Stroke. 2008;39:503-511
Published online before print January 3, 2008,
doi: 10.1161/STROKEAHA.107.491241
(Stroke. 2008;39:503.)
© 2008 American Heart Association, Inc.
Occurrence and Clinical Impact of Microembolic Signals During or After Cardiosurgical Procedures
Ralf Dittrich, MD
E. Bernd Ringelstein, MD
From the Department of Neurology (R.D., E.B.R.) and the Leibniz Institute for Atherosclerosis Research (R.D., E.B.R.), University of Muenster, Muenster, Germany.
Correspondence to Ralf Dittrich, MD, Department of Neurology, University Hospital of Muenster, Albert-Schweitzer-Strasse 33, 48129 Muenster, Germany. E-mail dittrir{at}gmx.de
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Abstract
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Background and Purpose— Microembolic signals (MESs) are
detectable within the transcranial Doppler frequency spectrum
downstream from vascular atherothrombotic or cardiothrombotic
lesions. A frequent occurrence of MESs has also been shown during
bypass surgery or after mechanical valve implantation. We sought
to compile the knowledge on MES prevalence, the clinical impact
of these cardiogenic MESs, and microemboli composition.
Summary of Review— We performed a systematic MEDLINE search and summarized the currently available literature about MESs during or after cardiosurgical procedures for this state-of-the-art report.
Conclusions— The nature of cardiogenic MESs is heterogeneous, and their prevalence is highly variable, reflecting their different origin from a broad spectrum of cardiosurgical conditions. The occurrence and number of MESs during cardiac catheterization and percutaneous coronary angioplasty seem to have a clinical impact but need to be explored further. In patients with prosthetic heart valves, in those with left ventricular assist devices, and during cardiac surgery, the occurrence of MESs has an important clinical impact, and MES monitoring has proven its reliability. Although the data encourage intensifying MES detection in cardiac disorders, their heterogeneous nature does not yet allow the use of MESs as a general surrogate parameter for neuronal damage or cardial thromboembolic risk.
Key Words: cardiac embolism • cardiac surgery • cognitive impairment • tcd • transcranial Doppler • ultrasound
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Introduction
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In the late 1960s, decompression bubbles in divers were described
by means of diagnostic ultrasound,
1 as well as arterial aeroembolism
during cardiac surgery.
2 These clinically silent signals, preferably
called microembolic signals (MESs), are detectable within the
transcranial Doppler frequency spectrum (TCD). Because of the
detection of MESs in patients with artificial heart valves,
it became evident that MESs can also originate from the heart
itself.
3 Their clinical impact depends on the presence of thromboembolic
diseases within the heart or other cardiogenic embolic sources,
eg, during or after cardiosurgical procedures. Despite the widespread
use of TCD monitoring in patients with cardiac sources of embolism,
a systematic overview, in particular with respect to cardiac
surgical procedures, about this topic is missing. Thus, the
goal of the following review is to summarize the present state
of knowledge about the cardiosurgical conditions leading to
MESs, their prevalence, clinical impact, and microemboli composition.
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Methods
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We performed a systematic MEDLINE search limited to the English
language containing the search terms "microembolic signals,"
"microemboli," or "high-intensity transient signals." These
search terms were combined with the different topics of the
review: "heart valves," "prosthetic heart valves," "artificial
heart valves," "assist device," "cardiac surgery," "bypass surgery,"
"coronary angioplasty," and "cardiac catheterization." Comments,
reviews, letters, case reports, animal studies, and in vitro
studies were not considered. The inclusion criteria were systematic
TCD monitoring in homogeneous patient groups providing new findings
and scientifically relevant results in the aforementioned topics.
We screened and extracted the articles and decided by consensus
about their inclusion.
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MESs in Prosthetic Heart Valves
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In patients with mechanic heart valves (MHVs), the frequency
of MESs
4–6 depends on the type of valve installed,
7–14 whereas the prevalence of MESs is much lower with bioprostheses
13–17 (see
Table 1
). The majority of MESs, particularly in MHV carriers,
reflect gaseous microemboli due to cavitation at the rim of
the MHV
18,19 and not to the shedding of thromboembolic material.
This hypothesis is supported by the stable number of MESs found
during repeated investigations and the lack of patients’
clinical deterioration over time.
6 Also, the rate of cardioembolic
stroke in these patients does not appear to be correlated with
the number of MESs detected.
15 No correlation could be identified
between the patient’s hemostaseology and either the number
of MESs or the type and extent of antithrombotic treatment.
20 Similarly, neurologic deficits based on the number of MESs detected
in MHV carriers could not be predicted.
21,22 No difference could
be demonstrated in MESs between symptomatic and asymptomatic
MHV carriers.
