Clinical manifestations and imaging features of inferior mesenteric vein-related colon ischemia

Abstract

BACKGROUND

Colon ischemia (CI) is a common disorder with heterogeneous etiology, whereas CI secondary to inferior mesenteric vein (IMV) pathology is rare and presents distinct diagnostic challenges. Delayed diagnosis and inappropriate management may worsen prognosis.

AIM

To explore the clinical characteristics of IMV-related CI and increase awareness of this rare condition.

METHODS

This retrospective case series described 11 IMV-related CI inpatients at Peking Union Medical College Hospital and summarized their clinical characteristics, imaging and endoscopic features, and prognosis. An additional cohort of 29 arterial-related CI patients was included, and univariate analyses were conducted to compare features between arterial- and IMV-related CI patients.

RESULTS

IMV-related CI patients were all male, with a median age of 44.5 (41.5-63.3) years. Tenesmus is a common symptom, occurring in 72.7% of patients. Concurrent venous thrombosis was identified in 5 patients (45.5%). On contrast-enhanced computed tomography, all patients demonstrated continuous thickening of the colonic wall. Vessel opacification defects were observed in 10 patients (90.9%), frequently accompanied by compensatory arterial enlargement (81.8%). Compared with arterial-related CI, IMV-related CI was more frequently associated with rectal involvement (90.9% vs 24.1%, P < 0.001) and luminal stenosis (81.8% vs 27.6%, P = 0.005).

CONCLUSION

IMV-related CI patients have a chronic course, thrombosis comorbidities, and predominant rectal involvement with marked stenosis. Anticoagulation constitutes a cornerstone of therapy.

Key Words: Colon ischemia; Inferior mesenteric vein; Rectum; Diagnose; Anticoagulation

Core Tip: As a rare subtype of colon ischemia (CI), inferior mesenteric vein (IMV)-related CI often presents with nonspecific symptoms that delay diagnosis. In this study, we reviewed 11 cases from our seven-year experience, highlighting the predominance of middle-aged males, chronic disease, rectal irritation, thrombotic comorbidities, and continuous involvement of the sigmoid and rectum. Identifying both direct and indirect signs of IMV lesions on computed tomography is crucial for accurate diagnosis. Comparative analysis with arterial-related CI patients revealed substantial differences, further highlighting the necessity for prompt recognition and early intervention in IMV-related CI patients.

INTRODUCTION

Colon ischemia (CI) represents the most common form of intestinal ischemia. When hypoperfusion occurs, it deprives the bowel of oxygen and nutrients, leading to hypoxia and direct cell death. As the ischemic period progresses, damage spreads from the mucosa to the serosa[1]. CI can present with a wide spectrum of clinical manifestations, ranging from transient lesions to severe forms with high mortality, depending on the underlying etiology and severity. Several classifications of CI have been proposed[2,3]. For example, CI may be classified as spontaneous or iatrogenic. CI is usually categorized into occlusive ischemic diseases, including embolic and thrombotic arterial occlusion as well as mesenteric venous thrombosis (MVT), and nonocclusive diseases due to alterations in systemic circulation and hypoperfusion of the mesenteric microvasculature, based on the underlying pathophysiological mechanisms[4].

Epidemiological data concerning CI remain limited and quite variable. The estimated annual incidence of acute CI is 15.6/100000 patient-years[5]. Both nonocclusive and arterial ischemia are recognized as the most common mechanisms, characterized by the involvement of watershed zones and typically sparing the rectum[6]. In contrast, venous ischemia, particularly related to the large bowel, is less frequently reported. MVT most commonly affects the superior mesenteric vein (SMV), with approximately 11% of cases involving the inferior mesenteric vein (IMV). Although both conditions may result in CI, lesions of the IMV specifically impact the distal gastrointestinal tract[7]. Only a very few case reports have described CI caused by IMV thrombosis and mesenteric arteriovenous fistula[8,9]. Some studies in the surgical field have shown that IMV ligation during colorectal surgery, even if the inferior mesenteric artery is preserved, can lead to CI, potentially affecting the anal-side colon of the anastomosis and extending to the rectum[10,11]. The diagnosis and differential diagnosis of IMV-related CI are always challenging due to its rarity. The delay in diagnosis might lead to a missed optimal timing of medications and cause poor prognosis of colectomy. Based on the experience of one medical center, this study systematically describes the clinical features of IMV-related CI and analyzes the difference in manifestations between IMV-related CI and arterial-related CI.

