Introduction
Cervical cancer is the fourth most common malignancy globally and is characterized
by geographic variation in incidence and mortality rates, secondary to inequalities
in vaccination and screening rates and availability of health care services.[1] In India, there were 123,907 new cases and 77,348 deaths in 2020 which contributed
to 1/5th of the global burden of new cases and deaths.[2] Surgery is the primary mode of management for early International Federation of
Gynecology and Obstetrics (FIGO) 2018 stage IA1, IA2, IB1, 1B2, and select IB3 and
IIA1 disease.[3] The 5-year survival rate for stage I disease is as high as 92%. Favorable survival
rates in early-stage operable disease is an outcome measure of tailored, quality radical
surgery.[4]
The quality of oncologic surgery impacts oncologic outcome of cancer survivors. The
European Society of Gynaecologic Oncology (ESGO) has developed a set of 15 quality
indicators which have been categorized as structural, process, and outcome indicators
with measurability and target specifications.[5] It has been suggested that the indicators be used as a reference guideline for self-assessment,
to develop quality assurance programs based on preset standard of care in the surgical
management of carcinoma cervix.
Periodic clinical audit using predefined, realistic standard quality measures is a
quality improvement exercise to improve patient outcomes; if identified deficiencies
are addressed. The objective of this audit was to assess the compliance of an ESGO-accredited
gynecologic oncology center in India, to the ESGO quality indicators for surgical
management of carcinoma cervix.
Materials and Methods
Electronic medical records of 82 patients with operable carcinoma cervix who underwent
surgical management in the department of gynecologic oncology in a tertiary care center
in South India, during the period June 1, 2017 to May 31, 2020 were retrieved and
retrospectively analyzed to assess compliance to the ESGO quality indicators.
ESGO quality indicators: ESGO has put forth 15 indicators under 5 categories. The
first set of quality indicators (QI, 1–2) is related to surgical volume and training.
The second set (QI, 3–5) of indicators pertains to overall management which includes
the number of ongoing clinical trials at the mentioned center, pretreatment discussion
at multidisciplinary meetings, and adequacy of preoperative evaluation. The third
set of quality indicators (QI, 6–8) concerns relevant and structural reporting of
surgical and pathological information and postoperative complications. The fourth
set of indicators (QI, 9–12) addresses surgical quality in terms of postoperative
urological fistula rate, tumor-free margin status, postoperative stage shift of T1b
disease, and 2-year recurrence rates of surgically managed pT1b1N0 disease. The final
set (13–15) of indicators refers to conformance to standards of care concerning intraoperative
lymph nodal assessment, counseling for fertility-sparing treatment when relevant,
and postoperative adjuvant radiation rate.
Inclusion Criteria
Patients with invasive carcinoma cervix with FIGO 2009 clinical stages IIA1 or less
who underwent primary surgical management during the study period were included.
Statistical Analysis
The data were analyzed using IBM SPSS Statistics for Windows, version 22 (IBM Corp.,
Armonk, New York, United States). Continuous variables are presented as mean or median
and categorical variables are presented as percentages.
Results
Compliance to Indicators Related to Surgical Volume and Training (QI, 1–2)
Over the 3 years, 82 patients underwent primary surgical management for carcinoma
cervix, with a mean number of 24 (range: 21–29) parametrectomies performed per year.
This met the minimum target but was short of the optimal target of 30. During this
period, 122 patients with cervical cancer underwent surgeries for diagnostic indications
such as examination under anesthesia and therapeutic indications ([Table 1]) which included radical hysterectomy following neoadjuvant chemotherapy, exenteration,
besides palliative surgeries. All patients were operated either by a certified gynecologic
oncologist or a trainee being supervised by a certified gynecologic oncologist, achieving
the prerequisite target.
Table 1
Surgical procedures performed (n = 122)
|
Surgery performed
|
Number (n = 122)
|
|
Primary surgery for carcinoma cervix
|
82
|
|
Pelvic exenteration for recurrent carcinoma cervix
|
5
|
|
Post-NACT radical hysterectomy
|
4
|
|
Post-RT hysterectomy for residual disease
|
4
|
|
Cone biopsy
|
11
|
|
Examination under anesthesia ± biopsy
|
3
|
|
Pyometra drainage
|
3
|
|
Palliative procedures for recurrence
(ileostomy, pyometra washout, biopsy for recurrence detection)
|
9
|
|
Resuturing for wound dehiscence following primary surgery
|
1
|
Abbreviations: NACT, neoadjuvant chemotherapy; RT, radiation therapy.
