Int J Cardiovasc Imaging (2014) 30:305–312 DOI 10.1007/s10554-013-0348-x
ORIGINAL PAPER
Echocardiographic measurement methods for left ventricular linear dimensions in children result in predictable variations in results Shelby Kutty • David Russell • Ling Li • Rimsha Hasan • Qinghai Peng • Peter C. Frommelt David A. Danford
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Received: 30 October 2013 / Accepted: 4 December 2013 / Published online: 10 December 2013 Ó Springer Science+Business Media Dordrecht 2013
Abstract Precise quantification of left ventricular (LV) cavity dimensions assumes great importance in clinical cardiology. Pediatric guidelines recommend the left parasternal short axis (PSA) imaging plane for measuring LV cavity dimensions, while measuring from the long axis (PLA) plane is the convention in adult echocardiography. We sought to compare measurements obtained by twodimensional (2D) and M-mode (MM) techniques in the two imaging planes. Healthy subjects were prospectively recruited for research echocardiography. Complete 2D, spectral and color flow Doppler examinations were performed in a non-sedated state. All subjects had structurally and functionally normal hearts. LV cavity dimensions were obtained in PLA and PSA views using 2D and MM yielding four measurement sets for each subject: PLA direct 2D; PLA 2D-guided MM, PSA direct 2D, PSA 2Dguided MM. A commercially available ultrasound system (Vivid E9, GE) was used and data stored digitally for subsequent analysis (EchoPAC BT11, GE). Acquisition and measurements were made by a single observer from at least three consecutive cardiac cycles, and averaged for each of the four categories. The study cohort consisted of 114 subjects (mean age 9 years, range 1–18; mean BSA 1.1 m2, range 0.42–2.6). The smallest estimate of LV enddiastolic dimension (LVED) was obtained by PLA 2D,
with larger estimates by PLA MM, PSA 2D, and PSA MM. Largest estimates of LV end-systolic dimension (LVES) are by 2D methods, with smaller estimates by both MM techniques. The smallest shortening fraction (SF) was by PLA 2D; other methods yielded larger SF. Temporal resolution is limited in 2D methodology and may account for the smaller LVED, larger LVES and smaller SF observed. Long axis methodology may predispose to off-center or non-perpendicular data acquisition and the potential for dimensional underestimation, particularly in diastole. Consistency in method for assessment of LV dimensions in children is an important factor for serial comparisons. Keywords Two-dimensional echocardiography Left ventricular dimensions Left ventricular function Pediatrics Abbreviations LV Left ventricle 2DE Two-dimensional echocardiography MM M-mode PLA Parasternal long axis PSA Parasternal short axis
Introduction S. Kutty (&) D. Russell L. Li R. Hasan Q. Peng D. A. Danford Division of Pediatric Cardiology, Children’s Hospital and Medical Center, University of Nebraska College of Medicine, 8200 Dodge St, Omaha, NE 68114, USA e-mail:
[email protected] P. C. Frommelt Herma Heart Center, Children’s Hospital of Wisconsin, Medical College of Wisconsin, Milwaukee, WI, USA
Left ventricular (LV) dilation can be a manifestation of volume overload and/or ventricular dysfunction, so precise quantification of LV cavity dimensions assumes great clinical importance. Accordingly, measurements of left ventricular (LV) cavity dimensions have been essential components of echocardiographic examinations from the earliest clinical applications of the technique [1]. In 1989 a committee of the American Society of Echocardiography
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(ASE) put forward recommendations for quantitation of the LV by two-dimensional echocardiography (2DE) [2]. In 2005, the ASE Guidelines and Standards Committee proposed guidelines for adult patient populations in which they described specific techniques to measure cardiac chambers, including the LV [3]. More recently the ASE Pediatric and Congenital Heart Disease Council recommended methods for chamber quantification, and protocols for morphometric evaluation of the heart in children [4]. The pediatric guidelines recommend making LV cavity measurements from the left parasternal short axis (PSA) imaging plane, [4] instead of using the parasternal long axis (PLA) plane, which is the recommendation for adult echocardiography [3]. Data on reproducibility of LV measurements in children by either method are limited, and the magnitudes of differences between the two recommended methods (adult vs. pediatric) have not been analyzed. Our goal was to compare the recommended measurement techniques and to assess the clinical factors associated with differences in measurements. Therefore, we sought to compare LV cavity measurements obtained by two-dimensional (2D) and M-mode (MM) techniques in the left PSA and PLA imaging planes in each subject of our study.
