Computed Tomography Parameters for Prognosis Prediction in Non-Occlusive Mesenteric Ischemia

Introduction

Non-occlusive mesenteric ischemia (NOMI) causes the development of ambiguous clinical symptoms in elderly patients. Because NOMI has high morbidity and mortality rates, urgent diagnosis in the emergency department and appropriate treatment could be lifesaving. NOMI accounts for 20% to 30% of all acute mesenteric ischemia (AMI) cases and is the most difficult and lethal subtype to diagnose [1–4].

In NOMI, intestinal ischemia can develop as a result of decreased blood flow by vasoconstriction in mesenteric circulation, without arterial or venous occlusion [4–6]. Intestinal ischemia is limited to the mucosa in the early phase; some lesions could potentially heal, and the tissue is still viable. If ischemia progresses, the damage also progresses to the deeper layers of the intestine. With full thickness infarction in the late injury phase, transmural ischemia is irreversible and intestinal necrosis occurs. Following intestinal necrosis, peritonitis, perforation, and multi-organ failure can develop, and the course can be fatal. Therefore, the necrotic intestinal segment should be surgically excised urgently in the late injury phase. However, because the irreversible and poorly perfused ischemic lesions are usually widespread and patchy, and there is no clear distinction between viable and necrotic tissue, extensive surgical resection is generally needed. The key point in the treatment of NOMI is to reduce spasms in mesenteric circulation and increase effective arterial perfusion with vasodilators. These phases of NOMI should be accurately and timely recognized, because treatment, survival, morbidity, and mortality differ according to early and late injury phases [5–13].

Imaging the mesenteric vascular tree with a multi-detector computed tomography (MDCT) is the most important radiological method in the early diagnosis of AMI and in determining its etiology. MDCT provides critical quantitative and qualitative data about the mesentery, bowel, vasculature, and peritoneum, and these data help differentiate different phases of NOMI [4,11,13].

Therefore, this study aimed to evaluate the association between CT imaging findings of the superior mesenteric artery (SMA), celiac trunk (CeT), inferior vena cava (IVC), and superior mesenteric vein (SMV) diameters, intestinal wall density, and outcomes in 40 patients with mesenteric ischemia.

Material and Methods

PATIENTS:

Ethical approval was obtained from our University Ethics Committee (2022/06) for our single-center retrospective study. Given the retrospective nature of the study, patient consent was not obtained.

Patients with a diagnosis of NOMI were included in the study by scanning the hospital database and management system between January 2016 and December 2021 and evaluating the MDCT and pathological examination results obtained from the Radiology Information Management System. NOMI was diagnosed radiologically using biphasic mesenteric CT scanning and/or based on surgical/pathology results.

The inclusion criteria were as follows: patients >18 years of age, those with biphasic mesenteric CT scan, and those whose diagnosis of NOMI was confirmed radiologically, surgically, or pathologically. The exclusion criteria were as follows: patients <18 years of age, those with CT protocols other than biphasic, those with the diagnosis of AMI subtypes other than NOMI or other abdominal pathologies.

A total of 85 patients with a diagnosis of AMI were studied. Twenty patients were excluded from the study due to occlusive AMI, 15 due to diagnoses other than NOMI, and 10 due to routine whole abdominal CT with contrast. A total of 40 patients with NOMI were included in the study, with a mean age of 72.7±12 years; 24 men (60%) and 14 women 14 (40%). The patients were divided into 2 groups: non-survivors, who died within 20 days of hospitalization, and survivors, who were alive after 20 days. All comorbidities of the patients were recorded.

IMAGING ANALYSIS:

This study was performed using a 64-detector CT (GE Revolution Evo 128 Section-2017, China). The CT protocol was categorized as an angiographic phase and a biphasic dynamic phase, consisting of arterial and venous phases. All of the CT examinations were evaluated retrospectively, according to a predefined scheme.

All abdominal CT scans were examined by 2 radiologists (who had 15 and 7 years of experience in abdominal scanning, respectively) with a PACS work station. The readers were blind to all clinical, laboratory, and pathological findings. Findings of NOMI on MDCT were evaluated under 2 categories, as qualitative and quantitative findings.

Qualitative findings were evaluated under the following 4 subcategories and recorded as present or absent.

Quantitative findings were evaluated under the following 2 subcategories: diameters of vascular structures and contrast enhancement of the intestinal wall.

Diameter measurements of veins were performed on axial sections. The IVC diameter was measured just above the level of renal vein confluence and the SMV diameter just before splenic vein confluence (Figure 4).

In addition, patients who underwent intestinal resection, and their comorbidities, were recorded.

STATISTICAL ANALYSIS:

The descriptive data are presented as frequencies (percentages), median (interquartile range), or mean±standard deviation. The normality of the continuous variables was assessed with the Shapiro-Wilk test and histogram graphs. Fisher’s exact test was performed to analyze the correlation between the qualitative findings, as present or absent, and patient outcome. For normally distributed variables, independent-sample t tests and one-way ANOVA were used. When the data did not meet the normality assumption, non-parametric Mann-Whitney U and Kruskal-Wallis tests were used for the comparison of continuous variables between the groups. Multivariate logistic regression analysis was used to investigate the predictors of quantitative parameters affecting survival in NOMI patients, after we controlled for age and sex. Receiver operating characteristic (ROC) curve analysis was used to evaluate the prognostic performance of quantitative variables between the survivor group and the non-survivor group among patients with NOMI, and the area under the ROC curve (AUC) was calculated.

All statistical analyses were performed using the Statistical Package for Social Sciences 26.0 for Windows (IBM Corp, Armonk, NY, USA). The results were considered to be significant at a level of P<0.05.

