Can POSSUM accurately predict post-operative complications risk in patients with abdominal Crohn s disease?

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1 COLORECTAL ANZJSurg.com Can POSSUM accurately predict post-operative complications risk in patients with abdominal Crohn s disease? Giampaolo Ugolini,* Isacco Montroni,* Giancarlo Rosati,* Federico Ghignone,* Maria Letizia Bacchi-Reggiani, Andrea Belluzzi, Lucia Castellani and Mario Taffurelli* *Department of Medical and Surgical Sciences, University of Bologna, Policlinico S.Orsola-Malpighi, Bologna, Italy and Department of Specialised, Experimental, and Diagnostic Medicine, University of Bologna, Policlinico S.Orsola-Malpighi, Bologna, Italy Key words complications, Crohn s disease, POSSUM, risk prediction, surgery. Correspondence Dr Isacco Montroni, Department of Medical and Surgical Sciences, University of Bologna, Policlinico S.Orsola-Malpighi, Via Massarenti 9, Bologna, Italy. isacmontroni@yahoo.com G. Ugolini MD, PhD; I. Montroni MD; G. Rosati MD, PhD; F. Ghignone MD; M. L. Bacchi-Reggiani MD; A. Belluzzi MD; L. Castellani MD; M. Taffurelli MD. Giampaolo Ugolini and Isacco Montroni contributed equally to this work. Accepted for publication 22 May doi: /ans Abstract Background: Although the majority of patients with Crohn s disease (CD) are young, they are often seriously ill when surgery is required. The Physiological and Operative Severity Score for the enumeration of Mortality and morbidity (POSSUM) is a risk prediction scoring system estimating 30-day complications. The primary endpoint was to evaluate POSSUM efficacy in this subgroup. The secondary endpoint was to determine any potential correlation between POSSUM, Harvey Bradshaw Index (HBI), length of stay (LOS) and anastomotic leak. Methods: All patients affected by abdominal CD who underwent elective and emergency surgery from 2006 to 2011 were prospectively enrolled in the study. POSSUM expected morbidity and mortality were compared to the observed outcomes (O/E ratio). Logistic regression analysis was performed to evaluate POSSUM and HBI adequacy. Correlation between POSSUM, HBI, LOS and anastomotic leak was investigated with linear regression analysis. Results: One hundred twenty-three patients underwent abdominal surgery. The overall 30-day mortality rate estimated by the Portsmouth-POSSUM was 1.22% (95% confidence interval (CI) ) while no deaths were observed (O/E = 0). The prediction regarding the post-operative complication rate was 22.04% (95% CI ) and the observed overall morbidity rate was 21.95% (O/E = 0.99). The mean HBI score was 6.85 while LOS was 9.4 days. POSSUM and HBI were found to be significant predictors of post-operative complications at the univariate logistic regression analysis (OR % CI and OR % CI , respectively). Linear regression analysis showed a significant correlation between POSSUM, HBI and LOS. Conclusion: POSSUM is precise in predicting post-operative complications in patients with abdominal CD. POSSUM correlates with HBI. Introduction Despite the improvement in available medical treatment, surgery is still an option in Crohn s disease (CD). A surgical approach should be limited to cases of failure of medical treatment when symptomatic strictures or bowel damage are unlikely to heal with a noninvasive approach. About 80% of patients with CD will require surgery during their lifetime and at least 40 50% of them will undergo a new CD-related operation within 10 years from their first procedure. 1 Patients affected by CD can be frail, and progressive deterioration of their quality of life is not only related to the natural history of the disease but also to immunosuppressors themselves (steroids, azathioprine, biologics, etc.). Surgery can sometimes be an unpleasant addition that might increase frailty. All surgical procedures have clearly been defined as consistent stressors in debilitated patients but surgical complications could have massive consequences in diminishing the functional reserve of the patient. Post-operative complications are not infrequent in CD surgery because of the clinical features of this subgroup of patients (low body mass index, ANZ J Surg 84 (2014) 78 84

