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Association of Serum Creatinine Level with Prognosis of Laparotomy for Acute Mesenteric Ischemia after Cardiovascular Surgery

Association of Serum Creatinine Level with Prognosis of Laparotomy for Acute Mesenteric Ischemia... Hindawi Surgery Research and Practice Volume 2022, Article ID 1737161, 7 pages https://doi.org/10.1155/2022/1737161 Research Article Association of Serum Creatinine Level with Prognosis of Laparotomy for Acute Mesenteric Ischemia after Cardiovascular Surgery Yusuke Miyagawa, Yuta Yamamoto , Masato Kitazawa , Shigeo Tokumaru, Satoshi Nakamura, Makoto Koyama, Takehito Ehara, Nao Hondo, Yasuhiro Iijima, and Yuji Soejima Division of Gastroenterological, Hepato-Biliary-Pancreatic, Transplantation and Pediatric Surgery, Department of Surgery, Shinshu University School of Medicine, 3-1-1 Asahi, Matsumoto, Nagano 390-8621, Japan Correspondence should be addressed to Yuta Yamamoto; yyamamoto@shinshu-u.ac.jp Received 21 October 2021; Accepted 14 March 2022; Published 28 March 2022 Academic Editor: Christophoros Foroulis Copyright © 2022 Yusuke Miyagawa et al. )is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Introduction. Acute mesenteric ischemia is a life-threatening complication after cardiovascular surgery with a mortality rate of 52.9–81.3%. However, few studies have evaluated the predictors of clinical outcome after treatment for acute mesenteric ischemia following cardiovascular surgery. )erefore, this study aimed to elucidate prognostic factors in patients who underwent lap- arotomy for acute mesenteric ischemia after cardiovascular surgery. Methods. We retrospectively analyzed 29 patients (20 men and 9 women; median age, 71.0 years) who underwent laparotomy for acute mesenteric ischemia after cardiovascular surgery between January 2010 and August 2020. )ese patients were classified into the survivor group (comprising patients who were discharged or referred to another hospital, n � 16) and the nonsurvivor group (comprising those who experienced in-hospital mortality, n � 13). We compared clinical parameters between the groups to identify the predictors of outcomes. Results. More patients in the nonsurvivor group underwent emergency cardiovascular surgery (62.5% vs. 100%, p � 0.017) and received he- modialysis (12.5% vs. 61.5%, p � 0.008) at the onset of acute mesenteric ischemia than those in the survivor group. )e pre- laparotomy serum creatinine level was higher in the nonsurvivor group than in the survivor group (1.27 vs. 2.33 mg/dL, p � 0.004). Logistic regression analysis revealed an association between preoperative serum creatinine level and in-hospital mortality (odds ratio 5.047, p � 0.046), and Cox regression analysis demonstrated a relationship between serum creatinine level and in-hospital mortality (hazard ratio 1.610, p � 0.009). )e area under the curve (receiver operating characteristic analysis) for the serum creatinine level was 0.813. Furthermore, the optimal cutoff value of the serum creatinine level was 1.59 mg/dL with a sensitivity and specificity of 0.846 and 0.687, respectively, in predicting in-hospital mortality. Conclusions. )e elevated serum creatinine level was associated with a poor clinical outcome after surgery for acute mesenteric ischemia following cardiovascular surgery. was reportedly 1–3% after cardiovascular surgery (CS) [5–8]. 1. Introduction Several factors, such as advanced age, hypertension, heart Acute mesenteric ischemia (AMI) is characterized by sudden failure, prolonged ventilation, use of norepinephrine, and acute arterial or venous occlusion or a fall in circulating elevated serum levels of procalcitonin, myoglobin, lactate, pressure, resulting in insufficient blood flow within the and aspartate aminotransferase (AST), are reported to be mesenteric circulation [1]. )e mortality rate remains ap- risk factors for AMI after CS [9–11]. proximately 50%, despite improvements in multimodal Renal failure [12] and a high Portsmouth physiological treatment approaches, including endovascular techniques, and operative severity score for the enumeration of mortality over the past decade [2–4]. )e estimated incidence of AMI and morbidity (P-POSSUM) [13] indicate an elevated risk of 2 Surgery Research and Practice mortality in AMI. In 1991, the POSSUM scoring system was Demographic data are presented as descriptive statistics. established to predict postoperative complications and Comparisons between qualitative variables were con- mortality using preoperative physiological scores and ducted using the chi-square test and Fisher’s exact test. intraoperative surgical scores [14]. Furthermore, the mor- Nonparametric data are presented as medians with tality risk formula was modified to establish a P-POSSUM interquartile ranges. )e Mann–Whitney test was used to score that can predict a mortality rate more accurately [15]. compare nonparametric data. Multiple logistic regression )e mortality rate in cases of AMI after CS was reportedly analysis was conducted to identify patient factors asso- 52.9–81.3% [7, 9]. However, a few studies have evaluated ciated with in-hospital mortality using variables with a p predictors of clinical outcomes of patients after surgery for value of <0.1 in univariate analysis. )e multiple logistic AMI following CS. Patients who underwent CS had various regression analysis results are described as odds ratios with primary diseases, such as hypertension, heart failure, and 95% confidence intervals (CIs). Additionally, Cox pro- diabetes mellitus. )erefore, we hypothesized that there are portional hazards regression analysis was performed to several predictive indicators of prognosis. )e present study evaluate the effect of several factors on survival after aimed to assess prognostic factors in patients who under- laparotomy for AMI following CS, using variables with a p went surgery for AMI after CS. value of <0.1 in the univariate