Abstract
Objective:
Acute mesenteric ischemia (AMI) is a surgical emergency for which delays in treatment have been closely associated with high morbidity and mortality. Although the duration of ischemia as a determinant of outcomes for AMI is well known, the objective of this study was to identify hospital-based determinants of delayed revascularization and their effects on postoperative morbidity and mortality in AMI.
Methods:
All patients who underwent any surgery for AMI from a multi-center hospital system between 2010 and 2020 were divided into two groups based on timeliness of mesenteric revascularization after presentation. Early revascularization (ER) was defined as having both vascular consultation ≤12 hours of presentation and vascular surgery performed at the patient’s initial operation. Delayed revascularization (DR) was defined as having either delays to vascular consultation or vascular surgery. A retrospective review of demographic and postoperative data was performed. The effect of DR on major postoperative outcomes, including 30-day and 2-year mortality, total length of bowel resection, and development of short bowel syndrome, were analyzed. Effects of delayed vascular consultation alone, delayed vascular surgery alone, no revascularization during admission, and admitting service on outcomes were also examined on subgroup analyses.
Results:
A total of 212 patients were analyzed. Ninety-nine patients received ER, whereas the remaining 113 patients experienced a DR after hospital presentation. Among the DR group, 55 patients (25.9%) had delayed vascular consultation, whereas vascular surgery was deferred until after the initial operation in 37 patients (17.4%). Fifty-one patients (24.0%) were never revascularized during admission. DR was a significant predictor of 30-day (odds ratio [OR], 2.09; 95% confidence interval [CI], 1.4-4.9; P = .03) and 2-year mortality (hazard ratio, 1.55, 95% CI, 1.0-2.3; P = .04). DR was also independently associated with increased bowel resection length (OR, 7.47; P < .01) and postoperative short bowel syndrome (OR, 2.4; P = .03) on multivariate analyses. When examined separately on subgroup analysis, both delayed vascular consultation (OR, 3.38; P = .03) and vascular surgery (OR, 4.31; P < .01) independently increased risk of 30-day mortality. Hospital discharge after AMI without mesenteric revascularization was associated with increased risk of short bowel syndrome (OR, 2.94; P < .01) and late mortality (hazard ratio, 1.60; P = .04).
Conclusions:
Delayed vascular consultation and vascular surgery are both significant hospital-based determinants of postoperative mortality and short bowel syndrome in patients with AMI. Timing-based management protocols that emphasize routine evaluation by a vascular surgeon and early, definitive mesenteric revascularization should be established and widely adopted for all patients with clinically suspected AMI at presentation.
Keywords: Acute mesenteric ischemia, Bowel resection, Consultation, Intestinal ischemia, Outcomes, Revascularization, Short bowel syndrome
Acute mesenteric ischemia (AMI) is a surgical condition of high acuity that is associated with high early mortality rates, reported between 25% and 70%, and poor long-term prognosis in survivors.1-3 Despite advances in radiographic techniques and many changes in the surgical management of these patients, such as incorporation of damage control surgery, and increased utilization of endovascular and retrograde open mesenteric stenting techniques, mortality in AMI over the past two decades has not significantly improved.4,5 Previous studies aimed at identifying hospital-based modifiable risk factors in AMI have demonstrated timing to surgery to be a significant predictor of outcomes.6 Delays in timing to surgery were shown to be associated with increased mortality in AMI, but it remains unclear whether this association is related to the timeliness of ischemic bowel resection, mesenteric revascularization, or both. Furthermore, although prompt revascularization has been well-described as a major component of AMI management, there is a paucity of outcomes data between patients diagnosed with AMI who experienced early vs late or no mesenteric reperfusion.7-9 The purpose of this study was to evaluate the effect of hospital-based timing delays to revascularization on mortality and postoperative complications in AMI.
METHODS
Patient selection.
Retrospective data from the University of Pittsburgh Medical Center multi-center hospital system, including major tertiary and quaternary referral centers, from January 1, 2010 to December 31, 2020 were reviewed. Patients undergoing surgery for suspected AMI were identified retrospectively using the previously reported methodology.10 Patients with bowel ischemia secondary to mechanical obstruction (ie. hernia, adhesion, volvulus), trauma, aortic occlusion, mesenteric aneurysm, abdominal aortic aneurysm repair, medial arcuate ligament syndrome, chronic mesenteric ischemia of any etiology, and mesenteric venous thrombosis were excluded from this study. To confirm vascular etiology of AMI, computed tomography (CT) images for all eligible patients were then reviewed (L.T., E.A.) for presence of occlusive or nonocclusive mesenteric vascular disease and confirmed by a senior vascular surgeon (R.C.). Patients who were found to have complete, irreversible bowel ischemia deemed incompatible with life during the initial operation by the operating surgeon were captured in our demographic results but excluded from subsequent analyses, due to assumed futility of operative intervention. This study was approved by the University of Pittsburgh Institutional Review Board (IRB 20050249). All patient information was de-identified, and patient consent was not required.
Study design.