22 The gaseous MESs associated with MHVs are characterized
by a higher relative intensity increase over the background
speckle as opposed to solid MESs. There is, however, considerable
overlap of the "loudness" of these various types of MESs, thereby
not allowing a clear differentiation between the 2.
23 This is
why inhalation of concentrated oxygen has been used to suppress
cavitation formation to distinguish solid thromboembolic from
gaseous material.
14,24,25 Because the solubility of oxygen in
blood is
5 times greater than that of nitrogen, the blood is
preferably saturated with oxygen instead of nitrogen. Oxygen
cavitation is short-lived, which means that many oxygen bubbles
do not reach the brain at all. Most of the oxygen cavitation
bubbles have a diameter of 3 to 5 µm, allowing them to
easily pass capillaries without doing harm to brain tissue.
In patients with MHVs, the number of MESs could significantly
be reduced by inhaling oxygen compared with a period without
oxygen inhalation.
18 Similarly, no effect on the MES rate was
seen in patients with solid microemboli derived from atherothrombotic
arterial sources during oxygen inhalation.
26
Quite contrary, a higher number of MESs per hour in MHV carriers with a medical history suggestive for stroke60 compared with asymptomatic MHV carriers11 was reported.5 In other studies, impaired working memory could be demonstrated in patients having received MHVs, presumably caused by continuous "showers" of cerebral microembolism.27,28 Also, increased levels of platelet-derived microparticles, an increased procoagulant activity, and an increased rate of MESs were found in MHV carriers symptomatic with cerebrovascular events.29 In 30 patients with bileaflet valves, a reduction of MESs by 16% to 41% after administration of acetylsalicylic acid of 81 to 531 MESs/h was demonstrated.25 Additionally, a higher number of MESs was found in patients with valve obstruction.30 Successful thrombolysis led to a marked decrease of MESs, whereas the number of MESs remained almost stable after unsuccessful thrombolysis. The fact that successful thrombolysis may lead to a higher number of gaseous MESs due to better leaflet mobility and that the authors used a nonvalidated threshold of 400 Hz to differentiate solid from gaseous MESs are limitations of that study. However, the described results indicate that microemboli in MHV carriers are at least in part composed of solid material.
In conclusion, the potential harm due to chronic MESs, particularly in patients with MHVs, seems to be low or negligible because the majority of these microemboli are gaseous and generated by microcavitation. However, owing to their mixed gaseous and solid origin, they cannot be used as an indicator of a thromboembolic threat or event.
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MESs in LVADs
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In patients with left ventricular assist devices (LVADs), thromboembolism
is 1 of the most frequent complications requiring effective
anticoagulation.
31 Depending on the device implanted, the MES
prevalence ranges from 20% to 100%.
32–40 A higher amount
of MESs corresponds to thromboembolic events in patients with
the Novacor N100 LVAD,
32,34,37 but not in patients with a DeBakey
device.
38,40 Patients with the Novacor N100 device and antithrombotic
therapy in addition to anticoagulation (eg, antiplatelet agents)
had significantly fewer MESs and thromboembolic events.
37 Again,
this phenomenon could not be demonstrated in patients with a
DeBakey device.
38 MESs in DeBakey LVAD carriers could be abolished
in part by oxygen inhalation, indicating that a substantial
number of these MESs are gaseous in origin
38,39 (see also
Table 2).
However, the use of time domain analysis to differentiate the
mixed composition of gaseous and solid emboli was unsuccessful.
39
View this table:
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Table 2. No. of Patients, Type of LVAD, MES Prevalence, MES Number, TCD Device, Recording Duration, and Association With Different Clinical Parameters in Patients With an LVAD
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A "hidden" procoagulable state is presumably the reason for the higher number of solid MESs in the patients who experience thromboembolic events. In conclusion, the MES load, MES composition, and the relation to thromboembolic events depend strongly on the device installed, the individual thromboembolic risk, and the extent of antithrombotic treatment. The heterogeneity of influencing factors does not allow us to draw a final conclusion about the predictive value of MES monitoring, but it might be possible for each individual type of LVAD.
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Monitoring of MESs During Cardiac Surgery
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The number of MESs during open-heart surgery is high, and often
showers of MESs are recorded, particularly during clamp placement
and removal in cardiopulmonary bypass grafting (CABG).
41–46 Also, residual air in the venous cannula increases the number
of MESs at the beginning of CABG.
47 These intraoperative MESs
can cause cognitive impairment. In patients having <200 MESs
during their CABG procedure, 8.6% showed postoperative neuropsychological
deficits, but this proportion rose to 43% in patients having
>1000 MESs.
48 Moreover, a higher occurrence of postoperative
neurologic complications in patients with a high number of MESs
(>60) during CABG was demonstrated.
43 In another study, a
reduction in postoperative cerebral glucose metabolism was found,
correlating with the number of MESs recorded (
r=–0.46,
P<0.05).
