The attitude and practice of general surgeons toward cytoreductive surgery and hyperthermic intraperitoneal chemotherapy: A cross-sectional study

Background Cytoreductive surgery (CRS) and hyperthermic intraperitoneal chemotherapy (HIPEC) mandate well-established HIPEC and oncology centers, which are not available in many medical institutions. This study assessed the knowledge, attitude, and practice toward CRS and HIPEC of general surgeons in Riyadh, Saudi Arabia. Patients and methods General surgeons (n = 266) from nine hospitals who treat patients with gastrointestinal cancer were surveyed. The responses of surgeons who work in HIPEC and academic centers (Group A) and surgeons working in tertiary and secondary hospitals (Group B) were compared. The survey response rate was 48.1% (128/266). Results Surgeons in group B treated significantly more patients with peritoneal carcinomatosis per year than surgeons in group A (P = .001). Group B reported having a HIPEC specialist at their hospital, and 71.4% reported that the nearest HIPEC center was within 30 miles, compared to 4.5% of respondents in group A (P = .001). Lack of access to a HIPEC specialist was reported by 15.5% of surgeons in group B and 0% of surgeons in group A (P = .006). HIPEC as a possible therapeutic option for appendiceal cancer was cited by 60.7% of surgeons in group B compared to 84.1% of surgeons in group A (P = .007) and as a therapeutic option for ovarian cancer by 52.4% of surgeons in group B and 81.8% of surgeons in group A (P = .001). Conclusion New strategies are needed to improve the knowledge and implementation of the referral system for HIPEC among general surgeons. Our study was limited by a low response rate.


Introduction
Peritoneal carcinomatosis (PC) is associated with cancers of the gastrointestinal (GI), reproductive, and genitourinary tracts. However, the most common associated cancers are ovarian, colon, and gastric [1]. PC is associated with a poor prognosis and was once believed to be an incurable component of intra-abdominal malignancies, as systemic chemotherapy resulted in no long-term survival and poor quality of life in patients with PC [1,2]. The development of cytoreductive surgery (CRS) and hyperthermic intraperitoneal chemotherapy (HIPEC) significantly improved the prognosis of patients with PC, originating from most GI and genitourinary carcinomas [1,3,4]. A recent trial reported that CRS and HIPEC for PC Results in 5-year disease-free survival rates of more than 30% of patients [5].
A lack of referrals to HIPEC experts and the underutilization of both CRS and HIPEC limit the success of these therapies and are due to several factors, including limited access to HIPEC experts, a perception of insufficient evidence for these therapeutic methods, and a lack of familiarity with the data regarding the outcomes, impacts, referral patterns, and management choices [6]. As multidisciplinary teamwork has been proven to improve the diagnostic accuracy and overall survival of patients with cancer, raising awareness among general surgeons regarding the appropriate utilization of CRS and HIPEC is essential [7]. An assessment of general surgeons' knowledge of HIPEC and PC is necessary to ensure appropriate treatment by highlighting the need for educational and training programs [8]. This study assessed the knowledge and experience regarding CRS and HIPEC for PC of general surgeons in Riyadh, Saudi Arabia.

Patients and Methods
This study was approved by the institutional review board committee at King Saud University Medical City. The general surgeons from nine hospitals were included in the study after applying a multistage sampling that started with a stratified sampling. The strata were composed of HIPEC centers, major tertiary and academic hospitals, and secondary hospitals. A representative, proportional sample from each stratum was used to form clusters that were proportional to the hospitals in each stratum: three HIPEC centers, three major tertiary and academic hospitals, and three secondary hospitals. All participants who were exposed to patients with gastrointestinal cancer were included in the study. We collected data regarding the surgeons' demographics and background, attitude, and knowledge regarding CRS and HIPEC. Surgeons were grouped by their work environments: surgeons working at HIPEC and academic centers were allotted to group A, while group B consisted of surgeons working at tertiary and secondary hospitals.

Data collection
Information regarding the study and the questionnaire was provided to all participants, and written informed consent was obtained. Both the questionnaire and the consent form were completed online using Google Forms [9]. This work has been reported in line with the STROCSS [10].

Survey questionnaire
A previously validated and published questionnaire [6] was modified by an expert oncology surgeon and a researcher using feedback from a small group of general surgeons for use in this study. The questionnaire included items regarding demographic information, practice and experience, the availability of HIPEC centers and specialists, factors that influenced referral decisions, and general knowledge regarding CRS and HIPEC.

Statistical analysis
Statistical Package for Social Sciences version 23.0 software (SPSS Inc, IBM, Armonk, New York, USA) was used for the statistical analyses in this study. The Results are expressed as numbers and percentages. The chi-square test was used to determine the significant differences between groups A and B. Statistical significance was set at P < .05.