Patients meeting appropriate inclusion and exclusion criteria were then divided based on both timing of vascular consultation and vascular surgery during admission as outlined in Supplementary Fig 1 (online only). Early vascular consultation was defined as having a documented evaluation by a vascular surgeon, time-stamped on completion, in the medical records within 12 hours of presentation. Consultation was considered delayed if vascular evaluation was not documented until after 12 hours after hospital presentation. No consultation was defined as the absence of a documented evaluation by a vascular surgeon during admission. With regard to timing of vascular surgery, all definitive mesenteric revascularization procedures performed at the patient’s initial operation were considered early and those deferred until the second or subsequent operation were considered delayed. No revascularization was defined as the absence of a documented revascularization procedure in the medical records during admission. We assigned all study patients to two main groups based on these parameters: early revascularization (ER) and delayed revascularization (DR). ER was defined as both early vascular consultation and early vascular surgery. All remaining patients who had either delayed consultation or delayed vascular surgery were assigned to the DR group. Study patients who had no mesenteric revascularization procedure performed during admission were analyzed in the DR group. We further examined four selected hospital-based factors—timing to vascular consultation, timing to vascular surgery, no revascularization, and admitting medical service—individually, by performing subgroup analyses designed to minimize the confounding effect these variables have on each other in the main analysis (Supplementary Table, online only). Overall trends in annual total operative cases and total deaths from AMI at our institution from 2010 through 2020 were also analyzed.
Data collection.
Demographics, medical comorbidities, clinical presentation, radiologic findings, operative data, and postoperative complications were obtained from the medical records. Etiologic classification of AMI was based on aggregated data involving interpretation of clinical presentation, evaluation of CT imaging, and operative findings. Arterial in situ thrombosis was differentiated from embolic disease on CT by underlying atherosclerotic mesenteric disease. Presenting symptoms, vital signs, and laboratory testing were recorded either at the time of initial evaluation in the Emergency Department or at time of CT image-guided diagnosis of AMI for prior hospitalized patients. All time values including time to initial operation were calculated using this initial time of presentation. Operative details including operative time, revascularization approach, length of bowel resection, and total number of operating room visits during admission were obtained from operative reports. Postoperative complications included bleeding, sepsis, cardiac, unanticipated return to operating room, acute kidney injury (AKI), respiratory failure, total parental nutrition (TPN) dependence, intensive care unit admission, and length of stay were assessed. AKI was defined as creatinine 1.5 mg/dL times higher than documented baseline levels. Sepsis was defined by heart rate >90 beats per minute and white blood cell count >12,000/mm3 in accordance with established criteria. Major cardiac complications included myocardial infarction, heart failure, and cardiac arrest.
Statistical analysis.
Primary outcomes of this study for main and subgroup analyses were 30-day and 2-year mortality. Secondary outcomes included total length of bowel resection and development of short bowel syndrome as defined by TPN dependence.
Continuous variables were evaluated with the Student t test or Wilcoxon rank-sum test depending on data distribution. Categorical variables were evaluated using the χ2 or Fischer exact test. Multivariable logistic regression models were used to identify independent factors associated with 30-day mortality, length of bowel resection, and TPN dependence. Two-year survival analysis was performed using Kaplan-Meier estimates, and differences were assessed using log-rank testing. Multivariate Cox proportional hazards model was used to identify independent predictors of all-cause 2-year mortality. All statistical tests were conducted using a level of significance of P < .05. Analyses were completed using STATA 16 (StataCorp LP, College Station, Tex).
RESULTS
Study population trends.
A total of 252 patients were included over the study period. Over time, the number of patients who underwent surgery for clinically suspected AMI per year at our institution increased, whereas annual overall mortality rates from AMI ranged from 15.0% to 60% from 2010 to 2020 without a clear statistical trend (Fig 1). Forty of these patients (15.9%) were taken emergently for initial exploratory laparotomy based on their critical clinical presentation and found to have complete, nonsurvivable bowel ischemia. Given the futility of revascularization in these patients, they were excluded from further analysis. Annual operative mortality rates for AMI undergoing any intervention were still high, ranging from 21.4% to 50%, with no significant trend over time.
Fig 1.
Annual operative cases and total deaths in acute mesenteric ischemia (AMI) from a multi-center hospital system between 2010 and 2020.
Clinical characteristics.
Of 212 patients with AMI analyzed, 99 patients (46.7%) were assigned to the ER group, whereas 113 (53.3%) patients were assigned to the DR group, based on timing of vascular consultation and vascular surgery. Fifty-five patients (25.9%) had delayed vascular consultation. Independent of consultation timing, vascular surgery was delayed beyond the initial operation in 37 patients (17.4%). Fifty-one patients (24.0%) were never revascularized during admission. Patients with ER were more likely to have a history of atrial fibrillation than patients with DR (40.4% vs 27.4%; P = .04), but there were otherwise no major significant differences in baseline demographics, comorbid medical conditions, or relevant medications between the ER and DR groups (Table I).
Table I.