2 POSSUM risk-prediction in Crohn s disease 79 malnourishment, infection, immunosuppression) often associated with an unfavourable surgical setting (emergency versus urgency), indications (perforation, peritonitis, obstruction) and reiteration (multiple procedures over time). Being able to estimate surgical risk is a key point for every patient but, above all, for CD patients where consequences could be dramatic in terms of quality of life impairment. The 30-day operative morbidity and mortality rate is one of the most accepted methods of evaluating the effectiveness of a surgical procedure. 2 One major limitation of any crude morbidity and mortality determination is that it does not include the physiological condition of the patient and the complexity of the procedures performed. For these reasons, 30-day mortality and morbidity alone are inadequate for estimating the benefits, risks or efficacy of an operation and, ultimately, the quality of care. In recent years, several risk prediction scoring systems have been developed for the prediction of post-operative mortality and morbidity, based on individual patient condition. Among these systems, the Physiological and Operative Severity Score for the enumeration of Mortality and morbidity (POSSUM) 3 5 has been introduced, validated and is utilized worldwide. The primary endpoint of this study was to evaluate POSSUM adequacy in predicting post-operative outcomes in this specific surgical population. The secondary endpoints were to evaluate the potential correlation between an elevated POSSUM score and anastomotic leak rate, length of stay (LOS) and the Harvey Bradshaw Index (HBI). Methods Data from consecutive patients affected by primary abdominal CD who underwent elective and emergency surgery from January 2006 to May 2011 were prospectively enrolled in the study and analyzed. Patients undergoing surgery exclusively for perianal disease (fistulain-anus, abscess, etc.) with no other abdominal procedure were excluded from the study. All patients included were operated on in a single surgical unit. Data collection included age, gender, social history, medications, body mass index at admission, albumin, erythrocyte sedimentation rate (ESR), C-reactive protein (CRP), admission date, procedure date, localization, behaviour and age at onset according to the Montreal classification, 6 disease activity according to the HBI, 7 associated perianal disease, associated extra-intestinal disease, familiarity for inflammatory bowel diseases (IBD), surgical setting (emergency versus urgency versus elective), type of procedure and type of anastomosis performed, American Society of Anesthesiology class, LOS (intended to discharge home or death). The POSSUM risk prediction score was calculated for each individual patient. All data were prospectively accumulated by the senior surgical resident staff (postgraduate years 4, 5, 6) during patient admission, hospital stay and follow-up visit, under the supervision of the attending surgeon in charge of the study (GU) and were entered into a database specifically designed for this purpose. 8 A 30-day post-operative follow-up visit was ultimately carried out for every patient to detect every unplanned event (mortality and morbidity) occurred in our population. POSSUM The POSSUM risk prediction scoring system is composed of two separate sections: a physiological (preoperative) and an operative score (OS). The physiological score (PS) includes 12 main parameters divided into four categories according to increasing severity while six parameters were again divided into four levels of severity which constituted the OS (Table 1). Morbidity risk was calculated according to the logistic regression equations proposed by Copeland. 3 The Portsmouth-POSSUM (P-POSSUM) 9 is considered a development of the previously described POSSUM score, the two systems both analyse the same PS and OS items stratified by severity giving a final score (which is the same for both tests, POSSUM and P-POSSUM). The final score is then put in a specific logarithmic equation (different from the POSSUM logarithm) in order to obtain a more accurate mortality prediction. The original paper by Prytherch only limited P-POSSUM prediction to the risk of 30 days post-operative mortality. The P-POSSUM equation was then utilized, in our study, for the mortality estimation while we used the POSSUM score prediction for the morbidity estimation. The online version of the POSSUM scoring system was used ( 10 ) to obtain the correct prediction. The only missing data were those regarding the measurement of blood loss, which was occasionally not recorded. In these cases, the minimum score of one was given (<100 ml), as suggested by the author of the POSSUM system. 