Received: 1 May 2017 | Accepted: 24 July 2017
DOI: 10.1002/jso.24812
RESEARCH ARTICLE
Effective and efficient lymphaticovenular anastomosis using
preoperative ultrasound detection technique of lymphatic
vessels in lower extremity lymphedema
Akitatsu Hayashi MD1,2
Hidehiko Yoshimatsu MD2 | Takumi Yamamoto MD, PhD3
1 Department of Plastic and Reconstructive
Surgery, Asahi General Hospital, Chiba, Japan
2 Department of Plastic and Reconstructive
Surgery, Graduate School of Medicine,
University of Tokyo, Tokyo, Japan
3 Department of Plastic Surgery, Tokyo
Metropolitan Bokutoh Hospital, Tokyo, Japan
Correspondence
Takumi Yamamoto, MD, PhD, Department of
Plastic Surgery, Tokyo Metropolitan Bokutoh
Hospital, 4-23-15 Kotobashi, Sumida-ku,
Tokyo 130-8575, Japan.
Email: vasko3rikov1meister918@yahoo.co.jp
Presented at the 2016 Annual Meeting of the American Society of Reconstructive
Microsurgery and the 2016 World Symposium for Lymphedema Surgery.
J Surg Oncol. 2017;1–9.
| Nobuko Hayashi MD1,2 |
Background: Identification of functional lymphatic vessels and localization of lymphatic
vessels are important for lymphaticovenular anastomosis (LVA). Indocyanine green
(ICG) lymphography is useful for localization of superficial lymphatic vessels where
dermal backflow is not observed, but not for lymphatic vessels in deep layer or where
dermal backflow is observed. Ultrasound has been applied in LVA and is considered
useful for localization of lymphatic vessels with ICG lymphography cannot be visualized.
Methods: Fifty-five secondary lower extremity lymphedema (LEL) patients who
underwent LVA were classified into two groups, ultrasound-detection-of-lymphatic
group (US group, n = 29) and non-ultrasound-detection-of-lymphatic group (non-US
group, n = 26), and assessed. Sensitivity and specificity to detect lymphatic vessel were
evaluated in US group. Intraoperative findings, required time for dissecting lymphatic
vessels and veins, length of skin incision, and postoperative lymphedematous volume
reduction were compared between the groups.
Results: Lymphatic vessels were detected in all incisions in both groups. LVA resulted in
232 anastomoses in US group and 210 anastomoses in non-US group. Sensitivity and
specificity of ultrasound for detection of lymphatic vessels were 88.2% and 92.7%,
respectively. Diameter of lymphatic vessels found in US group was significantly larger
than that in non-US group (0.66 ± 0.18 vs 0.45 ± 0.20 mm; P = 0.042). Time required for
dissecting lymphatic vessels and veins in US group was shorter than that in non-US
group (9.2 ± 1.7 vs 14.7 ± 2.4 min; P = 0.026). LEL index reduction was significantly
greater in US group than that in non-US group (26.7 ± 13.6 vs 7.8 ± 11.3; P = 0.031).
Conclusions: Ultrasound-guided detection of lymphatic vessels for lymphedema was
performed with high precision, and allows easier and more effective LVA surgery.
KEYWORDS
echo, LVA, microsurgery, secondary lymphedema
1 | I NTRODU C TI ON
Secondary lymphedema is progressive in nature, and its treatment is
challenging.1,2 Management options for lymphedema include both
wileyonlinelibrary.com/journal/jso © 2017 Wiley Periodicals, Inc. | 1
2 |
conservative methods, such as compression therapy, and surgical
3–11
treatment. Among the surgical procedures, lymphaticovenular
anastomosis (LVA), which can be performed under local anesthesia, is
an effective, minimally invasive treatment for refractory lymph-
edema.12–20 These advantages have made LVA an progressively
common surgical treatment for secondary lymphedema.
A positive correlation between the number of LVA performed and
therapeutic effectiveness has been reported.19 Preoperative identifi-
cation of functional lymphatic vessels and veins can contribute to
shorter operative time in an attempt to establish as many bypasses as
possible in performing LVA.
Indocyanine green (ICG) lymphography is a minimally invasive
imaging modality that can not only evaluate the severity of
lymphedema but also determine the location of lymphatic vessels by
visualizing superficial lymph flows.17,21–23 However, ICG lymphogra-
phy cannot visualize lymphatic flow in the deep layer of subcutaneous
tissue, or one that is masked beneath dermal backflow patterns,
24
particularly in stardust and diffuse patterns. ICG lymphography also
requires ICG injection before the examination, and an infrared sensor
device for visualization of the lymphatic flow. ICG lymphography
cannot be performed on patients who are allergic to iodine.
For detection of lymphatic vessels in a region masked by dermal
backflow pattern, or in patients with allergic reactions to ICG, we
believe ultrasound, which is more common and simple, could
