Irreversible Transmural Intestinal Necrosis in Acute Mesenteric Ischemia: Retrospective Cohort Study from a High-Volume Hospital

Abstract

Background:

Owing to the low incidence rate and nonspecific symptoms of acute mesenteric ischemia (AMI), the identification and prediction of irreversible transmural intestinal necrosis (ITIN) and extensive bowel resection (≥100 cm) (EBR) are difficult and critical. This study aimed to investigate the risk factors for ITIN and EBR in patients with AMI.

Methods:

The clinical data of 254 AMI patients were retrospectively analyzed. Furthermore, the incidence of ITIN and EBR were set as dependent variables, and relevant risk factors were screened using univariate and multivariate logistic regression analyses. The comparisons of surgical characteristics and postoperative recovery outcomes between the EBR and control group were also conducted.

Results:

The presence of hemorrhagic (odds ratio [OR] = 28.356, P < .001) or other types ascites (OR = 13.051, P = .003), peritonitis (OR = 8.463, P = .005), intestinal diameter >2.35 cm (OR = 5.493, P = .020), and serum creatinine (CREA) >95 μmol/L (OR = 4.866, P = .048) were identified as independent risk factors for ITIN in patients with AMI. In addition, serum C-reactive protein (CRP) >15 mg/L (OR = 38.023, P = .006), and CREA >100 μmol/L (OR = 6.248, P = .035) were proved to be independently associated with EBR for ITIN cases. Compared to the control group, EBR significantly increased the likelihood of requiring enterostomy (P = .001), blood transfusion (P = .002), and transfer to intensive care unit (P = .016), while also prolonging the recovery time for intestinal function (P = .014).

Conclusions:

Introduction

Acute mesenteric ischemia (AMI), a group of disorders resulting from inadequate blood flow in the mesenteric vessels to meet the metabolic demands of intra-abdominal organs, represents a critical surgical emergency involving the abdomen.^1,2 The term AMI primarily encompasses ischemic disorders affecting the superior mesenteric artery and vein, encompassing arterial embolism, arterial and venous thrombosis, as well as nonocclusive intestinal ischemia.^2,3 Based on an analysis utilizing the UK National General Practitioner Database, the overall incidence of AMI is 0.63/100,000 per year; however, another study conducted in Sweden reported a significantly higher incidence rate of 12.9/100,000.⁴

The low incidence rate and nonspecific symptoms and signs, which resemble those of other acute abdominal conditions such as intestinal obstruction, pancreatitis, and biliary infection, pose challenges in diagnosing AMI. In general, AMI should be considered in patients presenting with unexplained severe abdominal pain accompanied by distinctive clinical signs and symptoms.^5,6 Due to the duality of the intestinal blood supply and the development of collateral circulation, significant ischemia only occurs when there is a 50% reduction in the intestinal blood supply. Failure to promptly recognize and intervene in AMI can result in further deterioration of intestinal ischemia, leading to irreversible transmural intestinal necrosis (ITIN), severe septic shock, multiple organ failure, and potentially fatal outcomes.^7,8

Therefore, early diagnosis of AMI and the identification and prediction of risk factors associated with ITIN in AMI cases are crucially important. In addition, the identification of predictors linked to extensive bowel resection (≥100 cm) (EBR) can provide valuable guidance for the clinical management of ITIN.

The advancement of contrast-enhanced computed tomography (CT) technology has led to the replacement of angiography by CT angiography (CTA) as the gold standard for diagnosing AMI.^3,9 However, specific laboratory indicators for the diagnosis are still lacking.¹⁰ Previous studies have reported that the elevation of lactic acid, D-dimer, and glutathione transferase levels has a certain suggestive significance for the diagnosis and change in the AMI course.^10–13 In the past decade, few studies have investigated the risk factors for ITIN in AMI cases, and studies on intestinal resection are still lacking. Moreover, the studies published on AMI had limited sample sizes, leading to inadequate evidence.

In this study, the potential risk factors for AMI were categorized into three groups based on relevant literature: demographic characteristics, disease characteristics, and preoperative serological examination. Subsequently, univariate and multivariate analyses were conducted to identify and quantify the risk factors for ITIN and EBR using case data from one of the nation's largest medical centers.