MATERIALS AND METHODS

Study design and data collection

We searched the admission database at Peking Union Medical College Hospital from January 2016 to July 2023 and used the diagnostic code for CI or portal/MVT. The diagnosis of CI was established through a comprehensive assessment integrating clinical manifestations (abdominal pain, diarrhea, hematochezia), radiographic imaging, endoscopic findings, and histopathology[12]. Patients were included in the IMV-related CI group if they met the following inclusion criteria: (1) The diagnosis of CI was confirmed by two gastroenterologists according to the criteria (Li J and Ruan GC) on the basis of endoscopic and radiological findings; and (2) The demonstration of IMV lesions on contrast-enhanced computed tomography (CT) scans was confirmed by a senior radiologist (Liu W). Patients were excluded based on the following criteria: CI due to large bowel obstruction, idiopathic myointimal hyperplasia of the mesenteric vein, and idiopathic mesenteric phlebosclerosis. Patients lacking in-hospital imaging and endoscopic data were also excluded from the study. CI patients without predisposing shock, with radiological evidence of mesenteric arterial lesions, were enrolled as arterial-related CI (Figure 1).

Figure 1 Flowchart of patients in establishing cohort. CI: Colon ischemia; CT: Computed tomography.

The data included sex, age at diagnosis, and cardiovascular risk factors including history of smoking or alcohol consumption, diabetes, obesity, a history of myocardial infarction or stroke, and hypertension. Comorbidities such as malignancy, medication use, hematological disease, autoimmune disease, previous venous thrombosis events, and liver cirrhosis were also recorded. Clinical manifestations included abdominal signs and symptoms and abnormalities on physical examination. Laboratory, radiologic, and endoscopic examination results were recorded. All radiologic images of IMV-related CI patients were retrospectively reviewed, and the radiologic features, including the location of the involved bowel segment; the appearance and degree of wall thickness and enhancement; the presence of intramural, mesenteric or portal venous gas; mesenteric vessel patency; peritoneal fluid; mesenteric exudation; and the development of collateral vessels, were recorded.

The final diagnosis and the initial medications prescribed were recorded. Follow-up outcomes were determined by reviewing the chart and telephone calls until March 2025. Poor prognosis was defined as clinical deterioration (aggravated hematochezia, perforation, worsening obstruction, or hemodynamic instability) or the need for surgical intervention.

Statistical analysis

Statistical analyses were performed using SPSS version 26.0 software (SPSS, Inc., Chicago, IL, United States). Nonnormally distributed continuous data were reported as median (interquartile range). Categorical variables were reported as n (%). Univariate analysis of categorical variables was performed using a χ² or Fisher test depending on sample size. The Mann-Whitney U test was used for continuous variables. A two-tailed P value less than 0.05 was considered to indicate statistical significance.

RESULTS

Clinical and laboratory findings in IMV-related CI patients

Eleven patients with IMV-related CI were enrolled (Table 1). All were male, with a median age at diagnosis of 44.5 (41.5-63.3) years. All patients had a chronic disease course with a median disease duration of 7 (5-8.5) months. The most common symptoms were weight loss (100%), abdominal pain (81.8%), diarrhea (81.8%), hematochezia (72.7%) and tenesmus (72.7%). Two patients (18.2%) had mild to moderate fever, and 3 (27.3%) had bowel obstruction. Concurrent venous thrombosis, including deep vein thrombosis, pulmonary embolism and internal jugular vein thrombosis, was identified in 5 (45.5%) patients. Abdominal tenderness was noted in 6 patients (54.5%), and abdominal masses were palpable in 3 patients (27.3%). Laboratory investigations revealed elevated D-dimer levels in 81.8% of patients and elevated C-reactive protein levels in 55.6% of patients. Abnormal protein S and antithrombin III levels were observed in 54.5% and 50.0% of the patients, respectively. Tests for antiphospholipid antibodies, lupus anticoagulant, protein C deficiency, and activated protein C resistance yielded no positive results.

