Gynecologic Oncology 131 (2013) 347–351

Contents lists available at ScienceDirect

Gynecologic Oncology
journal homepage: www.elsevier.com/locate/ygyno

Surgical practice of UK gynaecological oncologists in the treatment of

primary advanced epithelial ovarian cancer (PAEOC):
A questionnaire survey
D.P.J. Barton ⁎, T. Adib, J. Butler
Department of Gynaecological Oncology, Royal Marsden Hospital, London, UK

H I G H L I G H T S

• We highlight variability in self reported surgical practice in the management of advanced ovarian cancer in the UK.
• Shorter operating times and lower rates of upper abdominal procedures and lymphadenectomies were associated with lower cytoreduction rates.
• This may explain the lower survival of UK advanced stage ovarian cancer patients compared to similar countries.

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

Article history: Objective. To assess the routine surgical practices of consultant gynaecological oncologists (CGOs) in the
Received 18 April 2013 United Kingdom in their management of primary advanced (FIGO stages III and IV) epithelial ovarian cancer
Accepted 3 August 2013 (PAEOC).
Available online 13 August 2013 Methods. The same anonymised questionnaire was sent twice to all consultant gynaecological oncologists
(CGOs) working in the UK. The questions enquired about surgical practice of the previous calendar year and
Keywords:
the respondents were asked to describe their usual or typical management of patients with PAEOC.
Surgical practice
Ovarian cancer
Results. 45 of 85 CGOs responded (53%). The mean number of ovarian cancer cases operated on by an individual
Optimal cytoreduction surgeon was 47 (range 6–100). 6% of the surgeons never perform pelvic lymphadenectomy, and 22% of the sur-
Gynaecological oncologists geons never perform para-aortic lymphadenectomy in the primary surgery (PS) group, compared to 8% and 30%
in the neoadjuvant chemotherapy (NAC) group. In the PS group 17% of the respondents perform pelvic lymphad-
enectomy routinely (80% or more of patients) compared to 11% of the respondents in the NAC group. The rates of
bowel surgery and surgery for upper abdominal disease were highly variable. The average operating time per case
was less than 3 h in 78% of the respondents.
Conclusions. The mean operating times, caseload, and types of procedure undertaken in the management of ad-
vanced ovarian cancer provide compelling evidence that in many UK cancer centres the surgical goal has not been
complete cytoreduction. These data have implications for the centralisation of surgical services, subspecialty train-
ing, and the lower survival of UK patients compared to other comparable countries.
© 2013 Elsevier Inc. All rights reserved.

Introduction
Ovarian cancer is the most lethal gynaecologic malignancy account-
ing for 6800 new cases and around 4300 deaths per year in the United
Kingdom, ranking as the fourth most common cause of cancer-related
deaths [1]. The most common histologic subtype is epithelial (EOC).
Ovarian cancer survival is lower in the UK than comparable countries
and this appears due to the poor survival of UK patients with advanced
stage disease [2–4]. The most important predictor of survival in ad-
vanced stage (International Federation of Obstetrics and Gynaecology
(FIGO) stages III and IV) primary EOC is the volume of residual disease
⁎ Corresponding author.
E-mail address: Desmond.Barton@rmh.nhs.uk (D.P.J. Barton).
after debulking surgery [5]. The ability to perform effective debulking
surgery often requires extensive upper abdominal resections, bowel re-
sections, pelvic lymphadenectomy and para-aortic lymphadenectomy.
Evidence from the SCOTROC-1 trial study suggests that UK compared
to non-UK ovarian cancer patients receive less extensive surgery and
are less likely to undergo optimal or complete cytoreductive surgery;
hence, we would argue that as a direct consequence of this surgical ap-
proach survival is lower [6]. There are currently no robust methods of
assessing the quality of ovarian cancer surgery in the UK and we set
out to assess the management and approach to advanced ovarian cancer
surgery in the UK by gynaecological oncologists against both national
and international comparisons. It has been proposed that lower UK
ovarian cancer survival may be due to a less radical approach to surgery
than other better performing countries and this study examines and

