Diagnosis of non-occlusive acute mesenteric ischemia in the intensive care unit
© The Author(s) 2016
Received: 17 June 2016
Accepted: 4 November 2016
Published: 17 November 2016
Non-occlusive mesenteric ischemia (NOMI) is a common complication and accounts for a major cause of death in critically ill patients. The diagnosis of NOMI with respect to the eventual indications for surgical treatment is challenging. We addressed the performance of the diagnostic strategy of NOMI in the intensive care unit, with emphasis on contrast-enhanced abdominal CT-scan.
This was a retrospective monocenter study. Patients with clinically suspected acute mesenteric ischemia were included if a comprehensive diagnostic workup was carried out including surgical and/or endoscopic digestive explorations. Patients with evidence of occlusive mesenteric ischemia were excluded. A definite diagnosis of NOMI only relied on surgical or endoscopic findings. Abdominal CT-scans were reviewed by two radiologists blinded from the final diagnosis.
A diagnosis of NOMI could be definitely confirmed or ruled out through surgical or endoscopic explorations of the digestive tract in 147 patients. With respect to their clinical characteristics, only a history of atrial fibrillation was an independent predictor of NOMI (odds ratio 8.3, 95% confidence interval 2.0–35.2, p = 0.004). Among them, 114 patients (75 with and 39 without NOMI) had previously been subjected to contrast-enhanced abdominal CT-scan. Portal venous gas, pneumatosis intestinalis and, to a lesser extent, abnormal contrast-induced bowel wall enhancement were poorly sensitive, but exhibited good specificities of 95, 85 and 71%, respectively. Nineteen out of 75 patients (25.3%) without any suggestive radiological signs finally exhibited mesenteric ischemia, including ten with intestinal necrosis.
The performance of abdominal CT-scan for the diagnosis of NOMI is limited. Radiological signs of advanced-stage ischemia are good predictors of definite mesenteric ischemia, while their absence should not be considered sufficient to rule out the diagnosis.
Acute mesenteric ischemia (AMI) is a dreaded complication in critically ill patients and remains a major diagnostic and therapeutic challenge in most cases. Importantly, AMI encompasses two different pathophysiological entities. Occlusive AMI is caused by the occlusion of large mesenteric arteries or veins due to arterial embolism or a local thrombotic process. AMI may also occur despite preserved patency of large mesenteric vessels, the so-called non-occlusive mesenteric ischemia (NOMI) . NOMI is a common complication in critically ill patients with acute circulatory failure and thereby accounts for a major cause of death in the intensive care unit (ICU) [2, 3]. In a large multicenter study of 780 ICU patients with AMI, the overall mortality rate was 58% . Nonetheless, surgical treatment within 24 h of diagnosis of AMI was identified as an independent predictor of survival, emphasizing the importance of early and reliable diagnosis.
The diagnosis and the treatment of AMI rely on a timely multidisciplinary management involving intensive care physicians, gastroenterologists, radiologists and surgeons . The diagnosis of AMI is often challenging in critically ill patients, most especially for NOMI. It can be suspected in the presence of clinical deterioration associated with digestive symptoms and biological manifestations suggestive of profound tissue ischemia or acute cell lysis. Contrast-enhanced abdominal CT-scan is the cornerstone of the diagnostic strategy and may provide direct or indirect arguments for impaired vascularization of the bowel . However, its accuracy for the diagnosis of NOMI in critically ill patients is questionable. A confirmatory diagnosis as well as the assessment of the extent of necrosis still commonly involves a direct visualization of the digestive tract by endoscopy and/or surgical exploration.
With respect to the frequent diagnostic uncertainty of NOMI in critically ill patients, a better assessment of the preoperative probability of mesenteric ischemia as well as the eventual possibilities of surgical treatment represents an important area of improvement in the management of the disorder. To this aim, we herein addressed the performance of the common diagnostic strategy of NOMI in the ICU, with particular emphasis on abdominal CT-scan.
Patients and methods
Patients and setting
We performed a retrospective monocenter study over an 8-year period (2007–2013) in a 24-bed tertiary medical ICU. The average number of admissions is 1600 per year, and the case-mix is distributed into 90% of medical patients and 10% of patients requiring emergency surgery at the time of admission or during the stay in the ICU. Patients with clinically suspected AMI were included if a comprehensive diagnostic workup including surgical and/or endoscopic explorations of the digestive tract was carried out, regardless of previous abdominal CT-scan imaging. Patients with evidence of occlusive AMI (i.e., interrupted blood flow in large mesenteric vessels) were excluded. This study was part of a project approved by the ethics committee of the French Intensive Care Society. Informed consent was waived due to the retrospective observational design of the study.
