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Relationship Between Echocardiographic Measurements and Body Size in Horses
Journal of Equine Veterinary Science 33 (2013) 107-114
Journal of Equine Veterinary Science journal homepage: www.j-evs.com
Original Research
Relationship Between Echocardiographic Measurements and Body Size in Horses Ali Al-Haidar DVM, DEA, PhD a , Aurelia Leroux DVM, DEA, PhD a, Lora Borde DVM, DEA, ECEIM a, Stefan Deleuze DVM, PhD, Dipl. ECARz a, Semona Cerri DVM, DEA, ECEIM a, Charlotte Sandersen DVM, PhD, Dipl. ECEIM a, Hélène Amory DVM, PhD, Dipl. ECEIM a, Fédéric Farnir PhD b a b
Clinical Department of Companion Animals and Equids, Equine Teaching Hospital, University of Liège, Liège, Belgium Department of Animal Production, Biostatistics, Bioinformatics, Economics and Animal Selection, University of Liège, Liège, Belgium
a r t i c l e i n f o
a b s t r a c t
Article history: Received 22 January 2012 Received in revised form 9 May 2012 Accepted 24 May 2012 Available online 3 November 2012
The objectives of this study were to evaluate the optimal body size variable, and to determine mathematical model that best fits echocardiographic measurements to body size in the equine species. One hundred fifty horses of various breeds, aged 1 week to 17 years, body weight (BW) 38-890 kg, and free from cardiac disease were used in this study. Based on their age (ie, younger or older than 2 years), animals were separated into two groups. In each horse, the BW, height at withers (HT), thoracic circumference (TC), and the body length were measured; the body surface area was calculated; and a standard two-dimensional and M-mode echocardiography was performed allowing classic cardiac measurements to be taken. Correlations between each echocardiographic measurement and each of the anthropometric variables were assessed via a Pearson’s product-moment analysis and using linear, logarithmic, and power regression analysis in all animals and within the two groups. The dimensional, but not functional, echocardiographic measurements showed a close correlation with all body size variables, especially during growth. The relationship between cardiac measurements and body size was best described using power regression models with TC as the anthropometric variable, but the relationship was also very accurately described using BW, body surface area, or body length. In the equine species, dimensional echocardiographic reference values should be established using power regression equations on TC. Such a correction for body size could increase the diagnostic value of echocardiography in equine cardiology. Ó 2013 Elsevier Inc. All rights reserved.
Keywords: Cardiology Diagnostic imaging Height Body weight Body surface area
1. Introduction Echocardiography is considered to be one of the most valuable diagnostic tools in the evaluation of cardiac anatomy and function, and in cardiac patients, decisions
Corresponding author at: Ali Al-Haidar, DVM, DEA, PhD, Faculty of Veterinary Medicine, Clinical Department of Companion Animals and Equids, Equine Teaching Hospital, University of Liège, Bat. B41, Sart Tilman, B 4000 Liège, Belgium. E-mail address: [email protected] (A. Al-Haidar). 0737-0806/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jevs.2012.05.063
are constantly made on the basis of quantitative echocardiographic measurements [1,2]. Therefore, the reliability and validity of those measurements are of great importance for differentiating between normal and pathological values. The availability of well-defined species-specific reference values derived from healthy subjects within broad population-based samples is thus recognized to be very useful [2,3]. In humans and various animal species, echocardiographic reference values have been documented, and the effects of several physiological variables, such as body size
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[2-13], ethnicity [14] or breed [1,2,5,12,15], sex [2,3,10-12], aging [1,2], growth [2,4,6,13,16-20], training [21-24], obesity [25], and pregnancy [24], have been demonstrated. The importance of body size as a major factor to be used to fit echocardiographic measurements has been demonstrated, and the need for establishing an appropriate correlation between M-mode measurements and body size in dogs, cats, or horses has been emphasized [8,9,26]. Furthermore, relationships between echocardiographic measurements and body weight (BW) seem to be stronger than those with age [26]. In human medicine, the anthropometric variable that should be used as the scaling factor for echocardiographic measurements is still controversial [2,3,19]. Most authors use BW or body surface area (BSA), whereas others prefer to use height, a factor considered more obesity-independent than BW [3]. The type of mathematical model that should be used to optimally describe the relationship between echocardiographic measurements and body size still needs to be identified. Some authors have indexed echocardiographic measurements to BW, whereas others have developed linear, logarithmic, power, or exponential regression models [18,19]. The same discrepancies concerning body size scaling of cardiac dimensions have been encountered in dogs [2]. In horses, the effects of training [22,23,27] and growth [16,17,26] on echocardiographic measurements have been documented, and the influence of breed has been suggested by several authors [13,15,26]. The relationship between echocardiographic parameters and body size in this species is controversial. Several authors have concluded that the correlation between the dimensional echocardiographic measurements and the BW is not significant [15,28,29]. These results could be due to the low range of body size of the horses included in those studies [8], as other studies, involving horses with a wider range of BW, demonstrated a significant linear correlation between echocardiographic parameters and BW, indicating the need for a correction for body size in this species [8,13,16]. However, all the studies performed in this field used BW as the only measure of body size, and all but one [13] used a linear regression model. Thus, it could be interesting to investigate whether another body size variable or another mathematical model could more accurately describe the relationship between cardiac measurements and body size in horses. The purpose of this study was to evaluate the body size variable and mathematical model that should be used to optimally describe the relationship between dimensional echocardiographic measurements and body size in the equine species.
range ¼ 1.3-10.06 years) were used in this study. Based on their age, animals were separated into two groups: the juvenile group including horses <2 years, and the adult group including horses >2 years. The juvenile group included 50 animals (24 Warmbloods, nine Ponies, three Thoroughbreds, one Standardbred, six Arabians, and seven Draft horses), with BWs ranging from 38 to 518 kg. The adult group included 100 animals (24 Warmbloods, 18 Ponies, 22 Thoroughbreds, 15 Standardbreds, 11 Arabians, and 10 Draft horses), with BWs ranging from 80 to 890 kg. All the studied animals were free of cardiac disease and were hospitalized in the equine teaching hospital of the University of Liège, Liège, Belgium, for a problem without any repercussion on general clinical examination (ie, painless ophthalmic problem, orthopedic problem without signs of pain at stall rest, dermatologic problem, recurrent colics, reproductive follow-up, preoperative examination for minor or elective surgery). These horses were thus all systemically healthy. Moreover, to be included in the study, the horses had to be free from cardiac disease on the basis of clinical, electrocardiographic, and two-dimensional and color flow mapping Doppler echocardiographic examinations. The body condition was evaluated for each horse following a scoring system consisting of six grades (1 ¼ very poor, 2 ¼ poor, 3 ¼ moderate, 4 ¼ good, 5 ¼ fat, and 6 ¼ very fat) [30]. Animals with a poor (score 2) or excessive body condition (score of 6) were not included in the study. BW of each horse was measured using an electronic walk-on scale (D410, Widra, Eupen, Belgium). The height at withers (HT) was measured using a height gauge as the perpendicular distance between the top of the withers and the ground when the animal was in a square position (Fig. 1) [31]. When studied horse was shod, the measured height was reduced by 1 cm to reduce the shoe effect. Using a measuring tape, the body length (BL) was measured as the distance from the point of the shoulder to the point of the buttock (the tuber coxae), and the thoracic circumference (TC) as the circumference of the thorax caudal to the elbow and 2.5 cm caudal to the highest point of the withers [32]. From BW measurements, the BSA was calculated using the following formula [8]: BSA ¼ 0.101.BW2/3.
