Surgical Endoscopy (2021) 35:4427–4435 and Other Interventional Techniques

https://doi.org/10.1007/s00464-020-07943-4

Short‑ and long‑term outcomes of laparoscopic versus open lateral

lymph node dissection for locally advanced middle/lower rectal cancer
using a propensity score‑matched analysis
Jun Watanabe1 · Atsushi Ishibe2 · Yusuke Suwa1 · Mayumi Ozawa2 · Kazuya Nakagawa2 · Hirokazu Suwa3 ·
Mitsuyoshi Ota1 · Chikara Kunisaki1 · Itaru Endo2

Received: 14 May 2020 / Accepted: 25 August 2020 / Published online: 1 September 2020
© Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract
Background There are few reports on large-scale trials for the long-term outcomes regarding laparoscopic lateral lymph
node dissection (LLND). We evaluated the short- and long-term outcomes of laparoscopic versus open LLND for locally
advanced middle/lower rectal cancer using a propensity score-matched analysis.
Methods From January 2005 to December 2016, consecutive clinical stage II to III middle/lower rectal cancer patients who
underwent total mesorectal excision (TME) plus LLND were retrospectively collected at three institutions. Laparoscopic
LLND was compared with open LLND for the surgical and oncological outcomes, including the long-term survival, using
a propensity score-matched analysis.
Results A total of 325 patients were collected. There were 142 patients who underwent open TME plus LLND (open
group) and 183 patients who underwent laparoscopic TME plus LLND (laparoscopic group). A total of 93 patients each
were matched to each group. Compared to the open group, the laparoscopic group had a significantly longer operative time
(327 vs. 377 min; p = 0.002) but significantly less blood loss (540 vs. 50 ml; p < 0.001), fewer Clavian-Dindo grade ≥ 2
postoperative complications (49.5% vs. 34.4%; p = 0.037) and shorter postoperative hospital stay (18 vs. 14 days; p = 0.008).
Furthermore, the rate of urinary retention was significantly lower in the laparoscopic group than in the open group (16.1%
vs. 6.5%; p = 0.037). The estimated 3-year overall survival, relapse-free survival, and cumulative incidence of local recur-
rence were 91.4%, 73.1%, and 3.4% in the open group and 90.3%, 74.2%, and 4.3% in the laparoscopic group (p = 0.879,
0.893, 0.999), respectively.
Conclusions This study showed that laparoscopic LLND had advantages over an open approach, such as less blood loss,
fewer postoperative complications, and a shorter postoperative hospital stay, and the oncologic outcomes were similar to
the open approach. Laparoscopic LLND could be a viable standard approach to LLND for advanced middle/lower rectal
cancer surgery.

Keywords Rectal cancer · Laparoscopic surgery · Lateral pelvic lymph node · Long-term outcome · Lateral lymph node
dissection

Lateral lymph node metastasis (LLNM) has been reported
to be present in 16% to 23% of lower rectal cancer cases,
and the prognosis for these cases is generally poor [1–5].
Electronic supplementary material The online version of this
article (https​://doi.org/10.1007/s0046​4-020-07943​-4) contains
supplementary material, which is available to authorized users.
* Jun Watanabe
nabe‑jun@comet.ocn.ne.jp
Extended author information available on the last page of the article
However, the 5-year survival rate of cases in which R0 resec-
tion was possible was reported to be 40% to 50% [2, 3, 5–9].
The 5-year survival rate for LLND cases was better than
in non-dissection cases according to a propensity score-
matched analysis of T3 and T4 lower rectal cancer cases
[10]. Therefore, lateral lymph node dissection (LLND) has
been widely performed in Japan.
Although LLND is technically difficult and complicated,
Uyama et al. first reported the performance of LLND for
advanced low rectal cancer with a laparoscopic approach
in 2001 [11]. Since then, several retrospective studies on

