Surgicalinterventionfor Lymphedema: Kristalyn Gallagher,, Kathleen Marulanda,, Stephanie Gray
Surgicalinterventionfor Lymphedema: Kristalyn Gallagher,, Kathleen Marulanda,, Stephanie Gray
Surgicalinterventionfor Lymphedema: Kristalyn Gallagher,, Kathleen Marulanda,, Stephanie Gray
Lym p h e d e m a
Kristalyn Gallagher, DO*, Kathleen Marulanda, MD, MS, Stephanie Gray, MD
KEYWORDS
Lymphedema Surgery Lymph node transfer Axillary reverse mapping
LYMPHA Lymphovenous anastomosis Vascularized lymph node transfer
Liposuction
KEY POINTS
Lymphedema is a chronic, progressive disease with no curative treatment.
Surgical treatment options are effective at managing early and late stage lymphedema.
Standardized methods for quantifying lymphedema, universal reporting standards, and an
increased amount of high-quality evidence are necessary to advance understanding and
management of lymphedema.
INTRODUCTION
Nonsurgical management involves meticulous skin care, limb elevation, lifelong external
compression therapy (both static and pneumatic), and physical therapy with manual
lymph drainage and massage to minimize symptoms. Surgical options have been
reserved for failure of conservative management historically, but recent data suggest
early intervention with surgical techniques may reduce incidence of symptom progres-
sion.7–9 Preventative surgical techniques have been described to reduce the initial
disruption of the lymphatics and maintain function. Microsurgical techniques, including
lymphaticovenous anastomosis (LVA), vascularized lymph node transfer (VLNT), and
lymphaticolymphatic bypass aim to restore the underlying physiologic impairment.
Additional surgical interventions such as liposuction and surgical excision remove
affected tissues to effectively decrease the drainage load. The successful selection of
surgical therapy depends on the stage of lymphedema with LVA and VLNT more suitable
for fluid-predominant disease and suction-assisted protein lipectomy (SAPL) for solid
disease. Open debulking and reductive procedures are used for management of late-
stage solid lymphedematous disease.
CLINICAL PRESENTATION
Patients who have undergone breast cancer treatment with surgery, radiation, and/or
chemotherapy have a lifetime risk of lymphedema occurrence17,18 and should be
monitored with a low threshold of suspicion. Most patients become symptomatic
within 8 months of surgery and 75% will present in the first 3 years.17
Surgical Intervention for Lymphedema 197
The two most commonly used staging systems for lymphedema are the Interna-
tional Society of Lymphology and Campisi systems (Table 1). Both systems agree
that lymphedema can be classified as subclinical, mild (early), moderate (intermedi-
ate), or severe (advanced). The symptoms of lymphedema by stage are listed in
Table 2. Early lymphedema typically presents with subjective symptoms, most
commonly heaviness in the affected limb without any appreciable swelling or
edema.10,19–21 These symptoms may be present for months or years before any
detectable physical change occurs. As interstitial fluid accumulates, patients experi-
ence increased extremity circumference followed by pitting edema that usually
worsens at the end of the day (Fig. 1). A 2 cm or greater difference in arm circumfer-
ence or a 200 mL limb volume difference between affected and nonaffected arms is
considered to meet diagnostic criteria for lymphedema, although no universal criteria
exist.22 Early symptoms are initially alleviated with compressive garments, limb eleva-
tion, and physical therapy with manual lymph drainage and massage to minimize
symptoms. As the disease progresses, irreversible, nonpitting edema develops. Pa-
tients report increased firmness, decreased functionality, and disfigurement.20,23 Sig-
nificant swelling and increased limb volume severely impair limb mobility and cause
chronic debilitating pain that impedes activities of daily living. This disease
Table 1
ISL and Campisi staging systems for comparison with proposed treatment
Abbreviations: CDT, complex decongestive therapy; ISL, International Society of Lymphology; LVA,
lymphaticovenous anastomosis; SAPL, suction-assisted protein lipectomy; VLNT, vascularized lymph
node transfer.