Results

CLINICAL OUTCOMES:

The mean age of 40 patients in the study was 72.7±12 years, and of those, 24 were men (60%) and 16 were women (40%). The mean ages of the survivor and non-survivor groups were 68.2±12 and 80.1±6 years, respectively (P=0.002).

CT FINDINGS:

The qualitative CT findings of patients with NOMI were analyzed with Fisher’s exact test in 2 groups: those who died and those who survived within 20 days of admission. Pneumatosis intestinalis, paper-thin bowel wall, pale mesentery, and solid-organ infarct in the non-survivor group; and bowel wall thickening, bowel wall enhancement, bowel wall mucosal-submucosal enhancement, and mesenteric congestion in the survivor group were observed significantly more often (Table 1).

When the quantitative variables in the survivor and non-survivor groups were compared, CeT, SMA, IMA, SMV, and IVC diameters and delta HU in the non-survivor group were significantly lower. There was no significant relationship between age and SMV/SMA ratio (Table 2).

In the analysis of the correlation between quantitative CT parameters, age, survival, and SMA, IMA, SMV, and IVC diameters were positively correlated with delta HU and negatively correlated with patient’s age. There was no significant correlation between the SMV/SMA ratio and survival (Table 3).

In the logistic regression analysis to detect independent variables that affected patient prognosis, the IVC diameter was found to be significantly correlated with patient prognosis (Table 4). To evaluate the predictive prognostic performance of IVC diameter, an ROC curve was used, and an AUC of 0.795 (95% CI: 0.658–0.932, P=0.002) was obtained in the analysis (Figure 6).

Discussion

In this study, we found a high correlation between early qualitative and quantitative MDCT parameters in NOMI patients with good prognosis, and we found late qualitative and quantitative MDCT parameters in patients with poor prognosis.

In the survivor group, the most significant qualitative parameters were mesenteric congestion, bowel wall thickening, and bowel wall hyperdensity. It is thought that these parameters indicate intestinal, mesenteric, and vascular changes, thus, effective reperfusion and reversible clinicopathologic status in the early period. In their study, Bagnacci et al also showed these findings in patients with good prognoses [14]. Additionally, Mazzei et al reported that there is a high correlation between bowel wall thickening and effective reperfusion [15].

In our study, pneumatosis intestinalis, pale mesentery, paper-thin bowel wall, and bowel wall hypodensity were highly associated with death. These qualitative CT parameters, considered to reflect late changes, are associated with poor prognosis in these patients. In another study, the presence or absence of bowel wall contrast enhancement or hypodensity were found to be the most important parameters in poor prognosis [15]. In addition, Bagnacci et al detected that the prevalence of pneumatosis intestinalis in survivor and non-survivor groups was not different, although they found similar results to our findings. On the other hand, Nakamura et al found 8 cases of pneumatosis intestinalis in 11 NOMI patients that underwent surgical resections, and Perez-Garcia et al determined that 76% of patients with pneumatosis intestinalis could be treated with surgical resection [16–20]. In their study, Miyazawa et al did not find a significant relationship between prognosis and pneumatosis in 21 patients with NOMI [21]. The presence of different findings could be due to different clinical and radiological stages of NOMI, the inclusion of patients with different comorbidities, and the use of different imaging protocols. The effect of this parameter on the prognosis should be evaluated with larger case series.

Of the qualitative parameters, CeT, SMA, SMV, IVC, and IMA diameters were found to be significantly smaller in the non-survivor group. Perez-Garcia et al also found that SMA diameter was statistically significantly lower in patients with NOMI, similar to our study [20]. In the regression analysis we performed to detect the independent variable affecting prognosis, we found that only IVC among measured diameters was significantly correlated with the prognosis of NOMI. In the ROC analysis we performed to detect the prognostic significance of the IVC, we detected a significant relationship between IVC and prognosis. Nakamura et al found that SMA and SMV diameters in the NOMI group were significantly smaller than those in the control group [17]. Some other studies have also revealed that the SMA diameter is significantly smaller than that of the control group [15–18]. Bagnacci et al also reported that mesenteric artery-vein and IVC diameters were significantly correlated with poor prognosis. The reason why all diameters were smaller in the non-survivor group in our study may be due to the fact that reperfusion injury response became more systemic during the ineffective reperfusion phase, and atherosclerosis could have affected the mesenteric arterial tree because the average age of our population was 80 years or older. In a study evaluating the effect of atherosclerosis on the prognosis of NOMI patients, atherosclerosis in SMA was associated with poor prognosis [19]. In several studies in the literature, as in our study, no significant relationship was detected between the SMA/SMV ratio and prognosis [14].

In our study, we found a significant correlation between delta HU and prognosis. Bagnacci et al found that delta HU that was measured in the non-contrast and arterial phases has a major effect on patient prognosis. We also identified a significant relationship between delta HU, a difference between bowel wall densities in arterial and portal venous phases, and patient prognosis. This situation suggests that detecting any enhancement difference in involved intestinal segments in both arterial and venous phases may be an important parameter indicating patient prognosis, similarly.

We determined that solid organ infarct was significantly correlated with poor prognosis. In their study, Perez-Garcia et al found that spleen infarct in patients with NOMI who underwent surgical treatment was more frequent than in those who were treated conservatively [20].

There are several limitations in our study. First, this was a single-center and retrospective study. Second, the number of patients was limited. Third, NOMI was diagnosed primarily with clinical and laboratory findings, the surgical diagnosis was made only in a few patients, and most patients were not diagnosed histopathologically.

Conclusions

NOMI is a challenging and life-threatening pathology requiring prompt diagnosis and intervention to reduce high mortality rates and complications. A systematic evaluation using multiphasic CT and qualitative and quantitative CT parameters could make important contributions to the early diagnosis and treatment of patients with NOMI.