Baseline demographics and clinical presentation of patients with AMI by timing of mesenteric revascularization
| All patients |
ER |
DR |
||
|---|---|---|---|---|
| N = 212 | n = 99 | n = 113 | P value | |
| Age, years | 69.1 ± 12.6 | 69.6 ± 12.6 | 68.6 ± 12.6 | .60 |
| Gender, female | 60 (128) | 58.6 (58) | 62.0 (70) | .62 |
| Race, white | 93.3 (182) | 94.4 (85) | 92.4 (97) | .57 |
| History of tobacco use | 68.5 (137) | 70.7 (65) | 66.7 (72) | .55 |
| BMI, kg/m2 | 28.1 ± 7.9 | 27.5 ± 7.8 | 28.7 ± 8.0 | .30 |
| Diabetes | 33.0 (70) | 26.3 (26) | 39.0 (44) | .05 |
| Hypercoagulable disease | 17.0 (36) | 20.2 (20) | 14.2 (16) | .24 |
| Hypertension | 78.3 (166) | 70.7 (70) | 85.0 (96) | .01 |
| CKD | 17.9 (38) | 13.1 (14) | 22.1 (25) | .09 |
| COPD | 26.4 (56) | 21.2 (21) | 31.0 (35) | .11 |
| Congestive heart failure | 16.5 (35) | 17.2 (17) | 16.0 (18) | .81 |
| Coronary artery disease | 41.5 (88) | 39.4 (39) | 43.4 (49) | .56 |
| Atrial fibrillation | 33.5 (71) | 40.4 (40) | 27.4 (31) | .04 |
| Peripheral vascular disease | 33.0 (70) | 30.3 (30) | 35.4 (40) | .43 |
| AAA | 9.0 (19) | 8.1 (8) | 9.7 (11) | .67 |
| Previous mesenteric intervention | 6.6 (14) | 7.1 (7) | 6.2 (7) | .77 |
| Preoperative antiplatelet use | .62 | |||
| ASA | 35.7 (75) | 32.6 (32) | 38.4 (43) | |
| Plavix | 2.9 (6) | 2.0 (2) | 3.3 (4) | |
| DAPT | 10.0 (21) | 12.2 (12) | 8.0 (9) | |
| Preoperative anticoagulation use | 24.9 (52) | 30.0 (29) | 20.5 (23) | .58 |
| Admitting service | <.01 | |||
| General surgery | 58.5 (124) | 45.5 (45) | 69.9 (79) | |
| Vascular surgery | 22.2 (47) | 36.4 (36) | 9.7 (11) | |
| Medicine/CCM | 19.3 (41) | 18.2 (18) | 20.4 (23) | |
| Outside transfer | 53.3 (113) | 57.6 (57) | 49.6 (56) | .24 |
| Hospital setting | .21 | |||
| Tertiary | 76.9 (163) | 80.8 (80) | 73.5 (83) | |
| Community | 23.1 (49) | 19.2 (19) | 26.6 (30) | |
| Etiology | ||||
| Embolism | 34.9 (74) | 49.5 (49) | 22.1 (25) | <.01 |
| In-situ thrombosis | 65.1 (116) | 50.5 (50) | 77.9 (88) | <.01 |
| Presenting symptoms | ||||
| Sepsis | 39.2 (83) | 35.4 (35) | 43.5 (48) | .29 |
| Pain out of proportion | 55.9 (118) | 57.6 (57) | 54.5 (61) | .65 |
| Peritonitis | 32.7 (69) | 33.3 (33) | 32.1 (36) | .85 |
| SBP, mmHg | 140 ± 35 | 146 ± 35 | 135 ± 35 | .03 |
| HR, beats/min | 95 ± 23 | 93 ± 24 | 96 ± 22 | .36 |
| WBC, 103/mm3 | 17.3 ± 9.1 | 17.0 ± 9.0 | 17.6 ± 9.1 | .62 |
| Creatinine, mg/dL | 1.2 ± 1.1 | 1.1 ± 0.9 | 1.2 ± 1.0 | .20 |
| Lactate, mmol/L | 3.2 ± 2.6 | 3.0 ± 2.4 | 3.3 ± 2.7 | .37 |
| Abdominal imaging type | .03 | |||
| None | 1.5 (3) | 1.0 (1) | 1.8 (2) | |
| Noncontrasted CT | 11.2 (23) | 5.2 (5) | 16.5 (18) | |
| CT with IV contrast | 56.3 (116) | 57.3 (56) | 55.0 (60) | |
| CTA | 30.6 (63) | 36.1 (35) | 25.7 (28) | |
| MRA | 0.5 (1) | 0 (0) | 1.0 (1) | |
| Portal venous gas or pneumatosis on imaging | 44.1 (90) | 26.0 (25) | 60.2 (65) | <.01 |
AAA, Abdominal aortic aneurysm; AMI, acute mesenteric ischemia; ASA, aspirin; BMI, body mass index; CCM, Critical Care Medicine; CKD, chronic kidney disease; COPD, chronic obstructive pulmonary disease; CT, computed tomography; CTA, computed tomography angiography; DAPT, dual antiplatelet therapy; DR, delayed revascularization; ER, early revascularization; HR, heart rate; IV, intravenous; MRA, magnetic resonance angiography; SBP, systolic blood pressure; WBC, white blood cell count.
Categorical variables are presented as percentage (number). Continuous variables are presented as mean ± standard deviation.
P values were calculated from the χ2 and Student t test.
Clinical presentation of patients with AMI stratified by timing of revascularization are presented in Table I. Over one-half of all patients with AMI (53.3%) were transferred from outside facilities, and the majority (76.9%) were managed at a tertiary care center, which did not differ significantly between the ER and DR groups. Fifty-six patients with AMI (26.4%) presented overnight between the hours of 10 p.m. and 5 a.m; however, time of presentation did not differ significantly between the ER and DR groups (30.3% vs 23.0%; P = .23). Patients with DR were more likely admitted to the General Surgery service (69.9% vs 45.5%; P < .01), whereas patients with ER were more likely admitted to the Vascular Surgery service (36.4% vs 9.7%; P < .01). The etiology of AMI significantly differed between the ER and DR groups. Patients with ER were significantly more likely to have embolic disease as the main etiology of AMI (49.5% vs 22.1%; P < .001), whereas patients who presented with AMI due to arterial in situ thrombosis tended to have DR (77.9% vs 50.5%; P < .01). Most patients presented acutely with any prior chronic symptoms, but 64 patients (30.2%) presented with acute or chronic disease, which did not significantly differ between the ER and DR groups. There were no major significant differences in presenting signs, symptoms, or laboratory testing between the ER and DR groups. Overall, venous phase contrast-enhanced CT was the most common imaging modality obtained for diagnosis of AMI. Non-contrasted CT imaging used as the primary diagnostic imaging modality was significantly associated with DR (16.5% vs 5.2%; P = .03), whereas CT angiography (CTA) was more likely to be obtained in patients who had ER (36.1% vs 25.7%; P = .03). Radiographic findings concerning for fullthickness bowel ischemia such as portal venous gas and pneumatosis was more likely to be found in patients with DR compared with those with ER (60.2% vs 26.1%; P < .01).