Methods

Study participants

The present retrospective control study included patients with AMI who received treatment at our medical center. The diagnosis of AMI was confirmed based on the presence of relevant abdominal symptoms, signs, and imaging examinations such as CTA and angiography. The excised specimen from patients undergoing bowel resection was subjected to pathological examination to confirm the presence of ITIN. Relevant clinical data were gathered utilizing an electronic medical records (EMR) system.

The inclusion criteria were as follows: (1) age ≥18 years; (2) hospitalization period ranging from January 2008 to December 2021; and (3) patients who underwent CTA or angiography during the disease course. The exclusion criteria were as follows: (1) chronic mesenteric vascular stasis and carcinoma thrombosis resulting from portal hypertension caused by liver disease; (2) concurrent mesenteric artery dissection; and (3) unavailability of relevant clinical data. This work was reported in line with the Strengthening The Reporting Of Cohort Studies in Surgery (STROCSS) criteria.¹⁴ The study was reviewed and approved by the Medical Ethics Committee of the First Medical Center of the Chinese PLA General Hospital.

Data collection and outcome evaluation

The dependent variables to be collected and analyzed in this study encompassed the presence of ITIN and the extent of bowel resection. Moreover, the predictor variables were collected and evaluated, which could be associated with ITIN or EBR, encompassed gender, age, body mass index, smoking and drinking history, nutritional risk score (NRS), occlusion site and characteristics, disease course, preoperative length of stay, presence of important comorbidities, anemia, hypoalbuminemia, intestinal obstruction, gastrointestinal hemorrhage, ascites, peritonitis, and preoperative anticoagulation or thrombolysis, intestinal diameter, preoperative level of serum white blood cell (WBC), %neutrophil (%NEUT), C-reactive protein (CRP), D-dimer, fibrinogen (Fib), alanine transaminase, aspartate transaminase, creatinine (CREA), and blood urea nitrogen (BUN). The acquired case data could be summarized into three categories: demographic characteristics, disease characteristics, and preoperative serological examination.

In this study, the important comorbidities for AMI cases included cardiac disease (myocardial infarction, heart failure, atrial fibrillation, coronary heart disease, and rheumatic heart disease), peripheral vascular, cerebrovascular, and connective tissue disease, hepatopathy, hemiplegic paralysis, moderate and severe nephropathy, tumor, inflammatory bowel disease, hypertension, diabetes, dyslipidemia, and a history of gastrointestinal surgery or ileus. Ascites were confirmed via abdominal CT, and their characteristics were further defined through abdominal puncture. The diameter of the intestinal tract was determined through preoperative imaging analysis. All imaging findings were retrospectively assessed by a senior radiologist, and all pathological findings were examined and analyzed by a senior pathologist.

The AMI patients included in the study were classified into two groups, namely the ITIN group and the control group, based on the pathological findings. Besides, the patients with ITIN were further classified into the EBR group and the control group, based on the extent of bowel resection. The median range (100 cm) of bowel resection was utilized for categorization.

Statistical analyses

All the statistical analyses in this study were performed using SPSS software version 26.0. Categorical data were presented as numbers (percentages) and were compared using two-sided chi-square or Fisher's exact tests. Q-Q plots were utilized to assess normal distribution for continuous variables, and mean with the standard deviation or median with the interquartile range was calculated to present the data. Subsequently, intergroup comparison was conducted using independent-samples T test or Mann–Whitney U test. Receiver operating characteristic (ROC) curves were plotted for continuous variable, and the thresholds corresponding to the maximum sum of sensitivity and specificity were determined as the cutoff values. The continuous variables were subsequently converted into binary variables for further analysis based on the specified cutoff values.

Univariate analyses were conducted to examine the correlations between covariates and dependent variables, and the covariates with P < .1 would be included in a multivariate logistic regression model to identify the independent predictors. All tests were considered statistically significant if P values <.05.