2. Material and Methods 2.1. Animals One hundred fifty horses (87 mares, 37 stallions, and 26 geldings) of different breeds (48 Warmbloods, 27 Ponies, 25 Thoroughbreds, 16 Standardbreds, 17 Arabians, and 17 Draft horses), weighing between 38 and 890 kg (median ¼ 238 kg, and interquartile range ¼ 245-492 kg), and aged from 1 week to 17 years (median ¼ 4 years, and interquartile
Fig. 1. Graphic illustration of the technique used for measuring body dimensions in horses used in the present study (reprinted from Hill and Klimesh [31], with permission from Cherry Hill). W, highest point of withers; G, ground; B, point of buttock; S, point of shoulder.
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Based on the information obtained in the horse’s file and from the owners, animals were assigned to three different classes of work level. The class “no or light level of work” included sedentary horses or horses lightly exercised at a frequency lower than 2 d/wk. The class “intense level of work” included horses performing competition at high level and trained more than 5 d/wk. The class “moderate level of work” included the remaining horses. One hundred of the studied animals were classified in the light or no level of work class, 29 in the moderate level of work class, and 13 in the intense level of work class (those latter horses were used for show jumping, endurance race, trot, or flat racing). In eight of the studied horses, collected data were not sufficient to determine the level of work class. These eight horses were not used for the level of work analysis. 2.2. Echocardiography Each horse underwent a standardized echocardiographic examination [28,33,34] in a quiet stable. None of the studied horses were sedated during the echocardiographic examination. A portable ultrasound system equipped with color flow mapping and spectral Doppler mode and with a 1.5-3.6 MHz transducer (Vivid I, General Electric Healthcare Europe GMBH, Diegem, Belgium) was used. An electrocardiogram was recorded simultaneously with the echocardiographic images, and the recordings were only made when the heart rate was within the physiological range (24-45 beat/min). All examinations were recorded digitally using a disk drive (Echopac, General Electric, Belgium) and analyzed offline. For recording, each echocardiographic examination was identified as file number rather as name, so it allowed a blinded analysis. Terminology and image orientation were those recommended by the echocardiographic committee of the specialty of cardiology (American College of Veterinary Internal Medicine) [35]. Imaging planes were selected according to identification of intracardiac landmarks as previously reported in horses [28,36-38]. Animals were first imaged from the right hemithorax by placing the ultrasound beam in the fourth or the fifth intercostal space, perpendicularly to the thorax wall, just dorsal to the olecranon. The position of the beam was adjusted to obtain a two-dimensional (2D) mode of the right parasternal long-axis four-chamber reference view. The beam was then rotated clockwise with slightly cranial and dorsal direction to obtain and record a 2D mode of the right parasternal long-axis five-chamber view showing the left ventricle and the left ventricular outflow tract, where the aorta was positioned perpendicular to the axial beam. Restarting from the 2D mode of the right parasternal longaxis four-chamber reference view, the beam was then rotated in a clockwise direction toward the olecranon to produce and record a 2D mode of the short-axis view of the left ventricle at the level of the chordae tendinae where the interventricular septum, the right and left ventricle, and the left ventricular free wall were bisected at right angle and the left ventricle was circular. In this view, the chordae tendinae were clearly visible, and papillary muscles and the mitral valve leaflets were not visible. In this view, M mode was then selected to obtain the M mode of the short-axis view of the left ventricle at level of the chordae tendinae
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by placing the cursor at the angle through the left ventricle, dividing the left ventricle in symmetric halves. Restarting from the 2D mode of the right short-axis view at the chordal level, the beam was then pivoted dorsally in the direction of the heart base and rotated slightly clockwise or anticlockwise until a clear 2D mode of the right parasternal image of the heart base at the level of the pulmonary valve was obtained and recorded. Then the animals were examined from the left hemithorax. The beam was placed in the fourth or fifth intercostal space perpendicular to the hemithorax wall just dorsal to the olecranon and was adapted to produce a 2D mode of the left parasternal long-axis four-chamber view, where the interventricular septum was as horizontal as possible. From this view, the beam was then moved ventrally and caudally to produce and record a 2D mode of the left parasternal long-axis angled view of the left ventricle where the largest diameter of the left atrium was obtained [37,39]. 2.3. Echocardiographic Measurements Each 2D view was recorded as loops of three cardiac cycles view, and three loops were recorded for each of those views. The M-mode short axis view of the left ventricle was recorded as a frame including two to three cardiac cycles. A total of three M-mode frames, obtained after repositioning the transducer in the 2D mode and the M-mode cursor between each recording, was recorded. For each measured parameter, a total of at least three measurements, obtained from three separate loops or frames, were performed. When the successive measurements of the parameter were highly reproducible, the total number of measurements was three, but when there was some variability in obtained measures, two additional measurements were performed. Therefore, all echocardiographic measurements were the mean for three to five cardiac cycles. Cardiac cycle with seconddegree atrioventricular block or any other arrhythmia and following cycle were always avoided. From the M mode of the right parasternal short-axis view of the left ventricle, the interventricular septal thickness, left ventricular free wall thicknesses, and left ventricular internal diameter were measured at end-diastole (d) and at end-systole (s), and the right ventricular internal diameter (RVID) was measured at end-diastole (Fig. 2). The left ventricular fractional shortening (FS) was calculated using the classical formula [2]. The pulmonary and the aortic internal diameters (Pu and Ao, respectively) were measured at the level of the Valsalva sinus from 2D mode of the right parasternal image of the heart base at the level of the pulmonary valve and 2D-mode of the right parasternal longaxis five-chamber view (Figs. 3 and 4, respectively). The left atrial internal diameter (LA) was measured from the 2D left parasternal long-axis angled view of left ventricle (Fig. 5). From those measurements, calculation of the LA/Ao and Pu/ Ao ratios was carried out [2]. 2.4. Statistical Analysis Correlations between each echocardiographic parameter and each of the anthropometric variables (ie, BW, TC, BL, HT, and BSA) were assessed using a Pearson product moment analysis including the effect of training.
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Fig. 2. M-mode right parasternal short-axis view of left ventricular at level of chordate tendinae. RVID, right ventricular internal diameter; IVS, interventricular septum; LVID, left ventricular internal diameter; LVFW, left ventricular free wall thickness; d, end diastole; s, end systole.
The relationship between those parameters was further evaluated by linear, logarithmic, and power regression analysis. The forms of the equations were as follows:
Linear regression : Y ¼ a þ b:X Logarithmic regression : Y ¼ a þ b:LnðXÞ Power regression : Y ¼ a:Xb where Y ¼ echocardiographic parameter, X ¼ anthropometric variable, b ¼ coefficient of regression, and a ¼ constant. These models were applied using StatView 5.0.1. (SAS institute, Inc., Cary, Nc) software to calculate coefficient of determination R2, coefficient of regression (b), and the constant (a) for each model. For all tests, a P value .05 was considered to be significant. This analysis was first performed on all studied animals, and therefore within each of the two age-groups. 3. Results When performed on all of the studied animals or within each age-group, the statistical analysis did not show a significant effect of the level of work on any of the echocardiographic parameters. The LA/Ao and Pu/Ao ratios
Fig. 3. 2-D-mode right parasternal view of heart base at level of the pulmonary valve. Pu, pulmonary internal diameter; AO, aortic artery; RV, right ventricle; RA, right atrium.
