The optimal organization of gynecologic oncology services: a systematic review

Abstract

Background

A system-level organizational guideline for gynecologic oncology was identified by a provincial cancer agency as a key priority based on input from stakeholders, data showing more limited availability of multidisciplinary or specialist care in lower-volume than in higher-volume hospitals in the relevant jurisdiction, and variable rates of staging for ovarian and endometrial cancer patients.

Methods

A systematic review assessed the relationship of the organization of gynecologic oncology services with patient survival and surgical outcomes. The electronic databases medline and embase (ovid: 1996 through 9 January 2015) were searched using terms related to gynecologic malignancies combined with organization of services, patterns of care, and various facility and physician characteristics. Outcomes of interest included overall or disease-specific survival, short-term survival, adequate staging, and degree of cytoreduction or optimal cytoreduction (or both) for ovarian cancer patients by hospital or physician type, and rate of discrepancy in initial diagnoses and intraoperative consultation between non-specialist pathologists and gyne-oncology–specialist pathologists.

Results

One systematic review and sixteen additional primary studies met the inclusion criteria. The evidence base as a whole was judged to be of lower quality; however, a trend toward improved outcomes with centralization of gynecologic oncology was found, particularly with respect to the gynecologic oncology care of patients with advanced-stage ovarian cancer.

Conclusions

Improvements in outcomes with centralization of gynecologic oncology services can be attributed to a number of factors, including access to specialist care and multidisciplinary team management. Findings of this systematic review should be used with caution because of the limitations of the evidence base; however, an expert consensus process made it possible to create recommendations for implementation.

INTRODUCTION

The annual incidence of gynecologic cancers exceeds a million cases worldwide, with half a million deaths annually¹. In some jurisdictions, gynecologic oncology services have been centralized² in one or more centres with higher patient volumes and interdisciplinary collaboration³. Those centres receive referrals from less-specialized hospitals within a network, region, or defined catchment area. The effectiveness of that model of service delivery has been shown for other cancer disease sites⁴, but its benefits have historically not been as clear for gynecologic oncology^5–7.

The present systematic review was designed to assess the relationship of the organization of gynecologic oncology services with patient survival, surgical outcomes, the delivery of chemotherapy, and some aspects of the role of specialist pathologists in gynecologic oncology. This choice of topic was based on perceived issues, including the absence of a health care system–wide network of care and a lack of collaboration, even in a setting in which most gynecologic oncologists are practicing in major centres with teaching hospitals and using a multidisciplinary team approach. Specific areas of potential concern for patient care included low rates of appropriate disease staging^8,9, geographic variations in treatment⁸, and variations in treatment delivered by subspecialists relative to other surgeons⁹. Our systematic review provides the basis for recommendations that are intended to promote evidence-based practice and to improve patient access to timely, consistent, high-quality care in a higher-resource location.

RESEARCH QUESTIONS

• □ Are outcomes better for patients with gynecologic cancer treated in designated centres (“centralized care”) compared with non-designated centres (“decentralized care”)?

• □ Are outcomes better for patients treated by gynecologic oncologists than by non-subspecialist physicians?

Outcomes of interest included overall or disease-specific survival, short-term survival, adequate staging, degree of cytoreduction or optimal cytoreduction (or both) for ovarian cancer patients by hospital or physician type, and rate of discrepancy in initial diagnoses and intraoperative consultation between non-specialist pathologists and gyne-oncology–specialist pathologists.

METHODS

The electronic databases medline and embase (ovid: 1996 through 12 December 2011) were searched using terms related to gynecologic malignancies combined with organization of services, patterns of care, and various facility and physician characteristics (Table i). The Cochrane Database of Systematic Reviews was searched for topic-specific reviews up to Issue 12 (December), 2011. Reference lists of included articles were scanned for additional citations. The search engine Google Scholar was used to identify articles using the terms “gynecological cancer” or “gynaecological cancer” and “centralisation” or “centralization” or “volumes.” Additional search terms were used to locate studies that addressed some aspect of quality in pathology diagnosis.

TABLE I.

