Introduction
Cervical cancer ranks fourth among the most frequently diagnosed cancer in women (570,000 cases) [
1], and radical hysterectomy (RH) with bilateral pelvic lymph node dissection is the recommended surgical treatment for women with early-stage disease [
2]. The guidelines from the National Comprehensive Cancer Network (NCCN), International Federation of Gynecology and Obstetrics (FIGO) and National Institute for Health and Care Excellence (NICE) state that “the standard approach for RH is with an open abdominal approach” [
2‐
4]. Although patient-related factors and clinical factors, such as obesity, diabetes, FIGO stage, the lack of standard medical care, surgical approach and hospital volume, are known to influence major complications during RH, there is growing recognition that surgeon volume also affects the outcomes for RH [
5‐
8].
Regarding cervical cancer, the current engagement literature is focused mostly on the effects of hospital volume on clinical outcomes, with less attention given to the effects of surgeon volume on perioperative outcomes. For patients with early-stage cervical cancer, surgery at high-volume centres is associated with lower reduced perioperative morbidity and improved survival, whereas for patients with locally advanced disease, hospital volume has a minimal impact on survival [
9‐
11]. In addition to resources available at the hospital, the outcome of a surgical procedure may depend mainly on surgeon volume [
12]. Accumulative evidence to date has suggested that higher surgeon volume leads to improved perioperative surgical outcomes for various cancer, such as oesophageal cancer, brain tumours, pancreatic cancer, bladder cancer, endometrial cancer, rectal cancer and lung cancer [
13‐
19]. However, some scholars argue that surgeon volume is not associated with complications [
20,
21]. Recognition of the volume-outcomes paradigm in high-risk cancer procedures has led to changes in practice. Consequently, some health systems are instituting a minimum surgeon volume standard for high-risk surgery, such as oesophagectomy [
19]. Wright et al. demonstrated that women treated by high-volume surgeons had fewer postoperative medical complications and lower transfusion requirements after abdominal RH (ARH) [
22]. To date, few studies have investigated the association between surgeon volume and outcomes of RH in a cohort of abdominal cases and laparoscopic cases, respectively. In addition, there is a paucity of data on surgeon volume in Asian populations.
The objective of this population-based analysis is to explore the association between annualized surgeon volume and complications in an ARH cohort and a laparoscopic radical hysterectomy (LRH) cohort, respectively.
Methods
Data source
Data from the Major Surgical Complications of Cervical Cancer in China (MSCCCC) project database were utilized. The MSCCCC database is a multicentre retrospective database established to measure surgical quality. Approximately 97.5% of cases from the database could be matched to the cases in the Chinese Clinical Cervical Cancer (FOUR-C) project (
http://www.chictr.org.cn/index.aspx, ChiCTR1800017778). The MSCCCC database gathers hospitalization information for 36,543 patients from 42 hospitals in 14 provinces of China from 2004 to 2016 (updated June 2020). The 42 hospitals consist of 32 general hospitals, 4 cancer centres and 6 women and children’s hospitals (W&C hospitals) [
23].
By using the discharge diagnosis of “cervical cancer” as the keyword or the International Classification of Diseases Tenth Revision code C53.9 for computerized search, specially-trained gynaecologists abstracted data from medical records and the hospital information system. The documentation used for data extraction on complications included inpatient medical records for surgical treatment, postoperative adjuvant therapy records within 6 months, outpatient records, and readmission to the another department for complication treatment within 2 years [
23]. The MSCCCC database collects data on patient demographics, clinical characteristics, and hospital factors. After completion of double data entry, data checking was carried out by two independent gynaecologists to eliminate input errors and logic errors. Data masking was used to protect patient privacy. Ethical approval was obtained from the Institutional Ethics Committee of Southern Medical University Nanfang Hospital (NFEC-2017–135).
