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Diffusion- and Perfusion-Weighted Brain Magnetic Resonance Imaging in Patients With Neurologic Complications After Cardiac Surgery
Robert J. Wityk, MD;
Maura A. Goldsborough, RN;
Argye Hillis, MD;
Norman Beauchamp, MD;
Peter B. Barker, DPhil;
Louis M. Borowicz, Jr, MS;
Guy M. McKhann, MD
Arch Neurol. 2001;58:571-576.
ABSTRACT
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Background Neurologic complications after cardiac surgery include stroke, encephalopathy,
and persistent cognitive impairments. More precise neuroimaging of patients
with these complications may lead to a better understanding of the etiology
and treatment of these disorders.
Objective To study the pattern of ischemic changes on diffusion- and perfusion-weighted
magnetic resonance imaging (DWI, and MRPI, respectively) in patients with
neurologic complications after cardiac surgery.
Methods All records were reviewed of our patients undergoing cardiac surgery
in the previous year who also underwent postoperative DWI or MRPI. Neurologic
symptoms, vascular studies, and the pattern of ischemic changes were recorded.
Acute ischemic lesions were classified as having a territorial, watershed,
or lacunar pattern of infarction. Patients with multiple territorial infarcts
in differing vascular distributions that were not explained by occlusive vascular
lesions were classified as having multiple emboli.
Results Fourteen patients underwent DWI and 4 underwent MRPI. Acute infarcts
were found in 10 of 14 patients by DWI as compared with 5 of 12 patients by
computed tomography. Eight patients presented with encephalopathy (associated
with focal neurologic deficits in 4), 4 with focal deficits alone, and 2 with
either fluctuating symptoms or transient ischemic attacks. Among patients
with encephalopathy, 7 of 8 had patterns of infarction suggestive of multiple
emboli, including 3 of 4 patients with no focal neurologic deficits. Several
patients had combined watershed and multiple embolic patterns of ischemia.
Findings of MRPI studies were abnormal in 2 of 4 patients, showing diffusion-perfusion
mismatch; both patients had either fluctuating deficits or transient ischemic
attacks, and their conditions improved with blood pressure manipulation.
Conclusions In patients with neurologic symptoms after cardiac surgery, DWI is more
sensitive to ischemic change than computed tomographic scanning and can demonstrate
patterns of infarction that may help us understand etiology. The most common
pattern was multiple embolic infarcts. Preliminary experience with MRPI suggests
that some patients have persistent diffusion-perfusion mismatch after surgery
and may benefit from therapeutic intervention.
INTRODUCTION
PREVENTION and treatment of neurologic complications remain a challenge
in the management of patients undergoing cardiac surgery. Stroke occurs in
approximately 2% to 3% of patients after coronary artery bypass grafting,
with higher rates after valve replacement or other cardiac surgical procedures.1, 2 Patients with stroke have poorer functional
outcomes and incur greater medical costs with longer hospital stays.1, 3 Many potential mechanisms have been
proposed for stroke after cardiac surgery, including perioperative embolism
from the heart or aortic arch, systemic hypoperfusion, ischemia from large-vessel
occlusive disease, or a combination of these factors.4, 5, 6, 7
Previous studies have identified risk factors for stroke after cardiac surgery,8, 9 but few studies have used advanced
imaging techniques to investigate patients with stroke in detail.10, 11
In addition to stroke, other neurologic complications in the postoperative
period include delirium, seizures, and persistent cognitive impairment. Approximately
10% of patients experience postoperative encephalopathy, and up to 37% of
patients display persistent cognitive decline on neuropsychological testing
