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Background. Cavitation has been claimed partly re- measured by a hydrophone intraoperatively and postop-
sponsible for the increased risk of thromboembolic com- eratively in 14 patients with mechanical valves, 10 pa-
plications, hemolysis, and fatal valve failure seen in tients with normal aortic valves, and 5 patients with
mechanical heart valve patients. In vivo studies have bioprosthesis. The total signal energy was evaluated as
investigated cavitation using high-pass filtering of the nondeterministic and deterministic energies.
high-frequency pressure fluctuations with the root mean Results. Nondeterministic energies were verified both
square values as an assessment of intensities. In vitro intraoperatively and postoperatively in all patients who
studies have shown that this well-known method may had a mechanical valve; this finding confirms the cavita-
not be ideal owing to loss of data as a consequence of tion potential of mechanical valves. None of the data
filtering, and because it requires a priori knowledge of recorded in patients with bioprosthetic or native valves
the valve resonance pattern. Therefore, a new method has contained nondeterministic energy.
been developed, which decomposes the signal into non- Conclusions. The study confirms the presence of cavita-
deterministic (cavitation) and deterministic (valve reso- tion in mechanical heart valve patients using the nondeter-
nance) signal components, and hence decreases data loss. ministic energy of high-frequency pressure fluctuations as a
This study aimed to evaluate cavitation in patients with quantitative measure of cavitation both intraoperatively
mechanical, biological, and native heart valves both intra- and postoperatively.
operatively and postoperatively using the new method. (Ann Thorac Surg 2006;81:34 41)
Methods. High-frequency pressure fluctuations were 2006 by The Society of Thoracic Surgeons
CARDIOVASCULAR
2006;81:34 41 CAVITATION EVALUATION IN VIVO
and to ensure that some of the cavitation signal is not The intraoperative measurements were performed
filtered away. Recently, we developed a signal analysis when the patient had been hemodynamically stable for at
method [14] to distinguish between the cavitation signal least 2 minutes after being weaned from cardiopulmo-
components and the closing sound without using a HP nary bypass. The sterilized hydrophone was placed
filter. The method is based on the cavitation bubble near the aortic annulus at the low aorticleft atrial junc-
implosion creating random or nondeterministic pres- tion, and data were acquired for approximately 30 sec-
sure fluctuations [15]. By comparing the previously onds, while registering blood pressure, heart rate, cardiac
used HP-filtered root mean square values [11] to the output, blood gases (pO2 and pCO2). Ejection fractions
nondeterministic energy extraction, we found a high were registered from the preoperatively performed
correlation between the two methods. Hence, using the echocardiography.
nondeterministic energy extraction method, an alter- On the fourth postoperative day, the hydrophone was
native method has been developed where bandwidth placed in a custom-made water-filled chamber and
limitation is avoided and knowledge of the valve- placed on the precordium in the left fourth intercostal
dependant cut-off frequency is not needed. The method space close to the sternum. This location has previously
has been tested in animal studies [16], which support the been shown to be the optimal position for mechanical
use of this method as an alternative to the previously aortic heart valve sound recordings [17]. The measure-
used method. ments were performed with the patients in supine posi-
From a practical clinical point of view, it would be ideal tion. Arterial blood pressure brachial cuff and pulse were
if cavitation could be assessed by noninvasive means. recorded.
Therefore, we have also developed a new transducer As the aim was primarily to reconfirm the findings
design that enables recordings of HFPF on the precordial obtained by Paulsen and colleagues [7] and additionally
skin. to investigate whether it was possible to perform nonin-
We hypothesize that the nondeterministic energy can vasive measurements, a preoperative measurement was
be used in humans as a quantitative measure of cavita- not performed.
tion both intraoperatively and postoperatively. The study was approved by the local Ethical Commit-
The aim of this study was to evaluate cavitation inten- tee and complied with the Helsinki II declaration.
