Is surgical Apgar score an effective assessment tool for the prediction of postoperative complications in patients undergoing oesophagectomy?

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1 Interactive CardioVascular and Thoracic Surgery 27 (2018) doi: /icvts/ivy148 Advance Access publication 9 May 2018 BEST EVIDENCE TOPIC Cite this article as: Li S, Zhou K, Li P, Che G. Is surgical Apgar score an effective assessment tool for the prediction of postoperative complications in patientsundergoing oesophagectomy? Interact CardioVasc Thorac Surg 2018;27: Is surgical Apgar score an effective assessment tool for the prediction of postoperative complications in patients undergoing oesophagectomy? Shuangjiang Li, Kun Zhou, Pengfei Li and Guowei Che* Department of Thoracic Surgery, West China Hospital, Sichuan University, Chengdu, China * Corresponding author. Department of Thoracic Surgery, West China Hospital, Sichuan University; Guoxue Alley No.37, Chengdu , China. Tel: ; fax: ; guowei_che@foxmail.com (G. Che). Received 4 November 2017; received in revised form 27 March 2018; accepted 5 April 2018 Summary A best evidence topic in thoracic surgery was written according to a structured protocol. The question addressed was whether the surgical Apgar score (SAS) was an effective assessment tool for the prediction of postoperative complications in patients undergoing oesophagectomy. In total, 7 papers were identified using the reported search, of which 6 cohort studies represented the best evidence to answer the clinical question. The authors, journal, date of publication, patient group studied, type, relevant outcomes and results of these papers are tabulated. Five of 6 cohort studies demonstrated that a low SAS was significantly associated with more postoperative complications in patients undergoing oesophagectomy. The rates of major individual complications in patients with a lower SAS were commonly higher than those in patients with a higher SAS. Two cohort studies further reported that a low SAS was significantly associated with the prolonged length of stay. The cut-off value of the SAS that had the discriminative power for patients who were considered at high risk, however, was not defined but was more likely to be 6 or less. Current available evidence suggests that the SAS system may serve as an effective assessment tool for the prediction of risk after oesophagectomy. Keywords: Surgical Apgar score Oesophagectomy Morbidity Prediction INTRODUCTION A best evidence topic was constructed according to a structured protocol. This is fully described in the ICVTS [1]. THREE-PART QUESTION In [patients undergoing esophagectomy], can [surgical Apgar score] predict the occurrence of [postoperative complications]? CLINICAL SCENARIO You are working at the thoracic surgery department of a highvolume national cancer centre. You are asked, by relatives, about likely outcomes of a patient who has underwent an oesophagectomy. A colleague suggests that the surgical Apgar score (SAS), which consists of 3 major intraoperative parameters [i.e. estimated intraoperative blood loss (EIBL), lowest mean arterial pressure and the lowest heart rate], may help to predict risk [2]. You are unfamiliar with this SAS tool in oesophagectomy. You resolve to search the literature and review the best evidence available. SEARCH STRATEGY A comprehensive literature search was conducted on MEDLINE and Embase databases from 1950 to October 2017 using the PubMed interface. Search strategy employed: [esophagectomy] OR [oesophagectomy] OR [esophageal resection] AND [surgical Apgar score]. SEARCH OUTCOME Seven papers were identified using the reported search. From these, 6 papers were identified that provided the best evidence to answer the question. These are presented in Table 1. RESULTS Janowak et al. [3] performed the earliest retrospective analysis based on a group of 168 patients undergoing oesophagectomy for malignant lesions. On the basis of the clinical practice of oesophagectomy, a modified oesophagectomy SAS system, which had an appropriate adjustment to the original point assignment criteria for EIBL range [2], was utilized intraoperatively VC The Author(s) Published by Oxford University Press on behalf of the European Association for Cardio-Thoracic Surgery. All rights reserved.

