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Indian J Gastroenterol (MarchApril 2014) 33(2):169174

DOI 10.1007/s12664-013-0377-3

CASE SERIES

Chronic mesenteric ischemia and therapeutic paradigm


of mesenteric revascularization
Shashidhar Kallappa Parameshwarappa & Ajay Savlania &
Sidharth Viswanathan & Srinivas Gadhinglajkar &
Kapilamoorthy Tirur Raman & Madathipat Unnikrishnan

Received: 26 April 2013 / Accepted: 29 July 2013 / Published online: 31 August 2013
# Indian Society of Gastroenterology 2013

Abstract Chronic mesenteric ischemia is a life-threatening


clinical problem resulting in death from inanition and/or bowel infarction, if left untreated, albeit low disease prevalence.
Typical presentation is postprandial abdominal pain, severe
weight loss, and altered bowel habit. Surgical revascularization of the superior mesenteric artery provides effective longterm treatment for chronic intestinal ischemia. Eleven patients
underwent superior mesenteric artery revascularization, nine
of them with open retrograde superior mesenteric artery bypass and two with angioplasty and stenting. All patients
except one made a satisfactory recovery in this cohort. Major
complication included one graft thrombosis leading to bowel
ischemia and death. The rest all recovered weight in 3
6 months with a follow up period of 6 to 28 months. Two
patients had recurrence of symptoms due to failing bypass
requiring stenting for assisted primary patency. Superior mesenteric artery revascularization can be performed with minimal morbidity and mortality, providing excellent symptom
relief and quality of life.
Keywords Gastrointestinal tract . Superior mesenteric artery .
Vascular disease
S. K. Parameshwarappa : A. Savlania : S. Viswanathan :
M. Unnikrishnan (*)
Division of Vascular Surgery, Department of Cardiovascular and
Thoracic Surgery, Sree Chitra Tirunal Institute for Medical Sciences
and Technology, Medical College PO, Trivandrum 695 011, India
e-mail: unni@sctimst.ac.in
S. Gadhinglajkar
Department of Cardiac Anaesthesia, Sree Chitra Tirunal Institute
for Medical Sciences and Technology, Medical College PO,
Trivandrum 695 011, India
K. T. Raman
Department of Imaging Sciences and Interventional Radiology,
Sree Chitra Tirunal Institute for Medical Sciences and Technology,
Medical College PO, Trivandrum 695 011, India

Introduction
Chronic mesenteric ischemia (CMI) is a life-threatening
clinical problem resulting in death from inanition and/or
bowel infarction, albeit low disease prevalence. The underlying initial pathophysiology involves failure to achieve
postprandial hyperemic intestinal blood flow with insidiously worsening ischemia eventually leading to bowel
gangrene. In normal individuals, intestinal blood flow
increases right from a cephalic phase, with a maximal
increase occurring in 30 to 90 min [1]. This hyperemic
response lasts between 4 and 6 h and varies with size and
composition of the meal [1, 2]. The majority of the
hyperemic blood flow goes to the small bowel and pancreas, with only a small proportion to the stomach and
colon [3].
Most patients develop sufficient collateral circulation to
the intestine to prevent ischemic symptoms. When the
superior mesenteric artery is occluded, the pancreatic duodenal arteries supply blood via the hepatic and gastroduodenal arteries to the bowel. When the celiac artery and
superior mesenteric artery (SMA) are occluded, the inferior
mesenteric artery supplies blood to the small bowel via the
left colic branch. A large meandering mesenteric artery, an
important vessel in the collateral circulation from the inferior mesenteric artery, is frequently seen. Symptoms usually
occur only if two or more vessels are occluded or critically
stenosed.
Although clinical triad of postprandial abdominal pain,
weight loss, and altered bowel habits of CMI is theoretically
described, this clinical entity goes underdiagnosed for a long
duration till all the other causes for abdominal pain are ruled
out, with inordinate delay, and the patients health status has
deteriorated seriously. This case series documents the safety
and efficacy of mesenteric revascularization in the treatment
of chronic mesenteric ischemia and its effect on body mass
index (BMI).

