Abstract
Introduction
In the UK, general surgeons must demonstrate competency in emergency general surgery before obtaining a certificate of completion of training. Subsequently, many consultants develop focused elective specialist interests which may not mirror the breadth of procedures encountered during emergency practice. Recent National Emergency Laparotomy Audit analysis found that declared surgeon special interest impacted emergency laparotomy outcomes, which has implications for emergency general surgery service configuration. We sought to establish whether local declared surgeon special interest impacts emergency laparotomy outcomes.
Methods
Adult patients having emergency laparotomy were identified from our prospective National Emergency Laparotomy Audit database from May 2016 to May 2019 and categorised as colorectal or oesophagogastric according to operative procedure. Outcomes included 30-day mortality, return to theatre and length of stay. Binomial logistic regression was used to identify any association between declared consultant specialist interest and outcomes.
Results
Of 600 laparotomies, 358 (58.6%) were classifiable as specialist procedures: 287 (80%) colorectal and 71 (20%) oesophagogastric. Discordance between declared specialty and operation undertaken occurred in 25% of procedures. For colorectal emergency laparotomy, there was an increased risk of 30-day mortality when performed by a non-colorectal consultant (unadjusted odds ratio 2.34; 95% confidence interval 1.10–5.00; p = 0.003); however, when adjusted for confounders within multivariate analysis declared surgeon specialty had no impact on mortality, return to theatre or length of stay.
Conclusion
Surgeon-declared specialty does not impact emergency laparotomy outcomes in this cohort of undifferentiated emergency laparotomies. This may reflect the on-call structure at Birmingham Heartlands Hospital, where a colorectal and oesophagogastric consultant are paired on call and provide cross-cover when needed.
Keywords: General surgery; Colorectal surgery, Laparotomy
Introduction
Patients undergoing emergency laparotomy have potentially life-threatening conditions that are associated with high mortality and morbidity, 80–90% of deaths arising from general surgery arise in patients undergoing emergency general surgery.1 In 2011, the Royal College of Surgeons of England and the Department of Health acknowledged that the standards of care for emergency laparotomy were often suboptimal and required improvement.2 This led to the establishment of the National Emergency Laparotomy Audit (NELA). Since the introduction of NELA in 2013, reported mortality has fallen from 11.8% to 9.5%.3 A number of interventions have been shown to improve mortality and length of stay following emergency laparotomy including the Emergency Laparotomy Quality Improvement Care Project and emergency laparotomy collaborative bundles.4,5 Nevertheless, mortality remains high, necessitating the identification of additional factors that impact outcomes.3
In the UK, all general surgeons must demonstrate competency in emergency general surgery before obtaining a certificate of completion of training. Subsequently, many consultants develop focused elective specialist interests which may not mirror the breadth of procedures encountered during emergency practice. In 2019, Boyd-Carson et al reported that declared surgeon special interest impacted outcome following emergency laparotomy.6 Colorectal laparotomies performed by a consultant without a specialist colorectal interest were associated with increased risk of 30-day mortality (odds ratio, OR, 1.23; 95% confidence interval, CI, 1.13–1.33) and return to theatre (OR 1.13; 95% CI 1.05–1.20).6 Oesophagogastric laparotomies performed by a consultant without a specialist interest in oesophagogastric were associated with increased 30-day mortality (OR 1.24; 95% CI 1.02–1.53).6 Such findings have major implications for the configuration of the emergency general surgery service. We therefore aimed to establish in our local trust whether declared surgeon special interest impacted outcomes following emergency laparotomy.
Methods
Birmingham Heartlands Hospital is part of the University Hospitals Birmingham NHS Foundation Trust. It is a large district hospital with a catchment population of approximately 750,000. This was an observational cohort study relying on prospectively collated registry data. Consecutive adult patients undergoing emergency laparotomy from May 2016 to May 2019 were identified from the Birmingham Heartlands Hospital NELA database. The on-call structure at Birmingham Heartlands Hospital is a seven-day rolling rota where a colorectal and oesophagogastric surgical consultant alternate 24-hour cover for seven days, prior to handing over to the next team. The colorectal team consists of eight consultant surgeons, the oesophagogastric team six consultant surgeons; four perform oesophagogastric cancer surgery and all six perform benign oesophagogastric and bariatric surgery.
