strain cardíaco na avaliação da função cardíaca fetal

C© 2008, the AuthorsJournal compilation C© 2008, Wiley Periodicals, Inc.DOI: 10.1111/j.1540-8175.2008.00761.x

Global Longitudinal Cardiac Strain and StrainRate for Assessment of Fetal Cardiac Function:Novel Experience with Velocity Vector ImagingPiers C.A. Barker, M.D.,∗ Helene Houle, B.A.,† Jennifer S. Li, M.D.,∗ Stephen Miller, M.D.,∗

James Rene Herlong, M.D.,∗ and Michael G.W. Camitta, M.D.∗

∗Duke Children’s Heart Program, Duke University Medical Center, Durham, North Carolina;and †Siemens Medical Solutions, Mountain View, California

Background: Cardiac strain and strain rate are new methods to quantitate fetal cardiac function.Doppler-based techniques are regional measurements limited by angle of insonation. Newer feature-tracking algorithms permit angle independent measurements from two-dimensional datasets. Thisreport describes the novel measurement of global strain, strain rate, and velocity using Velocity VectorImaging (VVI) in a group of fetuses with and without heart disease. Methods: Global and segmentallongitudinal measurements were performed on the right and left ventricles in 33 normal fetuses and 15fetuses with heart disease. Segmental measurements were compared to global measurements. Clinicaloutcome data were recorded for fetuses with heart disease. Results: Forty-eight fetuses were evaluatedwith VVI. Cardiac strain and strain rate in normal fetuses were similar to normal adult values, butlower than pediatric values (LV strain = −17.7%, strain rate −2.4/sec; RV strain = −18.0%, strainrate −1.9/sec). No difference was present between segmental and global measurements of cardiacstrain and strain rate, although basal and apical velocities were significantly different from globalvelocities for both right and left ventricles. In fetuses with heart disease, lower global cardiac strainappeared to correlate with clinical status, although there was no correlation with visual estimatesof cardiac function or outcome. Conclusion: Measurement of global longitudinal cardiac strain andstrain rate is possible in fetuses using VVI. Segmental measurements are not significantly differentfrom global measurements; global measurements may be a useful tool to quantitate fetal cardiacfunction. (ECHOCARDIOGRAPHY, Volume 26, January 2009)

fetal echocardiography, cardiac strain, velocity vector imaging

Quantification of fetal cardiac function haslong been an elusive goal in the evaluationof fetal cardiac physiology and adaptation todisease. The fetal circulation is unique in itssource of oxygenated blood, degree of intracar-diac and extracardiac mixing, and output of theright and left ventricles.1 Measurements of car-diac function validated in adults, such as theshortening fraction or ejection fraction, oftenfail to provide accurate results in fetuses dueto intrinsic differences in fetal wall motion andsmall ventricular volumes that magnify mea-surement error. More recently, measurement offetal cardiac strain and strain rate has been

Address for correspondence and reprint requests: Piers C.A. Barker, M.D., Room 7502D, Duke Hospital North, Box3090, Durham, NC 27710. Fax: +1-919-681-7892; E-mail:[email protected]

attempted to overcome the limitations of two-dimensional and M-mode imaging.2–4

Myocardial strain is defined as the changein length of an object relative to its baselinelength caused by an applied stress, with5 strainrate being derived from the velocity of the de-formation over time.6 In the practice of cardiacultrasound, the strain rate is typically mea-sured using tissue Doppler imaging to calculatethe velocities of two points set a small, fixeddistance apart, with cardiac strain then calcu-lated as the integral of the strain rate measure-ment.6 By analyzing segments of myocardiumdirectly rather than changes in ventricular di-mensions or volumes, cardiac strain, and strainrate may be better measurements of ventricu-lar contractility.7 However, assessment of onlycertain small segments of myocardium limitsthe extrapolation of these segmental results toglobal cardiac function.