Cohort identification
Women who underwent RH for cervical cancer between 2004 and 2016 were analysed. The inclusion criteria were as follows: (1) the patient had been diagnosed with stage IA1 with LVSI (lymphovascular space invasion) to stage IIB disease, according to the 2009 FIGO staging system; (2) the patient had undergone type B or C RH (Querleu and Morrow classification) [
24] + pelvic lymphadenectomy (PLN) ± para-aortic lymphadenectomy (PALA); and (3) the patient had undergone ARH or LRH. RH is mentioned as a treatment option for stage IIB disease in the Japan Society of Gynaecologic Oncology guidelines 2017 [
25]. Chemoradiotherapy and neoadjuvant chemotherapy (NACT) followed by RH are recommended for patients with stage IIB cervical cancer in the European guidelines [
26]. As such, we also included patients with FIGO stage IIB.
The exclusion criteria were as follows: (1) the patient was diagnosed with cervical cancer during pregnancy, was diagnosed with incidental cervical cancer after extrafascial hysterectomy or had a prior history of other malignancies; (2) the patient had an unknown lymphadenectomy status or did not undergo lymphadenectomy; (3) the patient underwent laparoscopic-assisted radical vaginal hysterectomy or robot-assisted RH; or (4) the patient had missing surgeon data or a missing date of operation.
Clinical and demographic characteristics
The demographic characteristics included age, year of surgery, urban‒rural distribution, mode of delivery, and comorbidities. Clinical characteristics that were analysed included FIGO stage, gross type of tumour, histological type, preoperative anticancer treatment, hysterectomy type and lymph node dissection. Other operation details included operative time and estimated blood loss.
The hospitals where patients were treated were characterized based on hospital function (general hospital, cancer centre, or W&C hospital), region of the country (north, south, central, east, southwest, northwest or northeast), and city scale (first-tier, second-tier, and third-tier or below). The levels of urban economic development were as follows: first-tier cities > second-tier cities > third-tier cities.
Surgeon volume
Surgeons were sequentially numbered. Then we calculated the total volume for each surgeon, and the annualized surgeon volumes was calculated as the total number of procedures that the surgeon performed divided by the number of years in which an individual surgeon contributed to at least one RH [
17,
22,
27]. Patients were stratified into two cohorts based on the hysterectomy approach: ARH group or LRH group. Surgeon volume cut-off points were then selected to divide patients into approximately equal tertiles. Abdominal surgeon cut-off points were as follows: low volume (≤ 8.1 procedures per year), intermediate volume (8.2–16.9 procedures per year), and high volume (> 16.9 procedures per year). Laparoscopic surgeon cut-off points were: low volume (≤ 11.0 procedures per year), intermediate volume (11.1–20.0 procedures per year), and high volume (> 20.0 procedures per year).
Outcomes
Complications were divided into intraoperative complications and postoperative complications. Intraoperative complications, which included ureteral injury, bladder injury, bowel injury, vascular injury, obturator nerve injury, and stomach injury, were recorded. Postoperative complications included bowel obstruction, pelvic haematoma, haemorrhage, vesicovaginal fistula, ureterovaginal fistula, ureteral fistula, rectovaginal fistula, venous thromboembolism and chylous leakage. We also recorded deaths from surgical complications.
Statistical analysis
The relationship between the number of surgeons and year was assessed by a nonparametric Spearman correlation test. Due to discontinuous data, one of the hospitals was not included in the graphs. Frequency distributions between categorical variables were compared using χ2 (Bonferroni corrected, if required) or Fisher’s exact test, and continuous variables were compared using one-way analysis of variance. The median and interquartile range (IQR) of surgeon volume were also reported for each tertile. Binary logistic regression models were used to determine predictors of treatment by the intermediate and high volume (highest 2/3 volume) surgeons. Demographic, clinical, and hospital characteristics constituted independent variables. To examine the association between surgeon volume and outcome, we built binary logistic regression models including surgeon volume while adjusting for the other variables described above. The results are reported as odds ratios (ORs) and 95% confidence intervals (CIs). A value of P < 0.05 was considered statistically significant. All analyses were performed with the SPSS 23.0 statistical software package (SPSS, Inc., Chicago, IL, USA).