11 Emergency surgery was defined as a non-elective procedure performed within 24 h of an unplanned hospital admission. Harvey Bradshaw Index The HBI was first proposed by Harvey and Bradshaw in 1980 in order to monitor the clinical activity of CD 7 based on five simple parameters. Patient general well-being is divided into five levels of severity, and abdominal mass and abdominal pain into four levels. One point is scored for each liquid bowel movement and for each complication (arthralgia, uveitis, erythema nodosum, aphtous ulcer, pyoderma gangrenosum, anal fissure, new fistula and abscess). Remission is considered when the final score is less than 5; mild to moderate disease is diagnosed when the total score is between 5 and 15 while severe disease is concerning for scores greater than 16. In our study, the score was calculated at hospital admission. Montreal classification The Montreal classification was chosen to stratify the patients according to three main items: age at onset, disease localization and behaviour. The age at onset is classified as A1 (<16 years old), A2 (17 40 years old) and A3 (>40 years old). Disease location is classified as L1 for ileal disease with or without involvement of cecum, L2 for colonic disease, L3 for disease extending to the ileum and colon, and L4 for upper gastrointestinal tract disease. If upper gastrointestinal tract disease is present in addition to L1, L2 or L3, the designation L4 is added as a modifier. Inflammatory disease behaviour with no signs of strictures or fistulas is classified as B1, stricturing behaviour as B2, penetrating

3 80 Ugolini et al. Table 1 The POSSUM physiologic and operative variables POSSUM physiological score Score Age (years) < >70 Cardiac signs No failure Diuretic, digoxin, antianginal or hypertensive therapy Warfarin therapy, peripheral oedema, borderline cardiomegaly, Respiratory history No dyspnea Mild COPD, dyspnea on Moderate COPD, limiting dyspnea exertion Raised jugular venous pressure, cardiomegaly Dyspnea at test (rate >30 mm), fibrosis or consolidation Electrocardiogram Normal Atrial fibrillation (rate 60 90) VES >5/min, Q waves or ST/T waves changes, any other abnormal rhythm Systolic blood pressure (mmhg) or >170 or <89 Pulse (beats/min) or >120 or <40 Haemoglobin (g/dl) or or <10.0 or >18.0 White cells count ( 10 3 /ml) or or < Potassium (mmol/l) or or <2.8 or >6.0 Creatinin (mg/dl) < >170 Sodium(mmol/L) > <125 Glasgow Coma Scale <8 POSSUM operative score Score Operative severity Minor Moderate Major Major+ Multiple procedures 1 2 >2 Total blood loss (ml) > >1.000 Peritoneal soiling None Minor (serous fluid) Local pus Free bowel content, pus or blood Presence of malignancy None Primary only Nodal metastases Distant metastases Mode of surgery Elective Emergency resuscitation of >2h possible, operation <24 after admission Emergency (immediate surgery <2 h needed) POSSUM logistic regression equation for morbidity: LogeR2/(1 R2) = (0.16 PS) + (0.19 OS); P-POSSUM logistic regression equations for mortality: LogR1/(1 R1) = ( PS) + ( OS). The P-POSSUM predictor equation was limited to mortality estimation rate while the POSSUM equation was used for morbidity risk calculation. COPD, chronic obstructive pulmonary disease; OS, operative score; POSSUM, Physiological and Operative Severity Score for the enumeration of Mortality and morbidity; PS, physiological score; R1, risk of mortality; R2, risk of morbidity; VES, ventricular extrasystole. behaviour as B3 and perianal disease as P. If perianal disease is present concomitantly with B1, B2 or B3, the designation P is added as a modifier. Complications A search of the literature for the most common post-operative complications associated with gastrointestinal surgery was performed A list of 27 complications, additionally divided into major and minor according to Clavien-Dindo classification, 15,16 was assembled and used in our study. Clavien-Dindo Grade I-II were considered as minor complications while grade III-IV-V were listed as major complications. Statistical methods The observed/expected (O/E) ratio was used to compare the observed over expected number of adverse events in order to identify the POSSUM score accuracy. An O/E ratio equal to 1 confers 100% predictive accuracy, a ratio less than 1.00 indicates the model overpredicts postsurgical complications while an O/E ratio greater than 1.00 indicates an under-prediction of the POSSUM scoring system. Logistic regression analysis was performed in order to evaluate the POSSUM score and HBI as possible predictors of post-operative adverse events. The POSSUM score was considered as the algebraic sum of the PS and the OS. Model discrimination and calibration were assessed using the area under the receiver operating characteristic (ROC) curve and the