28 ECHOCARDIOGRAPHY: A Jrnl. of CV Ultrasound & Allied Tech. Vol. 26, No. 1, 2009

FETAL GLOBAL LONGITUDINAL CARDIAC STRAIN AND STRAIN RATE

Both regional cardiac strain and strain ratehave been reported and validated as measuresof ventricular function in adults and children.6However, the majority of these studies havebeen based upon tissue or color Doppler mea-surements, including the first fetal studies.4,8,9

Tissue Doppler measurements have the advan-tage of less reliance on image quality and bor-der detection, and permit the acquisition ofdata at much higher frame rates than thoseavailable by traditional two-dimensional ultra-sound or cardiac magnetic resonance imaging.6However, tissue Doppler is inherently limitedby its dependence on the angle of insonation,which permits analysis of only those limitedsegments of myocardium that are parallel tothe ultrasound beam, and can be affected by re-gional cardiac translation.10 Both of these lim-itations pose significant problems in fetal pa-tients, given the variation in fetal position, andprevent measurement of global indices for theleft or right ventricle.

Speckle or feature tracking is a novel wayof assessing myocardial motion from the two-dimensional B-mode image. As opposed totissue Doppler, “speckles” derived from the sta-ble interference and backscatter of the ultra-sound signal in the myocardium are trackedfrom frame to frame with reference to their pre-vious position and distance of movement.7,11,12

From these data, both the velocity and the di-rection of myocardial motion (the velocity vec-tor) can be calculated for any region of themyocardium, regardless of angle to the ultra-sound beam, with strain rate and strain cal-culated by comparing adjacent velocity vectors.Further refinements of this tracking techniqueallow for the incorporation of manually tracedborders, annuli position, and speckle periodic-ity to create the potentially more accurate “fea-ture” tracking software used in this study.7,11

This method has been validated in adult pa-tients for the calculation of cardiac strain andstrain rate,13 but the application to fetal pa-tients has only recently been reported, andonly in normal fetuses.2,3,14 Recently, feature-tracking techniques have been applied to assessglobal cardiac strain and strain rate in animalinfarct models and humans after myocardial in-farction, in whom regional measurements maynot accurately reflect cardiac function due toinjured segments,15 as well as in adults withsystemic right ventricles to overcome the lim-itations of right ventricular (RV) geometry.16

However, this method has not yet been fullystudied in fetal patients, whose small cardiac

size and different physiology limit the useful-ness of regional measurements.

We therefore report our experience in thenovel use of velocity vector imaging (VVI) tocalculate global cardiac strain, strain rate, andvelocity in a series of fetuses with and withoutheart disease.

Methods

Longitudinal cardiac strain, strain rate, andvelocity analysis was performed on the fe-tal right ventricle and fetal left ventricle (ifpresent) obtained during a clinically indicatedfetal echocardiogram. The study was approvedby the Duke University Medical Center Institu-tional Review Board for Human Research andall subjects consented to participate. A researchversion of the commercially available VVI soft-ware (Siemens Medical Solutions, MountainView, CA, USA) was used for all measurements.

For each fetus, a high-resolution, zoomedloop of the apical four-chamber view incorpo-rating at least one complete cardiac cycle wasrecorded, with machine settings adjusted tomaximize frame rate. This image was storeddigitally and transferred to the offline worksta-tion (Syngo USWP, Siemens Medical Solutions)for later analysis. Syngo VVI was launchedfrom review of each DICOM digital clip. R-wavegating was performed using a superimposedM-mode tracing of left or RV wall motion todefine the onset of ventricular systole (initial in-ward motion of the ventricular wall) as a corol-lary of the electrical QRS and therefore the be-ginning and end of a cardiac cycle. This methodof R-wave gating was also used for fetuses eval-uated during an arrhythmia, with the cardiaccycle selected as representative of baseline si-nus rhythm (i.e., not during or at the onset ortermination of the abnormal rhythm).

After definition of the cardiac cycle, the en-docardium of the right and left ventricles wastraced manually from a single frame of thedigital loop that provided the clearest still-frame endocardial border definition (typicallymid-systole). The same cardiac cycle was usedfor both the left ventricular (LV) and RV trac-ing, except in three normal fetuses and twoabnormal fetuses in which separate apicalfour-chamber views were required. Endocar-dial tracing began at the edge of the atrioven-tricular valve annulus, extended to the apexof the ventricle without incorporation of thepapillary muscle complex, and returned basallyto the other edge of the atrioventricular valve

Vol. 26, No. 1, 2009 ECHOCARDIOGRAPHY: A Jrnl. of CV Ultrasound & Allied Tech. 29

BARKER, ET AL.

annulus. This therefore provided both the bor-der and annuli position information necessaryfor the “feature-tracking” component of theVVI algorithm. Twenty-two individual, equallyspaced velocity vectors were then automaticallycalculated for each frame of the cardiac cycleby the VVI algorithm and displayed for thecomplete loop. Accuracy of border tracking wasvisually confirmed by viewing the cardiac cy-cle with only border information displayed (i.e.,with velocity vectors removed). If necessary, in-dividual regions of the border were adjusteduntil the border was correctly tracked for eachframe.