Compliance to Indicators Related to Overall Management (QI, 3–5)
The center was involved in four clinical trials during the study period. However,
as against the prerequisite mandatory preop discussion of every patient at multidisciplinary
team (MDT) meetings, only 46% of our patients were discussed ([Table 2]). Preoperative investigations before surgery according to the ESGO-the European
Society for Radiotherapy and Oncology-the European Society of Pathology (ESGO-ESTRO-ESP)
guidelines include pelvic examination, preoperative biopsy, magnetic resonance imaging
(MRI), and extended investigations in case of suspicious nodal involvement.[6] Though 74% patients had undergone all the essential investigations, the target of
100% was not met.
Table 2
ESGO quality indicators
|
Quality indicators
|
Target
|
Achieved
|
|
No of radical procedures done per year
|
15
|
24
|
|
Surgeries performed or supervised by gynecologic oncologist
|
100%
|
100%
|
|
No. of clinical trials being conducted
|
> 1
|
4
|
|
Treatment discussed at MDT
|
100%
|
46% (37/82)
|
|
Complete preoperative workup
|
100%
|
74% (61/82)
|
|
Optimal surgical report
|
100%
|
7% (6/82)
|
|
Optimal pathological report
|
≥ 90%
|
49% (40/82)
|
|
Structured reporting of postoperative morbidity
|
≥ 90%
|
78% (64/82)
|
|
Urological fistula rate within 30
postoperative days
|
≤ 3%
|
0
|
|
Clear surgical margins
|
≥ 97%
|
82% (67/82)
|
|
T-upstaged T1b disease
|
< 10%
|
16% (9/55)
|
|
Recurrence of T1b1 disease
|
< 10%
|
15% (6/39)
|
|
Standard lymph node staging
|
≥ 98%
|
7% (6/82)
|
|
Fertility sparing treatment
|
100%
|
100%
|
|
Received adjuvant treatment
|
< 15%
|
51% (20/39)
|
Abbreviations: ESGO, European Society of Gynaeacological Oncology; MDT, multidisciplinary
team.
Compliance to Indicators Related to Surgical, Pathological, and Postoperative Complication
Reporting (QI, 6–8)
The next set of indicators was related to recording pertinent information. The ESGO-ESTRO-ESP
have set recommendations to record key elements in surgical and pathological reports
and structured recording of postoperative complications. Only 7% of patient's surgical
reports ([Table 3]) and 49% of the pathological reports met the ESGO standards ([Table 4]). As per the specifications, 78% had structured reporting of complications.
Table 3
Components of complete surgical report (n = 82)
|
Components of complete surgical report
|
Achieved
|
|
Surgical approach
|
100% (82)
|
|
Type of LN staging
|
100% (82)
|
|
Technique of sentinel lymph node detection
|
Not applicable
|
|
Localization of sentinel lymph node
|
Not applicable
|
|
Level of pelvic lymphadenectomy
|
98% (81/82)
|
|
Type of parametrial resection
|
11% (9/82)
|
|
Type of adnexal procedure
|
95% (78/82)
|
|
Duration of surgery
|
84% (69/82)
|
|
Blood loss
|
92% (75/82)
|
|
Intraop complication - type/grade/management
|
94% (77/82)
|
Abbreviation: LN, lymph node.
Table 4
Components of complete pathologic report (n = 82)
|
Components of complete pathologic report
|
Achieved
|
|
Description of the specimen
|
100% (82)
|
|
Macroscopic description of specimen
|
100% (82)
|
|
Macroscopic tumor site
|
85% (70/82)
|
|
Tumor dimensions
|
79% (65/82)
|
|
Histological tumor type and grade
|
97% (80/82)
|
|
Lymphovascular space involvement
|
96% (79/82)
|
|
Coexisting pathology
|
100% (82)
|
|
Distance of uninvolved cervical stroma
|
100% (82)
|
|
Margin status
|
83% (68/82)
|
|
Lymph node (LN) status, including sentinel lymph node
|
100% (82)
|
|
Pathologically confirmed distant metastases
|
99% (81/82)
|
|
Provisional pathological staging
|
83% (68/82)
|
|
The results of any frozen section specimen evaluation
|
100% (82)
|
Compliance to Indicators Related to Quality of Surgical Procedures (QI, 9–12)
Regarding indicators addressing quality of surgical procedures, there were no urological
fistulas during this period. As against the desired target of ≥ 97% who have disease-free
vaginal and parametrial margins postoperatively, 67/82 (82%) had clear margins, 5
patients had involvement of margin by invasive malignancy, and there was no comment
about margin status in 10 patients. Proportion of patients with stage T1b disease
who were upstaged based on tumor extent after surgery was 16%, as against the target
of 10%. Recurrence rate at 2 years in patients with stage TIb1 disease without nodal
involvement was 15% (6/39) in contrast to the advised target of < 10%. Four of the
six recurrences were treated with radiation, one received palliative chemotherapy,
and one opted for no treatment.
