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Ex Vivo Monitoring of Rat Heart Wall Motion

Using Piezoelectric Cantilevers

Rui Zhang1, Ya Chen2, Wen H. Ko1, David S. Rosenbaum3,4, Xin Yu2,3, Philip X.-L. Feng1

1Electrical Engineering, 2Biomedical Engineering, Case School of Engineering3Physiology and Biophysics, Case School of Medicine, 4MetroHealth System

Case Western Reserve University, Cleveland, OH 44106, USACorresponding Authors; Email philip.feng@case.edu, xin.yu@case.edu

Abstract We report on an experimental exploration ofex vivo

measurements and real-time monitoring of the motions of heart

wall for perfused rat hearts, by employing a surface-contact type

of electromechanical probes based on piezoelectric transduction.

In a hybrid experimental apparatus consisting of a conventional

heart perfusion system and external electromechanical probing

devices and circuitry, prototyped piezoelectric cantilever devices

are calibrated and tested. We demonstrate that the externalpiezoelectric cantilevers are capable of monitoring the dynamic

behavior of the isolated heart ex vivo, by measuring the motions

of the heart wall. For typical rat hearts with heart rates in the

range of ~150250bpm (beats per minute), cantilevers with

dimensions of t wL | 130m (0.38)mm (119)mm yield

electrical signal of ~50400mV. Measured data can also helpidentify signatures of various regimes (e.g., from healthy to

fatigued, to expiring) in the dynamical evolution during the

perfused hearts lifetime. Preliminary tests on parallel multi-

channel monitoring with probes positioned at multiple locations

on heart surface prove to be valid and useful in obtaining

information of regional displacement of heart wall.

I. INTRODUCTIONHeart is the foundation of advanced lives including human

being. Heart health and function monitoring are critical,

especially for patients who suffer from heart diseases. Heart

diseases are the top one cause of death in the United States

and several other countries (e.g., a total death of ~600,000 per

year in 20072009 in US means one death due to heart disease

every ~50 seconds) [1], and are the top reason for disease-

based deaths throughout the world. This drives researchers to

push the limits in advancing heart healthcare technology. We

perceive at least the following major challenges (i) early

detection of alarms of heart diseases for apparently healthypeople it is desirable to develop devices that are wearable or

implanted (with very low pain), especially for old people,athletes, and those who may have family history of heart

diseases; (ii) post-surgery chronic heart monitoring for

patients who are already receiving surgery and other treatment

what is desired includes low-pain implantable solutions that

are small, light, enduring, and compatible with telemetry.

To date it has been well recognized that regional strain and

stress on heart wall are related to development of disease [2],

and studying the electromechanical properties and monitoring

heart wall motion can help for heart diseases diagnosis [3].

From an engineering perspective, the heart is an amazing

electromechanical device with exquisitely elegant functions

and structures (Figure 1) enabled by soft materials and tissues

this causes some of the fundamental issues that are

challenging the devices and instruments to be interfaced with

heart for diagnosis and treatment. The prevalen

electrocardiography (ECG) today is easy to use but only

retrieves crude signals of overall heart function. Magnetic

resonance imaging (MRI) is a powerful tool for studying heartstructural and motional details and disease mechanisms

However todays MRI systems are bulky, highly complicated

and expensive, and often suffer from limitations in speed and

resolution. We have been exploring a new, low-cost approach

of directly probing heart wall motion by using distributed

surface-mount, and miniaturized (e.g., micro and nanoscale)

electromechanical devices for regional strain/stress and

motion sensing. Here we report our initial effort toward thi

goal, and describe our first experimental results.

Figure 1. A glance of the heart structures and functions from an engineer

viewpoint. (a) Illustration of the anatomy of the heart, showing the heachambers, vessels and valves. (b) Illustraton of the pacemakerand distaconduction system.

II. HEART WALL MOTIONThe heart is an electromechanical organ with great

structural and functional complexities. Its wall motion is

depending upon the compromised coronary arterial supply

Myocardial wall motion defects are essential and sensitive

markers for coronary artery disease and myocardial ischemia

The capability of directly probing regional or highly localized

heart wall motion may also have critical impact on arrhythmia

(a) (b)

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restoring synchronization between asynchronous chambers or

regions, early alarm of regional muscle fatigue or failure, etc.

