Surgical Oncology 27 (2018) 380e386

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Surgical Oncology
journal homepage: www.elsevier.com/locate/suronc

Surgical and oncological outcomes of an improved nerve-sparing

radical hysterectomy technique: 6 years of experience at two centres*
Sheng Yin a, 1, Si-Ning Ma a, 1, Yu-Qin Zhang a, Ting-Yan Shi a, Li-Bing Xiang b, Yu-Lan Ren b,
Rong-Yu Zang a, *
a
Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, Zhongshan Hospital, Fudan University, China
b
Department of Gynecologic Oncology, Fudan University Cancer Hospital, China

a r t i c l e i n f o a b s t r a c t

Article history: Objective: An improved nerve-sparing radical hysterectomy (NSRH), which is based on the paravesico-
Received 27 March 2018 vaginal space, has been recently introduced in a phase II, prospective clinical trial by our team. This
Received in revised form study aims to report the surgical and oncological outcomes of this improved NSRH.
3 May 2018
Methods: One hundred seventy-seven consecutive patients were enrolled in our study and underwent
Accepted 10 May 2018
the improved NSRH. The proportion of successful catheter removal and postvoid residual urine volume
(PVR) of 50 mL or less at postoperative day 7 or day 4 was used to assess surgical outcomes. The local
Keywords:
control rate (LCR), disease free survival (DFS), and overall survival (OS) were used to assess oncological
Cervical cancer
Nerve-sparing
outcomes.
Survival Results: Postoperative 30-day complications occurred in 27/177 (15.3%) patients. The rate of successful
catheter removal and PVR of 50 mL or less were 85.2% (23/27) and 66.7% (18/27) at postoperative day 7,
and 73.3% (110/150) and 35.3% (53/150) at postoperative day 4. A total of 13 (7.9%) patients showed
recurrence after a median follow-up time of 39.2 months (range 3.2e68.1 months). The estimated 2-year
and 5-year DFS rates were 92.2% and 91.1%, respectively. Seven (4.2%) patients presented local recur-
rence, and five (3.0%) patients were dead at the end of the follow-up period. The estimated 5-year LCR
and OS were 95.1% and 96.2%, respectively. In univariate analysis, International Federation of Gynecology
and Obstetrics (FIGO) stage, lymphovascular space invasion (LVSI), and lymph node metastasis were
found to be the prognostic risk factors of DFS. Patients with LVSI were associated with a worse DFS
according to the multivariate analysis.
Conclusions: The improved NSRH in our study may provide better surgical outcomes without compro-
mising the survival in patients with early cervical cancer.
© 2018 Elsevier Ltd. All rights reserved.

1. Introduction
Bladder dysfunction remains a major postoperative challenge
for patients with early-stage cervical cancer. Female pelvic neuro-
anatomy has shown that damage to the hypogastric nerves, pelvic
splanchnic nerves, and the inferior hypogastric plexus (IHP),
*
The study has been presented at the 5th Biennial Meeting of the Asian Society
of Gynecologic Oncology (ASGO 2017), Nov. 30-Dec.2, 2017, Tokyo, Japan.
* Corresponding author. Division of Gynecologic Oncology, Department of Ob-
stetrics and Gynecology, Zhongshan Hospital, Fudan University, 180 Fenglin Road,
Shanghai, China.
E-mail addresses: ryzang@yahoo.com, ryzang@163.com, zang.rongyu@zs-
hospital.sh.cn (R.-Y. Zang).
1
SY, SNM Contributing equally as the first authors.
especially the bladder branch of the IHP, is the cause of impaired
bladder function [1]. Preservation of the pelvic autonomic nerves
can shorten the duration of postoperative catheterisation (DPC),
thus improving the patients' quality of life.
Since the Japanese gynaecologist described the first nerve-
sparing technique in radical hysterectomy [2], an increasing num-
ber of international investigators have reported their experience
with preserving the autonomic nerves [3e5]. In 2008, Querleu and
Morrow [6] described NSRH as type C1 in the new classification of
surgery for early cervical cancer. However, with the development of
nerve-sparing surgery, no consensus has been reached on the
technique, especially the preservation of the bladder branch of the
IHP, until now. Moreover, as more favourable surgical outcomes of
NSRH have been reported compared with the conventional radical
hysterectomy (CRH), the oncologic outcomes of NSRH received