0090-8258/$ – see front matter © 2013 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.ygyno.2013.08.007
348 D.P.J. Barton et al. / Gynecologic Oncology 131 (2013) 347–351
compares self reported practice by UK consultant gynaecological oncol-
ogists (CGOs) [3].
Methods
We designed a questionnaire based on the typical pre-operative,
intra-operative and post-operative features of patients with presumed
or confirmed PAEOC. To avoid confusion, to keep the questionnaire
user-friendly and to simplify data interpretation in a relatively small
targeted group, no distinction was made between complete lymph
node dissection and lymph node sampling. The questions were presented
on one A4 page, using both sides. The answers were in the yes/no/don't
know format, or as percentages (to the nearest 5%) of the usual or typical
clinical practice of the CGOs (see Appendix). The questionnaires were
unmarked and anonymised responses were requested. The work ad-
dresses of all known practising CGOs in the UK were determined from
a database of gynaecology oncology cancer centres and each was sent
with the questionnaire in a personally addressed letter with a stamped
self-addressed envelope. This process was repeated one more time,
with the second letter sent about three months after the first with in-
structions not to respond to the second questionnaire if the CGO had
responded to the first questionnaire.
Results
Of 85 CGOs identified as practising in the UK, 26 responded on the
first round, and 19 on the second with a total of 45 (52.9%) respondents.
Not all respondents answered all questions. The average number of ad-
vanced ovarian cancer cases annually was 47 (median 45, range, 6–100)
(Fig. 1). Most surgeons' (24/41, 58%) average operating time was be-
tween 2 and 3 h (58%), with 8 (20%) reporting average times less than
2 h, and nine (22%) 3 or more hours (Fig. 2). An average of 37.4% of
the patients received neoadjuvant chemotherapy (median 30%, range
0–95%) prior to debulking surgery (Table 1).
The average proportion of patients receiving specific procedures
at primary debulking surgery (PDS) and neoadjuvant chemotherapy
(NAC) respectively were: pelvic node dissection: 27.6%, 20.8%, para-
aortic node dissection: 23.8%, 19.2%, bowel resection: 12.8, 13.5%,
stoma formation: 7.5%, 6.6%, splenectomy 0.6%, 1.4%, and diaphragmatic
stripping 2.7%, 5.7%. Pelvic lymphadenectomy was never performed by
6 of 35 respondents (17%) in PDS and 8 (22%) after NAC. Para-aortic
lymphadenectomy was never performed by 9 of 35 respondents
(26%) in PDS and 11 (37%) after NAC. A small number of surgeons per-
form lymphadenectomy regularly in the PDS group (that is, in 80–100%
of their cases) 6/35 (17%) perform pelvic lymphadenectomy and 4/35
(11%) perform para-aortic lymphadenectomy. Patients in the NAC
group underwent pelvic lymphadenectomy in 80–100% of the time by
4/37 (11%) of the surgeons, and underwent para-aortic lymphadenec-
tomy by 4/37 (11%) of the surgeons. Overall the rates for both bowel re-
section and stoma formation were low, but were higher for the PDS
group. 2/37 (5%) of the respondents in the PDS group and 5/37 (14%)
110
100
90
80
Cases per year
70
60
50
40
30
20
10
0
Fig. 1. Annual surgeon caseload of advanced ovarian cancer per year (thick line median,
narrow line interquartile range).
in the NAC group never perform bowel resections. 6/37 (16%) in the
PS group and 9/37 (24%) in the NAC group never raised a stoma in
any patients. Just over half of the respondents (57% in the PDS group
and 51% in the NAC group) perform bowel resections in up to 10% of
the patients.
The number of respondents who never performed splenectomy in
the PS group was 20/36 (72%) and 10/37 (46%) in the NAC group. Ap-
proximately 30% of the surgeons in both groups perform diaphragmatic
