVI [1,2,4]. However, the precise mechanisms by which
MLD increases venous blood flow are not fully understood. Previous data suggest that
MLD increases venous blood flow in superficial and deep veins regardless of the exact

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technique that is employed [2]. However, in the lower extremities, deep and,
particularly, superficial veins have a distinct anatomical distribution that may constrain
the efficacy of MLD [2].
Therefore, the aim of this study was to compare the changes in venous blood

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flow in deep and superficial veins during the application of MLD to the medial and

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lateral aspects of the thigh and leg. Vascular (cross-sectional area) and haemodynamic
(flow velocity and flow volume) changes were assessed in participants with and without

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CVI in deep (femoral and popliteal) and superficial (great saphenous and small
saphenous) veins. Based on the anatomy of the veins in the lower extremity, it was

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hypothesised that venous blood flow enhancement would be greater when MLD was

applied to the medial aspect of the thigh and leg, as the major veins course along this
side. Despite the fact that the small saphenous vein runs posteriorly and laterally across

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the leg [13], and the popliteal vein is deeply and centrally placed within the posterior
muscle compartment of the leg [14], higher augmentation of venous flow was expected

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when MLD was applied to the medial aspect of the leg as this is the path followed by
the great saphenous vein.

In addition, it was hypothesised that venous blood flow enhancement caused by

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MLD would be greater in subjects with CVI due to greater venous pooling in the leg.

<A>Materials and methods


<B>Participants
After screening 78 subjects, a convenience sample of 57 participants was
recruited to participate in this study, which included 28 (21 women and seven men)
participants with CVI (CVI group) and 29 participants without CVI (non-CVI group; 17

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women and 12 men). Participants with CVI were recruited from the outpatient clinic of
a health school.
The demographic and clinical data of the participants are presented in Table 1.
All participants with CVI had venous blood reflux and Clinical-Etiological-Anatomical-

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Pathological (CEAP) classification C35. Before study enrolment, participants were

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informed about the purpose and procedures of the study, and signed an informed
consent form. The study received ethical approval from the review board of the

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Scientific Council of the Faculty of Human Kinetics, Technical University of Lisbon.

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<insert Table 1 near here>

Exclusion criteria in this study included the presence of severe cardiac

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insufficiency, acute venous or arterial obstruction, arterial insufficiency, renal


insufficiency, uncompensated thyroid dysfunction, pregnancy, neoplastic pathology,

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systemic or limb infection, recent musculoskeletal injury in the lower extremity, and
peripheral neuropathy in the lower extremity. In total, 21 subjects were excluded: 11
had a clinical CEAP classification below C3 (only had varicose veins, talangiectasias or

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reticular veins), two had active ulcers (C6), three suffered from cardiac insufficiency,
three had arterial insufficiency, and two were over 65 years of age. In six participants
with CVI, data were not collected from the great saphenous vein due to previous
surgical treatment. For the same reason, the small saphenous vein was also excluded
from data collection in five of the participants with CVI.

<B>Clinical evaluations

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Venous duplex scanning (ESAOTE mylab 30cv, with 7-mm linear array
transducer scanned at 6 to 12 MHz) was undertaken with participants in a standing
position in order to confirm the diagnosis of CVI and to determine the exact anatomical
location (anatomical CEAP classification) of venous reflux (superficial, perforating

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and/or deep vein system) [15]. Clinical history, symptoms (fatigue, heavy sensation,

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itching, cramps and skin irritation) and severity of disease, according to CEAP clinical

class and venous clinical severity scores, were obtained following established guidelines

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[15].

