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Best Practice & Research Clinical Gastroenterology 31 (2017) 15e25

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Best Practice & Research Clinical Gastroenterology


journal homepage: https://ees.elsevier.com/ybega/default.asp

Acute mesenteric ischemia (part I) e Incidence, etiologies, and how to


improve early diagnosis
rkka
Jussi M. Ka inen, MD, PhD Specialist in Vascular and Gastrointestinal Surgery a, *,
Stefan Acosta, MD, PhD Professor of Vascular Surgery b
a
Heart Center, Kuopio University Hospital, P.O. Box 100, 70029 Kuopio, Finland
b
Department of Clinical Sciences Malmo, Lund University, Sweden

a b s t r a c t
Keywords: Acute mesenteric ischemia (AMI) is generally thought to be a rare disease, but in fact, it is more common
Acute mesenteric ischemia cause of acute abdomen than appendicitis or ruptured abdominal aortic aneurysm in patients over 75
Acute on chronic mesenteric ischemia
years of age. In occlusive AMI, surgical treatment without revascularization is associated with as high as
Nonocclusive mesenteric ischemia
Mesenteric venous thrombosis
80% overall mortality. It has been shown that early diagnosis with contrast-enhanced computed to-
Etiology mography and revascularization can reduce the overall mortality in AMI by up to 50%. However, only a
Incidence minority of patients with AMI are being treated actively with revascularization in the United States, and
Diagnosis the situation is very likely similar in Europe as well. What can we do to improve diagnostic performance,
Computed tomography so that more patients get proper treatment? The diagnosis is a collaborative effort of emergency
department surgeons, gastrointestinal and vascular surgeons, and radiologists. The etiological categori-
zation of AMI should be practical and guide the therapy. Furthermore, the limitations of the diagnostic
examinations need to be understood with special emphasis on computed tomography ndings on pa-
tients with slowly progressing acute-on-chronic mesenteric ischemia.
2016 Elsevier Ltd. All rights reserved.

Introduction multi-slice contrast-enhanced computed tomography (CT), the


most important diagnostic examination in AMI, to nearly all pa-
In 1926, A.J. Cokkinis wrote the diagnosis is impossible, the tients with acute abdominal pain at any given time. Second, our
prognosis hopeless and the treatment useless [1]. Ninety years later, endovascular capabilities have taken a leap from the conventional
it is still a common presumption that acute mesenteric ischemia time-consuming catheter-directed thrombolysis to mechanical
(AMI) is a rare condition which inescapably leads to the death of the thrombectomy using dedicated aspiration catheters, and to utiliz-
patient. The reason for such dreary reputation is not so much based ing stents that are designed especially for visceral arteries. We have
on facts but because AMI is too often found too late when the treat- seen that with early diagnosis and treatment, more than half of
ment outcome is inevitably poor. In the early 1990s in Finland, two- patients with AMI can be rescued [3]. In the United States, endo-
thirds of patients with AMI were treated with mere surgical explo- vascular treatment has become nearly as common therapeutic
ration or comfort care resulting in certain death. With good luck, in approach as open revascularization in AMI according to studies
one-third of the cases, the patient could be treated with bowel based on the Nationwide Inpatient Sample (NIS) by Schermerhorn,
resection yielding 50% survival. Open surgical revascularization was Lo, and colleagues [4,5]. The in-hospital mortality of American
attempted in only 7% of the cases and the results were discouraging. patients undergoing open or endovascular repair for AMI declined
The overall mortality of patients with AMI was more than 80% [2]. from 51% in year 1995 to 26% in 2010 [5].
What has changed in the past two decades? The most important However, what does not seem to have changed, is that even
evolutionary step is that today, we have the ability to perform today, according to NIS, the overall revascularization rate in AMI
was no more than 6% in the year 2010 in the United States [5]. In
another study, Beaulieu and co-workers found a total of 23744
hospital admissions for AMI registered in the NIS database from
* Corresponding author. 2005 through 2009. At that time, only 3% received an attempt at
E-mail addresses: jkarkkai@gmail.com (J.M. K
arkk
ainen), stefan.acosta@med.lu.
open (n 514) or endovascular (n 165) revascularization, while
se (S. Acosta).

http://dx.doi.org/10.1016/j.bpg.2016.10.018
1521-6918/ 2016 Elsevier Ltd. All rights reserved.
16 rkka
J.M. Ka inen, S. Acosta / Best Practice & Research Clinical Gastroenterology 31 (2017) 15e25

17% were treated with bowel resection alone, and an alarming rate
of 80% received no intervention whatsoever [6]. There are no other
large population based data of the revascularization rate in AMI, but
we can only assume that not all patients in Europe, either, get
timely diagnosis and proper treatment.
To overcome the diagnostic-related challenges in AMI, we must
rst acknowledge that AMI is not a rare entity but actually a quite
common condition in elderly patients. Second, we must understand
the complex pathophysiology and diverse clinical presentation of
the disease. The CT signs at early stages of AMI are often subtle and
difcult to detect, and therefore, the key to diagnosis is clinical
suspicion. Third, the modern treatment of AMI requires a multi-
disciplinary team of gastrointestinal surgeons, vascular surgeons,
and interventional radiologists. We need a practical etiological
categorization of AMI that will guide the treatment and a simple
algorithm for the various treatment options in different situations.

