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73

Original communication

Endovascular stent placement for


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isolated superior mesenteric artery


dissection with intestinal ischaemia
Baochen Liua, Chengnan Chua, Xinxin Fan, Weiwei Ding, and Xingjiang Wu
1
Research Institute of General Surgery, Jinling Hospital, Medical School of Nanjing University, Nanjing, China
a
These authors contributed equally to this paper

Summary: Background: Isolated superior mesenteric artery dissection (ISMAD) is rare, especially when associated with
intestinal ischaemia. We report our clinical experience managing this condition. Patients and methods: Medical records
from 22 patients with ISMAD and intestinal ischaemia were retrospectively analysed. Conservative treatment was given to
all patients as first line therapy. Subsequently, 15 patients received endovascular stent placement and three patients re-
ceived endovascular stent placement plus intestinal resection and anastomosis. Results: After conservative treatment,
the symptoms of three patients were remarkably relieved; however, a repeat contrast CT showed that stenosis was aggra-
vated. Hence, endovascular stent placement was performed in all 15 patients. Enteral nutrition was successfully restored
in 12 patients. Three patients showed signs of chronic intestinal ischaemia, including peritonitis and ileus. These patients
underwent intestinal resection and anastomosis. Enteral nutrition was restored at postoperative week two. No signs of
intestinal ischaemia recurred during two-years of follow-up. Conclusions: We recommend endovascular stent placement
as a feasible, effective, and minimally invasive procedure in patients with ISMAD and symptoms of intestinal ischaemia.

Keywords: Isolated superior mesenteric artery dissection, intestinal ischaemia, endovascular, stent placement

Introduction Patients and methods


Isolated superior mesenteric artery dissection (ISMAD) is Patients
a rare disease. Although its reported incidence is merely
0.06 % [1], it can cause severe intestinal ischaemia, intes- This retrospective study was conducted at our national in-
tinal infarction, and even death [2]. Early diagnosis and testinal stroke centre, which was set up in October 2010.
treatment of ISMAD is ideal. Identification of ISMAD has So far, 207 intestinal shock patients have been recorded in
been facilitated by the development of imaging technol- our centre. The medical records of consecutive patients
ogy, such as computer tomography angiography (CTA). with superior mesenteric artery (SMA) dissection who re-
Management is aimed at symptom relief and prevention ceived treatment during July 2010 to July 2016 were as-
of intestinal necrosis. Treatment involves a variety of op- sessed. Patients with ISMAD and intestinal ischaemia
tions, including conservative, surgical revascularization were included. Patients with SMA dissection associated
or endovascular approaches. with aortic or other visceral arteries were excluded.
To date, the natural history of ISMAD is not well under- Patients’ demographic and clinical characteristics,
stood because of the rarity and complexity of the condition including age, sex, medical history, risk factors, symp-
[3]. Furthermore, there is no consensus on management toms, Sakamoto’s classification, and follow-up period
guidelines [4–12]. The objective of this retrospective study were recorded.
was to describe our single-centre experiences with ISMAD
and intestinal ischaemia.
Diagnostic work-up and categorization

A contrast-enhanced CTA was performed on patients with


acute-onset abdominal pain when common causes were
excluded. An initial diagnosis of ISMAD was made accord-

© 2018 Hogrefe Vasa (2019), 48 (1), 73–78


https://doi.org/10.1024/0301-1526/a000738
74 B. Liu & C. Chu et al., Treatment for ISMAD