Operative details and perioperative complications.
All patients included in this study underwent at least one operative procedure for suspected AMI during their admission. Operative details and perioperative complications are summarized in Table II. Mean time from initial presentation to initial operation was high overall (13.0 ± 20.8 hours) but significantly higher with DR compared with ER (17.7 ± 28.4 vs 9.4 ± 10.9 hours; P < .01).The mean operative time was 161 ± 102 minutes, and this did not differ between the ER and DR groups. The majority of patients underwent more than one operation during admission, ranging from 2 to 9 total operating room visits. Indications for operating room visits after the initial operation included additional bowel resection, mesenteric revascularization, and definitive abdominal closure. Patients who had DR required more operating room visits than those who had ER (P = .02). Overall, 161 patients (76.0%) underwent vascular surgery for mesenteric revascularization during their admission, including both open and endovascular approaches. Open embolectomy (58.6% vs 14.2%; P < .001) and retrograde open mesenteric stenting (15.2% vs 8.0%; P < .001), were more likely to be performed in the ER group compared with the DR group. Almost all procedures (90.3%) performed in patients who had DR involved some bowel resection, whereas one-half (50.5%) of ER procedures did not require any bowel resection (P < .001). Postoperative sepsis (43.6% vs 27.6%; P = .02) and AKI (34.6% vs 21.4%; P = .04) were more likely to occur after DR than ER. Other perioperative complications including bleeding, re-thrombosis, major cardiac complications, unanticipated return to operating room, and dialysis requirement did not differ between these groups. Mean length of hospital stay was 21.3 ± 31.7 days and was not significantly different after DR compared with ER.
Table II.
Operative details and postoperative outcomes for patients with AMI by timing of mesenteric revascularization
| All patients |
ER |
DR |
||
|---|---|---|---|---|
| N = 212 | n = 99 | n = 13 | P value | |
| Time to initial operation, hours | 13.0 ± 20.8 | 9.36 ± 10.91 | 17.7 ± 28.4 | <.01 |
| Operative time, minutes | 161 ± 102 | 171.0 ± 76.2 | 169.3 ± 160.6 | .54 |
| Revascularization approach | <.01 | |||
| Embolectomy | 34.9 (74) | 58.6 (58) | 14.2 (16) | |
| Mesenteric bypass | 9.9 (21) | 11.1 (11) | 8.9 (10) | |
| ROMS | 11.3 (24) | 15.2 (15) | 8.0 (9) | |
| Endovascular | 28.3 (60) | 28.3 (28) | 28.3 (32) | |
| None | 24.0 (51) | 0 (0) | 100 (51) | |
| Bowel resection | 71.2 (151) | 49.5 (49) | 90.3 (102) | <.01 |
| Mean bowel resection length, cm | 81 ± 107 | 47 ± 81 | 111 ± 117 | <.01 |
| Total number of operating room visits | 2.3 ± 1.2 | 2.1 ± 1.3 | 2.5 ± 1.2 | .02 |
| Complications | ||||
| Bleeding | 11.1 (23) | 14.3 (14) | 8.2 (9) | .16 |
| Re-thrombosis | 3.4 (7) | 2.0 (2) | 4.6 (5) | .32 |
| Sepsis | 36.1 (75) | 27.6 (27) | 43.6 (48) | .02 |
| Major cardiac complications | 7.7 (16) | 9.2 (9) | 6.4 (7) | .45 |
| Unanticipated return to operating room | 30.8 (64) | 25.5 (25) | 35.5 (39) | .12 |
| AKI | 28.4 (59) | 21.4 (4) | 34.6 (38) | .04 |
| Dialysis requirement | 8.7 (18) | 5.1 (5) | 11.8 (13) | .09 |
| TPN-dependent | 23.0 (48) | 15.2 (15) | 30.0 (33) | .01 |
| Length of stay, days | 21.3 ± 31.7 | 19.0 ± 18.4 | 23.4 ± 40.0 | .32 |
| 30-day mortality | 33.5 (70) | 25.0 (24) | 39.6 (35) | .02 |
AKI, Acute kidney injury; AMI, acute mesenteric ischemia; DR, delayed revascularization; ER, early revascularization; ROMS, retrograde open mesenteric stenting; TPN, total parenteral nutrition.
Categorical variables are presented as percentage (number). Continuous variables are presented as mean ± standard deviation.
P values were calculated from the χ2 and Student t test.
Patient outcomes.
Thirty-day mortality in patients who had DR was significantly higher when compared with ER (39.6% vs 25.0%; P = .02; Table II). On multivariate analysis after adjusting for patient comorbidities and severity of illness at presentation, DR was found to be a significant independent predictor of early mortality (odds ratio [OR], 2.1; 95% confidence interval [CI], 1.1-4.1; P = .03). Other factors independently associated with early mortality included history of coronary artery disease (OR, 2.1; 95% CI, 1.1-4.0; P = .02), sepsis on presentation (OR, 2.02; 95% CI, 1.1-3.9; P = .03), lactate >2.5 mmol/L (OR, 3.26; 95% CI, 1.7-6.3; P < .01), and postoperative sepsis (OR, 2.62; 95% CI, 1.4-4.9; P ≤ .01), as seen in Table III. Mean follow-up time was 11.7 ± 16.8 months (median, 5.1 months; interquartile range, 1.5-15.6 months). DR was similarly a significant independent risk factor for all-cause mortality at 2 years (hazard ratio [HR], 1.55; 95% CI, 1.0-2.3; P = .04). One- and 2-year mortality in patients with DR were 58.7% and 62.9%, respectively, compared with 41.2% and 44.1% in patients with ER (P < .01; Fig 2). Other independent predictors of all-cause 2-year mortality on multivariate analysis were found to be largely consistent with risk factors of early mortality namely, sepsis on presentation (HR, 1.94; 95% CI, 1.3-3.0; P < .01), postoperative sepsis (HR, 1.81; 95% CI, 1.2-2.7; P < .01), and major cardiac complications (HR, 2.24; 95% CI, 1.2-4-2; P = .01), as listed in Table III.