Incidence

Between 1970 and 1982 in Malmo (Sweden), autopsies were


conducted on as many as 87% of the deceased in the population of Fig. 1. The age-related incidence rates of acute mesenteric ischemia (AMI), ruptured
abdominal aortic aneurysm (RAAA), acute pancreatitis, acute appendicitis and acute
approximately 250 000 inhabitants [7]. According to this data, the
cholecystitis in Kuopio/Finland between the years 2009 and 2013 [13].
annual incidence of AMI, diagnosed at autopsy or operation, was 12
per 100 000 inhabitans. The distribution of etiology in AMI was
In the United States, the National Health and Nutrition Examination
roughly 2/3 thromboembolic occlusive mesenteric ischemia, 1/6
Survey demonstrated that warfarin use has grown 2.5 times and
non-occlusive mesenteric ischemia (NOMI), and 1/6 mesenteric
statin use has almost tripled over a decade from 1999 to 2010 [5]. The
venous thrombosis (MVT). Thus, the most common cause of AMI
increased use of oral anticoagulants may have contributed to the
was acute occlusion of the superior mesenteric artery (SMA) with
decrease in the incidence of embolic events. Between 1970 and 1982
incidence rate of 8.6/100 000/year. The SMA occlusion was caused
in Malmo , SMA embolism was the most common cause of AMI with
by embolism in 70% and thrombosis in 30% of the cases [8]. The
embolism-to-thrombosis ratio of 1.4:1 [16]. From 1993 to 2000,
incidence rate of fatal NOMI was given as 2.0/100 000/year, and the
Endean et al. reported embolism-to-thrombosis ratio of 1:1 in 58
incidence rate of MVT with intestinal necrosis was estimated at 1.8/
cohort American patients with thromboembolic AMI [17] while Ryer et al.
100 000/year [9,10]. An interesting nding in the Malmo
reported 0.6:1 ratio in 78 patients between 1990 and 2010 [18].
was that the incidence of acute SMA occlusion was 1.5 times higher
Although there is no denitive proof of any change in the etiological
than the incidence of ruptured abdominal aortic aneurysm [7].
spectrum of AMI over time, it would seem that atherosclerotic
occlusive disease is currently the most common cause of AMI [19].
Recent data on the incidence of AMI

Due to current low autopsy rates, there is no recent population- Prevalence of asymptomatic mesenteric artery stenosis
based data that would be comparable to the Malmo cohort. The
analysis of the NIS registry indicated that the incidence of AMI A patient with acute abdominal pain and chronic calcied oc-
declined from 8.4 to 6.7/100 000/year between the years 1995 and clusion of the SMA represents a special challenge for the clinician.
2010 in the United States [5]. Similarly, in two contemporary Does the patient have AMI or is the SMA occlusion just an incidental
Swedish series of AMI, the reported incidence rates of acute oc- nding? The prevalence of asymptomatic mesenteric artery ste-
clusion of the SMA were lower than during the Malmo autopsy nosis has been reported as 6e29% depending on the study [20].
study; between 5.3 and 5.4/100 000/year [11,12]. From year Unfortunately, the studies vary a great deal in terms of the popu-
2009e2013 in Kuopio (Finland), practically all patients with acute lation (e.g. American, European, Korean), the denition of mesen-
abdomen from a well-dened population of 250 000 inhabitants teric artery stenosis (e.g. the numbers of celiac artery (CA) and SMA
were treated in one institution (Kuopio University Hospital); in stenoses are often merged and not given as separate values), the
Kuopio hospital area, the incidence rate of AMI was 7.3/100 000/ grade of the stenosis included (ranging from 1 to 100%, 50e100% or
year for all etiologies and 4.5/100 000/year for occlusive AMI [13]. 70e100%), and the methods of assessing the stenosis (ultrasonog-
The incidence of AMI increased exponentially with age (Fig. 1). In raphy, angiography, CT, or autopsy). What we really would like to
patients aged over 75 years, AMI was more prevalent cause of acute know, is 1) the prevalence of SMA occlusion or hemodynamically
abdomen than appendicitis (Table 1). signicant (70%) SMA stenosis, especially in the aged population,
and 2) how many of those people have signicant concomitant CA
Changes in cardiovascular risk factors over time and inferior mesenteric artery (IMA) obstruction (i.e. 2- or 3-vessel
disease). In addition, 3) the natural outcome of chronic SMA oc-
AMI is a disease of the elderly, and the population is aging in clusion is of great interest.
Finland, Sweden, United States, and many other western countries. The current data on the prevalence of asymptomatic mesenteric
Aging of the population means more burden from cardiovascular artery stenosis is listed in Table 2. Based on the available data, the
diseases. However, interestingly, the incidence of AMI does not seem following conclusions can be drawn:
to have increased. On the contrary, it has been shown that the inci-
dence of cardiovascular events have declined, at least in Finland, and  The prevalence of a hemodynamically signicant (>70%) SMA
the prevalence of cardiovascular risk factors (smoking, serum total stenosis is approximately 2% in elderly patients aged roughly 70
cholesterol, and systolic blood pressure) have also decreased [14,15]. years or more [21,22].
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Table 1
Incidence rates (IR; n/100 000/year) of acute abdomen diagnoses for two age groups in Kuopio/Finland. This table contains unpublished data derived from previously published
studies [13,19].

Age group 75 years >75 years

Mean population 226290 inhabitants 21894 inhabitans

n/years IR 95% CI n/years IR 95% CI

AMI (all etiologies) 34/5y 3.0 2.0e4.0 56/5y 51.2 37.8e64.6


Occlusive AMI 15/5y 1.3 0.6e2.0 41/5y 37.5 26.0e48.9
Embolism 5/5y 0.4 0.1e0.8 16/5y 14.6 7.5e21.8
Atherosclerosis/thrombosis 10/5y 0.9 0.3e1.4 25/5y 22.8 13.9e31.8
NOMI 10/5y 0.9 0.3e1.4 15/5y 13.7 6.8e20.6
Acute MVT 9/5y 0.8 0.3e1.3 0/5y e
Other 3/5y 0.3 e 0/5y e
RAAA 25/5y 2.2 1.3e3.1 23/5y 21.0 12.4e29.6
Acute appendicitis 1042/5y 92.1 86.5e97.7 44/5y 40.2 28.3e52.1
Acute cholecystitis 169/2y 37.3 31.7e42.9 104/2y 238 192e283
Acute pancreatitis 193/2y 42.6 36.6e48.6 33/2y 75.4 49.6e101.1

CI, condence interval, AMI, acute mesenteric ischemia; NOMI, non-occlusive mesenteric ischemia; MVT, mesenteric venous thrombosis; RAAA, ruptured abdominal aortic
aneurysm.

Table 2
The current data on the prevalence of asymptomatic mesenteric artery stenosis (based on a Pubmed search of English literature including the past 20 years).