Fig. 4. 2D-mode right parasternal long-axis five-chamber view of left ventricular outflow tract. AO, aortic internal diameter; RV, right ventricle; LV, left ventricle; RA, right atrium; LA, left atrium.
and FS were not significantly correlated to any of the body size variables (r value ranging from 0.17 to 0.12). Therefore, regression models were not applied to those parameters. All the echocardiographic measurements showed a significant correlation with each of the tested body size variables. However, the r value obtained for RVIDd, regardless of the tested body size variable, was lower (range: 0.42-0.50) than the value obtained for the other dimensional echocardiographic measurements (range: 0.66-0.92). The same results were obtained when the analysis was performed within each age-group. The r value ranged from 0.61 to 0.68 for RVIDd and from 0.78 to 0.92 for the other echocardiographic measurements in the juvenile group, and from 0.39 to 0.42 for RVIDd and from 0.57 to 0.87 for the other echocardiographic measurements in the adult group. Table 1 shows the coefficients of determination (R2) obtained between the dimensional echocardiographic measurements and each of the body size variables, using linear, logarithmic, or power regression models on all the studied animals. For each of the studied measurements, the R2 obtained using power regression analysis was higher than those obtained using linear or logarithmic regression analysis (Fig. 6). For most of the studied echocardiographic measurements, TC was the body size variable with the highest R2. The R2 values obtained using BW, BSA, or BL were slightly lower but closely comparable with those
Fig. 5. 2D-mode left parasternal long-axis four-chamber angled view of left ventricle. LA, left atrial internal diameter; LV, left ventricle.
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Table 1 Coefficient of determination (R2) of the linear, logarithmic, and power regression between echocardiographic measurements and various body size variables in 150 horses of different breeds, aged from 1 week to 17 years, and weighing 38-890 kg Echocardiographic measurements
BW Linear
Log.
Power
HT Linear
Log.
Power
BL Linear
Log.
Power
Linear
TC Log.
Power
Linear
BSA Log.
Power
RVIDd IVSd LVIDd LVFWd IVSs LVIDs LVFWs Ao Pu LA
0.23 0.65 0.77 0.61 0.67 0.59 0.67 0.79 0.76 0.76
0.23 0.71 0.79 0.64 0.72 0.61 0.70 0.80 0.74 0.81
0.24 0.80 0.85 0.76 0.78 0.68 0.79 0.87 0.85 0.83
0.24 0.65 0.79 0.56 0.66 0.66 0.63 0.80 0.71 0.76
0.23 0.59 0.71 0.49 0.58 0.59 0.57 0.69 0.63 0.70
0.23 0.70 0.81 0.62 0.66 0.71 0.65 0.79 0.76 0.77
0.25 0.73 0.83 0.64 0.75 0.64 0.73 0.84 0.79 0.81
0.25 0.68 0.77 0.60 0.69 0.60 0.67 0.77 0.72 0.76
0.25 0.80 0.85 0.73 0.77 0.69 0.77 0.86 0.84 0.81
0.22 0.73 0.84 0.69 0.76 0.64 0.76 0.85 0.81 0.83
0.21 0.73 0.82 0.68 0.76 0.63 0.75 0.84 0.79 0.83
0.22 0.80 0.87 0.79 0.81 0.68 0.83 0.88 0.87 0.83
0.24 0.70 0.81 0.65 0.72 0.62 0.71 0.83 0.79 0.81
0.23 0.71 0.79 0.64 0.72 0.61 0.70 0.80 0.74 0.81
0.24 0.80 0.85 0.76 0.78 0.68 0.79 0.87 0.85 0.73
BW, body weight; TC, thoracic circumference; HT, height at withers; BL, body length; BSA, body surface area; d and s, measurement at end-diastole and endsystole, respectively; RVID and LVID, right and left ventricular internal diameter, respectively; IVS and LVFW, interventricular septum and left ventricle free wall thickness, respectively; Ao, Pu and LA, aortic, pulmonary, and left atrial internal diameter, respectively; Log., logarithmic.
obtained using TC. The R2 values obtained using HT were lower than those obtained using the other body size variables. The same pattern occurred within each age-group. Table 2 shows the power regression equations between each dimensional echocardiographic measurement and BW, BSA, and TC, and compares those equations with those reported in a previous study in growing Spanish foals using power regression analysis on BW [13]. The power value obtained when BW was used as the anthropometric variable was close to 0.40, and it was close to 0.60 with BSA as the variable. When using TC, HT, or BL as an estimate of body size, the exponent value of the power regression equation was close to 1. 4. Discussion Analysis of the data in this study suggests that, as previously demonstrated in several species, there is a positive and strong correlation between cardiac dimensional measurements and body size in the equine species. On the contrary, no correlation was found between LA/Ao, Pu/Ao, or FS and body size, which is in agreement with most of the previous studies in veterinary and human medicine [1,2,9-11,13,15,17,28]. Many human and veterinary echocardiographic studies have reported to use BSA as scaling variable because of its recognized value and common use in normalizing hemodynamic data [6]. Moreover, the use of BSA in humans is straightforward because most of the ultrasound machines automatically calculate the BSA from the patient’s BW and HT. This is not true in veterinary medicine, which makes the use of BSA far less practical. Nevertheless, most human or canine studies have demonstrated that the regression equations based on BW provide almost identical corrections of echocardiographic measurements than those calculated by BSA [2,40]. The same finding is demonstrated in the present study, suggesting that establishing echocardiographic reference values correlated to BSA is less interesting than using the more user-friendly parameter BW. Height has been used in several human studies to scale echocardiographic variables to body size because it is simple to measure, constant (unlike the disease-related change in BW), and is considered an obesity-independent
variable [3]. It has been shown that the risk of a cardiovascular-adverse event in humans was better detected when using HT rather than BSA to index the measurements to the body size [3]. In contrast, other studies have demonstrated that using HT as the scaling variable for body size was on the contrary less accurate than when using BW or BSA [3,41]. In horses, under field conditions, more and more commonly encountered by equine cardiologists because of the increasing availability of portable ultrasound machines, HT is easier and more accurate to measure than BW. Height could thus be an attractive alternative body size scaling variable in this species. However, the results of the present study tend to show that, as suggested by several authors in human medicine, HT is a scaling parameter with lower accuracy than BW in horses. Perhaps this is because of the breed differences that occur at the same heights as found in the study done by Morrison et al 1992 [5]. An interesting result of this study is the close correlation between equine echocardiographic measurements and TC. Apart from RVIDd, the R2 values obtained using TC were higher than those obtained using BW, even if the differences were slight. The R2 values obtained using BL were closely comparable with those obtained using BW. This is not surprising because of the well-documented close relationship between TC or BL and BW in horses [30,32]. The high R2 obtained between echocardiographic measurements and TC in this study would justify echocardiographic reference values established as a function of this body size variable in horses. Most previous studies reporting the relationship between echocardiographic measurements and the body size in horses have relied on linear regression against BW [8,15,16,26]. In humans and dogs, many authors have also assumed that a linear relationship existed between cardiac dimensions and BW or BSA [1,5,10]. However, this is increasingly demonstrated to be flawed in those species [7], and numerous studies have demonstrated that the relationship between cardiac and body size measurements is more accurately expressed using curvilinear [4,7,8,18,20] or allometric models [3,4,6,9,12,19,20,40]. The results of the present study strongly suggest that the same could be true in horses.
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Fig. 6. Relation between left ventricular internal diameter (LVIDd) and body weight (BW) using linear, logarithmic or power regression. Linear regression between left ventricular internal diameter (LVIDd) and BW. Logarithmic regression between LVIDd and BW. Power regression between LVIDd and BW.
