Ann Thorac Surg 2003;75:1221-1226
© 2003 The Society of Thoracic Surgeons
Original article: cardiovascular
Atheroembolism in cardiac surgery
John R. Doty, MDa,
Robb E. Wilentz, MDb,
Jorge D. Salazar, MDa,
Ralph H. Hruban, MDb,
Duke E. Cameron, MDa*
a Division of Cardiac Surgery, The Johns Hopkins University School of Medicine, Baltimore, Maryland, USA
b Division of Pathology, The Johns Hopkins University School of Medicine, Baltimore, Maryland, USA
Accepted for publication October 24, 2002.
* Address reprint requests to Dr Cameron, Division of Cardiac Surgery, Blalock 618, The Johns Hopkins Hospital, 600 N. Wolfe Street, Baltimore, MD 21287, USA.
e-mail: dcameron{at}csurg.jhmi.jhu.edu
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Abstract
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BACKGROUND: Atheroembolism is a recognized complication of cardiac surgery, but its incidence and various outcomes have not been completely described. A retrospective study was undertaken to better characterize the syndrome.
METHODS: Records of 49,377 autopsies and surgical specimens from the Johns Hopkins Hospital between 1973 and 1995 were reviewed. Three hundred twenty-seven patients (0.7%) had an identifiable atheroembolism on histologic examination. Of these patients, 29 (0.2%) had undergone a cardiac surgical procedure within 30 days of autopsy or surgical resection. Patient charts and pathology specimens were reviewed for operative findings, postoperative outcomes, and histology.
RESULTS: Six of the 29 patients (21%) had atheroembolism to the heart, 7 patients (24%) had embolism to the central nervous system, 19 patients (66%) had embolism to the gastrointestinal tract, 14 patients (48%) had embolism to one or both kidneys, and 5 patients (17%) had embolism to a lower extremity. Sixteen patients (55%) had atheroembolism in two or more areas. In 6 patients (21%), death was directly attributable to atheroembolism, including intraoperative cardiac failure from coronary embolism (n = 3), massive stroke (n = 2), and extensive gastrointestinal embolization (n = 1).
CONCLUSIONS: Atheroembolism in cardiac surgery has a broad spectrum of clinical presentations, including devastating injuries and death. Although the true incidence is probably underestimated in this retrospective study, the high attendant mortality and morbidity of atheroembolism have been documented. Improvements in outcome are likely to be associated with preoperative identification of patients at high risk, modifications of perfusion technique, and interventions to minimize secondary thrombosis and progressive organ ischemia.
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Introduction
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Atheroembolism was first described in 1862 by Panum from the autopsy of the Danish sculptor Thorvaldson [1]. Histologic examination of the heart revealed atheromatous debris in a coronary artery distal to a ruptured plaque. Atheroembolism can produce a wide range of symptoms and clinical signs that may resemble more common syndromes, presenting a difficult diagnostic challenge for the clinician [2].
The effect of atheroembolism after major vascular surgery was first recognized by Thurlbeck and Castleman in 1957 [3]. In their series, atheroembolism was present at autopsy in more than 75% of the patients, and was either the cause of death or significantly contributed to mortality in nearly half. Other authors have noted similar outcomes of atheroembolism after cardiac catheterization, angioplasty, aortic surgery, and intraaortic balloon pump (IABP) placement [4, 5].
Operations on the heart and ascending aorta are known to produce atheroembolism, most commonly at the time at aortic cannulation and placement of the cross-clamp. Blauth and associates [6] and Piriou and colleagues [7] have previously reported correlations between atherosclerosis of the ascending aorta and atheroembolic events. However, the incidence and clinical spectrum of atheroembolism associated with cardiac surgery have not been completely described; this study was undertaken to further characterize the clinical syndrome of cholesterol embolization during cardiac surgery.
