Ann Vasc Dis Vol. 7, No.

1; 2014; pp 21–27 Online February 4, 2014

©2014 Annals of Vascular Diseases doi:10.3400/avd.oa.13-00107

Original Article

Subcutaneous Tissue Ultrasonography

in Legs with Dependent Edema and
Secondary Lymphedema
Kotaro Suehiro, MD, Noriyasu Morikage, MD, Masanori Murakami, MD,
Osamu Yamashita, MD, Koshiro Ueda, MD, Makoto Samura, MD,
Kaori Nakamura, and Kimikazu Hamano, MD

Objectives: To elucidate the differences in subcutaneous ultrasound findings between dependent edema
(DE) and secondary lower extremity lymphedema (LE).
Materials and Methods: Twenty legs in 10 patients with DE and 54 legs in 35 patients with LE, who first
visited our clinic between April 2009 and December 2012, were studied retrospectively. Subcutaneous echo-
genicity and echo-free space (EFS) were assessed at 8 points on the thigh and leg using an 8–12 MHz ultra-
sound transducer.
Results: In DE, echogenicity was increased most in the lower leg, without a difference between the medial
and lateral side. The EFS was most remarkable in the lower leg, and the lateral side was more severe. In the
early stages of LE, echogenicity was similarly increased in the medial thigh and in the leg, while remarkable
EFS was observed only in the lower leg. As clinical severity progressed, echogenicity increased in all parts of
the lower extremity. EFS also increased in all parts of the leg, but the lower leg was still the most severe.
Conclusion: Echogenicity seemed to progress differently in DE and LE, but EFS progressed similarly and
according to gravity. The current ultrasound findings may have added some diagnostic value in differentiating
these conditions.

Keywords: ultrasonography, subcutaneous tissue, dependent edema, lymphedema

Introduction changes, such as stasis dermatitis, hyperpigmentation,

lipodermatosclerosis, white atrophy, and venous leg
As the elderly population becomes larger, the num-
ulcers, as seen in advanced chronic venous insuffi-
ber of patients immobile because of severe gait
ciency.1) Without these typical symptoms, however,
disturbance is increasing. These people tend to sit
dependent edema is often misdiagnosed as lymph-
for prolonged periods of time. Prolonged sitting
edema because of the lack of objective diagnostic
with dependent legs leads to venous stasis, causing
means, particularly by inexperienced physicians. Since
“dependent edema.” Venous stasis can result in skin
these two types of leg edema are treated differently,
they should be properly differentiated. In this study,
Division of Vascular Surgery, Department of Surgery and we attempted to elucidate the differences in ultraso-
Clinical Science, Yamaguchi University Graduate School nographic findings between dependent edema and
of Medicine, Ube, Yamaguchi, Japan lymphedema.
Received: November 12, 2013; Accepted: December 16, 2013
Corresponding author: Kotaro Suehiro, MD. Division of
Vascular Surgery, Department of Surgery and Clinical Science,
Patients and Methods
Yamaguchi University Graduate School of Medicine, 1-1-1
This study was approved by the Institutional Review
Minamikogushi, Ube, Yamaguchi 755-8505, Japan
Tel: +81-836-22-2260, Fax: +81-836-22-2423 Board of Yamaguchi University Hospital (Ube, Yama-
E-mail: ksuehiro-circ@umin.ac.jp guchi, Japan), and the need for individual patient

Annals of Vascular Diseases Vol. 7, No. 1 (2014) 21

Suehiro K, et al.

Table 1 Patient characteristics

Dependent Edema (N = 10) Lymphedema (N = 35 )
Gender (male:female) 1:9 5:30 NS
Age (years; median [range]) 77 (49–83) 69 (45–85) NS
BMI (kg/m2; median [range]) 24.6 (18.9–38.9) 22.9 (18.9–38.9) NS
Cause of leg edema Gait disturbance due to: Cancer surgery due to:
Osteoarthritis 6 Uterine cancer 23
Post stroke 2 Ovarian cancer 5
Congenital 2 Prostate cancer 4
Bladder cancer 1
Penile cancer 1
Vulvar cancer 1
BMI: body mass index; NS: not significant