The CEAP classification considers: (1) clinical manifestations of the disease (C);

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(2) aetiological factors (E), separated in congenital, primary and secondary (e.g. post-

thrombotic); (3) anatomical distribution of the disease (A), which can affect superficial,
perforator or deep veins; and (4) underlying pathophysiological findings (P), such as

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reflux, obstruction or both reflux and obstruction. According to the CEAP classification,
there are six chronic venous disease categories that range from C0 to C6. C0 represents

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those individuals with objective evidence of venous disease (i.e. E, A and/or P), but
with no clinical manifestations. Class C1 is characterised by the presence of
telangiectasia or reticular veins. In Class C2, varicose veins are present. In Class C3,

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oedema of venous aetiology is present. In Class C4, there are skin trophic changes (e.g.
C4a, pigmentation and/or eczema; C4b, lipodermatosclerosis and/or white atrophy).
Classes C5 and C6 are associated with the occurrence of venous ulcers; C5 corresponds
to cases of prior ulceration that healed, and C6 corresponds to cases with active venous
ulcers [16].
The venous clinical severity score quantifies 10 items using the range: 0 (none),
1 (mild), 2 (moderate) and 3 (severe), with a total range score of 0 to 30 (best to worst)

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[17]. The items are: pain or discomfort; varicose veins; venous oedema; skin
pigmentation; inflammation; induration; number of active ulcers; duration of active
ulcers; size of active ulcers; and use of compression therapy.
The anatomical location of venous reflux and other clinical features of the CVI

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group are presented in Table 1. The non-CVI participants were also evaluated to

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exclude the presence of venous reflux.

All ultrasound tests were performed by a certified vascular sonographist and

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used the same ultrasound equipment. The leg with more complaints and worse clinical
signs was used to test the effects of MLD. In the non-CVI group, MLD techniques were

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applied to the dominant leg.

<B>Blood flow at baseline and during manual lymphatic drainage

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Four veins were assessed via venous duplex ultrasound using an assessment
protocol adapted from a previous study [2]. The great saphenous vein was insonated

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immediately below the confluence of the superficial inguinal veins, whereas the small
saphenous vein was insonated immediately below the saphenopopliteal junction. The
femoral vein was insonated below the confluence of the superficial inguinal veins, and

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the popliteal vein was insonated just below the saphenopopliteal junction.
The veins were scanned in B-mode for 4 seconds to measure their cross-

sectional area, using tracings of the contour of the veins in the ultrasound scan. Peak
and mean venous flow velocity were measured throughout the 4-second interval using
the time integral calculation. Three measurements of cross-sectional area and blood
flow velocity were taken for all four veins, and the average was computed for analysis
(Fig. 1).

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<insert Fig 1 near here>

Ultrasound measurements were taken at baseline (without MLD) and during the

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application of MLD [2] to the medial and lateral aspects of the thigh for the femoral

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vein and great saphenous vein, and during the application of MLD to the medial and

lateral aspects of the leg for the popliteal vein and small saphenous vein. Three separate

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ultrasound measurements were taken sequentially for each condition, and the mean of
these measurements was used for further analysis. Participants were in a supine position

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for the assessment of blood flow velocity in the femoral and great saphenous veins, and

in a prone position for assessment of the popliteal and small saphenous veins. The order
of blood flow measurements was randomised following a hierarchical procedure (see

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<insert Fig 2 near here>

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Fig. 2).

Before measurements were taken, the participants rested for 5 minutes in a

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supine position. Blood flow volume was calculated based on cross-sectional area and
blood flow velocity as:

Flow volume (cm3/second) = vein cross-sectional area (cm2) mean flow


velocity (cm/second)

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Percentage change in cross-sectional area, peak flow velocity, mean flow


velocity and flow volume was calculated as:

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Change (%) = (MLD baseline)/baseline) 100

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The sonographer was blinded to the application of MLD using an opaque screen.
The MLD technique (call-up manoeuvre) was executed by a certificated physical

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therapist (as expertise in MLD application may influence the results [18], the therapist
had more than 5 years of experience [19]) using two hands to apply an amount of

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pressure just sufficient to stretch the skin. Stretching of the skin was maintained for at

least 4 seconds. The MLD technique (call-up manoeuvre) started and ended on the order
of the sonographer, and therefore synchronised with the ultrasound recording. With two

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hands joined together and palms facing the limb, the MLD stroke starts by using the
medial border of the hand placed proximally to the participants limb to pull the skin

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and apply gentle pressure. Gradually, the two hands come into contact with the skin to
gently pull it proximally (Fig. 3).

