Keywords immediate lymphatic reconstruction - anatomy - imaging - lymphatic drainage
The lymphatic microsurgical preventative healing approach (LYMPHA) or immediate lymphatic
reconstruction (ILR) is performed at time of axillary lymph node dissection (ALND)
and reroutes lymphatic flow from divided arm lymphatics into nearby tributaries of
the axillary vein. Boccardo et al described this technique in 2009 and has reported
a 4% rate of lymphedema (LE) over a 4-year follow-up period compared with a 25 to
40% incidence with historic controls.[1 ]
[2 ] These results have been duplicated at other institutions.[3 ]
[4 ] The original LYMPHA technique identified arm lymphatics by injecting dye into the
medial-upper arm.[1 ] However, visualization of divided lymphatics draining the lateral upper arm or the
Mascagni–Sappey (M–S) pathway was not attempted. We believe better understanding and
mapping of the M–S pathway may have important implications in understanding which
patients are at higher risk of developing lymphedema and potential intraoperative
implications for surgeons performing ILR.
In 1874, Sappey proposed that skin territories were drained by a set of lymphatic
vessels, the “lymphosome relationship.”[5 ]
[6 ]
[7 ] In the modern era, a work by Suami et al utilizes fluorescent dyes to map lymphatic
vessels to their corresponding lymph nodes.[8 ] The upper arm has two lymphosomes, medial and lateral.[9 ]
[10 ] The M–S pathway has historically been used to describe lymphatics draining a territory
of the lateral-upper arm. For purposes of this paper, the M–S pathway will be referred
to as the “lateral pathway.” It has been noted by anatomists to have variable drainage
to the supraclavicular/infraclavicular versus axillary lymph nodes.[8 ] When the pathway avoids the axillary basin, it serves as an “escape route” outside
of the standard operative field and its continued patency would help to prevent LE.[6 ] Despite these cadaveric postulations, no intraoperative attempt to identify this
pathway has been described.
To comprehensively map all the lymphatics of the upper arm during ILR of the axilla,
we chose to inject each lymphosome of the upper arm to ensure that all pathways are
accounted for and, if possible, appropriately reconstructed. To differentiate each
lymphosome, a different dye was injected into each cutaneous region.
This study is a retrospective review of our experience with the goal of better understanding
the anatomy of the M–S pathway.
Methods
A retrospective review of a quality improvement lymphatic surgery database was performed.
Patients undergoing immediate lymphatic reconstruction at time of ALND between November
2017 and June 2018 were identified. Institutional Review Board approval was obtained
for this study. Patient demographics, clinical characteristics, and intraoperative
records were retrieved.
Surgical Technique
Prior to ALND, fluorescein isothiocyanate (FITC) is injected into the skin and deep
tissues of the medial-upper arm as previously described.[11 ] To map the M–S pathway, an ultrasound is performed to identify the cephalic vein
in the upper arm and 1 cc of isosulfan blue is injected into the skin and deep-soft
tissues 4 cm proximal to the elbow crease over the vein. In our experience, we have
found FITC and isosulfan blue to be optimal dyes for visualization in live surgery
and advocate for their usage. Following ALND, a Mitaka MM51 microscope (Mitaka Kohki
Co., Ltd, Japan) equipped with a 560 nm filter was utilized for visualization of the
divided arm lymphatics.
Results
A total of 29 eligible patients with de novo, unilateral breast cancer undergoing
ILR were identified during the study period. The mean patient age (standard deviation
[SD]) was 54.6 years (SD = 13.5 years) with a mean body mass index (BMI) of 26.6 kg/m2 (SD = 4.5 kg/m2 ). All patients underwent levels I and II nodal dissection. Mean number of positive
lymph nodes and total lymph nodes removed was 1.75 and 14, respectively, during nodal
surgery. Also, 55% patients received neoadjuvant chemotherapy. A mean number of 2.5
lymphatics were identified and a mean of 1.2 lymphatics were bypassed ([Supplementary Table S1 ]; available online only). No intraoperative or postoperative complications were noted.