Methods Study participants This was a single center prospective investigation from January 2012 to January 2013. Healthy volunteer children were recruited for research echocardiograms. Inclusion criteria were (1) subject age 1–18 years, (2) no previous history of any heart disease, hypertension or any other systemic disease, and (3) the provision of informed consent. The Institutional Review Board approved the study protocol and parents of all recruited subjects signed informed consent. Demographic data was collected, including gender, date of birth, height, weight, heart rate and systemic blood pressure. Body surface area (BSA) was calculated using the Haycock formula [5]. Echocardiographic evaluation All recruited subjects underwent complete 2DE with spectral and color flow Doppler examination in a nonsedated state utilizing a commercially available ultrasound system (Vivid E9, GE Healthcare, Milwaukee, WI). Images were consistently acquired during quiet respiration. The transducer frequency, 2D sector width and depth, and imaging processor settings were selected according to subjects’ body size with the aim of achieving the highest imaging frame rate while retaining image quality adequate
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for accurate measurement. All data was stored digitally for subsequent analysis with EchoPAC BT11 software. All subjects had structurally and functionally normal hearts, and none had abnormal ventricular septal motion. A single sonographer (LL) with 7 years’ experience acquired all the images and performed the measurements as detailed below. Left ventricular measurement techniques The LV internal diameter (LVD) measurements were made at two points in the cardiac cycle: end-diastole and endsystole. End-diastole was defined as the moment at which the cavity dimension is largest and end-systole as the moment the cavity dimension is smallest [3]. Linear measurements were obtained by two methods for each subject’s PSA and PLA images: (1) direct measurement of the 2D images and (2) MM measurement guided by the 2D image. In the PLA, LV dimension measurements by both MM and 2D were along the LV minor axis, at the tip of the mitral valve anterior leaflet to assure that measurements were made in mid-cavity and perpendicular to the interventricular septum [3]. MM and 2D directed measurements in PSA were made in mid-cavity and perpendicular to the surface of the interventricular septum, while keeping the LV geometry circular throughout the cardiac cycle [4]. This yielded four measurement sets of LVD for each individual subject: (1) PLA direct 2D; (2) PLA 2D-guided MM; (3) PSA direct 2D; and (4) PSA 2D-guided MM (Figs. 1, 2). Frame selection and caliper placement were done in a consistent manner for all studies. At least three consecutive cardiac cycles were measured, and the values were averaged for each of the four techniques. Statistical analysis Continuous variables were expressed as mean ±SD and ranges; discrete variables were expressed as percentages. The 2D and MM methods for PLA and PSA imaging planes were compared using paired t tests. Using linear regression, correlations were explored between the mean differences of enddiastolic LVD, end-systolic LVD and shortening fractions (SFs) with age, BSA, heart rate and systolic blood pressure. To assess the intraobserver and interobserver agreement, measurements were repeated in 20 randomly chosen subjects by the primary observer (LL) and by a second blinded observer (QP). Bland–Altman plots were derived to assess these agreements, identifying possible bias (mean divergence) and the limits of agreement (2 standard deviation of the divergence). In addition, intraclass correlation coefficients were calculated according to standard methodology. Threshold for statistical significance was P \ 0.05. Statistical analysis was performed using commercially available software (Minitab version 16.1, Minitab Inc., State College, PA).