Intended management of AMI
In our unit, the diagnosis of AMI relies on a multidisciplinary approach involving intensive care physicians, gastroenterologists, radiologists and surgeons. AMI was commonly suspected on the basis of clinical upper or lower digestive symptoms including abdominal pain, feeding intolerance, gastrointestinal hemorrhage, diarrhea, occlusion, associated or not with deterioration of organ failures, and biological manifestations of tissue ischemia (elevated arterial lactate levels) and cell lysis (increased serum levels of lactate dehydrogenase, creatine phosphokinase and transaminases). A moderate to high probability for AMI prompted further digestive investigations by contrast-enhanced abdominal tomodensitometry and/or upper and lower endoscopic explorations and/or laparotomy. Intestinal resection was indicated in case of localized bowel necrosis. The major steps of patients’ management such as indications for major surgery, transfer to the operating room, or decisions of withholding or withdrawing life support were discussed collectively.
Diagnostic criteria of acute mesenteric ischemia
Collection of data
The following data were collected, either extracted from our patient’s data management system (Centricity CliniSoft, GE Healthcare) or retrieved from individual medical files: demographics (age and gender), underlying comorbidities including cardiovascular diseases, the primary diagnosis warranting ICU admission, the severity of illness at the time of ICU admission as assessed by the Simplified Acute Physiology Score II (SAPS II) and the Sequential Organ Failure Assessment (SOFA) scores [7, 8]. Features associated with clinically suspected NOMI were the following: time from admission to clinical suspicion (i.e., to the first digestive exploration, CT-scan, surgery or endoscopy), digestive symptoms, arterial blood lactate, serum enzymes levels (lactate dehydrogenase, creatine phosphokinase, transaminases), concurrent organ failures as quantified by the SOFA score.
Statistical analyses were performed using the software Prism 5.0 (Graphpad, San Diego, CA). Categorical data are presented as numbers (%) and compared by Chi-square or Fisher’s exact test as appropriate. Continuous variables are expressed as median and interquartile range and compared using the nonparametric Mann–Whitney test. Variables found associated with a p value <0.20 in univariate analysis were entered into a multivariate backward stepwise logistic regression analysis in order to identify the factors independently associated with a definite diagnosis of NOMI. The goodness-of-fit of the model was checked by the Hosmer–Lemeshow test.
Characteristics of patients with and without non-occlusive mesenteric ischemia
Definite NOMI (n = 92)
NOMI ruled out (n = 55)
Peripheral vascular disease
End-stage renal disease
Main diagnosis at ICU admission
Severe sepsis or septic shock
Acute kidney injury
Illness severity at admission (points)
Diagnosis of NOMI
Time to diagnosis (days)a
Concurrent antibiotic treatment
Lower digestive symptoms
Upper digestive symptoms
Serum laboratory results
Arterial lactate (mmol/L)
Leukocyte count (G/L)
Diagnostic features of non-occlusive mesenteric ischemia
Number of patients (%)
Stomach and/or duodenum
Jejunum and/or ileum
Non-necrotic ischemic lesions
Extent of ischemia
Extensive (≥2 intestinal segments)
Upper digestive fibroscopy
Performance of abdominal CT-scan findings in the diagnosis of non-occlusive mesenteric ischemia
Definite NOMI (n = 75) (%)
NOMI ruled out (n = 39) (%)
Abnormal wall enhancement
Portal venous gas
AMI encompasses two different pathophysiological entities affected with distinct diagnostic and therapeutic issues. The diagnosis of occlusive AMI is often obvious, relying on the blockage of blood flow within large mesenteric arteries or veins on a contrast-enhanced CT-scan. The treatment combines surgical or instrumental arterial reperfusion and the eventual resection of necrotic bowel segments [9, 10]. In contrast, NOMI occurs despite seemingly preserved mesenteric blood flow and is most often associated with advanced age, cardiac insufficiency, atrial fibrillation, hemodialysis and prior episodes of hypotension [11–14]. It represents a significant complication in critically ill patients with severe and prolonged acute circulatory failure [2, 3]. However, prolonged hypoperfusion does not recapitulate the mechanisms that contribute to the advent of NOMI, that also involves mesenteric vasoconstriction, intestinal hypoxia while increased intestinal metabolic demand, ischemia–reperfusion injury, apoptosis and decreased proliferation of enterocytes . Tissue necrosis and disruption of the intestinal barrier may then result in bacterial translocation, systemic inflammatory response and multiple organ failure .
Regardless of the underlying ischemic process, occlusive or non-occlusive, the prognosis of AMI is poor as the overall mortality rate may reach 80% in most published cohorts [3, 16–18]. Leone and colleagues provided reliable prognostic data for AMI in an impressive multicenter series of 780 cases . The in-ICU mortality rate was 58%, and the possibility of an initial surgical treatment was identified as an independent predictor of survival. However, an important limit of the paper lies in the absence of formal diagnostic criteria for AMI. Indeed, the diagnosis of AMI could be supported by gastrointestinal endoscopy or surgery, or alternatively by CT-scan only in the majority (58%) of patients. Furthermore, the mechanism of mesenteric ischemia, occlusive versus non-occlusive, was not reported either.