results a month after surgery.12, 13, 14, 15, 16
There has been much speculation about the etiology of encephalopathy and cognitive
impairment associated with cardiac surgery. Possible factors include cerebral
microembolism (eg, from aortic arch atheroma or arising from extracorporeal
circulation devices), cerebral edema, cerebral hypoperfusion or hypoxia, and
toxic effects of anesthetic agents.16, 17
The results of intraoperative transcranial Doppler studies demonstrate microemboli
at the time of aortic clamp release, and the presence of emboli correlates
with short-term cognitive impairment.18, 19
Patients with severe aortic arch atheroma also have higher rates of stroke
after cardiac surgery.20, 21 The
relative importance of cerebral edema and hypoperfusion has been more difficult
to assess.22, 23
Newer imaging methods using magnetic resonance imaging (MRI) may clarify
the significance of small emboli in patients undergoing cardiac surgery with
cardiopulmonary bypass. Diffusion-weighted imaging (DWI) capitalizes on acute
changes in water molecule diffusion that occurs in ischemic tissue, and is
highly sensitive in detecting acute infarcts within the first 10 to 14 days.24, 25, 26 Because of the temporal
change in the apparent diffusion coefficient, DWI can distinguish recent infarcts
from areas of chronic ischemia. Magnetic resonance perfusion imaging (MRPI)
uses a bolus injection of gadolinium–diethylenetriamine pentaacetic
acid (DTPA) to identify areas of relatively decreased cerebral perfusion that
may be at risk for infarction.26, 27
We report our preliminary experience with diffusion and perfusion MRI in patients
with neurologic complications after cardiac surgery. In our series, DWI revealed
a more extensive pattern of emboli than previously identified, both in patients
with clinically apparent stroke as well as patients with only postoperative
encephalopathy. The findings in 2 of our patients with MRPI were instructive
in that they prompted changes in postoperative management.
PATIENTS AND METHODS
We reviewed the medical records and imaging studies of all patients
who had DWI performed after cardiac surgery between March 1999 and January
2000. Patients were identified by review of a prospectively maintained cardiac
surgery database and a registry of MRI studies. More than 1000 cardiac surgery
procedures are performed at our institution a year, and during the study period,
30 patients underwent brain imaging studies (either computed tomography [CT]
or MRI), although not all patients received a final diagnosis of stroke. At
our institution, DWI has been available since 1997 for selected patients with
stroke but became part of the routine sequence for brain MRI in mid 1999.
Additionally, MRPI has been available for clinical use since 1999. Medical
records were reviewed with attention to stroke risk factors, intraoperative
parameters, neurologic deficits, and the clinical impression by the consulting
neurologist prior to imaging studies. (All patients in this series were seen
in consultation by a neurologist.)
Computed tomographic studies were reviewed by a neuroradiologist who
was given the clinical history but not the MRI findings. Only CT scans performed
prior to MRI studies were analyzed. The MRI studies were then reviewed with
the prior CT scan available. The pattern of stroke was categorized as follows:
(1) territorial infarction in the distribution of a cerebral artery; (2) watershed
infarction in the border zone between vascular territories (either superficial
or deep territories)28, 29; and
(3) lacunar infarction, defined as a small (<1-cm) infarction in the distribution
of a penetrating artery. Embolic infarcts were suspected in patients with
territorial infarcts in the absence of large-vessel occlusive disease, particularly
if multiple or bilateral territorial infarcts were found.
Nonenhanced CT images were acquired in the axial plane using 5-mm collimation.