Compliance to Indicators Related to Standard of Care (QI, 13–15)
The final three indicators assess the compliance of management with standard of surgical
care. Only 7% of our patients had undergone lymph node staging according to the ESGO-ESTRO-ESP
guidelines as against the needed target of ≥ 98%. All eligible patients for fertility-sparing
surgery were counseled. Approximately 50% of patients with pT1b1N0 disease received
adjuvant radiation (target: < 15%) ([Table 4]).
Discussion
In India, cervical cancer contributed to 9.4% of the total cancer patients in 2020
and is one of the leading causes of cancer-related deaths in the country.[7] This is typical in the absence of an organized screening and vaccination program.
Gynecologic oncology subspeciality training began a few decades later in India compared
with the west. Our department began as a unit of gynecology, specializing in the treatment
of gynecologic cancer in 2011, which later transitioned into a department of gynecologic
oncology in 2016 in a tertiary referral center in southern India. Around 150 cases
of cervical cancer per year are seen in the outpatient department and around 500 patients
were seen over during this study period, of whom 82 underwent surgery for early disease.
Subspeciality training has been shown to be effective to impact treatment decisions
and improve survival outcomes of women with ovarian, endometrial, and cervical cancer.[8]
[9]
[10] This audit was performed to assess our compliance to set standards as an exercise
for self-improvement. A total of 5 out of 15 quality indicators were met by the center
([Fig. 1]).
Fig. 1 Compliance to European Society of Gynaeacological Oncology (ESGO) quality indicators.
Compliance to Indicators Related to Surgical Volume and Training (QI, 1–2)
Most patients present with advanced disease to our department in a tertiary referral
center, due to lack of organized, national screening programs and hence the optimum
target of ≥ 30 was not met. Data from other regional referral centers in India report
only 11.4% present with early, operable carcinoma cervix.[4] As an academic training center, we fulfilled the minimum criteria regarding case
volume, training, and research activities. All cases were performed or supervised
by trained gynecologic oncologists.
Compliance to Indicators Related to Overall Management (QI, 3–5)
Cervical cancer case burden and mortality afflicts the low- and middle-income countries
and with this consideration, the revised staging by FIGO does not mandate but encourages
preoperative usage of MRI,[11] due to its inherent soft tissue resolution and multiplanar capability. However,
despite cost constraints, there has been greater usage of MRI over the years by the
department,[12] in preoperative evaluation . However, patients with clinical impression of stage
IA1, post-cone, and those with severe financial limitation did not undergo a preoperative
MRI in this study. Preoperative MDT discussion with the involvement of multiple concerned
specialities allows comprehensive discussion and implementation of best, individualized
therapeutic strategy along with adherence to clinical guidelines. During this period,
only 46% of the patients were preoperatively discussed in MDT and after the results
of the audit, preoperative MDT discussion has been made mandatory in the department.
Compliance to Indicators Related Surgical, Pathological, and Postoperative Complication
Reporting (QI, 6–8)
Structured operative reports allow clear, scientific documentation of operative procedures
which capture and allow easy interpretation of discrete data elements. Similarly,
synoptic pathological reports allow concise recording of essential parameters, compliance
with standardized diagnostic criteria and terminology, and permit easy storage and
retrieval of information. Surgical and pathological reports are key components of
patient risk stratification and treatment plan decision. ESGO has laid requirements
for key elements to be incorporated in surgical and pathological reports.[6] In the absence of a reporting template, both surgical and pathological reports were
deficient. Assessment of the existing surgical reports revealed deficiency in recording
the type of parametrectomy ([Table 1]). Pathological reports were deficient in reporting tumor dimension, tumor location,
margin status, and provisional pathological staging ([Table 3]). Similarly, in the absence of any followed classification system of documenting
complications, complications were described in the electronic records of these patients
but were not graded.
Compliance to Indicators Related to Quality of Surgical Procedures (QI, 9–12)
The indicators describing the quality of surgical procedures were not achieved. The
use of MRI and multidisciplinary discussion help in proper patient selection, achieving
clear vaginal and parametrial margin status, and thereby decreasing the chance of
postoperative upstaging of tumors and morbidity associated with dual-modality treatment.
Clear surgical margins are an obligate requirement for optimal oncological outcome.
In our audit, 16% were upstaged following surgery.
The practice of intraoperative frozen section of pelvic lymph nodes and sentinel lymph
node assessment is not followed in our center and hence the target regarding lymph
node staging was not met.
