C L I N I C A L A R T I C L E

Deep inferior epigastric lymph node basin: Analysis of noveldonor site for vascularized lymph node transfer among10 consecutive patients

Oscar Ochoa MD FACS1 | Michael Metzner MD2 | Constantine Theoharis MD3 |

Minas Chrysopoulo MD FACS1 | Steven Pisano MD1 | Chet Nastala MD FACS1 |

Peter Ledoux MD1 | Gary Arishita MD1 | Ramon Garza III MD1 | Ted Snider MD3

1Plastic Reconstructive and Microsurgical

Associates (PRMA), San Antonio, Texas

2Department of Surgery, UT Health, San

Antonio, Texas

3South Texas Pathology Associates, San

Antonio, Texas

Correspondence

Oscar Ochoa, 9635 Huebner Road, San

Antonio, TX 78240.

Email: dr.ochoa@prmaplasticsurgery.com

AbstractIntroduction: Breast cancer-related extremity lymphedema is a potentially devastating condi-

tion. Vascularized lymph node transfer (VLNT) has shown benefit in lymphedema treatment.

Due to concerns over potential iatrogenic complications, various donor sites have been

described. The current study aims at defining the deep inferior epigastric lymph node basin as a

novel donor site for VLNT.

Methods: A retrospective study was performed on patients undergoing routine abdominal-

based breast reconstruction. Resection of all perivascular adipose and lymphatic tissue

surrounding the proximal deep inferior epigastric pedicle was performed at the time of pedicle

dissection and submitted for Pathologic evaluation. Patient demographics and pertinent

medical/surgical history was obtained from medical records.

Results: Specimens were obtained from 10 consecutive patients. Seven patients underwent

bilateral reconstruction for a total of 17 specimens obtained. Mean patient age and BMI were

48 years � 9.4 and 27 � 4.2, respectively. Fourteen out of 17 (82%) specimens contained viable

lymph nodes displaying a thin fibrous connective tissue capsule overlying an unremarkable sub-

capsular sinus with a cortex and paracortex containing germinal centers composed of B lympho-

cytes, tangible body macrophages, and T-cells. The medullary sinus space displayed a fatty

unremarkable hilum. The mean number and size of lymph nodes were 2.6 �1.2 nodes/specimen

and 3.67 mm � 2.3, respectively. All patients experienced an uneventful postoperative course

without evidence any of compromised flap viability.

Conclusion: Lacking previous description, the deep inferior epigastric lymph node basin is a

readily accessible donor site with significant anatomic advantages for potential VLNT during

autologous breast reconstruction.

1 | INTRODUCTION

Breast cancer-related upper extremity lymphedema is a devastating

potential ramification of lymphatic disruption caused by axillary lymph

node staging and/or management of lymph node metastasis. Disrup-

tion of afferent lymphatic flow leads to pressure-driven accumulation

of protein-rich fluid within the interstitial spaces leading to extremity

swelling and irreversible fibrosis (Warren, Brorson, Borud, & Slavin,

2007). Reported incidence of upper extremity lymphedema following

axillary lymph node dissection ranges between 12 and 49%

(Kwan et al., 2002; Petrek, Senie, Peters, & Rosen, 2001). Although

the introduction of sentinel lymph node biopsy techniques have

decreased the incidence of upper extremity lymphedema, reported

risk remains between 3.5 and 11% (DiSipio, Rye, Newman, & Hayes,

2013; Lumachi et al., 2009; McLaughlin et al., 2008).

Treatments for lymphedema range from conservative decongestive

therapy, which includes exercise, compression garments, and manual

lymph drainage to the growing field of microsurgical management

including vascularized lymph node transfers (VLNT). VLNTs are based

on the concept of implantation of healthy lymph node tissue into

Received: 3 November 2017 Revised: 11 July 2018 Accepted: 7 August 2018

DOI: 10.1002/micr.30372

Microsurgery. 2018;1–6. wileyonlinelibrary.com/journal/micr © 2018 Wiley Periodicals, Inc. 1

extremities where the lymphatic system has been disrupted, or where

the lymph nodes are absent secondary to surgical intervention. The

mechanism of how VLNTs function in reducing extremity lymphedema

is still debated, but 3 primary theories that have been proposed:

(1) release of obstructive scar tissue at recipient sites, (2) hydrostatic

“pumping” where the lymph node acts as a pump via arterial inflow and

venous outflow, and (3) lymphangiogenesis through growth factors such

as VEGF-C produced by the healthy transplanted lymph node tissue

(Chang & Kim, 2010; Cheng et al., 2014; Ito & Suami, 2014; Patel, Lin, &

Cheng, 2015; Viitanen, Visuri, Sulo, Saarikko, & Hartiala, 2015). Despite

an ill-defined mechanism of action, VLNTs have shown some promising

results in the treatment of lymphedema (Nguyen et al., 2017).