Table III.
Multivariate logistic regression for 30-day mortality, bowel resection, and short bowel syndrome and Cox proportional hazards model for 2-year mortality in patients with AMI
| OR | 95% CI | P value | |
|---|---|---|---|
| 30-day mortality | |||
| DR | 2.09 | 1.07-4.06 | .03 |
| History of COPD | 1.99 | 0.98-4.04 | .06 |
| History of coronary artery disease | 2.12 | 1.12-4.00 | .02 |
| Sepsis on presentation | 2.02 | 1.06-3.85 | .03 |
| Presenting lactate >2.5 mmol/L | 3.26 | 1.69-6.29 | <.01 |
| Open revascularization | 0.89 | 0.76-1.04 | .13 |
| Postoperative sepsis | 2.62 | 1.39-4.93 | <.01 |
| Postoperative AKI | 1.31 | 0.67-2.59 | .43 |
| Major cardiac complication | 3.09 | 1.0-3.79 | .05 |
| Unanticipated RTOR | 1.95 | 1.0-3.79 | .05 |
| 2-year mortality | HR | 95% CI | P value |
| DR | 1.55 | 1.03-2.32 | .04 |
| Nontertiary hospital setting | 1.46 | 0.95-2.24 | .09 |
| History of diabetes mellitus | 1.18 | 0.79-1.76 | .42 |
| History of CKD | 1.29 | 0.77-2.16 | .33 |
| History of coronary artery disease | 1.94 | 1.27-2.94 | <.01 |
| Sepsis on presentation | 1.51 | 0.99-2.28 | .05 |
| Pain out of proportion on exam | 0.85 | 0.57-1.26 | .42 |
| Presenting WBC >15,000/uL | 1.24 | 0.96-2.08 | .30 |
| Presenting lactate >2.5 mmol/L | 1.41 | 0.96-2.08 | .08 |
| Noncontrasted CT imaging | 0.93 | 0.53-1.65 | .81 |
| Postoperative sepsis | 1.81 | 1.22-2.67 | <.01 |
| Major cardiac complications | 2.24 | 1.21-4.16 | .01 |
| Unanticipated RTOR | 1.27 | 0.85-1.90 | .24 |
| Length of bowel resection | OR | 95% CI | P value |
| DR | 7.47 | 2.77-19.52 | <.01 |
| Active smoker | 2.85 | 1.11-7.29 | .03 |
| History of hypercoagulable disease | 0.4 | 0.12-1.28 | .12 |
| Pain out of proportion on exam | 0.39 | 0.13-1.11 | .10 |
| Peritonitis | 2.21 | 0.74-6.65 | .16 |
| Presenting AKI | 1.97 | 0.57-6.75 | .28 |
| Arterial embolism etiology | 0.87 | 0.34-2.26 | .78 |
| CTA imaging | 0.34 | 0.12-0.95 | .04 |
| Portal gas on imaging | 1.06 | 0.338-2.92 | .91 |
| Total number of operations | 4.49 | 0.2.38-8.48 | <.01 |
| Short bowel syndrome (requiring TPN) | OR | 95% CI | P value |
| DR | 2.40 | 1.11-5.04 | .03 |
| Pain out of proportion on exam | 0.60 | 0.29-1.23 | .17 |
| Presenting WBC >15,000/uL | 1.61 | 0.76-3.60 | .21 |
| Time to operating room >360 minutes | 1.52 | 0.72-3.20 | .27 |
| Total number of operations | 1.51 | 1.14-1.99 | <.01 |
AKI, Acute kidney injury; AMI, acute mesenteric ischemia; CI, confidence interval; CKD, chronic kidney disease; COPD, chronic obstructive pulmonary disease; CT, computed tomography; CTA, computed tomography angiography; DR, delayed revascularization; ER, early revascularization; HR, hazard ratio; OR, odds ratio; RTOR, return to operating room; TPN, total parenteral nutrition; WBC, white blood cell count.
Fig 2.
Kaplan-Meier curves demonstrating 2-year survival in patients undergoing surgery for acute mesenteric ischemia (AMI) by timing of mesenteric revascularization from 2010 to 2020. Overall mean postoperative follow-up time is displayed. DR, Delayed revascularization; ER, early revascularization.
Secondary outcomes analyzed included length of bowel resection and short bowel syndrome defined by TPN dependence. Measured total length of resected bowel was significantly higher in patients who had DR compared with those who had ER (111 ± 117 cm vs 47 ± 81 cm; P < .01), and DR was shown to be a significant risk factor for bowel resection (OR, 7.47; 95% CI, 2.8-19.5; P < .01) on adjusted analysis. Almost twice as many patients who had DR developed short bowel syndrome requiring TPN postoperatively compared with those who had ER (30.0% vs 15.2%; P = .01). DR was independently associated with short bowel syndrome by multivariate analysis (OR, 2.4; 95% CI, 1.1-5.0; P = .03). Multiple trips to the operating room was found to be an independent risk factor for both increased bowel resection (OR, 4.49; 95% CI, 2.4-8.5; P < .001) and short bowel syndrome (OR, 1.51; 95% CI, 1.1-2.0; P < .001). Smoking was also significantly associated with increased bowel resection (OR, 2.85; 95% CI, 1.1-7.3; P = .03), whereas having CTA abdominal imaging at presentation was found to be protective against bowel resection (OR, 0.34; 95% CI, 0.1-0.95; P = .04), as listed in Table III.
