key: cord-0960321-hisk4x70
authors: Ojha, Vineeta; Mani, Avinash; Mukherjee, Aprateem; Kumar, Sanjeev; Jagia, Priya
title: Mesenteric ischemia in patients with COVID-19: an updated systematic review of abdominal CT findings in 75 patients
date: 2021-11-10
journal: Abdom Radiol (NY)
DOI: 10.1007/s00261-021-03337-9
sha: 4018ccaff907aacbcd115a0c2f92d404892dd4d5
doc_id: 960321
cord_uid: hisk4x70

BACKGROUND: Acute mesenteric ischemia (AMI) is a less common but devastating complication of COVID-19 disease. The aim of this systematic review was to assess the most common CT imaging features of AMI in COVID-19 and also provide an updated review of the literature on symptoms, treatment, histopathological and operative findings, and follow-up of these patients. METHODS: A systematic literature search of four databases: Pubmed, EMBASE, WHO database, and Google Scholar, was performed to identify all the articles which described abdominal CT imaging findings of AMI in COVID-19. RESULTS: A total of 47 studies comprising 75 patients were included in the final review. Small bowel ischemia (46.67%) was the most prevalent abdominal CT finding, followed by ischemic colitis (37.3%). Non-occlusive mesenteric ischemia (NOMI; 67.9%) indicating microvascular involvement was the most common pattern of bowel involvement. Bowel wall thickening/edema (50.9%) was more common than bowel hypoperfusion (20.7%). While ileum and colon both were equally involved bowel segments (32.07% each), SMA (24.9%), SMV (14.3%), and the spleen (12.5%) were the most commonly involved artery, vein, and solid organ, respectively. 50% of the patients receiving conservative/medical management died, highlighting high mortality without surgery. Findings on laparotomy and histopathology corroborated strikingly with CT imaging findings. CONCLUSION: In COVID-19 patients with AMI, small bowel ischemia is the most prevalent imaging diagnosis and NOMI is the most common pattern of bowel involvement. Contrast-enhanced CT is a powerful decision-making tool for prompt diagnosis of AMI in COVID-19, thereby potentially improving time to treat as well as clinical outcomes. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00261-021-03337-9.

Mesenteric ischemia in paƟents with COVID-19 Ojha et al; 2021 • 47 studies, 75 paƟents • Small bowel > large bowel • Non-occlusive mesenteric ischemia is common. • SMA, SMV and spleen are most commonly involved artery, vein and solid organ, respecƟvely.

Coronavirus disease-2019 (COVID-19) pandemic has caused an ongoing global health crisis. Initially believed to affect primarily the respiratory tract, this disease is now known to cause multiorgan involvement [1, 2] . Thromboembolic complications, in both arterial and venous systems, are being increasing recognized in patients with COVID-19 infection [3, 4] . Arterial thromboses described in patients with COVID-19 include acute coronary syndrome, stroke, acute mesenteric ischemia (AMI), and acute limb ischemia [3, [5] [6] [7] . Due to the high incidence of micro-and macrovascular involvement in COVID-19, it has also been suggested that all hospitalized COVID-19 patients should get thromboembolism prophylaxis and should undergo routine monitoring of the coagulation profile [8] . AMI is a devastating complication with a very high mortality rate (~ 60 to 80%), which increases proportionately with increasing time to diagnose and treat this condition [9] . Patients with AMI in COVID-19 may present with varied symptoms ranging from abdominal pain, diarrhea, nausea, and vomiting to abdominal distension. Due to low specificity of symptoms and laboratory tests, imaging is the mainstay for diagnosis of AMI. Prompt diagnosis and immediate treatment are imperative to prevent mortality in these patients [10] . Although abdominal radiographs and ultrasonography are readily available modalities, they have low sensitivity and specificity for the diagnosis of AMI. CT is the first-line imaging modality and has replaced catheter angiography, which is now primarily reserved for the endovascular management of this condition [11] .

It is important for the clinicians and the radiologists to identify this abnormality early on CT to allow timely management and improve outcomes. However, the literature on AMI in patients with COVID-19 is heterogeneous and scattered. There is lack of a comprehensive systematic compilation of the data available in the literature pertaining to the CT imaging findings, management, laparotomy and histopathological findings, and outcomes in patients COVID-19 infection complicated by AMI. To our knowledge, this is the largest systematic review compiling data from the available literature on AMI in COVID-19 till date.

