Facts About Lymphedema
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Postmastectomy Lymphedema
Long-term Results Following Microsurgical Lymph Node
Transplantation
Corinne Becker, MD, Jalal Assouad, MD, Marc Riquet, MD, PhD, and Genevie`ve Hidden, MD
Background and Objectives: Lymphedema complicating breast
cancer treatment remains a challenging problem. The purpose of this
study was to analyze the long-term results following microsurgical
lymph node (LN) transplantation.
Methods: Twenty-four female patients with lymphedema for more
than 5 years underwent LN transplantation. They were treated by
physiotherapy and resistant to it. LNs were harvested in the femoral
region, transferred to the axillary region, and transplanted by microsurgical
procedures. Long-term results were evaluated according
to skin elasticity, decrease, or disappearance of lymphedema assessed
by measurements, isotopic lymphangiography, and ability to
stop physiotherapy.
Results: The postoperative period was uneventful; skin infectious
diseases disappeared in all patients. Upper limb perimeter returned
to normal in 10 cases, decreased in 12 cases, and remained unchanged
in 2 cases. Five of 16 (31%) isotopic lymphoscintigraphies
demonstrated activity of the transplanted nodes. Physiotherapy was
discontinued in 15 patients (62.5%). Ten patients were considered as
cured, important improvement was noted in 12 patients, and only 2
patients were not improved.
Conclusion: LN transplantation is a safe procedure permitting good
long-term results, disappearance, or a noteworthy improvement, in
postmastectomy lymphedema, especially in the early stages of the
disease.
(Ann Surg 2006;243: 313–315)
Lymphedema complicating breast cancer treatment remains
a challenging problem. Combined physiotherapy is not
performed equally in all centers, and many physicians remain
skeptical on the overall efficacy of surgical treatments.1
Furthermore, whatever the treatment proposed, the possibility
of cure remains questionable. Over the last 12 years, our team
has treated limb lymphedema by transplanting lymph nodes.2
The purpose of this study was to analyze the results obtained
with this procedure during a minimal 5-year follow-up.
PATIENTS AND METHODS
We retrospectively reviewed data of 24 female patients
suffering from lymphedema following breast cancer treatment
who underwent lymph node transplantation by one of us (C.B.)
in Cavell Institution in Brussels from 1991 to 1997. Mean age
was 58.7 years (range, 37–80 years) with a mean follow-up of
8.3 years (range, 5–11 years). Upper limb lymphedema was
right sided in 14 patients and left sided in 10 patients. All the
patients were previously seen by their oncologist and considered
in breast cancer remission. Breast carcinoma treatment
performed was mastectomy (n 3), mastectomy and radiation
therapy (n 11), and mastectomy, radiation therapy, and
chemotherapy (n 10). Axillary lymphadenectomy had been
performed in all cases. In 18 patients, upper limb lymphedema
was present for at least 1 year or greater (mean, 5.6
years; range, 1–15 years). In 6 patients, it was present for
only a few months (mean, 5 months; range, 3–8 months).
Patients complaining of pain and/or presenting with palsy
and/or with elephantiasis were excluded from the study. All
patients were undergoing physiotherapy and were considered
resistant to it.
Lymphedema was assessed by measurements, infectious
episodes, and isotopic lymphangiography.
Measurements were weekly during the preoperative
month and were performed before and after physiotherapy.
Sites measured were at the wrist, 10 cm above the wrist,
at the elbow, and 10 cm above the elbow. Results were then
compared with the contralateral limb measurements.
The number of previous infectious episodes (erysipela,
lymphangitis . . .) and the aspect of the teguments at presentation
(elasticity of the skin and infectious disease) were
recorded. In case of infectious disease, antibiotic therapy and
local treatment was performed.
Isotopic lymphangiography was performed in 20 patients.
In 15 patients, lymphoscintigraphy demonstrated absence of
both lymph nodes and drainage; and in 3 patients, drainage was
impaired without clearly demonstrating the absence of nodes. In
2 patients, lymphoscintigraphy was normal.
Patients were divided into 2 stages: stage I, early edema
with no or less than 2 infectious episodes, skin elasticity
preserved, and perimeter not exceeding 30% more than the
From Service de Chirurgie Thoracique, Hoˆpital Europe´en Georges Pompidou,
Paris, France.