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Vol.:(0123456789)
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laparoscopic LLND have been reported and have demon-
strated the safety and feasibility of laparoscopic LLND
according to the short-term outcomes [12–16]. However,
there have been few large-scale trials comparing open and
laparoscopic surgery for the long-term outcomes.
In the present study, we evaluated the short- and long-
term outcomes of laparoscopic versus open LLND for
locally advanced middle/lower rectal cancer using a pro-
pensity score-matched analysis.
Materials and methods
This retrospective, multicenter, case-matched study was
conducted to evaluate the short- and long-term outcomes of
laparoscopic versus open lateral pelvic lymph node dissec-
tion for locally advanced rectal cancer. From January 2005
to December 2016, consecutive patients who underwent total
mesorectal excision (TME) plus LLND were retrospectively
collected at three institutions of the Yokohama Clinical
Oncology Group (YCOG) in Japan. The study was approved
by the institutional review board for studies in humans of
each participating hospital. Due to the retrospective nature
of the study, written informed consent was not obtained. We
used the opt-out approach to disclose the study information.
This study was registered with the Japanese Clinical Trials
Registry (UMIN-CTR 000040406 [https​://www.umin.ac.jp/
ctr/index​.htm]).
The eligibility criteria were as follows: (1) histologically
proven middle or lower rectal cancer (2) clinical stage II to
III and (3) a history of TME plus LLND with curative intent.
The exclusion criteria were as follows: (1) a history of treat-
ment for other abdominal malignancy, (2) multiple primary
cancers, and (3) emergent cases. LLND was indicated in
patients with clinical stage II to III and patients with middle
or lower rectal cancer in which the lower edge of the tumor
was located distal to the peritoneal reflection. The choice
of surgical approach (open or laparoscopic) and whether
bilateral or unilateral LLND was performed were left to
the discretion of the institution or the individual surgeon.
Regarding preoperative treatment, patients who received
neoadjuvant chemotherapy underwent six cycles of mFOL-
FOX6. The doses of mFOLFOX6 were leucovorin 200 mg/
m2, oxaliplatin 85 mg/m2, bolus fluorouracil 400 mg/m2 on
day 1, and fluorouracil 2400 mg/m2 for a 46-h infusion).
Surgery was performed within 6 weeks after neoadjuvant
chemotherapy.
The main outcome was the percentage of postoperative
complications of Clavian-Dindo (CD) grade ≥ 2 within
30 days after surgery. Secondary outcomes were the dura-
tion of the operation, blood loss, conversion to open surgery,
postoperative complications (all grade and CD grade ≥ 3),
reoperation, mortality within 30 days after surgery, length
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Surgical Endoscopy (2021) 35:4427–4435
of hospital stays, pathological outcomes (p stage, proximal
margin and distal margin, positive rate of resection mar-
gin), and long-term outcomes (3-year overall survival [OS],
relapse-free survival [RFS], and cumulative incidence of
local recurrence). We obtained all the variable information
from the medical record.
We planned a study of independent cases and controls
with one control per case. Prior data indicated that CD
grade ≥ 2 postoperative complication rate for open group
was 0.5. If the CD grade ≥ 2 postoperative complication rate
for laparoscopic group was 0.3, the sample size was calcu-
lated to require 93 cases in each matched group and 186
cases in both groups to be able to reject the null hypothesis
that the failure rates for laparoscopic and open LLND were
equal with a probability (power) of 0.8. The type I error
probability associated with this test of this null hypothesis
was 0.05. We used an uncorrected chi-squared statistic to
evaluate this null hypothesis.
Laparoscopic LLND
The surgeons to participate in this study were qualified
based on the endoscopic surgical skill qualification system
of the Japan Society for Endoscopic Surgery (JSES) [17].
The laparoscopic surgery was performed using five ports: a
12-mm port in the umbilical region as a camera port, 5-mm
ports in the upper right, left, lower left quadrants, and a
12-mm port in the lower right quadrant. The regions with a
high frequency of LLNM were the internal iliac artery, the
internal pudendal artery and the obturator artery area. These
two areas were mainly dissected, and autonomic nerves were
completely preserved.
Follow‑up
The patient follow-up was conducted according to the Japa-
nese Society for Cancer of the Colon and Rectum Guide-
lines [18]. After hospital discharge, patients were followed
at the hospital as an outpatient every 3 months for the first
3 years, followed by every 6 months from 4 to 5 years by
tumor marker measurements (carcinoembryonic antigen and
carbohydrate antigen 19–9), every 6 months for the 5 years
by CT and every 1 year for 5 years by total colonoscopy.
Statistical analyses
Propensity score matching was performed using six factors:
sex, age, body mass index (BMI), tumor diameter, preopera-
tive treatment, and bilateral or unilateral LLND. Based on
these factors, we calculated the propensity score for each
patient with bivariate logistic regression. These propensity
scores were then used to match patients in the laparoscopic
group 1:1 with those in the open group (caliper = 0.2).
Surgical Endoscopy (2021) 35:4427–4435 4429

