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Specialist surgery for ovarian cancer in England
YGYNO-975825; No. of pages: 7; 4C: Gynecologic Oncology xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Gynecologic Oncology journal homepage: www.elsevier.com/locate/ygyno
Specialist surgery for ovarian cancer in England John Butler a,⁎, Carolynn Gildea b, Jason Poole b, David Meechan b, Andrew Nordin c,d a
Department of Gynaecological Oncology, Royal Marsden Hospital, London SW3 6JJ, UK Public Health England Knowledge & Intelligence Team (East Midlands), 5 Old Fulwood Road, Sheffield S10 3TG, UK c East Kent Gynaecological Centre, East Kent Hospitals University NHS Foundation Trust, QEQM Hospital, St Peters Road, Margate, Kent, UK d Gynaecological Site Specific Clinical Reference Group (SSCGR), National Cancer Intelligence Network (NCIN), 5th Floor, Wellington House, 133-155 Waterloo Road, London SE1 8UG, UK b
H I G H L I G H T S • In 1999 national guidance recommended centralisation and specialisation of ovarian cancer surgery. • Specialist surgery and centralisation for ovarian cancer in England have increased from 2000 to 2009. • Survival has also increased.
a r t i c l e
i n f o
Article history: Received 5 June 2014 Accepted 4 March 2015 Available online xxxx Keywords: Ovarian cancer Surgery Specialist Gynaecological cancer centres Gynaecological oncologist
a b s t r a c t Objective. The aim of this study is to evaluate the impact of the 1999 national recommendations for ovarian cancer surgery in England to be performed by specialist surgeons in specialist centres. Methods. A retrospective analysis of English cancer registry records, Hospital Episode Statistics (HES) data for all English NHS providers and General Medical Council (GMC) sub-specialty accreditation, to consider changes to the annual proportion of ovarian cancer (ICD10 C56-C57) patients undergoing major gynaecological surgery in gynaecological cancer centres (GCCs) or by specialist gynaecological oncologists (GOs). Results. From 2000 to 2009, 2428 consultants were responsible for surgery on 30,753 patients. There were significant increases in the proportions of patients undergoing surgery at GCCs (43% to 76%, P b 0.001), by GMC accredited GOs (5% to 36%, P b 0.001), and by high ovarian cancer caseload (≥18 cases) surgeons (22% to 56%, P b 0.001). Conclusion. There have been increased centralisation and specialisation of surgery for ovarian cancer patients since the NHS Cancer Plan (2000) and there has also been improved survival. However, by 2009, many ovarian cancer patients were still not receiving specialist surgery; the majority of patients were not operated on by GMC accredited gynaecological oncologists and there was considerable regional variation. Systems of accreditation should be reviewed and trusts should ensure that HES data accurately records clinical activity. © 2015 Elsevier Inc. All rights reserved.
1. Introduction Ovarian cancer is the fifth most common female malignancy and most lethal gynaecological malignancy with approximately 5750 new diagnoses and 3500 deaths each year in England [1]. Ovarian cancer survival in England and the UK has been persistently lower than other comparable countries [2–5] and this appears to be due to differences in treatment rather than adverse stage distribution or late diagnosis [6]. The Calman Hine Report (1995) [7] recommended the centralisation of cancer services and the formation of cancer networks, and these have been formally established since the NHS Cancer Plan [8]. In 1999, the Department of Health published the Improving Outcomes Guidance (IOG) in Gynaecological Cancers recommending that “Surgery for ⁎ Corresponding author. E-mail address: [email protected] (J. Butler).
ovarian cancer should be carried out by specialised gynaecological oncologists at Cancer Centres” [9]. 1.1. Specialised gynaecological oncologists It has been estimated that 478 lives a year could be saved if UK ovarian cancer survival matched the best in Europe [10]. After stage at diagnosis, the most important determinant for ovarian cancer survival is the volume of residual disease after staging surgery [11]. In comparison to general gynaecologists and general surgeons, gynaecological oncologists and high volume surgeons are more likely to completely resect all disease, perform a lymphadenectomy and treat patients according to guidelines [12], and have lower in-hospital mortality resulting in improved survival [13,14]. In the United Kingdom, there have been specialist training programmes in gynaecological oncology, accredited by the Royal
http://dx.doi.org/10.1016/j.ygyno.2015.03.003 0090-8258/© 2015 Elsevier Inc. All rights reserved.
Please cite this article as: Butler J, et al, Specialist surgery for ovarian cancer in England, Gynecol Oncol (2015), http://dx.doi.org/10.1016/ j.ygyno.2015.03.003
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J. Butler et al. / Gynecologic Oncology xxx (2015) xxx–xxx
College of Obstetricians (RCOG), since 1984. This is a two or three year fellowship programme completing a syllabus or specialised training in accredited gynaecology oncology centres [15]. Surgeons completing such approved UK programmes are accredited as gynaecology oncology sub-specialists by the General Medical Council (GMC). Other surgeons having completed training programmes overseas may also be listed as sub-specialists by the GMC. The GMC accreditation is not comprehensive, as many surgeons recognised nationally and internationally as very experienced gynaecological oncologists, and responsible for training and supervising sub-specialist trainees, are not listed as subspecialists. The British Gynaecological Cancer Society (BGCS) proposed that a gynaecological oncologist is a surgeon who works in a designated gynaecological cancer centre and spends 75% or more of their clinical sessions in gynaecological oncology. It has also proposed that surgical caseload is a key parameter for benchmarking performance [16]. These proposals have not been formalised and the BGCS does not maintain a register of gynaecological oncology specialists. Neither is there an international standard of what constitutes an adequate caseload for a gynaecological oncologist. Vernooij et al. defined case volumes as low (≤ 6 per year), intermediate (7–12 per year) and high (N12 per year) [17]. Bristow et al. defined low as b10 per year and high as ≥10 [18]. 1.2. Specialised gynaecological cancer centres It has been shown that outcomes in many cancers are improved when care is performed in specialised centres [19–22]. Ovarian cancer treated in high volume hospitals has been associated with increased likelihood of cytoreduction, shorter length of stay, and lower hospitalrelated cost of care [14]. The combination of high volume hospital and high volume surgeon is an independent predictor of improved disease specific survival [18]. Centralisation of care in specialist gynaecological oncology centres enables management by specialist multidisciplinary teams (MDTs) including integration of specialist medical, surgical and clinical oncology, radiology and nurse specialist services. It ensures continuity of care and improves the information provided to patients. Additionally, it advances expertise in specialist radical ovarian cancer surgery by facilitating the development of multidisciplinary surgical teams and joint surgery by sub-specialist gynaecological oncologists. There is no publically or easily available list of specialist gynaecological cancer centres. The National Cancer Peer Review Programme was able to provide lists of the MDTs who were reviewed as specialist in the review period 2004–2008, and also in the subsequent yearly review periods. However, no lists were available before 2004. Additionally, there were some differences between these lists, with some MDTs removed and some added. Furthermore, not all the MDTs included in these lists were regarded as specialist MDTs at the time of the review, either by peer review or the relevant cancer network. The purpose of this paper is to examine the extent to which there has been an increase in specialised ovarian cancer surgery since the publication of the IOG and cancer plan. 2. Materials and methods 2.1. Definition of ovarian cancer surgery Ovarian cancer (ICD10 C56–C57) patients aged 16–99 and diagnosed between January 1999 and December 2009 were identified from the National Cancer Data Repository for England and linked to Hospital Episodes Statistics (HES) [23] admitted patient care data to determine whether the patients received relevant surgery between 2000 and 2009. For each finished consultant episode, HES data includes the unique GMC number for the consultant responsible for the patient's care and details of the hospital provider. Patient postcodes were used to assign the relevant health administrative region (Strategic Health Authority, SHA).
