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A Reproducibility Study of a TDI-Based Method to Calculate Indices of Arterial Stiffness

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A Reproducibility Study of a TDI-Based Method to Calculate Indices of Arterial Stiffness
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  doi:10.1016/j.ultrasmedbio.2007.08.010 ●  Original Contribution A REPRODUCIBILITY STUDY OF A TDI-BASED METHOD TOCALCULATE INDICES OF ARTERIAL STIFFNESS M ARTIN  W. C LARIDGE ,* G ARETH  R. B ATE ,* J UDE  A. D INELEY , † P ETER  R. H OSKINS , † T IM  M ARSHALL , ‡ D ONALD  A. A DAM ,* A NDREW  W. B RADBURY ,* AND  A NTONIUS  B. W ILMINK * *Department of Vascular Surgery, University of Birmingham, Heart of England NHS Foundation Trust,Birmingham, UK;  † Department of Medical Physics, Edinburgh University, Edinburgh, UK; and  ‡ Department of Public Health and Epidemiology, University of Birmingham, Birmingham, UK (  Received   15  March  2007;  revised   10  August   2007;  in final form  27  August   2007) Abstract—The aim of the study was to investigate the reproducibility of estimation of Young’s modulus E andpressure strain elastic modulus Ep, derived from a tissue Doppler imaging (TDI) wall motion technique. Healthysubjects had their arteries insonated at the same sitting by two different observers and at two different sittingsby the same observer. From 32 subjects in the reproducibility study, within-scan coefficient of variation (CV) was4.5%. Intraobserver between-scan CV for E was 12.7% and for Ep 11.0%. Interobserver CVs were 8.3% and9.3%, respectively. TDI is a reproducible, valid and highly sensitive direct assessment of arterial wall parameters.It is at least as reproducible as other ultrasound based methods for assessing arterial stiffness and also providesincreased information about the arterial distension waveform. (E-mail: martin@claridge.org.uk) © 2008 World Federation for Ultrasound in Medicine & Biology.  Key Words:  Arterial stiffness, Common carotid artery, Distension waveform, Doppler ultrasound, Pressure strainelastic modulus, Reproducibility, Tissue Doppler imaging, Young’s modulus. INTRODUCTION An enlarging body of evidence suggests that increasedarterial stiffness is associated with markers of cardiovas-cular risk and that this stiffness may herald the onset of cardiovascular disease before manifestation of symptomsor detection of frank atherosclerotic lesions (Van Bortelet al. 2001; Glasser et al. 1997). Measurement of arterial stiffness may, therefore, become a part of the process of both risk assessment and monitoring of therapy in pa-tients with cardiovascular disease.The general term arterial stiffness describes therigidity of the arterial wall. Indices of arterial stiffnesscan be divided into two types: indices of “structuralstiffness” and indices of “material stiffness” (Hayashi1993). Indices of structural stiffness are descriptors of the overall stiffness of an artery. One commonly usedindex of structural stiffness is the “pressure strain elasticmodulus” Ep (eqn 1) first described by Peterson et al.(1960). This requires measurement of the fractional ar-terial distension from diastole to systole and the corre-sponding blood pressures.Ep    p * d   ⁄   d (1)where d is average diameter,   p is systolic minus dia-stolic pressure and   d is the difference in diameter atsystole and diastole.Young’s modulus E is the most common index of material stiffness. As E is a true material property, it isindependent of wall thickness and changes in E withinarteries will reflect changes in the composition of thewall ( e.g. , change in proportion of elastin and collagen).E may be cast in a similar form to that for Ep, as shownin eqn. 2.E   d⁄2h   Ep (2)where h is wall thickness.Arterial distension can be estimated from the B-scan image (Blankenhorn et al. 1988), from the M-mode trace (Gamble et al. 1994; Hoeks et al. l997), or from the radio-frequency (RF) echo pattern (Benthin et al. 1991; Address correspondence to: Martin W. Claridge, University De-partment of Vascular Surgery, Heart of England NHS FoundationTrust, 5 Netherwood House, Solihull Hospital, Lode Lane, SolihullB91 2JL, UK. E-mail: martin@claridge.org.uk  Ultrasound in Med. & Biol., Vol. 34, No. 2, pp. 215–220, 2008Copyright © 2008 World Federation for Ultrasound in Medicine & BiologyPrinted in the USA. All rights reserved0301-5629/08/$–see front matter 215  Hasegawa 2006; Kanai et al. 2003; Kawasaki et al. 1987;Meinders et al. 