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Gynecologic Oncology 90 (2003) 505–511 www.elsevier.com/locate/ygyno

Laparoscopic-assisted radical vaginal hysterectomy (LARVH):

prospective evaluation of 200 patients with cervical cancer
Hermann Hertel, M.D., Christhardt Köhler, M.D., Wolfgang Michels, Ph.D.,
Marc Possover, M.D., Roberto Tozzi, M.D., and Achim Schneider, M.D., M.P.H.*
Department of Gynecology, Friedrich Schiller University of Jena, Bachstrasse 18, D-07740 Jena, Germany

Received 27 February 2003

Abstract
Objective. The purpose of this study was to determine the survival of cervical cancer patients treated with laparoscopically assisted
radical vaginal hysterectomy (LARVH). We quantify morbidity and correlate survival with known risk factors.
Methods. Between August 1994 and June 2002, 200 patients with cervical cancer (TNM stage 1a1, L1 n ⫽ 6, 1a2 n ⫽ 21, 1b1 n ⫽ 89,
1b2 n ⫽ 26, 2a n ⫽ 11, 2b n ⫽ 45, 3a n ⫽ 1, 4 n ⫽ 1; squamous cell carcinoma 76.5%, adenocarcinoma 23.5%) were treated with LARVH
(type II n ⫽ 102, type III n ⫽ 98).
Results. Paraaortic lymphadenectomy was performed in 170 (85%) patients and pelvic lymphadenectomy was performed in all 200
patients. In 26 (13%) patients positive lymph nodes were found. Major intraoperative injuries occurred in 6% of patients. Postoperative
complications occurred in 8% of patients. Incidence of complications decreased significantly when comparing the first half with the second
half of patients. After a median follow-up time of 40 months, overall 5-year survival could be projected to 83%; 18.5% of patients
experienced recurrence with 35% exclusively extrapelvic and 11% of patients died of recurrence. Independent prognostic factors for
recurrence-free survival were tumor stage, lymph node status, and combined involvement of lymphovascular and angiovascular space. In
the absence of these risk factors projected 5-year survival was 98%.
Conclusion. Patients with tumor ⬍4 cm, negative lymph nodes, and the absence of the combination of angio- and lymphovascular space
involvement can be identified by laparoscopic staging and are ideal candidates for LARVH.
© 2003 Elsevier Inc. All rights reserved.

Keywords: Cervical cancer treatment; Laparoscopic-assisted radical vaginal hysterectomy; Survival

Introduction reintroduction of this type of surgery in combination with

Surgical treatment of patients with cervical cancer was
standardized 100 years ago by Schauta and his disciple
Wertheim in Vienna. Since only an abdominal approach
allowed removal of possibly affected regional lymph nodes,
the Wertheim operation prevailed. With the introduction of
laparoscopic lymphadenectomy radical hysterectomy got its
second chance. However, the Schauta operation has not
been done for more than 50 years in most institutions. Thus,
* Corresponding author. Department of Gynecology, Friedrich Schiller
University, Bachstrasse 18, 07740 Jena, Germany. Fax: ⫹49-3641-933064.
E-mail address: achim.schneider@med.uni-jena.de (A. Schneider).
laparoscopy was associated with a considerable learning
curve and the technique had to be standardized.
Several groups have performed a combination of a lapa-
roscopic and vaginal approach over the past 15 years [1– 6]
and for the community of gynecologic oncologists the most
important question arises: How safe is this operation with
respect to morbidity and cure? We developed and standard-
ized our own technique of laparoscopic-assisted radical vag-
inal approaches consistent with radicalness of a type II or
type III procedure [7–11]. In this study we focus on our
experience with survival, prognostic risk factors, and sur-
gery-associated short-term morbidity in patients with cervi-
cal cancer treated by a combined laparoscopic–vaginal ap-
proach.