Figure 2. Simplified illustration of the complexity of the heart wall musclestructure and organization the basket-weavingarthitecture of cardiac musclecells and the myrocardial fibers. (a) A perspective view of the weaving fibersin layers at various depth in the heart wall. (b) A simplified model showingthe weaving structure and orientation.

There are several types of muscle cells that participate in

and coordinate the complex motions in concert. The most

important of these include (i) the cardiac muscle cells

making the weaving myocardial fibers (see Figure 2a), (ii) the

vascular smooth muscle cells (abundant in the coronary

arterial tree), (iii) the conduction system muscle cells (e.g., in

the pacemaker region shown in Figure 1b). For this weaved

basket, advanced MRI techniques including tagging,

harmonic phase, and diffusion tensor MRI (DTMRI) have

been developed for regional wall motion and strain assessment

[4-7]. This work describes our initial effort and preliminary

results toward a convenient electromechanical monitoring and

diagnosis system using piezoelectric (PZE) devices, which,

with computer aid, can automatically detect and monitor local

heart wall motion ex vivo.

Figure 3. Piezoelectric (PZE) cantilever devices for electromechanical signal

transduction. (a) Illustration of a prototypical composite cantilever with anactive PZT layer sanwiched between two thin electrodes (metallic coatinglayers). (b) Simplified illustration of cantilever bending upon application ofexternal force at the cantilever tip.

III. PIEZOELECTRIC CANTILEVERSENSORSA.Piezoelectric Cantilevers

We explore piezoelectric (PZE) device technology because

of the direct electromechanical coupling effect in PZE

transducers. A PZE device as simple as a singly-clamped

cantilever beam (Figure 3) can be conveniently maneuvered to

probe static deflections and dynamic motions of other

mechanical systems. We have been exploring two scenarios

for a PZE cantilever device to interface with a beating heart

(i) making contact between the free end of the cantilever and

regions of interest on the heart wall, while keeping the other

end of cantilever clamped on a solid (not moving) substrate

(ii) mounting the base (clamped end) of the cantilever on the

beating hearts surface and having the cantilever body free to

move and vibrate. The former is suited forex vivo studies; the

latter is attractive for packaged implanted systems.

Figure 3 illustrates a generic cantilever device based upon a

~65Pm-thick PZE lead-zirconate-titanate (PZT) thin filmsandwiched between two metal electrodes, a bottom ~65Pm

thick brass layer, and a top ~15Pm silver coating. We exploi

the d31 coupling in such structures transverse (out-of-plane)

motion of the cantilever tip (free end) induces in-plane strain in

the PZT layer and causes surface charge and electrical potentia

between the two electrodes which is read out for monitoring of

motion. Within the scope of this work cantilever tip in

contact with heart wall with quasi-DC movements (beating

frequency much lower than the fundamental resonance of the

cantilever), the displacement, force, and the voltage signal are

in convenient linear relationship, i.e., VPZEvd31Gvd31F/keffin a simple lumped parameter model [8].

TABLE I. PIEZOELECTRIC MATERIALS OF INTEREST

MaterialPiezoelectric Coefficients

[pm/V or pC/N]

Youngs

Modulus

[GPa]

Density

[g/cm3]

PZTd33~100600, d31~50300

d15~100800~40150 ~7.57.8

ZnO d33~10, d31~4, d15~3 ~30140 ~5.6

AlN d33~5.6, d31~2.6, d15~2.5 ~330410 ~3.26

PVDF d33~2030, d31~20, d15~1040 ~215 ~1.76

Figure 4. The first generation of our prototyped piezoelectric (PZE) devicebased upon flexural-mode cantilevers using PZE thin film materials (e.g., PZTand PVDF). (a) A vibration energy converter in plastic package withcomplementary dual PZT layers, easily generating ~10V level voltage signalsfrom human body movements. (b) A PZT-based device with on-board energyconversion and harvesting circuit. (c) A much thinner PZT-based device. (dA PZE cantilever based on flexible PVDF material. Scale bars 1cm. (eMeasured time-domain voltage waveform (peak voltage ~2V) due to ringdown oscillations of a ~30Hz resonanst mode. (f) Voltage (peak voltage~32V) measured from ~110Hz oscillations. Legend initial tip deflection.