 In an autopsy cohort of 120 unselected Finnish subjects (mean age 62, range 18e93 years), four (3%) had >50% stenosis of the CA but none had SMA stenosis [24].
 In asymptomatic British patients undergoing abdominal ultrasonography (for unknown reasons), 18% of patients aged 65 years or more (n 97) had >70% stenosis of CA
or SMA (the rate of SMA stenosis was not reported). In patients under 65 years (n 87), only 3% had CA stenosis and none had SMA stenosis [25].
 CA stenosis rate and morphology was investigated in 400 Korean patients (mean age 57, range 17e85 years) referred for chemoembolization of hepatic tumors. More
than 50% CA stenosis with at least 10 mmHg gradient, based on angiography and CT, was found from 29 patients (7%). The cause of the stenosis was compression by
median arcuate ligament in 16, atherosclerosis in 3, and indeterminate in 10 patients [26].
 In 242 Dutch patients (median age 65 years) undergoing elective colorectal surgery, >50% CA stenosis was found in 21%, SMA stenosis in 3%, and IMA stenosis in 25%
based on preoperative CT [27].
 In 553 asymptomatic elderly American patients (mean age 77), 16% had CA stenosis and 2% had SMA stenosis dened as >70% by ultrasonography. Half of those with
SMA stenosis had also concomitant CA stenosis. None developed AMI during mean 6.5 years of follow-up [21,22].
 Out of 980 American patients with aortograms obtained for undisclosed reasons, 72 patients (mean age 68 years, range 31e95) with >50% mesenteric artery stenosis
were followed for 1e6 years. Four out of fteen patients with 3-vessel disease developed AMI, and 13 (86%) either developed AMI, had abdominal symptoms, or died
during the follow-up [23].

 In the elderly, 50e80% with SMA stenosis have concomitant degree of bowel injury in AMI [19]. A practical categorization
disease of the CA [21e23]. should guide the modern therapy. Therefore, the etiological cate-
 Isolated CA stenosis is much more common than SMA steno- gorization of AMI may need to be updated.
sis, and the etiology of isolated CA stenosis is more often
external compression by median arcuate ligament than Controversies regarding current classication of AMI
atherosclerosis especially in young people [24e27]. Isolated
CA stenosis is usually asymptomatic with the rare exception of The denition of arterial versus venous mesenteric ischemia is
median arcuate ligament compression syndrome (MALS). In clear-cut (Fig. 3). MVT is the usual cause of venous mesenteric
one study, only three of 21 patients with MALS had abdominal ischemia, and MVT is easy to detect in contrast-enhanced CT.
symptoms [28]. However, with early anticoagulation treatment, bowel ischemia is
 There are only little data on the natural outcome of asymptomatic often avoided in MVT. In other words, MVT does not automatically
mesenteric artery stenosis. It seems that isolated CA stenosis is not result in venous mesenteric ischemia [19,29].
a signicant risk factor for AMI. However, concomitant obstruc- Arterial AMI is dened as either occlusive or non-occlusive (i.e.
tion of SMA, CA and IMA is a major risk factor for symptomatic NOMI). This categorization is rather controversial. By denition,
mesenteric ischemia. In one study, as many as 86% of patients occlusive means 100% occlusion of the SMA whereas some might
with 3-vessel disease could be dened as symptomatic [23]. categorize 99% stenosis as non-occlusive. In modern practice, the
cut-off between total and near-total occlusion is impractical. First,
Etiologies and clinical presentation the differentiation of 100% versus 99% obstruction is often
impossible based on CT (as in, for example, Fig. 2C); nevertheless,
The classical etiological categorization of AMI the clinician has to choose the initial therapeutic approach based
on the CT ndings. Second, if the patient has AMI, revasculari-
Conventionally, AMI is stratied into four groups by etiology; zation is needed in both cases; total occlusion or severe stenosis.
arterial embolism, arterial thrombosis, venous thrombosis and It is generally accepted that 70% stenosis of the SMA is hemody-
NOMI [29]. Chronic atherosclerotic obstruction of the mesenteric namically signicant, and patients with concomitant severe
arteries is traditionally associated with chronic mesenteric obstruction of the CA and IMA are at risk of developing AMI upon
ischemia (CMI). This classical categorization has not evolved since chronic SMA stenosis; these cases should be categorized as
the time when angiography was the gold standard diagnostic occlusive [19,30,31].
investigation and bowel resection was the main therapeutic option. In most hospitals, it is the emergency department surgeon or
Owing to modern CT technology, we now get more information on the on-duty gastrointestinal surgeon who has to make the deci-
the morphology of the arterial obstruction (Fig. 2AeD) and on the sion whether to consult a vascular surgeon or an interventional
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of the SMA in 16%, in the root of the SMA in 39%, and in peripheral
branches in 16% of the cases (the clot location was unclassiable in
29%) [16].
In sudden embolic occlusion of the SMA root, most part of the
small intestine and right-side of the colon suffers from severe
ischemia, and the patient cannot usually survive without revas-
cularization. In about 30% of the cases, the SMA embolus is
located distal to the middle colic artery, in which case, the patient
might survive even without revascularization but may still need
massive bowel resection [16]. In embolic occlusion of a small
SMA branch, removal of the embolus is usually not possible
or necessary; the treatment is simple bowel resection of the
ischemic segment.
The risk factors for SMA embolism are atrial brillation, recent
myocardial infarction, congestive heart failure, and prior embolic
events (e.g. stroke) [32]. In addition, a new threat of mesenteric
artery embolism has emerged in conjunction with the development
of endovascular aortic repair technique extending above the
infrarenal segment. An incidence rate of 5% for bowel ischemia was
reported in a recent series from London (U.K.) of 99 patients un-
dergoing fenestrated endovascular aortic repair [33]. This serious
complication with 80% mortality was associated with shaggy
aorta, i.e. aortic irregularity and increased thrombus volume in the
paravisceral segment, and was thought to be related to graft
manipulation and catheterisation of visceral vessels.