Results

Patients characteristics

After a rigorous screening process, a total of 254 patients diagnosed with AMI and exhibiting comprehensive outcome indicators were selected as the subjects for this study. The distribution of occlusion site and characteristics in these patients was as follows: mesenteric artery embolism occurred in 67 (26.4%) cases, mesenteric artery thrombosis occurred in 17 (6.7%) cases, mesenteric vein thrombosis (MVT) occurred in 56 (22.0%) cases, and MVT combined with portal vein thrombosis occurred in 114 (44.9%) cases. Among the 254 patients, 101 (39.8%) received conservative treatment, 85 (33.5%) underwent laparotomy, and 68 (26.7%) underwent interventional surgery. In addition, 4 patients died during hospitalization, all of whom had undergone enterectomy, while the remaining individuals were successfully treated and discharged. The pathological diagnosis of ITIN was confirmed in 57 out of the 75 patients with AMI who underwent bowel resection.

Univariate and multivariate analysis of risk factors for ITIN

Univariate and multivariate analyses were conducted between 57 patients with ITIN and 197 control patients. The univariate analyses showed that the occurrence of ITIN was significantly correlated with the age (P = .002), preoperative NRS 2002 score (P < .001), disease course (P = .001), intestinal diameter (P < .001), presence of hypoalbuminemia (P = .006), intestinal obstruction (P < .001), ascites (P < .001), and peritonitis (P < .001), preoperative levels of serum WBC (P < .001), %NEUT (P < .001), CRP (P < .001), D-dimer (P = .003), CREA (P < .001), and BUN (P < .001) (Table 1).

Table 1.

Univariate Analysis of Risk Factors for Irreversible Transmural Intestinal Necrosis in Acute Mesenteric Ischemia

	Total (n = 254)	ITIN group (n = 57)	Control group (n = 197)	P
Demographic characteristics
Gender				.440
Male	172 (67.7)	41 (71.9)	131 (66.5)
Female	82 (32.3)	16 (28.1)	66 (33.5)
Age (years)				.002
≤60	176 (69.3)	30 (52.6)	146 (74.1)
>60	78 (30.7)	27 (47.4)	51 (25.9)
BMI (kg/m²)				.253
≤28	213 (83.9)	45 (78.9)	168 (85.3)
>28	41 (16.1)	12 (21.1)	29 (14.7)
Smoking history				.954
Absence	173 (68.1)	39 (68.4)	134 (68.0)
Presence	81 (31.9)	18 (31.6)	63 (32.0)
Drinking history				.517
Absence	183 (72.0)	43 (75.4)	140 (71.1)
Presence	71 (28.0)	14 (24.6)	57 (28.9)
Important comorbidities				.517
Absence	53 (20.9)	15 (26.3)	38 (19.3)
Presence	201 (79.1)	42 (73.7)	159 (80.7)
Anemia				.616
Absence	185 (72.8)	43 (75.4)	142 (72.1)
Presence	69 (27.2)	14 (24.6)	55 (27.9)
Hypoalbuminemia				.006
Absence	143 (56.3)	23 (40.4)	120 (60.9)
Presence	111 (43.7)	34 (59.6)	77 (39.1)
NRS 2002 score				<.001
<3	64 (25.2)	4 (7.0)	60 (30.5)
≥3	190 (74.8)	53 (93.0)	137 (69.5)
Disease characteristics
Occlusion site and characteristics				.396
MAE	67 (26.4)	19 (33.3)	48 (24.4)
MAT	17 (6.7)	3 (5.3)	14 (7.1)
MVT	170 (66.9)	35 (61.4)	135 (68.5)
Disease course (hours)	168 (72, 336)	72 (24, 228)	168 (72, 360)	.001
Intestinal obstruction				<.001
Absence	184 (72.4)	26 (45.6)	158 (80.2)
Presence	70 (27.6)	31 (54.4)	39 (19.8)
Gastrointestinal hemorrhage				.453
Absence	188 (74.0)	40 (70.2)	148 (75.1)
Presence	66 (26.0)	17 (29.8)	49 (24.9)
Ascites				<.001
Absence	188 (74.0)	8 (14.0)	180 (91.4)
Other types ascites	46 (18.1)	38 (66.7)	8 (4.1)
Hemorrhagic ascites	20 (7.9)	11 (19.3)	9 (4.6)
Peritonitis				<.001
Absence	147 (57.9)	9 (15.8)	138 (70.1)
Presence	107 (42.1)	48 (84.2)	59 (29.9)
Intestinal diameter (cm)	2.35 ± 0.53	2.68 ± 0.59	2.26 ± 0.47	<.001
Preoperative serological examination
WBC (10⁹/L)	10.96 (6.67, 16.11)	14.65 (11.20, 21.88)	9.68 (6.22, 15.35)	<.001
%NEUT	0.78 ± 0.14	0.88 ± 0.06	0.75 ± 0.15	<.001
CRP (mg/L)	8.07 (4.50, 9.31)	9.20 (6.20, 15.53)	8.07 (3.80, 8.07)	<.001
D-dimer (mg/L)	4.84 (2.27, 11.37)	7.62 (3.58, 14.55)	4.22 (1.83, 10.14)	.003
Fib (g/L)	4.32 (3.36, 5.58)	4.14 (3.35, 5.75)	4.37 (3.35, 5.50)	.827
ALT (U/L)	20.05 (12.08, 30.55)	16.20 (10.45, 29.05)	20.40 (12.40, 31.00)	.335
AST (U/L)	21.00 (15.48, 29.45)	21.10 (16.90, 35.90)	20.50 (15.30, 28.65)	.173
CREA (μmol/L)	71.90 (57.80, 93.73)	100.40 (67.25, 135.50)	69.70 (55.10, 86.90)	<.001
BUN (μmol/L)	5.45 (4.03, 7.85)	9.22 (5.99, 12.90)	5.17 (3.80, 6.62)	<.001