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Patients and methods
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The Johns Hopkins Hospital Pathology autopsy database was searched to retrospectively identify all patients with the diagnosis of atheroembolism. Of 49,377 autopsies performed at The Johns Hopkins Hospital between 1973 and 1995, 327 (0.7%) had atheroembolism evident on histologic examination. During the same time, 18,402 patients underwent cardiac surgery at the institution. By comparing the pathology and cardiac surgery databases, a total of 29 (0.2%) cardiac surgical patients were identified as having atheroembolism within 30 days of operation. Twenty-five patients had atheroembolism demonstrated on autopsy. Four additional patients had documented atheroembolism on biopsy specimens, 3 from bowel resections and 1 from a lower extremity amputation.
Data were collected for each patient, including demographics and preoperative status, age, sex, and presence or absence of several risk factors (Table 1).
Intraoperative data were also collected for each patient, including concomitant procedures, previous cardiac operation, site of aortic cannulation (ascending aorta versus femoral artery), and presence of palpable plaque in the ascending aorta (Table 2).
Total aortic cross-clamp time and cardiopulmonary bypass time were recorded. Placement of an IABP at any time during the hospital course was noted.
Postoperative data collected for each patient included the clinical findings and the time at which a presumptive diagnosis of atheroembolism was made. Results of diagnostic studies were obtained and included brain computed tomography (CT) scan, brain magnetic resonance imaging, abdominal CT scan, endoscopy, and arteriography. Baseline blood urea nitrogen (BUN) and creatinine levels were noted and compared with the peak postoperative value.
Autopsy and surgical biopsy data were reviewed to identify organ systems involved with atheroembolism. The severity of the embolism was graded according to number of organ systems involved. Histologic findings were correlated with clinical findings in each individual patient.
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Results
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Five distinct organ systems were involved with atheroembolism after cardiac surgery: heart, central nervous system, gastrointestinal tract, kidneys, and lower extremities. Six patients (21%) had atheroembolism to the heart, 7 patients (24%) had embolism to the central nervous system, 19 patients (66%) had embolism to the gastrointestinal tract, 14 patients (48%) had embolism to one or both kidneys, and 5 patients (17%) had embolism to a lower extremity. Sixteen patients (55%) had two or more areas involved with atheroembolism. The median number of organ systems involved was 2 (range 1–4).
In 6 patients (21%), death was directly attributable to atheroembolism. Of these patients, 2 died in the operating room, 3 died within 3 days of operation, and 1 died 5 weeks after operation. Three of these patients had atheroembolism to the heart: 2 who died in the operating room and 1 who died 2 days after operation. The remaining 3 patients died from either massive cerebral atheroembolism or extensive involvement of the gastrointestinal tract.
Central nervous system
Atheroembolism to the central nervous system exhibited a pattern of widespread involvement of both hemispheres and typically resulted in a clinical picture of obtundation or massive stroke, or both. Figure 1
is a brain CT from a patient who died 2 days after operation. Immediately after the operation, the patient was obtunded and subsequently developed a fixed right pupil on the first postoperative day. Brain CT demonstrated massive infarctions in the right cerebrum, left posterior cerebral artery territory, and cerebellum with associated herniation. Histologic examination at autopsy (Figure 2)
revealed multiple infarctions with large cholesterol emboli in the middle cerebral and left posterior cerebral arteries. Cholesterol emboli were also found in the cerebellum and midbrain, along with cerebral infarction, necrosis, and cyst formation.
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Fig 1. Brain computed tomography scans demonstrating massive right hemispheric infarction with herniation (A) and cerebellar infarction (B).
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Fig 2. (A) Large cholesterol embolus in right middle cerebral artery. (B) Cholesterol embolus in small cerebral artery with associated cerebral infarction, necrosis, and cyst formation.