Emergency laparotomies were categorised as colorectal, oesophagogastric or ‘general’. Patients were classed as having had a colorectal emergency laparotomy if they had a colectomy (right, left, transverse, sigmoid, Hartmann’s, anterior resection, sub-total or total colectomy) or colostomy formation or revision. Patients were classed as having had an oesophagogastric emergency laparotomy if they underwent repair of a bleeding or ruptured peptic ulcer or gastrectomy. Patients undergoing emergency laparotomy for small bowel pathology were excluded as these were deemed to be operations performed regularly by both colorectal and oesophagogastric surgeons.
Data collected included age, sex, American Society of Anesthesiologists (ASA) grade, NELA predicted mortality, the NCEPOD category, the grade of the most senior operating surgeon and the declared specialty of the responsible consultant surgeon. Study outcomes included 30-day mortality, return to theatre and length of stay.
Descriptive data are presented as mean (standard deviation, SD), median (range) or number and percentage in parenthesis as appropriate. Outcomes of 30-day mortality, return to theatre and length of stay were compared with univariate analysis, chi-square for categorical variables and Mann–Whitney U or Kruskal–Wallis for continuous variables. To test a possible association between surgeon-declared specialist interest and the outcomes a univariable logistic regression was performed with outcomes calculated as unadjusted odds ratios. The following factors were entered into the univariable model, age, sex, ASA grade, NELA predicted mortality, NCEPOD category, the grade of the most senior operating surgeon and the declared specialty of the responsible consultant surgeon. Significant factors on unadjusted logistic regression as well as declared surgeon specialist interest were entered into a multivariable logistic regression analysis. Data analysis was performed in IBM SPSS Statistics for Windows, Version 24.0. A p-value of less than 0.05 was considered significant.
Results
A total of 600 patients undergoing emergency laparotomy were identified during the study period. Of these, 358 were classified as colorectal (n = 287) or oesophagogastric (n = 71); the remainder (n = 242) were classifiable as general procedures. Of the general procedures, the primary procedure was small-bowel resection in 54% (n = 130), adhesiolysis in 28% (n = 67), hernia repair with small-bowel resection in 6% (n = 15), palliative bypass or open and closed laparotomy for inoperable pathology in 6% (n = 14), washout of an abscess or haematoma in 6% (n = 14) or splenectomy in 1% (n = 2). The baseline characteristics of both groups are displayed in Table 1.
Table 1.
Baseline characteristics grouped by operation type and consultant declared specialist interest
Characteristic | Colorectal laparotomies | Oesophagogastric laparotomies | ||
---|---|---|---|---|
Colorectal consultant (n = 221) | Non-colorectal consultant (n = 66) | Oesophagogastric consultant (n = 58) | Non-oesophagogastric consultant (n = 13) | |
Age, years, median (IQR) | 66 (51–76) | 69 (52–76) | 57 (48–65) | 55 (54–77) |
Male sex, n (%) | 110 (50) | 26 (39) | 30 (52) | 13 (100) |
ASA grade, n (%): | ||||
I | 14 (6) | 2 (3) | 4 (7) | 3 (23) |
II | 88 (40) | 14 (21) | 12 (21) | 6 (46) |
III | 85 (38) | 26 (39) | 15 (26) | 1 (8) |
IV | 32 (14) | 21 (32) | 23 (40) | 2 (15) |
V | 2 (0) | 3 (5) | 4 (7) | 1 (8) |
NCEPOD category n (%): | ||||
1 | 12 (5) | 8 (12) | 17 (29) | 2 (15) |
2a | 65 (29) | 30 (45) | 30 (52) | 11 (85) |
2b | 87 (39) | 25 (38) | 9 (16) | 0 (0) |
3 | 57 (26) | 3 (5) | 2 (3) | 0 (0) |
NELA P-POSSUM, predicted mortality median (IQR) | 4.5 (0.1–98.9) | 10.3 (0.4–63.7) | 12.45 (0.2–99.6) | 6.6 (0.2–88.2) |
Consultant present in theatre, n (%) | 210 (95) | 56 (85) | 55 (95) | 10 (77) |
ASA, American Society of Anesthesiologists, NCEPOD, National Confidential Enquiry into Patient Outcome and Death, NELA, National Emergency Laparotomy Audit; IQR, interquartile range.