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Fig. 1 Two-dimensional and M-mode measurements of left ventricular internal diameter in end-diastole and end-systole from the parasternal long axis view. LA Left atrium, LV Left ventricle, RV Right ventricle
Results The study cohort consisted of 114 subjects whose demographics are illustrated in Table 1. End-diastolic and endsystolic LV cavity dimensions and shortening fractions for the 4 different methods are shown in Table 2. The smallest estimate of LV end-diastolic dimension (LVED) was obtained by PLA 2D method, with larger estimates by PLA MM, PSA 2D, and PSA MM methods. The largest estimates of LV end-systolic dimension (LVES) were obtained by PLA 2D and PSA 2D methods. Both MM techniques had smaller estimates of LVES dimension. The smallest SF
was by PLA 2D; other methods yielded significantly larger SF. In comparison with the adult convention (PLA 2D), the mean differences in LV cavity measurements by the other 3 methods are shown in Table 3. Relative to PLA 2D, PLA MM consistently resulted in larger LVED, smaller LVES and larger LVSF. Relative to PLA 2D, PSA 2D yielded larger LVED and LVSF, while LVES measurements were similar. PSA MM consistently gave larger LVED, smaller LVES and larger LVSF relative to PLA 2D. Nonetheless, the magnitude of differences among the measurement methods did not vary with subject age, BSA, heart rate or
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Fig. 2 Two-dimensional and M-mode measurements of left ventricular internal diameter in enddiastole and end-systole from the parasternal short axis view. LA Left atrium; LV Left ventricle, RV Right ventricle
systolic blood pressure (Table 4). Intraclass correlation coefficients were high for both intraobserver and interobserver reproducibility comparisons between measurements (Table 5). Bland–Altman analysis showed good agreements for 2D and MM methods as represented in Fig. 3.
Discussion In echocardiography the geometric major axis of the LV cavity is the line that passes from the apex of the ventricle
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through the theoretical center of the cavity and extends through the base, penetrating the mitral valve at a midpoint on the anterior leaflet. The distance from apex to base along this line is the ‘‘length’’ element of the ellipsoid, cylinder, and sum of disks volumetric models. The minor axis is, by definition, a line in the plane orthogonal to the major axis of the cavity at an idealized level that can be taken as the equator of the ellipsoid model or as the diameter of the cylinder, cone, or spheric models. The ‘‘width’’ element of the volumetric model is the anterior– posterior dimension of the LV cavity (LV surface of the
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Table 1 Subject demographics Variable
Mean ± SD
Age (years)
8.9 ± 4.2 2
Body surface area (m )
SE mean
Range
0.41
1–18 0.42–2.6
1.11 ± 0.41
0.04
Systolic blood pressure (mmHg)
105.5 ± 11.1
1.08
79–135
Diastolic blood pressure (mmHg)
60.4 ± 7.7
0.75
38–88
Heart rate (beats/min)
83.0 ± 18.2
1.77
50–128
Table 2 Left ventricular dimensions (mm) and shortening fractions (%) by the different methods Variable
Mean ± SD
SE Mean
Range
ED long axis 2D
38.2 ± 6.3
0.59
24.7–58.7
ED long axis MM
38.9 ± 6.4
0.60
24.5–58.9
ED short axis 2D
39.7 ± 6.4
0.60
25.0–60.2
ED short axis MM
39.8 ± 6.5
0.61
25.3–60.2
ES long axis 2D
25.5 ± 4.9
0.46
16.8–45.6
ES long axis MM
23.9 ± 4.8
0.45
14.2–43.9
ES short axis 2D ES short axis MM
25.6 ± 4.6 24.5 ± 4.8
0.44 0.45
15.4–44.7 41.1–43.3
SF long axis 2D
33.4 ± 5.4
0.51
20.6–48.8
SF long axis MM
38.5 ± 5.1
0.48
25.4–57.7
SF short axis 2D
35.6 ± 4.5
0.43
25.1–44.7
SF short axis MM
38.5 ± 4.7
0.44
28.1–48.4
Table 3 Mean difference in left ventricular cavity measurements relative to the adult ‘standard’ parasternal long axis measurement Variable against PLA 2D
Mean difference
Paired t
P
ED long axis MM
?0.61
?5.53
\0.001
ED short axis 2D
?1.41
?7.64
\0.001
ED short axis MM
?1.51
?7.04
\0.001
ES long axis MM
-1.52
-10.51
\0.001
ES short axis 2D
?0.076
?0.41
0.680
ES short axis MM
-0.986
-4.62
\0.001
SF long axis MM SF short axis 2D
?5.11 ?2.15
?13.86 ?6.00
\0.001 \0.001
SF short axis MM
?5.12
?12.31
\0.001
interventricular septum to posterior wall endocardial surface) measured in mid cavity, usually at the level of the mitral valve anterior leaflet edge in the open position. The ‘‘width’’ measurement is at issue in comparing PLA and PSA imaging planes. Accurate measurement of the width is achieved when the dimension is taken in the true minor axis of the cavity, that is, in a plane that is precisely orthogonal to the major axis. A measuring line that is placed askew of the minor axis plane would produce an inaccurate, exaggerated measurement.