Conventional MRI sequences used in this evaluation included sagittal T1 (time
to repeat [TR], 800 milliseconds; echo time [TE], minimum; field of view [FOV],
24 cm; number of excitations [NEX], 1; matrix, 256 x 192; slice thickness,
5 mm; gap, 0 mm), axial fast-spin echo T2-weighted (TR, 4000 milliseconds;
effective TE, 85 milliseconds; FOV, 24 cm; NEX, 2; matrix, 256 x 192;
slice thickness, 5 mm; gap, 0 mm), and axial fluid attenuated inversion recovery
imaging (TR, 8800 milliseconds; TE, 133 milliseconds; inversion time, 2200
milliseconds; FOV, 24 cm; NEX,1; matrix, 256 x 192; slice thickness,
5 mm; gap, 0 mm). Diffusion imaging was performed using a single-shot, multislice,
spin-echo, diffusion-weighted echo planar imaging of the whole brain (TR,
10 000 milliseconds; FOV, 24 cm; NEX, 1; matrix, 128 x 128; slice
thickness, 5 mm; gap, 0 mm). Four gradient strengths were applied resulting
in a b-value of 0 and 1000 mm2/s applied sequentially in the X,
Y, and Z gradient directions. Isotropic DWIs and images of the average diffusion
coefficient (Dav = Dxx + Dyy + Dzz)
were reconstructed. Whole brain MRPI was performed using a multislice gradient-echo
scan with the sequence repeated every 2.0 seconds for 60 seconds during the
bolus injection of 20 mL of gadolinium-DTPA (Magnevist; Schering-Plough AG,
Kenilworth, NJ) injected at a rate of 5 mL/s (TR, 2000 milliseconds; TE, 60
milliseconds; flip angle, 90°; FOV, 24 cm; matrix, 128 x 64; slice
thickness, 5 mm; gap, 2.5 mm; axial slices, 17). Injection was via a 20-gauge
antecubital intravenous catheter using an MRI-compatible power injector (Spectris;
Medrad Inc, Indianola, Pa) with the contrast injection followed by a 20-mL
saline flush at a rate of 5 mL per second.per AU. Images of time-to-peak of
bolus were calculated on a computer (Sun ULTRA Sparc Workstation; Sun Microsystems
Inc, Palo Alto, Calif)using in-house software and viewed using Scion Image
software (Scion Corporation, Frederick, Md, 1998).
RESULTS
We identified 14 patients who underwent DWI studies after cardiac surgery
between March 1999 and January 2000 (Table
1). There were 9 men and 5 women with an average age of 69 years.
Twelve patients underwent coronary artery bypass grafting (1 with simultaneous
carotid endarterectomy), 1 had a mitral valve replacement, and 1 patient with
Marfan disease underwent repair of a dissecting aneurysm of the ascending
aorta. During the study period, there were approximately 1300 cardiac surgical
procedures of various types performed, of which 30 were associated with neurologic
complications. Of the 14 patients who underwent DWI studies, 13 (93%) had
coronary artery disease; 9 (64%), hypertension; 6 (43%), hyperlipidemia; 5
(36%), diabetes; and 4 (29%) were current smokers. The most common neurologic
symptom after surgery that prompted neurologic consultation was encephalopathy
in 8 patients, 4 of whom also had focal neurologic findings on examination.
Two patients presented with visual field deficits, 3 with hemiparesis, and
1 with a transient ischemic attack (TIA) of aphasia. At the time of hospital
discharge, the final neurologic diagnosis was stroke in 11 patients and seizure,
unexplained encephalopathy, and TIA in 3 others, respectively.
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Characteristics of 14 Patients Who Underwent DWI Studies After Cardiac
Surgery*
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Twelve patients underwent CT scans. The first scan was taken on postoperative
day 3 on average, with a range from day 0 to 6. Acute infarcts were seen in
5 of 12 scans and were classified as single territorial infarcts in 2 scans
and multiple territory infarcts in 3. In contrast, the first DWI study was
performed on postoperative day 6, on average (range, day 3-15), and revealed
acute infarcts in 10 patients (10 of 11 patients with final clinical diagnosis
of stroke). In 4 of 5 patients with acute infarcts demonstrated by CT, DWI
revealed additional infarcts in other vascular territories. For example, patient
7 had a single territorial infarct on CT, but MRI revealed several other lesions
in both hemispheres (Figure 1).
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Figure 1. Diffusion-weighted magnetic resonance
images (DWIs) of a patient with postoperative encephalopathy and mild aphasia
(patient 7) show a large left posterior temporal-parietal infarct (B) that
was evident on computed tomographic (CT) scans. In addition, however, DWI
also reveals small acute infarcts in the posterior occipitotemporal regions
bilaterally (A) as well as in the frontal cortex bilaterally (C) that were
not apparent on CT scan.
