Mesenteric Ischemia: Predicting Problems

Abstract

Background

Mesenteric ischemia is an uncommon diagnosis that is often overlooked until patients present with non-salvageable bowel. Our objective was to identify risk factors for mesenteric ischemia, clinical warning signs, and imaging findings that could suggest earlier diagnosis and intervention.

Methods

We queried our health system’s electronic health record (EHR) to identify patients with ischemic bowel and/or a diagnosis of mesenteric ischemia between November 2013 and December 2020. Using stringent exclusion criteria, we included patients whose event was likely caused by atherosclerotic disease. From the EHR, we abstracted these patients’ comorbidities and symptoms from the previous 6 months. We evaluated relevant computed tomography scans (CTs) obtained up to 2 years prior to admission and graded stenosis of the celiac artery and the superior mesenteric artery (SMA).

Results

Forty-five patients met inclusion criteria. The most prevalent comorbidities were hypertension, hyperlipidemia, and heart disease. Over half of the patients in the cohort had mentioned suspicious abdominal symptoms during the 6 months preceding admission. Of the patients who had a CT within the 2 years prior to admission, there was discordance between the formal interpretations and independent reviews with significant stenosis being noted more commonly on independent review. Furthermore, in-hospital mortality was significantly higher when pre-presentation imaging noted SMA stenosis >70%.

Discussion

These data suggest that patients who were at risk of developing mesenteric ischemia had underlying vascular disease, a history of concerning symptoms, and prior CT imaging consistent with mesenteric atherosclerotic disease which could potentially be acted upon before the manifestation of an acute event.

Keywords

mesenteric ischemia ischemic bowel vascular surgery general surgery acute care surgery

Key Takeaway

• Patients with chronic mesenteric ischemia often report nonspecific abdominal symptoms at episodes of care prior to presenting with infarcted bowel.

• SMA stenosis can be effectively evaluated on CT imaging other than CT angiography.

• Severe (>70%) SMA stenosis within 2 years of acute presentation is associated with increased in-hospital mortality in the setting of acute mesenteric ischemia.

Introduction

Mesenteric ischemia is a relatively rare cause of surgical emergency but with dire consequences. Literature tends to show a 50% mortality rate or higher.^1,2 Mesenteric ischemia is frequently categorized into occlusive vs nonocclusive, with occlusive further subdivided into arterial embolic, arterial thrombotic, or venous thrombotic etiologies. Karkkainen et al noted that half of the patients who presented with mesenteric ischemia due to atherosclerotic disease presented suddenly with seemingly no warning, while half demonstrated an acute-on-chronic picture.³ Of those with chronic mesenteric ischemia, symptoms are often vague but progressive and include abdominal pain (especially postprandial), food avoidance, weight loss, nausea, vomiting, and diarrhea.^2,4,5

People with mesenteric ischemia typically have comorbidities that lead to atherosclerotic disease, such as smoking, cardiovascular disease, and diabetes.⁴ Other demographic features common in patients with mesenteric ischemia are female sex and advanced age.⁶ Susceptible patients frequently present with nonspecific warning signs and are often misdiagnosed even with advanced imaging such as computed tomography (CT). Diagnostic delays lead to the risk of developing an acute event which is then associated with remarkable morbidity and mortality. In this study, we investigate a cohort of patients with arterial thrombosis causing mesenteric ischemia and evaluate their demographics, comorbidities, symptoms, and CT imaging for indications that could have been intervened upon prior to presenting with ischemic bowel.