170

Methods
The clinical data of all patients who underwent major arterial
intervention with involvement of mesenteric vessels at the
Sree Chitra Tirunal Institute for Medical Sciences and Technology, from November 2010 to October 2012, were retrospectively analyzed. Specifically excluded were patients who
had mesenteric ischemia of embolic origin and nonocclusive
mesenteric ischemia and those asymptomatic patients detected
on imaging during repair of abdominal and thoracoabdominal
aortic aneurysms. The atherosclerotic nature of the lesion was
determined on review of age, risk factors, atherosclerotic
plaque in the aorta and the iliac arteries on preoperative
noninvasive imaging (Fig. 1), and operative notes. Eleven
patients underwent mesenteric revascularization, 10 for atherosclerotic disease and 1 for Stanford B aortic dissection with
malperfusion. Nine of them underwent open retrograde surgical revascularization of SMA, and two underwent angioplasty
with stenting. All were males except a lone lady in this cohort
with age ranging from 41 to 69 years with mean age of
56.45 years. Preoperative weight varied from 32.8 to 61.6 kg
with mean of 46.73 kg, and BMI, from 14.34 to 21.31 with
mean of 17.56. Three patients had associated extreme
aortoiliac occlusive disease with subcritical lower limb ischemia at presentation, one had Stanford B aortic dissection with
bowel malperfusion, one had renovascular hypertension due
to renal artery stenosis, and one had type B descending thoracic aortic aneurysm. In surgical group, five patients had all
three vessels occluded, and four patients had two vessels
occluded, ie. SMA and celiac artery (CA) with significant
stenosis of the inferior mesenteric artery (IMA). In
endovascular group, one patient had SMA and CA stenosis.
One patient had high-grade SMA stenosis only (Table 1).
Duplex evaluation was standard in our protocol, and
256-slice CT angiogram was done before planning

Fig. 1 Volume rendered image showing ostial occlusion of the celiac


artery, SMA and IMA. Multiple collaterals filling up the celiac artery,
SMA and IMA from internal iliac and lumbar arteries

Indian J Gastroenterol (MarchApril 2014) 33(2):169174


Table 1 Demography and materials
Patient demographics
N
Age range in years, range (mean)
Sex (M/F)
Risk factors/comorbidities
Hypertension
Diabetes
Dyslipidemia
Smoking
COPD
Preoperative weight in kg (mean)
Preoperative BMI (mean)
Associated vascular disease
AI occlusion
Type B aortic dissection
Renal artery stenosis
Type B DTA aneurysm
Vessel involvement
SMA, CA, IMA occluded
SMA, CA occluded, IMA stenosed
SMA, CA stenosis
SMA stenosis

11
4169 (56.45)
10:01
8
4
6
10
2
46.73
17.56
3
1
1
1
5
4
1
1

BMI body mass index, AI aortoiliac, DTA descending thoracic aorta,


COPD chronic obstructive pulmonary disease, SMA superior mesenteric
artery, CA celiac artery, IMA inferior mesenteric artery

revascularization (Fig. 1). Surgical procedure involved midline transperitoneal laparotomy and dissection of the SMA
at the root of mesentery behind the duodenum. Inflow
taken from the infrarenal aorta, right common iliac artery,
or right limb of the aortobifemoral graft and outflow to the
SMA behind the duodenum at the root of mesentery
(Fig. 2ad). The internal iliac artery was used as a conduit
in six and coated Dacron in one, and two had composite
graft of the internal iliac artery and Dacron.
In endovascular group, the first patient underwent SMA and
bilateral renal artery stenting with 6 mm 12 mm and
5 mm 12 mm balloon mounted nitinol stents for SMA and
renal arteries, respectively. Second patient had thoracic
endovascular aortic repair with the Medtronic Valiant
42 mm 169 mm aortic stent graft along with SMA and celiac
artery angioplasty with stenting using 6 mm 19 mm and
7 mm 12 mm, balloon mounted bare metal nitinol stent,
respectively (Fig. 3).
All patients were followed up by a duplex flow to mesenteric vessels at 1 and 6 months and yearly thereafter following
procedure. Outcomes were measured by a symptomatic relief
and an increase in weight and BMI (Table 2). Follow up CT
angiogram at 1 year showed patent SMA bypass graft
(Fig. 4).