One of the most common VLNT donor sites for lymph node harvest

is the inguinal lymph node basin based off the superficial circumflex iliac

vessels or superficial inferior epigastric pedicle. The inguinal lymph node

basin could be used as an independent flap or, due to its favorable

location, as a composite flap through incorporation of the lymph node

harvest with an abdominal-based autologous flap for simultaneous

breast reconstruction and surgical treatment of lymphedema (Becker,

Assouad, Riquet, & Hidden, 2006; Nguyen, Chang, Suami, & Chang,

2015; Saaristo et al., 2012). However, concerns for potential iatrogenic

lymphedema of the lower extremity following inguinal lymph node

harvest (Pons, Masia, Loschi, Nardulli, & Duch, 2014; Vignes, Blanchard,

Yannoutsos, & Arrault, 2013) has led to the exploration of alternative

donor sites for VLNT. Alternative donor sites in clinical use include

axillary/lateral thoracic, submental, supraclavicular, and omental flaps

(Ciudad et al., 2017; Garza, Skoraki, Hock, & Povoski, 2017; Nguyen

et al., 2015; Oi & Chang, 2017; Patel et al., 2014; Scaglioni et al., 2018).

Unfortunately, each of the donor sites described are associated with

potential morbidity and variable complexity. Without a previous

description in the literature as a potential source for VLNT, this study

characterizes the deep inferior epigastric lymph node basin.

2 | METHODS

A retrospective study of prospectively recorded data was conducted

after institutional review board approval (UT Health, San Antonio, TX)

among 10 consecutive breast cancer patients that underwent deep

inferior epigastric perforator (DIEP) flap reconstruction by the first

author (O.O.) from March to August 2017. Among study patients, the

perivascular tissue attached to and completely encasing the proximal

deep inferior epigastric vessels was excised as an independent

incidental procedure. Patient preoperative demographics including

medical and surgical history were obtained from medical records and

recorded appropriately. Patients with a history of stage IV breast

cancer, recent viral illness or abdominal wall soft tissue infection, as

well as, other known malignancies were excluded.

2.1 | Surgical Technique

At the time of breast reconstruction, standard DIEP flap design using

the infraumbilical abdominal wall tissue was undertaken. Flap eleva-

tion and perforator selection was executed in standard fashion for

each hemi-abdomen (Clemens & Nahabedian, 2011). After perforator

selection, the ipsilateral anterior rectus sheath was incised vertically

along the caudal and lateral aspect. The incised edges of the rectus

sheath were reflected medially and laterally exposing the caudal

rectus abdominis muscle. The lateral edge of the caudal rectus abdo-

minis muscle was identified and released with bipolar cautery allowing

medial retraction (Figure 1). The proximal deep inferior epigastric

pedicle, located in the preperitoneal space, posterior to the rectus

muscle, was identified and exposed from the pedicle origin off the

external iliac vessels to the bifurcation of the medial and lateral

branches of the deep inferior epigastric pedicle (Figure 2).

Once exposed, the deep inferior epigastric pedicle proximal to the

bifurcation was skeletonized of all perivascular adipose and lymphatic

tissue until reaching the pedicle origin off the external iliac vessels

under loupe magnification. Of note, vascular perforators, originating

from the medial and/or lateral pedicle branches, supplying the adipo-

cutaneous substance of the DIEP flap are located far more distally and

unrelated to the LN basin discussed herein surrounding the proximal

pedicle. The pedicle perivascular tissue corresponding to each DIEP

flap dissected was excised and submitted for pathologic evaluation to

determine number and dimension of viable lymph nodes.

3 | RESULTS

Ten consecutive patients underwent breast reconstruction with DIEP

flaps and were included in the current study. Mean patient age was

48.1 � 9.4 years with an average BMI of 27.6 � 4.2. Seven out of

10 (70%) patients reported at least one previous abdominal surgery.

FIGURE 1 Intraoperative photo of deep inferior epigastric pedicle

exposure. With the DIEP flap reflected cranially, the caudal and lateralrectus sheath was incised vertically. The lateral leaf of the rectussheath was retracted laterally with lone star elastic hooks. The lateraledge of the rectus abdominis muscle was reflected medially with anAllis clamp. The deep inferior epigastric pedicle was identified in thepreperitoneal space encased in adipose and lymphatic tissue

2 OCHOA ET AL.

Bilateral breast reconstruction with DIEP flaps was performed in

7 patients while 3 patients underwent unilateral reconstruction for a

total of 17 flaps dissected with corresponding perivascular specimens

obtained for analysis.