49 Although neuropsychological impairment occurred
after the surgical procedure, its correlation with the number
of MESs or the decrease in cerebral glucose metabolism could
not be proven. Lee et al
50 demonstrated that a higher number
of intraoperative MESs corresponded with an impairment in an
auditory verbal learning test 2 weeks and 1 year after CABG
(
P
0.05). Interestingly, a specific verbal memory decline in
patients with predominantly left-sided MESs was observed, whereas
a higher number of right-sided MESs was associated with a nonverbal
memory deficit after open-heart surgery.
51 The correlation of
a high number of MESs, particularly during on-pump cardiac surgery,
with a relative reduction of prefrontal activation during functional
magnetic resonance imaging while performing verbal memory tasks
4 weeks postoperatively could also be demonstrated.
52 There
are additional reports on cognitive impairment and delayed recovery
after CABG due to intraoperative MESs.
53–57
The nature of these MESs, either solid or gaseous, is not fully understood. An increased number of MESs during aortal manipulation, especially in the case of severe aortal atherosclerosis, indicated the predominantly solid nature of MESs.44 In another study, the higher number of MESs in patients with valve replacement or CABG was associated with postoperative neuropsychological impairment. A much higher number of MESs (mean, 2083 per case during operation) in patients with valve replacement compared with those with CABG (mean, 50 MESs per case during operation, P0.05) was found. Interestingly, both conditions led to similar severe neuropsychological impairment. The authors concluded that this observation reflected the primarily gaseous nature of the MESs during valve replacement as opposed to the predominantly solid MESs during bypass surgery.54 Similar conclusions were drawn in a larger study with a more simple detection technique despite a lower number of MES detected.58
A considerable proportion of MESs during cardiac surgery appear to be gaseous. These gas bubbles are much larger than the cavitation-induced bubbles and may do harm to the brain. With respect to various surgical steps during CABG, the occurrence of MESs was analyzed.59 During the aortic clamp placement and its removal, more solid MESs were seen (mean MES increase, 1.5±1.5/min). By contrast, during perfusion interventions (eg, blood sampling, drug administration), more gaseous MESs could be registered (mean MES increase, 6.9±4.5/min). The number of MESs was significantly higher during perfusion interventions. Similarly, a higher number of MESs and more severe neuropsychological deficits were found when 
10 perfusion interventions became necessary during the entire course of the operation compared with patients with fewer interventions.60 Reduced purging and the use of continuous infusions instead of bolus injections significantly decreased the number of MESs during the surgical procedure.61 Also, when a large-bore syringe was used, the rate of MESs was significantly lower compared with that seen with a small-bore syringe.62 Moreover, it could be demonstrated that CO2 insufflation in the cardiothoracic wound during open-heart valve surgery reduced the number of gaseous MESs.63
Finally, a dramatic and significant reduction of MESs was achieved with off-pump CABG.50,64–70 Another study group71 not only confirmed the higher number of MESs during on-pump (mean, 335.1) compared with off-pump (mean, 144.7) surgery but also found a significantly lower 6-month postoperative "cognitive impairment-index" in the off-pump patient group, as assessed by counting the number of impaired test performances for each patient in 7 tests. A limitation of these results is the fact that a significant cognitive decline was not related to the number of MESs during operation. Others observed the same phenomenon, but the amount of MESs was not correlated with the S100 protein level, a marker of diffuse cerebral injury.69 In contrast, a significantly higher level of S100 protein in patients undergoing on-pump surgery and a higher intraoperative number of MESs in patients with retinal microvascular damage were reported.70
Further refinement of surgical techniques, like avoidance of aortic side clamping and the use of clampless devices, also reduces the number of solid MESs.46 In that study, automatic software had been used to discriminate between solid and gaseous MES, which could be a potential source of error. The additional use of a sutureless proximal aortic device led to a decrease of MESs during the surgical procedure.72 Arterial filters, in particular leukocyte-depleting filters, fat-removal filters, or an air bubble trap in the arterial line, could also considerably reduce the number of MESs.73–79 Because the number of MESs is higher in cases of longer-duration CABG procedures, shorter operation times may prevent harm due to MESs.80 In left heart valve replacement, the application of a new "dual-vent" de-airing technique could significantly reduce the number of carotid MESs.81 Furthermore, cannulation of the distal aortic arch led to a decrease of MESs compared with conventional cannulation of the ascending aorta.82,83 The use of a straight or curved aortic cannula, or cannulas of different diameters, had no influence on the number of MESs.84 However, optimized positioning in the aorta descendens was not associated with better performance in postoperative cognitive tests.85 The number of MESs again depends on the type of oxygenator device used, even when modern versions are used. The mean number of MES during the whole procedure was 309 for the DIDECO oxygenator but only 143 for the COBE oxygenator (P<0.00001).86
Not all protective efforts lead to a significant decline in MESs during cardiac surgery. A surface-modifying additive during conventional cardiopulmonary bypass surgery did not reduce the number of MESs.87 In addition, there was no difference in MES number when a minimally invasive versus a conventional mitral valve operation was performed.88 Finally, an symmetry connector system, to avoid partial clamping, was followed by an increased number of MESs, presumably due to gaseous microemboli.89
Another point of interest is the hemispheric distribution of MESs during cardiac surgery, but the results are ambiguous so far. Whereas some study groups described a preponderance of left-sided MESs,50,90 others either reported an equal distribution of MESs91 or found a preference for the right hemisphere.49,51 In conclusion, MESs are a common phenomenon during cardiac surgery. The composition of the microemboli is heterogeneous and reflects solid and gaseous particles. So far, it remains controversial which composition of MES represents the majority during cardiosurgical procedures. However, it is indisputable that a large number of MESs during cardiosurgical procedures leads at least to temporary if not permanent neuropsychological deficits due to neuronal damage. The type and degree of the resulting deficit depends on the hemisphere to which the higher number of MESs are channelled. Thus, MES monitoring by TCD is a reliable, easily accessible, noninvasive tool to guide and improve surgical techniques.