Search strategy

Initial search for articles (to 12 December 2011)
1.	((endometr* or uter* or cervi* or ovar* or vulva* or gynae* or gyne*) adj (cancer* or neoplas* or carcinom* or malignan* or tumor* or tumour*)).ti,ab.
2.	Organizational Policy/ or Efficiency, Organizational/or Models, Organizational/
3.	*health facilities/
4.	centralization.mp. or Centralized Hospital Services/
5.	(patterns adj5 care).ti.
6.	clinical competence.mp. or Clinical Competence/
7.	palliative care.mp. or Palliative Care/
8.	patient care.mp. or Patient Care/
9.	cancer care facilities.mp. or Cancer Care Facilities/
10.	(training or competency or proficiency).ti.
11.	Surgical Procedures, Operative/ or surgical volumes.mp.
12.	volume*.ti.
13.	(centrali?ation or speciali?ation or speciali?$).ti.
14.	regional*.ti.
15.	(subspecialty or specialty).ti.
16.	multidisciplinary.ti.
17.	multidisciplinary team management.mp. or Patient Care Team/
18.	1 and (2 or 3 or 4 or 6 or 8 or 9 or 10)
19.	1 and 5
20.	1 and 7
21.	1 and (11 or 12)
22.	1 and (13 or 14 or 15)
23.	1 and (16 or 17)
24.	18 or 19 or 20 or 21 or 22 or 23
25.	limit 24 to (english language and yr=“1995 -Current”)
26.	25 not screening.ti.

Additional search for pathology-related articles (to 1 February 2012)
1.	((endometr* or uter* or cervi* or ovar* or vulva* or gynae* or gyne*) adj (cancer* or neoplas* or carcinom* or malignan* or tumor* or tumour*)).ti,ab.
2.	patholog*.ti.
3.	1 and 2
4.	limit 3 to yr=“1995 -Current”
5.	limit 8 to english language

Articles were selected by the project methodologist and were reviewed by all authors. To identify existing relevant guidelines published between 1995 and 2011, a search was conducted of the Web sites of major guideline developers^a.

The search was repeated on 9 January 2015 to improve the currency of the evidence base.

Study Selection

Study designs eligible for inclusion were observational studies with a retrospective or prospective assessment of a cohort of patients and systematic reviews of such study designs. Case–control studies and case series were excluded to develop an evidence base of the highest possible quality.

Multidisciplinary care and supportive care delivery were outside the scope of the present review. Studies published in a language other than English and studies published before 1996 were excluded.

Data Extraction and Quality Assessment

Guidelines based on a systematic review of the relevant literature were assessed for quality using the agree ii instrument¹⁰, a 23-item tool that rates the quality of a guideline in various domains, including scope and purpose, stakeholder involvement, rigour of development, clarity of presentation, applicability, and editorial independence. Systematic reviews were assessed for methodologic quality using the checklist of items provided in amstar¹¹.

For individual studies, the determination of study quality was based on an assessment of study design, balance of baseline patient characteristics, completeness of follow-up, and whether the analysis was adjusted for comorbidities, age, and stage and grade of disease¹². Funding source and outcomes of interest were also extracted. Data extraction was verified by a project research assistant. All authors reviewed and discussed a draft of the evidence summary.

RESULTS

Systematic Reviews

The evidence search identified a guideline published in 1999 by the U.K. National Health Service, Guidance on Commissioning Cancer Services: Improving Outcomes in Gynaecological Cancers – The Manual¹³, and a summary of the associated systematic review¹⁴ that closely aligned with the objectives of our guideline development group. That publication was based on a systematic review of the literature and scored well on most of the agree ii domains. Its evidence base was therefore adopted, and a search for evidence published between 1999 and 2011 was undertaken.

Three additional systematic reviews^12,15,16 that addressed the organization of services for ovarian cancer were identified. The most up-to-date and comprehensive review¹⁵ aligned with the research questions. The working group considered using that systematic review as a source of primary studies; however, it was decided that, because the objectives of that review were so well aligned with the objectives of the present systematic review, the found review¹⁵ would be adopted in its entirety into the evidence base. An additional systematic review¹⁷ found in the January 2015 search was not retained for inclusion in the evidence base because it contained no studies beyond those already captured.

Individual Studies

The search of electronic databases encompassing 1996 to December 2011 identified 3350 unique English-language citations for screening. Ninety of those articles were retrieved for full-text review. Two additional articles for full-text review were identified from a scan of the reference lists of included articles, Google key word searching, and files of working group members. After review, fifteen articles that met the inclusion criteria were retained. Of 3832 non-duplicate records identified in the update search in January 2015, one additional article¹⁸ met the inclusion criteria and was added to the evidence base.