The types of emergency laparotomy are shown in Tables 2 and 3. The most common colorectal procedure was right hemicolectomy. The most common oesophagogastric procedure was repair of duodenal perforation. A consultant was present at the operating table in 93% of colorectal laparotomies and 92% of oesophagogastric laparotomies (Table 1). The proportion of procedures performed by a surgeon whose declared specialty differed from the operation performed was 25%.
Table 2.
Colorectal laparotomies
Procedure | Colorectal consultant (n = 221; 77%) |
Non-colorectal consultant (n = 66; 23%) |
---|---|---|
Right colectomy | 67 (30) | 20 (30) |
Stoma revision or formation | 58 (26) | 18 (27) |
Hartmann’s | 41 (19) | 15 (23) |
Sub-total collection | 33 (15) | 5 (8) |
Left colectomy | 5 (2) | 5 (8) |
Transverse colectomy | 0 (0) | 1 (2) |
Sigmoid colectomy | 4 (2) | 0 (0) |
Anterior resection | 7 (3) | 0 (0) |
Other | 5 (2) | 2 (3) |
Table 3.
Oesophagogastric laparotomies
Procedure | Upper gastrointestinal consultant (n = 49; 69%) | Non-upper gastrointestinal consultant (n = 22; 31%) |
---|---|---|
Duodenal perforation repair | 18 (37) | 13 (59) |
Other | 9 (18) | 0 (0) |
Hiatus hernia repair | 7 (14) | 0 (0) |
Gastric perforation repair | 5 (10) | 6 (27) |
Gastrectomy | 5 (10) | 3 (14) |
Laparotomy for bleeding peptic ulcer | 2 (4) | 0 (0) |
Laparotomy for bleeding duodenal ulcer | 3 (6) | 0 (0) |
Outcomes
All-cause 30-day mortality was 13.5% (n = 34) for patients having a general emergency laparotomy, 11.8% (n = 34) for patients having a colorectal emergency laparotomy and 19.7% (n = 14) for patients having an oesophagogastric emergency laparotomy (p = 0.532). Return to theatre was necessary in 1.9% (n = 5) of patients having a general emergency laparotomy, 5.9% (n = 17) of patients having a colorectal emergency laparotomy and 5.6% (n = 4) of patients having an oesophagogastric emergency laparotomy (p = 0.067). Median length of stay was 13 days (IQR 8–22 days) in patients having a general emergency laparotomy, 14 days (IQR 9–31 days) for patients having a colorectal emergency laparotomy and 21 days (IQR 6–26 days) for patients having an oesophagogastric emergency laparotomy (p = 0.017).
Analysis of the impact of surgeon-declared specialist interest on outcomes was performed. Of the colorectal emergency laparotomies, 77% (n = 221) were performed by a colorectal consultant, the remainder (23%; n = 66) were performed by an oesophagogastric consultant. For colorectal emergency laparotomy, there was an increased risk of 30-day mortality when performed by a non-colorectal consultant (unadjusted OR 2.34; 95% CI 1.10–5.00; p = 0.003). The risk of mortality increased with increasing age (unadjusted OR 1.03; 95% CI 1.01–1.06; p = 0.016), ASA (unadjusted OR 6.24; 95% CI3.42–11.38) p < 0.001), CEPOD category (unadjusted OR 0.46; 95% CI 0.29–0.72; p = 0.001), PPOSSUM mortality score (unadjusted OR 1.06; 95% CI 1.04–1.08; p < 0.001). Following adjustment for potential confounders (age, ASA, CEPOD category, PPOSSUM mortality score) there was no significant effect of surgeon-declared specialist interest on the risk of 30-day mortality (unadjusted OR 1.29; 95% CI 0.53–3.137; p = 0.579). Increased ASA remained the only significant factor affecting 30-day mortality for patients undergoing colorectal emergency laparotomy (unadjusted OR 4.82; 95% CI 2.36–9.86; p < 0.001). There was no increased risk of return to theatre (unadjusted OR 1.48; 95% CI 0.55–4.01; p = 0.443) or increased length of stay (unadjusted OR 1.05; 95% CI 0.60–1.81; p = 0.872) for patients undergoing a colorectal emergency laparotomy performed by a non-colorectal consultant.