Table 1 Clinical data from 11 patients with inferior mesenteric vein-related conditions.

No.	Sex	Age	Disease duration	Chief complaint	Complication	Comorbidity	Endoscopic appearance	Abnormal vessels	Etiology	Treatment	Prognosis
1	Male	62	5 months	Defecation difficulty, abdominal pain	Incomplete intestinal obstruction	PE, DVT; HBP; DM	Involvement of left colon and proximal rectum; multifocal lesions; congestion, edema, fragileness, ecchymosis, patchy erythema, erosion, ulceration, and stricture	IMV	Thrombosis, thrombophilia	Liquid diet, anticoagulation	Symptoms initially improved, but then worsened again, leading to surgery
2	Male	38	9 months	Abdominal pain with mucous bloody stools	Sigmoid colon perforation	PE; portal vein cavernous transformation	Not reach the cecum; involvement of left colon and entire rectum; multifocal lesions; congestion, edema, fragileness, patchy erythema, erosion, ulceration and stricture	SMV, IMV, PV	Thrombosis, thrombophilia	Liquid diet, prednisone, antibiotics	At the onset, inflammatory bowel disease with infection was considered, followed by surgery due to gastrointestinal perforation
3	Male	65	7 months	Diarrhea	None	CHD; DM	Not reach the cecum; involvement of both left and right colon, entire rectum; multifocal lesions; congestion, edema, patchy erythema and stricture	SMV, IMV, PV	Thrombosis	Anticoagulation	Surgery due to poor therapeutic effect
4	Male	63	5 years	Diarrhea	None	Portal vein cavernous transformation with parietal thrombus formation; dilatation of the small intestinal lymphangion	Involvement of entire colon and rectum; multifocal lesions; congestion, edema, and patchy erythema	SMV, IMV, PV	Abdominal tuberculosis	MCT diet; anticoagulation	Partial relief of symptoms
5	Male	60	2 years	Diarrhea	Protein-losing enteropathy	HBP	Not reach the cecum; involvement of left colon and entire rectum; multifocal lesions; congestion, edema, patchy erythema and erosion	IMV	Thrombosis	Liquid diet, anticoagulation, vasodilators	Surgery due to poor therapeutic effect
6	Male	36	5 months	Abdominal pain, mucous bloody stools	Incomplete intestinal obstruction	HBP; acute lymphocytic leukemia treated by allogeneic hematopoietic stem cell transplantation	Not reach the cecum; involvement of left colon and entire rectum; multifocal lesions; congestion, edema, fragileness, patchy erythema, erosion, ulceration and stricture	IMV	Thrombotic microangiopathy	Fasting, anticoagulation, vasodilators	Relief of symptoms
7	Male	69	8 months	Abdominal pain, diarrhea	None	Portal vein cavernous transformation; HBP	Not reach the cecum; involvement of left colon and entire rectum; multifocal lesions; congestion, edema, fragileness, patchy erythema, erosion, and stricture	IMV, PV	Thrombotic microangiopathy	Liquid diet, anticoagulation	Surgery due to poor therapeutic effect
8	Male	72	8 months	Abdominal pain, flatulence and reduced defecation	Incomplete intestinal obstruction	None	Not reach the cecum; involvement of left colon and entire rectum; multifocal lesions; congestion, edema, fragileness, patchy erythema, erosion, and stricture	IMV	Thrombosis	Liquid diet, anticoagulation	Relief of symptoms
9	Male	43	4 months	Abdominal pain and diarrhea	None	PE	Not reach the cecum; involvement of left colon and entire rectum; multifocal lesions; congestion, edema, fragileness, ecchymosis, hemorrhage, patchy erythema, erosion, ulceration, and stricture	IMV	Thrombosis, thrombophilia	Liquid diet, anticoagulation	Relief of symptoms
10	Male	46	7 months	Diarrhea	Hemorrhagic shock	DVT; membranous nephropathy	Not reach the cecum; involvement of both left and right colon, entire rectum; multifocal lesions; congestion, edema, fragileness, ecchymosis, erosion, ulceration, and stricture	SMV, IMV	Thrombosis	Liquid diet	Surgery due to hemorrhagic shock
11	Male	41	3 months	Diarrhea	None	DVT	Not reach the cecum; involvement of left colon and entire rectum; multifocal lesions; congestion, edema, fragileness, patchy erythema, erosion, ulceration, and stricture	SMV, IMV, PV	Thrombosis, thrombophilia	Liquid diet, anticoagulation	Relief of symptoms

