Patterns of
Lymphatic Drainage from the Skin in Patients with Melanoma
Roger
F. Uren, MD1,2,3, Robert
Howman-Giles,
MD1,2,3 and John F.
Thompson, MD3,4
1
Nuclear Medicine and Diagnostic Ultrasound, RPAH
Medical Centre, Sydney, New South Wales, Australia
2 Department of Medicine, University of Sydney,
Sydney, New South
Wales, Australia
3 Sydney Melanoma Unit, Royal Prince Alfred
Hospital, Camperdown, New
South Wales, Australia
4 Department of Surgery, University of Sydney,
Sydney, New South
Wales, Australia
An essential prerequisite for a successful sentinel lymph node
biopsy
(SLNB) procedure is an accurate map of the pattern of lymphatic
drainage from the primary tumor site in each patient. In
melanoma
patients, mapping requires high-quality lymphoscintigraphy, which
can
identify the actual lymphatic collecting vessels as they
drain into
the sentinel lymph nodes. Small-particle radiocolloids are
needed to
achieve this goal, and imaging protocols must be
adapted to ensure
that all true sentinel nodes, including those
in unexpected
locations, are found in every patient. Clinical prediction
of
lymphatic drainage from the skin is not possible. The
old clinical
guidelines based on Sappey’s lines therefore should
be abandoned.
Patterns of lymphatic drainage from the skin
are highly variable from
patient to patient, even from the same area of
the skin. Unexpected
lymphatic drainage from the skin of the back to
sentinel nodes in the
triangular intermuscular space and, in some
patients, through the
posterior body wall to sentinel nodes in the
para-aortic,
paravertebral, and retroperitoneal areas has
been found. Lymphatic
drainage from the head and neck frequently
involves sentinel nodes in
multiple node fields and can occur from the
base of the neck up to
nodes in the occipital or upper cervical areas
or from the scalp down
to nodes at the neck base, bypassing many node
groups. The sentinel
node is not always found in the nearest node
field and is best
defined as "any lymph node receiving direct
lymphatic drainage
from a primary tumor site." Lymphatic drainage
can occur from
the upper limb to sentinel nodes above the
axilla. Drainage to the
epitrochlear region from the hand and arm as well as to the
popliteal
region from the foot and leg is more common than was previously
thought. Interval nodes, which lie along the course of
a lymphatic
vessel between a lesion site and a recognized node
field, are not
uncommon, especially in the trunk. Drainage across
the midline of the
body is quite common in the trunk and in the
head and neck.
Micrometastatic disease can be present in any
sentinel node
regardless of its location, and for the SLNB
technique to be
accurate, all true sentinel nodes must be
biopsied in every patient.
Key
Words: lymphatic drainage • skin melanoma
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INTRODUCTION |
This article has been prepared to complement the review of sentinel
lymph
node biopsy (SLNB) in melanoma written by Mariani et al. (1)
and published in 2002. That review provided a detailed account
of the
technical aspects of SLNB in melanoma. In this article, we
concentrate on the common and less common patterns of lymphatic
drainage
that are seen in melanoma patients. It is critically important
for
any unexpected drainage pattern to be detected in
every such patient
for the SLNB method to be accurate.
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LYMPHATIC
MAPPING OF THE SKIN |
Lymphatic mapping of the skin has been studied for several centuries.
When
Sappey published an elegant and comprehensive atlas in 1874,
many
believed that there was little more to discover on this
topic (2).
Sappey defined demarcation lines that passed down
the midline front
and back, along a horizontal line around the
waist at the level of
the umbilicus anteriorly, and to the level of
the L2 vertebra
posteriorly. It was Sappey’s firm view that
lymph channels did not
cross these lines and that prediction of the
direction of lymphatic
drainage from the skin was quite simple if
these rules were followed.
Most clinicians were comfortable with this
system, and it was
followed in clinical practice for almost 100 y.
After the
development of lymphoscintigraphy in the 1950s (3),
however, interest in studying patterns of lymphatic drainage
in
patients with melanomas was rekindled. Researchers observed that
Sappey’s rules did not always prove to be correct (4,5).
They found that there were "zones of ambiguity" close to
Sappey’s lines at which prediction of the direction of
lymphatic
drainage was not possible. This finding led to the
concept that
within a 10-cm region straddling Sappey’s lines,
lymphatic drainage
was uncertain.
With this
knowledge, clinicians began to use lymphoscintigraphy in
patients with melanomas located in these ambiguous areas to
identify
lymph node fields that received lymphatic drainage before
elective
dissection (6–10).
These were patients
with melanomas near the midline, around the waist, and in
the head
and neck. The method proved very accurate in this role, and
nodal
recurrences rarely were seen outside the fields identified by
lymphatic mapping.
The
description by Morton and colleagues of the SLNB technique with
blue dye injections for patients with melanomas (11)
prompted
others to search for simpler alternative approaches. Alex et
al.
(12) and Krag et al. (13) adapted the
technique of Morton et al. by using a
radiocolloid to label the
sentinel node so that it could be found with a 
-detection
probe. Lymphoscintigraphy was also quickly
adapted to locate the
sentinel node and thus became an important and
integral part of the
procedure (14). At
present, preoperative
lymphoscintigraphy is a routine part of the
SLNB method practiced in
most major centers. It is combined with blue
dye injection before
surgery and a -detection
probe intraoperatively.
There is
general agreement that this combination is the most accurate
way to identify all true sentinel nodes in every patient. If
the
sentinel node is located accurately, then the benefits of
SLNB, such
as minimal surgery with low morbidity, will follow.
This approach,
when combined with a more detailed histologic examination
of sentinel nodes (15), will have
a significant impact
on staging patients with melanomas and ultimately may aid
in the
development of better therapies for patients who are
truly node
positive or node negative. It is quite possible that,
in the past,
many patients thought to be node negative were
in fact node positive
but that the true sentinel node was missed.
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SENTINEL
NODE |
"A sentinel lymph node is any lymph node which receives lymph
drainage
directly from a tumor site" (16).
A sentinel
node is not just the first node seen on dynamic imaging, because
there may be multiple separate lymph channels that have different
rates of lymph flow. If these channels drain to different nodes,
then
all of these nodes are sentinel nodes, regardless of
the time taken
for the lymph containing the radiocolloid to
reach them. A sentinel
node is also not necessarily the node closest
to the primary site.
Lymphatic vessels can bypass many nodes before
reaching the sentinel
node (Fig. 1).