A clinically agreed list of OPCS Classification of Interventions and Procedures (OPCS-4) codes [24,25] were used to identify a range of surgical procedures considered relevant for ovarian cancer [web appendix Table 1]. In order to maximise data capture, particularly for those undergoing surgery after neoadjuvant chemotherapy and with treatment delays, surgery was only considered to be relevant to the cancer if performed up to thirty days prior to or one year after the recorded date of diagnosis. For patients with relevant surgical procedures on more than one occasion, only the first occasion is included in the reported results. 2.2. Specialised gynaecological oncologists Each consultant's speciality was determined using either the lists of hospital consultants in England and Wales, obtained from the NHS Organisation Data Service [26] or the online GMC register [27]. In a small number of cases it was assumed that the consultants did not have a relevant speciality; specifically where the HES consultant code was incomplete, invalid or unknown or where the consultant could not be found on either list used. Five alternative definitions of a specialist consultant (gynaecological oncologist) were considered; firstly, those included in a GMC provided list of consultants with a recognised sub-speciality in gynaecological oncology, for surgery performed after their accreditation date. The other definitions were based on consultants whose specialism was listed as Obstetrics and Gynaecology (O&G) and were recorded as responsible for treating a minimum number of new patients in that calendar year. As there is no consistent definition of high and low caseload, consultants operating on 10, 15, or 20 plus patients were used to define high caseload and also 18 as this represented the median caseload of accredited gynaecological oncologists. 2.3. Specialised gynaecological cancer centres Using the National Cancer Peer Review Programme provided lists of the MDTs reviewed as local and specialist gynaecological teams, two lists of specialist gynaecological trusts were compared. A “2004–08 review period” list of specialist trusts includes the MDTs reviewed as specialist teams in the period 2004–08, where they were also subsequently reviewed as specialist teams or where their cancer network's IOG implementation plan recognised existing speciality with the provision for a transfer of services. A second list of specialist trusts includes the MDTs reviewed as specialist teams in the period 2011/12. There was one exception of an institution reviewed as a specialist team, but excluded since the Peer Review Programme and relevant cancer network consistently have stated that they do not recognise it as an agreed specialist centre. 2.4. Statistical methodology A Wilcoxon rank-sum test was used to test for a difference, between 2000 and 2009, in the caseload distributions for GMC accredited gynaecological oncology sub-specialists. For each caseload definition of specialist consultant, a two-sample proportion test was used to test for a change in the proportion of specialist consultants between 2000 and 2009. For each specialist definition, a chi-squared test for trend [28] was performed, in order to determine whether there was a statistically significant linear trend, over the 10-year period, in terms of the percentage of patients receiving specialist surgery. 3. Results A total of 30,753 (47.8%) of 64,293 ovarian cancer patients, diagnosed 1999–2009, received relevant surgery between 2000 and 2009. A total of 2428 consultants were responsible for their surgery including 1289 with an O&G specialism, and 66 with a gynaecological oncology
Please cite this article as: Butler J, et al, Specialist surgery for ovarian cancer in England, Gynecol Oncol (2015), http://dx.doi.org/10.1016/ j.ygyno.2015.03.003
J. Butler et al. / Gynecologic Oncology xxx (2015) xxx–xxx
3
Average Annual Number of Consultants
300
250 C a s e lo a d 1-2
200
3-5 6-10
150
11-15 16-18
100
19-20 >20
50
0 Obstetrics & Gynaecology
General Surgery
Other
Specialism
Fig. 1. Average annual number of consultants, by caseload and specialism.
sub-specialism. Most consultants were responsible for only a few patients, with, on average, 254 O&G consultants and 110 General Surgery consultants responsible for treating 1–2 cases per year. In contrast, 61 O&G consultants and no General Surgery consultants were responsible for treating more than 15 cases per year (Fig. 1). Most patients had surgery performed within 30 days of diagnosis although this decreased from 91.3% in 2000 to 74.3% in 2009. Very few patients (1.4–4%) underwent their first major surgery 6–12 months after diagnosis (Fig. 2).
consultants treating 18 or more cases per year increased from 22% in 2000 to 56% in 2009 (P b0.001) (Fig. 3). 3.2. Specialised gynaecological cancer centres Using the recent 2011/12 and 2004–08 lists of specialist MDTs to define the specialist trusts, the percentage of patients treated at specialist trusts increased considerably over the period considered. Using the 2011/12 definition, it increased from 43% in 2000 to 76% in 2009 (P b 0.001) (Fig. 4).