Of the oesophagogastric emergency laparotomies, 69% (n = 49) were performed by an oesophagogastric consultant, 31% (n = 22) by a colorectal consultant. For oesophagogastric laparotomies, there was no increased risk of 30-day mortality when performed by a non-oesophagogastric consultant (unadjusted OR 0.31; 95% CI 0.06–1.52; p = 0.144). The risk of 30-day mortality increased with age (unadjusted OR 1.05; 95% CI 1.00–1.09; p = 0.032), ASA (unadjusted OR 4.65; 95% CI 1.79–12.09; p = 0.002), CEPOD category (unadjusted OR 2.46; 95% CI 1.05–5.75; p = 0.038), PPOSSUM mortality score (unadjusted OR 1.05; 95% CI 1.02–1.09; p < 0.001). Following adjustment for potential confounders (age, ASA, CEPOD category, PPOSSUM mortality score and declared surgeon specialist interest) there was no significant effect of surgeon-declared specialist interest on the risk of 30-day mortality (adjusted OR 1.02; 95% CI 0.53–1.14; p = 0.674). PPOSSUM mortality score remained the only significant factor affecting 30-day mortality for patients undergoing oesophagogastric emergency laparotomy (adjusted OR 1.04; 95% CI 1.01–1.08; p = 0.042). There was no increased length of stay (unadjusted OR 1.23; 95% CI 0.45–3.36; p = 0.690) for patients undergoing an oesophagogastric emergency laparotomy performed by a non-oesophagogastric consultant. There were no returns to theatre in this group.
In keeping with NELA recommendations, the majority of laparotomies were performed by a consultant surgeon (91%; n = 543) with the remainder being performed by a surgical registrar (9%; n = 57).3 All-cause 30-day mortality was 3.39% (n = 2) for laparotomies performed by a surgical registrar and 14.52% (n = 80) for those performed by a consultant (p = 0.017). There were no significant differences between surgical registrar and consultant laparotomies regarding rates of return to theatre (3.39%; n = 2 vs 4.36%; n = 24) or median length of stay (14 days; IQR 9–29 days vs. 13 days; IQR 6–26 days).
Discussion
Declared surgeon specialist interest had a significant impact on 30-day mortality. For colorectal emergency laparotomy, there was an increased risk of 30-day mortality when performed by a non-colorectal consultant (unadjusted OR 2.34; 95% CI 1.10–5.00; p = 0.003). When adjusted for confounders within multivariate analysis, this effect disappeared and declared surgeon specialty had no impact on mortality, return to theatre or length of stay for either colorectal or oesophagogastric emergency laparotomy.
Emergency laparotomy outcomes were comparable to those reported in the literature with 30-day mortality of 11.8% for colorectal emergency laparotomy. A Danish population-based cohort study reported 30-day mortality of 18.5% (95% CI 17.1–19.9) in 2,904 patients undergoing emergency laparotomy.7 Skala et al reported a mortality of 14% following emergency colorectal resection.8 In our study, oesophagogastric laparotomies had a mortality of 19.7%. Adequately counselling the patient about this risk preoperatively forms an important part of the consent process. The most common oesophagogastric procedure was repair of a perforated peptic ulcer. These outcomes are comparable with those of Thorsen et al, who reported a 30-day mortality of 15.2%, which rose to 19.2% at 90-days for peptic ulcer perforations.9
In keeping with NELA recommendations, the majority of laparotomies were performed by a consultant surgeon (91%; n = 543), with the remainder performed by a surgical registrar (9%; n = 57).3 Outcomes of laparotomies performed by surgical registrars compared favourably to those performed by a consultant with all-cause 30-day mortality of 3.39% (n = 2) for laparotomies performed by a surgical registrar and 14.52% (n = 80) for those performed by a consultant (p = 0.017). There were no significant differences between surgical registrar and consultant laparotomies in rates of return to theatre (3.39%; n = 2 vs 4.36%; n = 24) or median length of stay (14 days; IQR 9–29 vs 13 days; IQR 8–26) respectively. One hypothesis is that favourable outcomes for laparotomies performed without a consultant present may reflect appropriate case selection of low risk patients and procedures.