Cardiac strain, strain rate, and velocity datawere automatically calculated from the veloc-ity vector information, and displayed in a six-segment model for both fetal ventricles. In addi-tion, the global peak systolic strain, global peaksystolic strain rate, and global peak systolic ve-locities were calculated from the entire velocityvector dataset as an average of all segments ofventricular motion, and displayed as a separatecurve.

Statistical Testing

Global longitudinal cardiac strain, strainrate, and velocities were compared to regionalmeasurements using Student’s t-test for bothnormal fetuses and fetuses with heart disease.A P-value of < 0.05 was used to define a signif-icant difference. Interobserver variability wastested between two observers (PB and HH) onten randomly selected datasets and intraob-server variability was tested for two observers(PB and HH) on five randomly selected datasetsusing coefficient of variation analysis.

For fetuses with heart disease, global longitu-dinal cardiac strain and strain rate were com-pared to visually estimated function (hypercon-tractile, normal, mildly decreased, moderatelydecreased, and severely decreased, as recordedby a skilled independent observer (MC) blindedto the results of the strain analysis) and ulti-mate fetal outcome. No comparisons were madebetween abnormal fetuses as a group and nor-mal fetuses due to the heterogeneity of fetalcardiac diagnoses.

Results

Forty-eight fetal patients were enrolled inthe study, consisting of 33 fetuses with normalcardiac anatomy and function, and 15 fetuseswith congenital or functional heart disease. The

median gestational age was 24 weeks (range17–38 weeks). Four fetuses with congenital orfunctional heart disease underwent multipleechocardiograms, permitting serial analysis offetal strain. Accurate endocardial border track-ing and calculation of velocity vectors were ac-complished on all right and left ventricles inall fetuses despite limitations in image qual-ity secondary to fetal position or maternal bodyhabitus, with the exception of one left ventriclein a single abnormal fetal patient due to exces-sive fetal motion. Longitudinal cardiac strainmeasurements were possible in all tracked fe-tuses, while strain rate and velocity measure-ments were limited to 22 normal fetuses and 12abnormal fetuses due to compression of framerate/time data in the other fetuses. Figure 1demonstrates typical LV velocity vectors andthe resultant strain calculations for a normal24-week fetus.

Table I demonstrates the results of globaland segmental longitudinal strain analysis forboth left and right ventricles in normal fe-tuses. The mean LV global peak systolic strainwas −17.7% (standard deviation 6.4) with amedian of −16.6% (range −9.2% to −32.9%).The mean RV global peak systolic strain was−18.0% (standard deviation 6.4) with a medianof −17.4% (range −6.7% to −33.4%). There wasno statistical difference between global strainand segmental strain measurements for eitherventricle.

Table II demonstrates the results of globaland segmental longitudinal strain rate analy-sis for both left and right ventricles in normalfetuses. The mean LV global peak systolic strainrate was −2.4/sec (standard deviation 1.2/sec)with a median of −1.9/sec (range −5.9/secto −0.7/sec). The mean RV global peak sys-tolic strain rate was −1.9/sec (standard devi-ation 0.8/sec) with a median of −1.7/sec (range−3.8/sec to −0.5/sec). There was no statisti-cal difference between global strain rate andsegmental strain rate measurements for eitherventricle.

Table III demonstrates the results of globaland segmental longitudinal velocity analysisfor both left and right ventricles in normalfetuses. The mean LV global peak systolicvelocity was 1.6 cm/sec (standard deviation0.6 cm/sec) with a median of 1.5 cm/sec (range0.5–3.0 cm/sec). The mean RV global peak sys-tolic velocity was 1.6 cm/s (standard devia-tion 0.5 cm/sec) with a median of −1.6 cm/sec(range 0.8–2.3 cm/sec). In contrast to strain andstrain rate measurements, the basal segmental



Figure 1. Velocity vector tracingof the left ventricular endocardium(endo) in a normal fetus at 24weeks of gestation with correspond-ing global and segmental straincurves. Global (average) peak sys-tolic strain curve is shown in black.Base left = septal base; mid-left =mid-septal; apex left = apical septal;apex right = apical free wall; mid-right = mid free wall; base right =basal free wall.

velocities for both the left and right ventricleswere significantly higher than the global ve-locity measurement, while the apical segmen-tal velocities were significantly lower than theglobal velocity measurement.