sities in mechanical heart valve patients intraoperatively
and postoperatively using the nondeterministic charac- Data Analysis
teristics of the HFPF generated during valve closure The intraoperative data were analyzed for all 29. Postop-
compared with biological and native heart valves. erative data were not obtained for all the included
patients owing to equipment failure (2 for mechanical
and 2 for native valves), and postoperative complications,
Patients and Methods namely, confusion and intensive care unit admission (2
The study comprised 29 patients (22 men and 7 women; for mechanical, 1 for bioprosthetic, and 1 for native
average age 67 years). The patients were divided into valves). Therefore, postoperative data were analyzed for
three subgroups: (1) 14 with aortic St. Jude Medical only 21 patients (10 mechanical, 4 biological, and 7 native
valves; (2) 5 with aortic Carpentier-Edwards pericardial valves). This group comprised 15 men and 6 women
bioprosthesis; and (3) 10 who underwent coronary artery (average age 66 years). Thirty seconds of continuous
bypass surgery (CABG). Preoperatively all CABG pa- recorded data were analyzed off-line using LabVIEW 6.0i
tients had normal aortic and mitral valves verified by (National Instruments). Cavitation was quantified based
echocardiography. Inclusion criteria were age greater on recorded pressure signatures and the method devel-
than 18 years, patient scheduled for elective heart valve oped by Johansen and associates [14], which entails
surgery or CABG, and patient giving consent (oral and separation of the HFPF signal into deterministic and
written). Exclusion criteria were hemodynamic unstabil- nondeterministic components. Motivated by the assump-
ity, implantation of composite grafts required, implanta- tion that the acoustic signal from cavitation is stochastic
tion of double valve prostheses, and coronary bypass (random) [15], the nondeterministic component should
surgery performed as a beating-heart procedure. primarily contain signal originating from cavitation, and
The HFPF was measured intraoperatively and postop- the deterministic component originating primarily from
eratively using a miniature hydrophone (type 8103; Brel the valve-closing sound. The method first calculates the
& Kjr, Nrum, Denmark) with an upper frequency ensemble averaged component in a time domain of 30
limit of 150 kHz. The hydrophone was connected to a consecutive closing sounds. Because each closing sound
preamplifier (type 2635; Brel & Kjr) with a built-in HP is within a very short time window, it is necessary to
filter at 20 Hz. Data were stored on a computer equipped exactly line up the data before averaging. This lining up
with a data acquisition card (AT-MIO16-E2; National is done by cross correlating every heart cycle with a
Instruments, Austin, Texas) at a sampling rate of 500 kHz. chosen template. Using the time variable in the cross
Data acquisition and off-line signal analysis were accom- correlation enables temporal line up with reference to the
plished using a custom-made program developed in chosen template. When the ensemble averaged time
LabVIEW 6.0i (National Instruments). The recorded sig- domain signal is calculated, the energy density spectrum
nals were visualized on-line using an oscilloscope (type is deduced to derive the deterministic signal energy,
PM 3305; Phillips, Einthoven, Holland). which originates from the valve-closing sound. The next
36 ANDERSEN ET AL Ann Thorac Surg
CARDIOVASCULAR
step is calculating the mean energy density spectrum or postoperatively. The intraoperative noise floor for the
from each single closing event. The energy is calculated two control groups (Fig 5) was between 0.77 Pa2 and 10.76
in the same way as for the ensemble averaged signal. Pa2, with a median value of 2.40 Pa2 for bioprosthetic
That leads to the total signal energy, which is the sum of valves; and between 0.76 Pa2 and 6.92 Pa2, with a median
the deterministic and nondeterministic energy. By sub- value of 2.80 Pa2 for native valves. The postoperative (Fig 5)
tracting the deterministic energy from the total energy, noise floor was between 0.006 Pa2 and 0.15 Pa2, with a
the nondeterministic (approximate cavitation parameter) median value of 0.06 Pa2 for bioprosthetic valves; and
energy can be deduced. between 0.004 Pa2 and 0.01 Pa2, with a median value of
0.008 Pa2 for native valves.
Results Hemodynamic parameters (cardiac output, heart rate,
pO2, pCO2, blood pressure, and ejection fraction) are
In all the mechanical heart valve measurements, both shown in Tables 1 and 2. No apparent relation was found
intraoperative and postoperative HFPF were found. The between nondeterministic energies and cardiac output,
total energy content in the intraoperatively recorded heart rate, pO2, pCO2, blood pressure, or ejection frac-
signal for one mechanical heart valve is shown in Figure 1.
tion; blood pressure and heart rate in the postoperative
It is seen that the signal contains a considerable amount
data collection setting did not show any relation either.
of energy within the hydrophones frequency range (20
Valve sizes were compared against the intraoperative
Hz to 150 kHz). The total energy consists of the nonde-
nondeterministic and deterministic values for the me-
terministic energy (Fig 2A) and the deterministic energy
chanical valves, but no clear relation was found.
(Fig 2B). The Figures show that the signal comprise
nondeterministic energy in the entire frequency range.