Methods

This was a retrospective study at a single independent academic medical center. Following study approval and waiver of informed consent by the Gundersen Clinic Ltd Human Subjects Committee/Institutional Review Board, we queried our health system’s electronic health record (EHR) system to identify all patients admitted to our hospital with ischemic bowel and/or a diagnosis of mesenteric ischemia between November 2013 and December 2020. Multiple tiers of exclusion were used (Figure 1) to identify those patients whose bowel ischemia was likely due to thrombotic mesenteric ischemia. We retrospectively reviewed these patients’ EHRs and abstracted demographic and clinical data, comorbidities, and patient-reported smoking status and substance use. Comorbidities including hypertension, hyperlipidemia, heart disease, chronic respiratory illness, peripheral artery disease, diabetes mellitus, coronary artery disease, obstructive sleep apnea, stroke, psychiatric diagnosis, chronic kidney disease, current dialysis, and hypothyroidism were collected via diagnosis codes and manual review. Individual patient EHRs of all episodes of care within 6 months prior to admission were reviewed to determine whether patients demonstrated concerning symptoms such as poor appetite, abdominal pain, nausea, vomiting, or diarrhea. Weight as documented up to a year prior to admission was collected. Palliative care consultation during admission and the availability of health care power of attorney information were recorded. Length of stay for patients who died during admission was calculated separately from those who did not. Twenty-eight patients had CT scans capturing the mesenteric vessels’ origins with or without contrast up to 2 years before their acute presentation. Radiologist interpretations of these studies were evaluated for specific mention of mesenteric or splanchnic calcifications or of atherosclerotic disease. The CT images were then evaluated by a vascular surgeon and a general surgeon who were both blinded to the radiologist interpretations. These individuals graded stenosis of the celiac artery and superior mesenteric artery on a scale of severity, with grade A being <50% stenosis, grade B 50%-70% stenosis, and grade C >70% stenosis. There was discrepancy in the initial review of 14 (50%) of the cases, which were then reviewed by another general surgeon as a tiebreaker. All three surgeons disagreed for 1 scan, so the grade of “B” was assigned.

Frequencies and percentages were used to summarize categorical variables, while means and standard deviations (SDs) were used to summarize numeric variables. A paired t test and associated 95% confidence interval was used to assess the difference in mean weight between this admission time and 1 year prior. Fisher exact and Pearson χ² tests were used to test for associations between mortality and CT imaging/grading. A level of .05 was used throughout for assessing statistical significance. All analysis was completed using the statistical software program R, version 4.2.3 (R Core Team, 2023).

Results

Forty-five patients with an average age of 70 (SD = 10) years at time of first surgery/admission met inclusion criteria. Seventy-one percent (32/45) were admitted to Gundersen Lutheran Medical Center from within our health system, with the remainder coming from referring facilities. Fifty-three percent of the cohort (24/45) were women, 43 of 45 were White, 2 of 45 were American Indian or Alaska Native, and 100% were of non-Hispanic/non-Latino/a ethnicity.

At the time of admission, 24% (11/45) were active smokers, 62% (28/45) were former smokers, and 13% (6/45) were never smokers. Forty-four percent (20/45) were being treated with an opioid prior to admission and 31% (14/45) reported alcohol use, but only 1 patient reported use of illicit drugs. The most prevalent comorbidities in our cohort (Table 1) were hypertension (91%), hyperlipidemia (87%), heart disease (84%), chronic respiratory illness (69%), peripheral artery disease (60%), and diabetes mellitus (58%).

Table 1.

Comorbidities of Patients With Ischemic Bowel And/or Mesenteric Ischemia (N = 45).

Comorbidity	n (%)
Hypertension	41 (91)
Hyperlipidemia	39 (87)
Heart disease	38 (84)
Chronic respiratory illness	31 (69)
Peripheral artery disease	27 (60)
Diabetes mellitus	26 (58)
Coronary artery disease	23 (51)
Arthritis	18 (40)
Obstructive sleep apnea	15 (33)
Stroke	14 (31)
Psychiatric diagnosis	13 (29)
Hypothyroidism	7 (16)

Sixteen percent (7/45) of patients were on dialysis prior to admission, and 56% (25/45) had mentioned suspicious abdominal symptoms at other episodes of care during the 6 months preceding this admission. Of the 35 patients who had weight documented within a year prior to admission, the average weight decreased significantly from 84 kg (SD = 27) to 81 kg (SD = 27) at admission (95% CI for mean weight loss = .65-5.2 kg, P = .014). Of our 45 patients, 27 (60%) had a power of attorney activated or documented on file. The palliative care team was consulted on 19 (42%) of our cohort.