https://doi.org/10.1016/j.suronc.2018.05.015
0960-7404/© 2018 Elsevier Ltd. All rights reserved.
 S. Yin et al. / Surgical Oncology 27 (2018) 380e386
more attention by surgeons. Although several studies including
some randomised controlled trials showed a similar rate of survival
of NSRH compared with CRH, inadequate evidence addressing the
oncological safety of nerve-sparing surgery have been collected due
to the various techniques applied and the different study designs in
previous reports [7e10].
We found a new clinical anatomy, the paravesico-vaginal space,
in our practice of the NSRH since 2006 [11,12]. Radical hysterectomy
was proved simpler when incorporating the paravesico-vaginal
space into nerve-sparing procedures. In our prospective study
(ClinicalTrials.gov Identifier: NCT02562729) [13], 49 patients were
enrolled and received the improved NSRH between September
2015 and August 2016. The bladder catheter was routinely removed
on postoperative day 4. Thirty-four (69.4%) patients had successful
catheter removal on postoperative day 4, and 17 (34.7%) patients
had a PVR less than 50 mL.
In this present cohort study, we aimed to report the surgical and
oncological outcomes of the improved nerve-sparing technique in a
large number of patients.
2. Methods
2.1. Patients
A multicentre, exploratory study was conducted in Zhongshan
Hospital and Cancer Hospital, Fudan University between November
2011 and August 2016. A total of 177 patients were included, with
115 patients undergoing the improved NSRH between November
2011 and May 2014 in Fudan University Cancer Hospital, and 62
patients undergoing the improved NSRH in Zhongshan Hospital,
Fudan University, in which 49 patients were enrolled in a pro-
spective study (ClinicalTrials.gov Identifier: NCT02562729) [13].
Patients who were diagnosed with International Federation of
Gynecology and Obstetrics (FIGO) stage Ib1 or IIa1 cervical cancer,
and who were aged between 18 and 70 years and with no neo-
adjuvant chemotherapy, were included. A flowchart of patient
population was shown in Fig. 1. Adjuvant concurrent chemo-
radiotherapy (CCRT) or CCRT followed by chemotherapy using
cisplatin was administered to patients with more than two
intermediate-risk factors including pathological tumour size
greater than 4 cm, stromal invasion of 50% or higher and lymph-
vascular space invasion (LVSI); or more than one high-risk factor
including lymph node metastasis, parametrial invasion and posi-
tive resection margin. In individual cases, adjuvant radiotherapy or
chemotherapy alone was offered. All the patients signed informed
consent.
2.2. Surgical techniques
Radical hysterectomy with or without salpingo-oophorectomy
following pelvic lymphadenectomy was performed in all the pa-
tients. Procedures of hypogastric nerve preservation in our
improved NSRH were the same as in the conventional NSRH. Sur-
gical procedures to identify the paravesico-vaginal space were
performed in three steps as reported in our previously published
paper [13] and Supplementary Fig. 1. The cardinal ligament was
dissected using Ligasure after we connected the paravesico-vaginal
space with the para-rectal space by blunt or sharp dissection
(Supplementary Fig. 2).
2.3. Assessment of postoperative bladder function
In the initial period of performing the improved NSRH (11/11/
2011-04/18/2012), we removed the catheter at postoperative day 7.
The results were beyond expectation; thus, we were able to remove
381
the catheter at postoperative day 4 in the second part of our study
(04/24/2012-8/23/2016). The proportion of successful catheter
removal and postvoid residual urine volume (PVR) of 50 mL or less
at postoperative day 7 or day 4 was calculated to assess the post-
operative bladder function. The PVR was measured by ultrasound
after spontaneous voiding. Patients who were unable to void
spontaneously or voided with difficulty underwent re-
catheterisation, and we would attempt to remove the catheter
again on postoperative day 14.
2.4. Data collection and follow-up
Radicality and survival were evaluated by LCR, DFS, and OS.
Disease local control was defined as patients who survived without
any signs of vaginal or pelvic recurrence according to the regular
gynaecological examination and imaging scans. For each patient,
medical records were abstracted for age at surgery, body mass in-
dex (BMI), FIGO stage, histology, operative time, estimated blood
loss, pathology, postoperative 30-day morbidity and mortality,
adjuvant therapy, DPC, PVR, LCR, DFS, and OS. BMI values were
classified according to the World Health Organization (WHO)
criteria [14]. All patients were followed up every 3 months after the
surgery for the first 2 years and every half year thereafter with a
physical gynaecological examination, tumour marker (squamous
cell carcinoma antigen) tests, and abdominal-pelvic ultrasound
imaging. Vaginal cytology, computed tomography (CT), magnetic
resonance imaging (MRI), and positron emission tomography
(PET)-CT would also be performed if indicated. The follow-up