3.1. Specialised gynaecological oncologists 3.3. Specialised treatment by strategic health authority (SHA) From 2000 to 2009, the number of GMC accredited gynaecological oncology sub-specialists (GMC GOs) increased from 12 to 65, with a corresponding reduction in the number of non-specialists from 762 to 504. Additionally, the median caseloads for these specialist consultants increased from 8.5 to 19 (P = 0.03) (Table 2). The number of consultants with a caseload of ≥18 increased from 26 in 2000 to 74 in 2009 (3.6% of consultants to 13.0%, P b 0.001), with a corresponding reduction in the number with a caseload of b 18, from 748 to 495. The percentage of patients treated by GMC accredited gynaecological oncology sub-specialists increased considerably over the period considered, rising from 5% in 2000 to 36% in 2009 (P b 0.001). There was also a steady increase in the percentage of patients treated by high caseload surgeons (≥ 10, ≥ 15, ≥18 and ≥ 20 per year, P b 0.001). The proportion of patients with surgery under
Results were also produced for each of the 10 SHAs in England, based on the trust of treatment. Although with more year-on-year variability, increasing trends in the percentage treated by specialist consultants or in specialist trusts were observed for all SHAs. There were, however, some large differences between SHAs in the percentages and in the scale of the increasing trends. The percentage treated by consultants with caseloads of ≥18 varied between SHAs from 0% to 39% in 2000 and from 30% to 72% in 2009, with a three-fold range in the level of increase, from 19 percentage points to 53 percentage points. The percentage treated in 2011/12 specialist trusts varied from 25% to 62% in 2000 and from 65% to 89% in 2009, with more than a three-fold range in SHA increases, from 15 percentage points to 48 percentage points.
100% 90% 80% 70% 60% 50% 40% 30% 20% 10% 0% 2000
2001
2002
2003
2004
2005
2006
2007
2008
Up to 1 month after diag
1-2 months after diag
2-3 months after diag
3-6 months after diag
6-9 months after diag
9-12 months after diag
2009
Fig. 2. Interval from diagnosis to date of first major surgery (months).
Please cite this article as: Butler J, et al, Specialist surgery for ovarian cancer in England, Gynecol Oncol (2015), http://dx.doi.org/10.1016/ j.ygyno.2015.03.003
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Table 2 Number of non-specialist and GMC accredited gynaecology oncology consultants, each year, with median caseload, 2000 to 2009. Year
Non-specialists Specialists Median caseload (non-specialists) Median caseload (specialists)
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
762 12 2 8.5
757 14 1 13
646 20 1 12.5
611 24 1 16.5
576 27 1 16
514 35 1 19
555 44 1 17
514 48 1 19.5
508 54 1 17
504 65 1 19
3.4. Para-aortic node dissection
4.2. Strengths and limitations
A surrogate of specialist surgery is more complex procedures that are performed by gynaecological oncologists such as para-aortic node dissection (PAND). In the study period 413 (6.6%) of 6285 patients whose surgery was performed by GMC accredited gynaecological oncologists were recorded to have received a para-aortic dissection compared to 398 (1.6%) of 24,468 whose surgery was performed by non-accredited specialists (P b 0.0001). The rates of PAND were also higher for high volume (N 18 cases) surgeons and for surgery performed within specialist trusts (Fig. 5).
To the best of our knowledge this is the largest study on the effect of recommendations for centralisation of ovarian cancer surgery. The data used for this analysis includes full coverage of England and relies on the accurate cancer registration of ovarian cancer, which is dependent on the reliable supply of data from hospital trusts to cancer registries. The cancer registry community invests considerable time and effort into quality assuring the data they hold, including the submission of annual performance indicators, which include information on ascertainment, timeliness and the death certificate only rate [29]. From April 2013, cancer registration within England became the responsibility of the National Cancer Registration Service, part of Public Health England. HES data does not record privately funded surgery received in private hospitals and so the annual consultant caseloads may be slightly higher than considered here if they also treat patients in private hospitals. HES data indicates the name of the consultant responsible for the episode of care. It is possible that other consultants provided surgical services for these patients, but this would not generally be identified in HES data. Additionally, in a number of cases the consultant recorded on HES is a non-surgical consultant, including allied oncology specialists, but it is expected that the number of such cases is relatively small. However, there is currently no better, nationally available source of surgeon information. A small number of the HES consultant codes were incomplete, invalid or unknown and a number of consultants could not be found on used lists of specialisms; respectively, this only affected the consultant recorded against 0.4% (124) and 0.9% (265) of patients receiving surgery.
4. Discussion 4.1. Main findings
Percentage of patients treated by specialist
There have been significant increases in the percentage of patients with ovarian cancer receiving specialist surgery using all measures across England. The percentage of patients receiving surgery in specialist trusts has increased from 43% in 2000 to 76% in 2009. The percentage of patients operated on by GMC accredited gynaecological oncology sub-specialists has increased from 5% in 2000 to 36% in 2009. There remained large differences between regions in England, with between 30% and 72% of patients receiving surgery from consultants with caseloads of ≥ 18 new patients per year and between 65% and 89% receiving surgery in 2011/12 specialist trusts. The interval from diagnosis to first major surgery increased during the study and this is likely to be due to increased use of neoadjuvant chemotherapy rather than treatment delays.
100 90 80 70 60 50 40 30 20 10 0 2000
2001
2002
2003
Specialist Consultants (caseload = ≥10 new patients) Specialist Consultants (caseload = ≥18 new patients) Specialist Consultants (GMC list of gynae oncologists)
2004
2005
2006
2007
2008
2009
Specialist Consultants (caseload = ≥15 new patients) Specialist Consultants (caseload = ≥20 new patients)
Fig. 3. Percentage of patients treated by specialist consultants (according to five alternative definitions of specialist consultants), 2000–09.
Please cite this article as: Butler J, et al, Specialist surgery for ovarian cancer in England, Gynecol Oncol (2015), http://dx.doi.org/10.1016/ j.ygyno.2015.03.003
Percentage of patients treated by specialist
J. Butler et al. / Gynecologic Oncology xxx (2015) xxx–xxx
5
100 90 80 70 60 50 40 30 20 10 0 2000
2001
2002
2003
2004
Specialist Trusts (from 2004-2008 review period)
2005
2006
2007
2008
2009
Specialist Trusts (from 2011/12 review period)
Fig. 4. Percentage of patients treated by specialist trust (according to two alternative definitions of specialist trusts), 2000–09.