The data was presented as the median and interquartile Results

range (IQR). The SPSS Statistics 24 (SPSS Inc., Chicago,
IL, USA) software program was used for the statistical
analyses. Differences between categorical and continuous
variables were tested using Pearson’s chi-squared test and
the Mann–Whitney U test, respectively. The 3-year OS,
RFS, and cumulative incidence of local recurrence were
evaluated using the Kaplan–Meier method with the log-
rank test. All p values were 2-sided, and values less than
0.05 were considered statistically significant.
A total of 325 patients from three institutions were col-
lected. There were 142 patients who underwent open TME
plus LLND (open group) and 183 patients who underwent
laparoscopic TME plus LLND (laparoscopic group). Before
matching, significant differences were observed between
the two groups in terms of the tumor diameter, preoperative
treatment, and LLND laterality (Table 1). After propensity
score matching, all covariates were balanced, and no statisti-
cally significant differences were present between the open
group (n = 93) and the laparoscopic group (n = 93) (Table 1).

Table 1  Patient and tumor characteristics

Variable Overall cohort After matching
Open (n = 142) Laparoscopy (n = 183) p value Open (n = 93) Laparoscopy (n = 93) p value

Age (years)* 63 (57–69) 65 (57–71) 0.216 64 (59.5–71.5) 64 (58.5–70.0) 0.883

Gender
Male 91 (64.1) 126 (68.9) 0.365 59 (63.4) 61 (65.6) 0.759
Female 51 (35.9) 57 (31.1) 34 (36.6) 32 (34.4)
BMI (kg/m2)* 22.8 (19.9–24.3) 22.7 (20.1–24.5) 0.950 23.0 (20.5–24.8) 23.0 (20.5–24.8) 1.000
PS
0 137 (96.5) 180 (97.8) 0.467 89 (95.7) 89 (95.7) 1.000
1 5 (3.5) 4 (2.2) 4 (4.3) 4 (4.3)
Tumor diameter (mm)* 50.0 (35–60) 40.0 (30–50) < 0.001 45.0 (35–60) 45.0 (30–51) 0.375
Tumor location
Middle rectum 74 (52.1) 96 (52.5) 0.951 49 (52.7) 47 (50.5) 0.769
Lower rectum 68 (47.9) 87 (47.5) 44 (47.3) 46 (49.5)
Clinical stage
II 27 (19.0) 46 (25.1) 0.190 21 (22.6) 18 (19.4) 0.589
III 115 (81.0) 137 (74.9) 72 (77.4) 75 (80.6)
Clinical LLNM 25 (17.6) 36 (19.7) 0.636 14 (15.1) 17 (18.3) 0.555
Preoperative treatment
None 141 (99.3) 109 (59.6) < 0.001 92 (98.9) 92 (98.9) 1.000
Chemotherapy 1 (0.7) 74 (40.4) 1 (1.1) 1 (1.1)
Chemoradiotherapy 0 (0) 0 (0) 0 (0) 0 (0)
Type of procedure
Low anterior resection 104 (73.2) 145 (79.2) 0.324 69 (74.2) 77(82.8) 0.271
Abdominoperineal resection 31 (21.8) 32 (17.5) 22 (23.6) 16 (17.2)
Hartmann procedure 2 (1.4) 0 (0) 2 (2.2) 0 (0)
Total pelvic exenteration 5 (3.5) 6 (3.3) 0 (0) 0 (0)
Adjacent organs resected 12 (8.5) 14 (7.7) 0.792 5 (5.4) 7 (7.5) 0.767
Diverting ostomy 57 (40.1) 74 (40.4) 0.957 34 (36.6) 43 (46.2) 0.234
Lateral lymph node dissection
Bilateral 142 (100) 172 (94.0) 0.003 93 (100) 93 (100) 1.000
Unilateral 0 (0) 11 (6.0) 0 (0) 0 (0)