The exponents of the allometric equations between echocardiographic dimensional measurements and BW were, in most cases, approximately 0.33 in dogs [4,8-10,20], and approximately 0.25 in humans [40]. The exponent
values obtained in the present study in horses were slightly higher, with values approximately 0.40 for most of the echocardiographic measurements. This suggests that the allometric shape of the relationship between cardiac and body size could be less marked in horses than in dogs and humans: the proportional increase in cardiac size for each unit of BW increase seems to be higher in the equine species as compared with smaller species. The exponents of the present study were also slightly higher than corresponding exponents reported in Spanish foals [13]. This could be due to the smaller range of the BW and the smaller number of horses included in this study, because it has been shown that sampling errors and sample size are both factors that greatly influence the allometric scaling exponent beta estimation of a relationship between two factors. A representative sample of large size is required to lower statistical inference errors in its calculation [42]. In veterinary medicine, allometric regression of echocardiographic measurements with BSA is reported less frequently than allometric regression with BW. However, in humans, the exponents of those equations were higher than those obtained with BW, with values ranging from 0.35 to 0.50 [40]. As for BW, in the present study, the allometric exponents with BSA in horses were slightly higher than in humans, with values ranging from 0.55 to 0.66. Those results suggest a specific relationship between cardiac and body size in the equine species, and this should be taken into account to establish echocardiographic reference values in this species. No significant effect of the training level on echocardiographic measurements could be shown in the present study. This is not in agreement with previous studies [22,23,27,43]. However, in those studies, the training effect has been studied in longitudinal studies, in Thoroughbred and Standardbred horses, and after an intensive race training of 4.5 and 24 months duration, respectively. The absence of a significant training effect in the present study could be due to the lack of accuracy of the exercise history obtained from the owners, the fact that the training effect was not studied using a longitudinal model, or the unequal distribution of the studied horses into classesdmost of the horses (ie, 100) belonged to the no to light level of work class, and only a few of them belonged to the moderate or high level of work class (ie, 29 and 13, respectively). Although no significant effect of the training could be shown in this study, it cannot be excluded that training had some effect on echocardiographic parameters in some horses included in the study. The main limitations of this study are the limited number of animals investigated and the lack of inclusion of the effects of breed, sex, or growth in the statistical model. However, the objective of the study was not to establish reference values of echocardiographic parameters in horses. Rather, it focused on evaluating the best anthropometric variable and the most appropriate regression analysis that should be used to correct the body size effect on echocardiographic measurements in the equine species. The findings of this study could be used in future studies to evaluate, after inclusion of the body size effect using the most appropriate body size variable and mathematical model, the effect of other physiologic variables, such as sex or breed, on echocardiographic parameters, and to
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Table 2 Allometric equations between echocardiographic measurements and BW, BSA, and TC in 150 horses of different breeds, aged from 1 week to 17 years, and weighing 38-890 kg, and comparison with the allometric equations between echocardiographic measurements and BW reported in 68 growing Spanish foals aged from 22 to 394 days (Rovira et al. 2009)13 Echocardiographic measurements
BW Equations (Present Study)
BSA Equations (Present Study)
TC Equations (Present Study)
IVSd LVIDd LVFWd IVSs LVIDs LVFWs AO Pu LA
0.3 BW 0.36 0.99 BW 0.38 0.24 BW 0.36 0.47 BW 0.36 0.64 BW 0.37 0.39 BW 0.37 0.57 BW 0.42 0.47 BW 0.41 0.89 BW 0.4
1.01 BSA 0.54 3.71 BSA 0.57 0.83 BSA 0.54 1.59 BSA 0.53 2.29 BSA 0.55 1.38 BSA 0.55 2.37 BSA 0.62 1.93 BSA 0.61 3.5 BSA 0.6
0.01 0.04 0.01 0.02 0.03 0.02 0.02 0.01 0.03
TC TC TC TC TC TC TC TC TC
1.01 1.09 1.04 1.02 1.05 1.06 1.19 1.17 1.13
BW Equations (From Rovira et al. 2009)13 0.09 0.41 0.18 0.26 0.42 0.15 0.29 NR NR
BW BW BW BW BW BW BW
0.32 0.32 0.30 0.30 0.21 0.39 0.37
NR, not reported.
determine the normal echocardiographic measurements in healthy horses and ponies. These further studies could define the accurate predictive range of normal values for echocardiographic measurements in equines. Definition of such accurate predictive range of normal echocardiographic measurements is essential to allow differentiating abnormal from normal measurements in a given patient. Aiming at evaluating the relationship between cardiac measurements and body size, in veterinary as well as in human cardiology, several studies have been previously carried out on subjects of mixed age (including or not growing subjects), sex, or breed [5,7-9,15,20], and even on animals of different species [8], without taking into account the effect of those physiological variables on the model. In those studies, inclusion of growing subjects and/or of animals of various breeds or species with a large range of body size allowed to more closely document the relationship between echocardiographic measurements and body size. In humans, it has been shown that the degree of variance of the echocardiographic measurements explained by the subject size is much greater in the child than in the adult, because of the bigger variance in body size during growth [40]. However, the allometric exponents (ie, allometric scaling of a variable (Y) as function of another variable (X) using the power model: Y ¼ aXb) between cardiac dimensions and BW were shown to be similar in growing children and adults [40], which suggests that both growing and adult subjects can be included in studies on the relationship between cardiac measurements and body size. In the present study, the inclusion of growing animals, as well as the wide variation in somatotype of the breeds examined, broadened the range of body sizes investigated, which allowed better documentation of the relationship between cardiac measurements and body size in the equine species. Moreover, the statistical model has been applied not only in the whole group of studied animals (ie, simultaneously on growing and adult horses) but also within each of the two age-groups. In our study, as previously reported in humans [40], echocardiographic measurements showed a higher correlation with body size variables during the growth than in the adulthood. However, results obtained within the adult group suggest that the close and significant correlation between echocardiographic parameters and body size variables also exists after growth.
5. Conclusion This study suggests that in the equine species, dimensional echocardiographic reference values should be established with a correction for body size, especially during growth. The most accurate and straightforward method of performing this body size correction is to establish the allometric regression equations between cardiac dimensional measurements and body size expressed as TC or BW. Such body size correction should allow increasing the diagnostic value of quantitative echocardiography in horses, because of the more accurate definition of the normal values of echocardiographic measurements in this species. Acknowledgments This work was carried out at the Equine Teaching Hospital, Faculty of Veterinary Medicine, University of Liège, Belgium, and has partly been supported by the “Fonds Spéciaux pour la recherche” from the University of Liège. Also, the authors thank the owners of the horses for allowing their animals to be included in the study. References [1] Vörös K, Hetyey C, Reiczigel J, Czirok GN. M-mode and twodimensional echocardiographic reference values for three Hungarian dog breeds: Hungarian Vizsla, Mudi and Hungarian Greyhound. Acta veterinaria Hungarica 2009;57:217-27. [2] Boon JA. Evaluation of size, function, and hemodynamics. In: Boon JA, editor. Veterinary echocardiography. 2nd ed. Ames, IA: Wiley-Blackwell; 2011. p. 153-256. [3] Lauer MS, Larson MG, Levy D. Gender-specific reference M-mode values in adults: population-derived values with consideration of the impact of height. J Am Coll Cardiol 1995;26:1039-46. [4] Sisson D, Schaeffer D. Changes in linear dimensions of the heart, relative to body weight, as measured by M-mode echocardiography in growing dogs. Am J Vet Res 1991;52:1591-6. [5] Morrison SA, Moise NS, Scarlett J, Mohammed H, Yeager AE. Effect of breed and body weight on echocardiographic values in four breeds of dogs of differing somatotype. J Vet Intern Med 1992;6: 220-4. [6] Kampmann C, Wiethoff C, Wenzel A, Stolz G, Betancor M, Wippermann C-F, et al. Normal values of M mode echocardiographic measurements of more than 2000 healthy infants and children in central Europe. Heart 2000;83:667-72. [7] Gonçalves AC, Orton EC, Boon JA, Salman MD. Linear, logarithmic, and polynomial models of M-mode echocardiographic measurements in dogs. Am J Vet Res 2002;63:994-9.