2 S. Li et al. / Interactive CardioVascular and Thoracic Surgery 687 (Table 1). An SAS of 6 was determined as the threshold value with regard to major, which were defined according to the National Surgical Quality Improvement Program adverse events definitions [9]. This cut-off score was used to divide 168 enrolled patients into the high-risk group (SAS <_6: n = 82) and the low-risk group (SAS >6: n = 86). The overall rate in patients with an SAS of <_6 was found to be significantly higher than that in patients with an SAS of >6 (45.1 vs 24.4%; P = 0.005). Patients with an SAS of <_6 had higher rates of pneumonia (18.3 vs 9.3%; P = 0.11), anastomotic leakage (19.5 vs 11.6%; P = 0.20), surgical site infection (23.2 vs 12.8%; P = 0.11), chylothorax (4.9 vs 1.2%; P = 0.20) and 30-day mortality (3.7 vs 1.2%; P = 0.36) than those of patients with an SAS of >6 but without reaching statistical significance. Finally, the multivariate logistic regression analysis confirmed that the SAS <_6 was a strongly independent predictor for major following oesophagectomy [odds ratio (OR) 3.75, 95% confidence interval (CI) ; ]. Eto et al. [4] retrospectively reviewed the clinical data of 399 patients undergoing oesophagectomy for malignancies. The authors accepted the original SAS criteria to assign points to each included intraoperative parameter [2] as shown in Table 1. The mean SAS in patients who developed postoperative complications (defined as [10] was significantly lower than that in patients without any complication (5.0 ± 0.1 vs 6.0 ± 0.1; ). A receiver operating characteristic (ROC) analysis further identified an SAS of 6 to be the optimal cut-off value with reference to postoperative, at which the joint sensitivity plus specificity was maximal. Given this cut-off, there were 154 patients with an SAS of <6 and 245 patients with an SAS of >_6, respectively. The rates of overall (46.1 vs 22.4%; ), respiratory complications (18.8 vs 8.3%; P = 0.003), anastomotic leakage (20.8 vs 7.8%; ) and surgical site infection (30.5 vs 12.7%; ) in patients with an SAS of <6 were all significantly higher than those in patients with an SAS of >_6. No significant difference was found between these 2 groups in terms of the incidences of recurrent laryngeal nerve paralysis (5.8 vs 2.9%; P = 0.15) and chylothorax (3.9 vs 1.2%; P = 0.090). The multivariate logistic regression analysis demonstrated that the SAS <6 could independently predict the occurrence of postoperative complications (OR 2.88, 95% CI ; P <0.001). Giugliano et al. [5] retrospectively evaluated the clinical data of 212 patients undergoing oesophagectomy for both malignant and non-malignant lesions. After adjusting the original point assignment criteria for EIBL range according to the clinical practice of oesophagectomy [2], a modified SAS system was adopted intraoperatively as shown in Table 1. The SASs of all enrolled patients were collapsed into 5 categorizations for further comparative analyses (0 2: n = 5; 3 4: n = 23; 5 6: n =81;7 8:n =96and9 10:n =7). The univariate analysis showed a significant decrease in both Clavien Dindo Grade >_II and Grade >_III complications with the increasing SAS levels () [10]. In addition, each one category decrease in the SAS was found to be significantly associated with the prolonged length of stay (). Both the patients with the SAS of 0 2 and the patients with an SAS of 3 4 had the highest probability of developing