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Monitoring of MESs During Cardiac Catheterization and Percutaneous Coronary Angioplasty
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Asymptomatic MESs were detected in >50% of patients during
left atrial catheterization.
92,93 The same phenomenon was discovered
during percutaneous transluminal coronary angioplasty.
94 The
majority (70%) of the 679 MESs occurred after injection of solutions;
hence, the authors concluded that these MES were predominately
gaseous. Other authors confirmed this finding and detected MESs
primarily during contrast agent injection.
95 Further evidence
for the primarily gaseous origin was the reduction in the number
of MESs by using solutions with a low gas content.
96 In all
of the aforementioned studies, clinically apparent neurologic
deficits did not occur after the procedure. The use of a guidewire
and different catheter types also influenced the number of MESs.
97 In a recent more sophisticated study, the authors verified the
primarily gaseous origin of MESs in 47 patients during left
heart catheterization by automated software (92.1% gaseous vs
7.9% solid MESs).
98 Interestingly, 3 (6.4%) patients had transient
neurologic deficits immediately after the procedure, and 7 (16.7%)
patients had cognitive impairment as assessed by neuropsychological
tests 24 hours after the procedure. Five (15.2%) patients had
new cerebral lesions detected by diffusion-weighted magnetic
resonance imaging 24 hours after catheterization. This finding
coincided with a higher number of solid MESs (
P=0.016). These
results suggest that the procedural occurrence of MESs during
catheterization is potentially harmful; it can damage the brain
parenchyma and cause at least transient neurologic symptoms.
However, in another study, only 1 of 46 patients developed a
new diffusion-weighted imaging lesion after the procedure.
99 In conclusion, the clinical impact of MESs during left heart
catheterization appears to be clinically relevant but needs
to be investigated further with standardized study protocols.
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Limitations of MES Monitoring
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Unfortunately, MES monitoring by TCD has general major limitations.
Studies conducted so far have used different monitoring times,
ultrasound devices, and monitoring protocols, thus hampering
the comparability of results. In addition, the overlapping physical
properties of the microemboli do not yet allow us to unequivocally
differentiate gaseous from solid MESs, despite promising technical
progress, like multifrequency TCD,
100 a longer sample volume
length for gaseous microemboli,
101 and Doppler time domain analysis.
39 Finally, there is a lack of large, prospective and long-term,
follow-up studies in all fields of cardiosurgical procedures.
These limitations are the major drawbacks for the validity of
MESs as a surrogate parameter that could replace clinical outcome
events.
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Summary
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The prevalence and number of cardiogenic MESs during all types
of cardiac interventions is high but depends strongly on the
underlying cardiosurgical condition. The clinical impact is
as heterogeneous as the number of settings in which MESs occur.
MESs in patients with MHVs are mainly cavitation-based, gaseous
in nature, and usually harmless to the brain. Quite contrary,
the differing load of solid particles in various cardioembolic
disorders allows us to define a hierarchy of embolic risk related
to the various diseases and procedures. Showers of solid or
large gaseous MESs during cardiac surgery, cardiac catheterization,
or percutaneous coronary angioplasty are harmful but are partly
preventable by both better technical equipment and improved
and meticulous surgical technique. MESs can provide clues to
successfully modify surgical interventions, and they may serve
as a guide to the choice of timing and technical guidelines
of a given intervention. However, MESs during or after cardiosurgical
procedures are not yet an accepted surrogate parameter for the
prediction of thromboembolic risk or neuronal damage with cognitive
decline.
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Acknowledgments
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Disclosures
None.
Received May 13, 2007;
accepted June 7, 2007.
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Abstract
Introduction