Hosmer-Lemeshow (HL) test. P-values 0.05 were considered to be significant. Statistical analyses were performed using STATA/SE version 11.2 for Windows (StataCorp LP, College Station, TX, USA). Results A total of 123 patients undergoing surgery for abdominal CD from January 2006 to June 2011 were enrolled. Patient characteristics are shown in Table 2. Data regarding the Montreal classification, the HBI and medical treatment at admission are reported in Table 2. The physiological and OSs were calculated for each patient. The overall 30-day mortality rate estimated by the P-POSSUM was 1.22% (95% confidence interval (CI) ) while no deaths were observed (O/E = 0). Twenty-seven patients had at least one post-operative complication (27/123, 21.95%; Table 3). Thirty were classified as minor complications and six as major complications for a total of 36 events. No patient died within 30 days from surgery. Table 3 shows the details of the complications occurred in our population. Among the minor complications, the most frequent were surgical site infec-

4 POSSUM risk-prediction in Crohn s disease 81 Table 2 Demographic and surgical data Demographic data No. (%) Demographic data No. (%) Montreal classification No. (%) Surgical procedures No (%) Patients 123 Crohn s related co-morbidities 34 (27.6) Localization at diagnosis Abdominal perineal resection (Miles procedure) Male 72 (58.53) None 89 (72.35) L1 78 (65.5) Total colectomy 2 Female 51 (41.46) Hepatic steatosis 12 (9.75) L2 17 (14.3) Segmental colonic resection 19 Age at admission (mean ± SD) 42.9 ± 15.8 Gallstones 11 (8.94) L3 20 (16.8) Small bowel resection 19 Age at diagnosis (mean ± SD) 32.9 ± 15.2 Primary sclerosing colangitis 0 L4 4 (3.2) Ileocecal resection 51 Duration of disease in months Biliary cirrhosis 0 L4 + L1/L2/L3 6 (5) Ileocolonic resection 27 Age at first Crohn s related surgery (mean ± SD) 37.8 ± 15.2 Peripheral arthritis 6 (4.87) Localization at admission Strictureplasty 89 Previous Crohn s related surgery (mean) 1.3 Ankylosing spondylitis 2 (1.62) L1 72 (58.5) BMI (mean) 21.4 Rheumatoid arthritis 1 (0.81) L2 11 (8.9) Total number of primary 98 anastomosis Albumin g/dl (mean, preoperative) 3.8 ( ) Erythema nodosum 2 (1.62) L3 32 (26.0) Total number of stomas 9 Erythrocytes sedimentation rate (ESR) mm/h (mean, preoperative) C-reactive protein (CRP) mg/dl (mean, preoperative) (2 120) Pyoderma gangrenosum 0 L4 4 (3.2) 4.52 ( ) Cutaneous CD 0 L4 + L1/L2/L3 4 (3.2) Emergent/urgent surgery 6 (5.6) Stomatitis 1 (0.81) Behaviour at diagnosis Elective surgery 117 (94.4) Medications Uveitis 1 (0.81) B1 21 (17.5) Post-operative length of 9.4 stay (days) Amino salicylic acid (ASA) 46 (37.4) Family history (first-degree) 6 (4.87) B2 85 (70.8) IBD Steroids (including Budesonide) 86 (69.9) Smoker B3 13 (10.8) Methotrexate 3 (2.4) Yes 49 (39.82) P 11 (9.1) Azathioprine 30 (24.4) Ex-smoker 29 (23.57) Behaviour at admission Harvey Bradshaw Index No. (%) Biologics 7 (5.7) No 45 (36.58) B1 0 Remission (<5) 41 (34.2) B2 71 (57.7) Mild (5 7) 36 (30) B3 52 (42.3) Moderate (8 15) 42 (35) P 14 (11.4) Severe (>16) 1 (0.83) 1 ESR and CRP data were available for only 74 (74/123, 60.1%) and 69 (69/123, 56.1%) patients, respectively. No patients had obvious respiratory impairment at preoperative pulmonary function tests or anomalies detected at preoperative chest X-ray. At least for 2 consecutive months before surgery. Thirteen patients underwent no therapy (13/123, 11%); 59 patients (59/123, 48%) underwent monotherapy; 51 patients (51/123, 41%) underwent combined medical therapy with at least two specific drugs. Data related to preoperative localization and behaviour at diagnosis were available for 119/123 (96.7%) patients reflecting the fact that some patients were previously diagnosed and treated in other hospitals and the information was missed on admission. HBI score was possible to be calculated on admission for 120/123 (97.5%) patients. Several patients underwent multiple procedures (i.e. ileocolonic resection + jejunal strictureplasty) for a total of 208. Ileocolic resections include stenotic ileocolic anastomosis resection and ileocecal resection with extension to the right colon when involved by active CD. An average of three stricturoplasties were performed on 29 patients as follows: 78 Heineke-Mickulicz, 6 Finney, 3 Jaboulay and 2 Michelassi. Total number of primary anastomosis includes anastomosis performed without diverting loop ileostomy (strictureplasties are excluded). BMI, body mass index; CD, Crohn s disease; IBD. inflammatory bowel disease; SD, standard deviation.