Study Characteristics and Quality Assessment

Improving Outcomes in Gynaecological Cancers – The Manual¹³ included recommendations for the clinical management and organization of services for all gynecologic oncology disease sites. The document scored well on the agree ii domains of scope and purpose, stakeholder involvement, applicability, and clarity of presentation.

A comprehensive ovarian cancer systematic review¹⁵ addressed whether any institutional or physician characteristics are associated with the outcomes of survival, tumour debulking, completeness of staging, and compliance with guidelines for the selection of chemotherapy. This systematic review rated highly on the amstar tool, indicating high-quality methods and reporting, but the body of evidence included in the review was judged to be of lower quality because of the risk of bias inherent in the retrospective nonrandomized design of the studies and other limitations.

Our review also found sixteen primary studies that addressed the centralization of gynecologic oncology services (Table ii). Study locations included the United Kingdom (three studies), elsewhere in Europe (six studies), the United States (five studies), and Canada (two studies). The research design of most studies was retrospective. Data sources included hospitals, regional or national administrative databases and registries, and patient charts. Time periods ranged from the 1990s to about 2005, with the most recent study including data up to 2006. Follow-up times also varied considerably, ranging up to 5 years. Two studies corrected for clustering of outcomes within facilities. The funding source was not stated for most studies; the rest had government funding or a combination of government and private funding. The numbers of patients ranged from 124 to more than 155,000.

TABLE II.

Characteristics of the included studies

Reference	Location	Disease site	Study design	Data source	Era of diagnosis or operative procedure	Follow-up	Correction for clustering	Funding	Pts (n)	Outcomes
Münstedt et al., 200319	Germany	Ovarian and endometrial	R	Hospital registry	1997 to Feb 2001	None	No	NS	1,119 (endometrial) 824 (ovarian)	Rates of surgical procedures, complications
MacDonald et al., 200520	U.S.A.	Endometrial	R	Patient records and tumour registry databases	1990–2003	Median: 3.7 years	No; two tertiary sites investigated	None stated	349	Overall survival, disease-specific survival, disease-free survival, or any local or distant disease event, local recurrence-free survival, and distant metastasis-free survival
Elit et al., 200821	Canada	Ovarian	R	Registry data, administrative data, patient charts	1996–1998	To latest available health insurance data	No	NCIC	1,341	Unnecessary repeated abdominal surgery and long-term survival
Kwon et al., 200822	Canada	Endometrial	R	Administrative data	1996–2000	2005	Yes	Government and private foundation	3,875	Overall survival
Brookfield et al., 200923	U.S.A.	All	R	Statewide database	1990–2000	None	Yes (in facilities)	NS	48,981	30-Day, 90-day, and 5-year overall survival
Kumpulainen et al., 200924	Finland	Ovarian	P	Questionnaire (verified by national registry)	1999	5 Years or death	No	Government	275	Long-term survival, 5-year disease-free survival, and cause-specific survival
Rachet et al., 200925	U.K.	All	R (BA)	National registry	1996–2006	Dec 2007	NA	Government	155,027	1-Year, 3-year relative survival
Vernooij et al., 200912	Netherlands	Ovarian	R	Hospital records	1996–2003	Feb 2006	No	Government	1,077	Adequate staging, optimal debulking, overall survival
Vernooij et al., 200926	Netherlands	Ovarian	R	Hospital records	1996–2003	Feb 2006	No	Government	761	Complete remission, recurrence rate, disease-free survival, overall survival
Bristow et al., 201027	U.S.A.	Ovarian	R	National database	1996–2005	None	No	NS	12,276	Overall survival and likelihood of receiving standard recommended care
Mercado et al., 201028	U.S.A.		R	State registries, hospital databases, AMA physician Masterfile, U.S. census	1991–2004	At least 1 year	No	Government and foundation	31,879	Surgery by specialist type, receipt of an ostomy (proxy for quality of care and life), and time to death
Chan et al., 201129	U.S.A.	Endometrial	R	Administrative data	1991–2002	200 Months	No	Academic	18,338	Overall survival, disease-specific survival
Fago-Olsen et al., 201130	Denmark	Ovarian	R	National registry	2005–2008	10 Sep 2009 or death	No	NS	2,023	Overall survival, optimal cytoreduction, disease-free survival
Yap et al., 201131	U.K.	Vulvar	R (BA)	Hospital data	1995–2003	Unclear	NA	NS	124	Rates of surgical procedures, 5-year cause-specific survival
Crawford and Greenberg, 201232	U.K.	All	R (BA)	Regional and national databases	1996–2003	Aug 2006	NA	NS	3406 (9 hospitals)	Overall survival
Paulsen et al., 201218	Norway	Ovarian	P	National registry; medical, surgical, and histopathology records	2002	0–106 Months	No	NS	198	8-Year survival, median survival

Pts = patients; R = retrospective; NS = not stated; NCIC = National Cancer Institute of Canada; P = prospective; BA = before and after; NA = not available; AMA = American Medical Association.