0090-8258/03/$ – see front matter © 2003 Elsevier Inc. All rights reserved.
doi:10.1016/S0090-8258(03)00378-0
506 H. Hertel et al. / Gynecologic Oncology 90 (2003) 505–511
Patients and methods
Between August 1994 and June 2002, 268 consecutive
patients underwent primary surgery for cervical cancer
FIGO stage 1a1 L1 to 2b of which 200 patients were treated
by LARVH at the Department of Gynecology at the
Friedrich Schiller University of Jena, Germany. Permission
to study the laparoscopic assisted radical vaginal approach
for treatment of patients with cervical cancer was given by
the Ethical Committee of the Friedrich Schiller University
of Jena. During this period 30 patients with early stage
cervical cancer ⬍2 cm underwent laparoscopic lymphade-
nectomy and radical trachelectomy [12–14] to preserve fer-
tility. In 15 patients radical abdominal hysterectomy was
performed due to the following indications: pelvic lymph
node metastasis not resectable laparoscopically with intact
capsule n ⫽ 5, pregnancy n ⫽ 2, laparoscopic injury of
renal vein n ⫽ 1, large fibroid uterus n ⫽ 4, or no consent
for laparoscopic approach n ⫽ 3. In 23 patients laparoscopy
was used as staging procedure and advanced disease such as
positive lymph nodes matted together or intraabdominal
tumor spread, or tumor involvement of bladder and/or rec-
tum was found and patients underwent primary radiotherapy
or chemoradiation.
The technique of laparoscopic lymphadenectomy and
radical vaginal hysterectomy has been previously described
in detail [7–10]. LARVH type II was performed with re-
section of the parametria according to the original descrip-
tion of Schauta and Stoeckel [1,2], LARVH type III was
performed according to the Latzko–Meigs Mackenroth [11]
procedure. The decision for LARVH type III was made
when one or more risk factors for recurrence such as lateral
parametric involvement, adenocarcinoma, deep (⬎50%)
cervical infiltration on cone biopsy, MRI or sonography,
vascular space involvement in cone or biopsy, or young age
were present.
The approach was started with the laparoscopic evalua-
tion of the abdominal cavity to exclude macroscopic tumor
spread. The vesicocervical septum, rectal pillars, and cul-
de-sac were inspected to exclude obvious tumor involve-
ment. Laparoscopic lymphadenectomy was followed by
radical transvaginal hysterectomy. A nerve-sparing tech-
nique for LARVH type III was used from August 1997 on
[15]. Sentinel lymph node identification was performed
from December 1998 on using 99mTc-ALBU-RES and blue
dye (Patentblue) injection for detection [16].
In 102 (51%) patients LARVH type II and in 98 (49%)
patients LARVH type III was performed. Risk factors for
recurrence in patients with LARVH type III were advanced
FIGO stage (⬎1b1, n ⫽ 58/98; 59.2%), adenocarcinoma (n
⫽ 31/98; 31.6%), deep (⬎50%) cervical infiltration on cone
biopsy, MRI or sonography (n ⫽ 55/98; 56%), vascular
space involvement in cones or biopsy (L1/V1, n ⫽ 36/98;
36.7%), or young age (ⱕ35 years, n ⫽ 22/98; 22.4%).
Neoadjuvant chemotherapy had been given to 4 (2%)
patients (FIGO stage: 1b1 n ⫽ 1, 1b2 n ⫽ 2, 2b n ⫽ 1; 1⫻
Cisplatin/Ifosfamide, 3⫻ Carboplatin/Taxol/Etoposide).
Adjuvant therapy was performed as follows: chemotherapy
in 13 (6.5%) patients (TNM stage: 1b1 n ⫽ 1, 1b2 n ⫽ 4,
2a n ⫽ 2, 2b n ⫽ 5, 4 n ⫽ 1; 3⫻ Cisplatin/Ifosfamide, 1⫻
Navelbine/5FU, 1⫻. Carboplatin/Taxol, 7⫻ Carboplatin/
Taxol/Etoposide; 1⫻ Vepeside/Holoxane/Carboplatin), ra-
diochemotherapy (Platin- and 5-FU-based) in 19 (9.5%)
patients (TNM stage: 1b1 n ⫽ 3, 1b2 n ⫽ 5, 2a n ⫽ 1, 2b
n ⫽ 10). In 71 (35.5%) patients with TNM stage 1b1 n ⫽
30, 1b2 n ⫽ 8, 2a n ⫽ 6, 2b n ⫽ 26, 3a n ⫽ 1 radiotherapy
was performed: brachytherapy in 27 patients, teletherapy in
11 patients, and combined radiation in 33 patients.
Lymphovascular space involvement was analyzed by HE
staining and by immunohistochemical staining using CD 34
and factor VIII as marker. Blood vessels were diagnosed
when the lumen of the vessel contained erythrocytes.
The follow-up data were registered prospectively. Our
clinically planned follow-up time is 5 years. During the first
3 years clinical examination is done four times per year and
then two times per year. In patients not followed-up in our
institution, and patients with more than 5 years of follow-
up, data were collected from the responsible gynecologist