B. Materials of ChoiceWe choose PZT as the active material for its large PZE

coefficient and easy availability for this study. Table I displays

a short list of materials that we find interesting for employmen

in our studies. We have also been exploring devices made o

polyvinylidene fluoride (PVDF) because of its attractive and

promising properties for implants on flexible substrates. Othe

(a) (b)

Base

Apex

Clamping

PZT Cantilever

L

w tTop Electrode

x

y

zBottom Electrode

E Fieldd31 Coupling

F

G0

x

y

(a)

(b)

Clamping Port Silver Coating PZT Layer Brass Electrode

(a) (b) (c) (d)

0.0 0.1 0.2

0

10

20

30

MeasuredSignal(V)

Time (s)

5.08 mm3.81 mm

0.1 0.2 0.3

0

1

2

MeasuredSignal(V)

Time (s)

5.08mm3.81mm3.18mm

(e) (f)

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materials of potential interest include zinc oxide (ZnO) and

aluminum nitride (AlN), particularly for recent developments

in engineering them into micro and nanoscale functional

devices that could be integrated and packaged in implanted

microsystems.

C.Prototyped DevicesWe first demonstrate several prototyped PZE cantilevers

using PZT and PVDF. The prototyped devices (see examples

in Figure 4) are first calibrated in DC/static operation, and are

then extensively tested in pulse and resonant modes. Early

generations of cantilevers are on the few-mm- to 1cm-scale in

size, with fundamental flexural resonance frequencies in the

~0.1kHz to ~1100kHz ranges, and easily generates voltage

signals up to ~10V. Our preliminary data and estimation show

that these devices and their performance can be suited for both

quasi-DC and resonant-mode applications, operating a

atmospheric pressure, either in customized macroscopic plastic

packages, or in micro polymeric thin film packages.

Figure 5. The heart perfusion system for ex vivo experimental studies with the isolated live rat heart. (a) Picture of a prototypical perfused rat heart with surfacemount external bulky electrodes for physiological measurements (e.g., see http//vflab.org). (b) Highly simplified schematic of our experimental approach using boththe external piezoelectric (PZE) devices on heart wall, and the conventional approach for heart function recording system in a canonical rat heart perfusion system. (cIllustration of the scheme of using a balloon ( i.e., simiar to balloon valvuloplasty) and its associated external perssure sensor for heart function recording. (I) and (IIare two specific options for implanting the balloon; we use option (II) in all the tests presented in this work.

IV. EXPERIMENTAL TECHNIQUESIn this early-stage effort of our exploration, as illustrated in

Figure 5, we combine the piezoelectric (PZE) cantilever

monitoring technique with well-established (commerciallyavailable) heart function recording systems. This helps to

reliably evaluate the new approach and calibrate the

measurements and the devices, both qualitatively and

quantitatively, against todays standard protocols.

A.Heart Perfusion System and Heart Function RecordingThe conventional real-time heart function recording is

realized in a heart perfusion system, as illustrated and shown

in Figure 5 and Figure 6. The system is based on the classical

Langendorff technique for isolated heart perfusion [9]. This

allows for convenient and prompt ex vivo studies, and manybrute-force (e.g., Figure 5a) experiments, on isolated hearts.

In the particular case of this study, the perfusion systemgreatly facilitates the continuous tests with the piezoelectric

cantilever probes in a considerably long time (depending on

the heart lifetime in the perfusion system, ~1-3 hours

typically). It provides not only the live heart, but also a

parallel monitoring option as a control experiment.

Male Sprague-Dawley rats of 1012 weeks old are

heparinized (1000 units/kg, i.p.) and anesthetized by sodium

pentobarbital (85 mg/kg. i.p.). The heart is excised, cannulated,

and perfused with Krebs-Henseleit (KH) buffer containing (in

mM) 118.5 NaCl, 4.7 KCl, 1.2 MgSO4, 1.2 KH2PO4, 1.5 CaCl2,

11.1 glucose, and 25 NaHCO3. Isolated hearts are perfused at a

constant pressure in the Langendorff-type perfusion system

The perfusate was maintained at 37C and equilibrated with 95

O2-5% CO2.