Data from Refs.19,24,27
198 Gallagher et al
Table 2
Symptoms of lymphedema by stage
Stage Symptoms
Subclinical 0 Heaviness
Tightness
Firmness
Pain
Aching
Soreness
Numbness
Limb fatigue
Limb weakness
Impaired limb mobility
Absence of swelling
Early (mild) I Above symptoms
Presence of swelling that decreases with compression or
elevation
Moderate (Intermediate) II Above symptoms
Disfigurement
Early skin changes
With or without cellulitis or infections
Presence of swelling that does not decrease with compres-
sion or elevation
Severe (Advanced) III Above symptoms
Disability
Recurrent cellulitis or infections
Late skin changes (hyperkeratosis, hyperpigmentation,
papillomas, induration)
CLINICAL MONITORING
DIAGNOSTIC IMAGING
Lymphography was historically used, but is seldom used currently owing to technical
difficulties with cannulization of the lymphatic vessels and morbidity associated with
200 Gallagher et al
Surgical techniques such as sentinel lymph node biopsy (SLNB), axillary reverse
mapping (ARM), and Lymphovascular anastamosis (“LYMPHA”) have been developed
to prevent or minimize the disruption of lymphatic flow from the upper extremity during
breast cancer surgery.44–46
Sentinel Lymph Node Biopsy
SLNB is a technique by which the tumor’s most proximal draining lymph node(s) are
identified with radioactive dye and/or isosulfan blue and excised. Reported rates of
lymphedema range from 1% to 7% after SLNB.45 Recent data from ACOSOG (Amer-
ican College of Surgeons Oncology Group) Z0011, ACOSOG Z1071, SENTINA
(Sentinel-Lymph-Node Biopsy in Patients With Breast Cancer Before and After
Surgical Intervention for Lymphedema 201
Fig. 2. Injection site for axillary reverse mapping procedure: 3 to 5 mL of isosulfan blue is
injected subcutaneously in the volar surface of the upper extremity.
202 Gallagher et al
Fig. 3. Blue arm lymphatics identified during axillary dissection and preserved.
should be removed along with the remaining axillary nodes. The oncologic resection
should not be compromised to minimize the risk of lymphedema (Fig. 4).
Lymphovascular Anastomosis Technique
The lymphovascular anastomosis (“LYMPHA”) technique performed at the time of
initial axillary dissection has shown a statistically significant reduction in the develop-
ment of lymphedema at 18 months (30% vs 4.05%; P<.01).45 This technique was orig-
inally described by Boccardo in 2009. Isosulfan blue is injected into the volar aspect of
the ipsilateral upper arm before incision (see Fig. 2). During axillary dissection, the blue
lymphatics are identified and the afferent lymphatics are clipped near insertion into the
node. After dissection, the afferent lymphatics are directly anastomosed into a collat-
eral branch of the axillary vein with microsurgical technique.45
SURGICAL TECHNIQUES
Surgical treatment options are divided into two general categories, reductive versus
physiologic procedures. In this section, we focus on the physiologic procedures,
which aim to assuage the physiologic disturbances that result from increased adipose
volume and fibrosis in the affected limb. Microsurgical procedures, including LVA and
VLNT, target the fluid component that predominates at earlier stages of the disease
(Fig. 4).
Lymphaticovenous Anastomosis
LVA, first described in 1969, is a microsurgical procedure that effectively bypasses
diseased lymphatics and restores adequate lymphatic drainage via direct drainage
into the venous system.19,62 Serial anastomoses are typically created between small
lymphatics and subdermal venules, preferably less than 1 cm in diameter, along the
entirety of the upper extremity. The minimally invasive approach allows multiple anas-
tomoses to be created via a single 1- to 2-cm incision. The procedure is typically per-
formed under locoregional anesthetic, which may be better suited for candidates with
extensive comorbidities.
Indications
LVA is indicated after failed management of conservative therapy, and early Interna-
tional Society of Lymphology stage II disease with evidence of partial lymphatic
obstruction.27 Functional lymphatic vessels, albeit partially functional, are required
Surgical Intervention for Lymphedema 203
Fig. 4. Algorithm for managing lymphedema. CDT, complex decongestive therapy; LVA, lym-
phaticovenous anastomosis; LLB, lymphaticolymphatic bypass; SAPL, suction-assisted protein
lipectomy; VLNT, vascularized lymph node transfer.