5 82 Ugolini et al. Table 3 The number of major and minor complications monitored and observed Major complications No. Minor complications No. Acute myocardial infarction 1 Atrial fibrillation (no haemodynamic instability) 1 Ventricular fibrillation or major arrhythmias 0 Other minor arrhythmias 0 Cardiac arrest 0 Pneumonia 2 Congestive heart failure 0 Surgical site infection 6 Deep venous thrombosis 0 Urinary tract infection 2 Pulmonary embolism 0 Central line infection 5 Respiratory failure 0 Other 4 Pulmonary oedema 0 Increase in creatinine >1.5 mg/dl from baseline 0 Pneumothorax 0 Unplanned in-hospital readmission without interventional treatment 4 Aspiration pneumonia 0 Operative/post-operative transfusion of 2 U of packed red cells and 6 Hb decreased by 2 g/dl (or more) from baseline Stroke/transitory ischemic attack 0 Severe sepsis 1 Renal impairment with haemodialysis 1 Anastomotic leak with re-intervention 1 Anastomotic leak without re-operation (conservative management) 2 Re-operation for other reasons (i.e. obstruction, bleeding, 0 abdominal abscess, evisceration) Death 0 Total (major) 6 Total (minor) 30 Total (major + minor) 36 complications Clavien-Dindo Grade I-II were considered as minor complications while grade III-IV-V were listed as major complications. Other includes: peripheral line infection, perianal abscess, home discharge with Foley catheter in place, pleural effusion with no heart failure or pneumonia. 36 complications observed in a total of 27 patients (27/123, 21.95%). Fig. 1. Linear regression analysis showed a positive correlation both between the POSSUM score and the HBI and between POSSUM and LOS (P < 0.05). Y-axis = HBI score (a) and LOS (days) (b); X-axis = POSSUM score. tion (6/30; 20%), post-operative blood transfusions of two units of packed red blood cells or more (6/30; 20%) and central line infection (5/30; 17%). A major complication analysis showed three anastomotic leaks. In two cases, conservative management was successfully chosen with percutaneous abdominal drainage, intravenous antibiotics and total parenteral nutrition while one patient required surgical re-exploration and temporary faecal diversion (loopileostomy). Four patients underwent unplanned readmission within 30 days after surgery, due to small bowel obstruction (three patients, resolved with medical treatment) and low-grade fever of unknown origin (one patient) resolved without need of antibiotics (imaging and laboratory work up failed to identify any clear source of infection). No patient was lost to follow-up. The prediction regarding the post-operative complication rate was 22.04% (95% CI ) while the observed overall morbidity rate (36 complications occurred in a total of 27 patients, 27/123) was 21.95% (O/E = 0.99). The mean POSSUM score of patients with anastomotic leaks was 27.3 while the mean POSSUM score of patients without any complications was The mean HBI score was 6.85 (7.75 for complicated patients) while LOS was 9.4 days (15.26 for complicated patients). Univariate logistic analysis showed that POSSUM score (PS + OS) is a significant predictor of adverse post-operative complications in CD (OR % CI P = 0.002; Area under ROC curve 0.701, HL test P = 0.712), as well as the HBI index (OR % CI P = 0.006; area under ROC curve 0.70, HL test P = 0.14). As shown in Figure 1, linear regression analysis showed a significant P-value in evaluating both the correlation between the POSSUM and the HBI score (P = 0.001) and between POSSUM score and LOS (P = 0.001). Because of the exiguity of the anastomotic complications, a linear regression analysis was not possible and comparison with the POSSUM score was unable to be carried out. Discussion Appropriate surgical treatment plays a key role in the management of patients with CD since it can alleviate symptoms, address serious