Discussion
Our findings suggest that in the ARH cohort, postoperative complication rates were higher among intermediate-volume surgeons, while patients treated by high-volume surgeons had fewer postoperative complications. However, in the LRH cohort, annualized surgeon volume had no effect on intraoperative or postoperative complications.
The trends in the number of surgeons and mean surgeon volume over time differed between the two surgical approaches. From 2004 to 2016, the number of laparoscopic surgeons and mean surgeon case volume rose annually. This increasing acceptance of the laparoscopic technique could be due to the short-term benefits of LRH, including a more cosmetically pleasing incision, less bleeding, less postoperative pain, and faster postoperative recovery. However, the opposite trend was observed in the ARH cohort. The number of abdominal surgeons and mean surgeon case volume had been decreasing since 2013. In addition, it is noteworthy that categorical definitions of surgeon volume varied substantially among the different studies. In the study by Wright et al. [
22], a high-volume surgeon and a low-volume surgeon were defined as a surgeon who performed more than 3.75 and less than 2.25 ARHs per year, respectively, but our definitions of high volume and low volume were greater than 16.9 and less than or equal to 8.1 ARHs per year, respectively. The surgeon volume gap between the two groups was much larger than that of the study by Wright et al. In addition, our results revealed a positive correlation between the number of surgeons and the number of patients. The increasing number of surgeons could effectively alleviate disease stress at the national level; however, additional investigations are needed to determine whether the regionalization of RH is occurring in China. Spontaneous regionalization of gynaecological malignancy procedures has occurred in the US. At the hospital level, Matsuo et al.’s analysis showed that 89 centres that performed at least one trachelectomy for cervical cancer per year and only 6 centres met the criteria for top-decile centres in the United States [
9]. The threshold of any RH to have a minimum trachelectomy volume of 1 case a year was 7.8 cases per year. These findings imply that trachelectomy may have already been regionalized to hospitals with high RH volumes. At the surgeon level, the surgical treatment of an increasing number of patients with endometrial cancer has been limited to a smaller number of surgeons. The increased complexity of treatment has resulted in more patients being referred from general gynaecologists to gynaecologic oncology subspecialists [
17].
Our data demonstrated that the association between surgeon volume and complications for cervical cancer was complex with an increased risk of postoperative complications among intermediate-volume surgeons but the lowest postoperative complication rates for the highest-volume surgeons in the ARH cohort. In the multivariable analysis of the ARH cohort, patients treated by intermediate-volume surgeons were more likely to experience postoperative complications (OR = 1.55, 95% CI = 1.11–2.15), especially bowel obstruction (OR = 1.75, 95% CI = 1.05–2.94) and ureterovaginal fistula (OR = 3.47, 95% CI = 1.27–9.53), than those treated by high-volume surgeons. In addition, the postoperative complication rate was higher in the low-volume surgeon group than in the high-volume surgeon group, and the difference approached significance (OR = 1.38, 95% CI = 0.97–1.96,
P = 0.07). This observation resembles that of Wright et al. [
22]. Their results showed that the perioperative complication rate was highest in the intermediate-volume surgeon group compared with the low-volume and high-volume surgeon groups (low vs. intermediate vs. high = 2.9% vs. 6.7% vs. 1.8%,
P < 0.001). Additionally, compared with patients treated by low-volume surgeons, those operated on by high-volume surgeons had fewer medical complications and shorter lengths of stay [
22]. However, no direct comparisons between the intermediate-volume surgeon group and other groups were performed in their study. Another study evaluating the influence of surgeon volume on morbidity with regard to hysterectomy reached the similar conclusions: outcomes are significantly worse among low-volume surgeons than among higher-volume surgeons for abdominal hysterectomy [
28]. The majority of high-volume surgeons benefited from the effect of a sufficient learning curve and close cooperation with an experienced surgical team, which translates into a lower complication rate. One possible reason for the intermediate-volume surgeon group having the highest rate of postoperative complications could be that they were more lenient in their selection of patients. Patients treated by intermediate-volume surgeons had a higher frequency of FIGO stage IIB, more preoperative radiotherapy, and a higher frequency of PLA + PALA and type C2 hysterectomy. In the Laparoscopic Approach to Cervical Cancer (LACC) trial, ARH was associated with higher disease-free survival and overall survival rates than minimally invasive RH among women with early-stage cervical cancer [
29]. The publication of the results of the LACC trial led to important changes in the management of cervical cancer patients worldwide [
30]. After this publication, the number of patients treated with minimally invasive RH decreased from 64.9% to 30.4% [
31]. ARH therefore has re-emerged as a mainstream treatment for cervical cancer, bringing attention to the effect of abdominal surgeon volume on the complication rates.