analysis. )e Cox pro- portional hazards regression analysis results are described as hazard ratios (HRs) with 95% CIs. A ROC curve was 2. Materials and Methods generated to investigate the discriminatory power of the equations in the analysis of mortality outcomes. )e op- 2.1. Study Design. )is retrospective cohort study included timal cutoff value was considered the point closest to 29 patients who underwent laparotomy for AMI after CS at perfect differentiation (0, 1). After laparotomy for AMI our hospital between January 2010 and August 2020. AMI following CS, survival rates were evaluated using the was diagnosed based on clinical symptoms such as ab- Kaplan–Meier product-limit method. All tests were two- dominal pain, ileus, and distension; laboratory test results tailed. Differences with a p value of <0.05 were considered indicating bowel necrosis; and triple-phase contrast-en- statistically significant. hanced computed tomography (CT) demonstrating bowel ischemia. If contrast-enhanced CT was not performed, AMI was confirmed during surgery. )ose who developed AMI 3. Results during index CS were excluded. Regarding laparotomy for During the study period, 2406 patients underwent elective or AMI, the primary surgery involved the resection of the is- emergency CS. Among them, 29 patients (1.21%) underwent chemic intestine and ostomy using the remaining oral in- laparotomy for AMI after CS. )e baseline characteristics of testine. When the progression of necrosis or ischemia of the these patients are summarized in Table 1. )e study cohort residual intestine was strongly suspected, a second surgery consisted of 20 male and 9 female patients with a median age was performed. of 71.0 years. )e ratio of survivors to nonsurvivors was 16 : Patients were classified into two groups as follows: the 13, and the in-hospital mortality rate was 44.8%. Regarding survivor group (n � 16), which comprised patients who were the details of the index CS, six patients (20.7%) underwent discharged or referred to another hospital, and the non- thoracic endovascular aneurysm repair, while five patients survivor group (n � 13), which comprised patients who (17.2%) underwent abdominal endovascular aneurysm re- experienced in-hospital mortality. We compared and ex- pair. Total arch replacement was performed for four patients amined clinical parameters between the two groups. Next, (13.8%), while Y-graft replacement was performed for five we conducted multiple logistic regression analysis and Cox patients (17.2%). Only one patient (3.5%) underwent cardiac proportional hazards regression analysis to determine surgery, which was coronary artery bypass grafting. prognostic indicators in patients who underwent laparot- More patients in the nonsurvivor group underwent omy for AMI after CS. Finally, receiver operating charac- emergency CS (62.5% vs. 100%, p � 0.017) and received teristics (ROC) curves were generated to compare the hemodialysis (12.5% vs. 61.5%, p � 0.008) at the AMI onset prognostic indicators. than those in the survivor group. Serum creatinine and AST )e P-POSSUM risk assessment method was used to levels prior to laparotomy for AMI were higher in the calculate the rate of mortality after surgery for AMI fol- nonsurvivor group than in the survivor group (33.5 vs. lowing CS. )e P-POSSUM scoring system comprises 12 74.0 IU/L, p � 0.045, and 1.27 vs. 2.33 mg/dL, p � 0.004, physiology scores and 6 operative scores, and the formula for respectively). No difference was observed in the proportion calculating the P-POSSUM-predicted mortality rate (R) of patients with nonocclusive mesenteric ischemia (NOMI) [14, 15] is as follows: (37.5% vs 46.2%, p � 0.638), as well as in P-POSSUM-pre- ln R dicted mortality rates (53.1% vs 97.7%, p � 0.092), between (1) � −9.065 + 0.1692 × PS + 0.1550 × OS. 1 − R the two groups (Table 2). )e results of logistic regression analysis revealed that the serum creatinine level prior to laparotomy for AMI was 2.2. Statistical Analysis. Statistical analysis was performed significantly associated with in-hospital mortality after lap- using the IBM software Statistical Package for the Social arotomy (odds ratio 5.047, 95% CI 1.027–24.798, p � 0.046) Sciences, version 23.0 (IBM Corp., Armonk, NY, USA). (Table 3). Surgery Research and Practice 3 Table 1: Patient characteristics. Variables Total (n � 29) Sex Male (%) 20 (69.0) Female (%) 9 (31.0) Age, years 71.0 (62.0–79.0) Type of acute mesenteric ischemia Occlusive mesenteric ischemia, n (%) 17 (58.6) Nonocclusive mesenteric ischemia, n (%) 12 (41.4) Detailed procedure of index cardiovascular surgery CABG, n (%) 1 (3.5) Total arch replacement, n (%) 4 (13.8) Ascending aorta replacement, n (%) 1 (3.5) Descending aorta replacement, n (%) 2 (6.9) Y-graft replacement, n (%) 5 (17.2) )oracic endovascular aortic repair, n (%) 6 (20.7) Endovascular aortic repair, n (%) 5 (17.2) Treatment of peripheral artery, n (%) 5 (17.2) Duration between cardiovascular surgery and acute mesenteric ischemia, days 1.5 (0–41.3) P-POSSUM-predicted mortality rate (%) 82.0 (33.0–98.3) Outcome after laparotomy Hospital discharge, n (%) 12 (41.4) Hospital transfer, n (%) 4 (13.8) In-hospital mortality, n (%) 13 (44.8) Median (interquartile range). CABG, coronary artery bypass grafting; P-POSSUM, Portsmouth physiological and operative severity score for the enu- meration of mortality and morbidity. Table 2: Comparison of the demographics of patients between the survivor and nonsurvivor groups. Demographic characteristics Survivor (n � 16) Nonsurvivor (n � 13) p value Age, years 78.0 (72.8–83.8) 77.0 (76.0–84.5) 0.779 Sex Male, n (%) 10 (62.5) 10 (76.9) 0.336 Female, n (%) 6 (37.5) 3 (23.1) Type of AMI Occlusive mesenteric ischemia, n (%) 10 (62.5) 7 (53.8) 0.638 Nonocclusive mesenteric ischemia, n (%) 6 (37.5) 6 (46.2) Duration between CS and AMI, days 1.5 (0.0–47.25) 1.5 (1.0–37.00) 0.619 Operative type Cardiac surgery, n (%) 1 (6.3) 0 (0) 0.552 )oracic aortic, n (%) 6 (37.5) 6 (46.2) 0.638 Abdominal aortic, n (%) 6 (37.5) 5 (38.5) 0.628 Peripheral artery, n (%) 3 (18.8) 2 (15.4) 0.604 Emergency CS Yes, n (%) 10 (62.5) 13 (100.0) 0.017 No, n (%) 6 (37.5) 0 (0) Comorbidities at the index CS Hypertension, n (%) 12 (75.0) 7 (53.8) 0.212 Diabetes mellitus, n (%) 4 (25.0) 2 (15.4) 0.435 Heart failure, n (%) 4 (25.0) 3 (23.1) 0.626 Peripheral artery disease, n (%) 3 (18.8) 1 (7.7) 0.383 Renal insufficiency, n (%) 2 (12.5) 3 (23.1) 0.396 Hemodialysis at the onset of AMI Yes, n (%) 2 (12.5) 8 (61.5) 0.008 No, n (%) 14 (87.5) 5 (38.5) Ventilator at the onset of AMI Yes, n (%) 5 (31.3) 5 (38.5) 0.493 No, n (%) 13 (68.7) 8 (61.5) Laboratory data prior to laparotomy for AMI White blood cell count,/μL 11085 (7908–14113) 10935 (6093–14898) 0.846 Lactate, mmol/L 15.0 (10.5–63.0) 11.8 (9.6–84.8) 0.371 4 Surgery Research and Practice Table 2: Continued. Demographic characteristics Survivor (n � 16) Nonsurvivor (n � 13) p value Creatinine, mg/dL 1.27 (0.91–1.94) 2.23 (1.65–3.09) 0.004 AST, IU/L 33.5 (20.5–85.3) 74.0 (41.0–273.3) 0.045 C-reactive protein, mg/dL 8.07 (0.98–16.26) 9.47 (3.07–16.68) 0.619 CT findings at the AMI onset Ascites, n (%) 9 (56.3) 8 (61.5) 0.774 Free air, n (%) 2 (12.5) 2 (15.4) 0.617 Intestinal pneumatosis, n (%) 5 (31.3) 2 (15.4) 0.292 Hepatic portal vein gas, n (%) 1 (6.3) 1 (7.7) 0.704 P-POSSUM-predicted mortality rate 53.1 (21.5–92.7) 97.7 (43.8–99.3) 0.092 Extent of bowel resection in laparotomy Small intestine, n (%) 7 (43.8) 9 (69.2) 0.170 Colorectum, n (%) 12 (75.0) 6 (46.2) 0.114 Median (interquartile range). AMI, acute mesenteric ischemia; AST, aspartate aminotransferase; CS, cardiovascular surgery; CT, computed tomography; P- POSSUM, Portsmouth physiological and operative severity score for the enumeration of mortality and morbidity. Table 3: Multiple logistic regression analysis of in-hospital mortality. Univariate analysis Multivariate analysis Variables Odds ratio 95% CI p value Odds ratio 95% CI p value Sex (male) 2.000 0.388–10.309 0.407 Age 1.027 0.950–1.111 0.496 Duration between CS and AMI 0.998 0.995–1.002 0.392 Nonocclusive mesenteric ischemia 1.429 0.323–6.324 0.638 ∗ 9 Emergency cardiovascular surgery 2.1 10 — 0.999 P-POSSUM-predicted mortality rate 1.015 0.993–1.038 0.184 Hypertension 0.389 0.081–1.872 0.239 Diabetes mellitus 0.545 0.083–3.590 0.528 Heart failure 0.900 0.162–5.007 0.904 ASO 0.361 0.033–3.962 0.405 Renal failure 2.100 0.294–14.978 0.459 Hemodialysis 11.200 1.751–71.637 0.011 6.353 0.745–54.195 0.091 Ventilator 1.375 0.295–6.402 0.685 White blood cell count 1.000 1.000–1.000 0.669 Lactate level 1.009 0.990–1.027 0.363 Creatinine level 5.795 1.307–25.700 0.021 5.047 1.027–24.798 0.046 AST level 1.000 0.997–1.002 0.885 CRP level 1.014 0.932–1.103 0.752 Cardiac surgery 0.000 - 1.000 Aortic surgery 1.833 0.279–12.066 0.528 Peripheral artery 0.778 0.111–5.600 0.812 Ascites 1.244 0.280–5.529 0.774 Free air 1.273 0.154–10.530 0.823 Intestinal emphysema 0.400 0.063–2.520 0.329 Hepatic portal vein gas 1.250 0.071–22.132 0.879 Resection of small intestine 2.893 0.622–13.455 0.176 Resection of the colorectum 0.286 0.059–1.375 0.118 AMI, acute mesenteric ischemia; ASO, arteriosclerosis obliterans; AST, aspartate aminotransferase; CRP, C-reactive protein; CS, cardiovascular surgery; CT, computed tomography; P-POSSUM, Portsmouth physiological and operative severity score for the enumeration of mortality and morbidity. 0.483–0.892, p � 0.087) for in-hospital mortality. )e opti- Cox regression analysis demonstrated that serum cre- atinine level and P-POSSUM-predicted mortality rate were mal cutoff value of the serum creatinine level was 1.59 mg/dL associated with in-hospital mortality after laparotomy fol- with a sensitivity of 0.846 and a specificity of 0.687 to predict lowing CS (HR 1.610, 95% CI 1.124–2.308, p � 0.003 and HR in-hospital mortality (Figure 1). 1.045, 95% CI 1.004–1.089, v � 0.033, respectively) (Table 4). )e Kaplan–Meier estimator revealed that patients with ROC analysis for the serum creatinine level showed an a high creatinine level prior to laparotomy for AMI fol- area under the curve (AUC) of 0.813 (95% CI: 0.646–0.979, lowing CS (≥1.59 mg/dL, n � 15) had a shorter survival time p � 0.004), and ROC analysis for the P-POSSUM-predicted after surgery for AMI than those with a low creatinine level mortality rate demonstrated an AUC of 0.687 (95% CI: (<1.59 mg/dL, n � 14) (p � 0.007) (Figure 2). Surgery Research and Practice 5 Table 4: Cox proportional hazard regression analysis of mortality. Univariate analysis Multivariate analysis Variables Hazard ratio 95% CI p value Hazard ratio 95% CI p value Sex (male) 1.808 0.388–10.309 0.369 Age 1.021 0.966–1.080 0.456 Duration between CS and AMI 0.999 0.996–1.002 0.435 Nonocclusive mesenteric ischemia 1.292 0.432–3.858 0.647 Emergency cardiovascular surgery 35.530 0.207–6085.317 0.174 P-POSSUM-predicted mortality rate 1.016 0.997–1.034 0.094 1.045 1.004–1.089 0.033 Hypertension 0.535 0.179–1.603 0.264 Diabetes mellitus 0.824 0.182–3.738 0.802 Heart failure 0.796 0.218–2.904 0.730 ASO 0.508 0.066–3.915 0.516 Renal failure 1.642 0.448–6.019 0.454 Hemodialysis 4.442 1.402–14.066 0.011 2.368 0.626–8.960 0.204 Ventilator 0.762 0.387–3.653 1.189 White blood cell count 1.000 1.000–1.000 0.682 Lactate level 1.008 0.996–1.021 0.176 Creatinine level 1.538 1.158–2.042 0.003 1.610 1.124–2.308 0.009 AST level 1.000 0.998–1.001 0.820 CRP level 1.003 0.945–1.065 0.916 Cardiac surgery 0.046 0.000–7760.923 0.616 Aortic surgery 0.908 0.198–4.173 0.901 Peripheral artery 1.673 0.358–7.819 0.513 Ascites 1.214 0.397–3.714 0.734 Free air 1.661 0.362–7.628 0.514 Intestinal emphysema 0.506 0.112–2.291 0.377 Hepatic portal vein gas 0.902 0.116–7.021 0.921 Resection of the small intestine 2.348 0.720–7.658 0.157 Resection of the colorectum 0.466 0.156–1.392 0.172 AMI, acute mesenteric ischemia; ASO, arteriosclerosis obliterans; AST, aspartate aminotransferase; CRP, C-reactive protein; CS, cardiovascular surgery; CT, computed tomography; P-POSSUM, Portsmouth physiological and operative severity score for the enumeration of mortality and morbidity. 