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Page 1: Subacute Superior Mesenteric Artery Embolization with ... · Subacute Superior Mesenteric Artery Embolization with Bowel Infarction ARare Complication of Catheterized Angiography

Subacute Superior Mesenteric Artery

Embolization with Bowel Infarction � A Rare

Complication of Catheterized Angiography

Tung-Lin Tsui,1,2 Teng-Fu Tsao,4 Yao-Tsung Chuang,2,3 Hsiang-Lin Lee5 and Chun-Hung Su2,3

Cholesterol embolization syndrome (CES) is an atheroembolization caused by cholesterol crystals from aortic

atheromatous plaques. The reported incidence of CES as a complication of catheterized angiography, which usually

presents as acute renal failure and blue toe syndrome, is low in clinical studies. Only a small number of CES cases

presenting as acute mesentery artery occlusion after invasive catheterization have been reported. We report a case of

a 73-year-old man with CES-caused subacute mesenteric artery occlusion followed by life-threatening bowel

infarction; 24 hours after catheterized carotid angiography, he was successfully treated by emergent operation.

Key Words: Catheterized angiography � Cholesterol embolization syndrome � Complication � Ischemic

bowel disease

INTRODUCTION

The rates of life-threatening complications such as

catheter-related cardiac arrhythmia and vessel perfora-

tion have been low in non-interventional angiography.

Cholesterol embolization syndrome (CES) is an athero-

embolization caused by cholesterol crystals from aortic

atheromatous plaques. It was first reported in 1945 by

Flory and may involve eyes, kidneys, and extremities.1,2

Complications from angiography such as blue toe syn-

drome or acute renal failure have been reported.3-5 CES

often occurs after a vascular procedure in patients with

systemic inflammation. Even though it is not a rare oc-

currence, only a minority of patients can be clinically

recognized; the clinical characteristics of CES and actual

incidence of this syndrome remain uncertain. Estimates

of the incidence of CES after vascular procedures have

ranged from 0.15% in clinical studies4 to 25% to 30% in

pathologic series.3 Only a few cases6,7 presented with

acute superior mesenteric artery embolization as a com-

plication of invasive catheterizations; the incidence is

unknown, and there is an extremely high mortality rate,

which may be up to 93%.6 Here, we present a case of

CES-caused subacute superior mesenteric artery occlu-

sion followed by bowel infarction after a catheterized

carotid angiography, which was quickly diagnosed and

successfully treated with emergent operation.

CASE REPORT

A 73-year-old man presented with right leg clau-

dication and dizziness for a period of 2 weeks. He had a

long history of hypertension, type 2 diabetes mellitus

and dementia for more than ten years with regular me-

dical control. The initial heart rhythm in ECG showed

Acta Cardiol Sin 2011;27:60�4 60

Subacute Superior Mesenteric Artery EmbolizationCase Report Acta Cardiol Sin 2011;27:60�4

Received: May 12, 2010 Accepted: October 7, 20101Intensive Care Unit, Puli Christian Hospital, Nantou; 2Institute of

Medicine, Chung Shan Medical University; 3Cardiac Intensive Care

Unit, Division of Cardiology, Department of Internal Medicine;4Diagnostic Radiology; 5Division of General Surgery, Chung Shan

Medical University Hospital, Taichung, Taiwan.

Address correspondence and reprint requests to: Dr. Chun-Hung Su,

Division of Cardiology, Department of Internal Medicine, Chung

Shan Medical University Hospital and Institute of Medicine, Chung

Shan Medical University, No. 110, Jian-Guo N. Rd., Sec. 1, Taichung

402, Taiwan. Tel: 886-4-2375- 7426; Fax: 886-4-2473-9220; E-mail:

[email protected]

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normal sinus rhythm, and the coagulation profile was

normal in prothrombin time, activated partial thrombo-

plastin time, and platelet count. There was neither sign

nor clinical history of hypercoagulation state. Therefore,

we did not check fibrinogen and fibrin degradation

products. On closer examination, the patient’s right fe-

moral pulsation could not be detected, and Doppler

exam revealed total occlusion of the left internal carotid

artery. He was then admitted for diagnostic angiography.