Figure 6. Pictures of the rat heart perfusion system employed in this work(a) The overall Langendorff perfusion system with rat heart, pump, circulationlines, the implanted balloon sensor and its data acquisition system (vendorADInstruments). (b) Close-in view of the rat heart in the perfusion buffer.

Embedded in the heart perfusion system, as shown in

Figure 5c, we insert a water-filled latex balloon into the lef

ventricle (i.e., similar to balloon valvuloplasty). The balloon isconnected to an external pressure transducer to record the lef

ventricular developed pressure (LVDP) and heart rate (HR)

The hearts rate-pressure-product (RPP), i.e., the product o

LVDP and HR, is then calculated as an index of the workload.

Heart

Function

Recording

Pressure

Perfusion

System

Heart Wall

Motion

Recording

(b)(a)

Left

Ventricle

Left

Atrium

Right

Atrium

Right

Ventricle

(II)

(I)

Tricuspid

Valve

Mitral

Valve

(c)

(a) (b)

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The measured rat heart rate can typically be in the range of

~150250 bpm (beats per minute) at the beginning of the

experiment (with a fresh and healthily perfused rat heart). The

heart rate decreases gradually as the time elapses. The

temperature of the perfusion buffer is a critical factor for

keeping the heart alive. When temperature deviates, the heart

function could degrade, and the amplitude of heart wall

movement may decrease dramatically. Figure 6 demonstrates

pictures and details of the rat heart perfusion system we have

been implementing in this study.

B.Piezoelectric Cantilever Monitoring SystemWe have built a convenient desktop apparatus for

interfacing the piezoelectric cantilever probes with the rat heart

in the operating perfusion system. Cantilever probes can be

positioned and adjusted by moving the arms (to which the

cantilevers are clamped) on the stage with control in all three

directions. Figure 7 demonstrates a picture of an early

generation of the implementation.

Figure 7. Picture of first-generation exprimental implementation of ex vivomonitoring of rat heart wall motion, by using surface-contacting piezoelectric

(PZE) cantilever probes. For each cantilever, its one end is clamped, and theother end (tip) is in contact with the heart wall muscle. In paralle, theperfused rat hearts basic function is also being monitored using the balloonvalvuloplasty technique. In this particular picture, the free ends of a pair ofcantilevers are gently contacting the left and right ventricle of the heart.

TABLE II. PARAMETERS OF SELECTED TESTED DEVICES

Cantilever Device

ID

Length

[mm]Width

[mm]Resonance

[Hz]

(I)-A 18.0 7.0 222.0

(I)-B 19.0 7.3 214.0

(II)-A1 1.5 0.3

(II)-A2 1.3 0.4

(II)-A3 1.4 0.3

(II)-B1 1.6 0.4

(II)-B2 1.5 0.3 (II)-B3 1.4 0.4

As we expect these cantilever devices to operate while

interfacing with perfused hearts in physiological solutions, we

need to package the devices so that their electromechanical

performance would not be compromised by any corrosion or

contaminants. Prior to testing, every device is coated by a thin

layer of parylene C (thickness on the order of ~5Pm).

We note that in Figure 7 the liquid solution for nurturing

the heart is temporarily moved away. In the present generation

of setup, both the heart and all the cantilevers and device arrays

(all micropackaged with ~5Pm parylene C thin layer) are

immersed in the fluid. Basic parameters of two generations o

devices tested in this work are summarized in Table II.

V. EXPERIMENTAL RESULTS AND DISCUSSIONSExtensive experimental observations and measurements

have been performed. First, the heart function is recorded

using the balloon implanted in the left ventricle, which

provides a reference and calibration for the performance of the

perfused rat heart. Then the piezoelectric cantilevers areapplied to make contact to the heart wall for direct

electromechanical probing.

A.Heart Function Recorded by Balloon in Left VentricleWithout engaging any piezoelectric devices, real-time heat

function is recorded by the left ventricular balloon and its

associated pressure sensor. Typical data traces of LVDP and

left ventricular pressure changing rate dp/dt are recorded for

~12 hours or even longer, throughout the whole lifetime o

the perfused heart. Figure 8 shows the measured data in a very

short 12s time interval. Table III summarizes the results from a

few repeated measurement runs by only using the implanted

balloon for monitoring and recording.