1.0 0.8 0.6 0.4 0.2 0.0 0.0 0.2 0.4 0.6 0.8 1.0 1 – specificity Serum creatinine level P-POSSUM-predicted mortality rate Random prediction Figure 1: Receiver operating characteristic curves for the serum creatinine level (bold solid line) and the P-POSSUM-predicted mortality rate (bold dotted line). )e area under the curve (AUC) of the serum creatinine level for in-hospital mortality is 0.813 (95% confidence interval [CI]: 0.646–0.979, p � 0.004) and that of P-POSSUM is 0.687 (95% CI: 0.483–0.892, p � 0.087). )e optimal cutoff value of the serum creatinine level was 1.59 mg/dL with a sensitivity of 0.846 and a specificity of 0.687 to predict in-hospital mortality. Sensitivity 6 Surgery Research and Practice 1.0 0.8 p = 0.007 0.6 0.4 0.2 0.0 0 100 200 300 400 500 Days after Laparotomy for AMI Low Creatinine Level Low Creatinine Level - Censored High Creatinine Level High Creatinine Level - Censored Figure 2: Survival probabilities in patients with a high creatinine level (≥1.59 mg/dL,n � 15) (solid line) and those with a low creatinine level (<1.59 mg/dL, n � 14) (dotted line) after laparotomy for acute mesenteric ischemia following cardiovascular surgery. )e plus and cross marks represent censoring in patients with high and low creatinine levels, respectively. AMI has two different etiological forms as follows: oc- 4. Discussion clusive mesenteric ischemia (OMI), including arterial )is study demonstrated that a higher serum creatinine level embolism, arterial thrombosis, and venous thrombosis, and was associated with poor clinical outcomes in patients who NOMI [1]. NOMI is a disorder that causes ischemia and underwent laparotomy for AMI after CS. )e serum cre- necrosis of the intestinal tract without organic obstruction in atinine level was superior to the P-POSSUM-predicted mesenteric blood vessels [23]; it is responsible for approx- mortality rate in predicting in-hospital mortality. Our results imately 20% of the AMI cases [1]. )e incidence of NOMI appear clinically relevant because they indicate that, in a after CS is reportedly 0.6–9.0% [24–26], and the mortality heterogeneous group of patients with AMI after CS with rate accounts for 22.0–57.5% of all deaths [11, 25]. In the complex clinical courses, mortality can be predicted by present study, the type of AMI (OMI or NOMI) did not assessing the serum creatinine levels prior to laparotomy for affect the outcome of the study cohort. Although NOMI AMI. usually occurs in critically ill patients, it does not have a Renal failure is reportedly associated with a high risk of worse prognosis than OMI after CS. AMI-related death postoperatively [12]. Furthermore, the )e present study had some limitations. First, this was a serum level of fibroblast growth factor 23 (FGF-23) corre- single-center retrospective study with a small cohort, and lates with the occurrence and severity of NOMI after CS [16]. this may have caused statistical errors. Second, only patients )e serum level of FGF-23 is increased due to hyper- who underwent abdominal surgery for AMI were evaluated. phosphatemia in patients with renal failure and is associated )us, the patient selection may have been biased. )ird, the with a high risk of mortality in patients with chronic kidney reason why the predictive value of the serum creatinine level disease [17–20]. )ese findings suggest that an elevated for in-hospital mortality was superior to that of P-POSSUM serum creatinine level can be a reliable marker of the in this cohort remains unclear. )erefore, further multi- harmful effect of renal failure on the clinical outcome of AMI center studies comprising a larger number of patients are after CS. needed to confirm the prognostic indicators of AMI after CS. POSSUM and P-POSSUM were designed to predict perioperative risk of general surgery [14, 15], and these 5. Conclusions scores are among the most common risk prediction models [21, 22]. As previously mentioned, the P-POSSUM scoring )e present study demonstrated that a higher serum cre- system has been reported to be useful for predicting the atinine level prior to laparotomy for AMI after CS was clinical outcome of patients with AMI [13]. Consistent with associated with a poor clinical outcome. Furthermore, the this result, in the present study, the P-POSSUM-predicted serum creatinine level plays an important role in the pre- mortality rate was associated with mortality after laparot- diction of in-hospital mortality after laparotomy for AMI omy for AMI in Cox regression analysis. following CS. Survival Probability Surgery Research and Practice 7 may indicate improved outcomes,” International Journal of Data Availability Colorectal Disease, vol. 34, no. 10, pp. 1781–1790, 2019. [13] H.-P. Hsu, Y.-S. Shan, Y.-H. Hsieh, E. D. Sy, and P.-W. 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Schmid, “Diagnosis and treatment of nonocclusive mes- trial,” Journal of Gastroenterology, vol. 55, no. 9, pp. 858–867, enteric ischemia after open heart surgery,” 0e Annals of 0oracic Surgery, vol. 72, no. 5, pp. 1583–1586, 2001. [11] J. Y. Lim, J. B. Kim, S. H. Jung, S. J. Choo, C. H. Chung, and J. W. Lee, “Risk factor analysis for nonocclusive mesenteric ischemia following cardiac surgery,” Medicine, vol. 96, no. 37, Article ID e8029, 2017. [12] H. Matthaei, A. Klein, V. Branchi, J. C. Kalff, and A. Koscielny, “Acute mesenteric ischemia (AMI): absence of renal insufficiency and performance of early bowel resection http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Surgery Research and Practice Hindawi Publishing Corporation

Association of Serum Creatinine Level with Prognosis of Laparotomy for Acute Mesenteric Ischemia after Cardiovascular Surgery