Fetuses with congenital or functional heartdisease demonstrated similar results, with nosignificant difference detected between globalstrain and global strain rate measurementscompared to regional measurements. Segmen-tal velocities did differ, however, with the LVapical septal and apical free wall velocities sig-nificantly lower than the global velocity, andthe basal free wall significantly higher. For theright ventricle, the mid-septal and apical sep-tal velocities were significantly lower, and thebasal free wall significantly higher compared tothe global RV peak velocity.

TABLE I

Ventricular Peak Global and Regional Strain Measurements in Normal Fetuses (n=33)

LV Mean LV Median LV Range LV SD RV Mean RV Median RV Range RV SD

Global strain −17.7 −16.6 −32.9 to −9.2 6.4 −18.0 −17.4 −33.4 to −6.7 6.4Septal base −15.9 −15.4 −44.8 to −2 8.7 −17.3 −15.2 −34.3 to −5.6 7.9Mid-septal −14.9 −13.4 −41.1 to −1.5 7.7 −17.4 −16.8 −31.5 to −6 6.7Apical septal −18.5 −19.4 −37.9 to −4.7 8.5 −16.1 −15.0 −39.2 to −2.5 9.3Apical free wall −19.3 −19.1 −41.9 to −2.6 9.5 −16.7 −15.5 39.2 to −1.5 10.1Mid free wall −19.1 −19.0 −39 to −6.3 8.3 −19.4 −19.5 −33.1 to −8.2 7.0Base free wall −17.8 −15.1 −37 to −5.7 9.4 −20.2 −18.2 −40 to −1.5 9.1

All values expressed as percent change in length.P > 0.05 for all regional strain measurements compared to global strain.LV = left ventricular; RV = right ventricular.

Table IV demonstrates global peak longitu-dinal strain and strain rate measurements infetuses with structural or functional heart dis-ease, compared with visually estimated func-tion and clinical outcome. There was an over-all trend toward lower global strain and strainrate compared to normal fetuses, but this wasnot uniform and varied depending upon diseasestate, with one fetus with aortic valve stenosisdemonstrating global peak cardiac strain morethan 1 standard deviation above the global peaksystolic strain in normal fetuses. There was nocorrelation between calculated cardiac strainand strain rate and visually estimated ventric-ular function, although in one patient followedserially (chaotic atrial tachycardia [CAT 1]),the improvement in ventricular functionmatched an improvement from a low cardiac


BARKER, ET AL.

TABLE II

Ventricular Peak Global and Regional Strain Rate Measurements in Normal Fetuses (n=22)


Global strain rate −2.4 −1.9 −5.9 to −0.7 1.2 −1.9 −1.7 −3.8 to −0.5 0.8Septal base −1.9 −1.7 −4.9 to −0.6 1.0 −1.9 −1.9 −4.1 to −0.9 0.8Mid-septal −2.1 −1.9 −7.5 to −0.6 1.5 −1.9 −2.0 −3.8 to −0.9 0.8Apical septal −2.7 −2.4 −8.2 to −0.6 1.7 −2.1 −1.8 −5.5 to −0.2 1.3Apical free wall −2.8 −2.7 −5.7 to −0.2 1.5 −2.5 −1.9 −5.9 to −0.4 1.6Mid free wall −2.4 −1.9 −5.7 to −0.7 1.4 −2.2 −2.3 −3.8 to −1 0.8Base free wall −2.5 −1.9 −7.8 to −0.9 1.7 −2.3 −2.2 −4.6 to −0.9 1.1

All values expressed as rate of change in length (per second).P > 0.05 for all regional strain rate measurements compared to global strain rate.LV = left ventricular; RV = right ventricular.

strain to closer to the normal value. Similarly,there was no correlation between calculatedstrain and strain rate and ultimate fetal out-come.

Intraobserver variability ranged between 5–12% for the left ventricle and 5–6% for the rightventricle. Interobserver variability ranged be-tween 10% for the left ventricle and 13% for theright ventricle.