Mesenteric arterial occlusive disease

Thrombosis represents the other half of the cases of acute SMA


Fig. 2. The different morphologies of SMA obstruction in patients with AMI. A) occlusion. Most often, acute thrombosis of the SMA is a complica-
Embolic occlusion (arrowhead) of the SMA in a 94-year old patient. B) Thrombotic tion of atherosclerotic occlusive disease. Thrombosis may also
occlusion (arrowhead) on superimposed calcied stenosis of the SMA. Incidentally, this
develop upon isolated dissection of the SMA or aortic dissection
SMA thrombosis proved to be chronic occlusion based on an earlier CT scan. The pa-
tient had AMI with bowel necrosis nevertheless. C) 99% atherosclerotic stenosis extending to the visceral arteries, but the natural history and the
(arrowhead) of the SMA without thrombosis; a narrow patent lumen was demon- treatment of these two conditions differ signicantly from the
strated in angiography. D) Chronic calcied (previously asymptomatic) occlusion atherosclerotic thrombosis, and therefore, both entities represent
(arrowhead) of the SMA that could not be recanalized by endovascular means.
their own distinct etiological category of AMI (not covered in this
Fulminant bowel and liver ischemia manifested after elective nephrectomy and the
patient was successfully treated with surgical SMA bypass and bowel resection. Cases
review). Atherosclerotic thrombus usually forms in the proximal
AeC were treated by endovascular means, and all four patients survived. SMA with superimposed high-grade stenosis or ruptured athero-
sclerotic plaque [17,19].
Unorthodoxly, we chose to rename the category of thrombosis
radiologist, or whether the treatment should go to another di- as mesenteric arterial occlusive disease (analogous to peripheral
rection without revascularization. The assessment of mesenteric arterial occlusive disease) (Fig. 3). Basically, this is a synonym for
artery stenosis and collateral circulation, based on CT, is atherosclerotic occlusive disease. In the conventional etiological
demanding even for vascular surgeons and radiologists, and may classication of AMI, the category of thrombosis is a bit contro-
be impossible for the gastrointestinal or the acute care surgeons versial, because the word thrombosis by itself includes the
who are not accustomed to interpret vascular images on a daily assumption that the arterial occlusion in AMI is always acute.
basis. Therefore, it is practical that patients who require revas- However, it is not. A signicant number of AMI patients develop
cularization as the primary treatment in AMI are categorized as acute intestinal ischemia upon chronic calcied occlusion (or se-
occlusive mesenteric ischemia (Fig. 3). In NOMI, the primary vere stenosis) of the mesenteric arteries; this is often referred to as
treatment is usually conservative (unless bowel necrosis has acute on chronic mesenteric ischemia in the literature [31]. In a series
already developed). of 37 patients with AMI caused by mesenteric arterial occlusive
disease, less than half presented with clearly visible thrombotic clot
Embolism in contrast-enhanced CT while the other half presented with
calcied obstruction of the SMA and other mesenteric arteries [19].
Acute occlusion of the SMA is the most common cause of AMI. In Thus, the atherosclerotic SMA obstruction in AMI can be either
roughly half of the cases, the acute occlusion is caused by embolism acute or chronic, and thrombotic or non-thrombotic (i.e. calcied);
that is usually of cardiac origin [17,19]. Typically, SMA embolism is these are all manifestations of the atherosclerotic vascular disease
characterized by acute onset of symptoms; the abdominal pain is (Fig. 2BeD).
severe without any localization. Pain out of proportions to the The clinical presentation of AMI caused by mesenteric arterial
clinical signs is often used to describe the early clinical presenta- occlusive disease is more varied than in embolic AMI depending on
tion in acute occlusion of previously healthy SMA. However, the the acuteness and extent of the arterial obstruction, and moreover,
clinical presentation and severity of the disease varies a great deal on the compensatory blood ow from the collateral arteries. Pa-
depending on individual anatomy and location of the occlusion in tients with acute thrombotic occlusion of the SMA may present
the mesenteric arterial tree [32]. In an autopsy study of 122 patients with fulminant bowel ischemia, or the symptoms can be insidious
with embolic AMI, the blood clot was located near the aortic ostium and obscure such as vague abdominal pain, diarrhea and vomiting.
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Fig. 3. A suggested practical etiological categorization of acute mesenteric ischemia. In occlusive mesenteric ischemia, the primary treatment approach is revascularization (red
color). In venous mesenteric ischemia and non-occlusive mesenteric ischemia, the initial treatment is usually conservative (blue color).