2001, 2004). These techniques werecompared by Stadler et al. (1997) who showed thatphase lock loop tracking showed overall superiority interms of reproducibility. The arterial distension wave-form (ADW) may also be measured from tissue Dopplerimaging (TDI) (Bonnefous et al. 2000; Dineley et al. inpress). This technique uses integration of wall velocitiesobtained from tissue Doppler imaging to calculate thearterial distension waveform. It has been shown using amoving platform phantom that the TDI technique has aminimum resolvable displacement of 22   m and a mea-surement accuracy of 8% using a physiological wallmotion with a peak displacement of 689   m (Hammeret al. in press).In superficial arteries, such as the carotid, it is alsopossible to measure the intima-media thickness (IMT)(Wendelhag et al. 1991; Kanters et al. 1998; van Bortel2005). In health and early disease, the IMT can be takenas a measure of wall thickness, hence, enabling estima-tion of Young’s modulus (E). The measurement of E hasbeen previously reported by Gamble et al. (1994).The aim of this study was to investigate thereproducibility of TDI in calculating, E and Ep in thecommon carotid arteries (CCAs) of human subjects.The study used a commercially available TDI basedmethod for estimation of the ADW, described byBonnefous (2001). METHODS Study design All subjects recruited into the study provided fullyinformed written consent. Ethical approval was grantedby Birmingham East District Research and Ethics Com-mittee. All subjects completed a questionnaire to provideinformation on past medical and drug history.  Arterial distension waveform capture All subjects were rested for 5 min before measure-ment and were placed supine on an adjustable couch,with a pillow under their head to minimise movement.The Distal CCA was imaged longitudinally using theL12/5 linear array of an HDI 5000 ultrasound imagingsystem (Philips Medical Systems, Bothell, WA, USA), ata point 3 cm proximal to the srcin of the carotid bulb.To ensure that the same segment of artery was insonatedat each sitting, a hardcopy of the B-mode image wasrecorded at each sitting, and compared with the imagerecorded at the first sitting. Scan-plane alignment wasperformed using B-mode imaging to ensure that echoesfrom the intima-media layers were clearly visible. At thispoint, tissue Doppler imaging (TDI) was enabled andreal-time images collected over at least three cardiaccycles were saved to disc. The data were transferredoff-line for analysis.Three blood pressure measurements in the rightbrachial artery using a Critikon automatic blood pressuremanometer (GE Healthcare, Bucks, UK) were takenwhilst the patient remained supine. One measurementwas taken before ADW capture, one whilst the data weretransferred off-line for analysis and one after data cap-ture was completed. The mean change in blood pressure(  p) of the three measurements was used in furthercalculations.  Arterial distension waveform analysis After transfer of the raw cineloop to the PC, acommercial software analysis package (HDI-Lab, PhilipsMedical Systems, Bothell, WA, USA) was used to obtainwall distension waveforms from the TDI data. The corefeature of this technique is that TDI data provides infor-mation on wall velocity as a function of time. Walldistension is then calculated by integration of velocitywith respect to time. This is performed for each scan-lineof the TDI image, providing some 50 measurements of the distension-time waveform over a 2 cm length of artery. A graphic representation of this is shown in Fig.1. The mean arterial diameter change (MADC) wascalculated from all lines in all cardiac cycles in which thearterial diameter change was measured by obtaining themaximum excursion for each line and then taking themean of all these values. Calculation of IMT and arterial diameter  IMT and arterial diameter was calculated from thesame segment of CCA in the same cineloop as ADWusing an automated edge detection program examiningthe B-mode image. (IMT plug-in, HDI-Lab, PhilipsMedical Systems, Bothell, WA, USA). This method iswell recognised and has been used in previous publishedresearch with good reproducibility (Kennedy et al. 2001;Fathi et al. 2004). Mean IMT for the far wall in all framesacross all cardiac cycles captured in the cineloop wasused, in view of published advice that IMT changesacross the cardiac cycle and that measurement of IMT inthe far wall as opposed to the near wall is more accurate(van Bortel 2005).  