substitute for ICG lymphography. Lymphatic vessels were reported
to be illustrated as intermittent homogeneous, hypoechoic and
specular misshapen images with ultrasonography in the lower leg of
25
healthy volunteers. This research suggested the possibility of
detecting lymphatic vessels under dermal backflow pattern of ICG
lymphography in affected limb site of lymphedema, but no research
has yet underlined the feasibility of ultrasound to detect the lymphatic
vessels of lymphedema patients based on direct intraoperative
observation during LVA.
We established a new detection technique of lymphatic vessel for
lymphedema patients using ultrasound. We conducted a retrospective
observational study to evaluate feasibility and effectiveness of
preoperative ultrasound detection technique for LVA in sites where
dermal backflow pattern was shown with ICG lymphography or in
patients allergic to ICG.
2 | P A T I E NT S A N D ME TH O D S
The study included 55 patients (2 men and 53 women) with
International Society of Lymphography stage 2 lower extremity
lymphedema, who underwent LVA between September of 2013 and
March of 2015.26 Patients were classified into two groups: those who
underwent LVA without preoperative ultrasound detection of
lymphatic vessel between September 2013 and May 2014 (non-
ultrasound-detection-of-lymphatic group [non-US group], n = 26; 1
man and 24 women) and those who underwent LVA with preoperative
ultrasound detection of lymphatic vessel between June of 2014 and
March of 2015 (ultrasound-detection-of-lymphatic group [US group],
HAYASHI ET AL.
n = 29; one man and 28 women). Leg dermal backflow stage had been
determined preoperatively by means of ICG lymphography.21 ICG was
injected to all patients who were not allergic to iodine. Three patients
were allergic to iodine.
ICG lymphography was performed as follows: 0.2 mL of ICG
(Diagnogreen 0.125%; Daiichi Pharmaceutical, Tokyo, Japan) was
injected subcutaneously into the second web spaces of the feet and
fluorescent images of lymphatic drainage channels were obtained
using a photodynamic eye infrared camera system (PDE; Hamamatsu
Photonics K.K., Hamamatsu, Japan).
All patients included in this study had received compression
therapy using elastic stockings for at least 3 months, which resulted in
no clinical improvement. Patients with recurrence after previous
cancer surgery were excluded from the study. This study was
conducted under the University of Tokyo Hospital institutional ethical
review board. All patients provided written informed consent for
participation in this retrospective observational study.
2.1 | Detection of lymphatic vessel using ultrasound
In the US group, based on the characteristic findings, lymphatic vessels
were identified preoperatively using ultrasound in the groin, the thigh,
the knee, and the lower leg, where ICG lymphography showed dermal
backflow or in patients on whom ICG could not be used. The lymphatic
vessels were identified at the center of probe and the exact sites were
marked with a pen and checked later by intraoperative direct
observation (Figures 1 and 2).25 To ensure that the identified vessels
were not blood vessels, the vessels were checked with color Doppler
mode. The sites where were not marked with a pen in the same
operation field were also checked later by intraoperative direct
observation. All ultrasound detections were performed by one of the
study authors (AH).
A true positive is a lymphatic vessel identified with ultrasonogra-
phy which was later confirmed by intraoperative direct observation. A
false positive is a lymphatic vessel seen with ultrasonography which
could not be later confirmed by intraoperative direct observation. A
true negative is a lymphatic vessel not seen with ultrasonography
which could not be later seen by intraoperative direct observation. A
false negative is a lymphatic vessel not seen with ultrasonography
which could be later seen by intraoperative direct observation.
Sensitivity and specificity of ultrasound detection technique of the
lymphatic vessels which were existed in dermal backflow area or non-
ICG enhanced area were evaluated by comparing the result with
intraoperative direct observation.
Ultrasound was performed with Noblus (Hitachi Medical Corpo-
ration, Tokyo, Japan) with a linear EUP-L65 probe in color Doppler
mode at a frequency of 18 MHz. The pressure of the probe on the skin
was minimized to avoid artificial deformation of underlying structure.
2.2 | Lymphaticovenular anastomosis
LVA was performed using previously documented procedures.27 All
surgeries were performed under local anesthesia. The lymphatic
HAYASHI ET AL.
| 3