A literature review identified conflicting evidence on the impact of declared surgeon specialist interest in emergency laparotomy outcomes. One systematic review found surgeon subspecialisation was associated with improved outcomes; this study, however, included 13 different surgical specialist interests and 42 different surgical procedures.10 Just four studies included gastrointestinal procedures and just one of these investigated the impact of surgeon specialist interest on outcomes.10
Boyd-Carson et al found declared surgeon specialist interest had a significant impact on 30-day mortality and return to theatre in 33,819 emergency laparotomies.6 Brown et al reported on the outcomes of 24,291 patients who underwent an emergency laparotomy on the gastrointestinal tract.11 They found that mortality was decreased for oesophagogastric (7.9% vs 12.9%; p < 0.001) and colorectal procedures (10.9% vs 14.2%; p < 0.001) when performed by surgeons with a specialist interest in the relevant area.11
A number of smaller cases series found that emergency laparotomy performed by a surgeon with the appropriate declared specialist interest were associated with reduced 30-day mortality,12–15 reduced morbidity,12,14–16 reoperation12 and length of stay.12,16 Two of these studies had prolonged periods of recruitment which predate general surgeon specialisation; clearly this introduces potential bias with improvements in techniques and outcomes generally during this time frame.13,16
In keeping with our findings, two retrospective cohort studies found that declared surgeon specialist interest (colorectal or general surgery) has no impact on mortality, morbidity or length of stay following emergency colorectal laparotomies on multivariate analysis (n = 115; n = 196, respectively).17,18
While the largest studies suggest that declared surgeon specialty has an impact on emergency laparotomy outcomes, this is in contrast to our findings. We hypothesise this finding is due to the nature of the on-call structure at our hospital. Alternating 24-hour colorectal and oesophagogastric surgical consultants allows specialty cross-cover when needed. This resulted in just 25% of cases being performed by a surgeon whose declared specialty differed from the operation performed. This was lower than the proportion reported by the largest of the cohort studies (45% and 35%, respectively).6,11 This may mitigate the impact of surgeon subspecialisation. Similar provision may not be feasible in smaller hospitals or those with unequal numbers of colorectal and oesophagogastric surgeons where this would have a significant impact on the delivery of elective services. A rota with both colorectal and oesophagogastric cover also has significant cost implications, countries with a large proportion of specialists such as the United States or Sweden spend between 25% and 55% above other high-income countries with an equal number of generalists and specialists with similar life expectancy and quality of life outcomes.19 We must acknowledge, however, our relatively small sample size of 350, compared with 24,291 and 33,819 for the larger cohort studies in the literature.6,11 This may indicate that our study is underpowered to detect the impact of surgeon-declared specialist interest on emergency laparotomy outcomes resulting in type II error.
A number of benefits were consistently identified in the literature from laparotomies performed by a surgeon with a specialist interest in the relevant area. The use of laparoscopic surgery is higher when the causative pathology is relevant to the surgeons’ declared subspecialty.11 For colorectal emergency laparotomy, colorectal surgeons are more likely to perform a primary anastomosis and less likely to form a stoma.13,14,16–18 We know that, for a large proportion of patients, a Hartmann’s procedure results in a lifelong stoma.20
This study includes a consecutive cohort of patients over a three-year period at a large UK acute hospital. Limitations include its retrospective design which can impact case identification. However, in this hospital, completion of the NELA database is compulsory and is led by a consultant surgeon and anaesthetist to ensure all NELA eligible cases are captured. Missing data from the NELA record were retrieved from the electronic patient record. Multivariate analysis was performed to mitigate for the effect of potential confounders. While the outcomes of a single hospital cannot reflect those nationwide, it is interesting to understand the differences and their potential relationship with the local on-call structure.
Conclusion
In conclusion, in this study declared surgeon specialist interest (colorectal or oesophagogastric) had no effect on the outcomes of general surgery emergency laparotomy (30-day mortality, return to theatre and length of stay). This is likely to reflect low percentage of cases performed by a surgeon whose declared specialty differed from the operation performed. The local on-call structure and close working relationship between colorectal and oesophagogastric surgeons may mitigate the impact of surgeon subspecialisation on emergency general surgery emergency laparotomy outcomes.