Values in parentheses are percentages, unless indicated otherwise

NIR near-infrared, BMI body mass index, PS performance status, ASA American Society of Anesthesiologists, UICC The Union for International
Cancer Control, LLNM lateral lymph node metastasis
*Values are median (interquartile range: 25–75th percentile)

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4430 Surgical Endoscopy (2021) 35:4427–4435

Table 1 shows the patient and tumor characteristics of the
entire cohort and the matched cases.
Table 2 shows the operative outcomes and postoperative
complications. Compared to the open group, the laparo-
scopic group had significantly longer operative times but
significantly less blood loss and transfusion. There was only
one case of conversion to open surgery in the laparoscopic
group. The rates of postoperative complications of all grades
and CD grade ≥ 2 was significantly lower in the laparoscopic
group (57.0% and 34.4%, respectively) compared to the open
group (73.1% and 49.5%, respectively). Furthermore, regard-
ing CD grade ≥ 2 postoperative complications, the incidence
of paralytic ileus, wound infection , and urinary retention
was significantly lower in the laparoscopic group than in
the open group. The rate of postoperative complications of
grade ≥ 3 did not differ significantly between the two groups,
and no mortality was observed in either group. The rate of
reoperation within 30 days after surgery did not differ signif-
icantly between the two groups. The length of postoperative
hospital stay was significantly shorter in the laparoscopic
group than in the open group. The postoperative adjuvant
chemotherapy rate was 32.3% in the open group and 46.2%
in the laparoscopic group, showing no significant difference
(p = 0.071).
Table 3 shows the pathological outcomes. Regarding
the p stage, rate of lateral lymph node metastasis, proximal
margin, distal margin, and positive rate of resection margin,
no significant differences were observed between the two
groups. The total number of lymph nodes harvested tended
to be higher in the open group than in laparoscopic group,
but there was no significant difference in the number of lat-
eral lymph nodes harvested between the two groups.
The median follow-up for matched patients was
55.6 months (IQR 45.8–66.0). The estimated 3-year OS
was 91.4% in the open group and 90.3% in the laparoscopic
group (p = 0.879) (Fig. 1). The 3-year RFS was 73.1% in the
open group and 74.2% in the laparoscopic group (p = 0.893)
(Fig. 2). Regarding local recurrence, the 3-year cumulative
incidence of local recurrence was 3.4% in the open group
and 4.3% in the laparoscopic group (p = 0.999) (Fig. 3).
Discussion
We conducted a multicenter retrospective case-matched
study to evaluate the short- and long-term outcomes of lap-
aroscopic versus open LLND for locally advanced middle/
lower rectal cancer using a propensity score-matched analy-
sis. This study was the first large-scale study to evaluate the
long-term results of laparoscopic LLND by comparing open
and laparoscopic surgery using propensity score matching.
In the short-term results, laparoscopic LLND showed sev-
eral advantages over open surgery, such as significantly less
blood loss, lower rates of blood transfusion, and postopera-
tive complications and a shorter postoperative hospital stay
despite a longer operative time. A previously reported meta-
analysis that included six studies of laparoscopic LLND,
including robotic surgery versus open LLND, showed a