Outcomes included various survival measures and the quality of surgery. By consensus, the guideline development group judged that the evidence base was of lower quality because of a lack of consistency in independent variables, outcome measures, study populations, and geographic locations, and because of limited control for clustering of outcomes. A meta-analysis was not considered feasible for the same reasons.

Outcomes

Systematic Reviews Addressing Centralization of Gynecologic Oncology Services

Improving Outcomes in Gynaecological Cancers (United Kingdom):

The major findings of Improving Outcomes in Gynaecological Cancers – The Manual¹³ were that survival is improved for ovarian cancer patients who are treated by expert multidisciplinary teams and who undergo surgery by a specialist gynecologic oncologist. The decision to recommend multidisciplinary care was based mainly on a study of ovarian cancer conducted in Scotland, which found that follow-up at a multidisciplinary clinic was an independent predictor of survival at 5 years. The recommendation for treatment by gynecologic oncologists for most patients was based on findings in a prospective study of all patients in Scotland, which found that women with stage iii cancer who were treated by gynecologic oncologists, compared with gynecologists, had a 25% lower death rate at 3 years. Based on those findings (and other lesser-quality evidence), centralization of services was advised, with all patients recommended for treatment by specialist gynecologic oncologists at designated cancer centres, except for those with stage ia or ib disease [stage ia according to the 2009 revised International Federation of Gynecology and Obstetrics (figo) staging system³³], grade 1 or 2 endometrial cancer, and pelvic masses for which the risk of malignancy is low. Cancer units serving smaller populations would refer patients to the designated centres while retaining responsibility for initial diagnostic procedures and surgery for lower-risk cases.

Du Bois et al., 2009:

A comprehensive systematic review of ovarian cancer studies published up to 2007¹⁵ included seventeen studies that reported survival outcomes and eight studies that reported surgical outcomes, all by hospital type. Eighteen of the studies reported survival outcomes, and thirteen reported surgical outcomes—all by physician type. Overall, the review found these trends, while cautioning that the limited evidence showed considerable heterogeneity:

• □ A positive impact on survival with higher degree of physician specialization in six of eleven studies of patients with advanced disease (figo stages iii–iv)

• □ A significant positive effect of physician discipline and subspecialization on surgical outcomes, including staging and extent of debulking

• □ No relationship between institutional characteristics and survival outcome (This association was not tested in a multivariate analysis, however; and could be clustered with other factors such as hospital volume.)

Primary Studies

Our review found sixteen additional studies that met the inclusion criteria and that were not included in the systematic reviews previously described.

Survival Outcomes by Hospital Type:

One study compared outcomes in the Anglia region of England, where centralization of gynecologic oncology services had been implemented by 2000 (Table iii). More than 97% of cases in the study had been histologically confirmed, and only the 60% of cases with stage and grade data were included in the survival analysis. Survival for patients with gynecologic cancer improved significantly post-centralization compared with the pre-centralization study period [hazard ratio (hr): 0.71; 95% confidence interval (ci): 0.64 to 0.79].

TABLE III.

Hazard ratio for survival by hospital type (specialization or centralization of services, or both, compared with decentralization)