The deterministic energy mostly dominates frequencies Comment
below 75 kHz with a gradual decrease in upper frequency
energy and energies with generally lower amplitude Thromboembolic complications in mechanical heart
compared with the nondeterministic energy. valve patients are the most frequent cause of complica-
In Figure 3, the total energy content for the same tions for heart valve replacement. Especially young pa-
mechanical valve is shown postoperatively. Figure 4 tients with a long life expectancy may face significant
shows the nondeterministic (Fig 4A) and the determinis- additive risk over several years; therefore, cavitation as a
tic (Fig 4B) energies contained in the signal. The signal potential contributor to thromboembolism should be
contains a greater amount of nondeterministic than de- investigated. Samboe and colleagues [10] showed that
terministic energy in the high frequencies. The nonde- thromboembolic complication may be caused by release
terministic energy representative for cavitation ranges of tissue factor. Our own studies have supported these
interoperatively (Fig 5) from approximately 345 Pa2 to findings by demonstrating hypercoagulability caused by
approximately 16,090 Pa2, with a median value of 6720 cavitation [16]. As cavitation bubble implosion is known
Pa2. The postoperative nondeterministic (Fig 5) energy to release high energies, it may be assumed that the
varied between 1.33 Pa2 and 39.3 Pa2, with a median value energies will be able to destroy the blood components
of 6.22 Pa2. None of the data obtained from bioprosthetic and hence activate the coagulation cascade. Therefore,
or native valves contained HFPF either intraoperatively it seems plausible that thromboembolic complications
Ann Thorac Surg ANDERSEN ET AL 37
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2006;81:34 41 CAVITATION EVALUATION IN VIVO
in mechanical heart valve patients canat least par- deterministic energy are not a definite proof of ca-
tiallybe attributed to cavitation. vitation. However, in vitro studies [1] have since
Using the deterministic/nondeterministic decomposi- demonstrated that root mean square values of HFPF
tion method to separate the closing sound from cavita- are a good assessment of cavitation intensities assessed
tion has the advantage that it does not require valve by high-speed visualization techniques. They support
specific HP filtering, as in the previously used method our assumption that nondeterministic energies are an
[11, 13]. Furthermore, there is no bandwidth limitation expression of cavitation.
introduced as a consequence of filtering. In Figures 1 and 2, it is seen that the intraoperative
The present study verified that the signal recorded in measurements appear to pick up signal at higher
all mechanical heart valve patients contained nondeter- frequencies than the postoperative measurements
ministic energies in the entire frequency range and only (Figs 3 and 4), and the difference between the median
deterministic energies in the lower frequency ranges. values in the two setups indicate a difference in mag-
This finding is in accordance with previous studies nitude of the recorded signal. However, it was ex-
where the valve-closing sound has been found to be pected that an attenuation of the higher frequencies
present in the lower frequencies; therefore, these find- would take place in the postoperative situation, as
ings support that the deterministic energies can be tissue and bone situated between the transducer and
used as an expression of the valve-closing sound in the valve entail low-pass filtering of the signal [19 21].
vivo, and the nondeterministic energies used for cavi- Anyway, this method still seems capable of detecting
tation monitoring. The HP-filtered HFPF and the non- pressure fluctuations with an acceptable signal-to-
38 ANDERSEN ET AL Ann Thorac Surg
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2006;81:34 41 CAVITATION EVALUATION IN VIVO
Hemodynamic parameters recorded intraoperatively for biological (C-E) and native (CAGB) valves.
BP blood pressure; CABG coronary artery bypass graft surgery; C-E Carpentier-Edwards bioprothesis; CO cardiac output; EF
ejection fraction; E-nondet. nondeterministic energy; F female; HR heart rate; M male.
than in valves not exposed to exercise conditions, so it Figures 2 and 4 shows that both intraoperative and
may be assumed that there is a possibility for higher postoperative measurements contain nondeterministic
cavitation intensities in patients during exercise. That signal components as an indication of cavitation; and
might be a particular concern for younger patients with Figure 5 shows the differences between the mechanical,
high exercise levels. bioprosthetic, and native valves with respect to energy
With regard to the remaining hemodynamic parame- contained in the signal. The low values found in the two
ters, no clear relation was found. control groups express the noise floor. The type of noise
Table 1 shows that there is a 4.5 times spread between observed is primarily noncorrelated, and therefore con-
the patient with the highest nondeterministic energy and tributes to the nondeterministic energy. However, the
the one with the lowest. Since all the patients had the energy in the noise is several orders of magnitude lower
same valve type implanted, it may be assumed that this than that of the signal of interest.