FIGURE 1 (Above, left) Identification of lymphatic vessels and veins using ultrasound were performed in the dermal backflow area of
indocyanine green lymphography of thigh. Identified point was marked with a pen. (Above, right) Lymphatic vessel (Yellow arrow) and vein
(Green arrow) which are suitable for anastomosis were detected by ultrasound preoperatively. (Below, left) Lymphatic vessel (Yellow arrow)
and vein (Green arrow) were dissected as ultrasound indicated. (Below, right) The lymphatic vessel and the vein were anastomosed side-to-
end using 11-0 nylon micro-sutures

vessels and veins which seemed suitable for anastomosis were
preoperatively identified with ultrasound in US group. Under surgical
microscope view, approximately 3 cm skin incisions were made around
the groin, the thigh, the knee, and the lower leg along the greater
saphenous vein. Elongation of skin incision was performed when the
lymphatic vessels or veins could not be found through the initial
incision. The veins and the lymphatic vessels were anastomosed with
either end-to-end or end-to-side fashion using 11-0 or 12-0 nylon
micro-sutures (Figures 1 and 2). Patency of LVA was confirmed by
observation of the anastomosis site under an operating microscope (ie,

FIGURE 2 (Above, left) Identification of lymphatic vessels and veins using ultrasound were performed in the lower leg. The patient has
allergic to contrast medium, so Indocyanine green was not able to be used. Identified point was marked with a pen. (Above, right) Lymphatic
vessels (Yellow arrow) and the branch from saphenous vein (Green arrow) which are suitable for anastomosis were detected by ultrasound
preoperatively. (Below, left) Lymphatic vessels (Yellow arrow) and Y-Shape vein (Green arrow) were dissected as ultrasound indicated. (Below,
right) The lymphatic vessel and the vein were anastomosed side-to-end using 11-0 nylon micro-sutures
4 | HAYASHI ET AL.

lymph-blood border movement across the anastomosis). One or two TABLE 2 Operation summary
weeks after surgery, preoperative conservative therapy was resumed. 442 lymphaticovenular anastomoses in 55
The surgeons all had more than 6 months of experience in lymphedema patients
microsurgery and had successfully completed free superficial inferior No. of LVAs per patient 5-14 (8.3)
epigastric artery flaps in rats.28 No. of microscopes used per patient 2-4 (3.1)
Operative time, h 3-6 (4.2)

2.3 | Effectiveness of ultrasound-guided LVA
Comparison was made between two groups on the following aspects:
patient characteristics, intraoperative findings, required time for
dissecting lymphatic vessels, and veins and skin incision length.
Lymphedematous volume was evaluated on the basis of the lower
extremity lymphedema index determined preoperatively and then
postoperatively 1 year after the surgery, and the reduction in volume
was compared between the two groups.29
2.4 | Statistical analyses
All values were reported as mean ± SD. Differences in the means
between groups were analyzed by Mann-Whitney U test. All P values
were two-sided, and statistical significance was accepted at P < 0.05.
3 | RE SULTS
Postoperative reduction in LEL index −6.8 to 48.3
(20.3)
LVAs, lymphaticovenular anastomoses; LEL, lower extremity lymphedema
Data are ranges (averages).
n = 11; stage 3, n = 34; stage 4, n = 5); 3 patients were not examined
preoperatively by ICG lymphography due to potential allergic reaction
to iodine.
Lymphatic vessels were detected in all incisions in both groups.
The LVA resulted in 442 anastomoses (232 anastomoses in US group
and 210 anastomoses in non-US group) in 55 patients with secondary
lymphedema of the lower extremities; the average number of
anastomoses per case was 8.3 (range, 5-14). The number of surgical
microscope used was 2-4 (average, 3.1), duration of operation was
3-6 h (average, 4.2 h), and average postoperative reduction in the
lower extremity lymphedema index ranged from −12.8 to 48.3
(average, 20.3) (Table 2).