by mail or phone. Patient characteristics and intra- and
postoperative data were registered prospectively (SPSS
10.1, SPSS, Inc., Chicago, IL). The Kaplan–Meier method
was used to calculate overall survival and to compare prog-
nostic factors in terms of recurrence-free survival. Prognos-
tic factors were analyzed in a univariate analysis using log
rank test. A multivariate analysis was performed using Cox
regression and stepwise backward elimination according to
Wald criteria to prove independent prognostic factors for
recurrence-free survival. Chi-square test was used to com-
pare complication rates between the first and the second 100
patients.
Results
The median age of patients was 46 (17–78) years and
median weight was 65 (44 –108) kg with a median Quetelet
index of 25 (14 –38). Stage of disease (TNM) was distrib-
uted as follows: stage 1a1, L1 (n ⫽ 6), stage 1a2 (n ⫽ 21),
stage 1b1 (n ⫽ 89), stage 1b2 (n ⫽ 26), stage IIa (n ⫽ 11),
stage IIb (n ⫽ 45), stage IIIa (n ⫽ 1), and stage IV (n ⫽ 1).
Squamous carcinoma was found in 150 (75%), adenocarci-
noma in 47 (23.5%), and neuroendocrine carcinoma in 3
(1.5%) patients. Lymphovascular space involvement was
found in 14 (7%), angiovascular space involvement in 24
(12%), and the combination of lymphovascular and angio-
vascular space involvement in 17 (8.5%) patients.
In 34 (34.7%), of 98 patients LARVH type III was done
due to presence of one risk factor. More than one risk factor
occurred as follows: 2 in 29 (29.6%), 3 in 29 (29.6%), and
4 in 6 (6.1%) of 98 patients. Risk for recurrence in patients
treated with type III radical hysterectomy was higher com-
 H. Hertel et al. / Gynecologic Oncology 90 (2003) 505–511
Fig. 1. Recurrence-free survival after a median follow-up time of 40 (1–93)
months in 98 patients treated with LARVH type III and 102 patients treated
with LARVH type II.
pared with patients treated with type II radical hysterectomy
(P ⫽ 0.066) (Fig. 1).
The average duration of surgery was 333 (151–556) min.
The average duration for LARVH type II was 298 min, and
for LARVH type III 371 min (P ⫽ 0.0001). BSO was
performed in 119 (59.5%) patients. Decision for BSO de-
pended on histology (adenocarcinoma), stage, and/or meno-
pausal status. Sacrocolporectopexy was performed in 48
(24%) patients: 46 with type III/IV and 2 patients with type
II radical hysterectomy to prevent constipation. Paraaortic
lymphadenectomy was performed in 170 (85%) patients and
on average 8 (1–27) lymph nodes were removed. Pelvic
lymphadenectomy was performed in all 200 patients and on
average 22 (3–57) lymph nodes were removed. In 25
(12.5%) patients positive pelvic and in 1 (0.5%) patient
positive paraaortic lymph nodes were found. Sentinel lymph
node detection was performed in 60 (30%) patients and on
average 3 (0 –14) sentinel lymph nodes were detected. Ma-
jor intraoperative injuries occurred to the ureter n ⫽ 7
(3.5%), blood vessel n ⫽ 4 (2%), or bowel n ⫽ 1 (0.5%).
Minor intraoperative injuries of less than 1 cm length oc-
curred to the bladder while opening the cervico-vesical
space in 14 (7%) patients. All injuries were recognized and
managed during surgery.
Postoperative major complications were surgical revi-
sion n ⫽ 7 (3.5%), ureterostenosis n ⫽ 7 (3.5%), and
uretero/bladder-vaginal fistula n ⫽ 2 (1%). Laparoscopic
revision was done in 5 patients (3⫻ diffuse bleeding, 1⫻
bleeding from the medial rectal artery and cardinal liga-
ments, 1⫻ bladder leakage from a dislocated suprapubic
catheter). One patient underwent laparotomy for diffuse
507
bleeding, and transvaginal revision was performed in 1
patient due to a large serocele. The uretero- and one vesico-
vaginal fistula closed by conservative treatment after 4
weeks postoperatively. Minor postoperative complication
was fever in 14 (7%) patients. Blood transfusion was nec-
essary in 39 (19.2%) patients with a median of 2 blood units
(1–20). One patient with postoperative hemorrhage and
coagulopathy receive 20 blood units and 8 units of fresh
frozen plasma.
Long-term morbidity was percutaneous nephrostomy in
four patients and ureteral stents in three patients due to
ureterostenosis. Two patients developed bowel obstruction
which was treated by laparotomy in one patient and con-
servatively in the other patient; 65% of intra- and postop-
erative complications occurred during the first 100 LARVH