Clavien Dindo Grade >_II (0 2: n = 5, rate- = 100%; 3 4: n = 17, rate = 73.9%; P <0.001) and Grade >_III complications (0 2: n = 3, rate = 60%; 3 4: n = 15, rate = 65.2%; P <0.001). The patients with an SAS of 9 10 had the lowest rates of Clavien Dindo Grade >_II complications (n = 1, rate = 14.3%) and anastomotic leakage (n = 1, rate = 14.3%). No Clavien Dindo Grade >_III complication was developed in the patients with an SAS of Finally, the multivariate logistic regression analysis indicated that each one category increase in the SAS was significantly associated with the decreased Clavien Dindo Grade >_II complications (OR 0.53, 95% CI ; P = 0.002), Clavien Dindo Grade >_III complications (OR 0.50, 95% CI ; ) and in-hospital mortality (OR 0.40, 95% CI ; P = 0.019). Nakagawa et al. [6] carried out the largest retrospective cohort based on 400 patients undergoing oesophagectomy for malignant lesions. An original SAS system was utilized to assign points to each estimated parameter during the oesophagectomy (Table 1) [2]. On the basis of an ROC curve, an SAS of 5 was determined as the threshold value with the maximum joint sensitivity plus specificity for predicting risk of (defined as the Clavien Dindo Grade >_III [10]. Then, this cut-off score was applied to divide the entire cohort into the group of patients with an SAS of <_5 (n = 181) and the group of patients with an SAS of >5 (n = 219). Patients with an SAS of <_5 had the significantly higher rates of overall (49.7 vs 25.1%; ), respiratory complications (21.5 vs 9.6%; ) and gastrointestinal complications (24.9 vs 14.2%; P = 0.008) than those of patients with an SAS of >5. The further multivariate logistic regression analysis demonstrated that an SAS of <_5 was significantly associated with overall (OR 2.86, 95% CI ; ), respiratory complications (OR 2.23, 95% CI ; P = 0.010) and gastrointestinal complications (OR 1.75, 95% CI ; P = 0.035) after oesophagectomy. Strøyer et al. [7] retrospectively analysed the clinical data of 234 patients undergoing Ivor-Lewis oesophagectomy for malignant oesophagogastric junction adenocarcinoma. The authors adopted an interquartile range for EIBL in their cohort of oesophagectomy to modify the point assignment criteria of the original SAS system [2] as shown in Table 1. The area under the ROC curve for the modified SAS on the prediction of major (defined as [10] was 0.57 (95% CI ; P = 0.090). The univariate analysis showed no significant difference in the median SAS between patients with complications and patients without complications (P = 0.084). Finally, the modified SAS was not found to have a significant predictive value for major when evaluated as continuous variables in the multivariate logistic regression analysis (OR 0.84, 95% CI ; P = 0.096). Xing et al. [8] performed a retrospective analysis based on a cohort of 189 patients undergoing oesophagectomy for malignancies. A tailor-made SAS system that modified the original point assignment criteria for EIBL range based on the clinical practice of oesophagectomy was utilized intraoperatively [2] as shown in Table 1. The threshold value of the modified SAS determined by an ROC analysis was 7 to discriminate whether patients were at the high risk of major (defined as the Clavien Dindo Grades III IV [10]. This cut-off score was used to divide 189 enrolled patients into the high-risk group (SAS <_7: n = 156) and the low-risk group (SAS >7: n = 33). The