ing to clinical manifestations and the presence of an iso- Results


lated SMA wall dissection on abdominal CTA.
The entry and re-entry sites of the dissection, dissection Patient characteristics
length, patency, and degree of luminal stenosis at the dis-
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sected segment of the SMA were assessed on CTA images. Twenty-six consecutive patients with SMA dissection were
ISMAD was categorized into four types based on Sakamo- eligible for this study. After exclusion of patients with SMA
to’s classification [13]. Type I: Patent true and false lumen dissection associated with aortic or other visceral arteries
that shows entry and re-entry sites. Type II: Patent true lu- (n  =  2) and patients who rejected treatment (n  =  2), the
men but no re-entry flow from the false lumen. Type III: medical histories of 22 patients (19 male and three female)
No visible false luminal flow (thrombosis false lumen), with ISMAD were retrospectively reviewed.
causing true luminal narrowing. Type IV: SMA dissection The mean age of the included patients was 51 ± 7 years
with occlusion of the SMA. (range, 38–67 years). All patients were admitted because
of ISMAD. Among them, seven patients were asympto-
matic dissections (31.8 %) (Table I), while the other 15 pa-
Therapeutic regimens and follow-up tients were symptomatic dissections (68.2 %) (Table II).
The accompanying symptoms included nausea (n  =  8),
All patients received conservative treatment for three vomiting (n = 5), fever (n = 1), bloody stool (n = 1), and radi-
to five days, including blood pressure control (under ating pain to the back (n  =  1). Risk factors in the eligible
130/80 mmHg for patients with hypertension), anticoag- patients included hypertension (n  =  11; 50 %), smoking
ulants (subcutaneous injection of low-molecular-weight (n = 10; 45.5 %), arteriosclerosis (n = 2; 0.1 %), and diabe-
heparin calcium (4000 IU) q12h during hospitalization), tes (n = 3; 13.6 %). Results of laboratory tests were within
complete bowel rest, and parenteral nutrition. For asymp- normal reference ranges, except for low albumin levels in
tomatic and symptom relief patients, follow-up CTA was six patients (27.3 %) and a high C-reactive protein level in
usually performed at one week, two weeks, one month, four patients (18.2 %). All patients attended follow-up vis-
and six months after admission, and annually thereafter its in the outpatient clinics; mean follow-up period was
according to protocol. For patients with aggravated ab- 16 ± 10 months (range, 3–40 months) (Table I, II).
dominal pain, CTA was immediately performed for re- All patients were diagnosed with ISMAD by CTA, the
view. If abdominal pain was relieved, and the CTA showed primary entry site was around the curvature of the SMA.
no progress in the dissection, the conservative treatment The median distance from the primary entry tear to the
was continued. If there was no abdominal pain relief or ostium of the SMA was 21 ± 6 mm (range, 8–32 mm). Ac-
there was pain relief but disease progression on CTA, pa- cording to Sakamoto’s classification[13], four patients were
tients underwent endovascular stent placement (ESP). type I (18.2 %), 10 patients were type II (45.5 %), six pa-
Patients who underwent ESP were instructed to gradually tients were type III (27.3 %), and two patients were type IV
restore enteral nutrition. At this time, exploratory laparot- (0.1 %).
omy was performed if there were signs of peritonitis or After conservative treatment, none of the asympto-
intestinal obstruction. matic patients (100 %) showed progress in dissection af-
Follow-ups were conducted in the outpatient clinic at ter repeated CTA. Three of the symptomatic patients
one and six months and every 12 months thereafter. CTA (20 %) were remarkably relieved of their symptoms. Ac-
findings and clinical manifestations were obtained to as- cording to Sakamoto’s classification, they are type I
sess treatment outcomes. (33.3 %), type II (33.3 %), and type III (33.3 %), respec-

Table I. Clinical characteristics of asymptomatic patients.

Patients Age (years)/ Symptoms Risk factors Sakamoto’s Treatment Conservative Follow-up
gender classification Treatment result months

1 44/M – Smoking II Conservative treatment Success 6

2 51/M – Hypertension II Conservative treatment Success 8

3 47/F – – II Conservative treatment Success 12

4 49/F – Hypertension III Conservative treatment Success 18

5 42/M – Hypertension Smoking IV Conservative treatment Success 40

6 62/M – Hypertension Smoking IV Conservative treatment Success 16

7 57/M – Diabetes I Conservative treatment Success 5

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B. Liu & C. Chu et al., Treatment for ISMAD 75

Table II. Clinical characteristics of symptomatic patients.

Patients Age (years/ Symptoms Risk factors Sakamoto’s Treatment Outcome Follow-up
gender) classification months
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1 38/M Abdominal pain, Hypertension II ESP Pain resolution 6


nausea, vomiting

2 41/M Abdominal pain Hypertension smoking II ESP Pain resolution 8

3 59/M Abdominal pain Smoking II ESP Pain resolution 12

4 53/M Abdominal pain Hypertension Smoking III ESP Pain resolution 18

5 48/M Abdominal pain Diabetes IV ESP Pain resolution 40

6 53/M Abdominal pain, – IV ESP + surgery Pain resolution 16


fever, nausea, vomiting,

7 54/M Abdominal pain, Hypertension I ESP Pain resolution 5


nausea, vomiting

8 55/M Abdominal pain, Hypertension III ESP Pain resolution 7


nausea, vomiting Smoking

9 45/M Abdominal pain Hypertension III ESP Pain resolution 38

10 49/M Abdominal pain Hypertension Smoking III ESP Pain resolution 10


radiating to the back

11 61/M Abdominal pain, nausea, – III ESP + surgery Pain resolution 12


vomiting, bloody stools

12 51/F Abdominal pain, nausea – III ESP + surgery Pain resolution 14

13 67/M Abdominal pain, nausea Smoking II ESP Pain resolution 8

14 48/M Abdominal pain, nausea Diabetes II ESP Pain resolution 3

15 44/M Abdominal pain, Traumatic Smoking II ESP Pain resolution 18

ESP: Endovascular stent placement.