period ended on August 16, 2017.
2.5. Statistical analysis
Statistical analysis was performed using the SPSS software
package for Windows (Statistical Package for the Social Sciences
19.0, SPSS Inc, Chicago, IL). The LCR, DFS, and OS rates were eval-
uated using the Kaplan-Meier method. Prognostic factors associ-
ated with the DFS were determined using the log-rank test and the
Cox proportional hazards regression model. A P-value of <0.05 was
considered to be statistically significant.
3. Results
3.1. Baseline and patient characteristics
A total of 177 consecutive patients were evaluable for this study.
The patient characteristics are shown in Table 1. The median patient
age was 48 years (range 25e70 y). Fourteen patients were cat-
egorised as underweight (BMI<18.5); 121 patients were normal
weight (BMI: 18.5e24.9); 37 patients were obese class I (BMI:
25e29.9); and 5 patients were obese class II (BMI
30). One hun-
dred forty-five (82.0%) patients were diagnosed with stage Ib1, and
32 (18.0%) with stage IIa1 cervical cancer. Histology results showed
152 (85.9%) cases of squamous cell carcinoma, 14 (7.9%) cases of
adenocarcinoma, and 8 (4.5%) cases of adenosquamous carcinoma.
3.2. Surgical outcomes
The median operative time was 76 min (range 32e340 min), and
the median blood loss was 200 mL (range 50e2200 mL). For the
postoperative pathology, 25 (14.1%) patients presented large
tumour size (>4 cm). Seventy-eight (44.1%) and 87 (49.2%) patients
were diagnosed with LVSI and deep stroma invasion, respectively.
Thirty-five (19.8%) patients presented lymph node metastasis, and
both positive surgical margin and parametrial invasion were found
in two (1.1%) patients, respectively.
382 S. Yin et al. / Surgical Oncology 27 (2018) 380e386
Fig. 1. The flowchart of patient population.
Postoperative complications within a 30-day period occurred in
27/177 (15.3%) patients. No grade III-V morbidity or mortality was
reported according to the Memorial Sloan-Kettering Cancer Center
(MSKCC) surgical secondary events grading system. The most
common complication was pelvic infection (n ¼ 11, 6.2%). Five
(2.8%) patients had urinary tract infection. Four patients had
postoperative haemorrhage, and one patient had an intraoperative
haemorrhage with an estimated blood loss of 2200 mL. The details
of the 30-day postoperative complications are listed in
Supplementary Table 1.
3.3. Postoperative bladder function
In 27 patients whose catheter was removed on postoperative
day 7, the catheter was successfully removed in 23 (85.2%) patients.
Only four (14.8%) patients were re-catheterised, and the catheters
of these four patients were successfully removed on postoperative
day 14. The PVR was 50 mL or less in 18 (66.7%) patients, and only 2
(7.4%) patients had a PVR greater than 200 mL (Supplementary
Table 2).
Of the 150 patients whose catheter was removed at post-
operative day 4, the catheter was successfully removed in 110
(73.3%) patients, and 40 (26.7%) patients were re-catheterised. In
the 110 patients who underwent successful catheter removal, 53
(48.2%), 46 (41.8%), and 11 (10.0%) had a PVR of 50 mL or less,
50e200 mL, and greater than 200 mL, respectively (Fig. 2A). In the
40 patients who were re-catheterised, 34 (22.7%) patients under-
went a successful catheter removal at postoperative day14,
whereas 6 (4.0%) patients required a longer catheterisation. The
longest DPC was 24 days. The median PVR was 100 mL (range
0e800 mL) on postoperative day 4. As shown in Fig. 2B, PVR was
50 mL or less in 53 (35.3%) patients, and all these patients under-
went successful catheter removal. Among the 52 (34.7%) patients
with a PVR of 50e200 mL, 6 patients had difficulty voiding and
were re-catheterised. A total of 45 (30.0%) patients had a PVR of
greater than 200 mL, and 10 of them reported satisfactory mictu-
rition and were not re-catheterised.
3.4. Local control rate, disease-free survival, and overall survival
Overall, 12 (6.8%) patients were lost to follow-up. The median
follow-up time was 39.2 months, ranging from 3.2 to 68.1 months.
A total of 13 (7.9%) patients had recurrence, in which 12 (92.3%)
patients had recurrence within 2 years after primary treatment. The
estimated 2-year and 5-year DFS rates were 92.2% and 91.1%,
respectively (Fig. 3A). Seven (4.2%) patients were diagnosed with
local recurrence, in which five patients had pelvic recurrence, and
two patients were diagnosed with vaginal recurrence. Six (3.6%)
patients had distant recurrences. The sites of relapse were as fol-
lows: two supra-clavicular metastasis, two pulmonary, one bone,
and one para-aortic lymph node metastasis. Five patients died
during the follow-up period, as follows: three from distant recur-
rence, one from local recurrence, and one from bone marrow
suppression after chemotherapy (Table 2).
The characteristics of patients with recurrence are shown in
Table 3. The estimated 5-year LCR and OS rate were 95.1% and
 S. Yin et al. / Surgical Oncology 27 (2018) 380e386 383