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<insert Fig 3 near here>

To assess testretest reliability of these evaluations, nine healthy participants

repeated the tests after a 1-week interval.

<B>Statistical analysis

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All statistical tests were performed using Statistical Package for the Social
Sciences Version 17 (IBM Corp., Armonk, NY, USA). The normality of distribution
was tested using the ShapiroWilks test. A mixed-factorial analysis of variance with
three factors was used to test the effects of the dependent variables and interactions:

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group (two levels: CVI groups vs non-CVI group), place of MLD application (three

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levels: baseline vs medial aspect vs lateral aspect; or two levels: medial aspect vs lateral

aspect only) and type of vein (two levels: deep vein vs superficial vein). Statistical

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analysis using this model was performed separately for the thigh and the leg.
Bonferronis correction was used to correct for multiple pairwise comparisons. The

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relationship between the magnitude of the effect of the MLD technique, in terms of

percentage change from baseline, and severity of CVI, as given by the venous clinical
severity score classification, was calculated using Spearmans rank correlation

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coefficient. Reproducibility was assessed by testretest reliability, calculating absolute


agreement using the intraclass correlation coefficient and 95% confidence interval (CI).

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Bland and Altman limits of agreement were also calculated. The significance level was
set at P<0.05.

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<A>Results

The demographic and clinical data of the participants are presented in Table 1.

All participants with CVI had pathological venous blood reflux in the lower extremity
and had a CEAP classification of C35.
No differences in height, weight and body mass index were found between the
CVI and non-CVI group. Nevertheless, the CVI group was slightly older than the non-

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CVI group {mean age 47 [standard deviation (SD) 12] years vs 39 (SD 14) years,
P=0.029}.

<B>Manual lymphatic drainage applied to the thigh

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Compared with baseline, MLD applied to the medial aspect of the thigh, but not
the lateral aspect, increased the cross-sectional area of the femoral vein in both groups

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(mean difference -0.042 cm2; P=0.008; 95% CI -0.074 to -0.009 cm2). The cross-

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sectional area of the great saphenous vein remained unchanged during application of
MLD to the thigh.

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Venous blood peak velocity (P=0.034), mean velocity (P=0.028) and blood flow

volume (P<0.001) in the femoral and great saphenous veins increased significantly in
response to the application of MLD to the medial and lateral aspects of the thigh (power

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=1.0), with larger increases with medial application (P0.001 for all variables; Fig. 4);
greater increases were seen in the great saphenous vein compared with the femoral vein

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(P<0.05).

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<insert Fig 4 near here>

No differences in the effect of MLD on venous blood flow and cross-sectional

area were found between the CVI group and the non-CVI group (see Table 2).

<insert Table 2 near here>

<B>Manual lymphatic drainage applied to the leg

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The cross-sectional area of the popliteal vein, but not that of the small saphenous
vein, increased similarly (P<0.001) regardless of whether MLD was applied to the
medial (mean difference -0.032 cm2; P<0.001; 95% CI -0.044 to -0.019 cm2) or lateral
(mean difference -0.026 cm2; P<0.001; 95% CI -0.037 to -0.015 cm2) aspect of the leg

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(Table 3), with no difference between the groups.

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<insert Table 3 near here>

Application of MLD to the leg increased peak (P<0.001) and mean blood

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velocity (P<0.001), and flow volume (P<0.001, power=1.000), with greater increases in

the popliteal vein than the small saphenous vein (P<0.001). However, percentage
changes in blood flow velocity and blood flow volume as a result of the application of

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MLD to the leg were similar in the two veins. The CVI group and non-CVI group
responded differently to the application of MLD to the leg, with the percentage increase

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in mean blood flow being higher in the small saphenous vein in the CVI group, and
higher in the popliteal vein in the non-CVI group.