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FIGURE 1.
Patient with melanoma on vertex of scalp just to left of midline and
lymphatic drainage down to left level V node at base of neck. (A)
Lymphoscintigraphy findings on delayed imaging 2 h after injection of 7
MBq of 99mTc-antimony sulfide colloid
intradermally at 4 points around excision biopsy site. Anterior and
left lateral views are shown, and lymphatic vessel can be faintly seen
passing directly to sentinel node in left lateral view. Lt = left; Rt =
right. (B) Patient at end of study. Sentinel node (SN) location is
marked on skin with "X." Injection site on scalp is indicated by thick
arrow.
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The best way to identify a sentinel node on lymphoscintigraphy
is
therefore to visualize the lymphatic collecting vessel on dynamic
imaging as it drains directly into the sentinel node (Fig.
2). In order to achieve this goal, there must be adequate
numbers
of radiocolloid particles in the lymph fluid during the
early dynamic
phase; small-particle radiocolloids therefore must
be used. This
lymphatic collecting vessel is the same one that
the surgeon sees
staining blue in the operative field during sentinel
node surgery.
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FIGURE 2.
Lymphoscintigraphy of patient with excision biopsy site on anterior
left thigh above knee. Two lymphatic collecting vessels can be seen
passing to left groin in 10-min summed dynamic image (top left). Medial
channel can be seen draining to sentinel node in femoral area, whereas
more lateral channel bypasses this node to reach another sentinel node
higher in groin. Delayed images show these 2 bright sentinel nodes with
faint second-tier activity between them. Depth of sentinel nodes
beneath skin is shown in left lateral view with point source on skin
marks (bottom right). Lt = left; Rt = right.
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LYMPHOSCINTIGRAPHY METHODS |
Lymphoscintigraphy to locate sentinel lymph nodes in patients
with
melanomas involves the intradermal injection of a radiocolloid
near
the melanoma site or excision biopsy site (1,14).
Injections of 5–10 MBq in a volume of 0.05–0.1
mL are used, and
typically 4 injections are required, although the number of
injections depends on the primary melanoma size. After tracer
injection,
dynamic imaging is performed to follow the course of
the lymphatic
collecting vessels until they reach the draining sentinel
nodes. An
image should be acquired as the vessels reach the
node field so that
sentinel nodes directly receiving the channels
can be identified and
distinguished from any second-tier nodes that
may be seen. This phase
of the study usually takes 10–20 min.
Delayed scans
are performed 2–2.5 h later, at which time all
regions that could possibly drain the primary melanoma site are
examined with static images of 5–10 min. Appropriate lateral,
posterior, oblique, or vertex views are also acquired as
necessary to
define the exact locations of all sentinel nodes. We
routinely use a
transmission source on all delayed images to
highlight the body
outline, and these images are especially useful
for retrospective
review of the images. We often repeat delayed
scans without the
transmission source, however, as in some
patients a faint sentinel
node in a new node field is obscured by the
scattered activity from
the source. Most of the images shown in this
article were acquired
without a transmission source for this reason,
and the body outline
was added later.
The surface
locations of all sentinel nodes are marked on the overlying
skin with an "X" of indelible ink; a permanent point tattoo
of carbon black (Fig. 1) can also
be applied and is a useful
guide for clinical or ultrasound follow-up over subsequent years.
The
depth of the sentinel node from the skin mark is measured
in an
orthogonal view with a radioactive marker placed on
the skin mark.
The depth can then be measured from the film directly
or by using
electronic calipers. Some centers use a -probe
in a nuclear medicine suite to further aid in the localization
of
sentinel nodes, but we have not found this procedure necessary.
Regardless
of how imaging data for a patient are presented to the
surgeon, it is
essential that the surgeon completely understands the
presentation.
The surgeon must be familiar with the appearance of
the images in
order to refer to them while searching for sentinel
nodes during
surgery. This very close communication with
surgical colleagues is
vital for the accuracy of the SLNB method.
We have
successfully used this protocol for over 3,000 patients with
cutaneous melanomas. More detailed descriptions of our technique
and
imaging protocol can be found elsewhere (14,16).
If possible,
lymphatic mapping should be done before wide local excision
of the primary melanoma, as the latter disrupts lymph drainage
pathways and may cause a lack of migration of the tracer or
the
identification of lymph nodes that are not true sentinel nodes.
A radiocolloid
must gain access to the lumen of the initial lymphatic
vessels under physiologic conditions to allow accurate mapping
of
lymphatic drainage. A brief consideration of the microanatomy
of the
lymphatic system is therefore relevant here.
Physiology
and Microanatomy of Cutaneous Lymphatics
The initial lymphatic capillaries are the terminal lymphatics
and
have no intraluminal valves. They also have an incomplete basement
membrane and do not have a complete muscle layer (17,18).
They are formed by overlapping endothelial cells, so that
there are
gaps of about 10–25 nm between the cells. Elastin fibrils
on the
outside of the endothelial cells are attached to
collagen fibers in
the interstitial matrix, so that the gaps between
the lymphatic
endothelial cells can be markedly widened by
movement of the tissues,
such as by exercise or massage. This action
also increases the volume
and flow of lymph. The entry of radiocolloid or
blue dye into the
lymphatic capillaries is thus increased
significantly by massage or
exercise of the part. External pressure, in
contrast, markedly
decreases lymph flow, and even quite light
pressure has this effect (Fig.
3). This is the principle behind the
current emergency treatment
of snake bite, which includes the application of direct
pressure over
the site of the bite, rather than the use of a proximal tourniquet,
as was previously recommended. The patient shown in
Figure
3 was unusual because he had remained seated in our
waiting area
during the whole period after injection of the tracer.
(Our patients
normally ambulate for the 2-h delay.) Pooling
of the tracer was seen
in the medial part of the right lymph vessel
and the inferior part of
the 2 left vessels. Pressure from the seat back
was the likely cause,
and massage with a medial to lateral stroke was
performed over both
channels, causing the sentinel nodes in each
axilla to brighten and a
second sentinel node to appear in the left
axilla. Lymph flow is also
decreased by low temperatures, and the scanning
room should be kept
at an ambient temperature of at least 21°C. The
lymphatic
capillaries follow a tortuous course and
frequently anastomose with
each other but continue to have no intraluminal
valves. They join
together eventually to form lymphatic collecting vessels
that have
a 3-layer wall and that do have intraluminal valves.