Lymphoscintigraphy
Superior results have been reported when perioperative lymphatic mapping is used65
to identify lymphatic vessels and determine functionality. ICG lymphoscintigraphy is a
simple tool, frequently used to locate functional lymphatics, determine severity of dis-
ease, and identify optimal placement for surgical incisions.41,66–69 Intraoperatively, the
204 Gallagher et al
dye illuminates functional lymphatics as it travels through the surgical field, which has
been shown to increase the number of anastomoses created70 despite an overall
shorter length of operation.
Postoperative anastomotic patency is subsequently monitored with lymphoscintig-
raphy; the rate of radiotracer clearance provides an indirect measure of lymphatic
flow.
Technique
There is no consensus in the literature regarding timing, location, number, or configura-
tion of anastomoses when performing a LVA; these decisions are primarily dictated by
surgeon preference. However, the likelihood of successful outcomes is determined pri-
marily on the surgeon’s ability to identify suitable venules and lymphatic vessels within
the affected limb. Ideally, both vessels should be of similar diameter, preferably less
than 0.8 mm, in close proximity to one another, and with minimal to no venous backflow
after division.24,71 Smaller veins are preferred because of the greater risk of increased
intraluminal pressure, and subsequent risk of venous reflux associated with larger veins.
The number and location of anastomoses varies and is highly dependent on the pres-
ence of functional and accessible vessels; both proximal and distal placements have
been widely reported. Stepped anastomosis creates multiple bypasses at various
levels of the affected extremity (ie, wrist, forearm, and arm in the upper extremity),72
which aims to improve success rates by providing additional routes for lymphatic
drainage. Previously, Huang and colleagues73 demonstrated that increased number
of anastomoses provided better results. However, that has been refuted in a large study
by O’Brien and colleagues, as well as a large prospective trial63 which showed no dif-
ference in results based on number of anastomoses.64,70 A variety of configurations
may similarly be used including end-to-end, end-to-side, or side-to-end anastomoses
without significant difference in outcomes. If anatomy permits, it is always preferred to
create multiple lymphaticovenous anastomoses via a single incision.
Results
LVA has been proven to be an efficacious treatment option for patients that have failed
nonoperative management. It is associated with a decrease in the overall incidence of
severe cellulitis, compression garment discontinuation, and a subjective improvement
in symptoms and QoL, compared with women who received conservative manage-
ment alone.19,74,75 In a systematic review of high-quality studies, 5 studies reported
QoL outcomes, and found 91.7% symptom improvement, 94.5% average satisfaction
rate, 90% improved QoL, and 50% subjective improvement in patients who under-
went LVA.42,63,76–78
However, studies have shown that the success of LVA is primarily restricted to early
stage disease; this is presumably owing to the ongoing presence of functional lym-
phatics that are subsequently irreversibly damaged in advanced disease. Chang
and colleagues63 found that, after LVA, stage I and II patients experienced a 61% volu-
metric reduction compared with 17% volumetric reduction in stage III patients after
1 year of follow-up. In another study, no limb volume reduction was seen in stage III
patients.72 Rates of recurrence are also closely associated with clinical staging. Pou-
mellec and colleagues72 reported 19.3% recurrence rates; however, all recurrences
were isolated to patients with stages III and IV lymphedema. This finding further sup-
ports the notion that LVA is better suited for patients with early stage lymphedema.
Complications
Complications are uncommon after lymphaticovenous bypass, with rates reported at
5.9%.27 Although the incidence is rare, known complications are infection, lymphatic
Surgical Intervention for Lymphedema 205
fistula, partial skin ulceration, and wound dehiscence.24,43,77 Given the low incidence
of complications, LVA seems to be a safe and feasible procedure.
Indications
Indications for VLNT include stages II to V lymphedema (Capisi staging system), ab-
solute occlusion of lymphatic pathways verified on imaging (MRI or lymphoscintigra-
phy), fibrosis preventing lymphaticovenous bypass, brachial plexus neuropathy,
chronic infections in the affected limb (ie, repeated episodes of cellulitis), and failed
conservative management.80–82 Conversely, some studies support the use of VLNT
in early-stage lymphedema owing to the progressive course of the disease. Although
lymph node transfer is not curative, early intervention may reduce the accumulation of
excess lymphatic fluid and thereby, inhibit the positive feedback cycle that drives the
progression of lymphedema.71,79,83
Technique
The recipient site may be selected as the axilla, elbow, or wrist of the affected limb.