Table 2  Operative outcomes Variable Open (n = 93) Laparoscopic (n = 93) p value

and postoperative complication
Operative time (min)* 327 (268–398) 377 (326–423) 0.002
Blood loss (ml)* 540 (300–1050) 50 (5–139) < 0.001
Transfusion 20 (21.5) 1 (1.1) < 0.001
Conversion to open surgery – 1 (1.1) –
Postoperative complication (All grade) 68 (73.1) 53 (57.0) 0.021
Postoperative complication (CD grade ≥ 2)
All 46 (49.5) 32 (34.4) 0.037
Anastomotic leakage 11 (11.8) 9 (9.7) 0.636
Ileus 14 (15.1) 5 (5.4) 0.029
Wound infection 13 (14.0) 4 (4.3) 0.022
Urinary retention 15 (16.1) 6 (6.5) 0.037
Urinary infection 3 (3.2) 3 (3.2) 1.000
Postoperative complication (CD grade ≥ 3) 19 (20.4) 13 (14.0) 0.244
Reoperation within 30 day after surgery 8 (8.6) 4 (4.3) 0.233
Mortality 0 (0) 0 (0)- –
Length of postoperative hospital stay (day)* 18 (14–26) 14 (12.5–22) 0.008
Adjuvant chemotherapy 30 (32.3) 43 (46.2) 0.071

Values in parentheses are percentages, unless indicated otherwise

NIR near-infrared, POD postoperative day
*Values are median (interquartile range: 25–75th percentile)

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Surgical Endoscopy (2021) 35:4427–4435 4431

Table 3  Pathological outcomes Variable Open (n = 93) Laparoscopic (n = 93) p value

p stage/yp stage
0 0 (0) 1 (1.1) 0.659
I 21 (22.6) 25 (26.9)
II 29 (31.2) 31 (33.3)
III 43 (46.2) 36 (38.7)
Pathological LLNM 9 (9.7) 11 (11.8) 0.636
Total lymph nodes harvested 37 (27.0–49.5) 28 (20.0–37.5) < 0.001
LLN harvested 15 (9.5–20.0) 11 (7.0–16.0) 0.104
Proximal margin (mm) 160 (134.5–220) 165 (137.5–201) 0.706
Distal margin (mm) 20.5 (12.25–35) 20 (10–32.5) 0.619
Positive rate of resection margin 3 (3.2) 3 (3.2) 1.000

Values in parentheses are percentages, unless indicated otherwise

NIR near-infrared, POD postoperative day
*Values are median (interquartile range: 25–75th percentile)

Fig. 1  Overall survival.

Kaplan–Meier curve for
comparison of OS. OS overall
survival

prolonged operative time, reduced blood loss and shortened
postoperative hospital stay [19]. These results were consist-
ent with those of our study.
In Western countries, LLND is less prevalent than Japan
because LLNM which extends beyond the internal iliac
region is considered a distant disease rather than a regional
disease [20]. Therefore, neoadjuvant chemoradiation therapy
(NACRT) followed by TME has become the standard treat-
ment for locally advanced lower rectal cancer. By contrast,
in Japan, LLNM is considered a regional disease [3, 16, 21].
The Japanese Society for Cancer of the Colon and Rectum
Guidelines 2019 suggests LLND for advanced rectal can-
cer patients with clinical T3-T4 as a treatment option. In
addition, it is strongly recommended to perform LLND in
cases suspected of lateral lymph node metastasis (LLNM)
[18]. In the JCOG0212 trial, the local recurrence rate was
significantly reduced by performing open LLND accord-
ing to long-term follow-up [22]. In a subgroup analysis, the
RFS of performing open LLND cases was significantly bet-
ter in clinical stage III than non-dissection cases [23]. Even
in patients treated with NACRT, which has been shown to
reduce the risk of local recurrence in many studies, the risk
of LLNM was shown to be greater if lateral lymphadenopa-
thy had been present before NACRT, and the local recur-
rence rate was reportedly as high as roughly 20% without
LLND [21, 24, 25]. Therefore, we consider that LLND is

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4432 Surgical Endoscopy (2021) 35:4427–4435

Fig. 2  Relapse-free survival.

Kaplan–Meier curve for com-
parison of RFS. RFS relapse-
free survival

Fig. 3  Cumulative incidence

of local recurrence. Kaplan–
Meier curve for comparison of
cumulative incidence of local
recurrence

important procedure even if NACRT is performed for locally
advanced middle/lower rectal cancer.
Regarding postoperative complications, the rate of
postoperative complication of CD grade ≥ 3 was 22% in a
randomized control led trial (JCOG0212 study) compar-
ing open rectal surgery with and without LLND [26]. This
value in the case-matched study by Yamaguchi et al. was
22.9% [16]. The incidence of postoperative complications
of CD grade ≥ 3 in the open group of the present study was
20.4%, which was consistent with the findings of previous
reports. In contrast, laparoscopic LLND was reported to be
associated with postoperative CD grade ≥ 3 rates of 9.3%
to 20.4%, and in the present study, this rate was 14.0% [16,
27, 28]. Furthermore, the rates of postoperative compli-
cations of all grades and CD grade ≥ 2 were significantly
lower in the laparoscopic group than in the open group,
demonstrating the advantages of laparoscopic LLND over
an open approach.