The results are also dependent on the accurate recording of relevant OPCS-4 surgery codes in the HES database for these patients, along with the correct recording of the consultant responsible for surgery. The list of relevant procedure codes utilised for the analysis resulted from considerable discussion and consultation, with the final list designed to be as inclusive as possible to ensure there was no bias in terms of variable or non-specific coding. A small number of patients appear to have received initial surgery in a non-specialist centre and further surgery in cancer centres (approximately 0.7% in 2000 and 2.2% in 2009). These cases were not classified as specialist surgery, since surgery for recurrence or progression could not be differentiated from definitive primary surgery before or after chemotherapy and the numbers of patients were very small.
4.2. Interpretation (in light of other evidence) The increase in surgery by GMC accredited gynaecological oncology sub-specialists is consistent with most new consultant appointees in gynaecological cancer centres having completed a formal subspeciality training programme in gynaecological cancer. However, the percentage receiving treatment by these accredited sub-specialists does not provide a true reflection of the percentage receiving specialist treatment, since many well-established specialists are not accredited by the GMC. The higher and increasing rates during the study of PAND
10% GMC accredited specialist
9% 8% 7%
High caseload (≥18 new patients)
6%
Specialist trust (2011/12)
5% Not a GMC accredited specialist
4% 3% 2%
Lower caseload (<18 new patients)
1%
Non-specialist trust
0% 2000-01
2002-03
2004-05
2006-07
2008-09
Fig. 5. Para-aortic node dissection (%) and specialist surgeon /specialist trust.
performed by GMC accredited specialists, high volume surgeons and within specialised trusts imply that more complex and specialist surgery is being performed by specialists within specialist centres. The large number of consultants responsible for patients receiving ovarian cancer surgery is not unexpected. In an average year, 66% (412) of the consultants that are responsible for ovarian cancer surgery have treated one or two patients. These are likely to be predominantly incidental early stage ovarian cancers, with a normal Risk of Malignancy Index, or patients presenting in extremis with bowel obstruction needing emergency surgery in the local hospital [30]. A highly effective cancer network, with excellent referral pathways from diagnostic units to specialist centres, will have a small number of “low risk masses” operated on by general gynaecologists which subsequently prove to be cancers on histology. However, the number will be small and general gynaecologists would be expected to operate on only a few cases per year if cases are appropriately being assessed and referred for pre-operative assessment by an effective MDT. The number of cases undergoing emergency bowel obstruction surgery by general surgeons, with a subsequent diagnosis of ovarian malignancy, should be minimised but these cases will continue to occur. For patients and those commissioning cancer services, cancer centres provide specialist expertise for surgery to be delivered by gynaecological oncologists as part of an MDT. A large number of the surgeons operating in gynaecological cancer centres are not GMC accredited sub-specialist gynaecological oncologists. Whilst all new appointments to subspecialty gynaecological oncology posts should have completed an appropriate subspecialty training programme and be registered as a sub-specialist with the GMC, there remains a lack of clarity with regards to individuals previously in consultant posts as there is no official retrospective accreditation process. The National Cancer Peer Review Programme and the new GMC revalidation programme should be utilised to ensure that ovarian cancer surgery is being performed within specialist centres by specialist surgeons. Consultant caseload data, based on consultants with surgical caseloads of 15 or more new cases, is now being utilised as one of the National Cancer Peer Review Clinical Lines of Enquiry metrics [31]. Caseload however in the UK setting may not be a useful surrogate for high quality surgery as high caseload was not associated with improved cytoreduction rates in part due to low operative times [32]. Clinical teams and cancer networks must ensure that staging and other clinical data are uploaded to the cancer registries, in order that details of surgery not performed within specialist centres can be analysed, and there should be local and national validation and quality assurance of HES data to enable robust and defensible patterns of care analyses to be performed.
Please cite this article as: Butler J, et al, Specialist surgery for ovarian cancer in England, Gynecol Oncol (2015), http://dx.doi.org/10.1016/ j.ygyno.2015.03.003
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J. Butler et al. / Gynecologic Oncology xxx (2015) xxx–xxx 50%
References
45% 40% 35% 30% 25% 20% 15% 10% 5% 0% 1995-99
2000-04
Sweden
US registries
Australian registries
England
2005-09 Norway
Fig. 6. Five year ovarian cancer net survival in Australian Registries, England, Norway, Sweden, and US registries, 1995–2009 (data from Allemani et al., 2014).
5. Conclusion During the time period of this study there has been an increase in ovarian cancer survival in England but this survival remains inferior to comparable countries such as Australia, Norway, Sweden, and the United States [5] (Fig. 6). The improved survival in England may be related to the demonstrated increases in specialist treatment both surgery and chemotherapy [33]. There is the potential for further research to better understand the extent to which the increases in specialist treatment have influenced patient care and outcomes, including differences in stage, treatment and survival between specialist and non-specialist centres. Further work is needed to understand the reasons for observed regional and international differences and the implications for patient care and outcomes. Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.ygyno.2015.03.003. Contribution to authorship All authors were involved in the design of the study and drafting of the manuscript. Ethical approval Although data sourced from the National Cancer Data Repository (NCDR) contains patient identifiable information, cancer registries have legal support to collect data relating to cancer under Section 251 of the NHS Act 394 2006 (and formerly under Section 60 of the Health and Social Care Act 2001). Therefore, ethics approval was not obtained. Funding Funding was obtained from the National Cancer Intelligence Network (NCIN) as part of an annual work programme undertaken by the former Trent Cancer Registry; this team is now part of the Public Health England Knowledge and Intelligence Team (East Midlands). Conflict of interest statement The author(s) declare that there are no conflicts of interest.
Acknowledgments Sue Knights from the National Cancer Peer Review Programme is acknowledged for the provision of lists of peer-reviewed specialist gynaecological cancer centres and also, for helpful discussions relating to some networks' complicated specialist centre implementation plans.
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Please cite this article as: Butler J, et al, Specialist surgery for ovarian cancer in England, Gynecol Oncol (2015), http://dx.doi.org/10.1016/ j.ygyno.2015.03.003
J. Butler et al. / Gynecologic Oncology xxx (2015) xxx–xxx [29] United Kingdom Association of Cancer Registries (UKACR), Data Quality Assurance Registration (DQAR) group. UKACR Annual Performance Indicators; 2012. [30] Bailey J, Tailor A, Naik R, Lopes A, Godfrey K, Hatem HM, Monaghan J. Risk of malignancy index for referral of ovarian cancer cases to a tertiary center: does it identify the correct cases? Int J Gynecol Cancer 2006;1(S):30–4 (2006 Jan-Feb;16). [31] National Cancer Action Team. National Cancer Peer Review Programme: Gynaecology Clinical Lines of Enquiry: Briefing Paper for National Cancer Peer Review 2012–2013; 2012.