stripping and 3% are doing so in 100% of the patients in the NAC group.
95% of the surgeons routinely document the sites and volume of any
residual disease and 100% document the extent of surgical cytoreduction.
Complete cytoreduction (no visible or palpable residual disease)
was achieved in an average of 35.6% PDS patients and 42.6% NAC pa-
tients, residual disease of b 1 cm in 47.3% of PDS patients, 55.6% of
NAC patients, and residual disease b 2 cm in 57.7% of PDS patients, and
63.2% of NAC patients. 9/35 (26%) of the respondents achieved complete
surgical cytoreduction in 70–80% of cases in the PS group whereas 16/33
(48%) of the respondents achieved levels of no residual disease in 70–
80% of cases in the NAC group. 4/34 (12%) of the respondents reported
never achieved complete cytoreduction in the PDS group, and 7/34
(21%) reported never achieving this in the NAC group. Surgical
cytoreduction to b1 cm diameter residual disease was achieved in 70–
80% of cases by 8/35 (23%) of the respondents in the PDS group. The
same level of cytoreduction was achieved by 11/33 (33%) of the respon-
dents in the NAC group.
Longer average operating times were associated with higher rates of
complete cytoreduction in both PDS and NAC patients (Figs. 2 and 3).
For the 8 surgeons (20%) with average operating times less than 2 h,
complete cytoreduction rates were 14% (PDS) and 12.1% (NAC), for
the 24 (58%) with operating times of 2 to 3 h rates were 35.8% (PDS)
and 45.8% (NAC), and for the 8 surgeons with operating times of 3 to
4 h rates were 58.3% (PDS) and 63.3% (NAC).
A correlation with complete debulking in PDS was present with
higher rates of pelvic lymphadenectomy (p = 0.020), para-aortic
lymphadenectomy (p = 0.008), splenectomy (p = 0.056), diaphrag-
matic stripping (p = 0.039) and residual disease b2 cm (p = 0.014)
or b1 cm (p = 0.025). For NAC patients complete cytoreduction was
associated with higher rates of splenectomy (p = 0.0034), and residual
disease b2 cm (p = 0.0529) or b1 cm (p = 0.0427) (Table 2).
Discussion
This survey has found a wide range in the surgical management of
PAEOC amongst consultant gynaecological oncologists in the UK. The
high caseload and relatively short median operative times are notewor-
thy and may be inter-related — that is with a restricted operating time
and a larger case load, the median operating time is low. As complete
cytoreductive surgery cannot be completed in less than 4 h in most
patients with advanced stage disease, the data on operating times
provide evidence that the surgical goal in many centres the UK is not
complete cytoreduction. This is likely to directly contribute to the poor
outcomes in UK ovarian cancer patients. The numbers of cases operated
on per year varied widely with a median of 45. There is evidence that
surgical workload is important to maintain skills, reduce complication
rates and maximise surgical endeavour, in order to achieve a high rate
of optimal or complete cytoreduction [7–9]. In the peer review of cancer
centres in the UK the benchmark for each individual gynaecological on-
cologists is 15 new cases per year [10]. In another report a minimum of
21 cases per institution per year was recommended [8]. In our study
higher caseload was not associated with greater rates of complete
cytoreduction for either PDS (p = 0.316) or NAC (p = 0.979). This
may in part be due to the lower rates of cytoreduction for surgeons
with lower average operative times, for example, the majority of sur-
geons (32/41, 78%) have average operating times of 3 h or less with
an average complete cytoreduction rate of 30.8%, compared to 54.3%
for the nine (22%) surgeons with average operating times of 3 or more
 D.P.J. Barton et al. / Gynecologic Oncology 131 (2013) 347–351 349