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<B>Clinical severity of chronic venous insufficiency and response to manual lymphatic


drainage

No correlations could be found between percentage increases in blood flow (i.e. peak
and mean flow velocity, and flow volume), cross-sectional area of veins and the severity
of CVI, with the correlation coefficients ranging between 0.203 and 0.249.

<B>Reproducibility

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High-to-moderate testretest reliability and agreement for venous cross-sectional


area and blood volume measurements was confirmed in this study, with cross-sectional
area and blood flow measurements showing better testretest reproducibility than blood

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velocity (Table 4).

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<insert Table 4 near here>

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<A>Discussion

This study found that MLD, which is based on manual stretching of the skin and

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underlying soft tissues, increases venous blood flow in superficial and deep veins, and

this occurs to a similar extent in participants with and without CVI. The increase in
venous flow was higher when MLD was applied to the medial aspect of the thigh,

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corresponding to the root of the great saphenous vein, compared with when MLD was
applied to the lateral aspect of the thigh. However, MLD was found to increase venous

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flow similarly when applied to either the lateral or the medial aspect of the leg.
This study found that MLD increases blood flow in both superficial and deep
veins, which is in agreement with previous observations [2]. Nevertheless, data

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collected from patients with heart failure and lower limb oedema point to small or even
insignificant effects of MLD on venous haemodynamics [8]. However, MLD is
commonly prescribed as a treatment for patients with CVI, especially when the
lymphatic system is affected and oedema is present [20]. Before CVI surgery, MLD
also appears to play an important role in improving the reflux volume index, disease
severity, quality of life [5] and venous oedema [4]. A small number of MLD sessions

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(i.e.10 sessions) without any other conservative treatments seems to have a positive,
although short-term, effect on symptoms, disease severity and venous oedema [1].
This study demonstrated that MLD produces the largest improvements in venous
blood flow when applied to the medial aspect of the thigh. MLD was applied exactly

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along the course of the great saphenous vein [13] and over the medial compartment of

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the thigh, which is crossed by the femoral vein [14]. This finding supports the
assumption that MLD should be applied over the trajectory of the great saphenous vein

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in patients with CVI [3,5]. In turn, MLD was found to increase blood flow in the
popliteal and small saphenous veins to a similar extent regardless of whether the

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technique was performed over the medial or lateral aspect of the leg. Anatomically, the

small saphenous vein lies posterior and laterally in the leg [13], while the popliteal vein
is deeply and centrally placed within the posterior muscle compartment of the leg [14].

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Therefore, both the popliteal vein and the small saphenous vein are placed relatively
equidistant from the medial and lateral aspects of the leg where the MLD manoeuvres

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were applied. Also, the smaller size of the leg, at least compared with that of the thigh,
makes it difficult to restrict the effect of the MLD technique to just one aspect. These
findings suggest that MLD must consider venous anatomy and venous blood flow

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direction, just like lymphatic anatomy and lymph flow direction, particularly in larger
body segments such as the thigh [79].
Inflammation of the skin, which is associated with venous stasis and venous

hypertension, leads to disease complications, such as lipodermatosclerosis, and the


development of fibrosis and microcirculatory changes that increase the risk of ulceration
[2123]. Other alterations, such as leg oedema [13] and diminished ankle mobility [24],
restrain the normal movement of the skin and the underlying soft tissues, thus

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contributing to blood stasis and CVI disease complications. Also, some of the
symptoms reported by patients with CVI [15,25] are presumed to be associated with the
inflammatory process triggered by adhesion of leukocytes to the endothelium, which is
a secondary event of venous stasis and considered to be an important

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physiopathological mechanism for the progression of severity of CVI [26]. This

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supports the benefit of many conservative treatments for CVI, such as exercise [27,28],

intermittent pneumatic pressure [29], kinesio taping [30], electrical muscle and nerve

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stimulation [31,32], which reduce or prevent leukocyte-activated vessel and tissue


inflammation by improving venous flow.