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FIGURE 3.
Lymphoscintigraphy of patient with excision biopsy site on upper back
close to midline. (Top row) Delayed images, obtained 2 h after
injection of tracer, show faint right axillary sentinel node and
brighter left axillary sentinel node. (Bottom row) Images taken
immediately after 2 min of massage show that tracer has moved to second
sentinel node in left axilla (arrow) and that right axillary sentinel
node is much brighter. Even light external pressure significantly
decreased lymph flow. Lt = left; Rt = right.
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The rates of lymph flow within lymphatic collecting vessels vary
in
different parts of the body (Table 1)
(19).
The most rapid flow occurs from the legs and
feet, followed by that
from the arms and hands. Flow from sites in the
trunk is 3 to 4
cm/min on average, while the slowest flow
occurs from the head, neck,
and shoulder regions. The lymphatic vessels have an
intrinsic pump
mechanism maintaining steady lymph flow (20),
but this mechanism
responds to an increase in hydrostatic pressure by significantly
increasing lymph flow (such as that which occurs in
the legs during
standing). Lymph flow is also increased by heat
and inflammation, and
although gravity affects the speed of flow
through hydrostatic
pressure, it does not influence the direction
of flow. The
intraluminal valves present in the lymphatic
collecting vessels
ensure that lymph flow is unidirectional toward
the draining lymph
nodes (17).
The paths taken by collecting vessels on their way to draining
node
fields vary from patient to patient and from skin site to
skin site.
These paths can sometimes be extremely complex and
tortuous (Fig.
4) (16). Lymphatic
vessels can converge to form
fewer larger vessels (Fig. 5) but
sometimes divide into multiple
vessels, most commonly in the upper thigh. The collecting vessels
usually pass through the subcutaneous fat layer and generally
do not
penetrate the deep fascia until a node field such
as the groin or
axilla is reached.
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FIGURE 4. Dynamic-phase
lymphoscintigraphy of patient with melanoma excision biopsy site (open
straight arrow) on right heel. Multiple lymphatic collecting vessels
can be seen passing up leg to right groin. These vessels reach multiple
sentinel nodes (curved arrow). Note tortuous path followed by 1 lymph
vessel to faint sentinel node high in groin (solid straight arrow). LT
= left; RT = right.
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FIGURE 5. Lymphoscintigraphy
of patient with excision biopsy site on posterior left calf. (Top row)
Summed dynamic images show 3 lymphatic collecting vessels converging to
single sentinel node in left groin. (Bottom row) Delayed images,
obtained 2 h later, show single left groin sentinel node. Note that
there are no second-tier nodes and that all tracer is retained in
sentinel node. Lt = left; Rt = right.
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Lymph Nodes
Lymph nodes trap radiocolloids by a complex physiologic process
and
do not act as simple mechanical filters. This process first involves
opsonization, the mechanism by which the particles are
recognized as
foreign (1). Opsonization can
occur in the lymph
fluid or in the node itself and aids in later phagocytosis of
the
particles. A matrix of reticulin fibrils forms a complex lattice
in
the sinuses of lymph nodes and slows the movement of
particles, such
as radiocolloids, so that they can be phagocytosed by
the macrophages
and tissue histiocytes that line the sinuses (21).
These phagocytic cells are most abundant in the subcapsular sinus.
Most of the tracer therefore is retained in this location.
Most of the radiocolloid that
reaches a lymph node will be retained in
the node by this process, regardless of the particle size, so
that
even when small-particle colloids, such as 99mTc-antimony
sulfide
colloid, are used, the sentinel node is often the only radiolabelled
node on delayed 2-h images (Figs. 2
and 5–11).
A small percentage of the tracer can pass to second-tier
nodes, regardless
of the particle size, and we have found this characteristic to
correlate directly with the speed of lymph flow in lymphatic
collecting
vessels (22). The higher the flow
rate, the greater the
incidence of radiocolloid passing to second-tier nodes. This
observation suggests that the physiologic process of phagocytosis
that
retains radiocolloid in the sentinel node can be overwhelmed
if too
many particles reach the node over a short time.
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FIGURE 11. (A) Adult with
left-arm melanoma shows single channel on dynamic lymphoscintigraphy
passing to single left axillary sentinel node, also seen on delayed
scan. (B) Two-year-old child with melanoma on right forearm shows
single right axillary sentinel node on delayed lymphoscintigraphy. Most
upper limb melanomas include axillary sentinel node. Lt = left; Rt =
right.
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Radiocolloids
The radiocolloids that best display lymphatic vessels and thus
allow
the identification of sentinel nodes are those that readily enter
the
lymphatic capillaries; these are radiocolloids with particle
sizes in
the range of 5–50 nm (23,24). These
particles easily enter the initial lymphatics under
physiologic conditions,
and their entry is enhanced by exercise or massage if
movement is
slow. With such small-particle radiocolloids, about
5%–8% of the
injected dose will migrate from the injection
site to the sentinel
node or nodes (24). Appropriate
small-particle
radiocolloids are ultrafiltered 99mTc-sulfur
colloid
(passed through a 100-nm filter), 99mT-nanocolloid
of albumin,
and 99mTc-antimony sulfide colloid.
Large-particle radiocolloids
(with particles of >200 nm in diameter),
such as unfiltered 99mTc-sulfur colloid, have
difficulty moving
through the interstitial matrix and enter the lymphatic capillaries
only in small numbers, even with exercise or massage. Lymphatic
collecting vessels thus are usually not seen on dynamic imaging
when
large-particle colloids are used. Most of the injected dose
remains
at the injection site, despite exercise or massage, with
only about
0.5% of the dose reaching the sentinel nodes (23).
Identification of the sentinel nodes then becomes problematic;
definitions
based on count ratios relative to the background are
relied upon. The
problem with this approach is that sometimes one
sentinel node has
very low activity compared with another sentinel
node and may not be
identified as a sentinel node without dynamic
imaging. These faint
nodes are sometimes the only positive sentinel
nodes in the node
field (Fig. 12).
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FIGURE 12.
Lymphoscintigraphy of patient with excision biopsy site on medial right
thigh anteriorly. (A) Summed dynamic image shows bright lymphatic
collecting vessel passing to right groin sentinel node. Very faint
second vessel can be seen medial to this vessel (arrow). (B) Delayed
image shows bright sentinel node and second faint sentinel node just
medial to this node (arrow). Second-tier node higher in groin receives
tracer from bright sentinel node and is actually "hotter" than faint
sentinel node. At histologic examination, bright sentinel node was
normal, but faint sentinel node contained micrometastasis. Lt = left;
Rt = right.