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[8] Brown DJ, Rush JE, MacGregor J, Ross JNJ, Brewer B, Rand WM. M-mode echocardiographic ratio indices in normal dogs, cats, and horses: a novel quantitative method. J Vet Intern Med 2003;17:653-62. [9] Cornell CC, Kittleson MD, Della Torre P, Häggström J, Lombard CW, Pedersen HD, et al. Allometric scaling of M-mode cardiac measurements in normal adult dogs. J Vet Intern Med 2004;18:311-21. [10] Kayar A, Gonul R, Or ME, Uysal A. M-mode echocardiographic parameters and indices in the normal German shepherd dog. Vet Radiol Ultrasound 2006;47:482-6. [11] Anderson B. M-mode echocardiography measuremants and calculations. In: Anderson B, editor. Echocardiography: the normal examination and echocardiographic measurements. 2nd ed. Manly, Australia: MGA Graphics; 2007. p. 167-82. [12] Bavegems V, Duchateau L, Sys SU, Rick AD. Echocardiographic reference values in whippets. Vet Radiol Ultrasound 2007;48: 230-8. [13] Rovira S, Muñoz A, Rodilla V. Allometric scaling of echocardiographic measurements in healthy Spanish foals with different body weight. Res Vet Sci 2009;86:325-31. [14] Chaturvedi N, Athanassopoulos G, McKeigue PM, Marmot MG, Nihoyannopoulos P. Echocardiographic measures of left ventricular structure and their relation with rest and ambulatory blood pressure in blacks and whites in the United Kingdom. J Am Coll Cardiol 1994;24:1499-505. [15] Slater JD, Herrtage ME. Echocardiographic measurements of cardiac dimensions in normal ponies and horses. Equine Vet J Suppl 1995;27:28-32. [16] Lombard CW, Evans M, Martin L, Tehrani J. Blood pressure, electrocardiogram and echocardiogram measurements in the growing pony foal. Equine Vet J 1984;16:342-7. [17] Stewart JH, Rose RJ, Barko AM. Echocardiography in foals from birth to three months old. Equine Vet J 1984;16:332-41. [18] Ichida F, Denef B, Dumoulin M, Van der Hauwaert LG. Cardiac chamber growth pattern determined by two-dimensional echocardiography. Heart Vessels 1988;4:26-33. [19] Gutgesell HP, Rembold CM. Growth of the human heart relative to body surface area. Am J Cardiol 1990;65:662-8. [20] Bayón A, Fernández del Palacio MJ, Montes AM, Gutiérrez Panizo C. M-mode echocardiography study in growing Spanish mastiffs. J Small Anim Pract 1994;35:473-9. [21] Lonsdale RA, Labuc RH, Robertson ID. Echocardiographic parameters in training compared with non-training greyhounds. Vet Radiol Ultrasound 1998;39:325-30. [22] Young LE. Cardiac responses to training in 2-year-old thoroughbreds: an echocardiographic study. Equine Vet J Suppl 1999;30:195-8. [23] Buhl R, Ersbøll AK, Eriksen L, Koch J. Changes over time in echocardiographic measurements in young Standardbred racehorses undergoing training and racing and association with racing performance. J Am Vet Med Assoc 2005;226:1881-7. [24] Armstrong WF, Ryan T. Echocardiography in sytemic disease and clinical problem solving. In: Armstrong WF, Ryan T, editors. Feigenbaum’s echocardiography. 7th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2010. p. 741-75. [25] Bazzano LA, Belame SN, Patel DA, Chen W, Srinivasan S, McIlwain E, et al. Obesity and left ventricular dilatation in young adulthood: the Bogalusa HEART Study. Clin Cardiol 2011;34:153-9.
[26] Collins NM, Palmer L, Marr CM. Two-dimensional and M-mode echocardiographic findings in healthy Thoroughbred foals. Aust Vet J 2010;88:428-33. [27] Buhl R, Ersbøll AK. Echocardiographic evaluation of changes in left ventricular size and valvular regurgitation associated with physical training during and after maturity in Standardbred trotters. J Am Vet Med Assoc 2012;240:205-12. [28] Long KJ, Bonagura JD, Darke PG. Standardised imaging technique for guided M-mode and Doppler echocardiography in the horse. Equine Vet J 1992;24:226-35. [29] Bakos Z, Vörös K, Jarvinen T, Reiczigel J. Two-dimensional and M-mode echocardiographic measurements of cardiac dimensions in healthy standardbred trotters. Acta Veterinaria Hungarica 2002;50: 273-82. [30] Carroll CL, Huntington PJ. Body condition scoring and weight estimation of horses. Equine Vet J 1988;20:41-5. [31] Hill C, Klimesh R. Maximum hoof power: How to improve your horse’s performance through proper hoof management. Vermont: Trafalgar Square Publishing; 2000. [32] Staniar WB, Kronfeld DS, Hoffman RM, Wilson JA, Harris PA. Weight prediction from linear measures of growing Thoroughbreds. Equine Vet J 2004;36:149-54. [33] Boon JA. The two-dimensional echocardiographic exam. In: Boon JA, editor. Veterinary echocardiography. 2nd ed. Ames, IA: WileyBlackwell; 2011. p. 37-98. [34] Boon JA. The M-mode and Doppler examination. In: Boon JA, editor. Veterinary echocardiography. 2nd ed. Ames, IA: Wiley-Blakwell; 2011. p. 101-49. [35] Thomas WP, Gaber CE, Jacobs GJ, Kaplan PM, Lombard CW, Moise NS, et al. Recommendations for standards in transthoracic two-dimensional echocardiography in the dog and cat. Echocardiography Committee of the Specialty of Cardiology, American College of Veterinary Internal Medicine. J Vet Intern Med 1993;7:247-52. [36] Reef VB. Echocardiograpic examination in the horse: the basics. Comp Cont Educ Pract 1990;12:1312-9. [37] Patteson MW, Gibbs C, Wotton PR, Cripps PJ. Echocardiographic measurements of cardiac dimensions and indices of cardiac function in normal adult thoroughbred horses. Equine Vet J Suppl 1995;19:18-27. [38] Kriz NG, Rose RJ. Repeatability of standard transthoracic echocardiographic measurements in horses. Aust Vet J 2002;80:362-70. [39] Amory H, Bertrand P, Delvaux V, Sandersen C. Doppler echocardiographic reference values in healthy donkeys. Available at: http:// www.ivis.org. [40] Neilan TG, Pradhan AD, King ME, Weyman AE. Derivation of a sizeindependent variable for scaling of cardiac dimensions in a normal paediatric population. Euro Heart J 2009;10:50-5. [41] Kitzman DW, Scholz DG, Hagen PT, Ilstrup DM, Edwards WD. Agerelated changes in normal human hearts during the first 10 decades of life. Part II (Maturity): a quantitative anatomic study of 765 specimens from subjects 20 to 99 years old. Mayo Clinic Proceed Mayo Clinic 1988;63:137-46. [42] Hui D, Jackson RB. Uncertainty in allometric exponent estimation: A case study in scaling metabolic rate with body mass. J Theor Biol 2007;249:168-77. [43] Buhl R, Ersbøll AK, Eriksen L, Koch J. Sources and magnitude of variation of echocardiographic measurements in normal standardbred horses. Vet Radiol Ultrasound 2004;45:505-12.