On subgroup analysis of only patients who had early vascular surgery at the initial operation, delayed vascular consultation alone remained an independent risk factor for 30-day (OR, 3.38; 95% CI, 1.1-10.0; P = .03) and 2-year mortality (HR, 2.28; 95% CI, 1.2-4.4; P = .01) in AMI (Table IV; Supplementary Fig 2, A, online only). The association between delayed vascular consultation and increased bowel resection or short bowel syndrome was not found to be statistically significant on multivariate analyses. Subgroup analysis of only patients who had early vascular consultation within 12 hours of presentation demonstrated delayed vascular surgery alone remained an independent risk factor for early 30-day mortality (OR, 4.31; 95% CI, 1.4-12.9; P < .01) but not late mortality on multivariate analysis (Supplementary Fig 2, B, online only). Delaying vascular surgery to the second or subsequent operation was also significantly associated with increased bowel resection (OR, 6.85; 95% CI, 1.3-36.5; P=.02). No revascularization during admission, when compared with any revascularization, was found to be an independent risk factor of increased bowel resection (OR, 15.96; 95% CI, 3.4-75.6; P < .01), short bowel syndrome (OR, 2.94; 95% CI, 1.3-6.6; P < .01), and 2-year mortality (HR, 1.6; 95% CI, 1.0-2.5; P = .04; Table IV). Survival at 2 years in patients with AMI who were never revascularized was only 27.5% compared with 52.8% in patients who had either early or delayed vascular intervention by Kaplan-Meier estimates, as seen in Supplementary Fig 2, C (online only) (P = .002). There were no significant differences in risk of bowel resection or mortality between no revascularization and delayed revascularization. Admission to the Vascular Surgery service appeared to be associated with decreased mortality at 2 years on univariate analysis, with survival estimated to be 56.9% compared with 40.8% of patients with AMI admitted to General Surgery or Medicine service (Supplementary Fig 2, D, online only) (P = .03), but this was not significant on multivariate analysis. Admission to the Vascular Surgery primary service was a significant protective factor against bowel resection (OR, 0.28; 95% CI, 0.1-0.8; P = .01).
Table IV.
Subgroup multivariate logistic regression and Cox proportion hazards models for primary and secondary outcomes in patients with AMI
| Length of bowel resection (OR) |
P value |
Short bowel syndrome (OR) |
P value |
30-day mortality (OR) |
P value |
2-year mortality (HR) |
P value |
|
|---|---|---|---|---|---|---|---|---|
| DR | 7.47 | <.01 | 2.4 | .03 | 2.09 | .03 | 1.55 | .04 |
| Delayed vascular consult only | 3.53 | .09 | 1.97 | .25 | 3.38 | .03 | 2.28 | .01 |
| Delayed vascular surgery only | 6.85 | .02 | 2.86 | .09 | 4.31 | <.01 | 1.73 | .11 |
| No revascularization during admission | ||||||||
| Versus all revascularization | 15.96 | <.01 | 2.94 | <.01 | 1.74 | .19 | 1.60 | .04 |
| Versus delayed revascularization only | 1.76 | .34 | 1.05 | .13 | 1.15 | .76 | 1.29 | .36 |
| Vascular surgery admitting service | 0.28 | .01 | 0.88 | .75 | 0.65 | .31 | 0.67 | .13 |
AMI, Acute mesenteric ischemia; DR, delayed revascularization; HR, hazard ratio; OR, odds ratio.
DISCUSSION
In this study directly comparing outcomes between patients stratified by early or late vascular surgery management in patients undergoing interventions for AMI, we demonstrated that delays in timing to mesenteric revascularization significantly predicted increased postoperative morbidity and mortality. Consultation with a vascular surgeon >12 hours after diagnosis and deferring vascular surgery to the second or subsequent operating room visit were the two major hospital-based variables contributing to delayed time to mesenteric revascularization. Thirty-day operative mortality in our cohort was 33.5% overall, but only 25.0% with early revascularization (P = .02). There was a two- to three-fold increased risk of 30-day mortality and short bowel syndrome and an almost eight-fold increased risk of bowel resection in patients who had DR compared with those who had ER. ER was associated with higher long-term survival in patients with AMI, with 1- and 2- year survival rates estimated to be 59.8% and 55.9%, respectively, compared with 41.3% and 37.1% in patients with DR (P = .03). Presenting and postoperative sepsis, lactate >2.5 mmol/L, and major cardiac conditions/complications were additionally associated with 2-year mortality in patients with AMI. Etiology of disease (embolism vs in situ thrombosis) itself was not found to be a significant, independent predictor of postoperative mortality or short bowel syndrome on either univariate or multivariate logistic regression modelling in this study. Embolic disease was protective against total bowel resection length on univariate analysis, but this was not found to be significant on multivariate logistic regression (OR, 0.87; 95% CI, 0.34-2.26; P = .78). This study was unique in capturing clinical sepsis as a variable, but otherwise, lactic acidosis and cardiac comorbidities were found to be predictors of mortality in other contemporary series as well.11-14
Our data extends findings from an early retrospective analysis by Eltarawy et al of 72 patients with AMI, which established a significant mortality risk from delays to any surgical consultation greater than 24 hours after diagnosis and delays to initial operation in the management of AMI.6 However, other retrospective series in patients with AMI have additionally reported significant mortality differences associated with surgical intervention performed within 12 hours of either symptom onset or hospital presentation.9 These findings helped to establish 12 hours from time of hospital presentation as the threshold between early and delayed vascular surgery consultation for this study. We demonstrated an increased risk of mortality and short bowel syndrome associated with delays to vascular surgery consultation, even in patients with early general surgery consultation or admission within 12 hours of presentation. Evaluation by a vascular surgeon >12 hours after presentation alone was independently found to be a significant predictor of 2-year mortality in patients with AMI, demonstrating a time-sensitive survival benefit to early vascular consultation in patients suspected of AMI.