Despite the finding of poor survival with minimally invasive surgery (MIS) in LACC trail, some studies were still conducted to re-establish the role of MIS and select the appropriate patient for MIS, considering the tumour size and the histological type [
32‐
35]. Thus, further exploration of the effect of surgeon volume on complications among patients who undergo LRH is also warranted. In our laparoscopy surgery cohort, surgeon volume had no significant effects on intraoperative complications or postoperative complications. It appears that the effects of surgeon volume on RH complications differ according to the surgical routes used. Similar results of endometrial cancer have reported that among patients who underwent abdominal hysterectomy for endometrial cancer, increased surgical volume was associated with reductions in perioperative surgical complications and medical complications [
36]. However, during laparoscopic hysterectomy, the surgeon volume appeared to have little effect on perioperative morbidity for endometrial cancer [
27]. A retrospective analysis of 1016 laparoscopic hysterectomies for benign gynaecologic problems found that increasing the surgical volume could not reduce the rate of serious complications [
37]. The population-based study by Ruiz et al. demonstrated that the comparative safety of abdominal and laparoscopic hysterectomy was influenced by surgeon volume, but that the volume-outcomes relationship was not present in robotic-assisted or vaginal hysterectomy [
28].
Interestingly, in ARH cohort, patients with stage IIB were less likely to be treated by high-volume or intermediate-volume surgeons. However, in LRH cohort, stage IIB disease was more frequently seen by high-volume or intermediate-volume surgeons than by low-volume surgeons. A possible explanation for this might be different guideline compliance rates in different kinds of hospitals. In the ARH cohort, 59.5% of patients treated by high-volume or intermediate-volume surgeons received treatment from a cancer centre, whereas in the LRH cohort, only 29.2% of patients treated by high-volume or intermediate-volume surgeons received treatment from cancer centre (Additional file
1: Table S2). This might be related to higher compliance with stage IIB treatment guidelines in cancer centres. Matsuo et al. had similar findings in their assessment of hospital volume. Matsuo et al. examined 5,964 women with cervical cancer who underwent RH (mostly ARH) and found that stage IIB disease was less frequently seen in the high-surgical volume group than in the other groups [
10]. In our study, patients treated by high-volume or intermediate-volume surgeons were less likely to receive neoadjuvant chemotherapy in both the ARH cohort (OR = 0.81, 95% CI = 0.72–0.91) and LRH cohort (OR = 0.69, 95% CI = 0.57–0.82). A similar observation was observed by Matsuo et al. who found that women in the high-volume group were less likely to receive neoadjuvant chemotherapy before RH [
10]. Adherence to guidelines by surgeons with different surgical experience merits further exploration.