PE: Pulmonary embolism; DVT: Deep vein thrombosis; HBP: Hypertension blood pressure; DM: Diabetes mellitus; IMV: Inferior mesenteric vein; SMV: Superior mesenteric vein; PV: Portal vein; CHD: Coronary heart disease; MCT: Medium-chain triglycerides.

Radiological features of IMV-related CI patients

All patients underwent contrast-enhanced CT for evaluation, with involvement extending from the cecum to the rectum. Vascular lesions primarily involved the IMV in all patients, with additional involvement of the SMV (36.4%) and portal vein (45.5%). The most frequently affected segments were the sigmoid colon (100%) and rectum (81.8%). All patients had continuous lesions with bowel wall thickening, ranging from 5.6 mm to 18.2 mm. Decreased enhancement in the arterial phase was noted in 10 patients (90.9%) and in the portal venous phase in 4 patients (36.4%). Intestinal luminal stenosis (81.8%) and the absence of colonic haustration (90.9%) were also common findings. Marked mesenteric exudation was observed in 7 patients (63.6%), and one patient presented with massive ascites. No patient had bowel wall pneumatosis. In terms of the vasculature, thrombus was not directly visualized in any of the patients. Defects in vessel opacification were identified in 10 patients (90.9%), accompanied by compensatory arterial enlargement (9, 81.8%) and collateral circulation formation (8, 72.7%) (Figure 2; Table 2).

Figure 2 Contrast-enhanced computed tomography. A: Diffuse thickening of the rectum and sigmoid colon with reduced enhancement, increased surrounding mesenteric exudation, and formation of collateral circulation, as indicated by the arrows; B: Compensatory enlargement of the inferior mesenteric artery, as indicated by the arrow.

Table 2 Computed tomography features in inferior mesenteric vein-related colon ischemia patients, n (%).

Characteristics	Patients (n = 11)
Involved bowel segments
Terminal ileum	2
Ascending colon	3
Transverse colon	6
Descending colon	8
Sigmoid colon	11
Rectum	9
Continuous lesions	11 (100)
Bowel wall thickening	11 (100)
Maximum thickness (mm), median (interquartile range)	13.5 (11.6-15.6)
Abnormal enhancement	10 (90.9)
Arterial phase
Attenuated	10 (90.9)
Enhanced	0
Unenhanced	1 (9.1)
Portal vein phase
Attenuated	4 (36.4)
Enhanced	1 (9.1)
Unenhanced	6 (54.5)
Luminal stenosis	9 (81.8)
Disappearance of the colonic haustration	10 (90.9)
Mesenteric exudation	10 (90.9)
Pneumatosis	0
Affected vessel
PV	5 (45.5)
SMV	4 (36.4)
IMV	11 (100)
Thrombus/embolus of IMV	0
Vascular opacification defect	10 (90.9)
Collateral circulation	8 (72.7)
Compensatory thickening of the arteries	9 (81.8)

PV: Portal vein; SMV: Superior mesenteric vein; IMV: Inferior mesenteric vein.