Table 1 96.2%, respectively (Fig. 3B and C).

Clinical and pathological characteristics. In univariate analysis, FIGO stage, LVSI, and lymph node
Characteristics (n ¼ 177) N (%) metastasis were found to be the prognostic risk factors of DFS
Age, median (range), years 48 (25e70)
(Supplementary Table 3). Both pathological tumour size greater
Body mass index than 4 cm and stroma invasion 50% or greater showed a trend for a
< 18.5 14 (7.9) worse DFS. Patients with LVSI were associated with a worse DFS
18.5e24.9 121 (68.4) according to the multivariate analysis (hazards ratio (HR): 5.350;
25e29.9 37 (20.9)
95% confidence interval (CI): 1.088e26.314; P ¼ 0.039)

30 5 (2.8)
FIGO stage, n (%) (Supplementary Table 4).
Ib1 145(82.0)
IIa1 32 (18.0)
Histology
4. Discussion
Squamous cell carcinoma 152(85.9)
Adenocarcinoma 14(7.9) In our previous study, we have reported the anatomy of the
Adenosquamous carcinoma 8 (4.5) paravesico-vaginal space and its anatomic boundaries, and
Othersa 3 (1.7)
demonstrated the efficacy and safety of the improved NSRH.
Operative time, median (range), min 76(32e340)
Estimated blood lose, median (range), mL 200 (50e2200) Herein, we aimed to introduce the surgical outcomes of the
Pathological tumour size improved NSRH technique in a large cohort of patients. The rate of
 4 cm 152(85.9) PVR of 50 mL or less (35.3% vs. 34.7%) and the proportion of suc-
> 4 cm 25 (14.1) cessful catheter removal (73.3% vs. 69.4%) at postoperative day 4
LVSI
Yes 78(44.1)
was similar in this cohort of patients when compared with our
No 99(55.9) prospective study. In addition, we presented the oncological out-
Stroma invasion comes of patients who underwent the improved NSRH.
< 50% 90 (50.8) The median operative time in this study was 77.0 min (range