Numerous factors affect surgical experience. First, surgical experience has been assessed and quantified by different metrics, such as annual surgeon volume (frequency), technique-specific volume, surgeon cumulative volume, and years of experience [
14,
38,
39]. Yasunaga et al. [
40] defined surgeon volume as the number of radical hysterectomies that each gynaecologist had performed as an operating surgeon over his or her professional career. Their study showed that higher surgeon volume (greater than 200 procedures) was associated with a reduced incidence of postoperative urinary disorders. However, they did not mention the surgical route of RH. Second, surgical educators recognize that skill sets may transfer between operations [
41]. Modrall et al. [
42] defined the aggregate annual volume per surgeon of upper gastrointestinal operations as the “surrogate volume”, including excision of oesophageal diverticulum, gastrectomy, gastroduodenectomy, and repair of diaphragmatic hernia. Among surgeons with low-volume oesophagectomy experience, increasing the volume of surrogate operations improved the outcomes observed for oesophagectomy. However, there has been little discussion about “surrogate surgery” in gynaecological cancer surgery. It was uncertain whether surrogate operative experiences, such as experiences of extrafascial hysterectomy in benign disease and cytoreductive surgery in ovarian cancer, yield improvements in outcomes for RH. Third, the characteristics of the surgeon, such as age, may have an effect on surgical experience. For example, a surgeon age of ≤ 51 and ≥ 56 years may increase short- and long-term mortality after oesophagectomy for cancer, as the highest surgical competence is achieved between 52 and 56 years of surgeon age [
43]. The reason for the decreasing performance among older surgeons might be related to mental fatigue, poorer compliance with evidence-based medicine, and higher administrative positions leading to reduced surgical frequency [
38].
Currently, artificial intelligence (AI) can be applied for the prediction, screening, detection of cervical cancer or precancerous lesion and predicting the prognosis of patients [
44,
45]. In addition, AI has the potential to distinguish surgeon experience and to provide access to standard surgical solutions that are independent of individuals’ experience and day-to-day performance changes. Chen et al.’s study demonstrated that machine learning can accurately classify surgeon experience based on individual stitches and sub-stitches in the vesico-urethral anastomosis of a robot-assisted radical prostatectomy [
46]. Saeidi et al. achieved the enhanced autonomy necessary to perform robotic laparoscopic anastomosis of the small bowel using the Smart Tissue Autonomous Robot (STAR) and they found that autonomous robotic laparoscopic surgery outperforms expert surgeons’ manual technique and robot-assisted surgery technique in terms of consistency and accuracy during laparoscopic small bowel anastomosis experiments [
47].
This population-based study is the first to examine changes in the number of surgeons and annual surgeon volume for cervical cancer over time, and to explore the association between surgeon volume and complications after ARH and LRH in China. First, a strength of our study is its large sample size. We reviewed 22,684 cases treated at 42 hospitals over a 13-year period so that data on the rare adverse events could be collected. Second, we also included clinical characteristics, such as FIGO stage, histology, preoperative treatment, hysterectomy type, and lymph node dissection type which may influence the treatment outcome [
23].
We also recognize several limitations to our findings. First, this study was a retrospective study in which the data were obtained from inpatient medical records or through readmission. Data on complications that may have occurred after discharge and that would have been treated by other hospitals could not be obtained. Therefore, future well-designed and prospective studies are needed to verify the work with a much larger cohort of patients. Second, we divided the patients into tertiles based on annualized surgeon volumes, but the results of the present study could not translate into clinically meaningful cut-off points. Third, although we considered a wide range of clinical characteristics and tumour characteristics, there might be other unmeasured confounding factors affecting complications, such as assistant surgeons [
48], uterine size, downstream care, surgical instruments, management of complications, preoperative frailty scores [
49] and subspecialty training background of each surgeon. In addition, skill transference between LRH and ARH remains unclear. Fourth, our study included only patients from 42 hospitals and the findings may not be representative of other areas in China.