Reprints: Marc Riquet, MD, PhD, Service de Chirurgie Thoracique, Hoˆpital
Europe´en Georges Pompidou, 20-40 rue Leblanc, 75015 Paris Cedex,
France. E-mail: marc.riquet@hop.egp.ap.ap-hop-paris.fr.
Copyright © 2006 by Lippincott Williams & Wilkins
ISSN: 0003-4932/06/24303-0313
DOI: 10.1097/01.sla.0000201258.10304.16
Annals of Surgery • Volume 243, Number 3, March 2006 313
contralateral arm (n 6); stage II, older edema, most often of
more than 1 year duration, more than 2 infectious episodes,
impaired skin elasticity, and perimeter measured between 30
and 50% more than the contralateral arm (n 18).
Surgical approach of the axillary region of the lymphedematous
limb was performed in search of receiving vessels:
fibrotic muscular and burned tissue were dissected and adhesions
released. Axillary vessels were dissected and the
periscapular pedicle was isolated. The circumflex posterior
branches were individualized and prepared for microanastomoses.
An incision was then performed in the inguinal region.
The dissection began by visualizing the superficialis circumflex
iliac vein. At that level are located lymph nodes irrigated
by the circumflex iliac vessels and without direct connection
with the lymphatic drainage of the inferior limb. These nodes
were dissected, freed, and elevated external to internal at the
level of the muscular aponeurosis. The nodes were then
harvested with an abundant amount of surrounding fat tissue.
Lymph nodes were then transplanted in the axillary
receiving site. Artery and vein were anastomosed with the
vessels previously prepared, using microsurgical techniques.
Both axillary and inguinal approaches were closed on suction
drainage.
In 7 cases, because of an incomplete result at the level
of the forearm, a second procedure was performed. Lymph
nodes were harvested in the same manner at the contralateral
inguinal site and were transplanted at the level of the elbow.
Following surgery, manual drainage (physiotherapy)
was performed on the first postoperative day and daily during
the first 3 months. Manual drainage was then performed twice
a week during the following 3 months and discontinued. No
elastic compression dressing was applied following surgery
to avoid compression on the transplanted lymph nodes and on
the microsurgical anastomosis. Antisludge treatment mainly
acetylsalicylates were administrated during the postoperative
period.
Long-term results were evaluated according to skin
elasticity and existence of infectious disease, decrease or
disappearance of the lymphedema assessed by measurements,
effects observed on isotopic lymphangiography, and ability to
stop or to discontinue physiotherapy after 6 months. Longterm
results were also evaluated according to the duration of
the lymphedema before surgery and occurrence of downstaging
after surgery.
RESULTS
The postoperative period was uneventful except for the
appearance of lymphorrhea in 8 patients, which resolved over
a few days. Infectious disease disappeared totally in 17
patients; and in the remaining 7 patients, only one episode of
skin infectious disease was recorded.
Upper limb perimeter returned to normal in 10 cases,
remained unchanged in 2 cases, and decreased more than
50% of its value in 6 patients and less than 50% of its value
in 6 other patients.
Control isotopic lymphangiography was performed in 16
patients. In 11 patients, lymph nodes and lymph drainage were
initially absent: in 4 patients, the transplanted lymph nodes were
visualized and new lymph drainage pathways appeared. In 3
patients, lymph drainage was impaired without clearly demonstrating
lymph nodes: in 1 of these patients, lymph node
was visualized. In 2 patients with normal isotopic lymphangiography,
results were unchanged. So, 5 of 16 (31%)
lymphoscintigraphies demonstrated the effectiveness of
lymph node transplantation.
Physiotherapy was discontinued after 6 months in 14
patients and after 12 months in 1 patient. In the 9 other
patients, physiotherapy remained necessary and was performed
once weekly in 7 patients. Physiotherapy was thus
discontinued in 15 patients (62.5%).
Ten patients were considered cured (good results)
(stage I, n 4; stage II, n 6). Two patients were not at all
improved, lymphedema remaining unchanged (stage I, n 1;
stage II, n 1). Downstaging (from stage II to stage I) was
observed in 12 patients.