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The relatively high pressure (>40 mmHg) produced by intermittent pneumatic

compression or compression bandages and stockings increases the velocity of venous


blood flow [33] but diminishes the cross-sectional area of veins [29,34]. Despite

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increasing venous flow velocity in deep veins, pressure applied to the lower extremity,
within the range of 80 to 100 mmHg or higher, forces the collapse of superficial veins

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[35]. In contrast, this study found that MLD increased the cross-sectional area of both
superficial and deep veins, most likely because the amount of pressure applied over the
skin and underlying tissues was adequate. In most cases during the application of MLD,

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the enlargement of veins was accompanied by increased blood flow, and therefore
venous blood flow increased substantially.
During ankle movements, changes in flow velocity in the femoral vein represent

approximately 20% to 40% [36] of baseline. In the great saphenous vein, ankle
movement increased flow velocity to 34.0 to 46.7 cm/second in healthy participants,
and slightly less in patients with CVI (21.0 to 43.1cm/second) [37]. This change in
venous flow is very similar to the results of the present study during MLD.

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Conservative CVI treatments, such as active tip-toe movement [38] and calf muscle
electrical stimulation, increase venous flow in the popliteal vein [32]; other treatments,
such as compression stockings, do not have a clear effect on venous flow [39].
Compared with these procedures, which predominantly enhance venous blood flow in

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the deep veins, MLD is able to increase blood flow in both superficial and deep veins.

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Moreover, the increase in venous blood flow during tip-toe movements seems to be

lower in patients with CVI compared with healthy counterparts [38], whereas MLD

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improves venous return by the same extent in healthy subjects and patients with CVI, as
shown in the present study.

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This study had a few limitations. These include the unknown effects of

uncontrolled factors involving the participants, such as breathing pattern during


measurements, hydration status, medication, emotional events and lifestyle factors that

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may influence venous flow. To account for these limitations, the data were also
analysed in terms of percentage change. Also, the real long-term effects of MLD and

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respective cost-effectiveness remain unknown.


In summary, MLD increases venous blood flow in deep (femoral vein and
popliteal vein) and superficial (great saphenous vein and small saphenous vein) veins.

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The increase in venous blood flow occurs to a similar extent in subjects with and
without CVI. However, the change in blood flow in the deep and superficial veins of the
thigh is significantly higher when MLD is applied to the medial aspect of the thigh,
compared with the lateral aspect of the thigh. In the leg, MLD shows equal efficacy in
increasing venous blood flow when applied to the medial or lateral aspect. Further
studies are needed to ascertain the long-term effects of MLD in the conservative
treatment of venous disease.

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Acknowledgements
The authors wish to thank Aida Paulino, Maria Conceio Branco and Manuel Machado
from Unidade Local de Sade de Castelo Branco for referring patients to this study. The

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authors also wish to thank Diana Arraia for her help in data collection, and Isabele

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Salavessa for reviewing the English.

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Ethical approval: The study received ethical approval by the review board of the
Scientific Council of the Faculty of Human Kinetics, University of Lisbon (Ref. No.

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Parecer 10/2013).

Funding: This work was partially supported by a PhD grant by the Portuguese

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Fundao para a Cincia e Tecnologia (Ref. No. SFRH/BD/62673/2009).

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Conflict of interest: None declared.

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[16] Rabe E, Pannier F. Clinical, aetiological, anatomical and pathological classification


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[17] Vasquez MA, Rabe E, McLafferty RB, Shortell CK, Marston WA, Gillespie D, et
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del Moral O, Cerezo Tellez E, et al. Effectiveness of early physiotherapy to prevent

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[21] Caggiati A, Rosi C, Casini A, Cirenza M, Petrozza V, Acconcia MC, et al. Skin

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iron deposition characterises lipodermatosclerosis and leg ulcer. Eur J Vasc Endovasc
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[25] Darvall KA, Bate GR, Adam DJ, Bradbury AW. Generic health-related quality of

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life is significantly worse in varicose vein patients with lower limb symptoms
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[28] Padberg FT Jr, Johnston MV, Sisto SA. Structured exercise improves calf muscle
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[29] Lurie F, Scott V, Yoon HC, Kistner RL. On the mechanism of action of pneumatic
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the lower limb by transcutaneous electrical nerve stimulation. Eur J Vasc Surg

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veins of the calf. Am J Physiol Heart Circ Physiol 2008;294:H211220.