Characteristics of patients are shown in Table 1. Preoperative leg

dermal backflow stage ranged from 1 to 4 (stage 1, n = 2; stage 2, 3.1 | Detection of lymphatic vessel using ultrasound
The number of true positive was 225, and that of false positive was 16.
The number of true negative was 204 and that of false negative was
TABLE 1 Patient characteristics
30. Sensitivity and specificity of ultrasound for detection of lymphatic
110 legs of 55 lower extremity lymphedema
vessels were 88.2% and 92.7%, respectively (Table 3). Lymphatic
patients
vessels in the thigh and knee region existed in a deeper layer than the
Age, yr 32-84 (50.7)
ones in the groin and the lower leg (Table 4).
Sexa
Male 2 (3.6%)
Female 53 (96.4%)
3.2 | Effectiveness of ultrasound-guided LVA
LDB stagea Significant differences were seen between US group (n = 29) and the
Stage I 2 (3.8%) non-US group (n = 26) in the diameter of lymphatic vessels (0.66 ± 0.18
Stage II 11 (21.2%) vs 0.45 ± 0.20 mm; P = 0.042) and the required time for vessel

Stage III 34 (65.4%)

dissection (9.2 ± 1.7 vs 14.7 ± 2.4 min; P = 0.026). The difference in

Stage IV 5 (9.6%)
Stage V 0 (0%) TABLE 3 Number of detected lymphatic vessels
Duration of edema, yr 0.7-19.0 US
(5.90)
+a −b
Cause of lymphedemaa
Intraoperative finding of lymphatic vessels
Uterine cervical cancer 35 (63.6%)
+a 225 30
Uterine corpus cancer 14 (25.5%)
−b 16 204
Ovarian cancer 4 (7.3%)
Bladder cancer 2 (3.6%) US, ultrasonography.
a
“+” denotes a state where a lymphatic vessel was found with ultrasonog-
LDB, leg dermal backflow. raphy or intraoperative direct observation.
Data are ranges (averages) otherwise indicated. b
“−” denotes a state where a lymphatic vessel was not found with
a
Data are counts (percentages). ultrasonography or intraoperative direct observation.
HAYASHI ET AL.
| 5

TABLE 4 Location of lymphatic vessels which could be detected lymphedema index of her right and left leg was 278.4 and 219.3,
using ultrasound in US group respectively. LVA using preoperative ultrasound detection technique
Incision site of lymphatic vessels and veins performed at five sites in the right leg

Groin Thigh Knee Lower leg and at two sites in the left leg. There were no complications related
with the operation. Twelve months after LVA, lower extremity
Depth from the body surface, cm
lymphedema index of her right and left leg decreased to 239.7 and
<0.5 2 0 0 41
208.4, respectively (Figure 3).
0.5-1 14 12 17 39
1-1.5 5 25 26 13
1.5-2 0 14 14 0
3.3.2 | Case 2
2.5< 0 2 1 0 A 72-year-old female underwent hysterectomy, pelvic lymph node
Total (n = 225) 21 53 58 93 dissection, and radiotherapy (50 Gy) for uterine cervical cancer
22 years before LVA. Lymphedema occurred in her left lower limb
US group, ultrasound-detection-of-lymphatic group.
3 month after hysterectomy. She began wearing strong compression
garment, but due to repeated episodes of cellulitis, she changed to

diameter of veins and the skin incision length were not statistically stockings with lower pressure. She visited our clinic 21 years after the

significant between the US group and the non-US group (0.67 ± 0.26 onset of lymphedema. Dermal backflow stage of ICG lymphography

vs 0.63 ± 0.22 mm; P = 0.724, 2.9 ± 0.4 vs 3.6 ± 0.8 cm; P = 0.126). was 1 (right) and 4 (left). Preoperative lower extremity lymphedema