We aimed to perform a narrative synthesis of the abdominal CT findings in patients with confirmed COVID-19 infection (on RT-PCR) who had mesenteric ischemia. The search strategy followed Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) checklist [12] . The study was registered with PROSPERO (CRD42021259511). An electronic search of four databases including Pubmed, Google scholar, Embase, and WHO library was performed on June 19, 2021, using the keywords "covid," "covid-19," "coronavirus," "SARS-CoV-2," "2019-nCoV," "n-CoV," "bowel ischemia," "mesenteric ischemia," "intestinal ischemia," "abdominal pain," "ischemic enteritis," and "ischemic colitis", interspersed with Boolean operators "OR" and "AND." The search was limited to articles published in 2020 and 2021. We carried out thorough additional search of the reference lists of the extracted articles to find out other potentially relevant articles. Duplicates were removed.

Our inclusion criteria included case reports or series involving patients with confirmed COVID-19 infection (on RT-PCR) diagnosed with mesenteric ischemia on imaging/surgery/biopsy, who underwent at least one abdominal CT scan. Other inclusion criteria were articles published in English, studies conducted on humans, and with extractable full text without any restriction applied to country of research. We excluded reviews, expert opinions, editorials, patients with presumed COVID-19 infection (without RT-PCR confirmation), and preprints. The titles and the abstracts of the included studies were screened by two independent reviewers based on the above criteria and any disagreements were resolved either by mutual consensus or by the senior author, if needed.

All the studies were rated for their quality according to the National Institutes of Health (NIH) Quality Assessment Tool for Case Series Studies, by two independent reviewers [13] . Due to rarity of this entity, most of the included studies were either case reports or very small series of patients.

After thorough scrutiny of full texts of the articles included in the initial review based on the inclusion criteria, we shortlisted the final list of the articles to be included in the systematic review. Further, data extraction was done by two independent reviewers from the full text of the articles into a Microsoft Excel database using the following fields: author, country, number of patients, demographics, clinical presentation, abdominal CT findings, details of treatment, and follow-up. For extracting the relevant granular data, we used various subfields like serum levels of acute phase reactants, type of bowel wall involvement, and distribution of the abdominal CT findings across various segments of bowel and types of vessels involved. We also extracted the laparotomy and histopathological findings in the included studies to compare with imaging findings. Any discrepancies were resolved by mutual consensus. Data were analyzed using Microsoft excel and a narrative synthesis of the findings (synthesis without meta-analysis (SWiM)) was conducted.

Due to substantial heterogeneity within the data, the assessment of the major abdominal CT findings was done according to the standard definition of AMI [11] . As per the definition, AMI is thought to be caused by mesenteric arterial thrombosis (MAT), mesenteric arterial embolism (MAE), mesenteric venous thrombosis (MVT), or non-occlusive mesenteric ischemia (NOMI). The following signs on abdominal CT were considered to be suggestive of AMI: bowel wall thickening (edema, hemorrhage), high attenuation of bowel wall (hemorrhagic infarct), hyperenhancement (congestion), hypoenhancement (hypoperfusion), filling defect in the mesenteric arteries or veins, wall thinning, ileus and dilatation of the bowel wall, pneumatosis, portomesenteric venous gas, and free peritoneal gas [3] .

Five hundred and seven unique articles were identified after initial search of the four databases (Fig. 1) . Out of these, 88 articles met the criteria for full-text review after initial screening. After scrutiny of these 88 articles, 47 articles which met the inclusion criteria qualified to be included in the final analysis. The demographic information about the population is given in Table 1 . In 47 studies, a total of 75 patients underwent abdominal CT scans, excluding the follow-up scans which are described later. Most of the studies were case reports (Supplementary Table 1 ). The methodologic quality of the studies, which was assessed using the NIH Quality Assessment Tool for Case Series/Reports, was fair for most of the studies indicating limited and low-quality data available in the literature pertaining to abdominal CT findings (Supplementary Table 2 ).