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Copyright © 2022 Yusuke Miyagawa et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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10.1155/2022/1737161
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Abstract

Hindawi Surgery Research and Practice Volume 2022, Article ID 1737161, 7 pages https://doi.org/10.1155/2022/1737161 Research Article Association of Serum Creatinine Level with Prognosis of Laparotomy for Acute Mesenteric Ischemia after Cardiovascular Surgery Yusuke Miyagawa, Yuta Yamamoto , Masato Kitazawa , Shigeo Tokumaru, Satoshi Nakamura, Makoto Koyama, Takehito Ehara, Nao Hondo, Yasuhiro Iijima, and Yuji Soejima Division of Gastroenterological, Hepato-Biliary-Pancreatic, Transplantation and Pediatric Surgery, Department of Surgery, Shinshu University School of Medicine, 3-1-1 Asahi, Matsumoto, Nagano 390-8621, Japan Correspondence should be addressed to Yuta Yamamoto; yyamamoto@shinshu-u.ac.jp Received 21 October 2021; Accepted 14 March 2022; Published 28 March 2022 Academic Editor: Christophoros Foroulis Copyright © 2022 Yusuke Miyagawa et al. )is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Introduction. Acute mesenteric ischemia is a life-threatening complication after cardiovascular surgery with a mortality rate of 52.9–81.3%. However, few studies have evaluated the predictors of clinical outcome after treatment for acute mesenteric ischemia following cardiovascular surgery. )erefore, this study aimed to elucidate prognostic factors in patients who underwent lap- arotomy for acute mesenteric ischemia after cardiovascular surgery. Methods. We retrospectively analyzed 29 patients (20 men and 9 women; median age, 71.0 years) who underwent laparotomy for acute mesenteric ischemia after cardiovascular surgery between January 2010 and August 2020. )ese patients were classified into the survivor group (comprising patients who were discharged or referred to another hospital, n � 16) and the nonsurvivor group (comprising those who experienced in-hospital mortality, n � 13). We compared clinical parameters between the groups to identify the predictors of outcomes. Results. More patients in the nonsurvivor group underwent emergency cardiovascular surgery (62.5% vs. 100%, p � 0.017) and received he- modialysis (12.5% vs. 61.5%, p � 0.008) at the onset of acute mesenteric ischemia than those in the survivor group. )e pre- laparotomy serum creatinine level was higher in the nonsurvivor group than in the survivor group (1.27 vs. 2.33 mg/dL, p � 0.004). Logistic regression analysis revealed an association between preoperative serum creatinine level and in-hospital mortality (odds ratio 5.047, p � 0.046), and Cox regression analysis demonstrated a relationship between serum creatinine level and in-hospital mortality (hazard ratio 1.610, p � 0.009). )e area under the curve (receiver operating characteristic analysis) for the serum creatinine level was 0.813. Furthermore, the optimal cutoff value of the serum creatinine level was 1.59 mg/dL with a sensitivity and specificity of 0.846 and 0.687, respectively, in predicting in-hospital mortality. Conclusions. )e elevated serum creatinine level was associated with a poor clinical outcome after surgery for acute mesenteric ischemia following cardiovascular surgery. was reportedly 1–3% after cardiovascular surgery (CS) [5–8]. 1. Introduction Several factors, such as advanced age, hypertension, heart Acute mesenteric ischemia (AMI) is characterized by sudden failure, prolonged ventilation, use of norepinephrine, and acute arterial or venous occlusion or a fall in circulating elevated serum levels of procalcitonin, myoglobin, lactate, pressure, resulting in insufficient blood flow within the and aspartate aminotransferase (AST), are reported to be mesenteric circulation [1]. )e mortality rate remains ap- risk factors for AMI after CS [9–11]. proximately 50%, despite improvements in multimodal Renal failure [12] and a high Portsmouth physiological treatment approaches, including endovascular techniques, and operative severity score for the enumeration of mortality over the past decade [2–4]. )e estimated incidence of AMI and morbidity (P-POSSUM) [13] indicate an elevated risk of 2 Surgery Research and Practice mortality in AMI. In 1991, the POSSUM scoring system was Demographic data are presented as descriptive statistics. established to predict postoperative complications and Comparisons between qualitative variables were con- mortality using preoperative physiological scores and ducted using the chi-square test and Fisher’s exact test. intraoperative surgical scores [14]. Furthermore, the mor- Nonparametric data are presented as medians with tality risk formula was modified to establish a P-POSSUM interquartile ranges. )e Mann–Whitney test was used to score that can predict a mortality rate more accurately [15]. compare nonparametric data. Multiple logistic regression )e mortality rate in cases of AMI after CS was reportedly analysis was conducted to identify patient factors asso- 52.9–81.3% [7, 9]. However, a few studies have evaluated ciated with in-hospital mortality using variables with a p predictors of clinical outcomes of patients after surgery for value of <0.1 in univariate analysis. )e multiple logistic AMI following CS. Patients who underwent CS had various regression analysis results are described as odds ratios with primary diseases, such as hypertension, heart failure, and 95% confidence intervals (CIs). Additionally, Cox pro- diabetes mellitus. )erefore, we hypothesized that there are portional hazards regression analysis was performed to several predictive indicators of prognosis. )e present study evaluate the effect of several factors on survival after aimed to assess prognostic factors in patients who under- laparotomy for AMI following CS, using variables with a p went surgery for AMI after CS. value of <0.1 in the univariate analysis. )e Cox pro- portional hazards