Reproducibility study Interobserver and intraobserver reproducibility wasassessed in healthy subjects. A subject was defined ashealthy if there was no evidence of ischaemic heartdisease, cardiac arrhythmia, heart failure, diabetes, renalfailure or hypertension. Subjects underwent direct ques-tioning in terms of past medical history, drug history andexercise tolerance to establish this.For interobserver reproducibility, the same patient 216 Ultrasound in Medicine and Biology Volume 34, Number 2, 2008  was assessed by two different observers at the samesitting. One observer had 1 year’s experience in ultra-sonography, and the other had 8 year’s experience. Eachobserver was unaware of the measurements of the otherobserver. For intraobserver reproducibility, the samesubject was assessed by the same observer at two sittingson a different day at least 24 h apart. Each assessmentconsisted of scan acquisition of the left and right com-mon carotid artery and blood pressure measurement. AB-mode image of the insonated artery was taken at eachscan acquisition to ensure that the same segment of arterywas insonated repeatedly. MADC, internal arterial diameterand IMT were assessed separately and  E   and  Ep  werecalculated separately using these data for each CCA. Statistical analysis After extraction and collation of the raw data usingMicrosoft Excel, the data were analysed using Stata 8.1for Windows (STATA Stata Corporation, College Sta-tion, TX, USA) in association with a statistician from theUniversity of Birmingham. The results of the reproduc-ibility study were analysed with Bland-Altman Plots andby calculating coefficients of variation. The coefficient of variation was defined as observer error (standard devia-tion of the mean difference between observations/   2 )multiplied by 100 divided by the pooled mean values. RESULTS A total of 32 subjects were analysed in the interob-server study and 30 subjects were analysed in the in-traobserver study. Two subjects did not return for thesecond sitting of the intraobserver study and, therefore,could not be included in that part of the reproducibilitystudy. The mean age of the study population was 43 y(range 18 to 72). The mean systolic blood pressure in thestudy group was 124 mm Hg (range 94 to 184) and themean diastolic blood pressure 75 mm Hg (range 54 to100). The Bland-Altman plots of the interobserver dif-ferences (Fig. 2) and intraobserver differences (Fig. 3) showed that no relationship exists between the differencein measurement and the estimated true value. The withinscan standard deviation of the difference between themeasurements was 18 microns for the interobserverstudy and 20 microns for the intraobserver study. Thewithin scan (variation between cardiac cycles with onescan) coefficient of variation (standard deviation/ mean,CV) was 14.5 %. Reproducibility statistics betweenscans are summarised in Table 1. DISCUSSION The reproducibility of our measurements is im-proved compared to the best reported in the literature Fig. 1. A Graphical representation of arterial distension waveform over four cardiac cycles and a segment of commoncarotid artery measuring approximately 2 cm. Dilations: how far in microns arterial wall moved apart during cardiaccycle. Scan line number: virtual line down which software calculated arterial wall dilation (48 lines in total). Time  total length in time of scan and scale over which arterial dilation occurred. Arterial stiffness reproducibility study ● M. C LARIDGE  et al.  217  Fig. 2. Bland-Altman plots showing interobserver variabilityfor calculated indices as measured in 32 arteries by two ultra-sonographers. The difference between the two measurements asa percentage of the mean measurement plotted on the y-axisagainst the mean of the two measurements on the x-axis. Thehorizontal lines depict the mean difference (bias) and the limitsof agreement (bias  2 SD) between the measurements.Fig. 3. Bland-Altman plots showing intraobserver variabilityfor calculated indices as measured in 32 arteries by the sameultrasonographer. The difference between the two measure-ments as a percentage of the mean measurement plotted on they-axis against the mean of the two measurements on the x-axis.The horizontal lines depict the mean difference (bias) and thelimits of agreement (bias  2 SD) between the measurements. 