Pooled incidence of various imaging findings and their distributions as inferred from the abdominal CT scans is described in Table 2 . The compilation of presenting symptoms, serology, and imaging findings as mentioned in the individual studies is given in Table 3 . Abdominal pain was the most common presenting symptom. The duration between positive RT-PCR and abdominal symptom onset (range 0 to 48 days) varied widely across the studies (Table 3) . Small bowel ischemia (41/75; 46.67%) was the most prevalent abdominal CT finding in patients with mesenteric ischemia. This was followed by large bowel ischemia (ischemic colitis) in 37.3% (28/75), arterial thrombi in 25% (17/68), and venous involvement in 20.6% (13/63). The less common findings were solid organ ischemia (12/63; 19%) , ascites (8/45; 17.7%), pneumoperitoneum (6/53; 11.3%), and gastric ischemia (1/75; 1.3%) ( Table 2, Figs. 2, 3) .

Among the patients who had identifiable bowel abnormalities on CT, non-occlusive mesenteric ischemia (NOMI) (36/53; 67.9%) was the most common pattern. Mural thickening and bowel wall edema were seen in 50.9% patients (27/53) . While bowel hypoperfusion and dilatation were seen in 20.7% (11/53) each, pneumatosis and signs of perforation in the bowel wall were seen in 16.9% (9/53) and 11.3% (6/53), respectively. Mucosal hyperenhancement and small intestinal obstruction were rare findings (1 patient each) ( Table 2 ).

Radiological signs of bowel ischemia, when present, were most commonly seen in the ileum and colon with equal frequency (17/53; 32.07% each), followed by the jejunum (7/53; 13.2%). Most studies did not specify the segment of the ileum or colon involved. Among the ones which described segmental involvement, distal ileum and ascending colon were more commonly involved than proximal ileum and descending colon, respectively. Involvement of cecum and rectum was rare ( Table 2 ).

Among the studies which described the distribution of arterial thrombi in patients with imaging features of AMI, superior mesenteric artery (SMA) (17/68; 24.9%) was most commonly involved, followed by aorta (6/68; 8.8%). Concomitant lower limb arterial thrombus was seen in 2 patients (5.4%). Among the aortic segments, descending thoracic 

Splenic infarct (8/64; 12.5%) was the most common associated imaging finding in COVID-19 patients with mesenteric ischemia, followed by renal infarct and mesenteric edema (4/64; 6.25% each). Various other rare imaging findings included associated pulmonary thromboembolism, portal venous gas, portal cavernoma, necrotizing pancreatitis, and myocardial infarct.

There was wide heterogeneity in the studies reporting various acute phase reactants. Pooled incidences as well as final outcomes in these patients are described in Table 4 Table 5 describes the frequency of treatment provided and the final outcomes, when described across the included studies (detailed description in 

Detailed description of the treatment provided, laparotomy and histopathological findings, outcomes, and follow-up is provided in Table 6 . Laparotomy findings were described in 31 patients. All the patients with diagnosis of mesenteric ischemia on imaging showed signs of bowel ischemia on laparotomy ranging from bowel necrosis, gangrene, and distension to pallor and yellowish discoloration. SMA thrombus was seen at laparotomy in 2 patients, who also had the same finding on CT. Signs of bowel perforation were seen in 6 patients at laparotomy, 5 of whom had such signs on imaging like pneumoperitoneum and abdominal collections ( Table 6 , Fig. 2 ). Histopathological findings were described for a total of 20 patients (Table 6 ). All the patients, radiologically diagnosed with mesenteric ischemia, showed various signs of bowel wall ischemia ranging from bowel wall necrosis, inflammation, or hemorrhages. Of note, 6 patients were seen to have microvascular thrombi, all of whom had no major vascular abnormalities on imaging. Arterial thrombus was seen in 2 patients, who were also seen to have arterial (SMA) thrombus on imaging. Mesenteric venous thrombus was seen in 5 patients, 4 of whom were seen to have mesenteric venous abnormality on imaging. No mesenteric vascular abnormality was seen in 5 patients, confirmed to have normal vessels on CT as well. Pneumatosis was seen in 1 patient on histopathology, who also had pneumatosis on imaging. 3 patients showed histopathological findings suggestive of direct SARS-CoV-2 viral involvement of the bowel mucosa, with 1 having cytological changes suggestive of viral inclusion bodies in the epithelial cells, second with viral clusters in bowel enterocyte, and the third with positive RNA ISH assay for SARS-CoV-2 ( Table 6 , Fig. 3 ).