Bold values indicate a statistical difference P < 0.05.

Data are reported as numbers (percentage), mean ± SD, or the median (IQR).

%NEUT, %neutrophil; ALT, alanine transaminase; AST, aspartate transaminase; BMI, body mass index; BUN, blood urea nitrogen; CRP, C-reactive protein; CREA, creatinine; Fib, fibrinogen; IQR, interquartile range; ITIN, irreversible transmural intestinal necrosis; MAE, mesenteric artery embolism; MAT, mesenteric artery thrombosis; MVT, mesenteric vein thrombosis; NRS, nutritional risk score; NEUT, neutrophil; SD, standard deviation; WBC, white blood cell.

The cutoff values of disease course, intestinal diameter, preoperative levels of serum WBC, %NEUT, CRP, D-dimer, CREA, and BUN were determined by plotting the ROC curves, followed by conversion of above outcome indicators into binary variables. Subsequently, the following variables were included in the multivariate logistic regression analysis: age >60 years, hypoalbuminemia, NRS 2002 score ≥3, disease course >96 hours, intestinal obstruction, ascites, peritonitis, intestinal diameter >2.35 cm, serum WBC >11 × 10^9/L, %NEUT >0.83, CRP >8.1 mg/L, D-dimer >3.12 mg/L, CREA >95 μmol/L, and BUN >6.9 μmol/L were further included in a multivariate logistic regression analysis.

Table 2.

Multivariate Analysis of Risk Factors Associated with Irreversible transmural Intestinal Necrosis

Variables	Coefficients	OR (95% CI)	P
Age >60 years	−1.016	0.362 (0.064–2.043)	.250
Hypoalbuminemia	0.364	1.439 (0.436–4.753)	.551
NRS 2002 score ≥3	0.376	1.457 (0.256–8.291)	.671
Disease course >96 hours	−1.187	0.305 (0.057–1.638)	.166
Intestinal obstruction	0.019	1.019 (0.303–3.431)	.975
Ascites			<.001
Other types ascites versus absence	2.569	13.051 (2.457–69.310)	.003
Hemorrhagic ascites versus absence	3.345	28.356 (7.181–111.971)	<.001
Peritonitis	2.136	8.463 (1.930–37.100)	.005
Intestinal diameter >2.35 cm	1.703	5.493 (1.315–22.944)	.020
WBC >11 × 10⁹/L	−0.047	0.954 (0.191–4.764)	.954
%NEUT >0.83	1.009	2.742 (0.607–12.383)	.190
CRP >8.1 mg/L	0.358	1.430 (0.402–5.085)	.581
D-dimer >3.12 mg/L	0.079	1.082 (0.220, 5.315)	.923
CREA >95 μmol/L	1.582	4.866 (1.011–23.415)	.048
BUN >6.9 μmol/L	1.252	3.499 (0.730–16.781)	.117
Constant values	−6.515	0.001	<.001

Bold values indicate a statistical difference P < 0.05.