Fourteen out of 17 study perivascular specimens (82%) contained

viable lymph nodes after histologic evaluation. The deep inferior

epigastric lymph nodes described herein were located along the corre-

sponding pedicle, 6–8 cm from the pedicle origin in the preperitoneal

space just proximal to its usual bifurcation (or trifurcation) into medial

and lateral branches. The medial and lateral branches continue distally

into their corresponding intramuscular portions, ultimately terminating

in perforators entering the adipocutaneous substance of the DIEP.

Each individual node displayed a thin fibrous connective tissue cap-

sule overlying an unremarkable subcapsular sinus in association with a

cortex containing follicles with germinal centers composed predomi-

nantly of B lymphocytes with occasional tingible-body macrophages.

The paracortex was composed predominantly of T cells. The medullary

sinus space displayed a fatty unremarkable hilum (Figure 3). Mean num-

ber of lymph nodes present per specimen was 2.6 � 1.2 with a mean

lymph node diameter of 3.67 � 2.3 mm. No complications were

associated with harvesting of the perivascular tissue surrounding the

deep inferior epigastric pedicle. All patients experienced an uneventful

postoperative course without evidence any of compromised flap

viability. Description of each individual patient and results are presented

in Table 1.

4 | DISCUSSION

Breast cancer-related extremity lymphedema is an extraordinarily

debilitating condition with significant detrimental effects on quality of

life (Ahmed, Prizment, Lazovich, Schmitz, & Folsom, 2008; Morgan,

Franks, & Moffatt, 2005). As a surgical treatment for extremity lymph-

edema, vascularized lymph node transfer (VLNT) has shown promising

results (Basta, Gao, & Wu, 2014; Becker et al., 2006). VLNT for breast

cancer-related upper extremity lymphedema can be performed in

conjunction with an abdominal-based free flap for breast reconstruction

(Becker et al., 2006; Nguyen et al., 2015; Saaristo et al., 2012) or as a

solitary free flap to the axilla (Becker et al., 2012; Vignes et al., 2013) or

other more distal extremity recipient sites (Cheng et al., 2013; Gharb

et al., 2011; Lin et al., 2009).

In an effort to minimize iatrogenic donor site morbidity associated

with lymph node harvest, various lymph node donor sites have been

described and are in clinical use (Ciudad et al., 2017; Garza et al.,

2017; Nguyen et al., 2015; Oi & Chang, 2017; Patel et al., 2014;

Scaglioni et al., 2018). Currently, the superficial inguinal lymph node

basin based off the superficial inferior epigastric or superficial circum-

flex iliac vessels is the most common donor site used for VLNT (Patel

et al., 2014). However, due to concerns over potential development

of secondary lymphedema of the lower extremity (Vignes et al., 2013),

investigation into alternative potential donor sites continues.

The current study characterizes a newly described lymph node

basin that, surprisingly, has escaped description in the literature

despite routine exposure during abdominal-based free flap breast

reconstruction through dissection of the proximal deep inferior

epigastric vascular pedicle. Lymphatic drainage of the anterior abdom-

inal wall is dependent on superficial and deep lymphatic systems. The

superficial lymphatic vessels drain the infraumbilical abdominal wall

soft tissues above the deep muscular fascia into the superficial

inguinal lymph node basin. In contrast, the deep lymphatic vessels of

the infraumbilical abdominal wall are associated with the abdominal

wall musculature (Hunstad & Repta, 2009) and fascia and follow the

deep inferior epigastric vessels (Felmerer, Muehlberger, Berens von

FIGURE 2 Intraoperative photo of deep inferior epigastric pedicle

and lymph node basin isolation. The deep inferior epigastric pedicleand attached lymph node basin (over a moist 4 × 4 sponge) wasdissected from the surrounding preperitoneal tissue

FIGURE 3 Photomicrograph (100×) of deep inferior epigastric lymph

node (stained with Hematoxylin and eosin) showed a thin fibrousconnective tissue capsule overlying an unremarkable subcapsular sinusin association with a cortex that contained follicles with germinalcenters composed predominantly of B lymphocytes with occasionaltingible-body macrophages. The paracortex was composedpredominantly of T cells. The medullary sinus space displayed a fattyunremarkable hilum

OCHOA ET AL. 3

Rautenfeld, & Vogt, 2002). In a cadaveric anatomic study performed

by Felmerer et al., authors injected the abdominal fascia with lymphat-

ically collected Turnbull's blue dye and were able to document the

presence of lymphatic vessels connected by ladder-like channels along

the deep inferior epigastric pedicle (Felmerer et al., 2002). The deep

inferior epigastric lymph nodes characterized in this study are posi-

tioned along these previously reported lymphatic vessels surrounding

the proximal vascular pedicle and form a component of the deep

lymphatic system draining the anterior abdominal wall.