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Lymphatic Mapping in Cutaneous Melanomas to Locate
Sentinel Nodes
Since 1984, the Sydney Melanoma Unit has been performing lymphatic
mapping
with 99mTc-antimony sulfide colloid to locate
draining node
fields in patients with intermediate-thickness melanomas located
in
the so-called ambiguous zones before elective dissection of
the
relevant node field. Over a 6-y period, we had performed about
200
studies (14).
As soon as Morton and
colleagues described successful SLNB in melanoma
patients by injection of blue dye (11),
we began to apply
the method described above to locate sentinel nodes by using
lymphoscintigraphy on the day before surgery. This meant that
all
patients with intermediate-thickness melanomas were studied
regardless of the sites of the lesions on the skin. Since
our
examination required us to locate every sentinel node and
not just to
image in standard positions, we began to observe drainage
to lymph
nodes in completely unexpected places (16,25).
Some were in new node fields not previously known to drain
the skin.
We quickly began to appreciate that there was unambiguous drainage
from very few sites on the skin and that, without preoperative
lymphoscintigraphy,
accurate SLNB was simply not possible in many
patients. This
variability in lymph drainage and drainage to
sentinel nodes in
unexpected places has also been observed by
others (9,26,27).
We have now performed
lymphatic mapping for over 3,000 patients with
cutaneous melanomas and have accumulated a large body of data
relating to common and uncommon cutaneous lymphatic drainage
pathways.
All of these studies were performed by a small group of
nuclear
medicine physician consultants and were not done by
trainees. The
surgical correlation and SLNB procedures were all
performed by a
group of specialists in melanoma surgery. The
following is a detailed
description of the patterns of lymphatic drainage
that we have
observed.
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PATTERNS
OF LYMPHATIC DRAINAGE FROM SKIN |
In the studied group of 3,059 patients, 7 showed no movement
of
tracer from the injection site over a 2.5-h period. These were
older
patients; 5 patients had melanoma sites on the head and
neck, and 2
patients had melanoma sites on the trunk. Lymphatic drainage
to
sentinel nodes occurred in a single node field in 1,963
patients
(64%), 2 node fields in 803 (26%), 3 node fields in
207 (7%), 4 node
fields in 62 (2%), and 5 node fields in 7. The
majority of skin sites
thus drained to a single node field.
Posterior Trunk
The locations of sentinel nodes draining the posterior trunk
are
summarized in Table 2. This group
includes 2 lymphatic
drainage pathways that were completely
unexpected and that, before
our description, were not known to receive
direct lymphatic drainage
from the skin of the back. These lymphatic pathways drain to
the
triangular intermuscular space lateral to the scapula, behind
the
axilla (28), and pass through the
posterior body wall
directly to sentinel nodes in the
retroperitoneal and paravertebral
areas (29).
The more common of these 2 pathways is drainage from the skin
of the
back to the triangular intermuscular space (Figs.
6 and 13).
We have observed this drainage pathway in 12% of our patients
with
back melanomas. Skin sites that we have found to drain to
the
triangular intermuscular space are shown in Figure
14. Sometimes
2 nodes in this space are seen one above the other, both
lying just
deep to the deep fascia, and the pathway then passes
anteriorly,
following the course of the circumflex scapular vessels
into the
posterior part of the axilla. Therefore, in some
patients, the tracer
will pass from a sentinel node in the
triangular intermuscular space
to a second-tier node in the axilla. We have
seen this phenomenon
occur in several patients. Without accurate
lymphatic mapping by
lymphoscintigraphy, this phenomenon could lead
to a radiolabelled
second-tier node being mistakenly identified as
the sentinel node and
removed from the axilla, while the true
sentinel node in the
triangular intermuscular space remains in the
patient. Histologic
examination of this radiolabelled axillary node
will yield a false
report of the lymph node status in the patient.
This situation would
occur if only a -probe
were used to find and remove radiolabelled nodes
from the axilla or
if the lymphoscintigraphy imaging protocol were
inadequate. Older
protocols called only for anterior views of the
axilla, but posterior
and lateral views are required to identify the
sentinel nodes in this
unexpected location, because attenuation of the
photons as they pass
through the patient’s body means that nodes in
the triangular
intermuscular space may not be seen at all in
an anterior view (Fig.
6). Drainage to a sentinel node in
the triangular intermuscular
space often occurs along with drainage to a
sentinel node in another
node field, but we have encountered 8 patients
with exclusive
drainage to a sentinel node in this unexpected
location.
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FIGURE 6. Lymphoscintigrams
of 2 patients with excision biopsy sites on upper back close to
midline. Each had sentinel node in left axilla, and summed dynamic
image for each (top left) shows lymphatic collecting vessels reaching
these sentinel nodes. (A) Faint sentinel node can be seen in right
triangular intermuscular space (TIS) on dynamic image (arrow). (B) No
TIS sentinel node can be seen on dynamic image. Delayed images show
sentinel node in right TIS in both patients (arrows). This node is
clearly seen in posterior and lateral views but is not seen in standard
anterior views of axillae. Lt = left; Rt = right; RTIM = right
triangular intermuscular space.
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FIGURE 13. Patient with
melanoma behind right shoulder. (A) Delayed lymphoscintigraphy images
show 2 sentinel nodes in right axilla (straight arrow) and second-tier
node in right axilla as well as sentinel node in right triangular
intermuscular space (curved arrow). Lt = left; Rt = right. (B) Patient
at end of study. "X" marks surface locations of right triangular
intermuscular space sentinel node (SN) and 1 right axillary sentinel
node. Melanoma site is indicated by thick arrow.
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FIGURE
14. Locations of all skin sites draining to sentinel node in
right or left triangular intermuscular space.
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The second unexpected lymphatic drainage pathway that we have
observed
draining the skin of the back is one that involves direct
passage
through the posterior body wall to sentinel nodes in
the
paravertebral, para-aortic, or retroperitoneal areas. This
drainage
pattern usually involves intra-abdominal sites, but
we have also seen
paravertebral nodes in the thorax as sentinel nodes
draining the skin
of the back. The skin sites that may drain
through this unexpected
pathway are concentrated mainly in the
posterior loin area (Fig.