average complete cytoreduction rates (%) % of surgeons (n = 41)

70

60

50

40

30

20

10

0
<2 2 to 3 3 to 4 >4
average complete cytoreduction
12.1 45.8 63.3 45
rates (%)
% of surgeons (n = 41) 19.5 58.5 19.5 2.4

Fig. 2. Average operating time (hours) and complete cytoreduction rates (PDS).

hours. Chi et al. reported a significant increase in operative times asso- Table 1
ciated with an increase in optimal (b1 cm) cytoreduction rates from Summary of results.

46% to 80% following a paradigm shift in surgical approach, in particular Response rate 45/85 (52.9%)
to the upper abdomen. In their series 52% of the patients had operative Caseload (number per year)
times of greater than 4 h in the later group compared to 25% in the ear- Average 46.5
Median 45
lier group [11]. The recent EORTC study reported median operative
Min 6
times for advanced stage ovarian cancer of 165 (up front surgery) and Max 100
180 min (neoadjuvant chemotherapy) with complete cytoreduction Patients receiving NAC (%)
rates of 19.4% and 51.2% respectively [12]. In contrast Braicu et al. re- Average 37.4
Median 30
ported the outcomes of 632 ovarian cancer patients including 446
Min 0
(74.2%) in stages III–IV and complete cytoreduction rates of 69.2% Max 95
with a median operative time of around 4 h (251 min, range 34–592) Average operating time (hours)
[13]. b2 8/41 (20%)
It is therefore important that caseload alone is not used as a marker 2–3 24/41 (58%)
3–4 8/41 (20%)
of quality in ovarian cancer surgery and arguably operative time is a
N4 1/41 (2%)
useful surrogate for radicality of surgery.
Responses to our questionnaire show that a median of 37% of the pa- PDS NAC
tients received neoadjuvant chemotherapy. Approximately two thirds (average %) (average %)
received 3 cycles and one third received more than 3 cycles of chemo- Infra-colic omentectomy 80.3 71.4
therapy. We did not ask what chemotherapeutic agents were used, Supra-colic omentectomy 53.3 54.5
but UK-based practice would be carboplatin +/− paclitaxel. The rates Pelvic lymphadenectomy/lymph node sampling 27.6 20.8
Para-aortic lymphadenectomy/lymph node sampling 23.8 19.2
of neoadjuvant chemotherapy appear high in a time period before the Bowel resection 12.8 13.5
publication of the EORTC trial, and may reflect a less aggressive surgical Stoma raised 7.5 6.6
approach to advanced disease [12]. Splenectomy 0.6 1.4
Although the response rate (53%) was lower than surveys of practice Diaphragmatic stripping 2.7 5.7
Residual disease b2 cm 57.7 63.2
in the USA (61%), Europe (63%) and Australia/New Zealand (81%), the
Residual disease b1 cm 47.3 55.5
total number of cases reported by the 37 surgeons who reported case- No residual disease 35.6 42.6
load was 1909. This is therefore likely to report the surgical manage-
ment of the majority of advanced stage ovarian cancer patients in the PDS NAC
UK [14–16]. Never perform pelvic lymphadenectomy/lymph node 6/35 (17%) 9/35 (26%)
Since Griffiths published data demonstrating that the extent of sampling (number, % of respondents)
surgery was proportional to the overall survival in ovarian cancer, Never perform para-aortic lymphadenectomy/lymph 8/37 (22%) 11/37 (30%)
node sampling (number, % of respondents)
cytoreductive surgery has remained one of the cornerstones of the
350 D.P.J. Barton et al. / Gynecologic Oncology 131 (2013) 347–351

average complete cytoreduction rates (%) % of surgeons (n = 41)

70

60

50

40

30

20

10

0
<2 2 to 3 3 to 4 >4
average complete cytoreduction
14 35.8 58.3 30
rates (%)
% of surgeons (n = 41) 19.5 56.1 19.5 2.4

Fig. 3. Average operating time (hours) and complete cytoreduction rates (NAC).