patients, compared to 35% of the second 100 LARVH
patients (P ⫽ 0.023).
In one patient primarily planned for LARVH conversion
to an abdominal approach was necessary due to severe
bleeding from the renal vein when starting laparoscopic
infrarenal lymphadenectomy. This patient was excluded
from evaluation. Conversion to laparotomy due to intraop-
erative complication was not necessary in any of the 200
patients. Bladder function was restored after a mean of 11
(1–50) postoperative days. Patients were discharged after 14
(5–32) days on average. The following complications oc-
curred after adjuvant radio- and or chemotherapy: ureter
stenosis n ⫽ 3 (1.5%), recto/uretero/bladder-vaginal fistula
n ⫽ 4 (2%), and bowel obstruction n ⫽ 1 (0.5%). Fistulas
closed after conservative treatment in two patients and were
surgically repaired in two patients. The patient with bowel
obstruction underwent laparotomy.
After a median follow-up time of 40 (1–93) months the
overall survival was ⬎36 months in 124 (62%) and ⬎60
months in 76 (38%) patients and projected to a 5-year
overall survival of 83% (Fig. 2). In 37 (18.5%) patients
recurrence occurred (pelvic n ⫽ 20, pelvic and extrapelvic
n ⫽ 4, extrapelvic n ⫽ 13) and 22 (11%) patients died of
recurrence.
Univariate statistical analysis showed that patients
with tumor TNM stage ⬎1b1 (Fig. 3, P ⬍ 0.0001), the
combination of lymphovascular and angiovascular space
involvement (Fig. 4, P ⬍ 0.0001) or lymph node metas-
tasis (n ⱖ 1) (Fig. 5, P ⬍ 0.0001), had a significantly
higher risk for recurrence in this cohort. The following
factors were evaluated as risk factors in terms of recur-
rence-free survival and showed no prognostic influence
(P ⬎ 0.05): tumor marker SCC (normal vs increased
level with a cutoff ⬎1.5 ng/ml), histologic subtype (ad-
eno vs squamous), histologic grading (G1 vs G2 vs G3),
or age (ⱕ35 years vs ⬎35 years).
Multivariate statistical analysis proved that tumor stage
(P ⫽ 0.002), lymph node metastasis (P ⬍ 0.0001), or
combination of lymphovascular and angiovascular space
508 H. Hertel et al. / Gynecologic Oncology 90 (2003) 505–511
Fig. 2. Survival after a median follow-up time of 40 (1–93) months in 200
patients treated with LARVH type II or III.
involvement (P ⬍ 0.0001) were independent prognostic
factors for survival in this cohort. The projected overall
5-year survival was 98% for patients (n ⫽ 110) lacking the
combination of the three independent risk factors identified
in this study (Fig. 6).
Adjuvant radiotherapy was performed in 29 (26.4%) of
the 110 patients: brachytherapy in 12 patients, teletherapy in
4 patients, and combined radiation in 13 patients.
Fig. 3. Recurrence-free survival after a median follow-up time of 40 (1–93)
months in 200 patients treated with LARVH type II or III according to
tumor stage.
Fig. 4. Recurrence-free survival after a median follow-up time of 40 (1–93)
months in 200 patients treated with LARVH type II or III according to
tumor spread in the angiovascular and/or lymphovascular space.
Discussion
Radical abdominal hysterectomy with pelvic and possi-
bly paraaortic lymphadenectomy represents the surgical
standard procedure for patients with FIGO stage I–II cervi-
cal cancer. Laparoscopic lymphadenectomy in combination
with vaginal radical hysterectomy is used as alternative
Fig. 5. Recurrence-free survival after a median follow-up time of 40 (1–93)
months in 200 patients treated with LARVH type II or III according to
lymph node involvement.
 H. Hertel et al. / Gynecologic Oncology 90 (2003) 505–511
Fig. 6. Survival after a median follow-up time of 44 (1– 89) months in 110
patients stage 1a-1b1 without independent risk factors.
surgical strategy. Experiences of various surgeons showed
that a laparoscopic-assisted approach in patients with gyne-
cologic malignancies is associated with low morbidity, little
blood loss, good cosmetic results and, early recovery [17–
20]. Spirtos and co-workers published a series of stage
1a2-1b cervical cancer patients treated with laparoscopic
radical hysterectomy (type III) and report a 10.3% recur-
rence rate (n ⫽ 8) measured after a median follow up time
of 66.8 months. Adjuvant treatment was done in 5 (9%)
patients. A 93.6% 5-year survival was projected in this
study [21]. When matching for tumor stage in our study 14