[34] Partsch H, Menzinger G, Borst-Krafek B, Groiss E. Does thigh compression
improve venous hemodynamics in chronic venous insufficiency? J Vasc Surg
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[35] Morris RJ, Woodcock JP. Evidence-based compression: prevention of stasis and
deep vein thrombosis. Ann Surg 2004;239:16271.

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[36] Staubesand J, Heisterkamp T, Stege H. Use of duplex sonography to investigate the


effect of active and passive movement at the ankle joint for promoting venous return.
Clin Anat 1995;8:96101.

return in the lower limb. J Bone Joint Surg Br 1999;81:7004.

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[37] Sochart DH, Hardinge K. The relationship of foot and ankle movements to venous

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[38] Crisostomo RS, Candeias MS, Armada-da-Siva PA. The use of ultrasound in the

evaluation of the efficacy of calf muscle pump function in primary chronic venous

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disease. Phlebology 2014;29:24756.

[39] Stein PD, Matta F, Yaekoub AY, Ahsan ST, Badshah A, Younas F, et al. Effect of

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compression stockings on venous blood velocity and blood flow. Thromb Haemost

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2010;103:13844.

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Table 1
Demographic and clinical data
CVI group

Non-CVI group
P

28

29

Age (years)

47 (12)

39 (14)

0.029

Height (cm)

164 (10)

165 (10)

0.719

Weight (kg)

69 (14)

66 (14)

0.349

BMI (kg/m2)

26 (4)

Venous clinical severity scorea

7 (4)

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(%)
Sex

Male
Comorbidities

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Female

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24 (4)

0.101

Categorical variables: frequency

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Quantitative variables: mean (SD)

21 (75)

17 (59)

7 (25)

12 (41)

6 (21)

1 (4)

3 (11)

0 (0)

1 (3)

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Surgical removal of small


and/or great saphenous vein
Active ulcer (contralateral
leg)
History

of

deep

venous

thrombosis (>1 year)


Diabetes

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Page 24 of 35

Arterial hypertension

0 (0)

4 (14)

2 (7)

4 (14)

1 (4)

C3

13 (46)

C4

11 (39)

C5

4 (14)

Cardiorespiratory

disease

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CEAP class

Superficial + deep veins

6 (21)

Superficial

perforator

5 (18)

12 (43)

Superficial

ed

veins
deep

an

Anatomical reflux
Superficial veins

5 (18)

24 (86)

14 (50)

Heavy legs

21 (75)

Pain

19 (68)

Skin irritation

12 (43)

Itching

17 (61)

Symptoms
Fatigue

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Cramps

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perforator veins

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Erysipelas (>1 year ago)

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(treated)

BMI, body mass index; CEAP, Clinical Etiological Anatomical Pathological; SD, standard deviation.
a

Venous clinical severity score: total scale range 0 to 30 (best to worst).

Significance level was set at P<0.05.

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Page 25 of 35

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Table 2

Venous blood flow during manual lymphatic drainage (MLD) application to the thigh

an

21.07
(10.70)
25.39
(15.14)a
22.81
(14.67)a,b

28

Lateral aspect

28

Baseline
Medial aspect

28 14.04 (8.60)
28
17.58
(12.53)a
28
15.70
(12.19)a,b

Lateral aspect

Flow volume
(cm3/second)

28

Medial aspect

Ac
c

Mean flow velocity


(cm/second)

Baseline

27 0.41 (0.14)
27 0.45 (0.17)a
28 0.46 (0.17)a

Peak flow velocity


(cm/second)

Baseline
Medial aspect
Lateral aspect

ep
te

Femoral vein
Cross-sectional area
(cm2)