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[32] Barton DP, Adib T, Butler J. Surgical practice of UK gynaecological oncologists in the treatment of primary advanced epithelial ovarian cancer (PAEOC): a questionnaire survey. Gynecol Oncol 2013 Nov;131(2):347–51. [33] Crawford R, Greenberg D. Improvements in survival of gynaecological cancer in the Anglia region of England: are these an effect of centralisation of care and use of multidisciplinary management? BJOG 2012;119(2):160–5, http://dx.doi.org/10. 1111/j.1471-0528.2011.02961.x.
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Contents lists available at ScienceDirect
Gynecologic Oncology journal homepage: www.elsevier.com/locate/ygyno
Specialist surgery for ovarian cancer in England John Butler a,⁎, Carolynn Gildea b, Jason Poole b, David Meechan b, Andrew Nordin c,d a
Department of Gynaecological Oncology, Royal Marsden Hospital, London SW3 6JJ, UK Public Health England Knowledge & Intelligence Team (East Midlands), 5 Old Fulwood Road, Sheffield S10 3TG, UK c East Kent Gynaecological Centre, East Kent Hospitals University NHS Foundation Trust, QEQM Hospital, St Peters Road, Margate, Kent, UK d Gynaecological Site Specific Clinical Reference Group (SSCGR), National Cancer Intelligence Network (NCIN), 5th Floor, Wellington House, 133-155 Waterloo Road, London SE1 8UG, UK b
H I G H L I G H T S • In 1999 national guidance recommended centralisation and specialisation of ovarian cancer surgery. • Specialist surgery and centralisation for ovarian cancer in England have increased from 2000 to 2009. • Survival has also increased.
a r t i c l e
i n f o
Article history: Received 5 June 2014 Accepted 4 March 2015 Available online xxxx Keywords: Ovarian cancer Surgery Specialist Gynaecological cancer centres Gynaecological oncologist
a b s t r a c t Objective. The aim of this study is to evaluate the impact of the 1999 national recommendations for ovarian cancer surgery in England to be performed by specialist surgeons in specialist centres. Methods. A retrospective analysis of English cancer registry records, Hospital Episode Statistics (HES) data for all English NHS providers and General Medical Council (GMC) sub-specialty accreditation, to consider changes to the annual proportion of ovarian cancer (ICD10 C56-C57) patients undergoing major gynaecological surgery in gynaecological cancer centres (GCCs) or by specialist gynaecological oncologists (GOs). Results. From 2000 to 2009, 2428 consultants were responsible for surgery on 30,753 patients. There were significant increases in the proportions of patients undergoing surgery at GCCs (43% to 76%, P b 0.001), by GMC accredited GOs (5% to 36%, P b 0.001), and by high ovarian cancer caseload (≥18 cases) surgeons (22% to 56%, P b 0.001). Conclusion. There have been increased centralisation and specialisation of surgery for ovarian cancer patients since the NHS Cancer Plan (2000) and there has also been improved survival. However, by 2009, many ovarian cancer patients were still not receiving specialist surgery; the majority of patients were not operated on by GMC accredited gynaecological oncologists and there was considerable regional variation. Systems of accreditation should be reviewed and trusts should ensure that HES data accurately records clinical activity. © 2015 Elsevier Inc. All rights reserved.
1. Introduction Ovarian cancer is the fifth most common female malignancy and most lethal gynaecological malignancy with approximately 5750 new diagnoses and 3500 deaths each year in England [1]. Ovarian cancer survival in England and the UK has been persistently lower than other comparable countries [2–5] and this appears to be due to differences in treatment rather than adverse stage distribution or late diagnosis [6]. The Calman Hine Report (1995) [7] recommended the centralisation of cancer services and the formation of cancer networks, and these have been formally established since the NHS Cancer Plan [8]. In 1999, the Department of Health published the Improving Outcomes Guidance (IOG) in Gynaecological Cancers recommending that “Surgery for ⁎ Corresponding author. E-mail address: [email protected] (J. Butler).
ovarian cancer should be carried out by specialised gynaecological oncologists at Cancer Centres” [9]. 1.1. Specialised gynaecological oncologists It has been estimated that 478 lives a year could be saved if UK ovarian cancer survival matched the best in Europe [10]. After stage at diagnosis, the most important determinant for ovarian cancer survival is the volume of residual disease after staging surgery [11]. In comparison to general gynaecologists and general surgeons, gynaecological oncologists and high volume surgeons are more likely to completely resect all disease, perform a lymphadenectomy and treat patients according to guidelines [12], and have lower in-hospital mortality resulting in improved survival [13,14]. In the United Kingdom, there have been specialist training programmes in gynaecological oncology, accredited by the Royal
http://dx.doi.org/10.1016/j.ygyno.2015.03.003 0090-8258/© 2015 Elsevier Inc. All rights reserved.