major rate in patients with an SAS of <_7 was significantly higher than that in patients with an SAS of >7 (63.5 vs 33.3%; ). In addition, patients with an SAS of <_7 had a significantly prolonged length of stay than that of patients with an SAS of >7 (32.2 ± 22.7 vs 25.4 ± 14.4 days; P = 0.030). No significant difference was found in the in-hospital mortality between patients with an SAS of <_7 and patients with an SAS of >7 (7.7 vs 3.0%; P = 0.47). Finally, the multivariate logistic regression analysis indicated that an SAS of <_7 was an independent risk factor for major following oesophagectomy (OR 2.81, 95% CI ; P = 0.030). ADULT CARDIAC

3 688 S. Li et al. / Interactive CardioVascular and Thoracic Surgery Best evidence papers Janowak et al. (2015), J Thorac Cardiovasc Surg, USA [3] Eto et al. (2016), World J Surg, Japan [4] Study period: Total sample size: n = 168 Male/female: 122/46 Mean age: 65 ± 10 years Co: overall, n = 83; pulmonary, n = 23; cardiovascular, n =58 n = 69; hybrid, n = 83; MIO, n =16 0 point: EIBL >300 ml, LMAP <40 1 point: EIBL = ml, LMAP = 2 points: EIBL = ml, LMAP = 3 points: EIBL <_150 ml, LMAP >_70 Threshold value of SAS = 6 Group A (SAS <_6): n =82 Group B (SAS >6): n =86 Study period: Total sample size: n = 399 Male/female: 357/42 Mean age: 65.7 ± 0.6 years Co: overall, n = 286 Operative procedures: thoracoscopic assist, n = 354; laparoscopic assist, n = point: EIBL >1000 ml, LMAP <40 1 point: EIBL = ml, LMAP = 2 points: EIBL = ml, LMAP = 3 points: EIBL <_100 ml, LMAP >_70 Overall (defined as the NSQIP adverse events) 30-Day mortality Pneumonia Anastomotic leakage Surgical site infection Clavien Dindo Grade III IV complications Chylothorax Overall (defined as Respiratory complications Anastomotic leakage Surgical site infection Recurrent laryngeal nerve paralysis Chylothorax Rate = 34.5% (n = 58) Group A: 37/82 (45.1%) Group B: 21/86 (24.4%) P = Rate = 2.4% (n =4) Group A: 3/82 (3.7%) Group B: 1/86 (1.2%) P = 0.36 Rate = 13.7% (n = 23) Group A: 15/82 (18.3%) Group B: 8/86 (9.3%) P = 0.11 Rate = 15.5% (n = 26) Group A: 16/82 (19.5%) Group B: 10/86 (11.6%) P = 0.20 Rate = 17.9% (n = 30) Group A: 19/82 (23.2%) Group B: 11/86 (12.8%) P = 0.11 Rate = 13.7% (n = 23) Group A: 14/82 (17.1%) Group B: 9/86 (10.5%) P = 0.26 Rate = 3.0% (n =5) Group A: 4/82 (4.9%) Group B: 1/86 (1.2%) P = 0.20 SAS <_6 vs SAS >6: OR 3.75, 95% CI ; Rate = 31.6% (n = 126) Group A: 71/154 (46.1%) Group B: 55/245 (22.4%) Rate = 12.5% (n = 50) Group A: 29/154 (18.8%) Group B: 21/245 (8.3%) P = Rate = 12.8% (n = 51) Group A: 32/154 (20.8%) Group B: 19/245 (7.8%) Rate = 19.5% (n = 78) Group A: 47/154 (30.5%) Group B: 31/245 (12.7%) Rate = 4.0% (n = 16) Group A: 9/154 (5.8%) Group B: 7/245 (2.9%) P = 0.15 Rate = 2.3% (n =9) Group A: 6/154 (3.9%) First article to demonstrate the predictive value of the SAS system in oesophagectomy The low SAS was predictive of major after oesophageal cancer resections