Indian J Gastroenterol (MarchApril 2014) 33(2):169174

171

Table 2 Methods, results, follow up, and complications


Methods and Results
Surgical group
Procedure executed
SMA bypass alone
Concomitant AF+SMA bypass
Graft used
IIA
Dacron
Composite (Dacron+IIA)
Endovascular group
Procedure executed
TEVAR+SMA+celiac artery stenting
SMA+renal artery stenting
Follow up (months)
Postoperative weight in kg (mean) at 6 months
Postoperative BMI (mean) at 6 months
Mean gain in weight (kg)/BMI
Complications
Mortality
Graft stenosis

6
3
6
1
2

1
1
628
51.95
19.67
5.22/2.11
1
2

AF aortofemoral, IIA internal iliac artery, TEVAR thoracic endovascular


aortic repair, BMI body mass index, SMA superior mesenteric artery

Results
All patients except one made satisfactory recovery in both the
groups. Major complication included one graft thrombosis
leading to bowel ischemia and death 3 weeks following surgery. The rest all recovered weight in 36 months in a follow
up period of 628 months. Mean gain in weight and BMI at
6 months were 5.22 and 2.11 kg, respectively. Two patients in
a long-term follow up, who continued to smoke, developed
Fig. 2 a Dissection and harvest
of the right internal iliac artery. b
Preparation of internal iliac artery
conduit for aortaSMA bypass. c
End-to-side anastomosis of
internal iliac conduit to SMA
behind the duodenum and end-toside anastomoses to the right limb
of aortobifemoral bypass graft for
concomitant aortoiliac occlusive
disease. d Completed SMA
bypass with internal iliac artery
conduit

Fig. 3 Angioplasty and stenting of SMA and celiac artery

recurrence of symptoms. These two patients had composite


graft of the internal iliac artery and Dacron. In these two
patients, the internal iliac artery was diseased, so it was
endarterectomized before using as a conduit for bypass. CT
angiogram showed smooth narrowing that corresponds to the
iliac segment of the prostheticinternal iliac composite SMA
graft. The distal SMA showed delayed filling from celiac collaterals (Fig. 5a). These two patients required angioplasty with
stenting to obtain assisted primary patency of the graft,

172

Fig. 4 Follow up CT angiogram at 1 year showing patent SMA bypass


graft

successfully; 7 mm 40 mm self-expandable nitinol stent was


deployed, and was further dilated using a 7 mm x 40 mm
balloon (Fig. 5b, c). Symptoms improved in these patients
following the procedure, and they remain symptomatic
(Table 2).

Discussion
Atherosclerosis is the leading cause of the visceral artery
occlusive disease responsible for chronic mesenteric ischemia.
A variety of other causes, including fibromuscular disease,
aortic dissection, isolated SMA dissection, neurofibromatosis,
rheumatoid arthritis, Takayasus arteritis [4], giant cell arteritis, polyarteritis nodosa, radiation injury, Burgers disease, and
systemic lupus, has been reported.
Fig. 5 a Smooth narrowing of an
internal iliac artery component of
composite graft delayed filling of
SMA from celiac branches. b
Angioplasty and deployment of
7 mm 40 mm self-expandable
nitinol stent. c Post-stent
angiogram showing reinstated
graft flow to SMA

Indian J Gastroenterol (MarchApril 2014) 33(2):169174

Patients with chronic mesenteric ischemia usually


undergo an extensive and protracted evaluation before
the ultimate correct diagnosis. This usually includes an
esophagogastroduodenoscopy, colonoscopy, ultrasound,
and computed tomography, and it is common for patients to undergo appendicectomy as well cholecystectomy.
Usually more than a year passes between the onset of symptoms and the correct diagnosis. These patients are usually
misdiagnosed and treated as gastric/duodenal ulceration,
gastroparesis, gastroduodenitis, gallbladder dysmotility, and
even renal calculi.
The majority of patients referred to our department with
chronic mesenteric ischemia have already undergone an extensive, prolonged work up, and the diagnosis is already
reached though with inordinate delay.
Significant steno-occlusive disease in all three visceral
vessels represents high-risk group for bowel infarction [5].
All patients with symptomatic CMI should undergo revascularization. The goal is to augment the mesenteric flow so to
relieve abdominal pain, to prevent bowel infarction, and to
restore nutritional status. The indication for revascularization
in asymptomatic patients with known visceral artery occlusive
disease is still unclear.
The optimal treatment (endovascular or open) for patients
with CMI remains unresolved. Significant advances have
occurred over the past several years, with an increased emphasis on the endovascular approach, which has become a
first-line therapy in many institutions due to theoretical advantages of a shorter hospital stay (or outpatient procedure),
reduced morbidity and mortality, and improved quality of life
[6]. However, there are no randomized controlled trials comparing the two approaches; nevertheless, the long-term vessel
patency rates appear to be inferior to those obtained with open
revascularization.
Feasibility of stenting or open surgery in our study was
dictated by the type of lesion and atherosclerotic load, whether
high-grade stenosis or ostioproximal long-segment occlusion;
hence, the two modalities could not be strictly compared in
our cohort.