BUN, blood urea nitrogen; CI, credible interval; CREA, creatinine; CRP, C-reactive protein; NEUT, neutrophil; NRS, nutritional risk score; OR, odds ratio; WBC, white blood cell.

Analysis for EBR in ITIN cases

The 57 AMI patients diagnosed with ITIN were categorized into the EBR group and control group based on the extent of bowel resection, comprising 29 and 28 patients, respectively. The comparisons of surgical characteristics and postoperative recovery outcomes between the EBR and control group were conducted. Compared to the control group, EBR significantly increased the likelihood of requiring enterostomy (P = .001), blood transfusion (P = .002), and transfer to intensive care unit (ICU) (P = .016), while also prolonging the recovery time for intestinal function (P = .014) (Table 3).

Table 3.

The Comparison of Surgical Characteristics and Postoperative Recovery Outcomes Between the Extensive Bowel Resection and the Control Group

	Total (n = 57)	EBR group (n = 29)	Control group (n = 28)	P
Length of bowel resection (cm)	116 (65, 200)	200 (155, 247)	65 (32, 82)	<.001
Intraoperative blood loss (mL)	200 (100, 350)	200 (200, 500)	200 (100, 300)	.095
Fistulization				.001
Absence	36 (63.2)	12 (41.4)	24 (85.7)
Presence	21 (36.8)	17 (58.6)	4 (14.3)
Blood transfusion				.002
Absence	25 (43.9)	7 (24.1)	18 (64.3)
Presence	32 (56.1)	22 (75.9)	10 (35.7)
Transferred to ICU				.016
Absence	11 (19.3)	2 (6.9)	9 (32.1)
Presence	46 (80.7)	27 (93.1)	19 (67.9)
Postoperative exhaust time (days)	5 (4, 7)	6 (5, 8)	5 (4, 6)	.014
Postoperative hospital stay (days)	15 (10, 21)	16 (12, 23)	14 (9, 19)	.218
Mortality				1.000
Absence	53 (93.0)	27 (93.1)	26 (92.9)
Presence	4 (7.0)	2 (6.9)	2 (7.1)

Bold values indicate a statistical difference P < 0.05.

Data are reported as numbers (percentage), or the median (IQR).

EBR, extensive bowel resection; ICU, intensive care unit.

Further analysis was conducted to explore the risk factors associated with EBR in patients with ITIN. The results of univariate analyses indicated that the occlusion site and its characteristics (P = .029), preoperative levels of serum CRP (P = .003), CREA (P < .001), and BUN (P < .001) were significant predictive factors for EBR (Table 4). ROC curves of serum CRP, CREA, and BUN were drawn to determine the cutoff values. Subsequently, the occlusion site and characteristics, serum CRP >15 mg/L, CREA >100 μmol/L, and BUN >9.2 μmol/L were included in the multivariate logistic regression analysis, and serum CRP >15 mg/L (OR = 38.023, P = .006), and CREA >100 μmol/L (OR = 6.248, P = .035) were proved to be independently associated with EBR for ITIN cases (Table 5).

Table 4.