Figure 8. Representative data of the perfused rat heart under healthycondition, measured in real time by only the balloon implanted in leftventricle (no any external cantilever probes touching the heart wall). (a) Lefventricular developed pressure (LVDP, in mmHg) as a fundtion of time. (bMeasured pressure changing rate dp/dtas a function of time.

TABLE III. MEASURED HEART PARAMETERS WITHOUT CANTILEVERS

Test Run

ID

Heart Rate (HR)

[beats per minute, bpm]LVDP

[mmHg]RPP

[mmHgbpm]

1 153 r 3 135 r 2 20655 r 710

2 150 r 3 120 r 2 18000 r 666

3 184 r 5 102 r 2 18765 r 890

B. Measurements with Piezoelectric (PZE) CantileversPrior to using the cantilevers for perfused heart wall motion

probing, we first perform a dry-run test by using air-filled

balloons to mimic simplified heart motions. Because the

fundamental flexural-mode resonance frequencies of the PZT

cantilevers in this work are usually in the range of ~200Hz to

~100kHz range, the rat heart motions are well in the close-to

DC or quasi-DC range. Because in all our tests, the cantilever

are in contact with the air balloon (i.e., heart model) or

perfused heart at the cantilevers tips, the tip motions closely

follow the contractions and heart beat cycles. The heart motion

does not drive the cantilever into its flexural-mode resonance.

0

50

100

150

200

LVDP

(mmHg)

0 2 4 6 8 10 12

-1000

-500

0

500

1000

dp/dt(mmHg/s)

Time (Sec)

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Such quasi-DC operations of the cantilever probes lead to a

simple linear relation between the piezoelectric voltage output

and the detected displacement of heart wall motion. The dry-

run test (using air balloon to simulate a beating heart)

indicates that for the early generations of devices (relatively

large), e.g., both (I)-A and (I)-B (listed in Table II), have high

conversion responsivity (i.e., gain), ~3V/mm (voltage per unit

cantilever deflection at its tip). In both the dry-run with heart

models and the perfused heart tests, the output voltage signals

are directly recorded and monitored by the oscilloscope using

Labview/DAQ software.

Figure 9. Voltage signal measured from a pair of PZT cantilevers touchingthe heart wall. (a) The free ends (tips) of the two cantilevers touching theheart wall of the left and right ventricle, respectively. (b) The free ends of thecantilevers are touching the base and apex of the heart wall, respectively.

Figure 9 demonstrates the voltage signals representing the

local heart wall motions, probed by a pair of PZT cantilevers.

In all these cases, the free ends of the cantilevers just barely

touch the heart wall. When the cantilevers tips make contact

to the left and right ventricles (Figure 9a) respectively, the

extracted heart rate is HR~229bpm. Measured voltage signal

is Vpp~150mV, and ~350mV, for device (I)-A and (I)-B

respectively. The asymmetry in the data amplitude from this

pair of devices is due mainly to the fact that one cantilever

device has been pre-bent (with a transverse crack developed

but not yet broken, at ~1/3 length near the clamped end), and

thus has much less strain developed given the same

displacement at the tip. When the devices tips are placed

against the base and the apex at a later time, the data show a

lower HR~43bpm, and lower Vpp~50mV and 150mV,

respectively, mostly due to the heart degradation during thetime of transition.

The effects of probing the heart wall motion by making

contacts with different depths and strengths are also explored.

A second generation (group (II) listed in Table II), smaller

cantilevers, in small parallel fingers-alike arrays, are used.

With control of the positioning arms, the devices are first

carefully placed to just barely touch the heart wall, and then

gradually move toward the heart center to start gently pressing

the heart wall. Figure 10 displays the measured data from a

pair of small cantilevers, (II)-B1 and (II)-B2, in contact with

the heart wall under three different depth/strength conditions.

Figure 10. Voltage signal measured from a pair of smaller cantilever devices

with varying the depth of the cantilever tip touching the heart wall. (a) Datfrom device (II)-B1. (b) Data from device (II)-B2. The data shown artruncated from much longer traces. For each device, data for three contacconditions are taken at three time intervals in series. Throughout these time

intervals, the implanted balloon recording ensures that the heart functions arenormal and stable. The offsets on the time axes are not adjusted among thdifferent traces.