Duration of the lymphedema before surgery was: a few
months (n 5) and 1 to 4 years, mean 2.4 years (n 5) in
case of good results, 3 and 4 years in case of bad results (n
2), 8 months and 1 to 15 years, mean 7.4 years (n 11) in
case of downstaging. In 1 patient with downstaging, the result
was considered as good (normalized) following elective liposuction.
During long-term follow-up, no breast cancer recurrence
was observed.
DISCUSSION
Autologous lymph node transplantation permits lymphedema
improvement with long-term downstaging commonly
obtained (except 2 patients), and physiotherapy discontinued
in 62.3% of patients. Lymphedema was considered cured in
42% of patients and fixating lymph nodes were detected in
31% of patients controlled by lymphoscintigraphy. Good
results were obtained more regularly when the duration of
lymphedema was the shortest before lymph nodes transplantation.
Effectiveness of the procedure was always durably
demonstrated with respect to skin infectious diseases.
Autologous lymph node transplantation for lymphedema
treatment is a recent microsurgical technique,3 the results
of which have yet to be fully evaluated.4 Results of the
transplantation of lymph nodes in the rat5,6 and in the dog7
prove very attractive. In humans, the major concern is to find
a fatty flap containing lymph nodes with their own vascularization,
the procurement of which should be performed without
injury. Our technique uses inguinal lymph node free flap2
made of the more superior external superficial lymph nodes:
an anatomic study based on the dissection of 50 inguinal
regions of fresh cadavers demonstrated that they mainly
received lymph from the abdominal wall and that their
procurement did not impair lymph drainage of the lower
limb.6 This procurement site is the only one used in this
report; however, lymph node transplantation may be used to
treat limb lymphedema with other procurement sites such as
cervical2 or axillary8 being possible.
No current gold standard for evaluation of lymphedema
exists;9 hence, evaluating results of treatments remains difficult
Becker et al Annals of Surgery • Volume 243, Number 3, March 2006
314 © 2006 Lippincott Williams & Wilkins
and appears controversial. Fluid displacement data, which would
have been a more objective methodology, was not available
because it was not routinely performed. Despite this, and
although circumferential data appear subjective and difficult
to interpret, results on lymphedema measurements were satisfactory
in this series, and many patients were able to
discontinue physiotherapy treatments.
Trevidic and Pecking9 have underlined the role lymphoscintigraphy
may have to objectively assess results obtained
and to select patients for surgery. However, in our
series, results obtained on reappearance of lymph drainage
are difficult to interpret meaningfully, and colloidal uptake by
transplanted lymph nodes was detected in only 31% of
patients. Appearance of lymphatic pathways toward the graft
site, which was sometimes also present, could suggest a
“lymphangiogenetic” effect of these grafts. These results,
also observed in experimental studies,5–7 would be of paramount
interest if confirmed by other series.
Transplanted lymph node colloidal uptake was all the
more frequent than the duration of lymphedema was shorter.
Shesol et al5 also observed, in a study in the rat, that radioactivity
appeared in 4 of 5 transplanted lymph nodes when
transplantation was immediately following lymphedema onset,
whereas it appeared in only 1 of 5 cases when transplantation
was delayed. This could suggest that it would be
perhaps better not to delay the indication for lymph node
transplantation.
Effect on skin infectious diseases was the most obvious.
A role by the transplanted lymph nodes immune effect
may be possible. Experimental studies have demonstrated
that autotransplanted lymph nodes rapidly recovered a normal
architecture.10 No study is available to validate our observations,
but Egawa et al11 reported reduction of lymphedema
after intraarterial injection of autologous lymphocytes probably
due to changes in blood protein components. Lymphoid
tissue present in transplanted lymph nodes may prevent infection
but may also reduce arm swelling by similar mechanism
of changes in protein components: this also may explain
partial benefits obtained when lymphatic pathways are not
restored.
CONCLUSION
Autologous lymph node transplantation appears to have a
favorable and persistent effect on postmastectomy lymphedema.
It is a safe procedure that may be advocated when discussing
surgical treatments, especially in early stages of the disease.
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Annals of Surgery • Volume 243, Number 3, March 2006 Postmastectomy Lymphedema
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