Univariate Analysis of Risk Factors for Extensive Bowel Resection (≥100 cm) in Irreversible Transmural Intestinal Necrosis

	Total (n = 57)	EBR group (n = 29)	Control group (n = 28)	P
Demographic characteristics
Gender				.612
Male	41 (71.9)	20 (69.0)	21 (75.0)
Female	16 (28.1)	9 (31.0)	7 (25.0)
Age (years)				.503
≤60	30 (52.6)	14 (48.3)	16 (57.1)
>60	27 (47.4)	15 (51.7)	12 (42.9)
BMI (kg/m²)				.218
≤28	45 (78.9)	21 (72.4)	24 (85.7)
>28	12 (21.1)	8 (27.6)	4 (14.3)
Smoking history				.631
Absence	39 (68.4)	19 (65.5)	20 (71.4)
Presence	18 (31.6)	10 (34.5)	8 (28.6)
Drinking history				.940
Absence	43 (75.4)	22 (75.9)	21 (75.0)
Presence	14 (24.6)	7 (24.1)	7 (25.0)
Important comorbidities				.704
Absence	15 (26.3)	7 (24.1)	8 (28.6)
Presence	42 (73.7)	22 (75.9)	20 (71.4)
Anemia				.248
Absence	43 (75.4)	20 (69.0)	23 (82.1)
Presence	14 (24.6)	9 (31.0)	5 (17.9)
Hypoalbuminemia				.145
Absence	23 (40.4)	9 (31.0)	14 (50.0)
Presence	34 (59.6)	20 (69.0)	14 (50.0)
NRS 2002 score				1.000
<3	4 (7.0)	2 (6.9)	2 (7.1)
≥3	53 (93.0)	27 (93.1)	26 (92.9)
Disease characteristics
Occlusion site and characteristics				.029
MAE	19 (33.3)	14 (48.3)	5 (17.9)
MAT	3 (5.3)	2 (6.9)	1 (3.6)
MVT	35 (61.4)	13 (44.8)	22 (78.6)
Disease course (hours)	72 (24, 228)	96 (60, 168)	60 (24, 258)	.557
Preoperative length of stay (days)	17 (8, 31)	21 (11, 31)	16 (7, 31)	.512
Preoperative anticoagulation or thrombolysis				.839
Absence	40 (70.2)	20 (69.0)	20 (71.4)
Presence	17 (29.8)	9 (31.0)	8 (28.6)
Intestinal obstruction				.236
Absence	26 (45.6)	11 (37.9)	15 (53.6)
Presence	31 (54.4)	18 (62.1)	13 (46.4)
Gastrointestinal hemorrhage				.839
Absence	40 (70.2)	20 (69.0)	20 (71.4)
Presence	17 (29.8)	9 (31.0)	8 (28.6)
Ascites				.274
Absence	8 (14.0)	2 (6.9)	6 (21.4)
Other types ascites	38 (66.7)	21 (72.4)	17 (60.7)
Hemorrhagic ascites	11 (19.3)	6 (20.7)	5 (17.9)
Peritonitis				.954
Absence	9 (15.8)	4 (13.8)	5 (17.9)
Presence	48 (84.2)	25 (86.2)	23 (82.1)
Intestinal diameter (cm)	2.68 ± 0.59	2.66 ± 0.51	2.70 ± 0.67	.800
Preoperative serological examination
WBC (10⁹/L)	14.65 (11.20, 21.88)	16.11 (10.48, 25.10)	13.92 (11.62, 18.02)	.342
%NEUT	0.88 ± 0.06	0.88 ± 0.07	0.88 ± 0.05	.906
CRP (mg/L)	9.20 (6.20, 15.53)	15.30 (8.07, 18.40)	8.07 (5.89, 9.98)	.003
D-dimer (mg/L)	7.62 (3.58, 14.55)	7.83 (3.85, 18.96)	6.53 (3.45, 12.21)	.507
Fib (g/L)	4.14 (3.35, 5.75)	4.42 (3.36, 6.36)	3.93 (3.27, 5.44)	.303
ALT (U/L)	16.20 (10.45, 29.05)	22.30 (13.90, 30.90)	13.85 (9.60, 28.90)	.180
CREA (μmol/L)	100.40 (67.25, 135.50)	119.70 (91.55, 157.45)	69.65 (61.03, 99.65)	<.001
BUN (μmol/L)	9.22 (5.99, 12.90)	11.59 (8.78, 16.56)	7.03 (5.22, 9.33)	<.001

Bold values indicate a statistical difference P < 0.05.

Data are reported as numbers (percentage), mean ± SD, or the median (IQR).