15). We have observed this pathway in
4% of patients with back
melanomas, making it much less common than the
pathway draining to
the triangular intermuscular space. If we
consider only the posterior
loin area, however, we find drainage through
this pathway in 24% of
patients. Again, drainage to sentinel nodes in
these unexpected areas
is usually accompanied by drainage to sentinel
nodes in expected node
fields (the axilla and groin); however, we have
encountered 4
patients with exclusive drainage to sentinel
nodes in these areas but
with no drainage whatsoever to nodes in the axilla or groin
(Fig.
7) (30). The importance
of identifying drainage to
sentinel nodes in the paravertebral,
para-aortic, and retroperitoneal
areas is that metastatic disease in one of these nodes
represents locoregional
metastasis, not systemic disease.
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FIGURE 15.
Location of skin sites draining directly through body wall to sentinel
nodes in paravertebral, para-aortic, and retroperitoneal areas.
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FIGURE 7.
Delayed lymphoscintigraphy images of patient with melanoma excision
biopsy site in posterolateral right loin area. Lymphatic channels
passed directly through body wall to sentinel node in retroperitoneal
area (vertical arrow) and sentinel node in right para-aortic region
(horizontal arrow). There was no drainage to sentinel nodes in either
axilla or groin. Depth of sentinel nodes is shown in right lateral view
with point source on posterior skin mark. Nodes lay 5 and 6.5 cm deep
relative to skin of back. Lt = left; Rt = right.
|
|
Most patients with melanoma sites on the posterior trunk do show
drainage to sentinel nodes in the expected node fields, such
as the
axilla and groin, but drainage to combinations of node
fields is also
very common and will be missed without preoperative lymphatic
mapping
by lymphoscintigraphy. It is also remarkable how
often lymph drains
from the upper back over the shoulder to nodes
in the supraclavicular
fossa or to other nodes in the neck (Figs. 8 and 16).
Careful imaging including vertex or lateral oblique
views is required
to ensure that all sentinel nodes are
identified around the base of
the neck, since such nodes are often obscured
by injection site
activity in straight anterior or posterior
views.
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FIGURE 8.
Lymphoscintigraphy of patient with excision biopsy site on upper back
to right of midline. (Left) Two lymph vessels can be seen on posterior
summed dynamic image, 1 passing over shoulder to sentinel node in right
supraclavicular fossa and 1 passing to sentinel node in right axilla.
(Right) Both of these sentinel nodes are visible on anterior delayed
image. However, sometimes neck nodes are obscured by activity at
injection site in such patients, and vertical oblique views are then
required to clarify situation. Lt = left; Rt = right.
|
|
Sappey’s vertical lines do not help predict lymph flow, and
lymphatic vessels often cross the midline to reach contralateral
sentinel
nodes in expected and unexpected node fields (Fig.
17). For
lesions at the level of the waist, lymph vessels may pass
down to the
groin or up to the axilla, although most pass up
to the axilla.
Occasionally, lymph vessels also cross the horizontal
line of Sappey
around the waist but usually do so to pass up
to the axilla from
below rather than to pass down to the groin
from above the line of
Sappey.
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FIGURE 17.
Locations of skin sites on back draining to right axilla (A) and left
supraclavicular fossa (B). Note that drainage from contralateral side
of back is common in each case.
|
|
Interval nodes, which are nodes that lie along the course of
a
lymphatic collecting vessel between a primary site and a draining
node
field, have been seen as sentinel nodes more commonly on the
back
than elsewhere in our patients with melanomas (see below).
Anterior
Trunk
Lymphatic drainage from the skin of the anterior trunk generally
occurs
to expected node fields, and there tends to be less passage of
lymph
vessels across the midline than in the posterior trunk (Table
2). Even on the anterior upper chest, vessels tend to
pass to
axillary nodes rather than up over the clavicle to neck nodes,
although exceptions do occur (Fig. 9).
Those that do pass
to neck nodes arise from a more restricted area of the anterior
upper
chest than is seen on the upper back (Fig.
18). Drainage
to interval nodes is also less common anteriorly than on
the back.
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FIGURE 9.
Delayed lymphoscintigraphy of patient with excision biopsy site over
manubrium. Drainage to sentinel node in supraclavicular fossa on each
side can be seen; there is no drainage to either axilla. Lt = left; Rt
= right.
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FIGURE 18.
Locations of skin sites on anterior trunk draining to right or left
supraclavicular fossa. This drainage occurs from more restricted area
than on back, but some patients do show such drainage from low in
anterior chest.
|
|
We did detect a new unexpected drainage pathway that passes from
the
periumbilical skin to a node that lies in the subcutaneous fat
over
the costal margin (31). The
lymphatic pathway then passes
medially and through the chest wall to internal mammary nodes
on the
same side as the costal margin node. The pathway always
meets a
costal margin node first, however; therefore, the
sentinel node in
these patients is the costal margin node, and
the internal mammary
node receives drainage as a second-tier node.
In fact, we have seen
an internal mammary node as a sentinel node for
the skin of the
anterior trunk in only 2 patients. One had
undergone lymph node
dissection of the ipsilateral axilla 20 y
earlier as a treatment for
lymphoma. This procedure presumably caused an
alternative lymphatic
drainage pathway to appear. The other patient
had undergone an
extensive excision biopsy of a melanoma in the
epigastrium and showed
drainage to a sentinel node in the right
internal mammary chain as
well as to a left axillary sentinel node.
Head
and Neck
Details for lymphatic drainage from the skin of the head and
neck are
shown in Table 3. The head and
neck are challenging areas
for accurate lymphatic mapping, both for nuclear medicine physicians
and for surgeons. Drainage to multiple sentinel nodes is
common (16,32),
and the nodes are often small (Fig. 19).
The
draining sentinel nodes often lie very near or sometimes immediately
beneath the melanoma site. Detection of such nodes by
lymphoscintigraphy is thus extremely difficult and sometimes
impossible.
However, if care is taken and such limitations are understood,
accurate lymphatic mapping and biopsy of sentinel nodes
can be
achieved in the head and neck just as elsewhere in
the body.
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FIGURE 19.