But 100% of patients demonstrated FITC in the axilla. Three of 29 patients (10%) demonstrated
blue dye in the axilla ([Fig. 1 ]). No lymphatic channels demonstrated the concurrent presence of both dyes. There
were no differences with respect to patient demographics, neoadjuvant treatment, and
nodes removed between patients who demonstrated blue dye in the axilla and those who
did not. Twenty-eight of the 29 patients (97%) were successfully underwent immediate
lymphatic reconstruction ([Fig. 2 ]).
Fig. 1 (A ) Following ALND, under white light, blue dye is visualized in lymphatic channels
3 and 4. (B ) Upon activation of the 560 nm filter, FITC was observed in lymphatic channels 1
and 2. Of note, no crossover of dyes was noted within any lymphatic channel. ALND,
axillary lymph node dissection; FITC, fluorescein isothiocyanate.
Fig. 2 In cases where both blue and FITC lymphatic channels are identified, attempts are
made to bypass both lymphosomes. The two arrows illustrate the accessory vein and
a side branch of the accessory vein visualized intraoperatively. FITC, fluorescein
isothiocyanate.
Discussion
Our study found that the Mascagni–Sappey pathway drained to the axillary basin in
10% of patients undergoing immediate lymphatic reconstruction (denoted by “*” in [Fig. 3 ]). Moreover, in the few cases where the lateral pathway was identified in the axilla,
it was distinct from lymphatics draining the medial-upper arm.
Fig. 3 Schematic illustration of the intraoperative anastomoses performed with corresponding
lymphatic channels 1,2,3 and 4.
Our intraoperative finding that the lateral pathway drains into the axilla in a small
subset of the population has significant implications. The lateral pathway has previously
been described as a potential “escape route” for the lymphatic system and may explain
why, even after regional lymph node radiation (RLNR), and ALND, the rate of lymphedema
is approximately 26 to 28% and not 100%.[12 ]
[13 ]
[14 ] This simple anatomic variation where the lateral upper arm lymphosome drains into
the axillary basin may help predict patients who may have a higher risk of LE after
ALND. It may also explain the low but persistent rates of lymphedema following traditional
ILR where only lymphatic channels of the medial-upper arm lymphosome have been previously
bypassed. The fact that our study did not identify any crossover between the lateral-
and medial-upper arm, also emphasizes that bypassing divided lymphatic channels of
the medial upper arm alone is unlikely to provide any relief to the lateral arm. In
the future, lymphatic surgeons may consider ensuring a bypass to each lymphosome identified
that drains into the axilla.
Limitations
There are limitations to the current study. While this study clearly demonstrates
our intraoperative findings as they relate to lateral pathway drainage to the axilla,
we are unable to qualify if this pathway is simultaneously draining to the supraclavicular/infraclavicular
nodes in patients. However, no patient in this study underwent a level III lymph node
dissection, precluding any evaluation of drainage to these nodal basins. There were
no differences in baseline demographics and preoperative treatment between groups,
further supporting that these findings reflect existing anatomic variations. Moreover,
we recognize the need for further study in a larger patient population with prolonged
follow-up to evaluate its true influence on LE development.
Conclusion
This study is consistent with prior anatomic publications as we have identified variability
of the lateral-upper arm drainage. Our study provides the first intraoperative assessment
of the lateral pathway in the axilla which may have clinical implications for the
lymphatic surgeon performing ILR. Specifically, bypass of the lateral pathway, along
with the traditional divided lymphatics of the medial-upper arm, would provide a more
comprehensive approach to immediate lymphatic drainage following ALND and may help
further reduce the rates of lymphedema. As the field of lymphatic surgery continues
to advance and lymphatic anatomy is further elucidated, we anticipate further studies
that link anatomic variations with differing rates of lymphedema development.