Reference	FIGO stage	Disease site	Pts (n)	Hospital type	HR	95% CI	p Value	Covariates in the adjusted model
Elit et al., 200821	I–IV	Ovarian	1341	Centres with GYO	Reference		NS	Age, comorbidity, residence location, stage and grade
				Other regional cancer centre	0.81	0.56 to 1.17
				Remaining centres	0.93	0.74 to 1.16
Kwon et al., 200822	All	Endometrial	3,875	Community	Reference			Age, income, comorbidity index, grade, stage, surgical staging, adjuvant therapy
				Teaching	0.76	0.54 to 1.08	NS
Brookfield et al., 200923	All	All	48,981	Teaching	Reference		0.08	Cancer type, hospital type, hospital volume, age, race, ethnicity, payer, lymph nodes examined, stage, grade, surgery, chemotherapy, radiation, clustering
	SEER summary stages			Non-teaching	1.08	0.99 to 1.18
Rachet et al., 200925	Not reported	(A) Cervical	155,027	Transition from de-central to central 2001–2006	A: +0.3%a	Not available	<0.05	Not reported
		(B) Endometrial			B: +0.3%		<0.01
		(C) Ovarian			C: +0.2%		<0.01
Vernooij et al., 200912	I–IV	Ovarian	1,077	General	Reference			Age, stage
				Specialized	0.8	0.7 to 1.0
Fago-Olsen et al., 201130	IIIC–IV	Ovarian	2,023	Other tertiary	Reference		<0.05	Age, ASA physical status score, ECOG score, comorbidity score, surgery, stage
					0.83c	0.70 to 0.98
Yap et al., 201131	I–IV	Vulva	124	Pre-central	51.3b	Not reported	0.055	Not available
				Post-central	73.8
Crawford and Greenberg, 201232	All	All	3406	Central	Reference		<0.001	Age, stage, grade, year of diagnosis
	TNM stages			De-central	0.71	0.64 to 0.79
Paulsen et al., 201218	IIIC	Ovarian	198	Non-teaching	Reference		NS	Age, histologic type, grade of differentiation, residual disease
				Teaching	1.38	1.00 to 1.89

^aMean annual change in survival 2001–2006 (restricted to patients who survived at least 1 year).

^bFive-year survival, death from a gynecologic malignancy during the 10-year study period.

^cDisease-specific survival.

FIGO = International Federation of Gynecology and Obstetrics; Pts = patients; HR = hazard ratio; CI = confidence interval; GYO = gynecologic oncologist; NS = nonsignificant; SEER = Surveillance, Epidemiology, and End Results; ASA = American Society of Anesthesiologists; ECOG = Eastern Cooperative Oncology Group. Values in boldface type are statistically significant.

Another study²⁵ looked at outcomes before and after the implementation of the U.K. National Health Service cancer plan for England in 2000 and found significant improvements in mean annual survival for cervical (p < 0.05), endometrial (p < 0.01), and ovarian cancer (p < 0.01) between 2001 and 2006.

In Denmark, the treatment of ovarian cancer was slowly centralized over a decade, and subsequently, a significant reduction in mortality for patients with stage iiic–iv ovarian cancer treated in tertiary centres, compared with other facilities, was found (hr: 0.03; 95% ci: 0.70 to 0.98)³⁰, although data on the involvement of gynecologic oncologists was unavailable.

In one of the few studies to control for the tendency of outcomes to be clustered within facilities²³, no significant differences in overall survival by hospital type over a 10-year period were found. A study of ovarian cancer found no difference in survival for centres with a gynecologic oncologist compared with other centres²¹. Another found no difference in the hr for overall survival of endometrial cancer patients between community and teaching hospitals²². One study²⁶ found a significant improvement in overall survival for patients in facilities with two or more medical oncologists (hr: 0.8; 95% ci: 0.7 to 1.0; data not shown in Table iv), that variable being used as a proxy for centralization.

TABLE IV.

Surgical outcomes, by hospital type (specialization and/or centralization of services vs. decentralization)

Reference	FIGO stage	Disease site	Pts (n)	Hospital type	Outcome (% or OR)	p Value or 95% CI	Covariates in adjusted model
Lymphadenectomy performed
Münstedt et al., 200319	IC–II (ASA<III)	Endometrial	1119	Primary	15.8	0.001	Not available
				Secondary	28.4
				Tertiary	52.6
				Central	47.9
	III (ASA<III)	Ovarian	824	Primary	0	0.046
				Secondary	20
				Tertiary	32
				Central	38
Vernooij et al., 200912	I–IIA	Ovarian	1077	General	Reference		Age, stage
				Semi-specialized	4.6	2.3 to 9.2
				Specialized	3.9	2.0 to 7.6
Yap et al., 201131	I–IV	Vulval	124	Pre-central	46	0.003	Not available
				Post-central	76
Optimal debulking
Vernooij et al., 200912	III	Ovary	1077	General	Reference		Age, stage
				Specialized	1.7	1.1 to 2.7

FIGO = International Federation of Gynecology and Obstetrics; Pts = patients; OR = odds ratio; CI = confidence interval; ASA = American Society of Anesthesiologists physical status score. Values in boldface type are statistically significant.