Patient with excision biopsy site on right side of nose. (A) (Top row)
Summed dynamic lymphoscintigraphy images. (Bottom row) Delayed
lymphoscintigraphy images. Two separate lymphatic vessels reach 2
sentinel nodes, 1 in parotid region and 1 in right submandibular
region. Lt = left; Rt = right. (B) Patient at end of study. Sentinel
node (SNs) are marked on skin with "X." Melanoma site on nose is
indicated by thick arrow. Multiple draining node fields are common in
head and neck.
|
|
Also, as we have found elsewhere, the clinical prediction of
lymphatic
drainage in the head and neck is unreliable, and 33% of
patients show
drainage to node sites that is discordant with the
clinical
prediction (32). Such drainage
often occurs to postauricular
nodes from the skin of the face and anterior scalp. These
nodes are
not usually excised in elective neck dissections for
melanoma.
Drainage also occurs across the midline, and we have
seen such
drainage in 15% of patients with head and neck melanomas
(Fig.
10). Such a contralateral node can occasionally be
the only site
of micrometastatic disease. Lymph drainage also
quite often occurs
from the base of the neck up to nodes in the
upper cervical or
occipital area. Again, for some patients with
this pattern, the only
positive node seen is an occipital node, even
though other sentinel
nodes are present in the axilla, upper cervical
area, and lateral
neck base. Drainage is also seen regularly from
the upper scalp
directly down to nodes at the base of the neck
or in the
supraclavicular region (Fig. 1).
Lymphatic vessels
reaching these nodes thus completely bypass all
the nodes in the
upper and middle cervical areas as well as the
preauricular
(parotid), occipital, and postauricular nodes.
These findings
reinforce the concept that the sentinel node is
not simply the node
closest to the primary melanoma site.
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FIGURE 10.
Dynamic and delayed lymphoscintigraphy of patient with excision biopsy
site on left cheek. Sentinel node can be seen in left submandibular
region (level I) (straight arrow). Another sentinel node can be seen in
right midcervical area (level III) (curved arrow). Such contralateral
drainage is not uncommon in head and neck. Lt = left; Rt = right.
|
|
Upper Limb
Lymph drainage from the skin of the upper limb occurs to the
axilla,
as expected, in almost all patients (Fig. 11).
However, this
scenario is often not the complete picture (Table
4). Drainage
to sentinel nodes in the epitrochlear region is more common
than
was previously thought, and we have observed drainage to this
site in
36 of 218 patients (16%) with melanomas located on
the forearm and
hand. We have also detected direct drainage to
sentinel nodes above
the axilla in the supraclavicular region, interpectoral
region,
lateral neck base, and triangular intermuscular space
in some
patients (16). These patients
also had a sentinel node
in the axilla, and lymph drainage to these unexpected sites occurred
through a separate, discrete lymph vessel. Relying exclusively
on -probe-guided
removal of axillary sentinel nodes in these
patients would have
missed these other sentinel nodes. Thus,
accurate lymphatic mapping
by lymphoscintigraphy is imperative.
An interval node is regularly seen lying medially in the arm
about
halfway between the shoulder and the elbow (Fig.
20). We
have seen one patient with drainage exclusively to this interval
node
in the middle inner arm, so that it was the only sentinel node.
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FIGURE 20. Patient with
excision biopsy site on left arm above and behind elbow. (A)
Lymphoscintigraphy shows that channels pass to interval node (1 of the
sentinel nodes in this patient) in medial arm (curved arrow) and to 2
sentinel nodes in left axilla. Lt = left; Rt = right. (B) Patient at
end of study. Melanoma site is indicated by thick arrow. Sentinel nodes
(SNs) are marked on skin with "X."
|
|
Lower Limb
The skin of the lower limb drains to the ipsilateral groin unless
there
has been prior surgery to the groin nodes. In this circumstance,
drainage
to the contralateral groin may occur, and we have found micrometastases
in such contralateral groin sentinel nodes (33).
Lymph drainage from the foot
and leg to the popliteal lymph nodes
may also occur, and we have observed such drainage in 38
of 481
patients (8%) with melanomas in these areas. The melanoma sites
draining to the popliteal nodes are quite variable, and it
is not
just the skin of the lateral heel that drains here, as
was previously
thought (34) (Fig.
21).
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FIGURE 21. Locations of skin
sites draining from posterior legs and feet to sentinel nodes in
popliteal fossae.
|
|
Interval Nodes
Interval nodes can be sentinel nodes, and we have seen 10 patients
for
whom these nodes were the only sentinel nodes. When present,
they
must be detected and removed if an SNLB procedure is to be
accurate.
We have shown that these interval nodes, when sentinel nodes,
contain
micrometastases with the same incidence as sentinel nodes
found in
standard node fields (35). We
found interval nodes
in 7% of patients overall, and they were more common on the
trunk
(12% posterior trunk and 8% anterior trunk) than in the
head and neck
(5%) or upper limb (4%) and were rare in the lower
limb (0.5%). In a
large multicenter study, McMasters and colleagues
(36)
also found that in melanoma patients, interval nodes
were positive
for metastases at the same frequency as sentinel
nodes in standard
node fields. In their 13 patients with positive
interval nodes, such
nodes were the only positive sentinel nodes in
11 patients (85%).
Although interval nodes may be
found at any point along the course
of a lymphatic collecting vessel, they are more common in
certain
locations, such as the midaxillary line, the upper back,
and the
medial aspect of the middle upper arm.
Interval nodes remain "hot" on
delayed scans because they retain
the radiocolloid, although it is notable that much of the
radiocolloid
reaching interval nodes passes to second-tier nodes. They
thus seem
to be more "porous" to radiocolloids than sentinel nodes in
standard node fields or unexpected node fields.
Lymphatic Lakes
Unlike interval nodes, lymphatic lakes do not need to be examined
during
SLNB procedures. They are focal dilatations of lymphatic collecting
vessels. They are seen during lymphoscintigraphy as
a focal area of
increased tracer retention along the course of
a lymphatic collecting
vessel during the dynamic early postinjection phase
of the study. The
activity rapidly passes through the lymph
vessel, however, so that
these lymphatic lakes are not visible on
delayed scans performed 2 h
later. Lymphatic lakes should not be mistaken
for interval nodes,
which retain tracer and are therefore hot on
delayed scans.
|
CONCLUSION |
Lymphatic drainage from the skin is highly variable from patient
to
patient, even when the same region of the body is being examined.
The
path taken by lymphatic collecting vessels is unpredictable,
as is
the ultimate location of the draining sentinel node or nodes,
as
several recent studies have confirmed (14,36–38).