Forty-three of 45 patients underwent a CT scan during their acute presentation. Radiologist interpretations specifically mentioned “mesenteric” or “splanchnic” calcifications in 51% (22/43) of these scans. Of the remaining 21 (49%) scans for which radiologists did not specifically mention mesenteric calcifications, 16 (76%) had mention of nonspecific atherosclerotic disease, leaving 5 patients (12%) with no mention of any atherosclerotic calcifications on CT. However, on independent review, all 5 were found to have at least some degree of mesenteric artery calcification. In the two years prior to admission, over half of the cohort (28/45) had undergone a CT scan visualizing the mesenteric vessels (Table 2). Of these, 5 (18%) had specific mention of mesenteric calcifications, and the other 23 all had nonspecific mention of atherosclerotic disease burden. Severity of the mesenteric stenosis within the celiac and superior mesenteric arteries on the preadmission scans was independently evaluated by surgeons. Of the 28 patients who had preadmission scans, superior mesenteric artery (SMA) stenosis was graded A for 18%, B for 18%, and C for 64%. Celiac arteries were graded A for 44%, B for 19%, and C for 37%.

Table 2.

Deaths During Admission by SMA and Celiac Occlusion Grade for Patients With Preadmission CT Scans, N = 28.

Artery	Overall	Occlusion grade			P ^a
Artery	Overall	A	B	C	P ^a
SMA	N = 28	n = 5	n = 5	n = 18
Died during admission	12 (43)	0 (0)	1 (20)	11 (61)	.030
Celiac	N = 27^b	n = 12	n = 5	n = 10
Died during admission	12 (44)	5 (42)	2 (40)	5 (50)	>.9

Data are presented as number of patients with preadmission CT scans (%). Bold value is considered statistically significant.

^aFisher exact test.

^bOne patient had an anatomic variant in which the celiac artery was absent.

The overall mortality rate during this admission was 47% (21/45). The mortality rate for patients with an SMA stenosis grade of C was significantly higher than for those with an A or B grade (61%, 11/18 vs 10%, 1/10, respectively; P = .016). The degree of celiac artery stenosis was not significantly associated with the rate of mortality during admission (P = .7). Length of stay was not associated with grade of stenosis, regardless of patient mortality during their admission. Using the SMA grade of C to predict mortality during admission, we generated a sensitivity of 0.56 and a specificity of 0.92. We did not find significant evidence that the SMA grade can be used to predict mortality during admission (P = .09).

Comment

Patients with ischemic bowel due to mesenteric ischemia frequently have preadmission comorbidities, symptoms, and CT imaging that have value in identifying at-risk pathology. Historically, the prevalence of mesenteric artery thrombosis has been reported in the 15% to 25% range, but more recent literature suggests that 40% of mesenteric ischemia cases are due to arterial thrombosis.¹ In addition, the overall prognosis is worse for patients with arterial thrombus than for those with arterial embolus.⁷ Our study captured a relatively precise sample of patients with atherosclerotic acute-on-chronic mesenteric ischemia who had demographics, comorbidities, and mortality rates similar to those reported in the literature.^3,4,6 Though the classical teaching is that symptoms occur with occlusion of multiple mesenteric vessels, severe (>70%) stenosis within the SMA alone is particularly problematic even in isolation.⁸ Our findings support this contention.