Survival Outcomes by Physician Type:

Six studies reported survival outcomes by physician type (Table v), including three studies of patients with ovarian cancer^21,24,28 and three studies of patients with endometrial cancer^20,22,29. Four of those studies included patients with figo stage i–iv disease^21,22,24,29. One study included only patients with stage ia–iia endometrial cancer²⁰.

TABLE V.

Hazard ratio for survival, by physician type

Reference	FIGO stage	Disease site	Pts (n)	Physician type	HR	95% CI	p Value	Covariates included in adjusted model
MacDonald et al., 200520	IA–IIA	Endometrial	349	GYO	1.3	0.9 to 1.7	0.13	Age, HIR disease, adjuvant radiation therapy
				GYN	Reference
Elit et al., 200821	I–IV	Ovarian	1,341	GYO	Reference		Not reported	Age, comorbidity, residence location, stage and grade
				GYN	1.02a	0.81 to 1.30
				GS	1.19	0.90 to 1.58
Kwon et al., 200822	All	Endometrial	3,875	GYO	1.23	0.95 to 1.59	Not reported	Age, income, co-morbidity index, grade, stage, surgical staging, adjuvant therapy
				Other	Reference
Kumpulainen et al., 200924	I–IV	Ovarian	275	GYO	Reference		0.403	Age group, FIGO stage, hospital volume, operating physician, residual disease, differentiation, and primary chemotherapy
				GYN	1.237	0.75 to 2.03
Mercado et al., 201028	IIIC/IV	Ovarian	31,897	GYO/GYN	Reference			Age, comorbidity, urban/rural hospital location
				GS	1.63	1.56 to 1.71	<0.0001
				Other	1.56	1.52 to 1.61	<0.0001
Chan et al., 201129	I–IVb	Endometrial	18,338	GYO	0.71c	0.62 to 0.82	0.001	Age, stage, grade
				Other	Reference

^aSurvival time from initial surgery to date of death from any cause. Follow-up to latest available health insurance data.

^bAmerican Joint Committee on Cancer codes.

^cDisease-specific survival.

FIGO = International Federation of Gynecology and Obstetrics; Pts = patients; HR = hazard ratio; CI = confidence interval; GYO = gynecologic oncologist; GYN = gynecologist; HIR = high–intermediate risk of local failure (stage IB; grade III, IC; grade II or III or stage IIA); GS = general surgeon. Values in boldface type are statistically significant.

The study that reported outcomes for advanced-stage patients (figo iiic or iv ovarian cancer) was the only one to find a significant effect of treatment by the combined reference group of gynecologic oncologists and gynecologists compared with general surgeons (hr: 1.63; 95% ci: 1.56 to 1.71) or with other physicians (hr: 1.56; 95% ci: 1.52 to 1.61)²⁸. The rest of the studies did not find a significant difference between subspecialists and other physician types.

Surgical Outcomes by Hospital Type:

A study³¹ found that before centralization in the West Midlands, England, 15 different surgical procedures had been described for the treatment of vulvar cancer³⁴. After centralization, only 4 types of surgery were performed, and 84% of patients who required lymph node dissection underwent the procedure, although heterogeneity of surgical technique remained evident. Implementation of centralization also coincided with improved histology reporting and achievement of adequate excision margins³¹.

In a population of patients for whom lymphadenectomy was recommended and feasible, the procedure was significantly more likely to be performed in central hospitals than in primary, secondary, and tertiary hospitals (endometrial cancer: p = 0.001; ovarian cancer: p = 0.046); however, even in the central sites, adherence to appropriate guidelines was found to be lacking¹⁹. Two other studies that assessed the rate of lymphadenectomy in patients for whom that procedure was recommended found that performance of the procedure was significantly more likely at semi-specialized [odds ratio (or): 4.6; 95% ci: 2.3 to 9.2] or specialized hospitals (or: 3.9; 95% ci: 2.0 to 7.6)^12,31 than at general hospitals, and more likely after than before centralization (76% vs. 46%, p = 0.003). One study that assessed optimal debulking also found that procedure to be significantly more likely in specialized than in general hospitals (or: 1.7; 95% ci: 1.1 to 2.7)¹².