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The pattern of stroke by DWI suggested multiple emboli in 7 patients.
Many of the infarcts identified by DWI were small and typically located in
the cortex of the hemispheres or in the cerebellum (Figure 2). Infarcts generally seemed equally distributed between
right and left hemispheres and involved both anterior and posterior circulations.
A few acute lesions were in the territories of penetrating arteries and were
small enough to be considered lacunar infarcts. Five patients had a watershed
pattern of infarction; 3 of these patients had coexistent multiple territorial
infarcts, while 2 had only watershed infarcts. Only 1 patient (No. 5) in our
series had significant postoperative hypotension requiring vasopressor agents;
DWI showed bilateral deep watershed infarcts as well as a number of small,
scattered lesions also suggestive of emboli in other territories. In several
of these patients with combined watershed and embolic patterns, the small
cortical infarcts seemed to cluster and coalesce in the watershed territory
(Figure 2).
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Figure 2. Diffusion-weighted magnetic resonance
images of a patient with postoperative encephalopathy without focal abnormalities
on initial neurologic examination (patient 2) reveal multiple infarcts in
both hemispheres. Most lesions are small and involve regions of the cortex,
but with preferential involvement of the watershed territory, particularly
near the vertex (C).
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Among the 8 patients presenting with postoperative encephalopathy, 7
had multiple infarcts apparent on DWI consistent with emboli, including 3
of 4 patients who had no focal neurologic deficits on examination. One patient
had normal findings on both DWI and MRPI studies performed on postoperative
day 7. The following day, he dramatically improved, and his delirium was thought
to have been metabolic in origin. Three other patients had normal DWI findings:
1 had clinical findings consistent with a lacunar stroke (pure motor hemiparesis);
1 later developed seizures; and 1 had TIAs without a persistent neurologic
deficit.
Four patients underwent MRPI studies; the findings in 2 of these were
instructive. One patient (patient 14) had several spells of "confusion" and
nonsensical speech several days after coronary artery bypass grafting. An
MRPI revealed extensive hypoperfusion of the left hemisphere that corresponded
with his known chronic left internal carotid artery occlusion. Both the number
and doses of antihypertensive medications were reduced. After the patient's
blood pressure rose from 110/60 mm Hg to an average of 140/80 mm Hg, his TIAs
ceased. Another patient (patient 13) had a deep watershed infarct apparent
on DWI, but had a larger perfusion abnormality in the middle and anterior
cerebral artery territories (Figure 3)
This patient had hemiparesis with marked fluctuations in the degree of weakness
over 24 hours. Average blood pressure was 130/60 mm Hg at that time. Antihypertensive
medications were reduced, resulting in an elevation of average blood pressure
to 160/70 mm Hg and an improvement in arm strength that remained through discharge.
The 2 remaining patients had normal results on MRPI studies.
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Figure 3. Fluid-attenuated inversion recovery
images (A and B) of a patient with fluctuating left hemiparesis after cardiac
surgery (patient 13) show bilateral white matter changes that seem chronic.
Diffusion-weighted magnetic resonance images (DWIs), however (C and D), reveal
subtle areas of acute infarction in the deep watershed territory only on the
right side. Magnetic resonance perfusion images (E and F) show areas of relative
hypoperfusion (white and lighter gray regions) involving the deep white matter
and anterior cerebral artery territory that is more extensive than the lesion
on DWI. The patient's fluctuations ceased and the hemiparesis improved over
several days after reduction of antihypertensive medications.
