Advances in Surgery 55 (2021) 75–87

ADVANCES IN SURGERY

Mesenteric Ischemia
When and How to Revascularize

Kristofor A. Olson, MD, PhD, Pedro G. Teixeira, MD*

Department of Surgery and Perioperative Care, The University of Texas at Austin Dell Medical
School, 1500 Red River Street, Annex, Austin, TX 78701, USA

Keywords
 Acute mesenteric ischemia  Chronic mesenteric ischemia
 Non occlusive mesenteric ischemia (NOMI)  Mesenteric venous thrombosis
 Surgical revascularization  Endovascular techniques  Surgical bypass

Key points
 Mesenteric ischemia requires a high index of suspicion, and prompt surgical
intervention is indicated to improve mortality.
 Revascularization should be performed early, with only frankly necrotic or
perforated bowel resected.
 Open revascularization approaches remain the gold standard for the treatment
of acute mesenteric ischemia, while endovascular approaches have gained favor
for chronic disease.

INTRODUCTION
Mesenteric ischemia occurs from hypoperfusion to the gut mucosa. The etiol-
ogies are multifactorial, and while progress has been made in efforts to revas-
cularize over the past 20 years, the acute forms of the disease still portend a
30% to 70% mortality rate. As an ailment predominately of the elderly, the
presence of underlying medical comorbidities often confounds and delays diag-
nosis, contributing to the high mortality of this disease. In this article, we
discuss the diagnosis and management of acute and chronic mesenteric
ischemia, recent developments in open and endovascular revascularization
techniques, approach considerations, and pitfalls.

The authors have nothing to disclose.

*Corresponding author. E-mail address: [email protected]

https://doi.org/10.1016/j.yasu.2021.05.006
0065-3411/21/ª 2021 Elsevier Inc. All rights reserved.
76 OLSON & TEIXEIRA

Table 1
The four ‘‘R’s’’ of mesenteric ischemia management [9]
Resuscitation Fluid resuscitation to restore perfusion to bowel mucosa,
crystalloid or colloid.
Rapid diagnosis High index of suspicion, CT angiography
Early revascularization Open vs endovascular approaches, as discussed in the
following sections
Reassessment Second-look laparotomy or laparoscopy depending on initial
approach to evaluate bowel viability after revascularization.
Reprinted by permission of Edizioni Minerva Medica from J Cardiovasc Surg. Apr 2017;58(2):339-50.

ANATOMY
The vascular supply to the gut is derived from the aorta via the celiac artery,
superior mesenteric artery (SMA), and inferior mesenteric arteries. Collateral-
ization is dense within the arcades of the mesentery, and anastomoses between
these vessels reinforce the blood supply. The major anastomoses between the
celiac and SMA are via the pancreaticoduodenal arteries. The inferior and su-
perior mesenteric arteries anastomose via the marginal artery of Drummond
and the Arc of Riolan. The distal gastrointestinal tract has arterial communica-
tion between the inferior mesenteric artery and internal iliac artery via the su-
perior and inferior hemorrhoidal arteries.

ACUTE MESENTERIC ISCHEMIA

Epidemiology
Acute mesenteric ischemia (AMI) presents in 0.1 to 1 in 1000 hospital admis-
sions, with a median age at presentation of 74 years [1,2]. As a disease of pre-
dominately the elderly, patients with AMI often present with nonspecific
symptoms in the setting of multiple medical comorbidities. Diagnosis, however
must be prompt as mortality rates of 50% have been reported even with early
identification of disease. For patients in the intensive care unit, the 30-day mor-
tality rate is as high as 71% [3].