Endoscopic findings in IMV-related CI patients

All patients underwent colonoscopic examinations. Nevertheless, due to factors such as intolerance to standard bowel preparation and complete colonic evaluation or the severity of bowel lesions, only 2 patients (18.2%) achieved cecal intubation. Both proximal rectum and sigmoid involvement were observed in all patients, and distal rectal involvement was present in 91.7% of the patients. Continuous lesions were documented in 91.7% of the patients. A crucial aspect of IMV-related CI was stenosis, which was found in 9 patients (81.8%). Ulcers were identified in 6 patients (54.5%), and were predominantly characterized as multiple, irregular, and deep. Additionally, several nonspecific findings included edema (100%), patchy erythema (100%), erosion (81.8%), and enhanced friability (72.7%). Four patients (36.4%) presented with dark purple mucosa (Figure 3). Complete loss of the vascular pattern was observed in all affected areas, and capillary dilation was noted in 3 patients. However, no patient had tortuous veins.

Figure 3 Colonoscopic features of inferior mesenteric vein-related colon ischemia. Continuous lesions characterized by mucosal congestion and edema, with focal dark purple area, nodular changes and irregular ulcers in distal rectum, as indicated by the arrows.

Diagnosis, medication, and prognosis of IMV-related CI patients

The etiologies of IMV lesions were identified as follows: Thrombophilia in 4 patients, portal vein cavernous transformation in 3 patients, intestinal thrombotic microangiopathy in 1 patient, membranous nephropathy in 1 patient, and idiopathic in 2 patients. All IMV-related CI patients initially received conservative medical treatment. Anticoagulant treatment was administered to 10 patients (90.9%), 8 of whom received low-molecular-weight heparin and 2 of whom were treated with new oral anticoagulants (NOACs). Eight patients (72.7%) continued long-term anticoagulant therapy. Two patients showed symptom improvement within 1 week, and 4 patients exhibited a trend toward improvement after 2 weeks of treatment. After 3 months of NOAC therapy without a clinical response, one patient was switched to therapeutic low-molecular-weight heparin, and symptom resolution was achieved within 1 week of regimen modification. Based on the clinical condition of the patients, antibiotics, vasodilators, and other medications were administered. Ultimately, four patients (36.4%) achieved complete symptom resolution. Six patients (54.5%) required surgical intervention. Surgery was performed in four patients attributed to persistent diarrhea, even though overall symptoms remained stable. Two patients required surgery due to gastrointestinal hemorrhage or colon perforation, without anticoagulation.

Comparison of clinical manifestations between IMV-related CI and classical arterial-related CI patients

Compared with 29 patients with arterial-related CI, males had a more prominent predominance of IMV-related CI (100% vs 62.1%, P = 0.019), while there were no significant differences in age at diagnosis among those with IMV-related CI. Patients with IMV-related CI often had a history of drinking (54.5% vs 17.2%, P = 0.042). IMV-related CI tended to follow a chronic course (100% vs 55.2%, P = 0.007), which was often accompanied by symptoms of tenesmus (72.7% vs 24.1%, P = 0.009) and a higher incidence of concurrent thrombotic events (45.5% vs 10.3%, P = 0.025).

Laboratory examination revealed that the D-dimer level was slightly greater in patients with IMV-related CI, although this difference did not reach statistical significance. Elevated myoglobin levels were observed in 3 arterial-related CI patients, whereas all IMV-related CI patients demonstrated normal muscle enzyme levels. Imaging revealed intestinal wall thickening occurred in both groups. IMV-related CI was associated with significantly increased odds of opacification defects of affected veins and the establishment of collateral circulation (P < 0.001).

Endoscopically, patients with arterial- and venous-related disease both presented with continuous lesions, whereas clear margins were more frequently observed in arterial-related CI patients (P = 0.037). Compared with arterial-related CI patients, IMV-related CI patients had a significantly lower success rate of cecal intubation (18.2% vs 62.1%, P = 0.031). Compared with arterial-related CI patients, IMV-related CI patients demonstrated a greater prevalence of rectal involvement, especially in the distal rectum (90.9% vs 24.1%, P < 0.001). Additionally, luminal stenosis was more prevalent in IMV-related CI patients (81.8% vs 27.6%, P = 0.005), with a likelihood of severe stenosis precluding endoscope passage (P = 0.369). In terms of prognosis, patients with IMV-related CI were more likely to have a poor prognosis, but the difference was not statistically significant (54.5% vs 20.7%, P = 0.056; Table 3).