Surgical Outcomes by Physician Type:

Two studies reported rates of lymphadenectomy performance by physician type (Table vi). One of them, which included endometrial cancer patients with figo stage ia–iia disease, reported a significant difference between gynecologic oncologists and gynecologists (79% vs. 23%, p = 0.006)²⁰. The other, which included ovarian cancer patients with figo stage i–iia disease, reported a significantly greater odds of lymphadenectomy being performed by a gynecologic oncologist (or: 9.5; 95% ci: 4.7 to 19.0) or semi–gynecologic oncologist (or: 8.5; 5% ci: 3.8 to 19.3)¹² than by a gynecologist. In another study²¹, the risk of repeat surgery was significantly higher with gynecologists (or: 6.54; 95% ci: 2.5 to 16.9) or general surgeons (or: 16.97; 95% ci: 6.4 to 45.3) than with gynecologic oncologists.

TABLE VI.

Surgical outcomes, by physician type (specialist or non-specialist)

Reference	FIGO stage	Disease site	Pts (n)	Physician type	Outcome measure	p Value or 95% CI	Covariates in adjusted model
Lymphadenectomy performed
MacDonald et al., 200520	IA–IIA	Endometrial	349	GYO	79%	0.006
				GYN	23%
Adequate staging
Vernooij et al., 200912	I–IIA	Ovarian	1077	GYN	Reference (OR)		Age, stage
				Semi-GYO	8.5	3.8 to 19.3
				GYO	9.5	4.7 to 19.0
Relative risk of repeat surgery
Elit et al., 200821	I–IV	Ovarian	1341	GYO	Reference (RR)		Age, comorbidity, residence location, stage, and grade
				GYN	6.54	2.5 to 16.9
				GS	16.97	6.4 to 45.3

FIGO = International Federation of Gynecology and Obstetrics; Pts = patients; CI = confidence interval; GYO = gynecologic oncologist; GYN = gynecologist; OR = odds ratio; RR = relative risk; GS = general surgeon. Values in boldface type are statistically significant.

Chemotherapy-Related Outcomes:

One study found that, in addition to being more likely to perform complete surgical staging, gynecologic oncologists were more likely than other physicians to deliver chemotherapy²⁹.

Organization of Gynecologic Pathology:

Four articles that addressed the rates of discrepancy in initial diagnoses and intraoperative consultation between non-specialist pathologists and gyne-oncology–specialist pathologists were identified^35–38. In one hospital, intraoperative consultation (that is, analysis of frozen sections) for gynecologic surgery by gynecologists was provided by surgical pathologists; subspecialized gynecologic pathologists provided that support for gynecologic oncologists. In that setting, the rate of major discrepancies between intraoperative consultation and final pathology was significantly increased for the non-specialist pathologists compared with the subspecialist pathologists (p = 0.0266)³⁵.

Another study that assessed the use of frozen sections in ovarian cancer found that non-specialist pathologists were significantly more likely than gynecologic oncologist pathologists to “misdiagnose” a tumour. The study found that accurate intraoperative diagnosis of borderline ovarian tumours depended mainly on the level of experience of the pathologist³⁶. Similarly, Bige et al.³⁷ looked at the accuracy of frozen sections in ovarian cancer with the aim of identifying the role of the gynecologic pathologist based on level of experience. Sensitivity and specificity were higher in the subspecialist group (p value not reported), and more malignant tumours diagnosed by frozen section were found to be discordant with the final diagnosis in the group of non–gynecologic oncology pathologists.

Another assessment of intraoperative consultation compared the diagnostic error rates in a specialist gynecologic pathology unit and in a general pathology laboratory. It found that errors attributable to the quality of technical preparation and pathologist misinterpretation were more common in the general pathology laboratory; however, because several pathologists worked in both laboratories, it was not possible to conclude that the observed discrepancy was a result of experience or expertise³⁸.

DISCUSSION

The present systematic review analyzes the evidence for organizational factors that affect patient outcomes (surgical and survival) in gynecologic oncology. The research method used was systematic and comprehensive, but the resulting evidence base was of limited quality and largely comprised nonrandomized retrospective studies with inconsistent definitions of comparison groups and outcomes. A significant limitation of the literature in this area is the failure account for the “clustering” phenomenon: the fact that patients treated within the same facility are not entirely independent, and that the outcomes of patients treated in a single facility tend to be similar²³. Most of the studies included in the evidence base did not account for clustering, and the effect of hospital type might therefore have been exaggerated. For that reason, it is difficult to draw strong conclusions from the available literature on this topic. In addition, although our review attempted to assess the effect of centralization on outcomes in gynecologic oncology, the systematic review and most of the included primary studies considered patients with ovarian cancer; fewer data were available on other gynecologic cancers. However, despite the lack of evidence from randomized studies, some trends were observed.