In case of just touching but not pressing the heart wall

larger devices (group (I) in Table II) yield larger Vpp, which is

evident from Figure 9 and Figure 10. As cantilever tips get to

press against the heart wall gradually, the signals first increase

as expected, and then there is no more appreciable signa

increase observed with further pressing of the devices against

the heart surface. Such information can help us better

understand the strength of the heart wall motion, especially

with more advanced future generations of devices. We also

note that the data traces from larger devices (gently touching

heart wall, Figure 9) appear to be proportional to the dp/ddata in Figure 8, while the voltage signals from the smaller

devices (under all contact conditions, see Figure 10) seem to

have the shape similar to that of the LVDP curve in Figure 8

We are currently making more effort to investigate this

intriguing phenomenon.

As we aggressively miniaturize these devices by using

micromachining techniques, their apparent signal levels

decline. Nonetheless, with significant volume reduction they

become better suited with flexible substrates [10,11] and

packages that are more amenable to harsh environments for

implants in living bodies. We envision that it is also possible

for us to take advantage of the resonant operations of the PZE

devices, combined with air-cavity packages possible inflexible substrate, cantilever- and membrane-structured

micro/nano resonators in various frequency ranges can be

exploited for local heart wall motion monitoring. Further, the

same types of PZE devices in micropackages can also be

employed for energy conversion from heart beats [12], which

could be exploited for self powering low-power implants

Moreover, for miniaturized devices and chip-scale implants

the signal transmission could be not only wired but also

wireless. As all these technical components are getting ready

the approach of using miniaturized PZE devices explored in

this work can lead to both external heart function monitoring

systems in research and clinic labs (e.g., supplementing the

3 4 5 6 7 8 9-0.2

-0.1

0.0

0.1

0.2

VoltageSignal(Volt)

Time (Sec)

Device (I)-BDevice (I)-A

2 3 4 5 6-0.2

0.0

0.2

0.4

VoltageSignal(Volt)

Time (Sec)

Device (I)-BDevice (I)-A

(a)

(b)

0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4

-0.2

0.0

0.2 Just Touching Heart WallTouching & Gently Pushing WallPushing Harder on Heart Wall

VoltageSignal(Volt)

Time (Sec)

0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4

-0.2

0.0

0.2 Just Touching Heart WallTouching & Gently Pushing WallPushing Harder on Heart Wall

VoltageSignal(Volt)

Time (Sec)

(a)

(b)

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conventional implanted balloon recording), and implanted

systems for surgery and patients chronic heart monitoring

and in all these applications, capable of offering high

sensitivity and high spatial and temporal resolutions for

parallel readout of heart wall motion at various locations.

VI. CONCLUDING REMARKSIn summary, we have shown that using external surface-

contact or surface-attached piezoelectric (PZE) cantilevers can

probe the rat heart wall motion and the heart function ex vivo.The cantilevers in the present work are made of PZT thin films

with strong PZE effect. The d31 coupling effect in the

cantilever is exploited to transduce the flexural mechanical

motion of the cantilever into electrical signal for readout. The

cantilevers have been limited to quasi-DC operation (heart

beating rate much lower than cantilevers resonance frequency)

with their tips closely following the movements of the regional

heart wall. Devices with sizes in the mm-scale and sub-mm-

scale are tested. The preliminary tests verify the feasibility of

monitoring heart wall movements with good resolutions in the

time domain, and at different locations on heart surface. The

heart wall displacement extracted from the measurement is

typically ~0.10.3mm, which is consistent with MRImeasurement. The output power level of typical PZE

cantilevers we have tested is in the range of ~110:

Combined with advances in PZE materials at micro and

nanoscale, implantable and flexible materials, and

micropackaging techniques, this approach is expected to have

the potential of being implanted, as well as offering very high

spatial and temporal resolutions by employing further

miniaturized devices.

ACKNOWLEDGMENT

We thank the Louis Strokes Cleveland Medical Center of

the Department of Veterans Affairs and the Case School of

Engineering for financial support. We are indebted to C. A.Zorman, M. A. Rogonjic, and K. N. Kortepeter for their

administrative support. We are grateful to the IEEE UFFC

IFCS/EFTF 2011 for the Student Travel Support Award (for

R.Z.). We thank R. C. Roberts and S. B. Lachhman for help on

materials and instruments.

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