difference could be attributed to the different amount of It is shown (Figs 1 and 2) that the main part of the
cavitation generated. It would have been interesting to be signal recorded at mechanical heart valves consists of
able to evaluate cavitation intensities under different left nondeterministic energy. It is also seen that the signal
ventricular pressure dp/dt conditions, but this was not contain both deterministic and nondeterministic energy
considered feasible either intraoperatively or postopera- in most of the frequency range of the hydrophone,
tively. The method most likely has its strength in moni- suggesting that the two components overlap in frequency
toring cavitation intensities in the individual patient and range. This finding further supports that parts of the
not as a comparison between patients. cavitation signal will be lost if a HP filter is used, and
We have earlier carried out in vitro studies showing parts of the closing sound will be included in the cavita-
that cavitation may generate frequency components tion signal using that method.
above 150 kHz, which is the upper frequency limit of the The nondeterministic energy can not be used as the
transducer used in this study [14]. Such high-frequency irrefutable fingerprint of cavitation, but can be assumed
components could not be detected with the hydrophone to be a good indicator of cavitation intensities compared
used in the present study. with the knowledge achieved from previous studies.
This study only comprised patients who had the St. Whether the signal contains other components is diffi-
Jude Medical aortic valves implanted; however, the used cult to say, but factors such as turbulence could be a
methodology could also have been applied to patients contributor due to its stochastic nature. Owing to the
implanted with a mechanical heart valve in the mitral time window we used and the frequency composition of
position, and a study that examines different types of turbulence ( 1,000 Hz), it is believed that turbulence is
mechanical heart valves in different positions is needed. an insignificant contributor to bias for these
Recently, an in vitro study has shown that some valve measurements.
types are more likely to produce cavitation than other It is believed that it is possible to develop this method
models [14]. of noninvasive assessment of cavitation further and
Ann Thorac Surg ANDERSEN ET AL 41
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2006;81:34 41 CAVITATION EVALUATION IN VIVO
thereby create a standardized postoperative setup that 11. Garrison LA, Lamson TC, Deutsch S, Geselowitz DB, Gau-
can be used for routine investigation of mechanical heart mond RP, Tarbell JM. An in-vitro investigation of prosthetic
heart valve cavitation in blood. J Heart Valve Dis 1994;
valve patients.
3(Suppl 1):8 22.
Methods based on detecting and evaluating cavitation 12. Zapanta CM, Stinebring DR, Sneckenberger DS, et al. In
using HFPF seem promising, but they still require further vivo observation of cavitation on prosthetic heart valves.
investigation. ASAIO J 1996;42:M550 5.
In summary, high-frequency pressure fluctuations re- 13. Johansen P, Lomholt M, Nygaard H. Spectral characteristics
of mechanical heart valve-closing sounds. J Heart Valve Dis
corded during valve closure comprised nondeterministic 2002;11:736 44.
energy both intraoperatively and postoperatively in me- 14. Johansen P, Fontaine AA, Deutsch S, Manning K, Nygaard H,
chanical heart valve patients, but not in patients with Tarbell JM. A new method for evaluation of cavitation near
bioprosthetic or native valves. This finding indicates that mechanical heart valves. J Biomech Eng 2003;125:66370.
cavitation only occurs at mechanical valves, and there- 15. Oba R, Ikohagi T, Ito Y, Miyakura H, Sato K. Stochastic
behavior (randomness) of desinent cavitation. J Fluids Eng
fore contributes to the explanation of the differences in 2002;108:438 43.
thrombogenicity among mechanical, bioprosthetic, and 16. Johansen P. Mechanical heart valve cavitation. Expert Rev
native heart valves. This study supports that the nonde- Med Devices 2004;1:89 98.
terministic method can be used as an alternative method 17. Johansen P, Andersen TS, Hasenkam JM, Nygaard H. In-
in cavitation research both intraoperatively and postop- vivo prediction of cavitation near a Medtronic Hall valve.
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of a priori knowledge of the valve characteristics [18]. Paulsen PK. Measurement of sounds generated by mechan-
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We wish to thank the Danish Heart Foundation (Grant 00-2-3- 10 12, 1994:55 60 (abstract).
45A-22853) for financial support. We also thank the surgeons 19. Durand LG, Langlois YE, Lanthier T, et al. Spectral analysis
and other personnel at the Department of Cardiothoracic and and acoustic transmission of mitral and aortic valve closure
Vascular Surgery, Skejby Sygehus, for their kind help during sounds in dogs. Part 1. Modeling the heart/thorax acoustic
our measurements. system. Med Biol Eng Comput 1990;28:269 77. [Erratum in
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20. Nygaard H, Thuesen L, Terp K, Hasenkam JM, Paulsen PK.
Assessing the severity of aortic valve stenosis by spectral
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