Please cite this article as: Butler J, et al, Specialist surgery for ovarian cancer in England, Gynecol Oncol (2015), http://dx.doi.org/10.1016/ j.ygyno.2015.03.003
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J. Butler et al. / Gynecologic Oncology xxx (2015) xxx–xxx
College of Obstetricians (RCOG), since 1984. This is a two or three year fellowship programme completing a syllabus or specialised training in accredited gynaecology oncology centres [15]. Surgeons completing such approved UK programmes are accredited as gynaecology oncology sub-specialists by the General Medical Council (GMC). Other surgeons having completed training programmes overseas may also be listed as sub-specialists by the GMC. The GMC accreditation is not comprehensive, as many surgeons recognised nationally and internationally as very experienced gynaecological oncologists, and responsible for training and supervising sub-specialist trainees, are not listed as subspecialists. The British Gynaecological Cancer Society (BGCS) proposed that a gynaecological oncologist is a surgeon who works in a designated gynaecological cancer centre and spends 75% or more of their clinical sessions in gynaecological oncology. It has also proposed that surgical caseload is a key parameter for benchmarking performance [16]. These proposals have not been formalised and the BGCS does not maintain a register of gynaecological oncology specialists. Neither is there an international standard of what constitutes an adequate caseload for a gynaecological oncologist. Vernooij et al. defined case volumes as low (≤ 6 per year), intermediate (7–12 per year) and high (N12 per year) [17]. Bristow et al. defined low as b10 per year and high as ≥10 [18]. 1.2. Specialised gynaecological cancer centres It has been shown that outcomes in many cancers are improved when care is performed in specialised centres [19–22]. Ovarian cancer treated in high volume hospitals has been associated with increased likelihood of cytoreduction, shorter length of stay, and lower hospitalrelated cost of care [14]. The combination of high volume hospital and high volume surgeon is an independent predictor of improved disease specific survival [18]. Centralisation of care in specialist gynaecological oncology centres enables management by specialist multidisciplinary teams (MDTs) including integration of specialist medical, surgical and clinical oncology, radiology and nurse specialist services. It ensures continuity of care and improves the information provided to patients. Additionally, it advances expertise in specialist radical ovarian cancer surgery by facilitating the development of multidisciplinary surgical teams and joint surgery by sub-specialist gynaecological oncologists. There is no publically or easily available list of specialist gynaecological cancer centres. The National Cancer Peer Review Programme was able to provide lists of the MDTs who were reviewed as specialist in the review period 2004–2008, and also in the subsequent yearly review periods. However, no lists were available before 2004. Additionally, there were some differences between these lists, with some MDTs removed and some added. Furthermore, not all the MDTs included in these lists were regarded as specialist MDTs at the time of the review, either by peer review or the relevant cancer network. The purpose of this paper is to examine the extent to which there has been an increase in specialised ovarian cancer surgery since the publication of the IOG and cancer plan. 2. Materials and methods 2.1. Definition of ovarian cancer surgery Ovarian cancer (ICD10 C56–C57) patients aged 16–99 and diagnosed between January 1999 and December 2009 were identified from the National Cancer Data Repository for England and linked to Hospital Episodes Statistics (HES) [23] admitted patient care data to determine whether the patients received relevant surgery between 2000 and 2009. For each finished consultant episode, HES data includes the unique GMC number for the consultant responsible for the patient's care and details of the hospital provider. Patient postcodes were used to assign the relevant health administrative region (Strategic Health Authority, SHA).
A clinically agreed list of OPCS Classification of Interventions and Procedures (OPCS-4) codes [24,25] were used to identify a range of surgical procedures considered relevant for ovarian cancer [web appendix Table 1]. In order to maximise data capture, particularly for those undergoing surgery after neoadjuvant chemotherapy and with treatment delays, surgery was only considered to be relevant to the cancer if performed up to thirty days prior to or one year after the recorded date of diagnosis. For patients with relevant surgical procedures on more than one occasion, only the first occasion is included in the reported results. 2.2. Specialised gynaecological oncologists Each consultant's speciality was determined using either the lists of hospital consultants in England and Wales, obtained from the NHS Organisation Data Service [26] or the online GMC register [27]. In a small number of cases it was assumed that the consultants did not have a relevant speciality; specifically where the HES consultant code was incomplete, invalid or unknown or where the consultant could not be found on either list used. Five alternative definitions of a specialist consultant (gynaecological oncologist) were considered; firstly, those included in a GMC provided list of consultants with a recognised sub-speciality in gynaecological oncology, for surgery performed after their accreditation date. The other definitions were based on consultants whose specialism was listed as Obstetrics and Gynaecology (O&G) and were recorded as responsible for treating a minimum number of new patients in that calendar year. As there is no consistent definition of high and low caseload, consultants operating on 10, 15, or 20 plus patients were used to define high caseload and also 18 as this represented the median caseload of accredited gynaecological oncologists. 2.3. Specialised gynaecological cancer centres Using the National Cancer Peer Review Programme provided lists of the MDTs reviewed as local and specialist gynaecological teams, two lists of specialist gynaecological trusts were compared. A “2004–08 review period” list of specialist trusts includes the MDTs reviewed as specialist teams in the period 2004–08, where they were also subsequently reviewed as specialist teams or where their cancer network's IOG implementation plan recognised existing speciality with the provision for a transfer of services. A second list of specialist trusts includes the MDTs reviewed as specialist teams in the period 2011/12. There was one exception of an institution reviewed as a specialist team, but excluded since the Peer Review Programme and relevant cancer network consistently have stated that they do not recognise it as an agreed specialist centre. 2.4. Statistical methodology A Wilcoxon rank-sum test was used to test for a difference, between 2000 and 2009, in the caseload distributions for GMC accredited gynaecological oncology sub-specialists. For each caseload definition of specialist consultant, a two-sample proportion test was used to test for a change in the proportion of specialist consultants between 2000 and 2009. For each specialist definition, a chi-squared test for trend [28] was performed, in order to determine whether there was a statistically significant linear trend, over the 10-year period, in terms of the percentage of patients receiving specialist surgery. 3. Results A total of 30,753 (47.8%) of 64,293 ovarian cancer patients, diagnosed 1999–2009, received relevant surgery between 2000 and 2009. A total of 2428 consultants were responsible for their surgery including 1289 with an O&G specialism, and 66 with a gynaecological oncology
Please cite this article as: Butler J, et al, Specialist surgery for ovarian cancer in England, Gynecol Oncol (2015), http://dx.doi.org/10.1016/ j.ygyno.2015.03.003
J. Butler et al. / Gynecologic Oncology xxx (2015) xxx–xxx
3
Average Annual Number of Consultants
300
250 C a s e lo a d 1-2
200
3-5 6-10
150
11-15 16-18
100
19-20 >20
50
0 Obstetrics & Gynaecology
General Surgery
Other
Specialism
Fig. 1. Average annual number of consultants, by caseload and specialism.
sub-specialism. Most consultants were responsible for only a few patients, with, on average, 254 O&G consultants and 110 General Surgery consultants responsible for treating 1–2 cases per year. In contrast, 61 O&G consultants and no General Surgery consultants were responsible for treating more than 15 cases per year (Fig. 1). Most patients had surgery performed within 30 days of diagnosis although this decreased from 91.3% in 2000 to 74.3% in 2009. Very few patients (1.4–4%) underwent their first major surgery 6–12 months after diagnosis (Fig. 2).
consultants treating 18 or more cases per year increased from 22% in 2000 to 56% in 2009 (P b0.001) (Fig. 3). 3.2. Specialised gynaecological cancer centres Using the recent 2011/12 and 2004–08 lists of specialist MDTs to define the specialist trusts, the percentage of patients treated at specialist trusts increased considerably over the period considered. Using the 2011/12 definition, it increased from 43% in 2000 to 76% in 2009 (P b 0.001) (Fig. 4).