consent was waived because of the retrospective nature
of the study.
We investigated patients who first visited our
clinic between April 2009 and December 2012 com-
plaining of leg edema who met the following inclu-
sion criteria:
Dependent Edema (DE)
 A patient who sits during most of the day
because of severe gait disturbance but is not
bedridden.
 Normal lymph transport, as confirmed by
lymphangioscintigraphy (LAS).
 No apparent symptoms indicating advanced
chronic venous insufficiency, such as stasis der-
matitis, hyperpigmentation, lipodermatosclero-
sis, white atrophy, or venous ulcers.
 Venous duplex ultrasound did not show any sig-
nificant abnormalities.
 Systemic diseases that might cause leg edema
were excluded.
Lymphedema (LE)
 Newly diagnosed with secondary leg lymph-
edema caused by oncologic surgery.
Impaired lymph transport, as confirmed by LAS.
No apparent gait disturbance.
 Venous duplex ultrasound did not show any sig-
nificant abnormalities.
 Systemic diseases that might cause leg edema
were excluded.
Twenty lower extremities in 10 patients with DE
and 54 lower extremities in 35 patients with LE met
the above requirements and were involved in the
study. The characteristics of these patients are sum-
marized in Table 1. The clinical stage of lymphedema
was decided on the basis of the Consensus Docu-
ment of the International Society of Lymphology.2)
Ultrasound
During each patient’s first visit, subcutaneous tissue
was scanned using an ultrasound system (LOGIQ S6;
GE Healthcare, Little Chalfont, Buckinghamshire,
UK) with an 8–12 MHz linear transducer. The points
of scanning were as follows:
Upper medial thigh: Middle of the upper half of
the thigh, immediately anterior to the great saphe-
nous vein.
Upper lateral thigh: Middle of the upper half of the
thigh, lateral aspect of the quadriceps femoris muscle.
Lower medial thigh: Middle of the lower half of
the thigh, immediately anterior to the great saphe-
nous vein.
Lower lateral thigh: Middle of the lower half of
the thigh, lateral aspect of the quadriceps femoris
muscle.
Upper medial leg: Middle of the upper half of the
leg, immediately anterior to the great saphenous vein.
Upper lateral leg: Middle of the upper half of the
leg, lateral aspect of the tibialis anterior muscle.
Lower medial leg: Middle of the lower half of
the leg, immediately posterior to the great saphenous
vein.
Lower lateral leg: Middle of the lower half of the
leg, lateral aspect of the tibialis anterior muscle.
At each scan point, the subcutaneous echogen­
icity was graded as described in our recent report
(Fig. 1):3)
Subcutaneous Echogenicity Grade (SEG).
Grade 0: No increased echogenicity in the subcu-
taneous layer.

22 Annals of Vascular Diseases Vol. 7, No. 1 (2014)

 Ultrasonography in Dependent Edema and Lymphedema

SEG 0 1 2

Echogenicity Low Increased Increased

Echogenic lines Clear Unclear but Unidentifiable

identifiable

SEF 0 1 2

Echo-free space No EFS Horizontally oriented Presence of

(EFS) EFS only vertically oriented EFS
(<45º to the skin) (≥45º to the skin)
bridging the
horizontally oriented EFS
Fig. 1 Definition of subcutaneous echogenicity (SEG) grade and subcutaneous echo-free space (SEF) grade.
Echographic images were obtained at the lower lateral thigh in three different patients with lymphedema.
Each image is approximately up to 3 cm in depth from the skin surface. The dermo-hypodermal junction and
the upper border of the muscular fascia are not identifiable in the most advanced case (right).