Viable lymph nodes located along the perivascular tissue encasing

the deep inferior epigastric pedicle were found in 14 out of 17 study

specimens (82%), 6–8 cm from its origin off the external iliac vessels

and just proximal to the normal bifurcation of medial and lateral

branches (Figure 4). As a potential source for VLNT, the viability of

the deep inferior epigastric lymph nodes described in the manuscript

is based on the histologic findings associated with normal viable

lymphatic tissue staining patterns and architecture. In addition, contin-

ued lymph node perfusion and viability after harvest along with the

deep inferior epigastric pedicle is suggested by intraoperative indo-

cyanine green angiographic imaging obtained after pedicle and lymph

node basin dissection verifying proof of concept with perfusion of the

lymph node basin while attached solely to the deep inferior epigastric

pedicle (Figure 5). Due to its location, not surprisingly, harvesting of

the deep inferior epigastric lymph node basin was not associated with

any complications in this study.

The deep inferior epigastric lymph node basin characteristics

reported in this study are comparable to other donor sites in clinical use.

Consistent with previous studies characterizing other lymph node basins

for VLNT, lymph node quantity within deep inferior epigastric lymph

node basin specimens (mean 2.6 nodes/specimen) is similar compared

to inguinal (Patel et al., 2014; Zeltzer et al., 2017), submental (Patel

et al., 2014), thoracodorsal and supraclavicular donor sites (Gerety et al.,

2016). Viable lymph nodes were identified in 14 out of 17 specimens

(82.3%) collected in the current study. In comparison to the most

popular donor site for VLNT, Zeltzer et al. reported the presence of a

viable lymph node unit in only 84% of inguinal lymph node samples

(Zeltzer et al., 2017). The ideal volume of transferred lymphatic tissue

for effective lymphedema treatment has yet to be determined and is an

area of active research. The mean diameter of histologically defined

lymph nodes in the current study specimens was 3.67 mm. Interestingly,

although a minimum lymph node volume has been suggested previously

(Zeltzer et al., 2017), omental flaps have shown effective long-term

improvements in extremity lymphedema through lymphoreticular bodies

despite lacking true lymph nodes (Nguyen et al., 2017).

Conceptually, the ideal lymph node donor site characteristics

should include functional lymph nodes with consistent vascular

TABLE 1 Patient population and lymph node basin characteristics

Individual lymph node size (mm)

Patient Age BMIPrior abdominalsurgeries (#)

Laterality ofreconstruction

Specimenside

Lymphnode number 1 2 3 4 5

1 54 25 1 Bilateral Right 0

Left 5 3.8 2.9 1.1 0.9 0.6

2 41 29 1 Unilateral Right 3 3 2 2

3 53 27 0 Bilateral Right 3 2 0.5 0.5

Left 1 3

4 61 22 0 Bilateral Right 2 2 4

Left 3 5 5 4

5 61 24 2 Unilateral Right 0

6 36 28 2 Bilateral Right 0

Left 1 6.5

7 42 30 0 Bilateral Right 3 9 7 6

Left 3 6 4 3

8 42 25 1 Bilateral Right 3 2 2 2

Left 2 7 2

9 53 29 3 Bilateral Right 4 5 4 3 3

Left 3 10 4 3

10 38 37 4 Unilateral Left 1 5

FIGURE 4 Schematic of deep inferior epigastric lymph node basin with

abdominal flap reflected medially. Lymph node basin was located alongthe proximal deep inferior epigastric pedicle between the bifurcation ofthe medial and lateral branches and origin from external iliac vessels