Preoperative
lymphoscintigraphy with small-particle radiocolloids allows
these lymphatic vessels to be visualized draining directly to
sentinel nodes. Careful imaging techniques will thus allow all
true
sentinel nodes to be identified in each patient, even if
these nodes
lie outside standard node fields or are interval nodes
lying between
the primary site and a node field. This information
is an important
contribution to the management of patients with
melanomas, as it will
lead to more accurate nodal staging of patients
with high-risk
melanomas.
We now know that the clinical
prediction of the pattern of lymphatic drainage
in an individual patient is unreliable and inaccurate. We
also now
know that we have an accurate method of mapping lymphatic
drainage in
every patient, making the difficulties associated
with clinical
prediction irrelevant. This technique, which
provides an accurate map
of lymphatic drainage in each patient, can thus
have a direct and
important impact on the clinical management of
patients with
melanomas.
|
ACKNOWLEDGMENTS |
We thank all of the excellent nuclear medicine technologists
whose
dedication has been so important to the success of our lymphatic
mapping work, including Kim Ioannou, Nicholas Trpezanovski, Angelique
Nguyen, Tracey Smith, Sally Raymond, and Ian Dyer. We
thank the other
nuclear medicine physicians who have added their
enthusiasm to our
work, including Drs. David Chung, Robert Mansberg,
John Roberts,
Reginald Hutcherson, and Elizabeth Bernard. We
also thank the
surgeons of the Sydney Melanoma Unit for referring their
patients and
providing the surgical correlation and validation of
the lymphatic
drainage patterns that we have documented, including
Professor
William McCarthy, Dr. Michael Quinn, Dr. Kirwin
Shannon, Professor
Christopher O’Brien, Dr. Andrew Spillane, Dr.
Robyn Saw, and Dr.
Jonathon Stretch.
|
FOOTNOTES |
Received May 20, 2002; revision accepted Sep. 25, 2002.
For correspondence or reprints
contact: Roger F. Uren, MD, Suite 206,
RPAH Medical Centre, 100 Carillon Ave., Newtown, New South Wales
2042, Australia.
E-mail: ruren@mail.usyd.edu.au
*
NOTE: FOR CE CREDIT, YOU CAN ACCESS THIS ACTIVITY THROUGH THE
SNM WEB SITE (http://www.snm.org/education/ce_online.html)
THROUGH APRIL 2004. 
|
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Nuclear Medicine
===========================
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http://www.springerlink.com/content/a7856676q28n3683/SPECT/CT scans allow precise anatomical location of sentinel lymph nodes in breast cancer and redefine lymphatic drainage from the breast to the axilla. Dec 2011
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http://www.ncbi.nlm.nih.gov/pubmed/22165580
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Effects of lymphatic drainage and omega-3 polyunsaturated fatty acids on intestinal ischemia-reperfusion injury in rats Jul 2011
Can lymphatic drainage of head and neck melanoma be predicted? June 2011
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http://onlinelibrary.wiley.com/doi/10.1002/hed.21089/abstractVessels, lymphatic drainage and the breast
http://www.dartmouth.edu/~humananatomy/part_2/chapter_7.html
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http://www.lymphedemapeople.com/thesite/lymphedema_laser_treatment_saras_experience.htm
Liposuction Treatment
http://www.lymphedemapeople.com/thesite/lymphedema_liposuction_treatment.htm
Lymphedema Treatment Programs
Canada
http://www.lymphedemapeople.com/thesite/lymphedema_treatment_programs_canada.htm
Lymphedema
Sleeves
http://www.lymphedemapeople.com/wiki/doku.php?id=lymphedema_sleeves
Lymphedema Surgeries
http://www.lymphedemapeople.com/thesite/lymphedema_surgeries.htm
Lymphedema Treatments are
Poorly Utilized
http://www.lymphedemapeople.com/thesite/lymphedema_treatments_are_poorly_utilized.htm
Manual
Lymphatic Drainage
http://www.lymphedemapeople.com/wiki/doku.php?id=manual_lymphatic_drainage_mld_complex_decongestive_therapy_cdt
Microsurgeries
http://www.lymphedemapeople.com/thesite/lymphedema_and_microsurgery.htm
Reflexology Therapy
http://www.lymphedemapeople.com/thesite/lymphedema_and_reflexology_therapy.htm
Short Stretch Bandages
http://www.lymphedemapeople.com/wiki/doku.php?id=short_stretch_bandages_for_lymphedema
Surgeries
http://www.lymphedemapeople.com/thesite/lymphedema_surgeries.htm
Treatment
Information for Lymphedema Forum
http://www.lymphedemapeople.com/phpBB2/viewforum.php?f=8
Why
Compression Pumps cause
Complications with Lymphedema
http://www.lymphedemapeople.com/phpBB2/viewtopic.php?t=327
===========================
Join
us as we work for lymphedema patients everywehere:
Advocates
for Lymphedema
Dedicated to
be an advocacy group for lymphedema
patients. Working towards education, legal reform, changing insurance
practices,
promoting research, reaching for a cure.
http://health.groups.yahoo.com/group/AdvocatesforLymphedema/
| Subscribe: |
AdvocatesforLymphedema-subscribe@yahoogroups.com |
Pat O'Connor
Lymphedema People / Advocates
for Lymphedema
===========================
For information about
Lymphedema
http://www.lymphedemapeople.com/wiki/doku.php?id=lymphedema\
For Information about
Lymphedema Complications
http://www.lymphedemapeople.com/wiki/doku.php?id=complications_of_lymphedema
For Lymphedema Personal
Stories
http://www.lymphedemapeople.com/phpBB2/viewforum.php?f=3
For information about How
to Treat a Lymphedema Wound
http://www.lymphedemapeople.com/wiki/doku.php?id=how_to_treat_a_lymphedema_wound
For information about
Lymphedema Treatment
http://www.lymphedemapeople.com/wiki/doku.php?id=treatment
For information about
Exercises for Lymphedema
http://www.lymphedemapeople.com/wiki/doku.php?id=exercises_for_lymphedema
For information on Infections
Associated with Lymphedema
http://www.lymphedemapeople.com/wiki/doku.php?id=infections_associated_with_lymphedema
For information on Lymphedema
in Children
http://www.lymphedemapeople.com/wiki/doku.php?id=lymphedema_in_children
Lymphedema Glossary
http://www.lymphedemapeople.com/wiki/doku.php?id=glossary:listing
===========================
Lymphedema People - Support
Groups
-----------------------------------------------
Children
with Lymphedema
The time has come for families, parents, caregivers to have a support
group of
their own. Support group for parents, families and caregivers of
chilren with
lymphedema. Sharing information on coping, diagnosis, treatment and
prognosis.