Postoperative reduction in the lower extremity lymphedema index was index of her right and left leg was 213.7 and 306.8, respectively. LVA

significantly greater in the US group than in the non-US group using preoperative ultrasound detection technique of lymphatic

(26.7 ± 13.6 vs 7.8 ± 11.3; P = 0.031) (Table 5). Incision elongation was vessels and veins were performed at two sites in the right leg and at

necessary in 34 sites out of 177 sites in the non-US group, whereas five sites in the left leg. Lymphatic vessels in the knee were present in a

incision elongation was never performed in 196 sites of the US group. deep layer rich with fatty tissue as ultrasound indicated. There were no
complications related with the operation. Twelve months after the
lymphatic surgery, right and left lower extremity lymphedema index
3.3 | Case report decreased to 201.2 and 262.9, respectively (Figures 4 and 5).

3.3.1 | Case 1
A 52-year-old female underwent hysterectomy and pelvic lymph node
dissection for uterine cervical cancer 6 years prior to LVA.
Lymphedema occurred in her right lower limb one month after
hysterectomy. She started wearing mild compression garment and did
not have a history of cellulitis. She visited our clinic 5 and half years
after the onset of lymphedema. Dermal backflow stage of ICG
lymphography was 4 (right) and 3 (left). Preoperative lower extremity
4 | DISCUSSION
The present study was conducted to detect the lymphatic vessels using
ultrasonography which used in normal daily practice in lymphedem-
atous limbs showing dermal backflow patterns with ICG lymphography
or in cases where ICG could not be used. The results of this study
showed high sensitivity and specificity of this technique. This study
also showed statistically larger size in the diameter of lymphatic

TABLE 5 Comparison between cases of US and non-US groups

US group (n = 29) Non-US group (n = 26) P
Age, yr 52.4 ± 12.6 49.6 ± 10.8 0.741
2
Body mass index, kg/m 23.6 ± 2.7 22.8 ± 3.4 0.658
Duration of edma, yr 6.3 ± 3.4 5.4 ± 2.8 0.539
No. of LVAs per patient 9.4 ± 1.6 8.1 ± 2.3 0.266
Diameter of lymphatic vessel, mm 0.66 ± 0.18 0.45 ± 0.20 0.042*
Diameter of vein, mm 0.67 ± 0.26 0.63 ± 0.22 0.724
Required time for dissecting lymphatic vessels and veins, min 9.2 ± 1.7 14.7 ± 2.4 0.026*
Length of skin incision, cm 2.9 ± 0.4 3.6 ± 0.8 0.126
Postoperative volume reduction in LEL index 26.7 ± 13.6 7.8 ± 11.3 0.031*

LVAs, lymphaticovenular anastomoses; LEL, lower extremity lymphedema; US group, ultrasound-detection-of-lymphatic group; non-US group, non-
ultrasound-detection-of-lymphatic group.
*P < 0.05.
6 | HAYASHI ET AL.

FIGURE 3 Clinical presentation of Case 1. (Left) Preoperative photograph of the patient. Lymphaticovenular anastomoses using
preoperative ultrasound detection technique of lymphatic vessels and veins performed in five sites of right leg and two sites of left leg. (Right)
Photograph of the patient 12 month after the operation. The lower extremity lymphedema index was decreased (38.9 at right leg, 10.9 at left
leg). She was fully released from compression therapy starting 9 months after surgery