218 Ultrasound in Medicine and Biology Volume 34, Number 2, 2008  using echo tracking (Stadler et al. 1997) and M-modeimaging (Kanters et al. 1998). Stadler et al. (1997) re- ported interobserver reproducibility only of 17% in 26subjects and Kanters et al. (1998) reported interobserverreproducibility of 19% for the right CCA and 25.4% forboth CCAs in 25 subjects. They also comment thatintraobserver reproducibility was equal or less than thesevalues. Selzer at al. (2001) reported a CV of 14.5% forEp and 13.1% for E in a study utilising computer analysisof approximately 70 sequential B-mode ultrasound im-ages per examination of the right CCA in 24 subjectsexamined 1 to 2 wk apart. Our study demonstrates a CVof 12.0% for EP and 14.9% for E in the left CCA and14.6% for Ep and 17.3% for E in the right CCA, Ourresults are, therefore, comparable, although our subjectswere examined only at least 24 h apart. We are able toshow a CV of 11.0% for Ep and 12.7% for E in botharteries, with better interobserver reproducibility, whichwas not reported by Selzer et al. (2001) in their study.The range of values for E and Ep that we have calculatedin healthy subjects is similar to that estimated in previousstudies (Nicholls and O’Rourke 2005). The TDI method develops a highly detailed plot of the arterial waveform from 200 to 400 frames per inter-rogation. A cineloop of 4 s duration provides informationover at least three cardiac cycles (see Fig. 1). We believe that this plot of approximately 20000 points is moredetailed than any other ultrasound based method of as-sessing arterial stiffness parameters so far reported in theliterature and the TDI system still maintains good repro-ducibility whilst collecting precise and highly detailedinformation. It is quick to use both in terms of datagathering and then later analysis. In our study, we inter-rogated a segment of artery approximately 2 cm in di-ameter. This technique does allow interrogation of agreater length of artery than this (up to 8 cm) but thereproducibility may not be as good. As with other ultra-sound techniques, accuracy of data collection is ham-pered by patient movement and cardiac arrhythmias (no-tably atrial fibrillation) but because it is quick to set upand to collect data, the effect of patient movement isminimised. This system could be used to collect data onother superficial arteries but will only function with alinear array ultrasound probe, thus limiting the depth of arteries that can be examined. In addition the minimumdiameter for the artery is 3 mm and a bifurcation cannotbe examined. The maximum duration of cineloop thatcan be collected is 4 s at present.The method for estimation of E and Ep ideallyrequires that the blood pressure is applicable to thearterial site of interest. In this article, the pressure wasmeasured in the brachial artery using a radial cuff. It isknown that there are differences in the pressure wave-form obtained at different locations in the circulation(Nicholls and O’Rourke 2005). A commercial device (Sphygmacor, Scanmed, Draycott, Gloucestershire, UK)is available for estimation of central pressure from radialartery pressure waveform obtained by tonometry andcalibrated by arm cuff pressure. This device operates onthe basis of a transfer function between the radial arteryand aorta, and is based on work from the group led byO’Rourke (O’Rourke et al. 1967; Karamanoglu et al.1993; Gallagher et al. 2004). However, there does notappear to be a similar transfer function or device avail-able for calculation of carotid pressures from arm pres-sure measurements. In a recent paper, Segers et al.(2005) studied blood pressure measurements at varioussites in 276 subjects. He estimated that the diastolicblood pressure was identical for brachial artery and ca-rotid arteries (to within 0.1%), and that the systoliccarotid artery blood pressure was lower than the brachialartery by less than 2%. This indicates that the use of  Table 1. Mean values and CV for indices measured in reproducibility study Interobserver study Intraobserver studyLCCA RCCA Combined LCCA RCCA CombinedElastic modulus (mm Hg) 873* 864* 868* 897‡ 805‡ 843‡797† 820† 808† 872§ 768§ 768§ 12.3% 13.5% 9.3% 12.0% 14.6% 11.0% 146 161 111 150 161 261 Young’s modulus (mm Hg) 3873* 4309* 1311* 4139‡ 4285‡ 1276‡3550† 4304† 1214† 3966§ 3982§ 1248§ 13.4% 17.3% 8.3% 14.9% 17.3% 12.7% 707 1021 193 861 1009 245 Value in bold  coefficient of variation; Value in italics  standard deviation; Ep  elastic modulus; E  Young’s modulus. *  First observer. †  Second observer.‡ First session.§ Second session.Arterial stiffness reproducibility study ● M. C LARIDGE  et al.  219
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