Pathogenesis
The mucosal hypoperfusion injury in AMI occurs from four etiologies: arterial
embolism, arterial thrombosis, mesenteric venous thrombosis (MVT), and
nonocclusive mesenteric ischemia (NOMI). Arterial thromboembolism,
commonly originating from the heart and occluding the SMA at variable levels
depending on the size of the embolized thrombus, accounts for more than half
of cases of AMI [4]. Arterial thrombosis occurs in the setting of chronic athero-
sclerotic disease, and when combined with arterial thromboembolism, it consti-
tutes the vast majority of AMI. Thrombosis occurs due to dissection of the
SMA, either at its ostium or via extension of aortic dissection, or from rupture
of atherosclerotic plaque. MVT, specifically, thrombosis of the superior mesen-
teric vein, is a rare cause of mesenteric ischemia. This decreased venous
outflow and subsequent congestion leads to ischemia. NOMI, hypoperfusion
MESENTERIC ISCHEMIA 77

of the bowel despite vascular patency, most commonly occurs during critical
illness with prolonged or escalating use of vasopressors [5], hypotension, and
abdominal compartment syndrome. Irrespective of the etiology, injury occurs
via hypoperfusion of the bowel mucosa.
Clinical presentation
Owing to the affected patient population and baseline medical comorbidities,
presenting symptoms for AMI are often nonspecific. Classically, AMI manifests
as abdominal pain out of proportion to examination. Clinical suspicion should
be high in patients with existing atrial fibrillation, mechanical heart valves, pre-
existing peripheral vascular disease, or a history of embolic events. The onset
of symptoms is often acute, severe, and rapidly progressing with embolic dis-
ease. A more subacute presentation may occur with thrombotic disease. Pa-
tients with MVT often present with vague abdominal symptoms, with slow
progression over weeks as venous congestion increases. The presentation of
NOMI is the most insidious, with patients ranging from asymptomatic to peri-
tonitic [5], and often in the setting of critical illness. Laboratory tests are unre-
liable for the diagnosis of AMI, and a normal serum lactate does not exclude
ischemia [6]. The gold standard imaging modality for diagnosis is CT
angiography.
Management of acute thrombotic or embolic mesenteric ischemia
Medical management
AMI requires prompt diagnosis. Per current World Journal of Emergency Sur-
gery guidelines, ‘‘severe abdominal pain out of proportion to physical examina-
tion findings should be assumed to be AMI until disproven’’ [7]. Patients
should be evaluated by CT angiography to evaluate the etiology of vascular
compromise, receive nasogastric decompression, and begin anticoagulation
via heparin drip [8]. Fluid resuscitation should be initiated and broad-
spectrum antibiotics started because of mucosal compromise and the possibility
of bacterial translocation [9]. Patients with peritonitis require emergent laparot-
omy, and delay to the operative suite should be minimized (Table 1).
Indications for interventions
The diagnosis of AMI mandates emergent surgical attention. The gold stan-
dard of treatment remains an open midline laparotomy. Revascularization
should take priority. The alimentary tract should be examined from distal
esophagus to rectum with only grossly necrotic or perforated bowel being re-
sected before revascularization [10]. Questionably viable bowel may be
observed until revascularization is complete, and subsequently re-evaluated
at a second-look laparotomy within 48 hours [6,11].
Open versus endovascular revascularization
While the open approach to revascularization via thromboembolectomy and/or
bypass has traditionally been utilized, recent studies have shown some promise
with endovascular approaches. No level 1 or level 2 evidence exists comparing
the two approaches, however, with the best evidence coming from single-
78 OLSON & TEIXEIRA

center, retrospective studies. In a review by Lim and colleagues, endovascular

strategies resulted in improved short-term morbidity and mortality, decreased
overall complication rates (20% vs 38%), and decreased rates and length of
bowel resection [11]. These data may be confounded by the severity of patient
disease, as patients with overt bowel ischemia, necrosis, or peritonitis were pref-
erentially and appropriately treated by an open approach. Nonetheless, endo-
vascular therapy may be preferable in a subset of patients. An algorithm
proposed by Zhao and colleagues suggests that patients without peritonitis,
with suitable anatomy, life expectancy less than 5 years, and poor nutritional
status should be considered for endovascular therapy [12]. A hybrid algorithm
for managing embolic and thrombotic AMI adapted from the studies by Zhao
and Karkkainen is presented in Fig. 1. [12,13]
Endovascular revascularization
Anatomic considerations for endovascular treatment include the angle and tor-
tuosity of the SMA, proximal and distal landing zones 1 cm and without main
arterial branch takeoffs, and no peritonitis or intestinal necrosis [12]. In