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Heart
Atheroembolism to the heart typically resulted in acute hemodynamic collapse in the operating room and an inability to wean the patient from cardiopulmonary bypass. Less commonly, isolated atheroembolism to a single coronary artery resulted in acute perioperative myocardial infarction. Figure 3
contains histologic sections from a patient who suffered hemodynamic collapse after removal of the aortic cross-clamp and died in the operating room. Histologic examination revealed cholesterol emboli in all coronary arteries. Focal contraction band necrosis and a zone of demarcation were noted in the posterior and inferior walls of the left ventricle. The cells surrounding small arteries with cholesterol emboli had loss of nuclei and cytoplasmic pallor consistent with ischemic damage. Dye injection of the coronary arteries demonstrated occlusion by cholesterol emboli.
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Fig 3. (A) Atheroembolism in intramyocardial artery with focal contraction band necrosis. The evident loss of nuclei and cytoplasmic pallor is consistent with ischemic damage. (B) Atheroembolism to epicardial coronary artery. Dye injection demonstrates occlusion from the embolism.
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Twelve patients (41%) had placement of an IABP during the hospital course. Eight of these patients (67%) had IABP placement prior to operation for angina, 3 (25%) had IABP placement intraoperatively for hemodynamic support, and 1 (8%) had IABP placement postoperatively.
Gastrointestinal tract
Atheroembolism to the gastrointestinal tract resulted in a variety of outcomes, including intestinal ischemia, gastrointestinal bleeding, perforation, and pancreatitis. Widespread involvement was common, usually with embolization to the superior and inferior mesenteric arteries. Figures 4 and 5
contain histologic sections from a patient
who had a protracted course after combined coronary artery bypass grafting and valve replacement, complicated by right below-knee amputation, renal failure, and multiple episodes of sepsis. Six weeks after operation, bloody stools and hemodynamic collapse developed and the patient died. At autopsy, multiple cholesterol emboli were found throughout the systemic circulation, most marked in the kidneys, small and large bowel, spleen, and pancreas. The patient had obvious severe necrotizing hemorrhagic pancreatitis in association with cholesterol emboli. Specimens from the jejunum and colon also demonstrated submucosal cholesterol emboli with overlying mucosal hemorrhage and necrosis. Renal sections showed multiple infarctions with hemorrhage and cholesterol emboli.
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Fig 4. (A) Atheroembolism to the kidney. Multiple infarctions with hemorrhage and associated emboli are visible. (B) Atheroembolism to the pancreas. This patient has severe necrotizing pancreatitis with associated emboli.
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Fig 5. (A) Atheroembolism to the spleen. Hemorrhagic infarction with associated cholesterol emboli is visible. (B) Atheroembolism to the colon, showing submucosal embolization with overlying mucosal hemorrhage and necrosis.
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Kidneys
Mean rise in serum BUN and creatinine for all patients was 3.4 times baseline and 2.6 times baseline, respectively. Mean rise in serum BUN and creatinine for patients with documented atheroembolism to one or both kidneys was 4.3 times baseline and 2.8 times baseline, respectively. Mean rise in serum BUN and creatinine for patients without documented atheroembolism to one or both kidneys was 3.4 times baseline and 2.0 times baseline, respectively. This difference was not statistically significant.
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Comment
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This study attempted to characterize the clinical syndromes associated with atheroembolism during cardiac surgery. Review of pathologic specimens demonstrated the classic pattern of tissue injury and necrosis and the various presentations of atheroembolism that occur after operations on the heart and ascending aorta. The true incidence of atheroembolism after cardiac surgery was almost certainly underestimated in this study, which is limited by the small number of patients identified in an autopsy review. Other authors have noted a similar low incidence of atheroembolism after catheterization or spontaneously, and have noted that the syndrome is highly variable and underrecognized [6–10].
When atheroembolism occurs after cardiac surgery, symptoms are often attributed to other causes, as the syndrome cannot be diagnosed accurately without tissue biopsy. In addition, many patients undergo cardiac catheterization or coronary angioplasty within a few days or weeks after the cardiac surgical procedure; determining with certainty which procedure resulted in embolization is difficult if the atheroembolism occurs later in the postoperative period [11, 12].