50% 87 (49.2)
32.0e340.0 min), which is the shortest operative time compared
Lymph node metastasis
None 142(80.2) with previous NRSH procedures. In addition to the simplified
Yes 35 (19.8) nerve-sparing technique due to the novel surgical landmark, the
Positive surgical margin 2 (1.1) energy-based surgical devices combining cutting and coagulation
Parametrial invasion 2 (1.1) may also contribute to the shortened surgical time. The median
Postoperative therapy
RT 1 (0.6)
blood loss was 200 mL (range 50e2200 mL). No intraoperative
CCRT 44 (24.9) complication of grade III-V morbidity or mortality was reported.
CCRT followed by chemotherapy 17 (9.6) These results indicated that our improved NSRH procedures may be
CT 7 (4) easy and safe for the fellow in training.
None 105 (59.3)
Despite the growing number of studies addressing the post-
NA 3 (1.7)
operative bladder function of NSRH, only a few previous studies
Abbreviations: FIGO, International Federation of Gynecology and Obstetrics; LVSI, conducted a catheter removal at postoperative day 3e5. In a study
lymphovascular space invasion. RT: radiotherapy; CCRT: concurrent chemo-
radiation; CT: chemotherapy; NA: not available.
from Charoenkwan [15], a PVR of less than 50 mL presented in 2 of
a
Two cases of small cell carcinoma of cervix, one case of cervical adenoid basal 22 (9.1%) patients at postoperative day 4. In Kavallaris' study [16],
carcinoma. 32 patients underwent laparoscopic NSRH, and the catheter was

Fig. 2. Surgical outcomes of 150 patients whose catheter was removed on postoperative day 4.
A. Duration of postoperative catheterisation (DPC); B. Postvoid residual urine volume (PVR).
384 S. Yin et al. / Surgical Oncology 27 (2018) 380e386

Fig. 3. Oncological outcomes of the 177 patients with stage Ib1 and IIa1 cervical cancer undergoing the improved NSRH.
A. Disease-free survival; B: local control rate; C: overall survival rate. The median follow-up time was 39.2 months, ranging 3.2e 68.1 months. Twelve (6.8%) patients were lost to
follow-up.

Table 2 removed at postoperative day 3. They reported that the residual

Recurrence and survival data. urine volume was less than 50 mL in all patients. According to the
Event N ¼ 165a report by Raspagliesi [17], a total of 23 patients underwent the
Local recurrence
NSRH using the Cavitron Ultrasonic Surgical Aspirator (CUSA), and
Pelvic 5(3.0%)b the catheter was removed on postoperative day 4. Nine (39.1%)
Vaginal 2(1.2%) patients had a PVR of less than 100 mL. In this study, the proportion
Distant recurrence of PVR of 50 mL or less was 35.3% on postoperative day 4. Inter-
Pulmonary 2 (1.2%)c
estingly, there are obvious differences between the proportions of
Supra-clavicular 2 (1.2%)d
Bone 1 (0.6%)e successful catheter removal (73.3%) and PVR of 50 mL or less
Para-aortic lymph node 1 (0.6%) (35.3%) in this study, which may suggest that a PVR of 50 mL or less
Death for cause cannot accurately assess bladder function recovery in patients who
Died of distant metastasis 3 (1.8%)
received the improved NSRH.
Died of other cause 1 (0.6%)f
Died of local recurrence 1 (0.6%)
Although a number of studies have showed that the short- and
a
long-term survival of NSRH do not differ from those of conventional
A total of 177 patients underwent the NSRH, and 12 (6.8%) pa-
radical hysterectomy, radicality after the nerve-sparing technique
tients were lost to follow-up.
b
One of the patients was died of the disease. still represents a controversial issue [9,18]. Because our study did
c
Two patients were diagnosed with adenosquamous carcinoma. not include a control group with patients who underwent the
One patient died of the disease, and the other was lost to follow-up. conventional radical hysterectomy, we compared the local recur-
d
One of the patients died of the disease.
e
rence rate and DFS of our study with the previous literature data.
The patient died.
f
The patient died of bone marrow suppression after adjuvant
Only two studies with a large number of patients and a long follow-
chemotherapy. up period were found. In a study from van den Tillaart, 122 cervical

Table 3
Characteristics of patients with recurrence.

Characteristics Patients with recurrence N ¼ 13 Patients with local recurrence N ¼ 7

FIGO Stage
Ib1 (145) 8 (5.5%) 4 (2.8%)
IIa1 (32) 5 (15.6%) 3 (9.4%)
Histology
Squamous cell carcinoma (152) 10 (6.6%) 6 (3.9%)
Adenocarcinoma (14) 1 (7.1%) 1 (7.1%)
Adenosquamous carcinoma (8) 2 a (25.0%) 0
Pathological outcomes
Pathological tumour size > 4 cm (25) 4 (16.0%) 2 (8.0%)
LVSI (78) 11 (14.1%) 6 (7.7%)
Stroma invasion (87) 9 (10.3%) 3 (3.4%)
Lymph node metastasis (35) 7 (20.0%) 3 (8.5%)
Positive surgical margin (2) 1 (50.0%) 0
Parametrial invasion (2) 0 0
Treatment
Surgery (105) 4 (3.8%) 3 (2.9%)
Surgery þ adjuvant therapy (69) 9 (13.0%) 4 (5.8%)