Discussion

Myocardial strain and strain rate have beenproposed as useful tools in the evaluation of car-diac mechanics. Myocardial strain and strainrate, being regional measurements, are rela-tively free of confounding factors such as car-diac translation, which may occur with respi-ration or motion of structures adjacent to theheart.10 The presence of multiple confoundingvariables such as fetal motion, high heart rates,and limited maternal transabdominal imaging

TABLE III

Ventricular Peak Global and Regional Velocity Measurements in Normal Fetuses (n=22)


Global velocity 1.6 1.5 0.5–3.0 0.6 1.6 1.6 0.8–2.3 0.5Septal base 2.1∗ 1.9 1.0–4.6 1.0 2.0∗ 2.1 0.8–3.1 0.6Mid-septal 1.4 1.2 0.2–3.4 0.9 1.4 1.3 0.6–2.6 0.5Apical septal 0.6∗ 0.6 0.0–1.5 0.4 0.8∗ 0.6 0.2–3.1 0.7Apical free wall 1.0∗ 0.8 0.2–2.4 0.6 1.1∗ 1.1 0.1–2.4 0.7Mid free wall 1.9 1.7 0.3–3.6 0.9 1.9 1.8 0.7–3.8 0.8Base free wall 2.5∗ 2.5 0.8–4.9 1.0 2.6∗ 2.5 1.2–4.7 0.9

All values reported as cm/sec.∗P < 0.05 for regional velocity measurement compared to global velocity measurement.LV = left ventricular; RV = right ventricular.

windows therefore makes these new measure-ments appealing for assessment of fetal cardiacfunction.

The majority of published studies havemeasured cardiac strain and strain rate us-ing tissue or color Doppler-derived velocities,although more recent speckle-tracking algo-rithms have permitted these measurements tobe performed on two-dimensional data at ac-ceptably high frame rates.11 These measure-ments have been validated in vivo and in vitrofor both tissue Doppler and two-dimensionallyderived data, and have compared favorably toMRI-tagging techniques.7,10,11,13 While tissueDoppler has the advantage of less reliance onimage quality and visual border detection, ithas the inherent disadvantage of all Dopplertechnologies by being dependent on angle of in-sonation.5 This therefore limits the number ofcardiac segments available for analysis to thoseparallel to the transducer beam, resulting in ex-clusion of the cardiac apex.



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BARKER, ET AL.

Dependency on angle of insonation is particu-larly problematic for fetal cardiology, given theextremely variable position of the fetus rela-tive to a transducer placed on the maternal ab-domen. In the first fetal study published usingtissue Doppler to calculate fetal cardiac strain,this angle dependence limited analysis to only75 of 120 fetuses (63%),8 although this im-proved in subsequent tissue/color Doppler stud-ies.4,9 A similar study reporting measurementof fetal tissue Doppler velocities, rather thanmyocardial strain, excluded 16% of potentialsubjects for similar reasons.17

In contrast, the two-dimensional feature-tracking program used in this study permit-ted the analysis of all visible ventricular seg-ments, independent of fetal position or angleof insonation. This resulted in only 1 ventricleout of a total of 104 ventricles being excludedfor analysis due to limited views (<1% of at-tempted measurements). Additionally, the in-clusion of all six segments permitted the calcu-lation of global peak longitudinal systolic strainand strain rate as novel measurements of fetalventricular function.

This study demonstrates that the feature-based VVI software can be successfully ap-plied to fetal 2-dimensional echocardiographicdatasets. This finding is similar to recentlypublished fetal studies examining normal fe-tuses.2,3 Calculated global and regional peaksystolic strain measurements for normal fe-tuses were similar for both the fetal left andright ventricles at approximately −18%, and−2.4 s−1 and −1.9 s−1, respectively. These mea-surements are similar to those published fromin vitro, adult, and fetal studies.3,6,8,10,13,18

However, calculated cardiac strain and strainrate were lower than two recently reported fe-tal and pediatric studies using tissue or colorDoppler methods,4,6,8,10,13,19 with the exceptionof LV peak strain rate, which was similar to thereported pediatric values. While overall therehas been a good reported correlation betweentissue Doppler and the two commonly usedfeature-tracking algorithms, discrepancies be-tween these methods have also been recentlyreported that prevent the final definition of anormal range for these values in fetuses.20–23

Calculated myocardial velocities were lowerthan previously reported studies,2–4,17 althoughthis study did not specifically analyze the veloc-ity at the atrioventricular annulus. It is not sur-prising that there was more variability betweenregional segments and global measurementsof velocity, based upon fiber orientation vari-

ation for both the left and right ventricles frombase to apex.12 Previous studies have shown fe-tal myocardial velocity to vary with gestationalage,2,4 consistent with fetal somatic growth, al-though the effect of gestational age was not as-sessed in this study.