Despite the critical role of vascular surgery in AMI management to re-establish mesenteric blood supply, there were significant delays to vascular surgery consultation >12 hours after presentation in 55 (25.9%) patients presenting with AMI in our series. This reflects the diagnostic challenges faced by evaluating physicians to accurately identify cases of bowel ischemia as AMI requiring mesenteric revascularization in a timely fashion. Factors that exacerbated these difficulties included suboptimal/lack of imaging, atypical presentation, complex or partially occlusive mesenteric lesions, and/or equivocal mesenteric pulse exam on initial exploration. Thirty-six patients (17.0%) had no vascular surgery consultation, representing a subset of patients with AMI surgically managed by General Surgery alone, who underwent resection of ischemic bowel without any treatment of the mesenteric vasculature. Many of these patients had atypical or partially occlusive mesenteric disease leading to intraoperative diagnostic uncertainty and failure to recognize the need for a revascularization procedure.
Therefore, this study highlights the need to systematically execute a well-balanced interdisciplinary approach in AMI with both general and vascular surgeons to concurrently address the need to resect nonviable ischemic bowel and re-establish mesenteric blood supply. General surgery evaluation alone is insufficient in the management of suspected AMI and can additionally lead to unnecessary delays to mesenteric reperfusion. Of the patients who had DR, 69.9% were admitted to the General Surgery service, whereas only 9.7% were primary Vascular Surgery patients. Additionally, higher concern for nonviable bowel ischemia on diagnostic imaging such as pneumatosis and portal venous gas and cases performed in a damage control fashion were associated with DR, likely reflecting an overemphasis on bowel viability.
Diagnostic challenges in AMI also affected timing of diagnosis and vascular consultation. Patients diagnosed with embolic disease were more likely to have ER, given the pathognomonic signs and symptoms indicating a diagnosis of AMI. Conversely, the difficulty of diagnosis in patients with lesions secondary to thrombotic disease invariably led to delayed diagnosis of AMI by the initial evaluating physician, resulting in delayed revascularization and poorer outcomes compared with those with embolic disease. We found a significant association between timing to revascularization and diagnostic imaging modality choice in our study. Multi-detector CTA has the highest diagnostic accuracy for AMI and alternative intra-abdominal diagnoses; however, only 30% of our patients with AMI were initially evaluated using CTA.15-17 The majority of patients were diagnosed and treated using suboptimal images, either with routine venous phase intravenous contrast CTs or noncontrasted CT imaging, both of which have significantly lower sensitivity and specificity for AMI compared with CTA reported in the literature.15 Patients with noncontrasted CT scans were found to more likely experience DR (16.5% vs 5.2%) consistent with data from a contemporary AMI series associating noncontrasted imaging with delayed diagnosis >24 hours.18 Our data further demonstrated a clinical benefit associated with CTA utilization, as CTA imaging was found to be protective against bowel resection on multivariate analysis (OR, 0.34; 95% CI, 0.1-0.95; P = .04). Efforts to increase and standardize CTA utilization in the diagnosis of all clinically suspected AMI would mitigate diagnostic delays and facilitate early vascular consultation and revascularization and should be part of a protocolized approach to these patients.
Performing early revascularization is a well-established principle of AMI management, supported by level II/III evidence from numerous retrospective series in AMI.19,20 Contemporary recommendations from AMI practice guidelines set forth by the European Society for Trauma and Emergency Surgery have strongly advocated performing vascular surgery in AMI on an urgent basis in all cases of mesenteric arterial embolic or thrombotic disease.21 Despite this, practices in timing and operative approach of mesenteric revascularization by vascular surgeons and institutions vary widely. Multiple prior cohort and population-based studies suggest that many patients with clinically diagnosed AMI requiring surgery do not undergo a revascularization procedure at all, even when secondary to embolic disease or in situ thrombosis. A survey of the National Inpatient Sample by Beaulieu et al showed that, of 4655 patients undergoing any surgery for a diagnosis of AMI, only 679 (14.6%) underwent a revascularization procedure in that admission, with the remaining under bowel resection only.22 In a single-center series of 323 patients with AMI from 1990 to 2015 reported by Acosta-Merida et al, only 44 (13.6%) were documented to have had a vascular procedure.23 These population studies, however, had missing clinical data, and no survival analysis was ever performed between patients with AMI who underwent revascularization and those who did not.
In our cohort, a definitive revascularization procedure was delayed in 37 of patients with AMI (17.4%) by the operating vascular surgeon. Delaying a definitive revascularization procedure until after initial abdominal exploration was independently associated with increased bowel resection (OR, 6.85; 95% CI, 1.3-36.5; P = .02) and 30-day mortality (OR, 4.31; 95% CI, 1.4-12.9; P < .01), even when early vascular consultation was obtained. In this institution’s experience, reasons for delayed revascularization after the index operation were found to be predominantly two-fold. First, the complexity of disease in patients with atypical or partially occlusive mesenteric lesions led some surgeons to defer revascularization given the diagnostic uncertainty and unclear benefit of performing a vascular procedure. Second, late vascular consultation precluded Vascular Surgery involvement at the initial exploration or subsequent operations performed by General Surgery in a subset of patients with AMI. Hemodynamic instability, gross intraabdominal contamination, and technical failure at the index operation were justifications for deferring revascularization in only a small minority of patients.