4 S. Li et al. / Interactive CardioVascular and Thoracic Surgery 689 Giugliano et al. (2017), J Surg Oncol, Japan [5] Threshold value of SAS = 6 Group A (SAS <6): n = 154 Group B (SAS >_6): n = 245 Study period: Total sample size: n = 212 Male/female: 175/37 Mean age: 63.5 (31 86) years Co: no data reported, n = 191; dysplasia of oesophagus, n = 9; other non-malignancy diseases, n =12 n = 45; transhiatal, n = 40; MIO, n = point: EIBL >400 ml, LMAP <40 1 point: EIBL = ml, LMAP = 2 points: EIBL = ml, LMAP = 3 points: EIBL<100 ml, LMAP >_70 SAS 0 2: n =5 SAS 3 4: n =23 SAS 5 6: n =81 SAS 7 8: n =96 SAS 9 10: n =7 Clavien Dindo Grade >_II complications Clavien Dindo Grade >_III complications Anastomotic leakage Length of stay Multivariate analysis of each one SAS category increase for predicting postoperative outcomes Group B: 3/245 (1.2%) P = SAS <6 vs SAS >_6: OR 2.88, 95% CI ; Rate = 52.4% (n = 147) 0 2: 5/5 (100%) 3 4: 17/23 (73.9%) 5 6: 45/81 (55.6%) 7 8: 43/96 (44.8%) 9 10: 1/7 (14.3%) Rate = 31.6% (n = 67) 0 2: 3/5 (60%) 3 4: 15/23 (65.2%) 5 6: 27/81 (33.3%) 7 8: 22/96 (22.9%) 9 10: 0/7 (0.0%) Rate = 17.9% (n = 38) 0 2: 2/5 (40%) 3 4: 6/23 (26.1%) 5 6: 12/81 (14.8%) 7 8: 17/96 (17.7%) 9 10: 1/7 (14.3%) P = 0.29 Overall: media n = 10 days; range = 1 87 days 0 2: median = 20 days 3 4: median = 16 days 5 6: median = 10 days 7 8: median = 9 days 9 10: median = 8 days Clavien Dindo Grade >_II complications: OR 0.53, 95% CI ; P = Clavien Dindo Grade >_III complications: OR 0.50, 95% CI ; Anastomotic leakage: OR 0.88, 95% CI ; P = 0.59 In-hospital mortality: OR 0.40, 95% CI ; P = The low SAS was significantly associated with the increased rate and the prolonged length of stay ADULT CARDIAC Nakagawa et al. (2017), Ann Surg Oncol, Japan [6] Study period: Total sample size: n = 400 Male/female: 338/62 Mean age: no data reported Co: hypertension, n = 89; diabetes, n = 28; respiratory Overall (defined as Respiratory complications Rate = 36.3% (n = 145) Group A: 90/181 (49.7%) Group B: 55/219 (25.1%) Rate = 15.0% (n = 60) Group A: 39/181 (21.5%) Group B: 21/219 (9.6%) There was a significant correlation between the low SAS and both in-hospital and long-term prognosis after oesophagectomy

5 690 S. Li et al. / Interactive CardioVascular and Thoracic Surgery Strøyer et al. (2017), J Surg Oncol, Denmark [7] dysfunction, n =72 n = 38; MIO, n = point: EIBL >1000 ml, LMAP <40 1 point: EIBL = ml, LMAP = 2 points: EIBL = ml, LMAP = 3 points: EIBL <_100 ml, LMAP >_70 Threshold value of SAS = 5 Group A (SAS <_5): n = 181 Group B (SAS >5): n = 219 Study period: Total sample size: n = 234 Male/female: 191/43 Mean age: 65 (58 70) years Co: COPD, n = 11; diabetes, n = 40; cardiovascular, n = 47 Diagnosis: oesophagogastric junction adenocarcinoma n = 193; robotically assisted procedure, n =41 0 point: EIBL >75th percentile, LMAP <40 1 point: EIBL >median-75th percentile, LMAP = mmhg, LHR = bpm 2 points: EIBL >25th percentile-median, LMAP = mmhg, LHR = bpm 3 points: EIBL <_25th percentile, LMAP >_70 Gastrointestinal complications Major (defined as Multivariate analysis of each one SAS category increase for predicting postoperative Rate = 19.0% (n = 76) Group A: 45/181 (24.9%) Group B: 31/219 (14.2%) P = SAS <_5 vs SAS >5 Overall : OR 2.86, 95% CI ; Respiratory complications: OR 2.23, 95% CI ; P = Gastrointestinal complications: OR 1.75, 95% CI ; P = Rate = 27.4% (n = 64) Group A: median SAS = 6 (5 7) Group B: median SAS = 6 (5 7) P = OR = 0.84; 95% CI = ; P = No difference in the modified SAS between patients with and without Group A (with ): n =64 Group B (without ): n = 170 Xing et al. (2016), J Thorac Dis, China [8] Study period: Total sample size: n = 189 Male/female: 161/28 Mean age: 64.6 ± 9.6 years Major (defined as Length of stay Rate = 58.2% (n = 110) Group A: 99/156 (63.5%) Group B: 11/33 (33.3%) Group A: 32.2 ± 22.7 days Group B: 25.4 ± 14.4 days P = The low SAS was significantly associated with the increased rate and the prolonged length of stay