Sponsored by Lymphedema People.
http://health.groups.yahoo.com/group/childrenwithlymphedema/
Subscribe: childrenwithlymphedema-subscribe@yahoogroups.com
......................
Lipedema
Lipodema Lipoedema
No matter how you spell it, this is another very little understood and
totally
frustrating conditions out there. This will be a support group for
those
suffering with lipedema/lipodema. A place for information, sharing
experiences,
exploring treatment options and coping.
Come join, be a part of the family!
http://health.groups.yahoo.com/group/lipedema_lipodema_lipoedema/?yguid=209645515
Subscribe: lipedema_lipodema_lipoedema-subscribe@yahoogroups.com
......................
MEN
WITH LYMPHEDEMA
If you are a man with
lymphedema; a man with a loved one with lymphedema who you are trying
to help
and understand come join us and discover what it is to be the master
instead of
the sufferer of lymphedema.
http://health.groups.yahoo.com/group/menwithlymphedema/
Subscribe: menwithlymphedema-subscribe@yahoogroups.com
......................
All
About Lymphangiectasia
Support group for parents, patients, children who suffer from all forms
of
lymphangiectasia. This condition is caused by dilation of the
lymphatics. It can
affect the intestinal tract, lungs and other critical body areas.
http://health.groups.yahoo.com/group/allaboutlymphangiectasia/
Subscribe: allaboutlymphangiectasia-subscribe@yahoogroups.com
......................
Lymphatic
Disorders Support Group @ Yahoo Groups
While we have a number of support groups for lymphedema... there is
nothing out
there for other lymphatic disorders. Because we have one of the most
comprehensive information sites on all lymphatic disorders, I thought
perhaps,
it is time that one be offered.
DISCRIPTION
Information and support for rare and unusual disorders affecting the
lymph
system. Includes lymphangiomas, lymphatic malformations,
telangiectasia,
hennekam's syndrome, distichiasis, Figueroa
syndrome, ptosis syndrome, plus many more. Extensive database of
information
available through sister site Lymphedema People.
http://health.groups.yahoo.com/group/lymphaticdisorders/
Subscribe: lymphaticdisorders-subscribe@yahoogroups.com
===========================
Lymphedema
People New Wiki Pages
Have
you seen our new
“Wiki” pages yet? Listed
below
are just a sample of the more than 140 pages now listed in our Wiki
section. We
are also working on hundred more.
Come
and take a stroll!
Lymphedema
Glossary
http://www.lymphedemapeople.com/wiki/doku.php?id=glossary:listing
Lymphedema
http://www.lymphedemapeople.com/wiki/doku.php?id=lymphedema
Arm
Lymphedema
http://www.lymphedemapeople.com/wiki/doku.php?id=arm_lymphedema
Leg
Lymphedema
http://www.lymphedemapeople.com/wiki/doku.php?id=leg_lymphedema
Acute
Lymphedema
http://www.lymphedemapeople.com/wiki/doku.php?id=acute_lymphedema
The
Lymphedema Diet
http://www.lymphedemapeople.com/wiki/doku.php?id=the_lymphedema_diet
Exercises
for Lymphedema
http://www.lymphedemapeople.com/wiki/doku.php?id=exercises_for_lymphedema
Diuretics
are not for
Lymphedema
http://www.lymphedemapeople.com/wiki/doku.php?id=diuretics_are_not_for_lymphedema
Lymphedema
People Online
Support Groups
http://www.lymphedemapeople.com/wiki/doku.php?id=lymphedema_people_online_support_groups
Lipedema
http://www.lymphedemapeople.com/wiki/doku.php?id=lipedema
Treatment
http://www.lymphedemapeople.com/wiki/doku.php?id=treatment
Lymphedema
and Pain
Management
http://www.lymphedemapeople.com/wiki/doku.php?id=lymphedema_and_pain_management
Manual
Lymphatic Drainage (MLD) and Complex Decongestive Therapy (CDT)
http://www.lymphedemapeople.com/wiki/doku.php?id=manual_lymphatic_drainage_mld_complex_decongestive_therapy_cdt
Infections
Associated with
Lymphedema
http://www.lymphedemapeople.com/wiki/doku.php?id=infections_associated_with_lymphedema
How
to Treat a Lymphedema
Wound
http://www.lymphedemapeople.com/wiki/doku.php?id=how_to_treat_a_lymphedema_wound
Fungal
Infections Associated
with Lymphedema
http://www.lymphedemapeople.com/wiki/doku.php?id=fungal_infections_associated_with_lymphedema
Lymphedema
in Children
http://www.lymphedemapeople.com/wiki/doku.php?id=lymphedema_in_children
Lymphoscintigraphy
http://www.lymphedemapeople.com/wiki/doku.php?id=lymphoscintigraphy
Magnetic
Resonance Imaging
http://www.lymphedemapeople.com/wiki/doku.php?id=magnetic_resonance_imaging
Extraperitoneal
para-aortic lymph node dissection (EPLND)
http://www.lymphedemapeople.com/wiki/doku.php?id=extraperitoneal_para-aortic_lymph_node_dissection_eplnd
Axillary
node biopsy
http://www.lymphedemapeople.com/wiki/doku.php?id=axillary_node_biopsy
Sentinel
Node Biopsy
http://www.lymphedemapeople.com/wiki/doku.php?id=sentinel_node_biopsy
Small
Needle Biopsy - Fine Needle Aspiration
http://www.lymphedemapeople.com/wiki/doku.php?id=small_needle_biopsy
Magnetic
Resonance Imaging
http://www.lymphedemapeople.com/wiki/doku.php?id=magnetic_resonance_imaging
Lymphedema
Gene FOXC2
http://www.lymphedemapeople.com/wiki/doku.php?id=lymphedema_gene_foxc2
Lymphedema Gene VEGFC
http://www.lymphedemapeople.com/wiki/doku.php?id=lymphedema_gene_vegfc
Lymphedema Gene SOX18
http://www.lymphedemapeople.com/wiki/doku.php?id=lymphedema_gene_sox18
Lymphedema
and
Pregnancy
http://www.lymphedemapeople.com/wiki/doku.php?id=lymphedema_and_pregnancy
Home page:
Lymphedema People
http://www.lymphedemapeople.com
Page Updated: Jan, 15, 2012
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ABSTRACT
INTRODUCTION