MLD application to
the thigh
n

Variables

CVI group
Percentage change from
Mean (SD)
baseline
Mean (SD)

Baseline
Medial aspect
Lateral aspect

27 5.09 (2.91)
27 6.82 (3.69)a
28 6.09 (3.44)a,b

Non-CVI group
Percentage change from
Mean (SD)
baseline
Mean (SD)

11 (26)
12 (22)

29 0.43 (0.20)
29 0.48 (0.20)a
29 0.44 (0.18)

13 (26)
3 (16)

29 20.14 (8.11)

21 (30)

29 24.59 (8.03)a

29 (33)

9 (24)b

29

19 (26)b

25 (41)

29 13.02 (6.48)
29 15.86 (6.44)a

40 (41)

12 (31)b

29

23 (36)b

39 (54)
28 (47)b

29 5.28 (3.60)
29 7.22 (3.68)a
29 6.22 (3.31)a,b

23.19
(7.80)a,b

14.93
(5.63)a,b

46 (49)
26 (38)b

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Lateral aspect

22

Baseline

22 13.41 (9.18)

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22

Medial aspect

22

Lateral aspect

22

19.19
(12.25)
28.82
(19.97)a
22.00
(14.70)a,b

20.31
(15.62)a
15.66
(11.01)a,b

Baseline
22 1.63 (1.96)
Medial aspect
22 2.41 (2.66)a
Lateral aspect
22 1.87 (2.28)a,b
CVI, chronic venous insufficiency; SD, standard deviation.
a

5 (25)
1 (21)

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Medial aspect

an

22

Ac
c

Flow volume
(cm3/second)

Baseline

ep
te

Mean flow velocity


(cm/second)

22 0.11 (0.07)
22 0.11 (0.08)
22 0.10 (0.07)

Peak flow velocity


(cm/s)

Baseline
Medial aspect
Lateral aspect

Great saphenous vein


Cross-sectional area
(cm2)

29 0.09 (0.04)
29 0.10 (0.05)
29 0.10 (0.05)

29

20.71
(14.43)
32.81
(24.77)a
25.68
(19.78)a,b

61 (71)

29

19 (33)b

29

29

64 (79)

29

24 (38)b

29

72 (88)
26 (49)b

29 1.34 (1.56)
29 2.26 (2.47)a
29 1.72 (1.80)a,b

14.02
(11.60)
22.92
(21.00)a
18.07
(16.31)a,b

8 (25)
6 (22)
55 (45)
23 (40)b

59 (41)
25 (37)b

72 (60)
34 (52)b

Significantly different from baseline (P<0.05).

Significantly different from MLD application to the medial aspect of the thigh (P<0.05).

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Table 3

Variables

Baseline
Peak flow velocity
(cm/second)

Medial aspect
Lateral aspect

Ac
c

Baseline

Mean flow velocity


(cm/second)

Medial aspect
Lateral aspect

Flow volume
(cm3/second)

28 0.21 (0.15)
28 0.27 (0.19)a
28 0.25 (0.17)a

ep
te

Baseline
Cross-sectional area (cm2) Medial aspect
Lateral aspect

Popliteal vein

CVI group
Percentage change from
Mean(SD)
baseline
Mean (SD)

MLD application
to leg

an

Venous blood flow during manual lymphatic drainage (MLD) application to the leg.

Baseline
Medial aspect
Lateral aspect

27 18.17 (8.53)
37.12
28
(20.38)a
33.90
28
(16.00)a
27 11.95 (6.28)
23.45
28
(14.21)a
21.43
28
(11.33)a
27 2.31 (2.74)
28 5.76 (5.64)a
28 4.99 (4.38)a

Non-CVI group
Percentage change from
n Mean (SD)
baseline
Mean (SD)

49 (80)
35 (68)

29 0.19 (0.12)
29 0.23 (0.15)a
29 0.23 (0.13)a

42 (99)
54 (118)

29 19.69 (9.78)
42.00
29
(20.48)a
42.78
29
(21.27)a

113 (86)
109 (101)
101 (72)
102 (95)
208 (231)
172 (173)