regression analysis results are described as hazard ratios (HRs) with 95% CIs. A ROC curve was 2. Materials and Methods generated to investigate the discriminatory power of the equations in the analysis of mortality outcomes. )e op- 2.1. Study Design. )is retrospective cohort study included timal cutoff value was considered the point closest to 29 patients who underwent laparotomy for AMI after CS at perfect differentiation (0, 1). After laparotomy for AMI our hospital between January 2010 and August 2020. AMI following CS, survival rates were evaluated using the was diagnosed based on clinical symptoms such as ab- Kaplan–Meier product-limit method. All tests were two- dominal pain, ileus, and distension; laboratory test results tailed. Differences with a p value of <0.05 were considered indicating bowel necrosis; and triple-phase contrast-en- statistically significant. hanced computed tomography (CT) demonstrating bowel ischemia. If contrast-enhanced CT was not performed, AMI was confirmed during surgery. )ose who developed AMI 3. Results during index CS were excluded. Regarding laparotomy for During the study period, 2406 patients underwent elective or AMI, the primary surgery involved the resection of the is- emergency CS. Among them, 29 patients (1.21%) underwent chemic intestine and ostomy using the remaining oral in- laparotomy for AMI after CS. )e baseline characteristics of testine. When the progression of necrosis or ischemia of the these patients are summarized in Table 1. )e study cohort residual intestine was strongly suspected, a second surgery consisted of 20 male and 9 female patients with a median age was performed. of 71.0 years. )e ratio of survivors to nonsurvivors was 16 : Patients were classified into two groups as follows: the 13, and the in-hospital mortality rate was 44.8%. Regarding survivor group (n � 16), which comprised patients who were the details of the index CS, six patients (20.7%) underwent discharged or referred to another hospital, and the non- thoracic endovascular aneurysm repair, while five patients survivor group (n � 13), which comprised patients who (17.2%) underwent abdominal endovascular aneurysm re- experienced in-hospital mortality. We compared and ex- pair. Total arch replacement was performed for four patients amined clinical parameters between the two groups. Next, (13.8%), while Y-graft replacement was performed for five we conducted multiple logistic regression analysis and Cox patients (17.2%). Only one patient (3.5%) underwent cardiac proportional hazards regression analysis to determine surgery, which was coronary artery bypass grafting. prognostic indicators in patients who underwent laparot- More patients in the nonsurvivor group underwent omy for AMI after CS. Finally, receiver operating charac- emergency CS (62.5% vs. 100%, p � 0.017) and received teristics (ROC) curves were generated to compare the hemodialysis (12.5% vs. 61.5%, p � 0.008) at the AMI onset prognostic indicators. than those in the survivor group. Serum creatinine and AST )e P-POSSUM risk assessment method was used to levels prior to laparotomy for AMI were higher in the calculate the rate of mortality after surgery for AMI fol- nonsurvivor group than in the survivor group (33.5 vs. lowing CS. )e P-POSSUM scoring system comprises 12 74.0 IU/L, p � 0.045, and 1.27 vs. 2.33 mg/dL, p � 0.004, physiology scores and 6 operative scores, and the formula for respectively). No difference was observed in the proportion calculating the P-POSSUM-predicted mortality rate (R) of patients with nonocclusive mesenteric ischemia (NOMI) [14, 15] is as follows: (37.5% vs 46.2%, p � 0.638), as well as in P-POSSUM-pre- ln R dicted mortality rates (53.1% vs 97.7%, p � 0.092), between (1) � −9.065 + 0.1692 × PS + 0.1550 × OS. 1 − R the two groups (Table 2). )e results of logistic regression analysis revealed that the serum creatinine level prior to laparotomy for AMI was 2.2. Statistical Analysis. Statistical analysis was performed significantly associated with in-hospital mortality after lap- using the IBM software Statistical Package for the Social arotomy (odds ratio 5.047, 95% CI 1.027–24.798, p � 0.046) Sciences, version 23.0 (IBM Corp., Armonk, NY, USA). (Table 3). Surgery Research and Practice 3 Table 1: Patient characteristics. Variables Total (n � 29) Sex Male (%) 20 (69.0) Female (%) 9 (31.0) Age, years 71.0 (62.0–79.0) Type of acute mesenteric ischemia Occlusive mesenteric ischemia, n (%) 17 (58.6) Nonocclusive mesenteric ischemia, n (%) 12 (41.4) Detailed procedure of index cardiovascular surgery CABG, n (%) 1 (3.5) Total arch replacement, n (%) 4 (13.8) Ascending aorta replacement, n (%) 1 (3.5) Descending aorta replacement, n (%) 2 (6.9) Y-graft replacement, n (%) 5 (17.2) )oracic endovascular aortic repair, n (%) 6 (20.7) Endovascular aortic repair, n (%) 5 (17.2) Treatment of peripheral artery, n (%) 5 (17.2) Duration between cardiovascular surgery and acute mesenteric ischemia, days 1.5 (0–41.3) P-POSSUM-predicted mortality rate (%) 82.0 (33.0–98.3) Outcome after laparotomy Hospital discharge, n (%) 12 (41.4) Hospital transfer, n (%) 4 (13.8) In-hospital mortality, n (%) 13 (44.8) Median (interquartile range). CABG, coronary artery bypass grafting; P-POSSUM, Portsmouth physiological and operative severity score for the enu- meration of mortality and morbidity. Table 2: Comparison of the demographics of patients between the survivor and nonsurvivor groups. Demographic characteristics Survivor (n � 16) Nonsurvivor (n � 13) p value Age, years 78.0 (72.8–83.8) 77.0 (76.0–84.5) 0.779 Sex Male, n (%) 10 (62.5) 10 (76.9) 0.336 Female, n (%) 6 (37.5) 3 (23.1) Type of AMI Occlusive mesenteric ischemia, n (%) 10 (62.5) 7 (53.8) 0.638 Nonocclusive mesenteric ischemia, n (%) 6 (37.5) 6 (46.2) Duration between CS and AMI, days 1.5 (0.0–47.25) 1.5 (1.0–37.00) 0.619 Operative type Cardiac surgery, n (%) 1 (6.3) 0 (0) 0.552 )oracic aortic, n (%) 6 (37.5) 