Fifteen patients with AMI (7.1%) were evaluated by a vascular surgeon and not revascularized. No revascularization on subgroup analysis in our study was found to be a significant risk factor for late mortality, with only a 27.8% survival at 2 years. Technical failure explained no revascularization in three cases. The remaining 12 patients presented with partially occlusive mesenteric disease and were determined to not require a revascularization procedure by the evaluating vascular surgeon due to adequate mesenteric vessel patency on intraoperative exam.
Although no formal evidence-based guidelines or recommendations have yet been released to establish a standard-of-care protocol for vascular management of AMI, several studies have outlined their proposed revascularization strategies based largely, on operative approach 24,25 Perhaps the most advanced prospective efforts in standardizing AMI treatment to date has been put forth by Rousel et al in their development of a multidisciplinary intestinal stroke center in Paris, France, based on a cerebrovascular unit model.25 Standardized treatment of AMI included a multimodal medical protocol, including fluid resuscitation, anticoagulation, and antibiotics and an endovascular-first approach when able. Results from their pilot study demonstrated an impressive 8.9% 30-day mortality and 89.2% 2-year survival; however, as with many single-center retrospective series evaluating comparative outcomes in AMI, these data were influenced by heavy selection bias.25 Findings from our study would support establishing a multidisciplinary timing-based protocolized approach as a more effective means to facilitate early revascularization and improve operative mortality in AMI, which we aim to develop and implement at our institution. Such a protocol would establish a mesenteric revascularization timing benchmark as one of the quality metrics of AMI management, similar to door-to-balloon time in acute myocardial infarction. It additionally will incorporate early, routine CTA diagnostic imaging and vascular surgery consultation to avoid diagnostic and treatment delays. We postulate that this systematic approach and the earlier involvement of vascular surgeons will improve survival outcomes.
Limitations to this study include its design as a retrospective cohort analysis and dependence on retrospective review of electronic medical records, including subjective data from operative reports. Additionally, accurate classification and etiology of mesenteric disease was limited and challenging in patients with suboptimal non-CTA abdominal imaging. The main factors contributing to timing to mesenteric revascularization, timing of vascular consultation and timing of revascularization procedure, were assessed as categorical binary variables rather than as continuous measurements, which would have allowed for more robust timing analysis. Similarly, our study did not capture timing from symptom onset or data from outside hospitals in transferred patients, which would, again, have provided more depth to timing analysis and allow us to establish an exact “golden window” for mesenteric reperfusion to utilize in quality metrics. In prospective follow-up studies, we aim to capture these data in a more precise manner and include it in future analyses. Finally, many survivors with AMI had poor follow-up, which limited long-term survival analysis.
CONCLUSION
AMI is a both a surgical and vascular emergency. Although prompt mesenteric revascularization is well-established as a critical component of AMI management, revascularization strategies have been found to widely differ among vascular institutions and surgeons. We described our experience with surgical management of AMI and assessed the effect of hospital-based timing delays on outcomes within a multi-center hospital system across nine individual hospitals over the past decade, representing the most contemporary and one of the largest AMI series to date. Delayed timing to mesenteric revascularization in AMI, caused by delays in vascular consultation and vascular surgery, is associated with higher 2-year mortality, total bowel resection length, and increased risk of short bowel syndrome. This provides rationale for establishing a timing-based and system-wide protocol for AMI management measuring presentation-to-mesenteric reperfusion time. It also would establish standards for early, routine evaluation by a vascular surgeon and performing a definitive revascularization procedure, when appropriate, no later than the initial operation in all patients requiring surgery for clinically suspected AMI.
Supplementary Material
ARTICLE HIGHLIGHTS.
Type of research: Single-center, retrospective cohort study
Key Findings: Of 212 patients undergoing surgery for acute mesenteric ischemia (AMI), 113 patients (53.3%) experienced a delay to mesenteric revascularization after hospital presentation due to late vascular consultation or revascularization procedure. These delays were significantly associated with predicted 30-day (odds ratio [OR], 2.09; P = .03) and all-cause 2-year mortality (hazard ratio, 1.55; P = .04). The delay to revascularization was also independently associated with total bowel resection length (OR, 7.47; P < .01) and risk of postoperative short bowel syndrome (OR, 2.4; P = .03).
Take Home Message: Early and routine vascular surgery consultation and definitive mesenteric revascularization may mitigate outcomes of patients suspected of AMI. Timing-based AMI management protocols need to be explicitly defined and widely implemented for all patients presenting with potential AMI.
Acknowledgments
L.T. is supported by a National Institutes of Health T-32 postdoctoral training grant (5T32AI074490). E.A. is supported by a National Institutes of Health T-32 postdoctoral training grant (5T32HL0098036). L.T. and E.A. are both additionally supported by the Physician-Scientist Institutional Award from the Burroughs Wellcome Fund held by the University of Pittsburgh.
Footnotes
The editors and reviewers of this article have no relevant financial relationships to disclose per the JVS policy that requires reviewers to decline review of any manuscript for which they may have a conflict of interest.
Additional material for this article may be found online at www.jvascsurg.org.
Presented at the Forty-eighth Annual Symposium of the Society for Clinical Vascular Surgery, Miami, Fla, March 13-17, 2021.
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