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COMMENT
To our knowledge, ours is the only series in the literature to report
the results of diffusion- and perfusion-weighted MRIs in patients after cardiac
surgery. Several pertinent findings emerged: (1) DWI was clearly more sensitive
than CT in detecting ischemic lesions; and (2) DWI also made small cortical
or periventricular infarcts more conspicuous than did conventional MRI sequences.30 In addition, however, DWI improved the specificity
of detecting acute ischemic lesions. Many patients with coronary artery disease
have coexistent cerebrovascular disease, with either old infarcts or chronic
periventricular ischemic matter changes evident on baseline imaging studies.23 These abnormalities make it difficult to distinguish
small, acute infarcts in postoperative patients from chronic lesions. Deep
watershed infarcts, for example, are often located in the white matter of
the centrum semiovale,29 a region in which
many patients have chronic ischemic changes. On the other hand, DWI allows
one to distinguish an acute lesion from chronic ischemia (Figure 3), with confirmation by measurement of the apparent diffusion
coefficient. In humans, the apparent diffusion coefficient typically remains
depressed for about 10 to 14 days, and thereafter normalizes, allowing one
to identify lesions that have occurred within the previous 2 weeks.26
The most common finding on DWI in our series was the presence of multiple
small infarcts, typically spread throughout the cortical regions of the anterior
and posterior circulations and suggestive of a shower of emboli of varying
sizes. Most of our patients with a single infarct evident on CT or conventional
MRI were found on DWI to have additional lesions. Several patients had a pattern
of multiple embolic infarcts that clustered and merged with watershed infarcts.
However, an association of watershed infarction with multiple emboli is not
surprising because small embolic particles are likely to migrate into distal
vascular territories.31 As postulated by Caplan
and Hennerici,32 the combination of small embolic
particles and hypotension (eg, during cardiopulmonary bypass) can lead to
delayed washout of emboli and produce watershed territory infarction. Most
of the patients with a pattern of multiple embolic infarcts presented with
encephalopathy, either alone or associated with focal neurologic findings.
Further study of patients with this pattern of infarction should include assessment
of long-term recovery and cognitive function. It would also be interesting
to determine if these patterns correlate with embolic counts from transcranial
Doppler studies or the presence of extensive aortic arch atheroma. Because
of the retrospective nature of our study, we cannot assess the frequency of
unexpected small infarcts in patients with encephalopathy after cardiac surgery;
only selected patients underwent DWI studies during the the study period.
Finally, we used MRPI in 4 of our patients and found significant perfusion
abnormalities with diffusion-perfusion mismatch in 2. In patients presenting
with acute ischemic stroke, diffusion-perfusion mismatch is thought to identify
a region of brain potentially at risk for infarction, but potentially salvageable
by reperfusion.33, 34, 35
Reperfusion may be accomplished by thrombolysis, mechanical opening of a stenotic
vessel (eg, carotid endarterectomy or angioplasty), or increasing cerebral
perfusion by blood pressure elevation. The protocol for blood pressure management
after cardiac surgery at our institution has been to maintain relatively low
blood pressures to prevent bleeding complications in the mediastinum and at
suture lines. Reduced blood pressure, however, may be detrimental to cerebral
perfusion in the setting of acute stroke owing to loss of cerebral autoregulation
or the presence of high cerebral resistance in patients with chronic hypertension.36
Two of our patients had fluctuating symptoms (recurrent TIAs in one,
fluctuating weakness in the other), which corresponded to a region of relative
hypoperfusion on MRPI. In both cases, increasing blood pressure by careful
reduction of antihypertensive medications was associated with amelioration
of symptoms. In studies of patients with acute ischemic stroke, diffusion-perfusion
mismatch tends to diminish over time as infarction progresses. An MRPI may
therefore be of greater importance if performed much earlier after cardiac
surgery than in our series.
In conclusion, our preliminary findings show the value of DWI and MRPI
in patients with neurologic complications after cardiac surgery. These new
imaging techniques better define the degree and distribution of ischemic injury
and may reveal regions of persistent hypoperfusion. This information is important
in the study of mechanisms of neurologic injury in patients unergoing cardiac
surgery, and is also relevant for the clinician searching for an explanation
of neurologic dysfunction in the postoperative patient.
AUTHOR INFORMATION
Acepted for publication July 11, 2000.