Table 3 Comparison of clinical characteristics of inferior mesenteric vein-related and arterial-related colon ischemia, n (%)/median (interquartile range).

Parameter	IMV-related CI (n = 11)	Arterial-related CI (n = 29)	P value
Sex (male)	11 (100)	18 (62.1)	0.019
Age (years)	44.5 (41.5-63.3)	66 (59.5-74)	0.064
Course (chronic)	11 (100)	16 (55.2)	0.007
HBP	4 (36.4)	12 (41.4)	1.000
CHD	1 (9.1)	4 (13.8)	1.000
DM	2 (18.2)	5 (17.2)	1.000
Smoking	5 (45.5)	9 (31.0)	0.469
Drinking	6 (54.5)	5 (17.2)	0.042
Abdominal pain	9 (81.8)	25 (86.2)	1.000
Diarrhea	9 (81.8)	22 (75.9)	1.000
Hematochezia	8 (72.7)	24 (82.8)	0.660
Tenesmus	8 (72.7)	7 (24.1)	0.009
Fever	1 (9.1)	12 (41.4)	0.068
Concurrent thrombosis	5 (45.5)	3 (10.3)	0.025
Emergency surgery	0	3 (10.3)	0.543
Poor prognosis	6 (54.5)	6 (20.7)	0.056
Laboratory test
WBC (× 109/L)	5.23 (4.07-6.37)	6.17 (4.62-8.36)	0.196
Hb (g/L)	130 (125-140)	111 (100-142)	0.175
Alb	36.0 (33.0-37.5)	35.0 (31.0-31.0)	0.473
hsCRP (mg/L)	9.96 (1.33-25.6)	15.9 (1.97-52.3)	0.664
ESR (mm/hour)	20.0 (9.00-36.8)	20.0 (18.0-44.0)	0.332
D-dimer (mg/L)	1.51 (0.89-3.15)	0.81 (0.49-2.50)	0.701
CT
Thickening	11 (100)	21 (72.4)	0.080
Stenosis	5 (45.5)	5 (17.2)	0.103
Dilation	1 (9.1)	3 (10.3)	1.000
Thrombus	0	1 (3.4)	1.000
Vascular opacification defect	8 (72.7)	0	< 0.001
Collateral circulation	9 (81.8)	2 (6.9)	< 0.001
Endoscopy
Cecum intubation	2 (18.2)	18 (62.1)	0.031
Right colon	4	16	1.000
Descending colon	4	20	0.596
Sigmoid colon	11	21	0.159
Proximal rectum (or upper rectum)	11	15	0.004
Distal rectum (or lower rectum)	10	7	< 0.001
Continuous lesions	10 (90.9)	21 (72.4)	0.399
Clear margins	0	12 (41.4)	0.017
Congestion and edema	11 (100)	29 (100)
Fragile	8 (72.7)	14 (48.3)	0.286
Ecchymosis, hematoma	2 (18.2)	2 (6.9)	0.300
Hemorrhage	1 (9.1)	1 (3.4)	0.479
Erosion	9 (81.8)	22 (75.9)	1.000
Stenosis	9 (81.8)	8 (27.6)	0.005
Endoscope unable to pass	3 (27.3)	4 (13.8)	0.369
Ulceration	6 (54.5)	18 (62.1)	0.727
Multifocal	5	16	1.000

IMV: Inferior mesenteric vein; CI: Colon ischemia; HBP: Hypertension blood pressure; CHD: Coronary heart disease; DM: Diabetes mellitus; WBC: White blood cell; Hb: Hemoglobin; Alb: Albumin; hsCRP: High-sensitivity C-reactive protein; ESR: Erythrocyte sedimentation rate; CT: Computed tomography.

DISCUSSION

IMV-related CI is quite rare and easily misdiagnosed. This study systematically described the clinical characteristics of IMV-related CI patients and revealed a predominance of middle-aged males, a chronic disease duration, rectal irritation symptoms, a high prevalence of thrombotic comorbidities, and continuous involvement of the sigmoid and rectum. Recognizing both the direct and indirect findings of IMV lesions on CT was pivotal for the diagnosis of IMV-related CI. The most common etiology was thrombophilia, and anticoagulation was the primary medication choice. Delayed diagnosis and anticoagulation resulted in poor prognosis. Furthermore, compared with arterial-related CI, IMV-related CI was associated with a greater likelihood of distal rectum involvement, a greater prevalence of colon stenosis, and less pronounced clear margins.