Axillary dissection may prove to be more challenging in patients who have undergone
prior radiation therapy owing to significant scar tissue formation. However, wrist
placement is less cosmetically pleasing owing to protrusion of the tissue and the
possible need for skin grafting. Cheng and colleagues82 suggests that wrist placement
is more suitable for functionality, but the elbow provides improved aesthetic results.
Ultimately, selection depends on surgeon preference, because recipient site selection
has not been shown to impact outcomes. The most crucial part of axillary dissection is
to ensure wide removal of all scar tissue; it is necessary to remove the obstruction to
allow for good flow through the underlying lymphatics and to have sufficient space for
placement of harvested lymph nodes.84,85 An external neurolysis should also be per-
formed if a neuroma is identified during dissection to avoid development of postoper-
ative pain.80,83 After careful identification of the thoracodorsal vessels, attention can
be turned to the lymph node flap.
Lymphodynamic evaluation is conducted preoperatively with the aid of multiple im-
aging modalities. ICG assesses the severity of dermal backflow, and locates any viable
and functional lymphatic vessels in the region. If an adequate amount of adequately
functioning vessels is identified preoperatively, then a lymphovenous shunt may be
considered, and the more invasive VLNT procedure can be avoided. Additionally, the
presence of lymphatic drainage obstruction can be confirmed on Tc99 lymphoscintig-
raphy. Lymphoscintigraphy does not provide good information about the spatial and
temporal resolution of the lymphatic system and involves exposure to radiation. If avail-
able, MRI and dynamic magnetic lymphangiography are preferred owing to the
increased sensitivity and specificity to identify anatomic and functional variations.
The optimal donor site remains unclear, but the most common location is the
inguinal region; it is based off the branches of the superficial circumflex iliac or
206 Gallagher et al
superficial inferior epigastric vessels. Groin flaps are chosen owing to their abundance
of lymph nodes in a well-understood anatomic region, an easily hidden scar, and a
dual role in total breast reconstruction.24 Dissection is delineated by 3 borders: the
inguinal ligament (caudal), the muscular aponeurosis (deep), and the cribriform fascia
(superficial). It is recommended that the surgeon not dissect lymph nodes beyond the
caudal and deep borders to avoid inadvertent removal of deeper lymph nodes to mini-
mize the risk of donor site lymphedema.86 Less commonly, the submental, supracla-
vicular, thoracic, and omental tissues are used as donor sites. The submental and
supraclavicular nodes require tedious dissection owing to nearby lymphatic ducts
and branches of the marginal mandibular nerve. Although the omental nodes are
the least likely to develop donor site iatrogenic lymphedema, the need for abdominal
surgery poses additional risks.
Anastomosis selection varies depending on the flap of choice; the superficial
circumflex iliac vessels are typically used in isolated VLNT, versus combined VLNT
with microvascular breast reconstruction, in which the deep inferior epigastric vessels
are preferred. Currently, no strict guidelines exist to determine which vessels should
be used for optimal results. A recent study by Nguyen and colleagues87 created an al-
gorithm for transferring vascularized inguinal lymph nodes during autologous abdom-
inal free flaps (AFP), specifically deep inferior epigastric perforator or transverse rectus
abdominis myocutaneous flaps; the goal was to provide an alternative vasculature se-
lection to the commonly used thoracodorsal vessels, which may be crucial later if the
initial flap fails. Nguyen and colleagues address 3 different scenarios: (1) hemiabdomi-
nal flap for bilateral mastectomy or prior midline incision—ipsilateral VLNT, ipsilateral
AFP, thoracodorsal pedicle; (2) unilateral reconstruction without prior violation of the
midline—contralateral VLNT, ipsilateral AFP, internal mammary artery pedicle; and
(3) a history of prior surgery with subsequent division of superficial vessels—VLNT
ipsilateral, AFP contralateral, and internal mammary artery pedicle. Their study
demonstrated promising results with 79% of patients reporting improved symptoms,
and reduction of excess limb volume from 21% preoperatively down to 10% at 1 year
of follow-up.