vessels, significant reduction in required time for dissecting lymphatic
vessels and veins, and significant decrease in lower extremity
lymphedema index in the US group. Although this study could not
show statistically significant differences in skin incision length
between the US and the non-US groups, incision elongation was
sometimes necessary in non-US group, which would result in longer
time for vessel dissection.
Several techniques have been reported for detection of lymphatic
vessel using ultrasound. Goldberg et al reported contrast-enhanced
ultrasonographic imaging of lymphatic vessel.30 Lymphosonography
can be used to detect lymphatic drainage pathways in a variety of
animal models using contrast medium. After subcutaneous, submuco-
sal, or parenchymal contrast medium injections, gray scale pulse
inversion harmonic imaging could be used to identify the number and
location of lymphatic vessels in their study. We reported ultrasound
visualization of lymphatic vessels in the lower leg of healthy volunteer
where linear pattern was shown with ICG lymphography without
contrast medium: intermittent homogeneous, hypoechoic, and specu-
lar misshapen images were the characteristic findings of lymphatic
25
vessels. The result of our previous study indicates that ultrasound-
guided detection of lymphatic vessels can be performed with high
precision. The present study revealed that ultrasonography alone
could detect the lymphatic vessels also in affected limb sites of
lymphedema where dermal backflow patterns were shown with ICG
lymphography.
Distinguishing lymphatic vessels from blood vessels or nerves is
crucial for successful LVA. Each vessel has their unique ultrasono-
graphic characteristics (Table 6).25,31,32 The smaller the lymphatic
vessels were, the more difficult it was to distinguish them from blood
vessels by their shapes. In this case, we recommend using color Doppler
mode and tracing vessels proximally to see if vessels converge to the
bigger blood vessel, another lymphatic vessel or lymph node. However,
when lymphatic vessels were smaller than 0.3 mm, they were often
mistaken for subcutaneous veins or nerves in our study, because it
was hard to judge the shape of small vessels even when color Doppler
mode was used. This could have contributed to a failed result; there
were 16 cases of false positive and 30 cases of false negative.
ICG lymphography is a very useful modality for evaluation
of lymphedema and intraoperative detection of lymphatic
vessels.17,21–23,33–38 However, ICG lymphography requires painful
ICG injection before the procedure and special instruments such as a
photodynamic eye infrared camera system for visualization of the
lymphatic flow. ICG lymphography has a depth limit, and it cannot
detect lymphatic vessels located deeper than 1.5 cm from the body
HAYASHI ET AL.
| 7

FIGURE 4 Clinical presentation of Case 2. (Left) Preoperative photograph of the patient. Lymphaticovenular anastomoses using preoperative
ultrasound detection technique of lymphatic vessels and veins performed in two sites of right leg and five sites of left leg. (Right) Photograph of
the patient 12 month after the operation. The lower extremity lymphedema index was decreased (41.9 at right leg, 12.5 at left leg)

surface.24 As shown in Table 4, detection of lymphatic vessel in the
thigh and the knee is difficult with ICG lymphography. Lymphatic
vessels in the thigh and the knee often reside in a deep, fatty layer,
making their detection even more challenging for surgeons; unsuc-
cessful detection of lymphatic vessels is common in this area.
Preoperative ultrasound detection of lymphatic vessels will address
this uncertainty, telling surgeons exact location of lymphatic vessels
even in the deep, fatty layer as shown in Figure 5. From this study, it
was suggested that ultrasonography can accurately detect the exact
location of lymphatic vessels and venules which run not only in a deep
layer but also in a superficial layer.
Finding veins appropriate for LVA is also difficult. Surgeons
often face a situation in which there is a suitable lymphatic vessel
but no suitable vein for LVA.39 In such cases, surgeons often
extend the incision to find a suitable vein, resulting in a longer scar.
From our study, ultrasound could detect not only lymphatic vessels
but also veins. Surgeons can select the vein with appropriate size
easily from among subcutaneous veins and branches of the greater
saphenous vein. In addition, surgeons choose a vein with less
backflow using “push and release” technique in ultrasound color
Doppler mode for prevention of venous reflux at the lymphatico-
venular shunt. In our study, we believe that these advantages of