Fig. 1. Algorithm for management of acute embolic/thrombotic mesenteric ischemia via

open versus endovascular approach [12,13]. AOD, atherosclerotic occlusive disease; CTA,
CT angiography; ET, endovascular therapy.
MESENTERIC ISCHEMIA 79

anatomically suitable patients, endovascular access to the SMA can be obtained

via either the brachial or femoral approach; however, brachial access is gener-
ally preferred owing to the steep angulation of the SMA from a retrograde
approach. In general, a 6 French sheath is introduced into the descending aorta,
and a guide catheter directed toward the SMA [13]. A hydrophilic guidewire is
passed distal to the lesion, and recanalization can be achieved in an antegrade
fashion via mechanical thrombectomy or thrombosuction, pharmacologic
thrombolysis with urokinase/streptokinase, angioplasty, and stenting (Fig. 2).
After initial thrombectomy, in the setting of incomplete resolution of the occlu-
sion or distal showering of thrombus, catheter-directed thrombolysis can be
considered to re-establish flow to distal branches. In a small case series, Genzel
reports success in revascularization of both the main trunk SMA and its side
branches with the use of a steerable sheath [14].
Open revascularization
In the setting of a laparotomy, owing to either bowel necrosis requiring resec-
tion, surgeon preference, or the lack of access to endovascular expertise, several
options exist for revascularization. Access to the SMA is obtained by reflecting
the transverse colon cephalad and the small bowel to the patient’s right. After
dissection through the root of the mesentery and achieving proximal and distal
control, a transverse arteriotomy is made distal to the thrombus, and balloon
catheters are used to remove proximal clot until pulsatile flow is returned.
Smaller diameter balloon catheters are then passed distally to remove any
showered clot or fragments. With restoration of pulsatile inflow, retrograde
flow, and local heparinization, the arteriotomy is then closed primarily with
polypropylene suture. The surgeon may then re-evaluate bowel viability and
place a temporary closure device over the abdomen to facilitate further resus-
citation and second look laparotomy.

Fig. 2. CT angiogram and 3D reconstruction showing near-complete occlusion of the SMA,

and angiogram after endovascular stent deployment.
80 OLSON & TEIXEIRA

Open bypass
In cases of long-segment occlusion, previous endovascular mesenteric stenting,
previous bypass, or multivessel disease, open bypass may be required. Bypass
may be performed in either an antegrade fashion from the supraceliac aorta or
retrograde fashion from the infrarenal aorta or common iliac arteries. Much
debate exists on the literature as to which approach is favorable. In the setting
of multiple vessel disease such as acute SMA thrombus with both celiac and
SMA arteriosclerosis, a branched polytetrafluoroethylene (PTFE) graft may
be used to restore antegrade flow to both vessels; however, single-vessel revas-
cularization is usually sufficient in the acute setting [13]. Proximal aortic control
is achieved via a transcrural approach of the supraceliac or lower thoracic
aorta. Supraceliac clamping and associated renal hypoperfusion may not be
desirable in critically ill patients with AMI, and therefore, a retrograde
approach from the infrarenal aorta or iliac arteries may be preferred. Saphe-
nous venous conduit and PTFE grafts have both been used with success for
retrograde revascularization. The desire to use autologous vein graft in the
contaminated abdomen must be weighed against the increased operative
time associated with vein harvest and the overall high mortality inherent to
this disease process, leading some authors to default to PTFE graft irrespective
of contamination [13]. In a single-center study by Scali and colleagues, 82 pa-
tients who underwent aortomesenteric bypass between 2002 and 2016 were
evaluated for postoperative morbidity and mortality, with comparable out-
comes for both the antegrade and retrograde bypass groups [15].
Antegrade bypass
Antegrade bypass is performed by mobilizing the left lobe of the liver and
dividing the left crus to expose the supraceliac aorta. The SMA is exposed
as previously described. After achieving proximal and distal control, an aortot-
omy is made in an unaffected region of the aorta, and the graft is sewn in an
end-to-side fashion. The use of a side-biting clamp can facilitate antegrade
aortic flow during construction of the anastomosis [15]. The graft is then
tunneled in a retropancreatic plane to reach a disease-free portion of the
SMA, where an end-to-side or end-to-end anastomosis is performed. In the
setting of multivessel disease, as may be present with acute on chronic mesen-
teric ischemia, a bifurcated graft may be used with an end-to-end celiac anasto-
mosis or end-to-side hepatic artery anastomosis.
Retrograde bypass
While antegrade bypass has been advocated for patients with chronic disease
and requiring multivessel revascularization, studies have shown that single-
vessel revascularization is sufficient in the setting of acute SMA occlusion
[13]. The added complexity of supraceliac aortic exposure with the possibility
of renal hypoperfusion due to supraceliac clamping lends some surgeons to pre-
fer a retrograde bypass approach. A location for retrograde inflow is selected
on the common or external iliac vessel, depending on ease of dissection and
presence of atherosclerotic disease. The SMA is dissected and ligated distal
MESENTERIC ISCHEMIA 81