Results
VLNT has been shown to have successful outcomes with decreases in limb circumfer-
ence and limb volume, as well as improvement in patient function and QoL. A large sys-
tematic review by Carl and colleagues27 found a 33% excess volume reduction and
16.1% absolute circumference reduction after lymph node transfer. Notably, patients
report a substantial improvement in limb functionality before any self-perceived
changes in limb appearance, suggesting that even a slight decrease in size may prove
beneficial with regard to limb mobility, and inevitably, better QoL. These functional im-
provements were reported as early as 1 month postoperatively, and continued
throughout the first year of follow-up. Similarly, psychosocial issues including appear-
ance, symptoms and mood also improved.88–91 Studies have shown that patients who
undergo lymph node transfer report 91.7% symptom improvement, 94.5% average
satisfaction rate, 90% improved QoL, and 50% subjective improvement.42,63,76–78
Despite the promising results, particularly in late-stage disease, VLNT is not a curative
therapy. Patients are recommended to continue conservative therapies, including
compressive bandages, elastic garments, and manual lymph drainage postoperatively.
Complications
The success rates for volume reduction, compression therapy discontinuation, and
improved QoL are similar to those reported for LVA; however, the complication rates
Surgical Intervention for Lymphedema 207
of donor site seroma, lymphocele, infection, delayed wound closure, and donor site
lymphedema make VNLT a higher risk surgery.62 VLNT is also associated with longer
durations of hospital stay, longer duration of operation, and greater anesthetic require-
ments (general vs local) when compared with LVA.92 A large, retrospective review of all
high-quality studies demonstrated a 30.1% complication rate after lymph node trans-
fer.27 This finding is further supported by Vignes and colleagues,90 who found an
equally high complication rate at 38%. Similar findings are reported after combined
VLNT and microvascular breast reconstruction with 25% recipient site complications
(delayed wound healing, partial mastectomy flap necrosis, and abdominal flap venous
thrombosis) and 20% donor site complications (abdominal wound healing or dehis-
cence, abdominal hernia, and groin seroma).87 The most dreaded complication after
lymph node transfer is iatrogenic lymphedema at the donor site. Despite low rates re-
ported in the literature, it remains a significant concern among clinicians.85,90,93–95
Studies have shown that, even with modified conservative surgical techniques, lym-
phoscintigraphy findings demonstrate subclinical disruptions in lymphatic flow post-
operatively.96 Given these findings, studies recommend supportive modalities
including reverse mapping, ICG, and lymphoscintigraphy to maximally mitigate the
risk of iatrogenic lymphedema. It should be noted, however, that complications are re-
ported inconsistently across the literature, even among high-quality studies.
COMBINATION PROCEDURES
The combination of physiologic procedures with reductive surgery, which allows for
removal of the chronic adipose and fibrotic tissue disrupting the lymphatic system, is
the most effective treatment for severe lymphedema. Multiple combinations of excisional
and physiologic procedures have been used, including VLNT with suction-assisted lipec-
tomy, VLNT with microvascular breast reconstruction, and some surgeons have also
attempted LVA with VLNT.87,92,94,97–100 Limb volume reduction was reported to be as
high as 91% after liposuction with VLNT.97 Owing to its low risk profile, liposuction is
an appealing adjunct treatment option, particularly in patients with nonpitting edema.
Studies have shown that, after LVA, 16.0% of patients benefit from additional liposuction
postoperatively. Likewise, when VLNT is used as the primary approach, additional reduc-
tive procedures are needed in 31.6% of patients.27 The promising outcomes after com-
bination therapy may represent an opportunity to minimize the need for serial invasive
surgical interventions and simultaneously yield better outcomes. Nevertheless, similar
to lymph node transfer, high rates of complications are associated with excisional pro-
cedures, as high as 39.3%,27 and therefore, careful patient selection is required with
the procedure reserved for those with severe disease.