ALT, alanine transaminase; BMI, body mass index; BUN, blood urea nitrogen; CREA, creatinine; CRP, C-reactive protein; Fib, fibrinogen; MAE, mesenteric artery embolism; MAT, mesenteric artery thrombosis; MVT, mesenteric vein thrombosis; NEUT, neutrophil; NRS, nutritional risk score; SD, standard deviation; WBC, white blood cell.

Table 5.

Multivariate Analysis of Risk Factors Associated with Extensive Bowel Resection (≥100 cm)

Variables	Coefficients	OR (95% CI)	P
Occlusion site and characteristics			.964
MAT versus MAE	0.579	1.785 (0.024–131.911)	.792
MVT versus MAE	0.115	1.122 (0.187–6.722)	.900
CRP >15 mg/L	3.638	38.023 (2.887–500.753)	.006
CREA >100 μmol/L	1.832	6.248 (1.137–34.348)	.035
BUN >9.2 μmol/L	1.217	3.377 (0.647–17.613)	.149
Constant values	−2.368	0.094	.019

Bold values indicate a statistical difference P < 0.05.

BUN, blood urea nitrogen; CREA, creatinine; CRP, C-reactive protein; CI, credible interval; MAE, mesenteric artery embolism; MAT, mesenteric artery thrombosis; MVT, mesenteric vein thrombosis; OR, odds ratio.

Discussion

The main consequences of mesenteric vascular diseases are intestinal ischemia and intestinal necrosis, with sustained intestinal mucosal ischemia (≥6 hours) leading to irreversible damage and necrosis.^4,5,15 The ischemic intestinal tract without necrosis necessitates prompt implementation of conservative or interventional treatment to restore vascular patency. Furthermore, swift removal of the necrotic intestine is crucial in preventing the entry of harmful substances resulting from intestinal necrosis into the systemic circulation after restoration of mesenteric blood supply, as this can exacerbate the systemic inflammatory response and lead to septic shock.^1,16,17 The identification and assessment of necrotic intestinal tracts, as well as the determination of the extent of bowel resection, can pose challenges that are both complex and crucial.

In this study, the presence of ascites, peritonitis, intestinal diameter >2.35 cm, and serum CREA >95 μmol/L were found to be significantly correlated with ITIN. The ischemia of mesenteric blood vessels can result in reduced intestinal activity, compromised or even absent intestinal peristalsis, thereby impacting the morphology and functionality of the digestive tract. The presence of long-term intestinal ischemia or necrosis is often accompanied by a decrease in food intake, significant weight loss, accumulation of intestinal gas, dilation of the intestinal loops, and even obstruction, ultimately resulting in malnutrition and potentially shock.^18–20 In the reversible stage of ischemia, increased permeability of the intestinal wall results in fluid leakage, while in the advanced stages of intestinal necrosis, secondary infection, paralytic ileus, and peritoneal response to ischemic injury may contribute to fluid loss and accumulation of free fluid within the peritoneal cavity.

The occurrence of persistent intestinal ischemia or necrosis in AMI cases leads to a significant influx of fluid into the intestine and abdominal cavity, thereby elevating the risk of malnutrition, hypoalbuminemia, ascites, hypovolemic shock, and susceptibility to abdominal infection.^21,22 In addition, inadequate nutrition, ascites, shock, and other factors can lead to reduced intestinal perfusion, thereby exacerbating the extent of intestinal ischemia and increasing the susceptibility to intestinal necrosis. Irrespective of the type of AMI, intestinal necrosis represents the ultimate stage of disease progression and is typically accompanied by clinical manifestations of peritonitis and hemorrhagic ascites, followed by systemic signs of infection in patients. Serum levels of WBC, %NEUT, and CRP—all markers for inflammation—are frequently elevated to varying degrees.²²

The occlusion site and characteristics, serum CRP >15 mg/L, CREA >100 μmol/L, and BUN >9.2 μmol/L were identified as the potential predictors for EBR. The symptoms of thrombosis are less severe compared to those of arterial embolism.¹⁹ Due to the direct supply of blood and oxygen through the artery, the clinical manifestations of arterial mesenteric vascular embolism are more urgent, increasing the likelihood of extensive intestinal necrosis and necessitating intestinal resection. Although thrombosis of the venous mesenteric vessels may result in intestinal edema, blood stasis, and compromised intestinal perfusion, the disease typically progresses subacutely.