Grade 1: Diffuse increases in echogenicity, but
identifiable horizontal or obliquely oriented echo-
genic lines caused by connective tissue bundles.
Grade 2: Diffuse increases in echogenicity. Echo-
genic lines are not identifiable.
Since echogenicity is a relative evaluation and is
easily changed by controlling B-mode gain, this was
first adjusted to be observed as black using normal
subcutaneous fat from another part of the body, or
from a healthy subject.
In this study, we also graded the extent of echo-
free space (EFS), which indicates identifiable edema
by ultrasound, as specified below:
Subcutaneous Echo-Free Space Grade (SEF)
Grade 0: No EFS.
Grade 1: Horizontally oriented (<45 degrees to
the skin) only.
Grade 2: Presence of vertically oriented (≥45 degrees
to the skin) EFS bridging the horizontally oriented
EFSs.
Statistical analysis
A Mann–Whitney U-test was used to compare
the SEG or SEF at the different scan points on the
leg, or between the same scan points from different
legs. Spearman’s rank correlation was used to test
the relationships between ISL stage and SEG or
SEF. Statistical analyses were performed using Dr.
SPSS II software (IBM, Armonk, New York, USA).
A P value less than 0.05 was considered statistically
significant.
Results
Subcutaneous echogenicity
The SEG in DE and LE are demonstrated in Fig. 2. In
DE, the SEG was higher in the upper medial leg and
the lower medial/lateral leg than in the upper medial
thigh. No significant differences were found between
the medial and lateral scan points at any of the same
extremity levels.
In LE, the SEG of each scan point was significantly
correlated with ISL stage. The difference in SEG
between the upper medial thigh and the medial/
lateral leg was not seen in any stage. In LE Stage I,
the SEG in the medial thigh was higher than that in
the lateral thigh. Differences in the SEG between
the medial and lateral parts at the same extremity

Annals of Vascular Diseases Vol. 7, No. 1 (2014) 23

Suehiro K, et al.

Medial
Lateral

††
2
*
† ††
†
§ * †
† †
§ †
SEG

† † †
§
1 †

0
upper thigh
lower thigh
upper leg
lower leg

upper thigh
lower thigh
upper leg
lower leg

upper thigh
lower thigh
upper leg
lower leg

upper thigh
lower thigh
upper leg
lower leg
DE LE Stage I LE Stage II LE Stage III
Fig. 2 S
EG in dependent edema and lymphedema. DE: dependent edema; LE: lymphedema.
*: P <0.05 between the medial and the lateral scan points at the same extremity level; §: P <0.05 com-
pared to the upper medial thigh in the same group; †: P <0.05 compared to the same scan point in DE.

level were not found in the leg nor in any part of upper/lower lateral leg in LE Stage I and in the lower
the lower extremities in LE Stages II and III. lateral leg in LE Stage II. On the contrary, the SEF
When the same scan points from DE and LE Stage was higher in the upper/lower medial thigh in LE
I were compared, the SEG was significantly higher in Stage II, and in all parts in LE Stage III, except in the
the upper/lower medial thigh and was lower in the lower lateral leg.
lower lateral leg in LE Stage I. In LE Stages II and III,
the SEG was higher in all identical parts to DE,
Discussion
except in the lower leg.
There were two major findings in the current study.
Subcutaneous echo-free space First, in DE, increases in subcutaneous echogenicity
The SEF in DE and LE are shown in Fig. 3. In DE, the and EFS were most evident in the lower lateral leg,
SEF was higher in all parts of the leg than in the upper while the upper medial thigh was preserved. Second,
medial thigh. The SEF was significantly higher in the in LE, increases in echogenicity were evident in the
lateral leg than in the medial leg. medial thigh and the leg in earlier stages of the dis-
In LE, the SEF of each scan point was signifi- ease, while EFS was evident in the lower leg.
cantly correlated with the ISL stage. For each stage,
a significant increase in the SEF in the lower leg Grading of subcutaneous echogenicity and
compared to the upper medial thigh was found. No echo-free space
significant differences were found between the SEF Increased echogenicity is not a finding specific to
in the medial or lateral parts of any extremity levels lymphedema, and is seen in various inflammatory
in any stage of LE. conditions.4) However, the histological characteristics
When the same scan points in DE and LE were of the extracellular matrix in chronic lymphedema are
compared, the SEF was significantly lower in the similar to those in chronic inflammation.5) Therefore,