Abbreviations: FIGO, International Federation of Gynecology and Obstetrics; LVSI, lymphovascular space invasion.
a
Both of the patients had pulmonary metastasis.
 S. Yin et al. / Surgical Oncology 27 (2018) 380e386
cancer patients with FIGO stage Ia to IIa received the NSRH. A total
of 24 (19.6%) patients had recurrence within 2 years of follow-up,
and the local recurrence rate was 8.3% [19]. In a study by Ditto,
170 cervical cancer patients with FIGO stage Ib1 to III received the
nerve-sparing procedure. A total of 22 (12.9%) patients had recur-
rence within a median follow-up period of 31 months, and the local
recurrence rate was 10% (17/170) [20]. In our study, 7.9% (13/165)
patients had recurrence, and the local recurrence rate was 4.3% (7/
165) with a median follow-up time of 39.2 months. These data
demonstrate that the radicality was not compromised when per-
forming our improved nerve-sparing technique, despite that our
study may include patients with relatively low FIGO stages.
Although Querleu and Morrow classified the nerve-sparing
technique as the type C1 radical hysterectomy, how to select pa-
tients for NSRH has not been proven to date. Some researchers
showed that the NSRH could be proposed to all cervical cancer
patients who were surgical candidates [21], whereas others
concluded that NSRH should be considered primarily for patients
with small tumours due to the low risk of parametrial and lymph
node involvement, which benefit the patients without necessi-
tating postoperative radiation [18]. To date, several studies have
shown that the nerve-sparing technique can be performed in
locally advanced cervical cancer (LACC). However, few can really
assess the impact of the nerve-sparing approach in influencing
survival outcomes in LACC [22]. In a study of Yang [23], they
concluded that laparoscopic NSRH is a feasible and safe procedure
for bulky cervical cancer (
6 cm) after neoadjuvant chemotherapy,
whereas they did not show survival data. A recent study concluded
that the 5-year DFS and OS were not affected by the nerve-sparing
approach in patients with FIGO stage Ib2-III, whereas they also
mentioned that their study was underpowered because of the small
sample size and relative short-term follow-up [24]. Thus, it is
valuable to conduct a study with relatively large scale to investigate
the oncologic outcomes of the nerve-sparing approach in patients
with indications.
Ideal surgical management of cervical cancer should reduce
early and late morbidity without compromising oncological out-
comes. In our study, type C1 radical hysterectomy, the standard
treatment for patients with cervical cancer with FIGO stage Ib1, was
performed according to the National Comprehensive Cancer
Network (NCCN) guideline. Several literature have presented that
the local recurrence rate and OS were comparable between type B
and type C radical hysterectomy for low-risk early staged cervical
cancer [25e27], whereas the former has far fewer complications
than the latter. However, the so-called “low risk” factors, such as
“tumour size of 2 cm or less, a pathological grade 1 to 2, and a less
than 50% stromal invasion, were not warranted. Further in-
vestigations should be conducted by large-scale prospective clinical
trials.
There are several limitations of our study. One was that we did
not include a subset of patients who underwent the conventional
radical hysterectomy during the same period to serve as a control
group. Another limitation was that we evaluated only the early
postoperative bladder function in the patients. A long-term period
of follow-up on bladder function may also be necessary. Finally, as
all the improved nerve-sparing surgeries in our study were per-
formed by laparotomy, further studies should be conducted to
ascertain whether our technique could also be applied in the
laparoscopic surgery.
In conclusion, the improved NSRH in our study may ameliorate
the surgical outcomes without compromising the survival in pa-
tients with early cervical cancer. Further studies should be con-
ducted to investigate the favourable candidates of this improved
NSRH, and to ascertain its feasibility in a laparoscopic surgery.
385
Declaration of interests
The authors declared no conflicts of interest.
Appendix A. Supplementary data
Supplementary data related to this article can be found at
https://doi.org/10.1016/j.suronc.2018.05.015.
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