Results
A total of 266 surgeons from nine hospitals in Riyadh were surveyed, and 128 responded (response rate: 48.1%). Overall, 98 respondents (76.6%) were male, and 44 were allocated to group A, while 84 were allocated to group B. Half of the respondents (65; 50.8%) identified as registrar or specialist surgeons, 46 (35.9%) identified as consultants, and 17 (13.3%) identified as fellows. A total of 97 respondents (75.8%) reported having > 5 years of experience practicing medicine. While 68 respondents (53.1%) identified as general surgeons, 60 (46.9%) specialized in acute care, breast and endocrine, colorectal, hepatobiliary, oncologic, or upper GI surgery. The respondents' characteristics are summarized in Table 1.
Exposure to HIPEC centers during residency or fellowship training was reported by 54.5% of respondents in group A and 51.2% in group B ( Table 2). A higher proportion of respondents in group B (41.7%) learned about CRS and HIPEC during training than in group A (31.8%). Most respondents (90.9% of group A and 91.7% of group B) reported having treated patients with GI cancers. The discussion of the management of those patients in a multidisciplinary tumor board meeting was reported by 77.3% of respondents in group A and 50% in group B. A higher proportion of respondents in group B (84.5%) reported treating at least 15 patients with GI cancer and peritoneal metastasis per year than in group A (50.0%) (P = .001). However, fewer respondents in group B reported having a HIPEC specialist in their center (42 (95.5%) in group A and 25 (29.8%) in group B). Only six respondents (7.1%) in group B reported that the nearest HIPEC center was at the same hospital, while 40 respondents (90.9%) in group A reported having a HIPEC center at the same hospital. The nearest HIPEC center was reported as within 30 miles by 71.4% of respondents in group B and 4.5% in group A and over 30 miles away by 21.4% of respondents in group B and 4.5% in group A (P = .001) (see Table 3).
A lack of access to HIPEC specialists was reported by 15.5% of respondents in group B and 0% in group A (P = .006). A similar proportion of respondents in group A (70.5%) and group B (70.2%) reported referring patients to a HIPEC specialist. Only 60.7% of respondents in group B cited HIPEC as a possible therapeutic option for appendiceal cancer compared to 84.1% of respondents in group A (P = .007). Similarly, only 52.4% of respondents in group B cited HIPEC as a treatment for ovarian cancer compared to 81.8% of respondents in group A (P = .001). Figs. 1-4 show the respondents' knowledge regarding the 5-year overall survival rate of patients undergoing CRS and HIPEC and the 30-day mortality rate after CRS and HIPEC in a specialized center, respectively.

Discussion
Our study assessed the exposure to the use of CRS and HIPEC for PC of surgeons in Riyadh, Saudi Arabia. The surgeons' knowledge and background regarding the indications for CRS and HIPEC, exposure to and experience with CRS and HIPEC, and their access to a HIPEC specialist are important factors that reflect on the management of patients with PC. Few similar studies have been reported, and this is the first study of its type to focus on surgeons in Saudi Arabia. The Results of this study will be useful when developing new training guidelines regarding the use of CRS and HIPEC for eligible patients.
CRS and HIPEC are well-established therapies for appendiceal cancer with PC and result in a favorable long-term survival rate [11]. However, only 60.7% of respondents in group B and 84.1% of respondents in group A recognized that CRS and HIPEC can be used to treat appendiceal cancer. A similar study reported that 91% of general surgeons identified appendiceal cancer as a peritoneal malignancy suitable for HIPEC treatment [8]. Our Results were consistent with a study that reported Abbreviations: GI-gastrointestinal.  that 51% of the respondents correctly identified appendiceal adenocarcinoma as an indication for CRS and HIPEC, 66% of the respondents identified high grade mucinous appendiceal cancer as an indication, and 68% of respondents reported low grade mucinous appendiceal cancer as an indication [12].
Stage III epithelial ovarian cancer has been reported to respond well to HIPEC and interval CRS, with a longer recurrence-free survival and overall survival than when surgery alone was used as treatment and no increase in the rates of adverse effects [13]. Based on this previous study, the National Comprehensive Cancer Network (NCCN) included HIPEC in their guidelines as a management option for interval debulking surgery (NCCN clinical practice guidelines Version 1.2019-March 8, 2019 OV-2) as mentioned by Stefano Cianci et al. [14,15] However, only 52.4% of the respondents in group B and 81.8% in group A correctly identified ovarian cancer as an indication for CRS and HIPEC.
In this study, 70.50% of respondents in group A and 60.7% in group B reported colorectal cancer carcinomatosis (CRC-C) as an indication for CRS and HIPEC; however, only 46% of respondents correctly identified CRC-C as an indication for CRS and HIPEC in a previous study, leading to the development of a referral checklist that includes a list of indications and contraindications for CRS and HIPEC [16]. The development of a referral checklist may be effective to provide patients with optimal care, as up to 90.9% of respondents in group A and 91.7% in group B reported treating patients with GI cancers, though only 54.5% of respondents in    group A and 51.2% in group B were exposed to a HIPEC center during residency or fellowship training and only 31.8% of respondents in group A and 41.7% in group B learned about CRS and HIPEC during their training programs. As every surgical team bears the responsibility to minimize morbidity and mortality and provide patients with optimal management options, it is essential that general surgery training programs should include surgical oncology rotations, seminars, and online webinars that discuss the management of patients with advanced malignancies. Adequate training and access to HIPEC specialists are crucial for general surgeons who treat patients with cancer.
As the management of patients with PC is complex, strategies to improve communication between HIPEC and non-HIPEC centers are necessary, including a referral system or a monthly multidisciplinary HIPEC meeting that includes representatives from all Riyadh medical centers to discuss and refer eligible patients. As multidisciplinary meetings have been reported to effectively alter the diagnosis and management of a significant number of patients [7], this strategy may be useful in improving patient outcomes. The healthcare provided to patients with cancer should be equal at all medical centers.
This study is not without limitations. The response rate is relatively low, which may be due to the length of the survey or the lack of interest or knowledge in the topic. Also as this study was conducted only in Saudi Arabia, we believe it may not be applicable globally and further studies are needed.
In conclusion, the lack of knowledge and access to CRS and HIPEC centers are major obstacles to the proper care of patients with PC. Therefore, new strategies to increase the awareness and knowledge of CRS and HIPEC are necessary, and the implementation of a practical HIPEC center referral system is essential.

Provenance and peer review
Not commissioned, externally peer-reviewed.

Ethical Approval
This study was approved by the institutional review board committee at King Saud University Medical City

Consent
Informed consent was obtained from all participants included in this study.