to disease. Traditionally, the use of a C-shaped graft has been described, with
an end-to-side anastomosis at the iliac artery and an end-to-end or end-to-side
anastomosis at the SMA.
A direct open retrograde revascularization (DORR) technique has been
recently described, where autologous vein graft is anastomosed to the right
common iliac in an end-to-side fashion and tunneled directly through the
base of the small bowel mesentery via blunt dissection to the SMA [16]. An
end-to-side or end-to-end anastomosis is performed distal to the occlusion of
the SMA. In situations where both celiac and mesenteric occlusions were pre-
sent, the SMA anastomosis was performed side-to-side with the vein graft
continuing to the hepatic artery for an end-to-side anastomosis. When
compared to the antegrade approach, the authors found a shorter operative
time (282 vs 375 min) for the DORR method, with otherwise similar outcomes
between the two approaches. When compared to the traditional ‘‘c-loop’’ retro-
grade approach, the DORR method carries hypothetical advantage of reducing
the possibility of reintervention due to graft kinking; however, these data have
not explicitly been enumerated.
Retrograde open mesenteric stenting
A hybrid approach has recently gained increasing traction as an alternative to
open bypass in patients not amenable to endovascular therapy because of sys-
temic risk factors, unsuitable anatomy, requirement for damage control laparot-
omy, or in patients with thrombosis in an area of stenosis [17]. Retrograde open
mesenteric stenting (ROMS) is performed as follows. After exposing and
achieving proximal and distal control of the SMA, an arteriotomy is made
distal to the lesion, and a guidewire and 6 French sheath placed in a retrograde
fashion. On-table angiography is performed, and a guidewire traversed proxi-
mally across the SMA lesion into the aorta. Balloon-expandable stents are de-
ployed from the ostium to the distal extent of the lesion. With inflow confirmed
via angiography, the sheath is removed, and the arteriotomy repaired with
polypropylene suture.
A multicenter retrospective review of 54 patients who underwent ROMS for
the treatment of acute and chronic mesenteric ischemia revealed patency rates
at 2 years of 76%, similar to those of patients receiving percutaneous endovas-
cular therapy. Unfortunately, 30-day mortality remained high in the AMI
cohort, with 45% of patients not surviving their hospitalization [18]. Still,
ROMS remains an attractive option for patients with atherosclerotic occlusive
disease requiring laparotomy without an additional trip to the endovascular
suite.
A recent study published by Andraska and colleagues compared ROMS
versus open mesenteric bypass in patients with AMI from 2008 to 2019 [19].
At their center, ROMS was performed in a conventional operating room
with a C-arm rather than in a hybrid endovascular suite. They found shorter
operative times (189 vs 302 minutes), with similar complication, reintervention,
and mortality rates to patients receiving open mesenteric bypass. To this end,
82 OLSON & TEIXEIRA

they recommend ROMS be considered the initial approach to the treatment of

AMI [19].