Journal of Equine Veterinary Science journal homepage: www.j-evs.com
Original Research
Relationship Between Echocardiographic Measurements and Body Size in Horses Ali Al-Haidar DVM, DEA, PhD a , Aurelia Leroux DVM, DEA, PhD a, Lora Borde DVM, DEA, ECEIM a, Stefan Deleuze DVM, PhD, Dipl. ECARz a, Semona Cerri DVM, DEA, ECEIM a, Charlotte Sandersen DVM, PhD, Dipl. ECEIM a, Hélène Amory DVM, PhD, Dipl. ECEIM a, Fédéric Farnir PhD b a b
Clinical Department of Companion Animals and Equids, Equine Teaching Hospital, University of Liège, Liège, Belgium Department of Animal Production, Biostatistics, Bioinformatics, Economics and Animal Selection, University of Liège, Liège, Belgium
a r t i c l e i n f o
a b s t r a c t
Article history: Received 22 January 2012 Received in revised form 9 May 2012 Accepted 24 May 2012 Available online 3 November 2012
The objectives of this study were to evaluate the optimal body size variable, and to determine mathematical model that best fits echocardiographic measurements to body size in the equine species. One hundred fifty horses of various breeds, aged 1 week to 17 years, body weight (BW) 38-890 kg, and free from cardiac disease were used in this study. Based on their age (ie, younger or older than 2 years), animals were separated into two groups. In each horse, the BW, height at withers (HT), thoracic circumference (TC), and the body length were measured; the body surface area was calculated; and a standard two-dimensional and M-mode echocardiography was performed allowing classic cardiac measurements to be taken. Correlations between each echocardiographic measurement and each of the anthropometric variables were assessed via a Pearson’s product-moment analysis and using linear, logarithmic, and power regression analysis in all animals and within the two groups. The dimensional, but not functional, echocardiographic measurements showed a close correlation with all body size variables, especially during growth. The relationship between cardiac measurements and body size was best described using power regression models with TC as the anthropometric variable, but the relationship was also very accurately described using BW, body surface area, or body length. In the equine species, dimensional echocardiographic reference values should be established using power regression equations on TC. Such a correction for body size could increase the diagnostic value of echocardiography in equine cardiology. Ó 2013 Elsevier Inc. All rights reserved.
Keywords: Cardiology Diagnostic imaging Height Body weight Body surface area
1. Introduction Echocardiography is considered to be one of the most valuable diagnostic tools in the evaluation of cardiac anatomy and function, and in cardiac patients, decisions
Corresponding author at: Ali Al-Haidar, DVM, DEA, PhD, Faculty of Veterinary Medicine, Clinical Department of Companion Animals and Equids, Equine Teaching Hospital, University of Liège, Bat. B41, Sart Tilman, B 4000 Liège, Belgium. E-mail address: [email protected] (A. Al-Haidar). 0737-0806/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jevs.2012.05.063
are constantly made on the basis of quantitative echocardiographic measurements [1,2]. Therefore, the reliability and validity of those measurements are of great importance for differentiating between normal and pathological values. The availability of well-defined species-specific reference values derived from healthy subjects within broad population-based samples is thus recognized to be very useful [2,3]. In humans and various animal species, echocardiographic reference values have been documented, and the effects of several physiological variables, such as body size
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[2-13], ethnicity [14] or breed [1,2,5,12,15], sex [2,3,10-12], aging [1,2], growth [2,4,6,13,16-20], training [21-24], obesity [25], and pregnancy [24], have been demonstrated. The importance of body size as a major factor to be used to fit echocardiographic measurements has been demonstrated, and the need for establishing an appropriate correlation between M-mode measurements and body size in dogs, cats, or horses has been emphasized [8,9,26]. Furthermore, relationships between echocardiographic measurements and body weight (BW) seem to be stronger than those with age [26]. In human medicine, the anthropometric variable that should be used as the scaling factor for echocardiographic measurements is still controversial [2,3,19]. Most authors use BW or body surface area (BSA), whereas others prefer to use height, a factor considered more obesity-independent than BW [3]. The type of mathematical model that should be used to optimally describe the relationship between echocardiographic measurements and body size still needs to be identified. Some authors have indexed echocardiographic measurements to BW, whereas others have developed linear, logarithmic, power, or exponential regression models [18,19]. The same discrepancies concerning body size scaling of cardiac dimensions have been encountered in dogs [2]. In horses, the effects of training [22,23,27] and growth [16,17,26] on echocardiographic measurements have been documented, and the influence of breed has been suggested by several authors [13,15,26]. The relationship between echocardiographic parameters and body size in this species is controversial. Several authors have concluded that the correlation between the dimensional echocardiographic measurements and the BW is not significant [15,28,29]. These results could be due to the low range of body size of the horses included in those studies [8], as other studies, involving horses with a wider range of BW, demonstrated a significant linear correlation between echocardiographic parameters and BW, indicating the need for a correction for body size in this species [8,13,16]. However, all the studies performed in this field used BW as the only measure of body size, and all but one [13] used a linear regression model. Thus, it could be interesting to investigate whether another body size variable or another mathematical model could more accurately describe the relationship between cardiac measurements and body size in horses. The purpose of this study was to evaluate the body size variable and mathematical model that should be used to optimally describe the relationship between dimensional echocardiographic measurements and body size in the equine species.
range ¼ 1.3-10.06 years) were used in this study. Based on their age, animals were separated into two groups: the juvenile group including horses <2 years, and the adult group including horses >2 years. The juvenile group included 50 animals (24 Warmbloods, nine Ponies, three Thoroughbreds, one Standardbred, six Arabians, and seven Draft horses), with BWs ranging from 38 to 518 kg. The adult group included 100 animals (24 Warmbloods, 18 Ponies, 22 Thoroughbreds, 15 Standardbreds, 11 Arabians, and 10 Draft horses), with BWs ranging from 80 to 890 kg. All the studied animals were free of cardiac disease and were hospitalized in the equine teaching hospital of the University of Liège, Liège, Belgium, for a problem without any repercussion on general clinical examination (ie, painless ophthalmic problem, orthopedic problem without signs of pain at stall rest, dermatologic problem, recurrent colics, reproductive follow-up, preoperative examination for minor or elective surgery). These horses were thus all systemically healthy. Moreover, to be included in the study, the horses had to be free from cardiac disease on the basis of clinical, electrocardiographic, and two-dimensional and color flow mapping Doppler echocardiographic examinations. The body condition was evaluated for each horse following a scoring system consisting of six grades (1 ¼ very poor, 2 ¼ poor, 3 ¼ moderate, 4 ¼ good, 5 ¼ fat, and 6 ¼ very fat) [30]. Animals with a poor (score 2) or excessive body condition (score of 6) were not included in the study. BW of each horse was measured using an electronic walk-on scale (D410, Widra, Eupen, Belgium). The height at withers (HT) was measured using a height gauge as the perpendicular distance between the top of the withers and the ground when the animal was in a square position (Fig. 1) [31]. When studied horse was shod, the measured height was reduced by 1 cm to reduce the shoe effect. Using a measuring tape, the body length (BL) was measured as the distance from the point of the shoulder to the point of the buttock (the tuber coxae), and the thoracic circumference (TC) as the circumference of the thorax caudal to the elbow and 2.5 cm caudal to the highest point of the withers [32]. From BW measurements, the BSA was calculated using the following formula [8]: BSA ¼ 0.101.BW2/3.
2. Material and Methods 2.1. Animals One hundred fifty horses (87 mares, 37 stallions, and 26 geldings) of different breeds (48 Warmbloods, 27 Ponies, 25 Thoroughbreds, 16 Standardbreds, 17 Arabians, and 17 Draft horses), weighing between 38 and 890 kg (median ¼ 238 kg, and interquartile range ¼ 245-492 kg), and aged from 1 week to 17 years (median ¼ 4 years, and interquartile
Fig. 1. Graphic illustration of the technique used for measuring body dimensions in horses used in the present study (reprinted from Hill and Klimesh [31], with permission from Cherry Hill). W, highest point of withers; G, ground; B, point of buttock; S, point of shoulder.