Compliance to Indicators Related to Standard of Care (QI, 13–15)
Twenty of 39 patients (51%) with pT1bN0 received adjuvant therapy. The overall adjuvant
treatment rate was 37.8% (31/82). Four patients among the 11 with high-risk factors
received adjuvant treatment for nodal involvement while 7 had vaginal or parametrial
involvement.
This high adjuvant rate among pT1bN0 is primarily due to selection of larger tumors
and subsequent postoperative radiation for intermediate risk factors. This audit's
revelation of high adjuvant radiation and high recurrence rate despite high adjuvant
treatment rate has been of concern. Efforts have been made to evaluate the cause and
rectify the increased rate of adjuvant treatment.
Results in the Context of Published Literature
Much progress has been made in cancer surgery secondary to subspecialization with
a focus on site-specific surgeon education and training in appropriate decision making.
Quality of cancer surgery and care is paramount to patient outcome and this has been
studied and highlighted since the start of the century.[13] The quality of surgery done has a role in local control and survival. The aim of
the surgery should be to remove the tumor completely, with tumor-free margins which
prevent local recurrence.
Surgical management of early cervical cancer with tumor-free margins has been associated
with more than 90% disease-free survival.[14] To achieve the desired surgical outcome, there should be a feedback system based
on evidence-based standards by which the performance of a surgical team is continually
assessed. Clinical audits and quality improvement projects with set clinical standards
help identify deficiencies and help improve patient care. To measure quality of surgery
and cancer care, professional bodies have proposed quality indicators which need to
be examined, validated, and incorporated into quality assurance programs.
Measurement of quality indicators gives quick objective insight into the efficiency
of an institution. Before the implementation of quality indicators into a quality
improvement program, their measurability, reliability, and their potential for use
need to be ascertained. Though several indicators have been put forth over the last
two decades, their efficiency in improving quality needs to be validated. The quality
indicators put forth by ESGO in 2020, focus on surgical management and have the advantage
of being put forth by an apex body. It helps to objectively measure the quality of
surgical care with realistic quality goals.
Since its introduction, ESGO quality indicators have been used for various purposes.
Ponce et al used six outcome indicators to report oncologic and surgical outcomes
following robotic radical hysterectomy in multiple centers in the Iberian Peninsula.
Five out of the six outcome indicators were met with the exception of high adjuvant
treatment rate (28%).[15]
The SUCCOR study reported a difference in oncologic outcomes following a retrospective
analysis of patients operated by open and minimally invasive approach across various
European centers.[16] A follow-up publication showed compliance to the ESGO quality indicator impacted
oncologic outcome impact.[17]
A high-volume center in China reported compliance with the ESGO quality indicators.
They had retrospectively assessed 5,952 patients who underwent surgery. The center
had met most targets but identified targets which required improved compliance, namely,
mandatory pretreatment discussion at multidisciplinary meetings, prerequisite preoperative
workup (19.7% patients had incomplete workup), postoperative upstaging rate of T1b
(14.7%), and an increased adjuvant rate which was 28.3%.[18] There have been no other reports from centers from developing countries which have
reported compliance with the ESGO quality indicators.
Our center, situated in southern India, is culturally and socially different from
established European centers. This audit has revealed deficiencies which need corrective
practices to be implemented. Greater adoption of preoperative advanced imaging, mandatory
preoperative MDT discussion, and structured surgical, postoperative complication,
and pathological reporting have been introduced. There is a need for uptake of these
quality indicators into a quality assurance program in all developing oncologic centers,
to ensure uniformity in surgical practices which in turn will result in the desired
oncologic outcome. Despite the need to measure up to quality indicators, these quality
indicators need to be tailored for non-European lower middle-income countries where
routine preoperative MRI scans, sentinel lymph node mapping, and intraoperative frozen
section may not be possible.
Strengths and Limitations of the Study
The strength of this study is that this is from a young gynecologic oncology department
from a single institution, located in a developing country, which desires to improve
patient care by critically analyzing itself. From the outcome of this study, it plans
to reaudit itself after implementation of corrective measures. The limitations of
this study is that during this retrospective audit, specific procedures considered
essential for meeting the quality standards, such as sentinel node dissection, were
not implemented during the study period and might be implemented only in research
settings in the institution.
Implications for Practice and Future Research
We have modified our surgical, pathological, and postoperative morbidity reporting
according to the guidelines. We plan to analyze our compliance after implementing
the above changes in clinical practice. While we need to be at par with western standards,
we also need to develop culture-sensitive quality indicators as sentinel lymph node
mapping in cervical cancer might not applicable in countries like India until they
become part of a mandatory guideline.