Weight loss is a known factor in diagnosis of chronic mesenteric ischemia and may prompt workup that reveals this condition.² We noted that of the 35 patients with weight data, there was a statistically significant average weight loss of 3 kg prior to their acute presentation. Of note, given the increased rates of obesity in our population, the classic findings of a cachectic patient may not always be present. Many patients remain overweight or obese despite their disease.⁸ Additional concerning symptoms include abdominal pain, poor appetite, nausea, vomiting, or diarrhea. Over half of the patients in this study reported at least 1 of these suspicious abdominal symptoms within 6 months prior to their admission. Symptom reporting, along with CT findings of atherosclerotic disease, should lead to a higher suspicion of potential mesenteric ischemia even in the absence of weight loss.

Within the CT results, nonspecific findings of atherosclerotic disease were common both prior to and at the time of admission. When patients presented in extremis with symptoms that ultimately led to the operating room and subsequent confirmation of ischemic bowel, the CT report often commented upon the mesenteric vasculature (51%). This was not the case for scans obtained prior to their admission (18%). On our review, however, over half of the patients with pre-acute presentation CT scans had greater than 70% SMA stenosis. In our study, matching with the literature, severe SMA stenosis in particular was found to be significantly associated with mortality. 8 The use of SMA grading within our sample was not predictive of mortality likely due to the small sample size (n = 28). The high specificity with moderate sensitivity suggests a potential predictive relationship between SMA grade and mortality, but additional study is warranted on this point.

The role of palliative medicine engagement with multiply comorbid patients is well established, and the vascular patient population has been notably underserved in this area.⁹ It is ideal to have mature processes in place for easing the stress of end-of-life care on patients and their families. While palliative care has better results when initiated prior to emergency general surgery, positive effects for those who receive the consultation afterward are evident.¹⁰ Fewer than half of our patients had discussions with the palliative care service, but over half had their wishes and/or health care power of attorney documented in the EHR. This aspect of our system allows for more personalized and appropriate end-of-life care, even without the involvement of palliative specialists.

Most of the preadmission CT scans were done without intravenous contrast, so we used the presence and amount of calcification as a proxy. Arterial calcification is noted to be an independent predictor of mortality, particularly abdominal visceral artery calcification.¹¹ The surgeons who evaluated the grade of stenosis were blinded to the initial CT impression, and the category in which patients were placed was based on their thorough review of the images. More accurate methods of objectively quantifying the burden of calcification and degree of stenosis for coronary artery disease exist.¹² This technology has been adapted for use in mesenteric vasculature and is a promising screening tool for the identification of chronic mesenteric ischemia.¹³ It was not available to us, nor would it likely be available to the general surgeons or other physicians who encounter these patients and their CT scans first, particularly in more rural and under-resourced environments. Regardless, a heavy mesenteric atherosclerotic disease burden should prompt referral to vascular specialists for further evaluation and possible intervention.

As a relatively rare and difficult to diagnose condition, mesenteric ischemia warrants a high degree of suspicion to appropriately diagnose and treat before harm reaches the patient. Hindsight is often much clearer in these cases, which is not to say that the providers who missed the diagnosis were negligent; rather, that it is truly a difficult problem to pinpoint. It is important to not rely solely on written radiology reports to influence our clinical decision-making, but to look at the images ourselves and ensure concordance with the clinical presentation. Often, the absence of acute imaging findings may give us false reassurance and cause us to overlook a progressive problem. For mesenteric vessel atherosclerosis and subsequent stenosis, a CT-angiogram is a much better imaging study, but often it is not the first imaging a patient receives at symptom onset. Fortunately, the calcifications in question can still be appreciated on non-contrast imaging.

Our study has several limitations. Notably, it is a retrospective, single-center study with a small sample size. We used multiple tiers of exclusion that could have omitted patients whose condition was being driven primarily by atherosclerotic disease. Other causes of ischemic bowel can certainly be exacerbated by concomitant vascular disease. However, homing in on less clinically ambiguous cases permitted a more specific focus on the disease process. Another limitation is that while we reviewed CT scans from 2 years prior to admission, we reviewed episodes of care from within only 6 months. Because many of our patients were from out of system, we have incomplete data for weight prior to admission and are likely missing clinical documentation regarding symptoms.