24 Annals of Vascular Diseases Vol. 7, No. 1 (2014)

 Ultrasonography in Dependent Edema and Lymphedema

Medial
Lateral
*

§† §
2
* †
§

† †

§ †
SEF

†
§§
§†
1 § †
† †
§
†

0
upper thigh
lower thigh
upper leg
lower leg

upper thigh
lower thigh
upper leg
lower leg

upper thigh
lower thigh
upper leg
lower leg

upper thigh
lower thigh
upper leg
lower leg
DE LE Stage I LE Stage II LE Stage III
Fig. 3 S
 EF in dependent edema and lymphedema. DE: dependent edema; LE: lymphedema. *: P <0.05 between
the medial and the lateral scan points at the same extremity level; §: P <0.05 compared to the upper
medial thigh in the same group; †: P <0.05 compared to the same scan point in DE. Note that fluid accu-
mulation was not seen (SEF 0) in the lateral thigh of the legs with Stage I lymphedema.

the application of these ultrasound findings to inflam- vertical fibrous septa separating the superficial fas-
mation, i.e., the increased echogenicity of subcutane- cial system.7) Fluid accumulation in these spaces will
ous fat, to evaluate extremity lymphedema would be form a “cobblestone” appearance. In the current
appropriate. We recently confirmed that the SEG was study, this sequence of fluid accumulation was graded.
well correlated with ISL stage in secondary lower Because the terms “horizontally” and “vertically”
extremity lymphedema.3) were not clearly defined in the literature, we used a
In mild edema, a thin EFS is seen along with hori- measurement of 45° to differentiate these conditions
zontally or obliquely oriented echogenic lines, i.e., the for convenience. Some of the vertically oriented EFSs
superficial fascia, in which collagen fibers are run- may have been dilated lymphatics, but identification
ning in all directions. Since most of the superficial is quite difficult.
nerves, arteries, veins, and lymphatics are embedded
in this layer,6) initial accumulation of fluid in this Subcutaneous echogenicity
space may be reasonable. The EFS in the sub-dermal Since edema is currently considered to be caused by
area or above the deep (muscular) fascia may be an imbalance between capillary filtration and lymph
seen in earlier stages of edema, both of which are drainage, but not venous capillary reabsorption,8)
again horizontally oriented. In advanced edema, a any form of edema can present with symptoms mim-
vertically oriented EFS becomes evident along with icking lymphedema.9) Therefore, we tried to investi-
an increase in width of the horizontally oriented gate the changes in echogenicity in legs with DE as
EFS. This vertically oriented space is considered to well as LE.
be formed by an extension of the superficial fascial A new finding in the current study regarding echo-
system tightly encasing the superficial fat in vertically genicity was the difference of distributions in DE
oriented compartments and/or the interconnecting and LE. In DE, the lower the leg level, the higher the