References
- 1.Royal College of Surgeons of England Emergency General Surgery. London: RCS; 2012. [Google Scholar]
- 2.Royal College of Surgeons of England The Higher Risk General Surgical Patient: Towards improved care for a forgotten group. London: RCS; 2011. [Google Scholar]
- 3.National Emergency Laparotomy Audit Fourth Patient Report of the National Emergency Laparotomy Audit (NELA) December 2016 to November 2017. London: Royal College of Anaesthetists; 2018. [Google Scholar]
- 4.Huddart S, Peden CJ, Swart M et al. Use of a pathway quality improvement care bundle to reduce mortality after emergency laparotomy. Br J Surg 2015; : 57–66. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Aggarwal G, Peden CJ, Mohammed MA et al. Evaluation of the collaborative use of an evidence-based care bundle in emergency laparotomy. JAMA Surg 2019; : e190145. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Boyd-Carson H, Doleman B, Herrod PJJ et al. Association between surgeon special interest and mortality after emergency laparotomy. Br J Surg 2019; : 940–948. [DOI] [PubMed] [Google Scholar]
- 7.Vester-Andersen M, Lundstrøm LH, Møller MH et al. Mortality and postoperative care pathways after emergency gastrointestinal surgery in 2904 patients: a population-based cohort study. Br J Anaesth 2014; : 860–870. [DOI] [PubMed] [Google Scholar]
- 8.Skala K, Gervaz P, Buchs N et al. Risk factors for mortality-morbidity after emergency-urgent colorectal surgery. Int J Colorectal Dis 2009; : 311–316. [DOI] [PubMed] [Google Scholar]
- 9.Thorsen K, Søreide JA, Søreide K. Long-term mortality in patients operated for perforated peptic ulcer: factors limiting longevity are dominated by older age, comorbidity burden and severe postoperative complications. World J Surg 2017; : 410–418. [DOI] [PubMed] [Google Scholar]
- 10.Chowdhury MM, Dagash H, Pierro A. A systematic review of the impact of volume of surgery and specialization on patient outcome. Br J Surg 2007; : 145–161. [DOI] [PubMed] [Google Scholar]
- 11.Brown LR, McLean RC, Perren D et al. Evaluating the effects of surgical subspecialisation on patient outcomes following emergency laparotomy: A retrospective cohort study. Int J Surg 2019; : 67–73. [DOI] [PubMed] [Google Scholar]
- 12.Kulaylat AS, Pappou E, Philp MM et al. Emergent colon resections: does surgeon specialization influence outcomes? Dis Colon Rectum 2019; : 79–87. [DOI] [PubMed] [Google Scholar]
- 13.Boyce SA, Bartolo DC, Paterson HM, Unit EC. Subspecialist emergency management of diverticulitis is associated with reduced mortality and fewer stomas. Colorectal Dis 2013; : 442–447. [DOI] [PubMed] [Google Scholar]
- 14.Biondo S, Kreisler E, Millan M et al. Impact of surgical specialization on emergency colorectal surgery outcomes. Arch Surg 2010; : 79–86. [DOI] [PubMed] [Google Scholar]
- 15.Zorcolo L, Covotta L, Carlomagno N, Bartolo DC. Toward lowering morbidity, mortality, and stoma formation in emergency colorectal surgery: the role of specialization. Dis Colon Rectum 2003; : 1461–1468. [DOI] [PubMed] [Google Scholar]
- 16.Di Carlo A, Andtbacka RH, Shrier I et al. The value of specialization: is there an outcome difference in the management of fistulas complicating diverticulitis. Dis Colon Rectum 2001; : 1456–1463. [DOI] [PubMed] [Google Scholar]
- 17.Wright GP, Flermoen SL, Robinett DM et al. Surgeon specialization impacts the management but not outcomes of acute complicated diverticulitis. Am J Surg 2016; : 1035–1040. [DOI] [PubMed] [Google Scholar]
- 18.Gibbons G, Tan CJ, Bartolo DC et al. Emergency left colonic resections on an acute surgical unit: does subspecialization improve outcomes? A N Z J Surg 2015; : 739–743. [DOI] [PubMed] [Google Scholar]
- 19.Cutler DM, Ly DP. The (paper) work of medicine: understanding international medical costs. J Econ Perspect 2011; : 3–25. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Hallam S, Mothe BS, Tirumulaju R. Hartmann’s procedure, reversal and rate of stoma-free survival. Ann R Coll Surg Engl 2018; : 301–307. [DOI] [PMC free article] [PubMed] [Google Scholar]