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Surgical Endoscopy (2021) 35:4427–4435
One issue with surgery for rectal cancer is that urinary
disorders and sexual dysfunction can be caused by damage
to the autonomic nerves, such as the pelvic plexus and pel-
vic splanchnic nerves, resulting in the deterioration of the
quality of life. Autonomic nerve-preserving LLND, which
has been developed in Japan, has enabled local control of
patients while avoiding this complication [2, 26, 29, 30].
Regarding the pathological outcomes, fewer total lymph
nodes were harvested in the laparoscopic group than in the
open group. In the management of colorectal cancer, an
adequate number of harvested lymph nodes are important
for accurate tumor staging and determining the patient prog-
nosis [31, 32]. The NCCN Guidelines Version 3.2020 rec-
ommends testing a minimum of 12 lymph nodes to establish
the N stage. In the present study, the median total number
of lymph nodes harvested was 28, and the median number
of lateral lymph nodes harvested was 11, indicating that this
result was acceptable.
Regarding the oncologic outcomes, the long-term out-
comes were similar between the laparoscopic and open
groups in the present study. The JCOG0212 trial showed
that local recurrence tended to be less common in the open
TME + LLND group than in the open TME-only group,
with recurrence occurring at a rate of 7.4% in the open
TME + LLND group and 12.6% in the open TME-only group
[22]. The actual LLNM rate in the LLND group was 7.0%.
In the present study, although the LLNM rate was 11.8% in
the laparoscopic group, the local recurrence rate was 4.3%
(4/93), indicating that lateral dissection may be effective in
controlling local recurrence for advanced rectal cancer.
Several limitations associated with the present study
warrant mention. First, although this study reduced the
selection bias by performing propensity score matching,
it was a retrospective study and not randomized. Second,
the median follow-up for matched patients was 55.6 months
(IQR 45.8–66.0), which is limited for adequately assessing
the long-term outcome. Third, the patients analyzed in this
study had not received NACRT. Whether or not laparoscopic
LLND will achieve similar results even after NACRT is
unclear at present. Therefore, further prospective, rand-
omized trials are needed to address these issues. However,
the authors believe that this report provides useful results
that will lead to future research.
Conclusion
This propensity score-matched study showed that, in the
short term, laparoscopic LLND had several advantages over
an open approach, such as less blood loss, fewer postop-
erative complications and a shorter postoperative hospital
stay, and the oncologic outcomes were similar to the open
approach. Laparoscopic LLND could be a viable standard
4433
approach to LLND for advanced middle/lower rectal cancer
surgery.
Compliance with ethical standards
Disclosures Drs. Jun Watanabe, Atsushi Ishibe, Yusuke Suwa, Mayumi
Ozawa, Kazuya Nakagawa, Hirokazu Suwa, Mitsuyoshi Ota, Chikara
Kunisaki, and Itaru Endo have no conflicts of interest or financial ties
to disclose.
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Surgical Endoscopy (2021) 35:4427–4435 4435

Affiliations

Jun Watanabe1 · Atsushi Ishibe2 · Yusuke Suwa1 · Mayumi Ozawa2 · Kazuya Nakagawa2 · Hirokazu Suwa3 ·
Mitsuyoshi Ota1 · Chikara Kunisaki1 · Itaru Endo2

1 3
Department of Surgery, Gastroenterological Center, Department of Surgery, Yokosuka Kyosai Hospital,
Yokohama City University Medical Center, 4‑57, Yokosuka, Japan
Urafune‑cho, Minami‑ku, Yokohama 232‑0024, Japan
2
Department of Gastroenterological Surgery, Yokohama City
University Graduate School of Medicine, Yokohama, Japan

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