In slowly progressing mesenterial atherosclerosis, the collateral cholecystecomy for gastrointestinal issues without relief of symp-
arteries are often well developed and the bowel is accustomated to toms before the disease culminated in AMI. Due to the variable na-
withstanding ischemia, and therefore, it may take several days to ture of mesenteric arterial occlusive disease, the diagnosis and the
weeks before the disease evolves into irreversible bowel ischemia. presentation pattern of thrombotic AMI is much more complicated
Among the 37 AMI patients with mesenteric arterial occlusive than of embolic AMI. There are often other factors (besides the
disease, only 20% had symptoms for less than 24 hours while 40% obstruction of the mesenteric arteries) that contribute to the
had more than three days of symptoms prior to the nal diagnosis development of AMI, such as dehydration, low cardiac output, ane-
[19]. Even so, the prognosis was favorable after endovascular mia, and hypercoagulable states. Sometimes, mere uid resuscita-
revascularization especially in patients with slowly progressing tion, correction of anemia, and administration of antibiotics may
AMI. The mythical six-hour limit until irreversible bowel necrosis reverse the acute ischemic process, but even so, the patient will
occurs in AMI can go down to history. And even though time is remain at risk of recurrent AMI unless treated with revascularization.
bowel, there is no general rule as to how long the bowel can stay Acute-on-CMI should be suspected in patients with acute
viable in atherosclerotic occlusive AMI. abdominal pain, or slowly progressing abdominal symptoms, and
prior history of other manifestations of the atherosclerotic vascular
Acute on chronic mesenteric ischemia disease (i.e. coronary artery disease, peripheral arterial occlusive
disease, cerebrovascular disease). Patients with progressive symp-
Prior history of CMI (postprandial abdominal pain, fear of eating, toms of CMI are at high risk of developing AMI at any given day and
and weight loss) is common in the acute-on-chronic presentation should be treated accordingly. The situation is comparable to acute
pattern of AMI. These premonitory symptoms have been reported coronary syndrome. If a patient has chest pain and ischemic EKG
prior to the nal admission in 25e84% of patients with AMI caused changes at rest, the risk of acute myocardial infarction is eminent.
by mesenteric arterial occlusive disease [3,31]. In a contemporary Similarly, if abdominal pain persists after a meal, the patient may
series of 55 such patients, up to 80% were initially misdiagnosed and already have gone into an irreversible state of acute intestinal
inappropriately treated at hospital with medical therapy [31]. ischemia. Angiography and revascularization has to performed ur-
Some patients had even undergone exploratory laparotomy or gently, regardless of whether the target is coronary or mesenteric
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arteries. Inammatory markers (C-reactive protein) is often strik- complications such as portal hypertension and hypersplenism may
ingly elevated only after 24 hours of continuous symptoms in the develop several months after the acute thrombotic event
acute-on-chronic condition [34]. Metabolic acidosis indicates that (Fig. 5BeD) [36]. The treatment of acute MVT aims at ensuring
irreversible bowel necrosis may already have developed. blood return from the intestine until sufcient venous collaterals
develop. The therapeutic options range from simple anti-
Non-occlusive mesenteric ischemia (NOMI) coagulation to invasive catheter-directed thrombolysis, and very
rarely, surgical venous thrombectomy may be needed. During the
In systemic circulatory failure, the blood ow is redistributed to course of treatment, the superior mesenteric vein either recanalizes
vital organs, and consequently, vasoconstriction of the mesenteric or obliterates.
arteries may cause severe intestinal hypoperfusion despite the
mesenteric arteries being patent. This is called NOMI. The potential Diagnostic examinations
clinical scenarios in which NOMI can develop are severe heart failure,
hypovolemia, sepsis, use of vasoconstrictive medication (inotropes) Laboratory tests
or intra-aortic balloon pump, hypotension caused by dialysis or
major surgery (especially cardiac or aortic surgery), and abdominal Classically, patients with AMI have leukocytosis, metabolic
compartment syndrome [35]. The diagnosis of NOMI can be acidosis, elevated D-dimer, and elevated serum lactate. The chal-
extremely challenging especially in patients that are intubated and lenge is that the conventional laboratory tests are very unspecic at
mechanically ventilated in the intensive care unit. In early NOMI, the presentation such as leukocytosis or D-dimer. None of them can be
initial treatment is usually conservative and aims at restoring in- used to rule in the possibility of AMI. D-dimer may be used as an
testinal perfusion by treating the underlying condition. Worsening exclusion test, where a negative test very likely excludes acute
metabolic acidosis and distended abdomen may indicate the need thromboembolic occlusion of the SMA at presentation [37,38].
for laparotomy. The role of imaging in NOMI is to rule out occlusive Arterial lactate is often negative in the early phase of AMI. In a study
mesenteric ischemia and to detect signs of bowel gangrene (Fig. 4). In of 50 AMI patients, half had negative lactate values at admission [3].
the Malmo autopsy cohort, there were 62 patients with fatal NOMI, The arterial lactate level rises when the liver is unable to clear it
of whom 25 (40%) had stenosis of the SMA and 14 of those subjects anymore, and when the test is positive, there may already be
had concomitant stenosis of the CA [9]. Although there was no advanced irreversible bowel ischemia without possibilities to save
indication whether or not those lesions were hemodynamically the ischemic bowel with revascularization [39]. A biomarker
signicant, in retrospect, it may be argued that those patients were capable of detecting early hypoperfusion in AMI, when irreversible
misclassied since NOMI essentially excludes signicant mesenteric bowel injury has not yet developed, would be of great clinical value.
artery stenosis. Anyhow, endovascular stenting is an option to Unfortunately, there are currently no standardized blood tests that
consider whenever signicant SMA stenosis complicates NOMI. could be used widely in patients with acute abdominal pain to
screen for AMI in such way as the troponin test is used for screening
Mesenteric venous thrombosis (MVT) acute myocardial infarction in patients with acute chest pain [38].
Known pitfalls at admission are referring AMI patient with
MVT is dened as acute thrombosis of the superior mesenteric elevated troponin test to a cardiologist or making incorrect diag-
vein and its branches with or without extension of the thrombus to nosis because of elevated pancreas amylase or abnormal liver test.
the portal vein (Fig. 5A). Intestinal ischemia rarely develops unless These abnormal laboratory tests are relatively common in AMI [40].
the peripheral veins of the mesentery (venous arcades and vasa In Kuopio (Finland), nearly 30% of patients with AMI were rst
recta) are involved. Thus, isolated portal vein thrombosis seldom referred to an internist at the emergency department due to cardiac
causes bowel infarction. In acute MVT, mild intestinal oedema may comorbidities or obscure symptoms (e.g. diarrhea and vomiting)
gradually develop into arterial spasm and transmural bowel [3]. A few patients were rst seen by a neurologist either because of
infarction within days to weeks. A subacute form of MVT de- simultaneous embolic stroke and SMA embolism, or transient
velops gradually within several weeks and the pain may be mild, ischemic attack and acute-on-CMI. Thus, AMI is not exclusively
sometimes accompanied by (bloody) diarrhea. In chronic MVT, surgeons' headache.

Fig. 4. A young obese patient with severe respiratory failure due to unknown respiratory infection. CT showed dilated colon (white arrowheads), diminutive aorta (black
arrowhead), and narrow SMA (white open arrowhead) as a sign of severe NOMI, mesenteric vasoconstriction and septic shock. In laparotomy, the entire colon appeared to be
gangrenous and the colon was resected following damage control principles. Unfortunately, the patient died a month later due to many complications associated with prolonged
invasive ventilation in the intensive care unit.
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Fig. 5. A) This previously healthy 40-year old patient with acute MVT (white arrowheads) and oedematous small bowel segment (white open arrowheads) was treated with
anticoagulation alone for six months. The patient was screened negative for hypercoagulable disorders, and the MVT was determined as idiopathic. Unfortunately, ve years later,
although the patient had patent MVT (B), the portal vein was occluded with cavernomatous transformation of the hepatoduodenal ligament (C; black arrowheads). The patient
developed severe portal hypertension and hypersplenism (B; asterisk) with pancytopenia and oesophageal varices (D). The liver function remained normal.