6 (46.2) 0.638 Abdominal aortic, n (%) 6 (37.5) 5 (38.5) 0.628 Peripheral artery, n (%) 3 (18.8) 2 (15.4) 0.604 Emergency CS Yes, n (%) 10 (62.5) 13 (100.0) 0.017 No, n (%) 6 (37.5) 0 (0) Comorbidities at the index CS Hypertension, n (%) 12 (75.0) 7 (53.8) 0.212 Diabetes mellitus, n (%) 4 (25.0) 2 (15.4) 0.435 Heart failure, n (%) 4 (25.0) 3 (23.1) 0.626 Peripheral artery disease, n (%) 3 (18.8) 1 (7.7) 0.383 Renal insufficiency, n (%) 2 (12.5) 3 (23.1) 0.396 Hemodialysis at the onset of AMI Yes, n (%) 2 (12.5) 8 (61.5) 0.008 No, n (%) 14 (87.5) 5 (38.5) Ventilator at the onset of AMI Yes, n (%) 5 (31.3) 5 (38.5) 0.493 No, n (%) 13 (68.7) 8 (61.5) Laboratory data prior to laparotomy for AMI White blood cell count,/μL 11085 (7908–14113) 10935 (6093–14898) 0.846 Lactate, mmol/L 15.0 (10.5–63.0) 11.8 (9.6–84.8) 0.371 4 Surgery Research and Practice Table 2: Continued. Demographic characteristics Survivor (n � 16) Nonsurvivor (n � 13) p value Creatinine, mg/dL 1.27 (0.91–1.94) 2.23 (1.65–3.09) 0.004 AST, IU/L 33.5 (20.5–85.3) 74.0 (41.0–273.3) 0.045 C-reactive protein, mg/dL 8.07 (0.98–16.26) 9.47 (3.07–16.68) 0.619 CT findings at the AMI onset Ascites, n (%) 9 (56.3) 8 (61.5) 0.774 Free air, n (%) 2 (12.5) 2 (15.4) 0.617 Intestinal pneumatosis, n (%) 5 (31.3) 2 (15.4) 0.292 Hepatic portal vein gas, n (%) 1 (6.3) 1 (7.7) 0.704 P-POSSUM-predicted mortality rate 53.1 (21.5–92.7) 97.7 (43.8–99.3) 0.092 Extent of bowel resection in laparotomy Small intestine, n (%) 7 (43.8) 9 (69.2) 0.170 Colorectum, n (%) 12 (75.0) 6 (46.2) 0.114 Median (interquartile range). AMI, acute mesenteric ischemia; AST, aspartate aminotransferase; CS, cardiovascular surgery; CT, computed tomography; P- POSSUM, Portsmouth physiological and operative severity score for the enumeration of mortality and morbidity. Table 3: Multiple logistic regression analysis of in-hospital mortality. Univariate analysis Multivariate analysis Variables Odds ratio 95% CI p value Odds ratio 95% CI p value Sex (male) 2.000 0.388–10.309 0.407 Age 1.027 0.950–1.111 0.496 Duration between CS and AMI 0.998 0.995–1.002 0.392 Nonocclusive mesenteric ischemia 1.429 0.323–6.324 0.638 ∗ 9 Emergency cardiovascular surgery 2.1 10 — 0.999 P-POSSUM-predicted mortality rate 1.015 0.993–1.038 0.184 Hypertension 0.389 0.081–1.872 0.239 Diabetes mellitus 0.545 0.083–3.590 0.528 Heart failure 0.900 0.162–5.007 0.904 ASO 0.361 0.033–3.962 0.405 Renal failure 2.100 0.294–14.978 0.459 Hemodialysis 11.200 1.751–71.637 0.011 6.353 0.745–54.195 0.091 Ventilator 1.375 0.295–6.402 0.685 White blood cell count 1.000 1.000–1.000 0.669 Lactate level 1.009 0.990–1.027 0.363 Creatinine level 5.795 1.307–25.700 0.021 5.047 1.027–24.798 0.046 AST level 1.000 0.997–1.002 0.885 CRP level 1.014 0.932–1.103 0.752 Cardiac surgery 0.000 - 1.000 Aortic surgery 1.833 0.279–12.066 0.528 Peripheral artery 0.778 0.111–5.600 0.812 Ascites 1.244 0.280–5.529 0.774 Free air 1.273 0.154–10.530 0.823 Intestinal emphysema 0.400 0.063–2.520 0.329 Hepatic portal vein gas 1.250 0.071–22.132 0.879 Resection of small intestine 2.893 0.622–13.455 0.176 Resection of the colorectum 0.286 0.059–1.375 0.118 AMI, acute mesenteric ischemia; ASO, arteriosclerosis obliterans; AST, aspartate aminotransferase; CRP, C-reactive protein; CS, cardiovascular surgery; CT, computed tomography; P-POSSUM, Portsmouth physiological and operative severity score for the enumeration of mortality and morbidity. 0.483–0.892, p � 0.087) for in-hospital mortality. )e opti- Cox regression analysis demonstrated that serum cre- atinine level and P-POSSUM-predicted mortality rate were mal cutoff value of the serum creatinine level was 1.59 mg/dL associated with in-hospital mortality after laparotomy fol- with a sensitivity of 0.846 and a specificity of 0.687 to predict lowing CS (HR 1.610, 95% CI 1.124–2.308, p � 0.003 and HR in-hospital mortality (Figure 1). 1.045, 95% CI 1.004–1.089, v � 0.033, respectively) (Table 4). )e Kaplan–Meier estimator revealed that patients with ROC analysis for the serum creatinine level showed an a high creatinine level prior to laparotomy for AMI fol- area under the curve (AUC) of 0.813 (95% CI: 0.646–0.979, lowing CS (≥1.59 mg/dL, n � 15) had a shorter survival time p � 0.004), and ROC analysis for the P-POSSUM-predicted after surgery for AMI than those with a low creatinine level mortality rate demonstrated an AUC of 0.687 (95% CI: (<1.59 mg/dL, n � 14) (p � 0.007) (Figure 2). Surgery Research and Practice 5 Table 4: Cox proportional hazard regression analysis of mortality. Univariate analysis Multivariate analysis Variables Hazard ratio 95% CI p value Hazard ratio 95% CI p value Sex (male) 1.808 0.388–10.309 0.369 Age 1.021 0.966–1.080 0.456 Duration between CS and AMI 0.999 0.996–1.002 0.435 Nonocclusive mesenteric ischemia 1.292 0.432–3.858 0.647 Emergency cardiovascular surgery 35.530 0.207–6085.317 0.174 P-POSSUM-predicted mortality rate 1.016 0.997–1.034 0.094 1.045 1.004–1.089 0.033 Hypertension 0.535 0.179–1.603 0.264 Diabetes mellitus 0.824 0.182–3.738 0.802 Heart failure 0.796 0.218–2.904 0.730 ASO 0.508 0.066–3.915 0.516 Renal failure 1.642 0.448–6.019 0.454 Hemodialysis 4.442 1.402–14.066 0.011 2.368 0.626–8.960 0.204 Ventilator 0.762 0.387–3.653 1.189 White blood cell count 1.000 1.000–1.000 0.682 Lactate level 1.008 0.996–1.021 0.176 Creatinine level 1.538 1.158–2.042 0.003 1.610 1.124–2.308 0.009 AST level 1.000 0.998–1.001 0.820 CRP level 1.003 0.945–1.065 0.916 Cardiac surgery 0.046 0.000–7760.923 0.616 Aortic surgery 0.908 0.198–4.173 0.901 Peripheral artery 1.673 0.358–7.819 0.513 Ascites 1.214 0.397–3.714 0.734 Free air 1.661 0.362–7.628 0.514 Intestinal emphysema 0.506 0.112–2.291 0.377 Hepatic portal vein gas 0.902 0.116–7.021 0.921 Resection of the small intestine 2.348 0.720–7.658 0.157 Resection of the colorectum 0.466 0.156–1.392 0.172 AMI, acute mesenteric ischemia; ASO, arteriosclerosis obliterans; AST, aspartate aminotransferase; CRP, C-reactive protein; CS, cardiovascular surgery; CT, computed tomography; P-POSSUM, Portsmouth physiological and operative severity score for the enumeration of mortality and morbidity. 