This work was supported in part by the Charles A. Dana Foundation, New
York, NY (Dr McKhann), and grant 1 RO1 NS 35610 from the National Institutes
of Health, Bethesda, Md (Ms Goldsborough, Mr Borowicz, and Dr McKhann).
From the Departments of Neurology (Drs Wityk, Hillis, and McKhann),
Surgery (Ms Goldsborough), and Radiology (Drs Beauchamp and Barker), Johns
Hopkins Hospital, and the Zanvyl Krieger Mind/Brain Institute, Johns Hopkins
University (Mr Borowicz and Dr McKhann), Baltimore, Md.
Reprints: Robert J. Wityk, MD, Department of Neurology, Johns Hopkins
Hospital, Meyer 5-181, 600 N Wolfe St, Baltimore, MD 21287 (e-mail: rwityk{at}jhmi.edu).
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Cerebral Infarction: Incidence and Risk Factors after Diagnostic and Interventional Cardiac Catheterization--Prospective Evaluation at Diffusion-weighted MR Imaging
Busing et al.
Radiology 2005;235:177-183.
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Postoperative Stupor and Coma
Gootjes et al.
Mayo Clin Proc. 2005;80:350-354.
ABSTRACT
Cerebral lipiodol embolism during transcatheter arterial chemoembolization
Yoo et al.
Neurology 2004;63:181-183.
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Evaluation of brain injury after coronary artery bypass grafting. A prospective study using neuropsychological assessment and diffusion-weighted magnetic resonance imaging
Knipp et al.
Eur. J. Cardiothorac. Surg. 2004;25:791-800.
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Diffusion-Weighted Magnetic Resonance Imaging in Internal Carotid Artery Dissection
Koch et al.
Arch Neurol 2004;61:510-512.
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Diffusion-Weighted Magnetic Resonance Imaging and Neurobiochemical Markers After Aortic Valve Replacement: Implications for Future Neuroprotective Trials?
Stolz et al.
Stroke 2004;35:888-892.
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Comparison of cerebral embolization during off-pump and on-pump coronary artery bypass surgery
Lund et al.
Ann. Thorac. Surg. 2003;76:765-770.
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Impact of single clamp versus double clamp technique on neurologic outcome
Grega et al.
Ann. Thorac. Surg. 2003;75:1387-1391.
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Embolic Stroke Syndrome Underlies Encephalopathy and Coma Following Cardiac Surgery
Boyajian and Otis
Arch Neurol 2003;60:291-291.
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Diffusion- and Perfusion-Weighted Magnetic Resonance Imaging of the Brain Before and After Coronary Artery Bypass Grafting Surgery
Restrepo et al.
Stroke 2002;33:2909-2915.
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Lesion Patterns and Mechanism of Ischemia in Internal Carotid Artery Disease: A Diffusion-Weighted Imaging Study
Kang et al.
Arch Neurol 2002;59:1577-1582.
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Encephalopathy and Stroke After Coronary Artery Bypass Grafting: Incidence, Consequences, and Prediction
McKhann et al.
Arch Neurol 2002;59:1422-1428.
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Cardiac Surgery and Magnetic Resonance Imaging of the Brain
Wityk and Restrepo
Arch Neurol 2002;59:1074-1076.
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Brain Damage After Coronary Artery Bypass Grafting
Bendszus et al.
Arch Neurol 2002;59:1090-1095.
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Acute Ischemic Stroke Patterns in Infective and Nonbacterial Thrombotic Endocarditis: A Diffusion-Weighted Magnetic Resonance Imaging Study
Singhal et al.
Stroke 2002;33:1267-1273.
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DWI vs. CT for Neurologic Evaluation After Cardiac Surgery
JWatch Neurology 2002;2002:3-3.
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Stroke after cardiac surgery: short- and long-term outcomes
Salazar et al.
Ann. Thorac. Surg. 2001;72:1195-1201.
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Protecting the Brains of Patients After Heart Surgery
Caplan
Arch Neurol 2001;58:549-550.
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