LIPECTOMY
SAPL involves the removal of fat and fibrosis with suction technique.23–26,62,101 Lipec-
tomy addresses the solid component (fibrosis and hypertrophied subcutaneous adi-
pose tissue) that typically presents later as chronic, nonpitting lymphedema of an
extremity after the fluid component has been conservatively drained.19,75 Patients
often complain of discomfort and dysfunction in the affected arm despite conservative
management.102 Indications for lipectomy include stage II and III disease that has
failed conservative management. Contraindications include active cancer, infection,
wounds, or insufficient conservative management.103 If there is more than 4 to
5 mm of pitting edema in the affected extremity, the patient should attempt conserva-
tive measures rather than undergo liposuction, because liposuction is a method to
remove fibrotic adipose tissue, not fluid.102
208 Gallagher et al
SURGICAL EXCISION
Surgical excision or radical debulking for severe lymphedema was first described in
1912 as the Charles procedure. Several modifications of the Charles procedure
have also been reported. Indications for this procedure include advanced (end-stage)
fibrosclerotic lymphedema not amenable to other procedures, recurrent episodes of
cellulitis, and severe disfigurement or dysfunction, and an inability to exclude sarcoma
on the affected extremity.23–26,62,106–109 The major disadvantage is that superficial skin
lymphatic collaterals are removed or further obliterated.20,24,25 Additionally, there is
significant morbidity, scarring, and risk of skin graft failure with these operations.
When lymphedema recurs at the hand or foot, regrafting and finger or toe amputations
may prove necessary.
During the Charles procedure, longitudinal skin incisions are made along the length
of lymphedema. The excess skin and subcutaneous tissue of the lymphedematous
limb are excised circumferentially down to the level of the deep fascia.20,25,62 Care
is taken not to injure the deep fascia. Split thickness skin grafts are then harvested
from the excised skin and are implanted onto the deep fascial layer. Sterile dressings
are applied and the skin flaps are monitored postoperatively for adequate blood sup-
ply and infection.
Given the risks and morbidities listed, several versions of the modified Charles pro-
cedure were developed for severe lymphedema treatment. In the first modified
Charles procedure, the initial debulking procedure is performed. A portion of the split
thickness skin graft is deepithelialized and is buried into the deep subcutaneous tis-
sues. The goal of this modification is to connect the deep subfascial lymphatics
Surgical Intervention for Lymphedema 209
with the superficial dermal lymphatics, thereby facilitating lymph drainage.110 Other
modifications include use of negative pressure dressings, perpendicular cross-
incisions, and combination procedures with liposuction and VLNT to decrease the
amount of skin removed and allow primary closure.100,107–109,111
SUMMARY
Breast cancer–related lymphedema is a lifelong disease that is difficult to treat and re-
quires multimodal therapy. A systematic review by Carl and colleagues27 using
MINORS criteria to distinguish high-quality studies attempted to create an algorithm
for management of lymphedema. The microsurgical technique LVA at the time of axil-
lary lymph node dissection has been proposed as a primary preventative treatment for
arm lymphedema. The after treatments are suggested according to the International
Society of Lymphedema Staging System. Conservative measures such as physio-
therapy and compression garments are appropriate for stage 0 (subclinical) lymphe-
dema. LVA or VLNT procedures are best suited for early stage I lymphedema (soft,
pitting edema with little to no fibrosis). Suction-assisted protein liposuction should
be considered for moderate stage II (nonpitting edema with fibrosis) and severe stage
III lymphedema (nonpitting edema with severe fibrosis and hypertrophic skin
changes). Surgical excision (the Charles procedure and its modifications) should be
reserved for severe stage III lymphedema with severe disfigurement or disuse.23,24
Most patients do report decreased edema and improved QoL after surgical interven-
tion; however, compression garments or physiotherapy are still recommended post-
operatively to maintain or further reduce limb volume.
Further research must be conducted in establishing best practices in lymphedema
prevention and treatment. A standardized staging system for lymphedema would
allow for accurate comparison of outcomes based on intervention type. There are
also inconsistent methods of recording surgical outcomes and reporting outcomes
and QoL indicators. At this time, there are limited large, randomized, controlled trials
in the lymphedema literature that focus specifically on breast cancer related lymphe-
dema. Much of the data come from observational studies that combine data from both
upper extremity and lower extremity lymphedema. Lack of consistent quantitative
reporting prevents comprehensive conclusions regarding which surgical approaches
are associated with the greatest subjective improvements. Even the studies that did
include QoL outcomes and reported overall improvement in function, symptom
severity, and aesthetics after surgery, these data cannot be reliably used because
they are inconsistently documented among the studies.
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