The studies which described findings on follow-up CT are detailed in Table 7 . 4 studies showed signs of progression. While 1 study with ascending colon involvement at baseline showed with progressive involvement of descending colon on follow-up, 1 study with only SMV and PV thrombus at baseline showed frank bowel infarction at follow-up. 1 study with spleno-portal thrombosis at baseline developed liver, mesenteric, and splenic ischemia at follow-up. A patient treated endovascularly for SMA thrombus showed fully patent SMA at follow-up.

Abdominal CT may depict wide range of imaging findings of mesenteric ischemia caused due to COVID-19 infection. In this systematic review, we have cohesively compiled the data from the literature regarding the common and uncommon imaging findings of mesenteric ischemia in patients with COVID-19 as deciphered on abdominal CT. Since, most studies were case reports or series with fair quality, there is a potential risk of bias. However, this bias is unavoidable due to scarcity of data on this potentially important topic in the literature. Although, most of the data are non-blinded, descriptive, and preliminary, we aimed to describe the imaging findings, treatment, and outcomes in these patients and the shortcomings were not sufficient to invalidate our findings. On pooled analysis, small bowel ischemia (46.67%) was the most prevalent abdominal CT finding among the 75 patients diagnosed with mesenteric ischemia in COVID-19, although ischemic colitis was more prevalent diagnosis in two largest series included [7, 14] . Arterial thrombi (25%) were more commonly seen than venous thrombi (20.6%), a finding similar to the general population with AMI [11] . The most common pattern of bowel involvement in our study was NOMI (67.9%). This is in contrast to the more accepted theory that MAT is the most common cause of AMI (40-50%) in general population and the incidence of NOMI in AMI is ~ 20% [9] . This finding in our study of COVID-19 patients may be related to the increasing consensus that microvascular obstruction may be a more prevalent mechanism of AMI in these patients, who may not show occlusive thrombi in big mesenteric vessels. Although the exact pathophysiological mechanism behind the causation of AMI in COVID-19 is not known, four putative mechanisms acting in varying combinations are described [4, 15] . Firstly, a hypercoagulable state due to systemic inflammatory response, immobilization, and hypoxia may lead to mesenteric vascular thrombosis, consistent with our findings of arterial, mesenteric, and portal venous thrombosis. However, conclusive demonstration of large mesenteric vessel (arterial or venous) thrombosis is limited in literature. Preliminary pathological studies have demonstrated bowel necrosis with microvascular thrombosis in the submucosal arterioles, thereby pointing toward an in situ thrombosis of mesenteric microvasculature rather than a thromboembolic event resulting from an upstream thrombus [7] . Indeed, microvascular thrombi were seen on histopathology in 6 patients who did not have vascular abnormality on CT in our study. Secondly, severe COVID-19 pneumonia is also associated with hemodynamic compromise (shock) which may lead to NOMI, often compounded by the use of vasopressors in the critical patients. These two mechanisms together may explain high prevalence of NOMI in our study. Also, most patients in our series were Intensive Care Unit (ICU) patients. Various groups, for this reason, have also suggested that when a chest CT is done in ICU patients to rule out pulmonary thromboembolism, the scan may be extended to abdomen to rule out AMI, given the benefit weighs over the risk of radiation exposure in this setting.

Other two putative mechanisms of AMI in COVID-19 include elevated levels of von Willebrand factors in severe COVID-19 and the expression of angiotensin-converting enzyme 2 (ACE-2) on the vascular endothelium [15] . The ACE-2 acts as a receptor for the SARS-CoV-2 virus and may result in endothelial cell tropism of the virus and consequent direct vascular endothelial damage and thrombosis. However, another interesting finding was noted in our study. There was evidence for direct SARS-CoV-2 viral involvement of the bowel mucosa in 3 patients, implying a possibility that direct viral invasion of the bowel may be another mechanism for bowel changes visualized in AMI. Indeed, the feco-oral route of the disease transmission has also been implicated in COVID-19 following examination of anal swabs and fecal samples in some studies [16, 17] . It also suggests that some of the symptoms of AMI in patients with COVID-19 may be due to viral enteritis rather than vascular ischemia per se.