Measuring LV cavity dimensions from the PLA plane is the standard convention in adult echocardiography [3]. The PLA plane ensures (1) a perpendicular orientation between the measurement and the LV long axis, and (2) anatomic landmarks that permit easy and efficient identification of the minor axis of the LV cavity. Pediatric guidelines recommend the PSA imaging plane for LV cavity measurements because: (1) the PLA imaging plane does not account for the lateral motion of the LV that may be seen in children, (2) PLA does not guarantee circular LV shortaxis geometry throughout the cardiac cycle, (3) PLA forces the use of a single diameter, in contrast to the multiple diameters available from short-axis images, and (4) the diameter with the best blood-endocardium interface can be obtained from PSA view [4]. Although these are helpful observations, the anatomic landmarks for identifying the minor axis of the LV cavity may be less reliable from PSA. If the LV cavity is imagined as a cylinder, one can orient the 2D view in the minor axis plane only by satisfying the eye that the cavity boundaries form a perfect circle. Any measurement taken from the short axis view of a noncircular cavity would not be truly in the minor diameter plane and, therefore, has the potential of introducing meaningful measurement error into any volumetric assumptions made from it. In the present study, we assessed the differences between the two recommended measurement methods to evaluate whether LV diastolic and systolic dimensions taken from the PSA plane are comparable to dimensions from the PLA plane. Our main finding was that measurements of LV dimension in pediatric subjects vary depending on the technique used. LV dimension and SF differences between methods were large enough to be clinically relevant, so the method used for measurement does matter. Importantly, given that the magnitude of these differences varied little by age, BSA, heart rate and blood pressure, it is possible that the method-based variation could be true in adult populations too. If it were just a pediatric issue, more pronounced differences would have been expected with younger age, smaller body surface area and lower blood pressure, but this was not the case. Multiple factors are likely accountable for the methodbased variation in echocardiographic LV measurement. Two-dimensional methods provide better spatial orientation, while MM provides better temporal resolution. The limited temporal resolution of 2D may account for the smaller LVED, larger LVES and smaller SF observed with 2D relative to MM. Systolic LV dimension changes rapidly surrounding the time at which the minimum dimension occurs. Interval sampling for LVES with the slow frame rate of 2D imaging will likely miss the precise moment at which the true minimum dimension occurs, resulting in an overestimate of LVES. M-mode has far superior temporal
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Table 4 Correlation of mean differences of end-diastolic and end-systolic dimensions and shortening fractions with age, body surface area, systolic blood pressure and heart rate Variable against PLA 2D
Age
BSA 2
Adjusted r (%)
P
Systolic blood pressure 2
Adjusted r (%)
P
2
Adjusted r (%)
P
Heart rate Adjusted r2 (%)
P
ED long axis MM
0
0.897
0
0.924
0
0.914
0
0.935
ED short axis 2D
0
0.310
0
0.411
0
0.663
0
0.391
ED short axis MM ES long axis MM
0 0.1
0.856 0.286
0 0
0.770 0.528
0 0
0.658 0.579
0 0
0.409 0.989
ES short axis 2D
3.9
0.023
3.7
0.023
0
0.601
0
0.437
ES short axis MM
0
0.322
0.2
0.275
0
0.515
0
0.968
SF long axis MM
0
0.617
0.6
0.199
0
0.806
0.6
0.204
SF short axis 2D
0.9
0.162
0.4
0.237
0
0.904
0.8
0.178
SF short axis MM
0.8
0.183
3.9
0.020
0
0.695
0
0.682
Bold values denote the statistical significance Table 5 Intraobserver and interobserver concordance of measurements
Intra-observer reproducibility
Inter-observer reproducibility
Intraclass correlation
95 % CI
Intraclass correlation
95 % CI
ES long axis 2D
0.998
0.996–0.999
0.980
0.950–0.992
ES long axis MM
0.997
0.994–0.999
0.976
0.942–0.990
ES short axis 2D
0.998
0.997–0.999
0.981
0.954–0.992
ES short axis MM
0.999
0.997–0.999
0.979
0.949–0.991
ED long axis 2D
0.998
0.997–0.999
0.988
0.971–0.995
ED long axis MM
0.999
0.999–0.999
0.999
0.979–0.996
ED short axis 2D
0.999
0.999–0.999
0.989
0.973–0.995
ED short axis MM
0.999
0.998–0.999
0.986
0.966–0.994