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Based on the information obtained in the horse’s file and from the owners, animals were assigned to three different classes of work level. The class “no or light level of work” included sedentary horses or horses lightly exercised at a frequency lower than 2 d/wk. The class “intense level of work” included horses performing competition at high level and trained more than 5 d/wk. The class “moderate level of work” included the remaining horses. One hundred of the studied animals were classified in the light or no level of work class, 29 in the moderate level of work class, and 13 in the intense level of work class (those latter horses were used for show jumping, endurance race, trot, or flat racing). In eight of the studied horses, collected data were not sufficient to determine the level of work class. These eight horses were not used for the level of work analysis. 2.2. Echocardiography Each horse underwent a standardized echocardiographic examination [28,33,34] in a quiet stable. None of the studied horses were sedated during the echocardiographic examination. A portable ultrasound system equipped with color flow mapping and spectral Doppler mode and with a 1.5-3.6 MHz transducer (Vivid I, General Electric Healthcare Europe GMBH, Diegem, Belgium) was used. An electrocardiogram was recorded simultaneously with the echocardiographic images, and the recordings were only made when the heart rate was within the physiological range (24-45 beat/min). All examinations were recorded digitally using a disk drive (Echopac, General Electric, Belgium) and analyzed offline. For recording, each echocardiographic examination was identified as file number rather as name, so it allowed a blinded analysis. Terminology and image orientation were those recommended by the echocardiographic committee of the specialty of cardiology (American College of Veterinary Internal Medicine) [35]. Imaging planes were selected according to identification of intracardiac landmarks as previously reported in horses [28,36-38]. Animals were first imaged from the right hemithorax by placing the ultrasound beam in the fourth or the fifth intercostal space, perpendicularly to the thorax wall, just dorsal to the olecranon. The position of the beam was adjusted to obtain a two-dimensional (2D) mode of the right parasternal long-axis four-chamber reference view. The beam was then rotated clockwise with slightly cranial and dorsal direction to obtain and record a 2D mode of the right parasternal long-axis five-chamber view showing the left ventricle and the left ventricular outflow tract, where the aorta was positioned perpendicular to the axial beam. Restarting from the 2D mode of the right parasternal longaxis four-chamber reference view, the beam was then rotated in a clockwise direction toward the olecranon to produce and record a 2D mode of the short-axis view of the left ventricle at the level of the chordae tendinae where the interventricular septum, the right and left ventricle, and the left ventricular free wall were bisected at right angle and the left ventricle was circular. In this view, the chordae tendinae were clearly visible, and papillary muscles and the mitral valve leaflets were not visible. In this view, M mode was then selected to obtain the M mode of the short-axis view of the left ventricle at level of the chordae tendinae
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by placing the cursor at the angle through the left ventricle, dividing the left ventricle in symmetric halves. Restarting from the 2D mode of the right short-axis view at the chordal level, the beam was then pivoted dorsally in the direction of the heart base and rotated slightly clockwise or anticlockwise until a clear 2D mode of the right parasternal image of the heart base at the level of the pulmonary valve was obtained and recorded. Then the animals were examined from the left hemithorax. The beam was placed in the fourth or fifth intercostal space perpendicular to the hemithorax wall just dorsal to the olecranon and was adapted to produce a 2D mode of the left parasternal long-axis four-chamber view, where the interventricular septum was as horizontal as possible. From this view, the beam was then moved ventrally and caudally to produce and record a 2D mode of the left parasternal long-axis angled view of the left ventricle where the largest diameter of the left atrium was obtained [37,39]. 2.3. Echocardiographic Measurements Each 2D view was recorded as loops of three cardiac cycles view, and three loops were recorded for each of those views. The M-mode short axis view of the left ventricle was recorded as a frame including two to three cardiac cycles. A total of three M-mode frames, obtained after repositioning the transducer in the 2D mode and the M-mode cursor between each recording, was recorded. For each measured parameter, a total of at least three measurements, obtained from three separate loops or frames, were performed. When the successive measurements of the parameter were highly reproducible, the total number of measurements was three, but when there was some variability in obtained measures, two additional measurements were performed. Therefore, all echocardiographic measurements were the mean for three to five cardiac cycles. Cardiac cycle with seconddegree atrioventricular block or any other arrhythmia and following cycle were always avoided. From the M mode of the right parasternal short-axis view of the left ventricle, the interventricular septal thickness, left ventricular free wall thicknesses, and left ventricular internal diameter were measured at end-diastole (d) and at end-systole (s), and the right ventricular internal diameter (RVID) was measured at end-diastole (Fig. 2). The left ventricular fractional shortening (FS) was calculated using the classical formula [2]. The pulmonary and the aortic internal diameters (Pu and Ao, respectively) were measured at the level of the Valsalva sinus from 2D mode of the right parasternal image of the heart base at the level of the pulmonary valve and 2D-mode of the right parasternal longaxis five-chamber view (Figs. 3 and 4, respectively). The left atrial internal diameter (LA) was measured from the 2D left parasternal long-axis angled view of left ventricle (Fig. 5). From those measurements, calculation of the LA/Ao and Pu/ Ao ratios was carried out [2]. 2.4. Statistical Analysis Correlations between each echocardiographic parameter and each of the anthropometric variables (ie, BW, TC, BL, HT, and BSA) were assessed using a Pearson product moment analysis including the effect of training.
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Fig. 2. M-mode right parasternal short-axis view of left ventricular at level of chordate tendinae. RVID, right ventricular internal diameter; IVS, interventricular septum; LVID, left ventricular internal diameter; LVFW, left ventricular free wall thickness; d, end diastole; s, end systole.
The relationship between those parameters was further evaluated by linear, logarithmic, and power regression analysis. The forms of the equations were as follows:
Linear regression : Y ¼ a þ b:X Logarithmic regression : Y ¼ a þ b:LnðXÞ Power regression : Y ¼ a:Xb where Y ¼ echocardiographic parameter, X ¼ anthropometric variable, b ¼ coefficient of regression, and a ¼ constant. These models were applied using StatView 5.0.1. (SAS institute, Inc., Cary, Nc) software to calculate coefficient of determination R2, coefficient of regression (b), and the constant (a) for each model. For all tests, a P value .05 was considered to be significant. This analysis was first performed on all studied animals, and therefore within each of the two age-groups. 3. Results When performed on all of the studied animals or within each age-group, the statistical analysis did not show a significant effect of the level of work on any of the echocardiographic parameters. The LA/Ao and Pu/Ao ratios
Fig. 3. 2-D-mode right parasternal view of heart base at level of the pulmonary valve. Pu, pulmonary internal diameter; AO, aortic artery; RV, right ventricle; RA, right atrium.
Fig. 4. 2D-mode right parasternal long-axis five-chamber view of left ventricular outflow tract. AO, aortic internal diameter; RV, right ventricle; LV, left ventricle; RA, right atrium; LA, left atrium.
and FS were not significantly correlated to any of the body size variables (r value ranging from 0.17 to 0.12). Therefore, regression models were not applied to those parameters. All the echocardiographic measurements showed a significant correlation with each of the tested body size variables. However, the r value obtained for RVIDd, regardless of the tested body size variable, was lower (range: 0.42-0.50) than the value obtained for the other dimensional echocardiographic measurements (range: 0.66-0.92). The same results were obtained when the analysis was performed within each age-group. The r value ranged from 0.61 to 0.68 for RVIDd and from 0.78 to 0.92 for the other echocardiographic measurements in the juvenile group, and from 0.39 to 0.42 for RVIDd and from 0.57 to 0.87 for the other echocardiographic measurements in the adult group. Table 1 shows the coefficients of determination (R2) obtained between the dimensional echocardiographic measurements and each of the body size variables, using linear, logarithmic, or power regression models on all the studied animals. For each of the studied measurements, the R2 obtained using power regression analysis was higher than those obtained using linear or logarithmic regression analysis (Fig. 6). For most of the studied echocardiographic measurements, TC was the body size variable with the highest R2. The R2 values obtained using BW, BSA, or BL were slightly lower but closely comparable with those
Fig. 5. 2D-mode left parasternal long-axis four-chamber angled view of left ventricle. LA, left atrial internal diameter; LV, left ventricle.