Imaging closer look at the individual studies in the two reviews revealed
that the studies were performed exclusively in patients with clin-
CT has replaced conventional angiography as the gold standard ical suspicion of AMI, and roughly 70e100% of the study patients
imaging modality in AMI. Digital subtraction angiography is an had advanced bowel ischemia (i.e. AMI that was diagnosed at
invasive procedure that is currently used to perform therapeutic laparotomy or autopsy, or withdrawal of active treatment that
interventions more commonly than just plain diagnostics. The resulted in rapid death) [44e50]. In practice, AMI is rarely sus-
utility of duplex ultrasound is limited to screening for CMI. Ultra- pected prior to imaging. Furthermore, the goal is to detect AMI
sound is not recommended in AMI (if CT is available). It is time before advanced bowel ischemia has developed. At early phase of
consuming and of limited diagnostic value; visualizing the the disease, CT ndings are much more subtle and difcult to
mesenteric vessels is often obscured by extensive bowel gas that is detect. In two recent studies from Sweden and Finland with total of
associated with intestinal paralysis in AMI. Gadolinium enhanced 147 AMI patients, the suspicion of AMI was mentioned in the CT
magnetic resonance imaging can be used to detect proximal referral in only one-third of the cases and more than 70% of the CTs
obstruction of the SMA and CA, but it has less value in the evalu- were performed in venous phase alone [19,51]. The sensitivity of CT
ation of distal arterial occlusions and other intestinal ndings in in AMI was no more than 67e85% in these two studies that were
AMI [41]. Moreover, magnetic resonance imaging takes too much performed in the clinical routine in patients with unclear acute or
time in a severely ill patient. Plain radiographs are not useful in subacute abdomen; half of the patients with AMI had advanced
AMI; gas in the portal veins is a sign of extensive intestinal pneu- bowel ischemia (dened as above) whereas the other half had
matosis and implies that bowel necrosis has developed. reversible bowel ischemia.
Thus, without clinical suspicion of vascular disease, the routine
Accuracy of CT CT of the acute abdomen will be performed in venous phase alone
[52]. Nevertheless, most of the vascular and intestinal ndings can
When AMI is suspected, CT should be performed with contrast be detected from the venous phase images. What seems to be more
enhancement in arterial and venous phases (the biphasic protocol) important than the contrast enhancement protocol is clinical sus-
[41]. The arterial phase (with 1 mm slice thickness) enables accu- picion, which is a major factor in the correct interpretation of the CT
rate detection of vascular pathology and detailed reconstructions of ndings in AMI [19,51]. A study of 97 AMI events from Finland
the main mesenteric arteries and even collaterals. The venous demonstrated that the initial CT report was correct in 97% of the
phase is required for the assessment of bowel wall and solid organ cases where the clinician had mentioned AMI suspicion in the CT
perfusion, and other pathology. The sensitivity and specicity of referral, and where not, the corresponding rate was only 81%
biphasic CT in AMI has been estimated as 89e100% in two sys- (p 0.04). Also, the need for bowel resection was signicantly
tematic reviews [42,43]. However, this may be an overestimate. A higher in the latter group [19]. Direct inquiry for mesenteric
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ischemia encourages the radiologist to examine and report even CT ndings may be minimal; the signs to look for are those related
the faintest intestinal and vascular abnormalities. However, it to bowel necrosis. Sometimes, irregular narrowing (i.e. vasospasm)
should be mandatory that the radiologists assess and report the of the SMA and mesenteric arcades may be visible in NOMI, but it is
patency of the mesenteric vessels routinely in the abdominal CT difcult to detect in CT (Fig. 4). Diminutive aorta and inferior vena
evaluation, not only when asked to. cava in CT are signs of severe systemic shock in NOMI [53,54].
Synchronous embolism (e.g. in arm, leg, brain, or abdominal
Ischemia-specic CT ndings in AMI solid organs) was found in 68% of patients with SMA embolism in
the Malmo autopsy study [16]. Synchronous embolism within the
CT ndings in AMI can be either specic or non-specic for artery of spleen, liver or kidney may not be visible in CT, but
bowel ischemia (Table 3). Decreased or absent bowel wall enhance- sometimes it can be detected as uneven perfusion pattern, i.e., solid
ment is probably the most specic CT sign of intestinal ischemia organ infarction. Solid organ infarction is found in CT in 15e36% of
with 96% specicity, but it has very low sensitivity (16e62%) [52]. patients with AMI, and not exclusively in patients with embolism
Sometimes, the bowel wall may become abnormally hyper- but also in patients with mesenteric arterial occlusive disease
enhanced in AMI, for example, during reperfusion conditions [44,46,50].
following occlusive AMI or NOMI. Impaired venous drainage of
contrast medium in MVT may also cause increased enhancement of Can patient have AMI even in absence of ischemia-specic CT
the bowel wall. Pneumatosis intestinalis have been reported in ndings?
6e28% of cases with AMI and portomesenteric venous gas in 3e14%
[52]. Although pneumatosis is very specic for bowel ischemia, it In a study of 27 patients with AMI caused by mesenteric arterial
has low sensitivity, and pneumatosis does not yet prove that the occlusive disease, contrast-enhanced CT and conventional digital
bowel damage is irreversible. subtraction angiograms were obtained from all patient; twenty
patients with intermittent CMI were used as a control group, and all
Non-specic CT ndings in AMI images were blindly evaluated by three experienced radiologists
knowing that the patients were suspected of mesenteric ischemia
A very common but probably the least specic nding in AMI is [34]. In this study, one third of patients with AMI presented without
bowel wall thickening. In contrast, the bowel wall may become any ischemia-specic CT signs (dened as thrombotic SMA clot,
dilated and paper thin in transmural infarction [53]. Mesenteric fat absent or decreased bowel wall enhancement, or pneumatosis).
stranding is caused by oedema of the mesentery, and a small There were moderate to substantial interobserver variability in the
amount of ascites can be found in many patients with AMI. Another CT interpretation of these ndings. Another interesting observation
very common but unspecic CT nding is luminal dilatation of the in that study was that the presence of ischemia-specic CT signs
small (or large) bowel which is caused by intestinal paralysis in was noted in 77% of patients who required bowel resection, but also
AMI. in 50% of patients who did not need bowel resection (after endo-
The vascular CT ndings are not direct signs of bowel ischemia vascular revascularization). Hence, neither pneumatosis nor
but represent the etiology in AMI. An embolic or thrombotic clot of decreased bowel wall enhancement are denitive signs of irre-
the SMA usually suggests acute arterial occlusion, and therefore, is versible bowel necrosis. In contrast, the study showed that all pa-
considered a strong sign of AMI. Chronic occlusive mesenteric tients with AMI had at least some level of abnormal intestinal
atherosclerosis is not a specic nding and may be incidental. ndings in their CT scans, such as mesenteric fat stranding in 96%,
However, if the SMA and the other mesenteric arteries are severely bowel lumen dilatation in 93%, and bowel wall thickening in 70%.
obstructed, and there are associated intestinal ndings (specic or Only few of the control group patients with CMI had such ndings
unspecic), AMI is a likely cause of acute abdominal pain. Thus, as (due to chronic ischemic colitis) [34].
discussed before, the chronic state may eventually become acute In conclusion, the answer to the question whether a patient may
without visible thrombosis in CT. Sometimes, the acute thrombotic have AMI even in absence of ischemia-specic CT ndings is yes.
clot is so small that it cannot be visualized by imaging [19]. Nevertheless, unspecic intestinal CT ndings can usually be
Intraluminal lling defect and engorgement of the superior detected, but these ndings are easily disregarded in the CT analysis
mesenteric vein together with mesenteric oedema are indications without the clinical suspicion of AMI. The same applies to patients
of acute MVT in a patient with acute abdominal pain. In NOMI, the with NOMI as well [19]. In case of SMA embolism, the embolic clot