Studies found a positive relationship between completeness of cytoreduction and survival in advanced disease²⁴. In patients with early-stage disease confined to the ovary, treatment involves extensive surgical staging to rule out occult metastatic disease³⁹. A previously published high-quality systematic review that assessed the relationship between organizational factors and outcomes in ovarian cancer concluded that subspecialty care (by a gynecologic oncologist) is associated with better surgical outcomes than is care delivered by non-subspecialists and has a positive effect on survival for patients with advanced disease; institutional characteristics were found to have a smaller effect on outcomes¹⁵. Our review concurs with the finding that, for advanced-stage ovarian cancer patients, care delivery by subspecialist gynecologic oncologists is associated with better outcomes.

With respect to pathology, our review found that intraoperative consultation should be rendered by gynecologic pathologists when feasible, or that gynecologic pathologists should be available to provide consultation³². Such consultation would require centralization to ensure a sufficient caseload. A significant improvement in overall survival for ovarian cancer patients was also found in facilities with a higher number of medical oncologists, suggesting that, where geographic distance allows, delivery of chemotherapy in addition to surgery could benefit from concentration in a specialized centre²⁶. However, the latter finding (from a single study) might in fact reflect a benefit of hospital type.

Three studies found a significant improvement in survival for gynecologic oncology patients after centralization of services (compared with an earlier decentralized model). Studies also found that, in more centralized models of care, surgery was more likely to be standardized and lymphadenectomy to be performed when indicated. In one study, the improvements were attributed to multiple features of centrally organized care, including central pathology review for high-risk endometrial cancer, state-of-the-art imaging, more extensive specialist surgery resulting in better staging and more tailored adjuvant therapy, use of the Risk of Malignancy Index to make appropriate referrals, multidisciplinary review for patients having non-specialist surgery, and early discussion of cases in the “unit” hospital. Overall, the major differences were summarized as “access to specialized surgery” and “management within a multidisciplinary team”³⁵. At the same time, one study found no difference in survival for ovarian cancer patients treated in centres with subspecialist gynecologic oncologists than in other centres. Compared with studies that assessed survival, studies of surgical outcomes were more likely to find significant differences. The reasons for that discrepancy are not clear and could be the subject of future research.

CONCLUSIONS

The evidence found in the present review is consistent with previous research showing a likely benefit from the delivery of gynecologic oncology care in specialized centres with subspecialists working as part of a multidisciplinary team—particularly for patients with more advanced ovarian cancer. It should be cautioned, however, that unlike other disease sites such as pancreas and esophagus⁴, the evidence for this finding is far from strong.

Because of the lower-quality nature of the evidence base, an expert consensus process was used to create an organizational guideline, the results of which are published separately⁴⁰. Briefly, the consensus process led to recommendations for the performance of definitive surgery for most invasive cancers by subspecialist gynecologic oncologists within designated gynecologic oncology centres. The recommendations indicate that some services, such as radiation therapy, could be provided in other affiliated centres. Multidisciplinary team management is also endorsed, and recommendations are provided for human and physical resource needs and some aspects of pathology. The recommendations are intended to minimize provincial variations in practice and to make best use of limited resources.

Our review also found that, even when practice and outcomes appeared to have improved under a centralized model, heterogeneity of technique remained, even among groups of subspecialists. That finding suggests that a plan to implement care in centralized or specialized facilities featuring subspecialists and multidisciplinary care should also include the adoption of appropriate guidelines across the care continuum and of the necessary system processes and evaluation plans. It will be a challenge to implement those changes across a health care system spanning a large and variable geographic area with a range of independent hospitals.

CONFLICT OF INTEREST DISCLOSURES

We have read and understood Current Oncology’s policy on disclosing conflicts of interest, and we declare the following interests: TC has received consultant fees from LifeLabs Medical Laboratory Services and has managerial responsibility as a section head for Cytopathology and Gynaecological Pathology at Mount Sinai Hospital, Toronto, Ontario.