The finding that global measurements ofpeak longitudinal strain and strain rate arenot significantly different from multiple seg-mental measurements suggests that globalmeasurements may be a more useful tool toquantitate fetal cardiac function, and may besuperior to tissue Doppler measurements.Specifically, global measurements based ontwo-dimensional datasets permit angle inde-pendent analysis and avoid any variation inthe placement of the sample volumes or re-gions of interest in such a small structure asthe fetal heart. In adult patients with systemicright ventricles, global measurements havebeen proposed as a method to avoid confound-ing wall motion abnormalities and local noisewhich may more greatly impact regional mea-surements.16 To this end, a lower global mea-surement may also provide a clue to look moreclosely at the individual segments for regionalhypokinesis.

For fetuses with congenital or functionalheart disease, the global peak longitudinalstrain and strain rate demonstrated a tendencytoward lower values, although this was not uni-form as demonstrated by the fetus with aorticvalve stenosis, the fetus with ventricular sep-tal defect/aortic stenosis and coarctation of theaorta, the fetus recovered from CAT 1, and thefetal right ventricle in the donor in one caseof twin-twin transfusion syndrome (TTTS 2).It is possible to speculate that the increasedstrain and strain rate in these fetuses repre-sent myocardial compensation for the struc-tural heart disease (increased afterload in thecase of aortic stenosis and ventricular septal de-fect/coarctation) and functional heart disease(increased cardiac output of the right ventri-cle in the donor twin). However, this theorydoes not fully explain the increase in strainand strain rate in the recovering fetus with ar-rhythmia, or the lower strain and strain ratethroughout gestation of the fetus with con-genitally corrected transposition of the greatarteries (CCTGA 1). Instead, these differencesmore likely underscore the limitations of ourunderstanding of fetal cardiac adaptation todisease.

The lack of significant correlation betweencalculated strain and strain rate, and visually



estimated cardiac function and outcomes in fe-tuses with heart disease further highlights ourlimitations in assessing fetal cardiac functionand estimating prognosis. In the case of thetwo fetuses who died in utero, it is possible thatthey were well compensated at the time of thefetal study, and decompensated before the nextvisit. While the small number of abnormal fe-tuses and the variability in pathology limitedour ability to analyze this group in more detail,the application of VVI to much larger groupsof abnormal fetuses opens the field for furtherinvestigation.

Limitations

The small size of the current study preventsdefinition of normal values for fetuses at dif-ferent gestational ages, as well as preventsmore detailed assessment of the relationshipbetween calculated measurements and postna-tal outcome. RV strain and strain rate were cal-culated using a LV-derived six-segment model,which may not accurately reflect the more com-plex geometry of the right ventricle, but issimilar in approach to previous studies usingtissue Doppler from an apical view as the mea-surement tool. Circumferential and radial mea-surements were not analyzed in this study,and could provide useful comparisons to LVmeasurements. Unfortunately, compression offrame rate/time data limited the calculation ofstrain rate and velocity in a few fetuses, but thisdid not affect the strain measurement as strainis calculated directly from speckle motion by theVVI algorithm. Finally, the very nature of fetalimaging, due to the effect of fetal movement,size, position, and maternal factors complicateefforts to obtain two-dimensional datasets foranalysis, although it is reassuring that ade-quate images with accurate border trackingcould be obtained for all patients but one inthis study.

Conclusion

Fetal global peak longitudinal strain, strainrate, and velocity can be successfully calculatedindependent of angle of insonation using VVI.Global peak longitudinal strain and strain ratedo not differ from regional measurements. Pre-liminary experience suggests that normal fetalleft and right ventricular global peak longitu-dinal strain and strain rate measurements aresimilar to those of the normal adult heart. This

novel use of VVI is a promising tool for furtherinvestigation into fetal cardiac physiology.

Acknowledgments: The authors are particularly in-debted to the sonographers and staff of the Duke UniversityPediatric Echo Laboratory for their assistance with imageacquisition for this project.

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strain cardíaco na avaliação da função cardíaca fetal

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