In conclusion, we found that patients who are at risk of developing acute mesenteric ischemia have underlying vascular disease, have reported concerning abdominal complaints, and frequently have prior CT imaging that indicates potential vascular compromise. Maintaining a high degree of suspicion for mesenteric ischemia in patients with concerning symptoms and prior imaging may lead to more timely assessment and ultimate prevention of an acute presentation.

Footnotes

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Bonnie E. Holley

References

Bala

Catena

Kashuk

, et al. Acute mesenteric ischemia: updated guidelines of the world society of emergency surgery. World J Emerg Surg. 2022;17(1):54. doi:10.1186/s13017-022-00443-x

Park

Gloviczki

Cherry

, et al. Contemporary management of acute mesenteric ischemia: factors associated with survival. J Vasc Surg. 2002;35(3):445-452. doi:10.1067/mva.2002.120373

Kärkkäinen

. Acute mesenteric ischemia in elderly patients. Expert Rev Gastroenterol Hepatol. 2016;10(9):985-988. doi:10.1080/17474124.2016.1212657

Terlouw

Moelker

Abrahamsen

, et al. European guidelines on chronic mesenteric ischaemia - joint United European gastroenterology, European association for gastroenterology, endoscopy and nutrition, European society of gastrointestinal and abdominal radiology, Netherlands association of hepatogastroenterologists, Hellenic society of gastroenterology, cardiovascular and interventional radiological society of Europe, and Dutch mesenteric ischemia study group clinical guidelines on the diagnosis and treatment of patients with chronic mesenteric ischaemia. United European Gastroenterol J. 2020;8(4):371-395. doi:10.1177/2050640620916681

van Dijk

van Noord

de Vries

, et al. Clinical management of chronic mesenteric ischemia. United European Gastroenterol J. 2019;7(2):179-188. doi:10.1177/2050640618817698

Hohenwalter

. Chronic mesenteric ischemia: diagnosis and treatment. Semin Intervent Radiol. 2009;26(4):345-351. doi:10.1055/s-0029-1242198

Schoots

Koffeman

Legemate

Levi

van Gulik

. Systematic review of survival after acute mesenteric ischaemia according to disease aetiology. Br J Surg. 2004;91(1):17-27. doi:10.1002/bjs.4459

Huber

Björck

Chandra

, et al. Chronic mesenteric ischemia: clinical practice guidelines from the society for vascular surgery. J Vasc Surg. 2021;73(1S):87S-115S. doi:10.1016/j.jvs.2020.10.029

Kwong

Curtis

Mell

. Underutilization of palliative care for patients with advanced peripheral arterial disease. Ann Vasc Surg. 2021;76:211-217. doi:10.1016/j.avsg.2021.07.003

10.

Yefimova

Aslakson

Yang

, et al. Palliative care and end-of-life outcomes following high-risk surgery. JAMA Surg. 2020;155(2):138-146. doi:10.1001/jamasurg.2019.5083

11.

Sadat

Mariam

NBG

Usman

, et al. Association between abdominal visceral artery calcification and all-cause mortality-A computerized tomography imaging-based longitudinal follow-up study. Angiology. 2019;70(3):237-243. doi:10.1177/0003319718796889

12.

Agatston

Janowitz

Hildner

Zusmer

Viamonte

Detrano

. Quantification of coronary artery calcium using ultrafast computed tomography. J Am Coll Cardiol. 1990;15(4):827-832. doi:10.1016/0735-1097(90)90282-T

13.

Terlouw

van Noord

van Walsum

Bruno

Moelker

. Mesenteric artery calcium scoring: a potential screening method for chronic mesenteric ischemia. Eur Radiol. 2021;31(6):4212-4220. doi:10.1007/s00330-020-07530-0