The epidemiology and demographic data concerning venous-related CI, especially IMV-related CI, are limited. In contrast to previous epidemiological patterns in CI, which revealed a female predominance and an advanced mean age of 65 years[5,13], our findings demonstrated significant demographic divergence, with a male predominance and a mean age of 56 years, which is consistent with the features of MVT[7]. As a vascular disorder, CI has previously been found to be associated with risk factors commonly linked to vascular lesions, such as advanced age, diabetes mellitus, and hypertension[4]. However, these features were not prominently observed in IMV-related CI patients. The patients always exhibit local intra-abdominal factors, as well as inherited or acquired thrombophilia, which aligns with the significant proportion of concomitant venous thromboembolic events observed in our cohort[14-16].

Most of the patients in this study exhibited a chronic course. However, previous studies have indicated that chronic MVT comprises merely 20%-40% of MVT cases. This discrepancy may be attributed to the fact that MVT, predominantly involving the SMV, prefers acute small bowel pathology, which was not included in our study. The colonic circulation primarily drains into the IMV, and IMV involvement accounts for only 0% to 11% of cases of MVT[7]. CI can manifest nonspecifically as various degrees of abdominal pain, diarrhea, and hematochezia. Notably, we identified significant pronounced rectal irritative symptoms, which was consistent with radiological evidence of a prominent rectal lesion. A chronic course may lead to weight loss, and a limited subset of patients may progress to a critical state due to hemorrhage or perforation. Additionally, a subset of patients with MVT present features of portal hypertension or remain asymptomatic, as detected incidentally on abdominal imaging.

Laboratory evaluation is integral to the process of diagnosis and etiological screening. As in other thrombosis diseases, D-dimer is regarded as a routine biomarker. Several studies have reported that D-dimer levels are helpful for diagnosing or indicating transmural injury in acute MVT patients[17]. However, D-dimer is a fibrin degradation product, and its level depends on the timing of the test and the severity and duration of ischemia. The diagnostic utility of D-dimer for acute mesenteric ischemia exclusion demonstrates limited generalizability to chronic intestinal ischemia populations[15]. Similarly, elevated D-dimer levels were not significantly relevant in our cohort, which may be attributed to the predominantly chronic disease course rather than the acute phase. No biomarker has yet been shown to be sensitive or specific enough to establish or exclude a chronic CI diagnosis. Testing for genetics can be conducted to exclude hereditary etiology.

Splanchnic vein thrombosis primarily affects the portal vein and mesenteric vein[18]. Venous drainage largely parallels the arterial supply. Veins from the right colon converge into the SMV, and the left colon drains into the IMV. The superior rectal vein drains the upper two-thirds of the rectum into the IMV, and the lower third is drained by the middle and inferior rectal veins into the internal iliac veins[19]. The IMV usually appears slender and has great individual variation. The diagnostic hallmark of CI venous occlusion is intravascular thrombosis, with a finding of luminal filling defects[20], albeit a rare observation. Indirect signs, such as suboptimal opacification of the mesenteric vein and the formation of collateral circulation for vein drainage, suggesting a chronic course, are more common. Bowel wall thickening is often prominent. A meta-analysis revealed that in the venous-related acute mesenteric ischemia subgroup, decreased or absent bowel wall enhancement was significantly related to transmural intestinal necrosis, reflecting impaired bowel wall perfusion and irreversible damage[21].