3.1. Specialised gynaecological oncologists 3.3. Specialised treatment by strategic health authority (SHA) From 2000 to 2009, the number of GMC accredited gynaecological oncology sub-specialists (GMC GOs) increased from 12 to 65, with a corresponding reduction in the number of non-specialists from 762 to 504. Additionally, the median caseloads for these specialist consultants increased from 8.5 to 19 (P = 0.03) (Table 2). The number of consultants with a caseload of ≥18 increased from 26 in 2000 to 74 in 2009 (3.6% of consultants to 13.0%, P b 0.001), with a corresponding reduction in the number with a caseload of b 18, from 748 to 495. The percentage of patients treated by GMC accredited gynaecological oncology sub-specialists increased considerably over the period considered, rising from 5% in 2000 to 36% in 2009 (P b 0.001). There was also a steady increase in the percentage of patients treated by high caseload surgeons (≥ 10, ≥ 15, ≥18 and ≥ 20 per year, P b 0.001). The proportion of patients with surgery under
Results were also produced for each of the 10 SHAs in England, based on the trust of treatment. Although with more year-on-year variability, increasing trends in the percentage treated by specialist consultants or in specialist trusts were observed for all SHAs. There were, however, some large differences between SHAs in the percentages and in the scale of the increasing trends. The percentage treated by consultants with caseloads of ≥18 varied between SHAs from 0% to 39% in 2000 and from 30% to 72% in 2009, with a three-fold range in the level of increase, from 19 percentage points to 53 percentage points. The percentage treated in 2011/12 specialist trusts varied from 25% to 62% in 2000 and from 65% to 89% in 2009, with more than a three-fold range in SHA increases, from 15 percentage points to 48 percentage points.
100% 90% 80% 70% 60% 50% 40% 30% 20% 10% 0% 2000
2001
2002
2003
2004
2005
2006
2007
2008
Up to 1 month after diag
1-2 months after diag
2-3 months after diag
3-6 months after diag
6-9 months after diag
9-12 months after diag
2009
Fig. 2. Interval from diagnosis to date of first major surgery (months).
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Table 2 Number of non-specialist and GMC accredited gynaecology oncology consultants, each year, with median caseload, 2000 to 2009. Year
Non-specialists Specialists Median caseload (non-specialists) Median caseload (specialists)
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
762 12 2 8.5
757 14 1 13
646 20 1 12.5
611 24 1 16.5
576 27 1 16
514 35 1 19
555 44 1 17
514 48 1 19.5
508 54 1 17
504 65 1 19
3.4. Para-aortic node dissection
4.2. Strengths and limitations
A surrogate of specialist surgery is more complex procedures that are performed by gynaecological oncologists such as para-aortic node dissection (PAND). In the study period 413 (6.6%) of 6285 patients whose surgery was performed by GMC accredited gynaecological oncologists were recorded to have received a para-aortic dissection compared to 398 (1.6%) of 24,468 whose surgery was performed by non-accredited specialists (P b 0.0001). The rates of PAND were also higher for high volume (N 18 cases) surgeons and for surgery performed within specialist trusts (Fig. 5).
To the best of our knowledge this is the largest study on the effect of recommendations for centralisation of ovarian cancer surgery. The data used for this analysis includes full coverage of England and relies on the accurate cancer registration of ovarian cancer, which is dependent on the reliable supply of data from hospital trusts to cancer registries. The cancer registry community invests considerable time and effort into quality assuring the data they hold, including the submission of annual performance indicators, which include information on ascertainment, timeliness and the death certificate only rate [29]. From April 2013, cancer registration within England became the responsibility of the National Cancer Registration Service, part of Public Health England. HES data does not record privately funded surgery received in private hospitals and so the annual consultant caseloads may be slightly higher than considered here if they also treat patients in private hospitals. HES data indicates the name of the consultant responsible for the episode of care. It is possible that other consultants provided surgical services for these patients, but this would not generally be identified in HES data. Additionally, in a number of cases the consultant recorded on HES is a non-surgical consultant, including allied oncology specialists, but it is expected that the number of such cases is relatively small. However, there is currently no better, nationally available source of surgeon information. A small number of the HES consultant codes were incomplete, invalid or unknown and a number of consultants could not be found on used lists of specialisms; respectively, this only affected the consultant recorded against 0.4% (124) and 0.9% (265) of patients receiving surgery.
4. Discussion 4.1. Main findings
Percentage of patients treated by specialist
There have been significant increases in the percentage of patients with ovarian cancer receiving specialist surgery using all measures across England. The percentage of patients receiving surgery in specialist trusts has increased from 43% in 2000 to 76% in 2009. The percentage of patients operated on by GMC accredited gynaecological oncology sub-specialists has increased from 5% in 2000 to 36% in 2009. There remained large differences between regions in England, with between 30% and 72% of patients receiving surgery from consultants with caseloads of ≥ 18 new patients per year and between 65% and 89% receiving surgery in 2011/12 specialist trusts. The interval from diagnosis to first major surgery increased during the study and this is likely to be due to increased use of neoadjuvant chemotherapy rather than treatment delays.
100 90 80 70 60 50 40 30 20 10 0 2000
2001
2002
2003
Specialist Consultants (caseload = ≥10 new patients) Specialist Consultants (caseload = ≥18 new patients) Specialist Consultants (GMC list of gynae oncologists)
2004
2005
2006
2007
2008
2009
Specialist Consultants (caseload = ≥15 new patients) Specialist Consultants (caseload = ≥20 new patients)
Fig. 3. Percentage of patients treated by specialist consultants (according to five alternative definitions of specialist consultants), 2000–09.
Please cite this article as: Butler J, et al, Specialist surgery for ovarian cancer in England, Gynecol Oncol (2015), http://dx.doi.org/10.1016/ j.ygyno.2015.03.003
Percentage of patients treated by specialist
J. Butler et al. / Gynecologic Oncology xxx (2015) xxx–xxx
5
100 90 80 70 60 50 40 30 20 10 0 2000
2001
2002
2003
2004
Specialist Trusts (from 2004-2008 review period)
2005
2006
2007
2008
2009
Specialist Trusts (from 2011/12 review period)
Fig. 4. Percentage of patients treated by specialist trust (according to two alternative definitions of specialist trusts), 2000–09.