Following venous embolization, sufficient collateral circulation is usually established to compensate for the loss of blood volume; thus, there is seldom an immediate impact on blood circulation in the corresponding organs.^22,23 With accurate diagnosis and prompt intervention before the onset of intestinal necrosis, restoration of intestinal blood flow can reverse intestinal ischemia, thereby mitigating the risk of extensive bowel necrosis and EBR.

The specific indicators of AMI are absent, potentially leading to the manifestation of rebound pain and muscle tension characteristics associated with peritonitis.²⁴ In the early stage of AMI, ischemia and hypoxia induce intestinal constriction and spasms. However, in the late stage, the intestinal tract becomes relaxed and dilated, leading to blood stasis and edema in the intestinal wall. In addition, a significant amount of fluid infiltrates both the intestinal and abdominal cavities. The intervention or intravenous thrombolytic therapy can be implemented at the aforementioned stages to timely restore intestinal blood supply and maintain intestinal viability, although with the potential for evident ischemia-reperfusion injury.^24–26

If intestinal ischemia is not promptly relieved, it can lead to histological necrosis of the bowel, necessitating the performance of bowel resection. If surgery is not performed for intestinal necrosis, the severity and extent of intestinal necrosis will worsen and expand due to infiltration of various inflammatory cells, disruption of capillary integrity, mucosal edema, tissue death, shedding, ulcer formation, as well as muscle and serous membrane necrosis. This can lead to peritonitis and necessitate extensive removal of the intestine.^27–29

In cases of extensive intestinal necrosis, a significant amount of colloidal and crystal fluid exudes, leading to decreased blood volume, electrolyte imbalance, and acid-base disturbances. The combination of inadequate perfusion and absorption of necrotic toxins results in renal injury and dysfunction. The serum levels of CREA and BUN, which are the most crucial biomarkers for assessing renal function, exhibited a significant increase. In addition, extensive enterectomy may result in the development of short bowel syndrome and other consequential complications, necessitating long-term reliance on parenteral nutrition. Therefore, it is particularly crucial to establish a consensus with patients suffering from bowel syndrome before surgery.^29,30

Although we have gathered ample case data on AMI and investigated the associations between demographic, disease, and serological examination characteristics with ITIN and EBR, there are still certain limitations that need to be acknowledged. First, this analysis was conducted using a retrospective database from a single center, which limits the level of evidence. Second, the inclusion of case data spanning a significant time period may introduce information bias. In addition, the clinical incidences of AMI and ITIN (dependent variables) were relatively limited, which had a certain impact on the accuracy of the analysis results.

Subsequently, multicenter, large-scale, and prospective studies with long-term follow-up are needed to validate and augment the findings of this study.

Conclusions

The presence of ascites, peritonitis, intestinal diameter >2.35 cm, and serum CREA >95 μmol/L were independently correlated with ITIN for AMI cases, while serum CRP >15 mg/L and CREA >100 μmol/L independently increased the risk of EBR. The present study identified the risk factors associated with ITIN and EBR in cases of AMI, which could be further applied in clinical practice.

Footnotes

Acknowledgments

We thank all patients whose data were used for the study.

Authors' Contributions

Z.Y.: Conceptualization, Methodology, Software, and Writing-review and editing. X.D.: Data curation, Formal analysis, and Writing—original draft. R.L.: Investigation, Methodology, and Visualization. C.X.: Formal analysis and Visualization. S.Z.: Conceptualization and Supervision. Z.Y.: Formal analysis and Software. Y.G.: Supervision, Methodology, and Writing-review and editing. P.L.: Conceptualization, Project administration, and Writing-review and editing.

Data Availability Statement

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Ethics Approval and Consent to Participate

The retrospective study was reviewed and approved by the Medical Ethics Committee of the First Medical Center of the Chinese PLA General Hospital. As this study does not involve patient intervention, information disclosure, and long-term follow-up, informed consent was not required.

Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

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