MANAGEMENT OF MESENTERIC VENOUS THROMBOSIS

Medical management
Therapeutic anticoagulation is the mainstay of initial treatment for patients
with acute MVT [20,21]. Initial therapy with low-molecular-weight heparin
bridged to warfarin or an oral anticoagulant is usually sufficient for successful
treatment, with better prognosis than patients with embolic or thrombotic dis-
ease [22]. Imaging studies should be reviewed to rule out the presence of bowel
ischemia. In the face of ischemia or peritonitis, the patient should be taken to
the operating room for laparotomy as described for embolic and thrombotic
AMI. Patients should remain on anticoagulation from 6 months to lifelong ther-
apy depending on the underlying etiology. Fatal recurrences have been re-
ported in up to 25% of cases [23].
Indications for interventions
For patients with signs/symptoms of peritonitis or imaging findings concerning
for ischemia, operative intervention is required for resection of necrotic bowel.
As for embolic and thrombotic AMI, equivocal appearing segments should be
left until revascularization is complete and reassessed at second-look
laparotomy.
Open surgical versus endovascular
Little high-quality evidence exists with regard to endovascular versus surgical
approaches to MVT [24]. Catheter-directed thrombolysis via the SMA,
percutaneous transhepatic thrombectomy, and open embolectomy have all
been reported [25]. A small case series of 32 patients comparing postopera-
tive catheter-directed thrombolysis versus systemic anticoagulation after
open embolectomy showed improved thrombus removal and decreased 30-
day mortality in the CDT group; however, massive abdominal hemorrhage
was significantly more common, occurring in 20% of patients in this series
[26].
More aggressive approaches to the treatment of MVT have been described.
Catheter-directed thrombolysis of the superior mesenteric vein is within the
armamentarium of the interventional radiologist. Transjugular intrahepatic
portosystemic shunt, percutaneous transhepatic, transileocolic venous, and
transplenic venous approaches have previously been described [27]. However,
their necessity is rare and reserved for patients with only the most severe and
progressive mesenteric venous occlusion.

MANAGEMENT OF NON-OCCLUSIVE MESENTERIC ISCHEMIA

The hallmark of NOMI is intestinal hypoperfusion despite vascular patency
[5]. Often associated with critical illness, its causes are multifactorial and may
result in a spectrum of bowel injury from patchy ischemia to long-segment ne-
crosis. Mortality rates exceed 80%. The focus of treatment should be directed
MESENTERIC ISCHEMIA 83

at correcting the underlying cause and restoring intestinal perfusion [2,4,7]. In

the setting of bowel necrosis or perforation, prompt exploration and resection
should be performed.

CHRONIC MESENTERIC ISCHEMIA

Epidemiology and pathogenesis
Chronic mesenteric ischemia occurs in the setting of severe SMA stenosis pre-
dominately from atherosclerotic disease. The prevalence of CMI is very low,
reported at 30 per 100,000 [28]. The extensive collateral circulation to the
bowel and the slow progression of mesenteric artery stenosis belie the rarity
of this disease. Risk factors for the development of chronic mesenteric ischemia
owe to the pathophysiology of atherosclerotic disease: smoking, hyperlipid-
emia, hypertension, and cardiovascular disease.
Clinical presentation
Patients with chronic mesenteric ischemia classically present with postprandial
abdominal pain [2,29]. Such pain can result in weight-loss due to decreased
caloric intake, frequency, and fear of eating. As expected, recurrent postpran-
dial pain has significant impacts on patient quality of life [30]. These symptoms
are often nonspecific, leading to a broad differential diagnosis. Clinically signif-
icant ischemia from chronic mesenteric atherosclerotic disease requires three
factors: medical history supportive of the diagnosis; mesenteric artery stenosis
of one or more vessels over 70%; and imaging, surgical, or endoscopic findings
consistent with ischemia [31].
Medical management
Owing to the impacts on quality of life, initial management of chronic mesen-
teric ischemia hinges on lifestyle modification. Decreased meal size and
increased meal frequency may improve symptoms of postprandial pain. Treat-
ment of underlying medical comorbidities which contribute to further athero-
sclerotic disease is mandatory and may be best addressed via a
multidisciplinary care team.
Indications for interventions
As previously noted, the impacts on patient quality of life cannot be under-
stated in. To this end, symptoms refractory to medical management and life-
style modification are a clinical indication for intervention in patients with
mesenteric artery stenosis [30]. Patients must have symptoms and imaging find-
ings consistent with the diagnosis, including single- or multi-vessel disease with
greater than 70% occlusion (Fig. 3). In a study of 79 patients following revas-
cularization via open antegrade, retrograde, or endovascular approaches, revas-
cularization resulted in a clinically significant improvement in quality-of-life
scores after revascularization [30].
Surgical versus endovascular
Given the typical presentation and often incidental diagnosis of mesenteric ste-
nosis on imaging, endovascular approaches are favored for revascularization.
84 OLSON & TEIXEIRA