resolution and so is not subject to frame rate dependent sampling error. Both short axis methods (2D and MM) consistently yielded larger LVED compared to PLA 2D in our study. We speculate that long axis methodology may predispose to off-center data acquisition and the potential for dimensional underestimation, particularly in diastole. The consequentially larger SF observed in those methods occurred most likely because of larger LVED. Our finding that MM produced larger LVED relative to 2D in PLA imaging plane is in agreement with others [4, 6]. A nonperpendicular orientation of the cursor line relative to the interventricular septum could be responsible for this difference. Moreover, as the MM beam is stationary while the heart is moving, the diastolic measurement is at a slightly different location than the systolic measurement [7]. Acquisition and measurement techniques employed, the individual performing the study and patient population all affect measurement variability in an echocardiographic examination. Respiration related beat-to-beat variations in 2DE measurements of cardiac dimensions and volumes have been shown in children [8] and adults, [9–11] so averaging multiple beats improves reproducibility of 2DE measurements [12]. For 2DE derived LV ejection fraction measurement, reproducibility of ±7 %, [13] and test–retest
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reliability of ±5 % [14] has been reported. For LV diastolic volume, the 95 % confidence limits of measurement are ±11 % [13]. In a longitudinal observational study of children with known or suspected dilated cardiomyopathy, measurements of LV internal chamber dimensions consistently exhibited the best reproducibility of all echocardiographic measures, with low interobserver mean percentage error for LVED in PSA by both 2D and MM techniques (3.8 %) [12]. Others have compared pediatric 2DE measurements made in local laboratories with those made in a central core facility, and the highest reliability was observed for LV dimensions [15]. Our results demonstrate that consistency with measurement protocols within an echocardiography laboratory is very important to reduce variability, and could foster quality improvement. The value of consistency is increasingly recognized in quality improvement initiatives. Measurement technique variability may lead to artifactual increases and decreases in perceived pediatric ventricular size and function measurements unless serial determinations are performed consistently. It has been shown that continuous quality improvement programs are essential for maintaining excellence in the performance and interpretation of 2DE [10, 16–18]. Significant mistakes may occur if
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Fig. 3 Bland-Altman analysis of agreements between two-dimensional and M-mode measurements of left ventricular internal diameter in 20 randomly chosen studies
rigorous quality standards are not employed in the echocardiography laboratory. Technical standardization is beneficial even for experienced sonographers to improve measurement quality within an echocardiography laboratory [19, 20].
therefore not be assessed. The magnitude of inconsistencies between sonographers and any measurement differences related to it were also not evaluated. Finally, it was beyond the scope of this investigation to determine whether the PSA or PLA method has superior accuracy.
Limitations
Conclusions
In the present study, a single sonographer performed all acquisitions on the same echocardiography equipment. The same sonographer performed all measurements following standard guidelines. However, several limitations must be acknowledged. For the measurements performed, enddiastole was defined as the frame in which the LV cavity dimension was greatest and end-systole as the frame in which the dimension was smallest. Because published guidelines do not provide specific definitions for end-systole and end-diastole applicable for both PSA and PLA technique, it is possible that the definitions used in this investigation may be different than those used in some clinical laboratories. The influence of variable standards for timing the cardiac cycle on LV measurement could
Measurements of pediatric LV linear dimensions result in predictable variations in results depending on the technique used. Consistency in the method of assessment is an important factor for serial comparisons of LV dimension in children. Acknowledgments The authors express thanks to Mora Link, RDCS, lead sonographer, Cardiac diagnostics laboratory at the Children’s Hospital and Medical Center. We also would like to thank Carolyn Chamberlain, RN, BSN, MPH and the Pediatric Research Office of the University of Nebraska Medical Center. SK receives support from the American Heart Association, the American College of Cardiology Foundation and the Children’s Hospital and Medical Center Foundation. Conflict of interest
None.
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