management of PAEOC [17]. Initial stage of disease, extent of The issue of pelvic and/or para-aortic lymph node sampling and dis-
cytoreduction and response to platinum-based chemotherapy are the section remains controversial. From the questionnaire responses it
main predictors of survival. The definition of maximal cytoreduction seems reasonable to infer that the respondents were generally of the
has changed over the years, from less than 2 cm in maximal diameter, view that resection of the nodes achieved little and this correlates with
to more recently being defined as no (visible) residual disease, which the low rates of complete cytoreduction. Fournier et al. have shown
has a consistent effect of improving disease free survival, overall survival that para-aortic lymph nodes are involved in up to 94% of the cases of
and disease-specific survival [5,18,19]. Of the important prognostic fac- ovarian cancer, and these are best detected when a full lymph node dis-
tors in PAEOC only the extent of surgical cytoreduction can be influenced section is performed, rather than lymph node sampling [24]. There were
by medical intervention. Our study showed that 34% of the respondents no significant differences in incidence of lymph node involvement be-
were achieving complete cytoreductive rates in only 25% of their patients tween the upfront surgery and neoadjuvant chemotherapy groups in
and only 13% of the surgeons achieved no visible residual disease in 75% that study. Nevertheless, the role of radical lymphadenectomy has
or more of cases overall. been questioned not on the grounds of technique but in regard to mor-
There was a higher optimal cytoreduction rate in NAC-treated pa- bidity and patient benefit [20].
tients compared to the PS group. However, many patients in both Radical pelvic surgery with visceral resection is a well established
groups did not have the retro-peritoneal nodes resected (sampled or practice amongst gynaecological oncologists for ovarian cancer to re-
block-dissected). move all visible pelvic disease. Yet only relatively recently has this
There was substantial variation in the management of pelvic and surgical goal in the pelvis also been considered the goal for upper ab-
para-aortic lymph nodes in both groups. This is to be expected due to dominal disease. In part this reflected the lack of surgical experience
the controversy regarding the role of lymphadenectomy in advanced of gynaecological oncologists in operating in the upper abdomen. The
ovarian cancer surgery [20–23]. addition of radical upper abdominal surgery have seen optimal and
complete cytoreduction rates rise to over 75%. Chi et al. report that pro-
cedures such as splenectomy, distal pancreatectomy, liver resection and
diaphragmatic stripping resulted in cytoreduction to less than 1 cm in
more than 90% of the patients. Of great importance is that such
Table 2
Correlation of complete cytoreduction and operative procedures, p (spearman rank
cytoreduction significantly improved disease free interval and disease
correlation). specific survival [25]. Our study shows that few gynaecological oncolo-
gists in the UK are performing radical (upper abdominal) procedures in
Parameter PDS NAC
the majority of cases. Furthermore not all patients in the UK are operat-
Pelvic LN 0.02 0.73 ed by CGO and therefore the proportion of ovarian cancer patients re-
Para-aortic LN 0.01 0.11
ceiving radical procedures will be underreported in this survey. This
Bowel resection 0.71 0.18
Stoma raised 0.53 0.19 finding is not unique to the UK — there is variation in practice amongst
Splenectomy 0.06 b0.01 gynaecological oncologists in the United States, in Europe, and in
Diaphragmatic stripping 0.04 0.49 Australia and New Zealand [14–16].
Caseload 0.32 0.98
These reports on surgery for advanced ovarian cancer and the find-
Residual disease b2 cm 0.01 0.05
Residual disease b1 cm 0.03 0.04
ings of our study suggest that the concept of complete cytoreduction
Infra-colic omentectomy 0.06 0.02 has not been widely accepted. For example, in our study the rates of
Supra-colic omentectomy 0.57 0.17 node sampling/dissection (pelvic and para-aortic), the percentage of
PDS = primary debulking surgery, NAC = neoadjuvant chemotherapy. The bold complete cytoreduction (no visible disease), the lack of a fixed retrac-
emphasis is p b 0.05 tion system in most surgical practice, the rate of diaphragmatic
 D.P.J. Barton et al. / Gynecologic Oncology 131 (2013) 347–351
stripping and the response that 78% of the surgeons spend less than 3 h
operating per case suggest that for many surgeons the goal is not com-
plete cytoreduction. We would argue that what is important is striving
surgically to achieve complete cytoreduction, rather than who achieves
this — be this the gynaecological oncology team or in conjunction with
other surgical colleagues.
The data from our study have been generated by an anonymised
questionnaire. We acknowledge that there are inherent problems such
as poor recall, and retrospective personal bias. But there are, we believe,
some important findings. It is evident that most cancer centres in the UK
do not have and/or maintain a surgical database. The surgical community
is struggling with quality control and there is a need for surgical
management of primary advanced EOC to be standardised after the
centralisation of ovarian cancer services. This study reports the practice
of gynaecological oncologists in the UK for a time period (2006) for
which we now have mature survival data. The evidence from this study
supports the hypothesis that the surgical approach to advanced ovarian
cancer by gynaecological oncologists in the UK is less radical than from
that of countries with better outcomes in ovarian cancer. To improve
ovarian cancer survival in the UK there needs to be greater access to rad-
ical surgery. Although this may be provided in different models of health
care provision is probably best achieved by greater centralisation of sur-
gery to centres able to achieve high complete cytoreduction rates, and a
system that supports the longer operative times that this approach re-
quires. Self-reported high caseload does not correlate to improved out-
comes in the UK setting which may reflect lack of ability or belief in
radical surgery to achieve complete cytoreduction for ovarian cancer,
and caseload should not be used as the only surrogate for quality in the
UK setting.
Conflict of interest statement
The authors declare that there are no conflicts of interest.
Appendix A. Supplementary data
Supplementary data to this article can be found online at http://dx.
doi.org/10.1016/j.ygyno.2013.08.007.
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