Despite a better awareness of the disorder, the diagnosis of NOMI remains particularly challenging in critically ill patients, and diagnostic uncertainty may ultimately require surgical explorations for an accurate assessment of the bowel. Every effort should be made to refine the diagnostic performance for AMI, in order to avoid unnecessary and aggressive surgical interventions in patients without digestive ischemia, and also in patients with end-stage extensive necrosis ineligible for segmental intestinal resection. We herein assessed a stringent diagnostic workup in which AMI could only be definitely confirmed or ruled out by direct visualization of the digestive tract by endoscopic or surgical explorations. We addressed the performance of the main diagnostic steps including clinical and biological manifestations and abdominal CT-scan. Clinical symptoms and biological markers of tissue ischemia and acute cell lysis may commonly suggest the diagnosis of mesenteric ischemia, but clearly lack sensitivity and specificity in this setting [19, 20]. More relevant information is expected from abdominal CT-scan .
The performance of CT-scan has been reported as good to excellent in the diagnosis of AMI with sensitivity and specificity, generally about 90% . However, it should be emphasized that these studies were performed in the setting of occlusive AMI, in which the diagnosis is made much easier by the blockade of mesenteric blood flow. In contrast, few studies have addressed its diagnostic value in NOMI. We report here that abdominal CT-scan has limited performance in this setting. Portal venous gas or pneumatosis intestinalis appeared as specific radiological signs (specificities 95 and 85%, respectively). Nonetheless, both may be seen in non-ischemic conditions including connective tissue disorders, inflammatory bowel diseases, cytotoxic chemotherapy and major bowel distension . Abnormal wall enhancement was associated with a lower but still reasonable specificity of 71%. However, a major limit of those three CT-scan signs lied in their poor sensitivity (19, 32 and 62%, respectively), making their diagnostic contribution irrelevant in most patients.
Which clinical implications can be drawn from our findings? Although we pointed out the limitations of CT-scan, we keep thinking that it should remain the cornerstone of the diagnostic workup of AMI in the ICU. However, only a surgical exploration is currently able to provide an accurate assessment of bowel viability and to delineate the frankly necrotic sections requiring segmental intestinal resection. On the other hand, partially ischemic bowel regions might be liable to salvage after intraoperative visualization of restored mesenteric perfusion, spontaneously or after injection of a fluorescent dye . The presence of portal venous gas or pneumatosis intestinalis surely indicates urgent exploratory laparotomy. The same should probably apply to abnormal wall enhancement. Finally, the still unanswered question remains about surgical indications in patients with negative abdominal imaging. Although it is difficult to provide firm recommendations, we would then propose a pragmatic approach in which surgical indications should be based on eventual clinical deterioration despite optimal medical treatment and advanced organ failure supports.
Finally, the most important treatment for NOMI is preventive and every effort should be made to limit the duration and severity of acute circulatory failure. Our therapeutic goals in this setting still remain largely based on macroscopic circulatory parameters, whereas microcirculatory disorders may also contribute to organ failures in an independent manner . Reliable assessment of microcirculatory tissue perfusion in critically ill patients has been made possible by technological advances. However, the therapeutic implications remain questionable .
Our study has strengths and limitations that deserve to be mentioned. Its main strength lies in its stringent methodology despite its retrospective design. A definite diagnosis or conversely elimination of mesenteric ischemia required confirmatory investigations by surgery and/or endoscopy and could only be presumed on CT-scan. Furthermore, the investigators who interpreted the CT-scan imaging and those who confirmed the diagnosis of mesenteric ischemia through endoscopic and surgical reports were different and kept blinded from other concurrent investigations. With respect to limitations, this was a single-center study performed in a medical ICU setting where the large majority of patients are referred for a wide range of medical conditions. The retrospective design of the study may have led to incomplete identification of patients with suspected mesenteric ischemia. This is the reason why we only included patients with a significant clinical probability of AMI who were therefore explored by an abdominal CT-scan, or directly by endoscopy or surgery. In addition, urgent endoscopy can only explore the upper (oesophagus, stomach and duodenum) and lower (rectum and colon) extremities of the digestive tract, leaving unexplored the jejunum and ileum in between. We cannot exclude that some patients only explored by endoscopy without further surgery may still display mesenteric ischemia in non-visualized intestinal regions.
AMI remains a diagnostic and therapeutic challenge in critically ill patients, especially in case of non-occlusive forms. The diagnostic contribution of abdominal CT-scan is limited in this setting. Radiological signs of advanced-stage ischemia represent undisputed indications for surgical intervention to assess the extent of bowel necrosis and the possibility of intestinal resection. The absence of radiological signs suggesting mesenteric ischemia should not be considered sufficient to rule out the diagnosis and still warrants further digestive explorations by endoscopy and/or laparotomy in case of high clinical suspicion.
SB, AO, BD, FP were involved in study concept and design; SB, AO, GG, JC, SL, RC, HG acquired the data; all authors were involved in analysis and interpretation of data; SB, FP drafted the manuscript; all authors critically revised the manuscript; FP was involved in study supervision. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
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