tively. However, a CTA performed on the 14th day after Discussion


admission showed that stenosis was aggravated (Figure
1). Conservative treatment failed to relieve abdominal The rare disease, ISMAD, was first reported in 1947 by Bau-
pain in the other 12 symptomatic patients. ersfeld [1]. With increasing use of contrast-enhanced CT
ESP was performed successfully in all 15 patients scans for abdominal patients, ISMAD has been reported
(8 × 60  mm bare mental stent, BARD, in six patients; more frequently in recent years [14]. While potential aetio-
6 × 60  mm bare mental stent, BARD, in seven patients; logical factors of ISMAD are identified in the literature and
6 × 40 mm bare mental stent, BARD, in two patients). Be- include arteriosclerosis, medial degeneration of the arterial
cause of the too narrow angle between aorta and SMA wall, trauma, and inflammation [15, 16], the exact cause re-
(< 45°), three of the patients were changed to the brachial mains unclear. Therefore, a treatment guideline for patients
approach, while the other remained in the femoral ap- with ISMAD has not yet been established. This study pre-
proach group. There were no treatment-related complica- sents a case series of patients with ISMAD to provide more
tions. Abdominal pain was alleviated after the procedure information on the management of this condition.
and disappeared gradually within three to five days. The pathogenesis of ISMAD may include shearing stress
Enteral nutrition was gradually restored in all 15 pa- of the SMA [17]. In our case series, the primary entry site of
tients. During this time, three (20 %) patients showed signs the dissection was located at the proximal segment of the
of chronic intestinal ischaemia, including peritonitis, ileus, SMA. This segment is the transition portion, connecting
and a rapid decrease in albumin levels. Infusion of human the fixed segment under the pancreas to the unfixed seg-
serum albumin failed to increase albumin levels. CT scan ment at the mesenteric root. Due to this anatomical struc-
indicated partial intestinal ischaemia and intestinal wall ture, the anterior wall may be subject to abnormal shearing
oedema. Surgery was performed and nonviable bowel was stress, resulting in ISMAD.
resected. Abdominal pain and signs of peritoneal irritation Sakamoto et al. categorized ISMAD into four types de-
disappeared on postoperative day one to two. Enteral nutri- pending on CT imaging [13]. According to our study, each of
tion was successfully restored within two weeks. these types was associated with persistent abdominal pain,
At the last follow-up, all patients were alive and had ex- which could not be relieved by conservative treatment, as
perienced no recurrence of symptoms. well as symptoms related to intestinal ischaemia. These

© 2018 Hogrefe Vasa (2019), 48 (1), 73–78


76 B. Liu & C. Chu et al., Treatment for ISMAD

findings indicate that the selection of a therapeutic regimen mia or intestinal necrosis. The stented cases in our series
should not be based on imaging findings alone [18, 19]. showed no procedure-related complications, pain was re-
Conservative treatment is recommended as first-line solved in three to five days, and all stents were patent on
therapy for ISMAD [4, 20, 21]. In the current study, all pa- CTA during the follow-up period. The covered stent was
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tients received conservative treatment, including hypo- reported to be used to repair the dissection [25]. In our
tensive and antiplatelet medication, bowel rest, intrave- opinion, bare stents are more suitable. Covered stents can
nous fluids, and nutritional support. Abdominal pain was more easily cover the SMA branches, affecting the blood
markedly relieved in 20 % of patients, but CTA revealed supply of the intestine.
that the compression of true lumen became more serious. Three patients in our case series are particularly nota-
These findings are in accordance with a previous study ble. After stent placement, during the reperfusion period,
[22]. In contrast, Park et al. [20] reported on 53 ISMAD these patients experienced bloating, diarrhoea and hypo-
patients who received conservative treatment as first-line proteinaemia, and enteral nutrition could not be restored.
therapy. Over a 23-month period of follow-up, the extent CT scan showed lesions confined to a short length of the
of the false lumen was diminished in 41.3 % of patients, intestine, which developed into an intestinal stenosis (Fig-
the length of the dissection was diminished in 23.9 % of ure 2). The patients suffered protein losing enteropathy
patients, and the dissection was completely remodelled in [26,  27]. As intestinal stenosis was limited, intestinal re-
15.2 % of patients. Cho et al. [4] found similar results in 15 section and anastomosis were performed; 30–60  cm of
ISMAD patients who received conservative treatment. the intestine were resected. In these cases, ESP was par-
These data suggest that most patients with ISMAD can be ticularly important. ESP can result in immediate revascu-
successfully managed with conservative treatment. This larization, therefore, a suspicious ischaemic intestine can
approach likely failed in our symptomatic patients because be rescued. Performing laparotomy or fenestration lapa-
they were suffering from intestinal ischaemia, which re- rotomy without ESP makes it difficult to ensure the intes-
sulted in persistent abdominal pain, and/or signs of perito- tine will remain viable. These three patients returned to
neal irritation. However, taking both symptomatic and their normal diet within 15–20 days. During follow-up, no
asymptomatic dissection into consideration, we received intestinal necrosis, morbidity or mortality developed in
similar results as in Park’s and Cho’s studies. In the studies these patients and CTA revealed the stents to be patent.
of Park et al. [20] and Cho et al. [4], 17.4 and 43.3 % of the
patients, respectively, were asymptomatic. In our study,
the percentage was 31.8 %. Therefore, ISMAD, especially
asymptomatic dissection, can be successfully managed in Limitations
first-line therapy.
Endovascular treatment of an isolated SMA dissection Three major limitations exist in our study. First, it was a
has been first reported by Leung [23], and since then, nu- retrospective review. Second, the absence of other treat-
merous studies of stent placement for spontaneous iso- ment groups, which do not allow for direct comparison
lated dissection of SMA have been reported [24]. Unlike with other strategies. Finally, the number of patients was
conservative treatment, endovascular therapy can imme- relatively small and the duration of the follow-up was re-
diately relieve mesenteric ischaemia and prevent further latively short. Prospectively randomized clinical studies
progression. We performed stent placement as our pa- with a large number of patients and long follow-ups are
tients were symptomatic and because dissection of the needed to explore whether the endovascular treatment is
SMA can rapidly progress into chronic intestinal ischae- appropriate in terms of patients’ long-term outcome.