Table 3
Computed tomography (CT) ndings in acute mesenteric ischemia (AMI).

Specic
 SMA embolus (oval shaped clot in a previously unaffected artery)
 SMA thrombosis (blood clot with superimposed calcied lesion)
 Mesenteric venous thrombosis (with surrounding oedema of the mesentery)
 Unenhanced or poorly enhanced bowel wall segment(s)
 Intestinal pneumatosis
 Portal venous gas
Non-specic
 Chronic calcied occlusion or hemodynamically signicant (70%) stenosis of the SMA
 Concomitant severe obstruction of CA and/or IMA (2- or 3-vessel disease)
 Abnormal (increased) enhancement of the bowel wall
 Bowel wall thickening (oedema, hyperdense hemorrhage)
 Luminal dilatation of the intestine (paralysis, transmural bowel necrosis)
 Mesenteric fat stranding
 Ascites
 Free gas (bowel perforation)
 Solid organ infarction (synchronous embolism or organ hypoperfusion)
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is the most specic CT nding. In a study including 24 patients with atherosclerotic etiology was twice as common cause of AMI as
embolic AMI, the embolic clot was detected in CT in all expect two embolism. Another distinctive difference between these two age-
patients with distal small branch embolism [19]. In ve of the 24 groups was the higher incidence of MVT in the younger popula-
cases with SMA embolism, neither decreased bowel wall tion. Patients with MVT were signicantly younger (mean age 53
enhancement nor pneumatosis could be detected by an experi- years) than patients with arterial AMI (mean age 76e79 years) [19].
enced radiologist. Unsurprisingly, the elderly patients had more cardiovascular
comorbidities and the in-hospital mortality was higher.
Characteristics of AMI in elderly patients In the analysis of the two age groups with AMI (Table 4),
younger patients were more prone to undergo bowel resection
As shown in Fig. 1, the spectrum of differential diagnoses in than the elderly patients (although the difference was not statis-
acute abdomen is very different in the elderly than in the younger tically signicant). This may be due to the higher proportion of
patients. The incidence of AMI is roughly 10-fold in 80-year-old acute-on-chronic presentations of AMI among the elderly. It was
people versus in 60-year-old population [8,13]. The proportion of shown that these patients with slowly progressing disease had
patients with atherosclerotic etiology of AMI is signicantly higher better outcome after emergency endovascular revascularization
in the elderly (Table 4). Based on the Kuopio cohort, embolic eti- than patients with fulminant AMI [3]. Perhaps the most important
ology of AMI was as common as mesenteric arterial occlusive dis- message of this review is that there is only a small step from CMI to
ease in patients aged 75 years or less. In patients over 75 years, the AMI. This is relevant especially when interpreting CT ndings of an

Table 4
Characteristics of 95 patients with acute mesenteric ischemia (AMI) stratied by age. This table contains unpublished data derived from a previously published study [19].

Age group 75 years (n 36) >75 years (n 59) pa

Comorbidities
Age, mean standard deviation, years 63 10 83 5 <0.001
Sex, male 29 (81) 16 (27) <0.001
Obesity (body mass index 30 kg/m2) 12 (33) 9 (15) 0.050
Hypertension 16 (44) 44 (75) 0.004
Hyperlipidemia 9 (25) 24 (41) 0.182
Diabetes 12 (33) 14 (24) 0.484
Chronic renal insufciency 1 (3) 3 (5) 1.000
Atrial brillation 8 (22) 24 (41) 0.065
Coronary artery disease 10 (28) 31 (53) 0.020
Peripheral arterial disease 10 (28) 14 (24) 0.808
Chronic heart failure 3 (8) 12 (20) 0.153
Stroke or transient ischemic attack 6 (17) 20 (34) 0.068
Recent major surgery (30 days) 1 (3) 6 (10) 0.247
History of DVT or pulmonary embolism 1 (3) 2 (3) 1.000
Medication
Warfarin 5 (14) 11 (19) 0.778
Acetylic salicylic acid 14 (39) 37 (63) 0.034
Clopidogrel 2 (6) 4 (7) 1.000
Statin 15 (42) 33 (56) 0.208
AMI etiology
Embolism 8 (22) 16 (27) 0.594
Mesenteric arterial occlusive disease 9 (25) 28 (48) 0.029
Non-occlusive mesenteric ischemia 10 (28) 15 (25) 0.800
Mesenteric venous thrombosis 9 (25) 0 (0) <0.001
Clinical characteristics
Duration of symptoms
<24 hours 13 (36) 18 (31) 0.654
1e3 days 11 (31) 23 (39) 0.509
>3 days 12 (33) 18 (31) 0.822
Acute kidney injury 5 (14) 10 (17) 0.778
Acute myocardial infarction 1 (3) 4 (7) 0.647
Clinical AMI suspicion prior to imaging 8 (22) 21 (36) 0.251
Primarily admitted to surgical emergency unit 27 (75) 43 (73) 0.502
Diagnostic delay, median (IQR), hours 5.5 (2e29) 13.3 (2e24) 0.750
Laboratory ndings
WBC count, median (IQR), 109/L 12.9 (10e19) 13.0 (9e17) 0.378
CRP, median (IQR), mg/L 145 (31e207) 149 (30e213) 0.936
Plasma creatinine, median (IQR), mmol/L 76 (62e106) 78 (62e112) 0.840
GFR <30 ml/min/1.73m2 4 (11) 7 (12) 1.000
Metabolic acidosis 11 (31) 12 (20) 0.321
Therapy and outcome
Endovascular therapy 13 (36) 35 (59) 0.028
Surgical revascularization 0 (0) 2 (3) 0.524
Laparotomy 18 (50) 20 (34) 0.120
Bowel resection 15 (42) 15 (25) 0.098
Massive unresectable bowel necrosis 2 (6) 3 (5) 0.921
In-hospital death 7 (19) 23 (39) 0.047

Data are presented as n (%) unless otherwise stated.