Fig. 3. CT showing chronic atherosclerotic disease with calcification at the ostia of the celiac
and superior mesenteric arteries.

Findings suggestive of bowel infarct, such as when an acute embolus occludes a

stenotic mesenteric vessel, demand laparotomy for bowel resection and revas-
cularization as described earlier in this chapter. In these patients an open revas-
cularization approach, such as ROMS described earlier, may be used [18]. For
patients without an acute abdomen, endovascular approaches are now strongly
favored over open revascularization. A systematic review and meta-analysis of
100 studies comparing endovascular versus open revascularization showed im-
provements in 30-day mortality and decreased in hospital complication rates
with an endovascular approach [32]. However, similar to findings reported
in AMI, open surgery was associated with a lower risk of 3-year symptom
recurrence than endovascular stenting. There was no significant difference
identified in 3-year overall survival.

POSTOPERATIVE CARE
As a mainstay of medical management of mesenteric ischemia, patients are
placed on anticoagulation at diagnosis, and should remain anticoagulated after
revascularization. No level one evidence exists to suggest the duration of anti-
coagulation, but given the age of onset and presence of underlying comorbid-
ities, lifetime anticoagulation is likely. Transition from heparin to vitamin K
antagonists and novel oral anticoagulants have both been used for this purpose.
Patients undergoing endovascular therapy should be placed on aspirin for life,
MESENTERIC ISCHEMIA 85

with dual antiplatelet therapy for 1 to 3 months postoperatively [22]. Patients

with AMI should continue to undergo further postoperative resuscitation
and, in the case of bowel resection, return to the operating room for second
look laparotomy in 24 to 48 hours.

LONG-TERM FOLLOW-UP
Long-term care should be directed at addressing the patient’s underlying med-
ical comorbidities to minimize the risk of recurrent disease. Risk factor and life-
style modification, as well as management of hyperlipidemia, hypertension, and
diabetes, are necessary. Patients with bypass graft or stent placement should
have surveillance imaging obtained via duplex ultrasound or CT angiography
within 6 months, with frequent follow-up thereafter to enable early intervention
on recurrent disease [6]. Current Society for Vascular Surgery guidelines
recommend duplex ultrasonography at 1, 6, and 12 months, and then annually
thereafter [33].

SUMMARY
Mesenteric ischemia remains a relatively rare albeit high-mortality disease. In
its acute form, delay in diagnosis and lack of prompt intervention contribute
to the high mortality rate. Rapid diagnosis, anticoagulation, resuscitation,
revascularization, and reassessment are the guiding principles in the manage-
ment. In the operating room, a focus on revascularization should take priority
unless frankly necrotic or perforated bowel is encountered. Classically open
revascularization approaches have been used and described, owing to the fre-
quency of concomitant damage control laparotomy and familiarity of the sur-
geon, but recent developments, with improvement in early diagnosis, have
allowed endovascular techniques to be further explored. Much debate in
the literature and little high-quality evidence exists to define the appropriate
conditions and support one treatment modality over another for acute dis-
ease. However, the success of endovascular approaches for the treatment
of chronic mesenteric ischemia suggests further study is warranted in this
area.

CLINICS CARE POINTS

 Mesenteric ischemia requires a high index of suspicion, and prompt surgical

intervention is indicated to improve mortality.
 Revascularization should be performed early, with only frankly necrotic or
perforated bowel resected.
 Open revascularization approaches remain the gold standard for the treatment
of acute mesenteric ischemia, while endovascular approaches have gained
favor for chronic disease.
86 OLSON & TEIXEIRA

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