Atheroembolism should be suspected when the patient sustains a devastating injury, such as acute cardiac failure in the operating room or massive neurologic damage during the immediate postoperative period. The surgeon should also consider atheroembolism in the setting of acute abdominal pain, rectal bleeding, and lower extremity ischemia just after cardiac surgery. Progressive renal failure and labile blood pressure should also alert the surgeon to involvement of the kidneys.
Few diagnostic tests can accurately diagnose atheroembolism. Brain CT and magnetic resonance imaging can reveal signs of acute infarction and suggest the diagnosis if multiple areas are involved but cannot distinguish between atheroembolism and other types of embolic events. Endoscopy is useful in patients with gastrointestinal symptoms, as biopsies can be obtained to confirm the diagnosis [13]. Biopsy specimens from skin manifestations such as live do reticularis, the "purple-toe" syndrome, and the "blue-toe" syndrome must be from deep tissue in order to obtain vessels of the appropriate diameter to demonstrate the cholesterol embolus [14]. Similarly, renal biopsy will demonstrate the classic lesions, and should be considered early because the course of renal failure in these patients is often fatal [15]. One useful and noninvasive test that is easy to perform at the bedside is ophthalmoscopy, as recently reported by Gittinger and Kershaw [16]. Multiple bilateral retinal cholesterol emboli may establish the diagnosis in association with manifestations in another organ system. Invasive testing such as renal biopsy or gastrointestinal biopsy also have a role, as these procedures may help establish a firm diagnosis of atheroembolism in cases of inexorable clinical deterioration without obvious cause.
Treatment options for atheroembolism after cardiac surgery are limited and often ineffective. The only useful therapy for patients with atheroembolism to the central nervous system, heart, and kidneys is supportive, with the hope that the injury is survivable. Patients with gastrointestinal involvement such as bleeding ulcers or colonic perforation should undergo prompt laparotomy for repair or resection as indicated [17, 18]. Extremity involvement should be treated with amputation if necessary. Scattered case reports have described improvement after treatment with lipid-lowering agents or pentoxifylline [19, 20]. Anticoagulants such as heparin and warfarin, however, may precipitate and exacerbate atheroembolism, presumably by preventing formation of a thrombus over a ruptured atheromatous plaque [21]. This fact has important implications in cardiac surgery, as many patients may require anticoagulation for valvular prostheses, assist devices, or myocardial ischemia.
Preoperative detection of atheromatous lesions in the thoracic aorta may help diminish or prevent atheroembolism, as these injuries have been associated with a high incidence of neurologic complications after cardiac surgery [22, 23]. Blauth and associates [6] reported on 46 patient autopsies in which severe atherosclerosis of the ascending aorta was accompanied by evidence of atheroemboli elsewhere. In that study, significant risk factors for atheroembolism included peripheral vascular disease, hypertension, older age, and coronary artery disease. Kolh and associates [24] documented a marked increase in intensive care unit stay, overall hospital stay, and total hospital cost in patients sustaining atheroembolism after cardiac surgery. Intraoperative transesophageal echocardiography and epiaortic ultrasound can identify protruding atheromata with mobile components [25]. Alteration of the cannulation site and avoidance of aortic manipulation for coronary artery bypass based on such findings may reduce the incidence of atheroembolism [26]. Dual-helical CT may also image the distal ascending aorta and proximal aortic arch, which are not as easily seen with transesophageal echocardiography [27]. Computed tomography is less invasive and can be used in the preoperative setting to evaluate the entire aorta.
In conclusion, atheroembolism during cardiac surgery presents with a wide range of clinical syndromes, often with a devastating or fatal outcome. The surgeon should suspect atheroembolism in the setting of profound neurologic injury, cardiovascular collapse, or synchronous involvement of more than one organ system. The diagnosis is confirmed by tissue biopsy or eye examination and is suggested by multiple lesions on brain imaging. Treatment is largely supportive, avoiding anticoagulation and employing laparotomy and amputation when indicated.
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Abstract
Introduction