4 OCHOA ET AL.

anatomy allowing uncomplicated and efficient dissection located in an

adjacent or easily accessible operative field with negligible or absent

donor site morbidity. The deep inferior epigastric lymph node basin

described in this study meets all above characteristics specifically

when utilized in conjunction with an abdominal-based breast recon-

struction such as a DIEP or muscle-sparing TRAM flap for simulta-

neous breast reconstruction and VLNT. In bilateral breast

reconstruction cases, flap vascular anastomosis would be required to

vessels in the axilla, such as the thoracodorsal vessels, in order to inset

the lymph node cluster in the native axillary LN bed. In this setting,

lymph node basin location along the abdominal flap vascular pedicle

carries significant advantages regarding optimization of continued

lymph node function after flap transfer. Specifically, the standard

paired vascular free flap anastomoses, not only provide abdominal flap

perfusion and venous outflow, but also simultaneously supply the

lymph node basin. This characteristic overcomes some important limi-

tations associated with inguinal VLNT. When performed in conjunc-

tion with breast reconstruction, arterial inflow to the inguinal lymph

node basin is dependent on random perfusion through the abdominal

flap. Inguinal lymph node perfusion in this circumstance is unpredict-

able (Saaristo et al., 2012) and may be additionally compromised if

lower abdominal (i.e., Pfannenstiel) incisions are present. In contrast,

the deep inferior epigastric lymph node basin is axially perfused

through small un-named branches directly from the deep inferior epi-

gastric pedicle. This has been shown in the current study through

indocyanine green angiographic imaging. When performing inguinal

VLNT in conjunction with breast reconstruction, Saaristo

et al. describes assessing lymph node perfusion clinically and perform-

ing an additional arterial anastomosis to the retrograde thoracodorsal

artery if perfusion is inadequate through the abdominal flap (Saaristo

et al., 2012). Parallel to arterial perfusion, venous outflow of the deep

inferior epigastric lymph node basin is provided through the deep

inferior epigastric vein. This configuration allows lymph node basin

venous outflow through a single venous anastomosis. With simulta-

neous inguinal VLNT and abdominal-based breast reconstruction, an

additional lymph node venous anastomosis is invariably required for

proper lymphatic decompression through lymphovenous shunting

(Cheng et al., 2013; Lin et al., 2009). Additional vascular anastomoses

associated with inguinal VLNT can, not only be technically challenging,

but also increase operative time (Saaristo et al., 2012).

Alternatively, treatment of upper extremity lymphedema and

unilateral breast reconstruction could be accomplished using the con-

tralateral DIEP flap pedicle for lymph node harvesting for axillary

nodal reconstitution while maintaining preferred usage of the internal

mammary vessels for ipsilateral pedicle anastomosis. While this may

facilitate optimal flap positioning, venous outflow to the deep inferior

epigastric lymph node basin on the contralateral pedicle may be

suboptimal and possibly require an additional venous anastomosis for

proper lymphovenous shunting.

As the first to describe the deep inferior epigastric lymph node

basin, the current anatomic study has important limitations to con-

sider. The relatively small sample size (17 specimens) could be

expanded to include a greater number of patients to further character-

ize this novel lymph node basin. More importantly, the current study

is lacking clinical data to demonstrate efficacy regarding improve-

ments in upper extremity lymphedema. Given the number and size of

the lymph nodes present within this lymph node station as reported

by the current study in comparison to other donor sites in clinical use,

there is no theoretic reason to dismiss the deep inferior epigastric

lymph node basin as a viable donor site for VLNT. Furthermore,

utilization of the axillary (thoracodorsal) vessels for anastomosis in

bilateral cases may result in suboptimal lateral positioning of the flap

substance compared to cases where the internal mammary vessels are

utilized as the recipient vessels. The benefits gained by elimination of

donor site morbidity and ensured perfusion of the lymph node basin

based on its location in relation to the pedicle are worth noting

making this technique an additional potential option in the armamen-

tarium of the reconstructive surgeon.

5 | CONCLUSION

Breast cancer-related lymphedema is a devastating potential compli-

cation related to axillary lymphatic disruption. As an emerging

modality, VLNT has shown promising results in the treatment of

lymphedema. However, donor site morbidity is a significant limitation

of VLNT promoting ongoing research for alternative sites for lymph

node harvest. Due to its favorable location and unique characteristics,

the deep inferior epigastric lymph node basin presented in the current

study holds significant promise as a valuable source for VLNT.

CONFLICTS OF INTEREST

The current study was independently funded. The authors have no

financial conflicts of interest to disclose.

FIGURE 5 Intra-operative photograph of indocyanine green

fluorescence angiography of the deep inferior epigastric pedicle andattached lymph node basin. Positioned over a moist 4 × 4 sponge, thedeep inferior epigastric pedicle and attached lymph node basinshowed appropriate uptake of indocyanine green indicative ofmaintained perfusion

OCHOA ET AL. 5

ORCID

Oscar Ochoa http://orcid.org/0000-0003-2570-5739

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How to cite this article: Ochoa O, Metzner M, Theoharis C,

et al. Deep inferior epigastric lymph node basin: Analysis of

novel donor site for vascularized lymph node transfer among

10 consecutive patients. Microsurgery. 2018;1–6. https://doi.

org/10.1002/micr.30372

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