Catheterized angiography was arranged via a left

transfemoral approach. Total occlusion of the left inter-

nal carotid artery and diffuse atherosclerosis with 95%

stenosis over the right external iliac artery were de-

tected, which were compatible with both the carotid

Doppler examination and clinical manifestations. An im-

mediate percutaneous transluminal angioplasty (PTA) of

the right iliac artery was indicated to prevent critical

right leg ischemia. The right iliac artery lesion was

crossed by a 0.035 cm � 150 cm guide-wire (Terumo),

and then PTA was performed by deployment of a 10 �

49-mm Wall-stent (Boston Scientific) followed by an 8 �

40-mm Smash balloon (Boston Scientific) for secondary

dilatation at maximal 8 atm. The final angiography re-

vealed 5% residual stenosis with optimal distal blood

flow. At the time we finished this procedure, the patient

did not feel abdominal pain, and there were no signifi-

cant complications.

However, about 18 hours after the procedure, the pa-

tient started to complain of abdominal distension and

poor appetite. On physical examination, mild abdominal

tenderness without muscle guarding or rebounding pain

was detected. In the following 2 hours, tachycardia

(heart rate: 120 beats per minute), shock (a gradual sys-

tolic blood pressure decrease from 160 to 120 mmHg)

and fever (body temperature: 37.8 �C) were detected.

The patient developed a disoriented consciousness, and

livedo reticularis was found bilaterally over the lower

extremities. A complete blood cell count revealed leu-

kocytosis (white blood cell count: 10,640/mm3) with an

extremely left-shifting and young cell presentation (seg-

ments: 36% and bands: 57%). Additionally, serology

analysis showed a high C-reactive protein (CRP) con-

centration (17.7 mg/dl) and acute renal failure. Arterial

blood gas revealed metabolic acidosis. Given the impres-

sion of septic shock, the patient was transferred to inten-

sive care unit 20 hours after procedure.

We surveyed possible sources of infection and de-

tected no significant evidence of pneumonia, pyuria, or

subcutaneous wound infection. Gastric fluid drained

from the nasogastric tube revealed positive for occult-

blood. Abdominal distension was found, and abdominal

sonography showed dilated bowel lumen without either

ascites or intra-abdominal abscess formation. Emergent

abdominal computed tomography (CT) scan for further

infection surveillance showed multiple mixed non-calci-

fied and calcified plaques along the wall of the ab-

dominal aorta and loss of contrast enhancement in some

of the superior mesenteric artery and vein branches. In

addition, diffuse segmental and distended small bowel

loops were also found (Figures 1A, B). The CT scan

suggested the possibility of ischemic bowel disease. Ap-

proximately 24 hours after the procedure, operation was

performed and a large part of the ischemic and conges-

tive intestine (from the jejunum to the descending colon)

was resected (Figure 2A). The pathology report of the

resected small intestine and colon also revealed a diffuse

ischemic infarct with focal hemorrhage, which con-

firmed the diagnosis (Figure 2B).

Both hemodynamic status and toxic signs improved

significantly after the operation. The patient was ob-

served as having returned to alert consciousness 8 hours

after the operation, and he was successfully weaned

from mechanical ventilation. He was transferred to

general ward on the 4th post-operation day, and an oral

diet was started on the 6th post-operation day. Although

anorexia and bilateral gangrenous toes were noted, there

were no more clinical septic signs seen as of 120 days

after the operation.

DISCUSSION

Atheromatous material may dislodge either from

atherosclerotic debris within the thoracic aorta spon-

taneously or from manipulation of the aorta during car-

diac surgery or angiography. However, the actual mecha-

nism of how inflammation leads to CES is unknown.