Annals of Vascular Diseases Vol. 7, No. 1 (2014) 25

Suehiro K, et al.
echogenicity. This may indicate that this distribution
simply follows gravity. However, in LE, increased
echogenicity was noticed in the medial side of the
extremity, particularly in earlier stages. Since second-
ary lower extremity lymphedema is caused by con-
gestion in the ventromedial bundle (VMB), this
distribution seems reasonable. As the LE stage pro-
gresses, increases in echogenicity extended widely,
which indicates that chronic inflammation caused by
lymph congestion spread from around the VMB to
the entire extremity.
Subcutaneous echo-free space
In DE, the most remarkable EFS (i.e., edema) was
found in the lower leg, which is again presumed to be
caused by gravity. An interesting finding is that edema
was more severe on the lateral side. One possible
explanation is that fluid in the medial side of the leg
may be better drained by the VMB. Another possible
explanation is a difference in compliance of the
superficial fascia. The primary function of the super-
ficial fascia is to encase, support, and shape the fat of
certain body regions and to hold the skin onto the
underlying tissue.6) Since it has been reported that the
amount and thickness of superficial fascia varies in
different parts of the body,6,10) it is estimated that the
compliance of the subcutaneous tissue may be differ-
ent in the medial and lateral lower leg.
Although mild edema was found in the medial
thigh in LE Stages I and II, more severe edema was
generally seen in the lower leg in all stages of LE.
However, this distribution was different from that of
echogenicity. It is now estimated that the extent of
chronic inflammation resulting from lymph conges-
tion may follow the distributions of lymph trunks,
but fluid accumulation may be affected by both lym-
phatic transport and gravity. In LE Stage III, edema
in the lower lateral leg seemed even more severe than
in the medial side. It is assumed that advanced LE
may show a mixed picture of LE and DE, because
these patients can suffer significant gait disturbance
from the heaviness of the extremity, reduced joint
movement due to fibrosis of the surrounding tissue,
and other related issues.
Limitations
Our SEG and SEF have not been supported by any
pathological basis, but were simply defined based on
empirical facts; accordingly, they might not hold
26
validity. These grades should be further examined in
studies including larger numbers and wide varieties
of subjects.
The finding of increased subcutaneous echogenic-
ity involves potential problems. Since the superficial
fascial system varies significantly as the level of adi-
posity changes, the connective tissue becomes indis-
tinct in obese subjects.7) This is particularly evident
in the upper medial thigh, where more fat is accumu-
lated than in other parts of the lower extremity, such
that the interpretation of the visibility of echogenic
lines in this region more difficult. Furthermore, obe-
sity itself is known to impede lymphatic flow, which
leads to collection of protein-rich lymphatic fluid in
the subcutaneous tissue and subsequent fibrosis
mimicking lymphedema.11) Presently, there are no
means to clearly separate normal and pathological
fat accumulation, otherwise these conditions might
not able to be separated. In increased edema, the
extremity may present as lymphedema, CVI, or both.
Each of these conditions exhibits a characteristic
skin presentation caused by inflammation from dif-
ferent mechanisms, but these are not able to be dif-
ferentiated by ultrasound at present.
Conclusion
We found that SEG, indicating subcutaneous inflam-
mation, progresses differently in DE and LE, but SEF,
indicating edema, similarly progressed according to
gravity in edematous legs. The diagnosis of these two
types of edema should be made by taking a medical
history, careful physical examinations, and other var-
ious examinations. The current ultrasound findings
may have some added diagnostic value in differenti-
ating these conditions.
Acknowledgement
The authors gratefully thank Dr. Takako Hamamoto
(Tokyo Vascular Clinic, Tokyo, Japan) and Dr. Yoshi-
hiro Ogawa (Limbs Tokushima Clinic, Tokushima,
Japan) for their suggestions and encouragement
during this study.
Disclosure Statement
The authors have no conflicts of interest to declare.
Annals of Vascular Diseases Vol. 7, No. 1 (2014)

References
1) Partsch H. Intermittent pneumatic compression in immo-
bile patients. Int Wound J 2008; 5: 389-97.
2) International Society of Lymphology. The diagnosis and
treatment of peripheral lymphedema. 2009 Concensus
Document of the International Society of Lymphology.
Lymphology 2009; 42: 51-60.
3) Suehiro K, Morikage N, Murakami M, et al. Significance
of ultrasound examination of skin and subcutaneous
tissue in secondary lower extremity lymphedema. Ann
Vasc Dis 2013; 6: 180-8.
4) Fornage BD. Sonography of the skin and subcutaneous
tissues. Radiol Med 1993; 85: 149-55.
5) Földi M, Földi E. Földi’s Textbook of Lymphology.
Munchen: Urban & Fischer Verlag, 2011: 266-93.
6) Abu-Hijleh MF, Roshier AL, Al-Shboul Q, et al. The
membranous layer of superficial fascia: evidence for its
Annals of Vascular Diseases Vol. 7, No. 1 (2014)
Ultrasonography in Dependent Edema and Lymphedema
widespread distribution in the body. Surg Radiol Anat
2006; 28: 606-19.
7) Lockwood TE. Superficial fascial system (SFS) of the
trunk and extremities: a new concept. Plast Reconstr Surg
1991; 87: 1009-18.
8) Levick JR, Michel CC. Microvascular fluid exchange and
the revised Starling principle. Cardiovasc Res 2010; 87:
198-210.
9) Mortimer PS, Levick JR. Chronic peripheral oedema: the
critical role of the lymphatic system. Clin Med 2004; 4:
448-53.
10) Li W, Ahn AC. Subcutaneous fascial bands—a qualita-
tive and morphometric analysis. PLoS ONE 2011; 6:
e23987.
11) Yosipovitch G, DeVore A, Dawn A. Obesity and
the skin: skin physiology and skin manifestations of
obesity. J Am Acad Dermatol 2007; 56: 901-16; quiz
917-20.
27