6 POSSUM risk-prediction in Crohn s disease 83 complications, improve quality of life and, in some settings, be lifesaving. Nowadays, evaluation of surgical complications should be mandatory for assessing the quality of care provided, above all, for particular subsets of patients. The efficacy of every surgical performance should no longer be measured regardless of the so-called case mix, which takes into account the specific physiopathological conditions and the complexity of the procedures performed. For this purpose, several risk prediction scoring systems have been developed and internationally validated Among these, POSSUM is utilized worldwide and it has been demonstrated to be an accurate model for predicting post-operative outcomes in colorectal surgery. 20 It has also been validated in specific subgroups of surgical procedures (pancreatic and hepato-biliary resections, vascular surgery 21,22 ) and in particular groups of patients, such as the elderly. 23 Although 30-day mortality is usually utilized as a measure of surgical outcomes, it might be inaccurate in specific subsets of patients where expected mortality is extremely low, such as in young patients undergoing abdominal surgery. On the other hand, despite the young age, patients with CD are frequently affected by co-morbidities leading to worse surgical outcomes. The postoperative morbidity rate (above all, anastomotic leaks and septic complications) and LOS could be accurate surrogate outcomes for evaluating surgical effectiveness in patients with abdominal CD. 24 The POSSUM and the P-POSSUM score are probably the best risk-predicting scoring system in evaluating clinical outcomes since they give an accurate prediction of both 30-day mortality and morbidity. 3 5 Colorectal-POSSUM (CR-POSSUM) and the Association of Colon-Proctology of Great Britain and Ireland (ACPGBI) scoring system are other well-established risk-predicting scoring systems for colorectal surgery. Despite their increased viability and ease compared to the POSSUM, the CR-POSSUM is not able to predict 30-day complication rate while the ACPGBI scoring system is limited to colorectal cancer patients. Since surgery for CD is affected by low postoperative mortality but elevated morbidity, the CR-POSSUM scoring system was estimated unsuitable for our purpose. No risk-predicting IBD-specific model has currently been designed and there is only one peer-reviewed experience with the POSSUM score in the scientific literature for this population that included patients affected by both Ulcerative Colitis and CD. 28 Crohn s disease is extremely heterogeneous in terms of clinical presentation, medications used, surgical procedures and observed complications. The aim of our study was to identify, despite this tremendous variability, a correlation between POSSUM expectations and observed results. Our data show that the POSSUM risk prediction scoring system is an accurate tool in estimating surgical outcomes because its prediction is comparable to the observed complication rate (as demonstrated by the O/E ratio, the C-statistic and the HL test). The HBI is an easy-to-use instrument for evaluating CD clinical activity and it correctly portrays the clinical condition of the patients. 29 The HBI and the POSSUM score are composed of completely different subsets of items. Linear regression analysis clearly showed a close relationship between the POSSUM and the HBI scores, reinforcing the hypothesis that the POSSUM could be appropriately utilized for this specific subgroup of patients. Not very surprisingly, in the linear regression analysis, the POSSUM score was also correlated with LOS. Patients with severe physiological and/or operative conditions usually have longer in-hospital stay for extended treatment. Potential limitations are the observational design of the study in a single-institution setting and the elevated number of patients undergoing steroidal therapy compared to the low rate of biologic treatments. Additional limitation was given by the absence of deaths and the consequent inability to perform an effective logistic regression analysis to evaluate the P-POSSUM score ability to predict mortality in this subset of patients. Similarly, the small number (three) of anastomotic leaks did not allow us to carry out a statistical comparison with the POSSUM score. No consistent discrepancies in the POSSUM score were observed between patients with anastomotic leakage and patients with no complications, as was shown by Egberts et al. in their series. 29 In conclusion, although the majority of patients with IBD are young, they are often seriously ill when surgery is required. Careful evaluation and monitoring of post-operative complications are crucial in order to improve the standard of care in this frail population. The POSSUM score is a useful tool in predicting the outcome of a surgical procedure in patients with abdominal CD by accurately estimating post-operative morbidity. 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