Acknowledgements
We are grateful to Min Hao (Department of Obstetrics and Gynecology, The Second Hospital of ShanXi Medical University), Wuliang Wang (Department of Obstetrics and Gynecology, The Second Affiliated Hospital of Zhengzhou University), Ying Yang (Department of Obstetrics and Gynecology, Xinqiao Hospital, Third Military Medical University), Shan Kang (Department of Obstetrics and Gynecology, The Fourth Hospital of Hebei Medical University & The Tumor Hospital of Hebei Province), Bin Ling (Department of Obstetrics and Gynecology, China-Japan Friendship Hospital), Xinli Sun and Hongwei Zhao (Department of Gynecology, Shanxi Provincial Cancer Hospital), Yu Guo and Lihong Lin (Department of Gynecology, Anyang Tumor Hospital), Li Wang (Department of Gynecology, The Affiliated Tumor Hospital of Zhengzhou University), Weidong Zhao (Department of Gynecology and Oncology, Anhui Provincial Cancer Hospital), Yan Ni (Department of Obstetrics and Gynecology, The Yuncheng Central Hospital of Shanxi province), Donglin Li and Wentong Liang (Department of Obstetrics and Gynecology, Guizhou Provincial People`s Hospital), Jianxin Guo (Department of Obstetrics and Gynecology, Daping Hospital, The Third Military Medical University), Xuemei Zhan and Mingwei Li (Department of Gynecology, Jiangmen Central Hospital), Weifeng Zhang (Department of Obstetrics and Gynecology, Ningbo Women & Children's Hospital), Peiyan Du (Department of Gynecological Oncology, Cancer Center of Guangzhou Medical University), Ziyu Fang (Department of Obstetrics and Gynecology, Liuzhou Workers' Hospital), Long Chen (Department of Obstetrics and Gynecology, Qingdao Municipal Hospital), Encheng Dai and Ruilei Liu (Department of Obstetrics and Gynecology, Linyi People's Hospital), Mubiao Liu and Yuanli He (Department of Obstetrics and Gynecology, Zhujiang Hospital, Southern Medical University), Jilong Yao and Zhihua Liu (Department of Obstetrics and Gynecology, Shenzhen Maternity & Child Healthcare Hospital), Xueqin Wang (Department of Obstetrics and Gynecology, The Fifth Affiliated Hospital of Southern Medical University), Yan Xu (Department of Obstetrics and Gynecology, Guangzhou Panyu Central Hospital), Ben Ma (Department of Obstetrics and Gynecology, Guangzhou First People's Hospital), Zhonghai Wang (Department of Obstetrics and Gynecology, Shenzhen Nanshan People's Hospital), Lin Zhu (Department of Gynecology, The Second Hospital of Shandong University), Hongxin Pan (Department of Obstetrics and Gynecology, the 3rd Affiliated Hospital of Shenzhen University, Luohu People's Hospital), Qianyong Zhu (Department of Obstetrics and Gynecology, No.153. Centre Hospital of Liberation Army, Hospital No.988 of the Chinese People's Liberation Army Joint Support Force), Xiaohong Wang (Department of Obstetrics and Gynecology, Jinan City People's Hospital, Former Laiwu People's Hospital), Dingyuan Zeng and Zhong Lin (Department of Obstetrics and Gynecology, Maternal and Child Health Care Hospital of Liuzhou), Shaoguang Wang (Department of Obstetrics and Gynecology, Yantai Yuhuangding Hospital), Bin Zhu (Department of Obstetrics and Gynecology, Yiwu Maternal and Child Health Hospital), Anwei Lu (Department of Obstetrics and Gynecology, Maternal and Child Health Care Hospital of Guizhou Province), Mei Ji (Department of Obstetrics and Gynecology, the First Affiliated Hospital of Zhengzhou University), Qianqing Wang (Department of Obstetrics and Gynecology, Central Hospital Affiliated to Xinxiang Medical University), Zhumei Cui (Department of Gynecology, The Affiliated Hospital of Qingdao University Medical College), Biliang Chen (Department of Gynecology, Xijing Hospital of Air Force Medical University), Qinghuang Xie (Department of Gynecology, Foshan Women and Children Hospital), Qiubo Lv (Department of Gynecology, Beijing Hospital), Chang Liu (Department of Gynecology, the First Hospital of Lanzhou University), and Yi Zhang (Department of Gynecology, the First Hospital of China Medical University) for providing medical records.
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