(10.3%) recurrences occurred in 136 comparable patients
(stage 1a2-1b2) with 52 patients (38.2%) receiving adjuvant
treatment and median follow up of 36 (1– 88) months.
Delgado et al. [22] published survival data in a group of 645
patients with stage 1 squamous cervical cancer treated by a
radical abdominal approach. The 3-year disease-free inter-
val ranged from 94.8% in patients with tumor size ⱖ3 mm
to 59.5% in patients with tumor size ⱖ21 mm. The overall
survival was 80% in this study. Thus, the 3-year results of
Delgados study are comparable with the results of the study
of Spirtos and our series. Magrina [23] summarized survival
rates of stage 1b cervical cancer patients after radical ab-
dominal hysterectomy in a metaanalysis of seven publica-
tions and found a total 5-year survival rate of 85.7% (80 –
90%). Artman et al. [24] published a series of 153
conventionally treated stage 1b cervical cancer patients with
a 5-year survival rate of 84%. Additionally, an 83% 5-year
survival rate in a group of 309 cervical cancer patients
(stage 1a-2b) was reported by Trimbos et al. [25]. In our
study of 200 cervical cancer patients the projected 5-year
509
survival after a median follow-up time of 40 months was
83%. Thus, in comparing our survival rates with those of
studies using the abdominal approach, there seems to be no
obvious advantage for either approach.
We compared the perioperative morbidity of our study
with results of other studies performing radical hysterec-
tomy for cervical cancer treatment. Magrina [23] described
complication rates of 1.1–7.4% associated with the radical
abdominal approach. Usually bladder, ureter, rectum, or
blood vessels are involved. In 78 patients with successfully
completed laparoscopic approach Spirtos et al. [21] de-
scribed an intraoperative morbidity of 6.4%: bladder injury
n ⫽ 3, blood vessel injury n ⫽ 2. In 5 (6%) of 84 patients
conversion to laparotomy was necessary due to of surgical
problems in 2 patients, bladder injury in one patient, and
vessel injury in 2 patients. In our cohort intraoperative
problems occurred more frequently (bladder injury n ⫽ 14,
7%, ureter injury n ⫽ 7, 3.5%, blood vessel injury n ⫽ 4,
2%, bowel injury n ⫽ 1, 0.5%). Conversion to laparotomy
was not necessary in all our patients since all complications
were managed transvagnially or laparoscopically. Raatz and
Börner [26] describe experiences of 71 patients with stage
1a2-2b cervical cancer treated with laparoscopic-assisted
radical vaginal hysterectomy. Intraoperative complications
occurred as bladder injury in 3 (4.2%) patients, ureteral
injury in 3 (4.2%) patients, and blood vessel injury 1 (1.4%)
patient. In our cohort major postoperative complications
occurred as ureterostenosis (3.5%), urinary fistula (1%), and
ileus (1%). The incidence of complications is compareable
to those of other studies of radical abdominal hysterectomy
(Table 1).
Looking at the learning curve the incidence of compli-
cations decreased significantly in our series when compar-
ing the first half with the second half of patients. This
related mainly to injury of bladder or ureter since we dis-
sected part of the vesico-cervical ligament laparoscopically
and identified the ureter by the click maneuver [10] with
higher accuracy.
Another aim of this study was to compare results with
known risk factors in terms of recurrence-free survival (tu-
mor stage, lymphovascular/angiovascular space involve-
ment, lymph node metastasis, tumor marker SCC, histologic
subtype, histologic grading, age) as identified by various
studies with univariate and multivariate analyses (Table 2).
TNM stage, positive lymph nodes were associated with a
significantly worse prognosis as described by others [22,
27–31]. Additionally, we found that the combination of
angio- and lymphovascular space involvement was an in-
dependent risk factor (P ⬍ 0.0001), but the presence of
lymphovascular space involvement alone was not sufficient
for predicting recurrence. In order to evaluate angio- and
lymphovasculare space involvement sufficient large punch
biopsy must be taken for histopathological evaluation by the
gynecopathologist prior to surgical staging. When involve-
ment of angio- and lymphovascular space has been ruled
out, the tumor is evaluated as FIGO 1b1, and the laparo-
510 H. Hertel et al. / Gynecologic Oncology 90 (2003) 505–511