Figure 1. Patient 2, Computer tomography angiography (CTA).


A: Isolated superior mesenteric dissection; B: after two weeks of conservative treatment, the true lumen was more compressed; C: three months
after endovascular stent placement, the true lumen was patent and there was revascularization.

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B. Liu & C. Chu et al., Treatment for ISMAD 77
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Figure 2. CTA
A: An isolated superior mesenteric dissection;
B: signs of intestinal ischaemia, including
severe intestinal expansion, and intestinal
oedema, in several segments of the bowel;
C: SMA trunk and branches 14 days after
placement of the bare-mental stent;
D: CT lesions in a short segment of the intes-
tine, which became an intestinal stenosis;
F: a deterministic intestinal resection and
anastomosis were performed. Defected
intestinal mucosa and oedema of the intesti-
nal wall in the resected segment; F: six-month
follow-up demonstrating patency of true
lumen and flow in the branches.

Conclusions 5. Jia ZZ, Zhao JW, Tian F, Li SQ, Wang K, Wang Y, et al. Initial and
middle-term results of treatment for symptomatic spontane-
ous isolated dissection of superior mesenteric artery. Eur J
ISMAD with symptoms of intestinal ischaemia is chal- Vasc Endovasc Surg. 2013;45(5):502–8.
lenging to manage. Our case series indicates that ESP can 6. Kim HK, Jung HK, Cho J, Lee JM, Huh S. Clinical and radiologic
provide immediate relief of mesenteric ischaemia and course of symptomatic spontaneous isolated dissection of the
prevent further progression. For those patients who un- superior mesenteric artery treated with conservative manage-
ment. J VASC SURG. 2014;59(2):465–72.
derwent intestinal resection, ESP shortens the length of 7. Zerbib P, Perot C, Lambert M, Seblini M, Pruvot FR, Chambon
resection and ensures the intestine remains viable. We JP. Management of isolated spontaneous dissection of supe-
recommend ESP as a feasible, effective, and minimally rior mesenteric artery. Langenbecks Arch Surg. 2010;395(4):
invasive procedure in patients with ISMAD and symp- 437–43.
8. Wu XM, Wang TD, Chen MF. Percutaneous endovascular treat-
toms of intestinal ischaemia. ment for isolated spontaneous superior mesenteric artery dis-
section: report of two cases and literature review. Catheter
Cardiovasc Interv. 2009;73(2):145–51.
9. Gobble RM, Brill ER, Rockman CB, Hecht EM, Lamparello PJ,
Jacobowitz GR, et al. Endovascular treatment of spontaneous
Acknowledgments dissections of the superior mesenteric artery. J Vasc Surg.
2009;50(6):1326–32.
Supported by the National Natural Science Foundation of 10. Wu B, Zhang J, Yin MD, Wang L, Song JQ, Li X, et al. Isolated su-
China (Grant No. 81770532, Dr. Weiwei Ding) and Jiangsu perior mesenteric artery dissection: case for conservative
treatment and endovascular repair. Chin Med J (Engl). 2009;
Province Medical Foundation for Youth Talents (Grant 122(2):238–40.
No. QNRC2016901, Dr. Weiwei Ding). 11. Froment P, Alerci M, Vandoni RE, Bogen M, Gertsch P, Galeazzi
G. Stenting of a spontaneous dissection of the superior mes-
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vent Radiol. 2004;27(5):529–32.
12. Yoon YW, Choi D, Cho SY, Lee DY. Successful treatment of isolated
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