FIGURE 5 (Left) Detection of lymphatic vessel (Yellow arrow) and vein (Green arrow) in the knee was performed in Case 2. Lymphatic
vessel in the knee resided in rich fatty tissue in the deep layer. (Right) Lymphatic vessel in rich fatty tissue (Yellow arrow) and vein (Green
arrow) were dissected as ultrasound indicated in the incision site of knee
8 |
TABLE 6 Characteristics of lymphatic vessel, blood vessel, and nerve
Shape
Lymphatic vessel Spicular missshapen
Blood vessel Round
Nerve Honey comb
Oval (superficial verve)
preoperative ultrasound detection technique reduced the time
required for vessel dissection and thus the total operation time,
and also decreased the lower extremity lymphedema index
significantly.
The identification of large lymphatic vessels with abundant lymph
flow is an important factor determining the therapeutic effect of LVA
in patients with lower extremity lymphedema. Seki et al reported that
high-flow lymphatic vessels can be detected in the superior-edge-of-
the-knee incision.40 Using our method, expanded lymphatic vessels
can be detected not only in the superior-edge-of-the-knee region but
in all regions, not expanded and too thin lymphatic vessels hardly can
be detected. It appears that lymphatic vessels with expanded lumen in
ultrasound image reflect functional and high-flow lymphatic vessels. In
our study, it is assumed that this advantage of preoperative ultrasound
detection technique enabled us to dissect larger diameter of lymphatic
vessels and resulted in significant decrease in lower extremity
lymphedema index. The results of our study indicated that the
lymphatic image in ultrasonography shows functional lymphatic
vessels.
This study demonstrated that ultrasonography can detect
lymphatic vessels even in regions with dermal backflow patterns,
where the lymphatic vessels are concealed by the patterns. On the
other hand, ICG lymphography is useful for evaluation and diagnosis
of lymphedema. Taking each characteristic into consideration,
lymphatic vessel detection using ultrasonography technique would
complement ICG lymphography technique. Our previous study
reported elastography which is performed by ultrasonography could
be a useful alternative evaluation for lymphedema severity when
ICG lymphography is not available.41 We suggest that ultrasonogra-
phy imaging is more useful for diagnosis and treatment of
lymphedema.
This study has several limitations. First, acquisition of accurate
ultrasonographic image is highly operator dependent. Because our
ultrasound scanning of lymphatic vessel was performed by one
examiner, inter-operator reliability could not be evaluated. Also due to
the size of superficial lymphatic collectors being very small, technical
errors, such as misinterpretation can occur. Second, we did not
statistically examine the relationship between characteristic of
lymphatic vessels in ultrasound visualization and the severity of
lymphatic change according to the normal, ectasis, contraction,
sclerosis type classification (NECST classification).42 While this is a
subject of future studies, our clinical experience indicates that
characteristics of lymphatic vessels in ultrasound may change with
severity of lymphatic change.
HAYASHI ET AL.
Echogenic texture Color Doppler mode
Hypoechoic Not colored
Hypoechoic Colored/not colored
Bright with hypoechoic fascicles Not colored
One hypoechoic fascicle (superficial nerve)
5 | CONCL US IO NS
To our knowledge, this is the first attempt to detect the lymphatic vessels
with ultrasonography in lymphedema patients. Ultrasound-guided
detection of lymphatic vessels was performed with high precision,
enabling efficient, and effective LVA. With further study in affected
limbs of lymphedema including primary lymphedema, this technique
may aid lymphatic microsurgery for lymphedema in the future.
ACKNOWLEDGMENTS
We gratefully acknowledge the support of Isao Koshima, Mitusnaga
Narushima, Mitsunobu Harima, Daisuke Mito, Ryohei Ishiura, Megumi
Furuya (The University of Tokyo), Kazufumi Tachi (Asahi General
Hospital), and Akari Hayashi, without which this study could not have
been completed.
CONFLICTS OF INTEREST
The authors have no conflicts of interest to declare.
ORCID
Akitatsu Hayashi http://orcid.org/0000-0002-3615-8163
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SYNOPSIS
This study demonstrated that ultrasound-guided detection of lymphatic vessels complemented the drawbacks of Indocyanine green lymphography
for lymphedema. Ultrasonography can detect lymphatic vessels even in regions with dermal backflow patterns, where the lymphatic vessels are
concealed by the patterns. This technique also enabled efficient and effective LVA than ever in this study. This technique is minimally invasive and
may aid lymphatic microsurgery for lymphedema in the future.
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How to cite this article: Hayashi A, Hayashi N, Yoshimatsu
H, Yamamoto T. Effective and efficient lymphaticovenular
anastomosis using preoperative ultrasound detection
technique of lymphatic vessels in lower extremity
lymphedema. J Surg Oncol. 2017;1–9.
https://doi.org/10.1002/jso.24812