DVT, deep vein thrombosis; IQR, interquartile range; WBC, white blood cell; CRP, C-reactive protein; GFR, glomerular ltration rate.
a
Fisher's exact test or the chi-squared test was used to compare nominal data and the ManneWhitney U test for nonparametric data.
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elderly patient with prolonged abdominal symptoms and elevated symptoms of acute-on-CMI are often obscure; the early CT ndings
inammatory markers (C-reactive protein); if there are abnormal are difcult to interpret and easily missed. The current role of
intestinal ndings (listed in Table 3) and severe calcied obstruc- biomarkers in the early diagnosis of AMI is limited. Although
tion of several mesenteric arteries (SMA being the most important), normal D-dimer may exclude acute thromboembolic occlusion of
the patient is likely suffering from acute episode of mesenteric the SMA and acute MVT, it is not known, how the D-dimer behaves
ischemia and needs emergent revascularization. in acute-on-chronic presentation of AMI, or in NOMI.

Do we need to fear contrast-induced renal failure?

Chronic renal insufciency and acute kidney injury are consid- Practice points
ered as risk factors for contrast-induced renal failure in patients
with CT performed for acute abdominal pain. On the other hand, CT  Acute occlusion of the SMA should be suspected in pa-
without contrast enhancement is associated with diagnostic delay tients with acute abdominal pain and atrial fibrillation,
and increased mortality in AMI [51]. Among the 95 Finnish AMI acute or recent cardiac infarction, prosthetic heart valve,
patients with CT obtained prior to treatment, only 5% of patients or other synchronous embolic event (e.g. stroke, limb
with arterial AMI had chronic renal insufciency prior to admission embolism, spleen infarction).
[19]. The prevalence of acute kidney injury at admission (prior to  AMI should be suspected in patients with acute or sub-
imaging) was 13% and 40% in AMI patients with mesenteric arterial acute abdominal pain (diarrhea/vomiting), and prior
occlusive disease and NOMI, respectively; none of the patients with manifestations of the atherosclerotic vascular disease
SMA embolism or MVT had acute kidney injury. In general, the risk (e.g. coronary heart disease, peripheral vascular disease,
of contrast-induced renal failure in patients with AMI is negligible cerebrovascular disease), or prior symptoms of CMI.
especially if the patient has had normal kidney function before  CT of the acute abdomen should be performed with
falling ill [55]. The acute kidney injury in AMI is usually caused by contrast enhancement, without fear of contrast-induced
the disease itself, especially in NOMI. AMI patients are often nephropathy, if severe illness is suspected. The visceral
dehydrated because of bowel paralysis, vomiting and diarrhea. vessels and associated intestinal findings should be
Intravascular administration of isotonic crystalloids should be assessed and reported routinely by radiologists.
started prior to imaging. At discretion, CT can be performed with  Acute occlusion of the SMA is the most common cause of
reduced amount of contrast agent in patients with impaired renal AMI. However, some patients develop AMI upon severe
function. However, contrast-enhanced CT should not be denied to a chronic occlusive disease of the mesenteric arteries. In
severely ill patient because of the fear of contrast-induced renal these patients, even the unspecific CT findings together
failure; as a consequence, the inevitable delay in the diagnosis of with prolonged symptoms and elevated inflammatory
AMI is a greater risk. In some situations, the rst image acquisition markers are suspicious of acute intestinal ischemia.
can be performed without contrast enhancement, and if the diag-  CMI patients with progressive symptoms and severe
nosis is not apparent in the unenhanced CT (e.g. cholecystitis, weight loss are at eminent risk of developing fulminant
appendicitis, diverticulitis, or pancreatitis), the examination should AMI. These patients require rapid revascularization, with
be continued immediately with contrast-enhanced protocol. similar urgency as patients with acute coronary
syndrome.
Prognosis

An active endovascular-rst strategy in Kuopio with 76%


revascularization rate resulted 42% overall mortality rate in pa- Research agenda
tients with occlusive AMI [3]. In comparison to the previous 82%
mortality for AMI in Finland, this is a signicant improvement [2].  The utility of the next generation dual-energy CT in
Even so, it has to be individually considered, when the aggressive increasing visualization of the differences between
treatment is futile and doomed to result in unnecessary suffering. ischemic and perfused bowel segments should be
Due to the old age and comorbidities in AMI patients, the long- investigated in human patients with AMI.
term survival is poor regardless of the treatment. The most frag-  Research in the field of biomarkers should be targeted to
ile and severely ill patients should be treated with adequate discover a blood test capable of detecting early intestinal
comfort care alone. hypoperfusion (NOMI) in patients requiring treatment in
the intensive care unit for any underlying disease or
Summary surgery.

AMI appears to be relatively common in elderly patients e more


common than appendicitis in patients aged over 75 years (Table 1).
This is important to acknowledge, because clinical suspicion is Conict of interest
a major factor in the early diagnosis AMI and in the correct inter-
pretation of CT ndings. If AMI is suspected, contrast-enhanced CT None.
should be performed without fear of contrast-induced nephropa-
thy, preferably in arterial and venous phases. Clinicians should be
aware that the clinical presentation of AMI varies a great deal Acknowledgements
depending on the etiology, and moreover, on the presentation
pattern of the arterial obstruction. The management and prognosis The authors would like to acknowledge Interventional Radiol-
of patients with acute occlusion of the SMA, acute-on-CMI, and ogist of Finland society and Rattima
ki Cardiovascular Society for
intermittent CMI are different, and these conditions should be funding the writing of this review. The funders did not have any
distinguished. CMI may insidiously evolve to AMI, and the role in the making of this manuscript.
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