Endoscopy serves as a pivotal diagnostic tool in CI patients. Endoscopic lesions of arterial-related CI typically include continuous changes with descending colon or sigmoid colon involvement, with nonspecific presentations, including congestion, edema, ulceration, and erosion[22]. In addition to the similarities in endoscopic findings, two major features of venous-related CI were identified in this study and compared with those of arterial-related CI. First, in contrast to the conventionally recognized pattern in which arterial-related CI typically spares the rectum, IMV-related CI has a propensity to affect the rectum. Despite the dural blood supply of the rectum, the middle and distal rectal vein might not be able to compensate for thrombosis or obliteration of the IMV. The exact pathogenesis underlying this distinctive involvement remains elusive. Second, stenosis emerged as a significant clinical manifestation. Moreover, only a limited number of patients with IMV-related CI were able to undergo a complete colonoscopy. Relying solely on colonoscopic evaluation poses an impediment to gauging the full extent of ischemic injury. The specific pathohistological manifestations are ghost cells and mucosal ischemia; however, the positivity rate in endoscopic and surgical specimens is low[23].

For management, therapeutic decisions hinge on the detection of peritoneal signs, which may necessitate emergent surgical intervention. After the exclusion of acute abdomen, anticoagulation therapy is considered the first-line treatment for acute MVT or the exacerbation of chronic MVT[24]. Consequently, pharmacotherapy was the initial treatment modality in our cohort. The widely accepted approach involves initial anticoagulation with unfractionated heparin or low-molecular-weight heparin[25]. Despite the advantages of oral administration and absence of necessity of strict laboratory monitoring, the use of NOACs remains controversial. Low-molecular-weight heparin appeared more effective in certain patients, likely due to enhanced antithrombin-mediated inhibition of activated factor Xa, providing a broad-spectrum anticoagulant effect[26]. Clinical responses are heterogeneous, necessitating prompt formulation adjustments when required. The optimal anticoagulation duration lacks consensus, although a minimum anticoagulation duration of 3-6 months is recommended. Lifelong anticoagulation may be warranted in individuals with an irreversible hypercoagulable state[27]. Two patients did not receive anticoagulation therapy in time, and both experienced poor clinical outcomes. We also observed that compared with the more rapid alleviation observed in arterial-related cases, IMV-related CI tended to result in a delayed response to therapy. Missed cases can yield irreversible and even fulminant disease that may necessitate surgical resection.

CI is generally associated with a milder course than small bowel ischemia because of several protective mechanisms[28]. Previously, CI was considered a relatively benign and self-limiting condition, with symptoms resolving within 2-3 days and mucosal healing occurring within 1-2 weeks. However, this perspective is contingent upon the assumption that CI results from a transient disruption in arterial blood flow. One patient was diagnosed with SMV thrombosis at another hospital. Upon admission to our hospital, imaging revealed resolution of the thrombus, but signs of ischemia, such as intestinal wall thickening, still presented. The prognosis of IMV-related CI patients is influenced by the rapidity of thrombus formation, as well as the extent and location of vascular involvement[29]. With respect to acute events, the lack of well-developed collateral circulation results in severe clinical presentations. Conversely, in subacute or chronic MVT patients, while venous obstruction may precipitate ischemia, the development of robust collateral circulation may mitigate the onset of ischemic injury. Nevertheless, a significant proportion of these patients ultimately receive surgical intervention for exacerbation or persistence of symptoms throughout the long-term disease course. This may correlate with the presence of irreversible tissue lesions.

Owing to its rarity and limited knowledge, this study represents the first comprehensive attempt to summarize the clinical characteristics of CI lesions caused by IMV-related diseases. Moreover, we excluded congenital vascular malformations and idiopathic mesenteric phlebosclerosis[30,31], whose disease behavior differed from that of our IMV-related CI patients. This study has several limitations. As a comprehensive tertiary hospital, the inpatients enrolled potentially had more complex comorbidities and severe conditions than those from another hospital. With an increase in clinical awareness of this condition, multicenter cohorts should be included to validate these findings.

CONCLUSION

As a rare subtype of CI, IMV-related CI shows different disease behaviors. Tenesmus, a high prevalence of thrombosis comorbidities, rectum involvement and stenosis under endoscopy, and indirect signs of IMV lesions contributed to the early diagnosis of IMV-related CI. Revealing the etiology of IMV lesions and appropriate anticoagulation is fundamental for protecting against poor prognosis.