The results are also dependent on the accurate recording of relevant OPCS-4 surgery codes in the HES database for these patients, along with the correct recording of the consultant responsible for surgery. The list of relevant procedure codes utilised for the analysis resulted from considerable discussion and consultation, with the final list designed to be as inclusive as possible to ensure there was no bias in terms of variable or non-specific coding. A small number of patients appear to have received initial surgery in a non-specialist centre and further surgery in cancer centres (approximately 0.7% in 2000 and 2.2% in 2009). These cases were not classified as specialist surgery, since surgery for recurrence or progression could not be differentiated from definitive primary surgery before or after chemotherapy and the numbers of patients were very small.
4.2. Interpretation (in light of other evidence) The increase in surgery by GMC accredited gynaecological oncology sub-specialists is consistent with most new consultant appointees in gynaecological cancer centres having completed a formal subspeciality training programme in gynaecological cancer. However, the percentage receiving treatment by these accredited sub-specialists does not provide a true reflection of the percentage receiving specialist treatment, since many well-established specialists are not accredited by the GMC. The higher and increasing rates during the study of PAND
10% GMC accredited specialist
9% 8% 7%
High caseload (≥18 new patients)
6%
Specialist trust (2011/12)
5% Not a GMC accredited specialist
4% 3% 2%
Lower caseload (<18 new patients)
1%
Non-specialist trust
0% 2000-01
2002-03
2004-05
2006-07
2008-09
Fig. 5. Para-aortic node dissection (%) and specialist surgeon /specialist trust.
performed by GMC accredited specialists, high volume surgeons and within specialised trusts imply that more complex and specialist surgery is being performed by specialists within specialist centres. The large number of consultants responsible for patients receiving ovarian cancer surgery is not unexpected. In an average year, 66% (412) of the consultants that are responsible for ovarian cancer surgery have treated one or two patients. These are likely to be predominantly incidental early stage ovarian cancers, with a normal Risk of Malignancy Index, or patients presenting in extremis with bowel obstruction needing emergency surgery in the local hospital [30]. A highly effective cancer network, with excellent referral pathways from diagnostic units to specialist centres, will have a small number of “low risk masses” operated on by general gynaecologists which subsequently prove to be cancers on histology. However, the number will be small and general gynaecologists would be expected to operate on only a few cases per year if cases are appropriately being assessed and referred for pre-operative assessment by an effective MDT. The number of cases undergoing emergency bowel obstruction surgery by general surgeons, with a subsequent diagnosis of ovarian malignancy, should be minimised but these cases will continue to occur. For patients and those commissioning cancer services, cancer centres provide specialist expertise for surgery to be delivered by gynaecological oncologists as part of an MDT. A large number of the surgeons operating in gynaecological cancer centres are not GMC accredited sub-specialist gynaecological oncologists. Whilst all new appointments to subspecialty gynaecological oncology posts should have completed an appropriate subspecialty training programme and be registered as a sub-specialist with the GMC, there remains a lack of clarity with regards to individuals previously in consultant posts as there is no official retrospective accreditation process. The National Cancer Peer Review Programme and the new GMC revalidation programme should be utilised to ensure that ovarian cancer surgery is being performed within specialist centres by specialist surgeons. Consultant caseload data, based on consultants with surgical caseloads of 15 or more new cases, is now being utilised as one of the National Cancer Peer Review Clinical Lines of Enquiry metrics [31]. Caseload however in the UK setting may not be a useful surrogate for high quality surgery as high caseload was not associated with improved cytoreduction rates in part due to low operative times [32]. Clinical teams and cancer networks must ensure that staging and other clinical data are uploaded to the cancer registries, in order that details of surgery not performed within specialist centres can be analysed, and there should be local and national validation and quality assurance of HES data to enable robust and defensible patterns of care analyses to be performed.
Please cite this article as: Butler J, et al, Specialist surgery for ovarian cancer in England, Gynecol Oncol (2015), http://dx.doi.org/10.1016/ j.ygyno.2015.03.003
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J. Butler et al. / Gynecologic Oncology xxx (2015) xxx–xxx 50%
References
45% 40% 35% 30% 25% 20% 15% 10% 5% 0% 1995-99
2000-04
Sweden
US registries
Australian registries
England
2005-09 Norway
Fig. 6. Five year ovarian cancer net survival in Australian Registries, England, Norway, Sweden, and US registries, 1995–2009 (data from Allemani et al., 2014).
5. Conclusion During the time period of this study there has been an increase in ovarian cancer survival in England but this survival remains inferior to comparable countries such as Australia, Norway, Sweden, and the United States [5] (Fig. 6). The improved survival in England may be related to the demonstrated increases in specialist treatment both surgery and chemotherapy [33]. There is the potential for further research to better understand the extent to which the increases in specialist treatment have influenced patient care and outcomes, including differences in stage, treatment and survival between specialist and non-specialist centres. Further work is needed to understand the reasons for observed regional and international differences and the implications for patient care and outcomes. Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.ygyno.2015.03.003. Contribution to authorship All authors were involved in the design of the study and drafting of the manuscript. Ethical approval Although data sourced from the National Cancer Data Repository (NCDR) contains patient identifiable information, cancer registries have legal support to collect data relating to cancer under Section 251 of the NHS Act 394 2006 (and formerly under Section 60 of the Health and Social Care Act 2001). Therefore, ethics approval was not obtained. Funding Funding was obtained from the National Cancer Intelligence Network (NCIN) as part of an annual work programme undertaken by the former Trent Cancer Registry; this team is now part of the Public Health England Knowledge and Intelligence Team (East Midlands). Conflict of interest statement The author(s) declare that there are no conflicts of interest.
Acknowledgments Sue Knights from the National Cancer Peer Review Programme is acknowledged for the provision of lists of peer-reviewed specialist gynaecological cancer centres and also, for helpful discussions relating to some networks' complicated specialist centre implementation plans.
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Please cite this article as: Butler J, et al, Specialist surgery for ovarian cancer in England, Gynecol Oncol (2015), http://dx.doi.org/10.1016/ j.ygyno.2015.03.003