Most commonly, embolism is thought to result from

dislodgement of atheromatous material as the catheter is

manipulated across areas of severe atherosclerosis within

the aorta. The abdominal aorta is one of the most heavily

involved areas containing atherosclerotic plaques; there-

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fore, procedures involving catheter-related mechanical

injury to these regions could potentially disrupt plaque

material and induce CES. Therefore, the frequency of

CES should be decreased if procedures are performed

via the brachial artery approach. In our patient, PTA of

the right external iliac artery was performed in the

downstream site of the mesenteric artery. Thus, we be-

lieved the CES and bowel infarction was caused by the

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Tung-Lin Tsui et al.

Figure 1. (A) Coronal reconstructed contrast-enhanced CT scan shows multiple bowel loop dilatation with loss of the normal wall enhancement

(white arrows), multiple plaques with or without calcification (black arrows) along the wall of abdominal aorta. A linear air density (white

arrowhead) noted in one of the right mesenteric vein is thought to be a possible venous gas embolism due to bowel ischemia and necrosis. The right

iliac artery (black arrowheads) is high-density change due to a metallic stent in place. (B) Oblique thin-labeled maximum-intensity projection of a

contrast-enhanced CT scan shows the filling defects (white arrows) in the jejunal and ileal branches of the superior mesenteric artery. The thrombi

(white arrowheads) are also noted in some branches of the superior mesenteric vein.

Figure 2. (A) The photograph of the resected small intestine (from jejunum) to the descending colon reveals grossly diffuse distended and ischemic

bowel wall. In addition, hemorrhage and congestion were noted over omentum with some engorged vessels. (B) Sections of the bowel show varying

degrees of ischemic or hemorrhagic infarction with necrotizing inflammation, villi or mucosal sloughing, severe congestion, edema and/or

submucosal hemorrhage, as well as severe serosal congestion. Evidence of intimal thickening is seen in sections of the medium-sized muscular

arteries.

A B

A B

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carotid angiography procedure.

Among 1,786 consecutive patients in one prospec-

tive study,2 25 patients were diagnosed as having CES

(1.4%); 12 patients were diagnosed with definite CES,

and 13 patients were diagnosed with possible CES. The

in-hospital mortality rate was 16.0% (4 patients) among

patients with CES, which was significantly higher than

in those without CES (0.5%, p < 0.01). Although the in-

cidence of catheter-related embolism has been low in

clinical studies, the incidence of embolism after cardiac

catheterization in necropsy studies has been reported to

be as high as 30%.3 Acute coronary syndromes and

multivessel coronary artery disease are univariate pre-

dictors of CES. Hypertension, smoking, cerebrovascular

disease, and aortic aneurysm are also associated with an

increased post-procedure CES risk. No significant dif-

ferences in atrial fibrillation, hypercholesterolemia, and

diabetes mellitus were found between patients with and

without CES. The elevated baseline CRP level was an

independent predictor of CES (> 1.0 mg/dl).

In another study, an embolic event temporally re-

lated to femoral catheterization occurred in 10 (17%) of

59 patients with atherosclerotic aortic debris compared

to 2 (3%) of 71 control patients without atherosclerotic

aortic debris (p = 0.01).8 This may also imply the exis-

tence of debris as a risk factor of CES: interestingly, no

patients with atherosclerotic aortic debris who under-

went brachial catheterization had an embolic event.8 The

strongest correlation of aortic debris in the clinical litera-

ture has been between advanced age and peripheral vas-

cular disease, which is similar to our case. Our patient

received carotid angiography by a femoral approach, and

severe atherosclerotic aortic debris was confirmed by

abdominal CT, which is compatible with previous re-

ported risk factors for catheter-related CES.

Clinical manifestations of CES range from mild to

catastrophic. In the ACC/AHA guidelines for percu-

taneous coronary intervention, “definite CES” is defined

as a patient who has cutaneous signs including livedo

reticularis, blue toe syndrome, and digital gangrene with

or without renal impairment. In our patient, livedo

reticularis and acute renal failure were noted 18 hours

after the procedure, but possibly caused by septic shock.