29 12.30 (7.89)
27.90
29
(16.73)a
28.07
29
(17.14)a
29 2.26 (2.16)
29 6.36 (5.41)a
29 6.88 (6.15)a

132 (113)
134 (106)
161 (145)
153 (119)
292 (433)
300 (406)

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Page 28 of 35

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29 0.05 (0.03)
29 0.06 (0.03)
29 0.06 (0.04)

14 (24)
13 (25)

29 11.86 (5.25)
14.59
29
(5.98)a
13.99
29
(7.82)a

23 10.10 (2.67)

Medial aspect

23 12.74 (4.66)a

37 (66)

Lateral aspect

23

Baseline
Medial aspect
Lateral aspect

23 5.95 (2.26)
23 7.88 (3.57)a
23 9.09 (8.06)a

14.31
(10.82)a

ep
te

Mean flow velocity


(cm/second)

14 (22)
9 (26)

Baseline

Peak flow velocity


(cm/second)

23 0.05 (0.03)
22 0.06 (0.04)
23 0.05 (0.03)

an

Baseline
Cross-sectional area (cm2) Medial aspect
Lateral aspect

us

Small saphenous vein

23 0.30 (0.28)
22 0.46 (0.49)a
23 0.55 (0.95)a

18 (29)

51 (104)
49 (76)

29 7.20 (3.94)
29 9.28 (5.98)a
29 8.61 (5.76)a

27 (38)
20 (32)

38 (58)
57 (74)

29 0.40 (0.38)
29 0.55 (0.52)a
29 0.52 (0.52)a

42 (45)
38 (58)

Ac
c

Baseline
Flow volume (ml/second) Medial aspect
Lateral aspect
a
Significantly different from baseline (P<0.05).

32 (55)

21 (32)

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Page 29 of 35

Table 4
Reproducibility of ultrasound measurements

ICC

95% CI

Bland and Altman analysis


Mean
95% limits of
difference
agreement
-0.14 to 0.14

-15.94 to 2.91
-12.56 to 2.42

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Cross-sectional area
9
0.97
0.84 to 0.96
0.00
of vein (cm2)
Peak flow velocity
9
0.47
0.84 to 0.96
6.21
(cm/second)
Mean flow velocity
9
0.50
-0.13 to 0.89
-5.07
(cm/second)
Flow volume
9
0.90
0.58 to 0.98
-0.92
(cm3/second)
ICC, intraclass correlation coefficient; CI, confidence interval.

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ICC

us

-5.11 to 3.27

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Testretest reliability: ICC and 95% CI.

Ac

ce
pt

ed

Agreement: mean difference and respective Bland and Altman 95% limits of agreement.

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Page 30 of 35

Fig. 1. Representative ultrasound images showing the effect of manual lymphatic


drainage (MLD) in increasing cross-sectional area (A: baseline; B: during MLD) and

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Fig. 2. Randomisation (R) for vascular ultrasound assessments.

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blood flow velocity (C: baseline; D: during MLD) in the popliteal vein.

Fig. 3. Femoral vein and great saphenous vein ultrasound data collection: (A) at

an

baseline, (BD) during manual lymphatic drainage (MLD) application to the medial

aspect of the thigh, and (EG) during MLD application to the lateral aspect of the thigh.
Popliteal and small saphenous vein ultrasound data collection: (H) at baseline, (IK)

ed

during MLD application to the medial aspect of the leg, and (LN) during MLD

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application to the lateral aspect of the leg.

Fig. 4. Change (%) in flow volume in (A) the femoral vein and (B) the great saphenous
vein during manual lymphatic drainage (MLD) application to the medial and lateral

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aspects of the thigh, and in (C) the popliteal vein and (D) the small saphenous vein
during MLD application to the medial and lateral aspects of the leg.

28
Page 31 of 35

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Figure 1

Page 32 of 35

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Figure 2

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Figure 3

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Figure 4

Page 35 of 35

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