Indian J Gastroenterol (MarchApril 2014) 33(2):169174

Several recent trials comparing the outcomes after


endovascular and open treatment for chronic mesenteric ischemia have suggested that the endovascular approach should be
used selectively and restricted to higher-risk patients who
cannot tolerate open repair [79] or as a bridge to open
revascularization whenever feasible by allowing time to optimize the patients comorbidities and nutritional status [7].
Ostioproximal long-segment occlusion mandates surgical
bypass for treatment. The critical ongoing issues with regard
to open revascularization remain unresolved as well. These
include the type of revascularization, the number of vessels to
be vascularized, and the optimal conduit.
Mesenteric bypass, either antegrade multivessel bypass
from the supraceliac aorta or isolated retrograde SMA revascularization from the infrarenal aorta or common iliac artery,
has emerged as the most common options, with the current
debate focusing on the specific configuration. The advantages
of antegrade bypass include the fact that the supraceliac aorta
is usually uninvolved with atherosclerosis and that the limbs
of the graft follow a direct path while maintaining a prograde
flow. Disadvantages are the technically challenging nature,
and complications like hemodynamic instability and renal
ischemia are more. The advantages of retrograde bypass include the fact that infrarenal aortacommon iliac artery can be
exposed more easily faster, is less hemodynamic instability,
and is generally more familiar to most vascular surgeons.
Multivessel revascularization offers the hypothetical advantage that if one of the graft limbs (or stents) occludes, the
patient may not necessarily develop recurrent symptoms or
acute intestinal ischemia. Proponents of isolated retrograde
bypass to the SMA emphasize that the procedure
revascularizes the primary vessel of concern predominantly,
if not the exclusive SMA, and that multivessel reconstructions
add to the complexity of the procedure. Moreover, concomitant aortofemoral bypass as required in three out of nine
surgical patients curtails prudent revascularization of the critically mandated SMA. Cunningham et al. reported an 86 %
symptom-free rate at 5 years after surgical revascularization of
a single vessel, ie. superior mesenteric artery even in patients
with multiple-vessel occlusions [10].
Both prosthetic and autogenous conduits have been used
for the various mesenteric bypass procedures, although reports
comparing their long-term patency rates have been somewhat
inconclusive [11]. Notably, Kihara and colleagues reported
that patency rates for vein grafts were significantly lower than
those for prosthetic grafts [12]. Hence, it is our choice of
autologous internal iliac artery.
Technical success rates exceed 90 % in the most recent
endovascular series [7, 8, 1315] and are essentially close to
100 % for open repair [79, 16]. Both the endovascular and
open approaches are successful in terms of relieving symptoms, with early symptom relief rates exceeding 80 % for
endovascular treatment [14, 15] and 90 % for open

173

revascularization [17]. Objectively, documented patency rates


are significantly lower after endovascular treatment as compared to open surgical revascularization. However, perioperative morbidity, mortality, and hospital stay rates are significantly lower for the endovascular approach. Limitations of our
study are that the numbers are small, follow up is midterm,
and comparison between open and endovascular procedure
was not meaningful.
In our series of 11 patients, two had angioplasty with
stenting, and nine, open surgical graft to SMA; one patient died
due to subacute graft thrombosis and bowel gangrene after
discharge. All the others including two patients, who required
reintervention, are symptom free and keep good health.

Conclusion
SMA revascularization for CMI was performed with minimal
morbidity and mortality providing excellent symptom relief
and quality of life in medium term except in one patient.
Endovascular, whenever feasible, should be the preferred
option for combined viscerorenal occlusive disease as well
associated aortic aneurismal disease. BMI significantly improves in 6 months following surgery. In our experience
where composite graft has been used, the diseased, so
endarterectomized iliac artery component of the composite
graft had significant stenosis in the follow up period. Angioplasty with stenting is viable and effective salvage procedures
for assisted primary patency of failing SMA bypass grafts.

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