Specifically, the CES presented with subacute me-

senteric artery occlusion and bowel infarction. In addi-

tion, CES also caused gangrene in the toes that was

found 5 days subsequently. Although a pathologic study

did not find any definite cholesterol crystals in the

mesenteric artery, the diagnosis of CES should be seri-

ously considered. The other possibility, namely throm-

bus formation caused by routine premedication of he-

parin 5000 units, was thought to be low; however, we

could not exclude this possibility completely. Staphylo-

coccus Lugdunensis endocarditis may cause bowel is-

chemia which related to possible embolization, but there

was no positive blood culture for infective endocarditis

or echocardiographic evidence of endocardial involve-

ment in this patient.9

Despite the availability of aggressive means to man-

age acute ischemic events, the prognosis of patients with

catheter-related embolisms remains poor. The reported

mortality rate among patients with catheter-related em-

bolism has been reported to be between 16% and

81%.2,4,8,10 The mortality rate was higher in elderly pa-

tients and patients with peripheral vascular disease.

In patients without detected aortic cholesterol de-

bris, the risk of CES wasn’t different between trans-

femoral approach and transradial approach.2 Invasive

aortic procedures are planned in a patient with echo-

cardiographically-detected atherosclerotic aortic debris

(especially mobile aortic debris); the risk of embolism

can be significantly reduced by substituting brachial for

femoral catheterization and by avoiding intra-aortic bal-

loon pump placement.8 Better understanding and early

recognition of CES will reduce patient mortality and

morbidity after cardiac catheterization. Transesophageal

echocardiography (TEE) images of the aorta can be used

to assess the risk of embolism.8 In our patient, we ar-

ranged carotid and right iliac angiography for both

definite diagnosis and simultaneous PTA after Doppler

exam and physical examination. TEE is an invasive pro-

cedure, and not usually performed before angiography.

If CT is arranged before angiography, the risk of CES

could be predicted by the finding of severe athero-

sclerotic aortic debris.

Insufficient blood supply caused by mesenteric ar-

tery occlusion will result in inflammation or injury of the

intestine. Clinical presentations include sepsis, bowel

perforation, or intestinal gangrene and require more

aggressive interventions such as surgery and intensive

care. No observational studies about mesenteric artery

occlusion related to CES have been documented, only

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case reports are available.6,7 In 2008, Miklik reported on

an acute superior mesenteric artery occlusion that was

caused by CES and successfully solved by immediate

local thrombolysis with recombinant t-PA (alteplase).6 In

addition, another author reported successful local throm-

bolysis treatment and reperfusion of the superior me-

senteric artery with streptokinase four hours after injec-

tion; however, the patient died four days later due to sep-

tic shock with metabolic acidosis.7 The major selection

criteria for fibrinolysis include pain with less than 12

hours of evolution, partial mesenteric artery occlusion,

absence of peritoneal signs, severe acidosis, or organ

failure. In our case, the patient had no acute onset of

symptoms such as abdominal pain or peritoneal signs

after angiography. All the symptoms occurred 18 hours

after procedure, presenting as nausea, abdominal disten-

tion and gastrointestinal bleeding, the latter being a con-

traindication for thrombolytic therapy. In this situation,

the best treatment choice was starting surgical treatment

as soon as possible after the definite diagnosis.

In conclusion, CES should be considered in elderly

patients with peripheral arterial disease who are plan-

ning to undergo catheterized angiography. Transbrachial

or transradial approaches may be better choices to avoid

dislodgement of atheromatous material when the cathe-

ter is manipulated across areas of detected aortic choles-

terol debris within the abdominal aorta. Although the

incidence is very rare, subacute CES with mesentery ar-

tery occlusion should be kept in mind in elderly patients

with multiple risk factors who underwent transfemoral

angiography and demonstrate a non-specific clinical pre-

sentation. Early diagnosis with emergent operation is the

only way to successfully treat such patients.

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