Table 1
Review of the literature comparing perioperative morbidity associated with radical hysterectomy for cervical cancer by different approaches

Laparoscopic approach Abdominal approach

This Spirtos Raatz and Magrina Artman Massi Magrina Mirhashemi
study et al. [21] Bömer [26] [23] et al. [24] et al. [33] et al. [34] et al. [35]

Patients (n) 200 78 71 Metaanalysis of 7 studies 137 228 375 106

Bladder injury (%) 7 3.8 4.2 0.4–4.3 N/A N/A N/A N/A
Ureter injury (%) 3.5 0 4.2 3.5 N/A N/A N/A N/A
Bowel injury (%) 1 0 0 1.4–2.1 N/A N/A 1.5 N/A
Blood vessel injury (%) 2 2.6 (serious) 1.4 3.3 N/A 0.9 N/A N/A
Ureteral stenosis (%) 3.5 0 3.75 1 3.6 1.3 0.3 N/A
Urinary fistula (%) 1 1.3 1.4 2.1 2.6 1.8 0.6 N/A
Ileus (%) 1 0 0 N/A 1.6 N/A 4 8.5
Blood transfusion (%) 19.2 1.3 42 N/A 92 N/A N/A 32
No. of blood units given (n) 2 N/A N/A N/A 3.25 N/A 2 N/A
Mortality (%) 0 0 0 0.7 0 0.8 0 0

Note. N/A, not available in the study.

scopic evaluation of pelvic lymph nodes (combined with Acknowledgments

sentinel technique) confirms negative lymph nodes the three
independent risk factors identified in this study are lading. We appreciate the assistance of Mrs. Kathleen Polte in
These patients are ideal candidates for LARVH. Addition- data collection and monitoring.
ally, in the patients (n ⫽ 110) lacking the three independent
risk factors, the overall incidence of perioperative compli-
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