Mural thickening and bowel wall edema were more commonly seen than bowel wall hypoenhancement in our study, consistent with the theory that bowel wall thickening has a higher sensitivity compared to bowel wall hypoperfusion which, in turn is more specific and points toward irreversible ischemia [11] . Pneumatosis was seen in ~ 17% of the patients, although this should be interpreted with caution as this may be seen secondary to mechanical ventilation in patients with severe COVID-19.

We also assessed the segment-wise involvement of the bowel wall, arteries, and veins in AMI in COVID-19, which has not been described before. We found that the ileum and colon were involved almost equally among the study population, with distal ileum and ascending colon being the most commonly involved segments. Among the arteries, SMA was most commonly involved, followed by the aorta (DTA being the most common aortic segment involved). Among the veins, SMV was most commonly involved followed by the portal vein. Spleen was the most common solid organ involved in our study. Dane et al. in their study suggested that the solid organ infarction in patients with COVID-19 may result from microthrombi and these patients often have patent vasculature, consistent with our findings [18] .

Serum D-dimer and CRP were the most commonly raised serum acute phase reactant in our analysis. Although blood tests may reveal elevated levels of these reactants in AMI, they are non-specific and may be elevated in severe COVID-19 infection even without AMI [11, 19] . As regards the onset of symptoms, we noted that abdominal ischemic symptoms could present as late as 48 days after positive RT-PCR for COVID. It is imperative that the clinicians managing patients with COVID-19 should monitor these patients for these potential late complications, as delay in the diagnosis can lead to increased mortality [20] . Most patients in our study received surgical treatment and among them, 30% died. On the contrary, 50% of the patients died among those who received medical management. Surgical treatment and thrombolysis have been conventionally considered the mainstay of treatment of AMI. In those without bowel necrosis or those who have contraindication to thrombolysis, endovascular treatment like catheter-directed thrombolysis may be considered and may reduce the need for more invasive surgery [11] . However, surgical treatment has remained the treatment of choice as far as AMI in COVID-19 is considered.

Findings on laparotomy and histopathology in our study was in striking agreement to the CT imaging findings in AMI. Imaging accurately identified SMA thrombus, mesenteric venous thrombosis, pneumatosis, or normal macrovascular structures. Given the high specificity of imaging in our study as well previous literature, it is worthwhile to perform contrast-enhanced abdominal CT scan containing arterial and venous phases for any COVID-19 patient with unexplained or new onset abdominal pain suspected for AMI [21] .

As regards the final outcomes, 42.8% of the patients died. The mortality in patients with AMI depends upon the time to diagnosis and initiation of the management. Also, according to a previously published systematic review found that patients with NOMI or MAT were more likely to die than those with MVT [10] . Indeed, in our series, NOMI and MAT were commonly seen which could have contributed to the high mortality rate. The high mortality rate in our study may also have been compounded due to other coexisting conditions in patients with COVID-19 resulting in delay in the diagnosis and management [20] .

The major limitations of our study include the small sample size and reporting bias (probability of reporting severe cases). Also, since the data are extremely heterogeneous in terms of quality of methodology, data availability, and imaging findings, the results of this study should be interpreted with caution and only in appropriate clinical context. Presence of different types of scanners, parameters of acquisition, and the experience of the radiologists may have induced some heterogeneity in the reported abdominal CT findings. However, we believe that this would not have impacted the common imaging findings in our study.

In conclusion, contrast-enhanced CT plays a pivotal role in the early identification and follow-up of AMI in patients with COVID-19. While small bowel ischemia is the most prevalent abdominal CT finding, non-occlusive mesenteric ischemia (NOMI) (due to microvascular involvement) is the most common pattern of bowel involvement. Bowel wall thickening is more common than bowel hypoperfusion. While ileum and colon both are equally involved bowel segments, SMA, SMV, and the spleen are the most commonly involved artery, vein, and solid organ, respectively. 50% of the patients with conservative/medical management died, highlighting high mortality without surgery. Findings on laparotomy and histopathology corroborate strikingly with CT imaging findings. It is imperative that the radiologists and clinicians are familiar with the imaging manifestations of AMI in COVID-19 on CT, so that they can make informed decision regarding management and improve outcomes in this devastating condition.

The online version contains supplementary material available at https:// doi. org/ 10. 1007/ s00261-021-03337-9.

Funding This research received no specific grant from any funding agency, commercial, or not-for-profit sectors.

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The authors declare that they have no conflict of interest.