1.0 0.8 0.6 0.4 0.2 0.0 0.0 0.2 0.4 0.6 0.8 1.0 1 – specificity Serum creatinine level P-POSSUM-predicted mortality rate Random prediction Figure 1: Receiver operating characteristic curves for the serum creatinine level (bold solid line) and the P-POSSUM-predicted mortality rate (bold dotted line). )e area under the curve (AUC) of the serum creatinine level for in-hospital mortality is 0.813 (95% confidence interval [CI]: 0.646–0.979, p � 0.004) and that of P-POSSUM is 0.687 (95% CI: 0.483–0.892, p � 0.087). )e optimal cutoff value of the serum creatinine level was 1.59 mg/dL with a sensitivity of 0.846 and a specificity of 0.687 to predict in-hospital mortality. Sensitivity 6 Surgery Research and Practice 1.0 0.8 p = 0.007 0.6 0.4 0.2 0.0 0 100 200 300 400 500 Days after Laparotomy for AMI Low Creatinine Level Low Creatinine Level - Censored High Creatinine Level High Creatinine Level - Censored Figure 2: Survival probabilities in patients with a high creatinine level (≥1.59 mg/dL,n � 15) (solid line) and those with a low creatinine level (<1.59 mg/dL, n � 14) (dotted line) after laparotomy for acute mesenteric ischemia following cardiovascular surgery. )e plus and cross marks represent censoring in patients with high and low creatinine levels, respectively. AMI has two different etiological forms as follows: oc- 4. Discussion clusive mesenteric ischemia (OMI), including arterial )is study demonstrated that a higher serum creatinine level embolism, arterial thrombosis, and venous thrombosis, and was associated with poor clinical outcomes in patients who NOMI [1]. NOMI is a disorder that causes ischemia and underwent laparotomy for AMI after CS. )e serum cre- necrosis of the intestinal tract without organic obstruction in atinine level was superior to the P-POSSUM-predicted mesenteric blood vessels [23]; it is responsible for approx- mortality rate in predicting in-hospital mortality. Our results imately 20% of the AMI cases [1]. )e incidence of NOMI appear clinically relevant because they indicate that, in a after CS is reportedly 0.6–9.0% [24–26], and the mortality heterogeneous group of patients with AMI after CS with rate accounts for 22.0–57.5% of all deaths [11, 25]. In the complex clinical courses, mortality can be predicted by present study, the type of AMI (OMI or NOMI) did not assessing the serum creatinine levels prior to laparotomy for affect the outcome of the study cohort. Although NOMI AMI. usually occurs in critically ill patients, it does not have a Renal failure is reportedly associated with a high risk of worse prognosis than OMI after CS. AMI-related death postoperatively [12]. Furthermore, the )e present study had some limitations. First, this was a serum level of fibroblast growth factor 23 (FGF-23) corre- single-center retrospective study with a small cohort, and lates with the occurrence and severity of NOMI after CS [16]. this may have caused statistical errors. Second, only patients )e serum level of FGF-23 is increased due to hyper- who underwent abdominal surgery for AMI were evaluated. phosphatemia in patients with renal failure and is associated )us, the patient selection may have been biased. )ird, the with a high risk of mortality in patients with chronic kidney reason why the predictive value of the serum creatinine level disease [17–20]. )ese findings suggest that an elevated for in-hospital mortality was superior to that of P-POSSUM serum creatinine level can be a reliable marker of the in this cohort remains unclear. )erefore, further multi- harmful effect of renal failure on the clinical outcome of AMI center studies comprising a larger number of patients are after CS. needed to confirm the prognostic indicators of AMI after CS. POSSUM and P-POSSUM were designed to predict perioperative risk of general surgery [14, 15], and these 5. Conclusions scores are among the most common risk prediction models [21, 22]. As previously mentioned, the P-POSSUM scoring )e present study demonstrated that a higher serum cre- system has been reported to be useful for predicting the atinine level prior to laparotomy for AMI after CS was clinical outcome of patients with AMI [13]. Consistent with associated with a poor clinical outcome. Furthermore, the this result, in the present study, the P-POSSUM-predicted serum creatinine level plays an important role in the pre- mortality rate was associated with mortality after laparot- diction of in-hospital mortality after laparotomy for AMI omy for AMI in Cox regression analysis. following CS. Survival Probability Surgery Research and Practice 7 may indicate improved outcomes,” International Journal of Data Availability Colorectal Disease, vol. 34, no. 10, pp. 1781–1790, 2019. [13] H.-P. Hsu, Y.-S. Shan, Y.-H. Hsieh, E. D. Sy, and P.-W. Lin, )e data that support the findings of this study are available “Impact of etiologic factors and Apache II and POSSUM from the corresponding author upon reasonable request. scores in management and clinical outcome of acute intestinal ischemic disorders after surgical treatment,” World Journal of Conflicts of Interest Surgery, vol. 30, no. 12, pp. 2152–2162, 2006. [14] G. P. Copeland, D. Jones, and M. Walters, “POSSUM: a )e authors declare that there are no conflicts of interest scoring system for surgical audit,” British Journal of Surgery, regarding the publication of this paper. vol. 78, pp. 355–360, 1991. [15] M. S. Whiteley, D. R. Prytherch, B. Higgins, P. C. Weaver, and W. G. Prout, “An evaluation of the POSSUM surgical scoring Authors’ Contributions system,” British Journal of Surgery, vol. 83, pp. 812–815, 1996. [16] J. Stroeder, M. Klingele, H. 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Published: Mar 28, 2022

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