6 S. Li et al. / Interactive CardioVascular and Thoracic Surgery 691 CLINICAL BOTTOM LINE A low SAS can serve as an excellent predictor for postoperative complications in patients undergoing oesophagectomy. The rates of major individual complications in patients with a lower SAS are commonly higher than those in patients with a higher SAS. A low SAS may be significantly associated with the prolonged length of stay. The cut-off value of the SAS for risk is likely to be 6 or less. The SAS system may serve as an effective assessment tool for the prediction of after oesophagectomy. Conflict of interest: none declared. ACKNOWLEDGEMENTS The authors thank Stanley Crawford, from the Institution of Medical English, West China Medical Center, Sichuan University, Chengdu, China, for his help with the English language editing of this article. REFERENCES Co: hypertension, n = 41; diabetes, n = 11; coronary heart disease, n = 11; COPD, n =3 Operative procedures: all thoracotomy 0 point: EIBL >600 ml, LMAP <40 1 point: EIBL = ml, LMAP = 2 points: EIBL = ml, LMAP = 3 points: EIBL <_200 ml, LMAP >_70 Threshold value of SAS = 7 Group A (SAS <_7): n = 156 Group B (SAS >7): n =33 [1] Dunning J, Prendergast B, Mackway-Jones K. Towards evidence-based medicine in cardiothoracic surgery: best BETS. Interact CardioVasc Thorac Surg 2003;2: In-hospital mortality Rate = 6.9% (n = 13) Group A: 12/156 (7.7%) Group B: 1/33 (3.0%) P = 0.47 SAS <_7 vs SAS >7: OR = 2.81; 95% CI = ; P = CI: confidence interval; COPD: chronic obstructive pulmonary disease; EIBL: estimated intraoperative blood loss; LHR: lowest heart rate; LMAP: lowest mean arterial pressure; MIO: minimally invasive oesophagectomy; NSQIP: National Surgical Quality Improvement Program; OR: odds ratio; SAS: surgical Apgar score. [2] Gawande AA, Kwaan MR, Regenbogen SE, Lipsitz SA, Zinner MJ. An Apgar score for surgery. J Am Coll Surg 2007;204: [3] Janowak CF, Blasberg JD, Taylor L, Maloney JD, Macke RA. The Surgical Apgar Score in esophagectomy. J Thorac Cardiovasc Surg 2015;150: [4] Eto K, Yoshida N, Iwatsuki M, Kurashige J, Ida S, Ishimoto T et al. Surgical Apgar Score predicted postoperative after esophagectomy for esophageal cancer. World J Surg 2016;40: [5] Giugliano DN, Morgan A, Palazzo F, Leiby BE, Evans NR, Rosato EL et al. Surgical Apgar score (SAS) predicts perioperative, mortality, and length of stay in patients undergoing esophagectomy at a highvolume center. J Surg Oncol 2017;116: [6] Nakagawa A, Nakamura T, Oshikiri T, Hasegawa H, Yamamoto M, Kanaji S et al. The Surgical Apgar Score predicts not only short-term complications but also long-term prognosis after esophagectomy. Ann Surg Oncol 2017;24: [7] Strøyer S, Mantoni T, Svendsen LB. Evaluation of the surgical Apgar score in patients undergoing Ivor-Lewis esophagectomy. J Surg Oncol 2017;115: [8] Xing XZ, Wang HJ, Qu SN, Huang CL, Zhang H, Wang H et al. The value of esophagectomy surgical Apgar score (esas) in predicting the risk of major after open esophagectomy. J Thorac Dis 2016;8: [9] Khuri SF, Daley J, Henderson W, Barbour G, Lowry P, Irvin G et al. The National Veterans Administration Surgical Risk Study: risk adjustment for the comparative assessment of the quality of surgical care. J Am Coll Surg 1995;180: [10] Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004;240: ADULT CARDIAC

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