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Table 1 Coefficient of determination (R2) of the linear, logarithmic, and power regression between echocardiographic measurements and various body size variables in 150 horses of different breeds, aged from 1 week to 17 years, and weighing 38-890 kg Echocardiographic measurements
BW Linear
Log.
Power
HT Linear
Log.
Power
BL Linear
Log.
Power
Linear
TC Log.
Power
Linear
BSA Log.
Power
RVIDd IVSd LVIDd LVFWd IVSs LVIDs LVFWs Ao Pu LA
0.23 0.65 0.77 0.61 0.67 0.59 0.67 0.79 0.76 0.76
0.23 0.71 0.79 0.64 0.72 0.61 0.70 0.80 0.74 0.81
0.24 0.80 0.85 0.76 0.78 0.68 0.79 0.87 0.85 0.83
0.24 0.65 0.79 0.56 0.66 0.66 0.63 0.80 0.71 0.76
0.23 0.59 0.71 0.49 0.58 0.59 0.57 0.69 0.63 0.70
0.23 0.70 0.81 0.62 0.66 0.71 0.65 0.79 0.76 0.77
0.25 0.73 0.83 0.64 0.75 0.64 0.73 0.84 0.79 0.81
0.25 0.68 0.77 0.60 0.69 0.60 0.67 0.77 0.72 0.76
0.25 0.80 0.85 0.73 0.77 0.69 0.77 0.86 0.84 0.81
0.22 0.73 0.84 0.69 0.76 0.64 0.76 0.85 0.81 0.83
0.21 0.73 0.82 0.68 0.76 0.63 0.75 0.84 0.79 0.83
0.22 0.80 0.87 0.79 0.81 0.68 0.83 0.88 0.87 0.83
0.24 0.70 0.81 0.65 0.72 0.62 0.71 0.83 0.79 0.81
0.23 0.71 0.79 0.64 0.72 0.61 0.70 0.80 0.74 0.81
0.24 0.80 0.85 0.76 0.78 0.68 0.79 0.87 0.85 0.73
BW, body weight; TC, thoracic circumference; HT, height at withers; BL, body length; BSA, body surface area; d and s, measurement at end-diastole and endsystole, respectively; RVID and LVID, right and left ventricular internal diameter, respectively; IVS and LVFW, interventricular septum and left ventricle free wall thickness, respectively; Ao, Pu and LA, aortic, pulmonary, and left atrial internal diameter, respectively; Log., logarithmic.
obtained using TC. The R2 values obtained using HT were lower than those obtained using the other body size variables. The same pattern occurred within each age-group. Table 2 shows the power regression equations between each dimensional echocardiographic measurement and BW, BSA, and TC, and compares those equations with those reported in a previous study in growing Spanish foals using power regression analysis on BW [13]. The power value obtained when BW was used as the anthropometric variable was close to 0.40, and it was close to 0.60 with BSA as the variable. When using TC, HT, or BL as an estimate of body size, the exponent value of the power regression equation was close to 1. 4. Discussion Analysis of the data in this study suggests that, as previously demonstrated in several species, there is a positive and strong correlation between cardiac dimensional measurements and body size in the equine species. On the contrary, no correlation was found between LA/Ao, Pu/Ao, or FS and body size, which is in agreement with most of the previous studies in veterinary and human medicine [1,2,9-11,13,15,17,28]. Many human and veterinary echocardiographic studies have reported to use BSA as scaling variable because of its recognized value and common use in normalizing hemodynamic data [6]. Moreover, the use of BSA in humans is straightforward because most of the ultrasound machines automatically calculate the BSA from the patient’s BW and HT. This is not true in veterinary medicine, which makes the use of BSA far less practical. Nevertheless, most human or canine studies have demonstrated that the regression equations based on BW provide almost identical corrections of echocardiographic measurements than those calculated by BSA [2,40]. The same finding is demonstrated in the present study, suggesting that establishing echocardiographic reference values correlated to BSA is less interesting than using the more user-friendly parameter BW. Height has been used in several human studies to scale echocardiographic variables to body size because it is simple to measure, constant (unlike the disease-related change in BW), and is considered an obesity-independent
variable [3]. It has been shown that the risk of a cardiovascular-adverse event in humans was better detected when using HT rather than BSA to index the measurements to the body size [3]. In contrast, other studies have demonstrated that using HT as the scaling variable for body size was on the contrary less accurate than when using BW or BSA [3,41]. In horses, under field conditions, more and more commonly encountered by equine cardiologists because of the increasing availability of portable ultrasound machines, HT is easier and more accurate to measure than BW. Height could thus be an attractive alternative body size scaling variable in this species. However, the results of the present study tend to show that, as suggested by several authors in human medicine, HT is a scaling parameter with lower accuracy than BW in horses. Perhaps this is because of the breed differences that occur at the same heights as found in the study done by Morrison et al 1992 [5]. An interesting result of this study is the close correlation between equine echocardiographic measurements and TC. Apart from RVIDd, the R2 values obtained using TC were higher than those obtained using BW, even if the differences were slight. The R2 values obtained using BL were closely comparable with those obtained using BW. This is not surprising because of the well-documented close relationship between TC or BL and BW in horses [30,32]. The high R2 obtained between echocardiographic measurements and TC in this study would justify echocardiographic reference values established as a function of this body size variable in horses. Most previous studies reporting the relationship between echocardiographic measurements and the body size in horses have relied on linear regression against BW [8,15,16,26]. In humans and dogs, many authors have also assumed that a linear relationship existed between cardiac dimensions and BW or BSA [1,5,10]. However, this is increasingly demonstrated to be flawed in those species [7], and numerous studies have demonstrated that the relationship between cardiac and body size measurements is more accurately expressed using curvilinear [4,7,8,18,20] or allometric models [3,4,6,9,12,19,20,40]. The results of the present study strongly suggest that the same could be true in horses.
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Fig. 6. Relation between left ventricular internal diameter (LVIDd) and body weight (BW) using linear, logarithmic or power regression. Linear regression between left ventricular internal diameter (LVIDd) and BW. Logarithmic regression between LVIDd and BW. Power regression between LVIDd and BW.
The exponents of the allometric equations between echocardiographic dimensional measurements and BW were, in most cases, approximately 0.33 in dogs [4,8-10,20], and approximately 0.25 in humans [40]. The exponent
values obtained in the present study in horses were slightly higher, with values approximately 0.40 for most of the echocardiographic measurements. This suggests that the allometric shape of the relationship between cardiac and body size could be less marked in horses than in dogs and humans: the proportional increase in cardiac size for each unit of BW increase seems to be higher in the equine species as compared with smaller species. The exponents of the present study were also slightly higher than corresponding exponents reported in Spanish foals [13]. This could be due to the smaller range of the BW and the smaller number of horses included in this study, because it has been shown that sampling errors and sample size are both factors that greatly influence the allometric scaling exponent beta estimation of a relationship between two factors. A representative sample of large size is required to lower statistical inference errors in its calculation [42]. In veterinary medicine, allometric regression of echocardiographic measurements with BSA is reported less frequently than allometric regression with BW. However, in humans, the exponents of those equations were higher than those obtained with BW, with values ranging from 0.35 to 0.50 [40]. As for BW, in the present study, the allometric exponents with BSA in horses were slightly higher than in humans, with values ranging from 0.55 to 0.66. Those results suggest a specific relationship between cardiac and body size in the equine species, and this should be taken into account to establish echocardiographic reference values in this species. No significant effect of the training level on echocardiographic measurements could be shown in the present study. This is not in agreement with previous studies [22,23,27,43]. However, in those studies, the training effect has been studied in longitudinal studies, in Thoroughbred and Standardbred horses, and after an intensive race training of 4.5 and 24 months duration, respectively. The absence of a significant training effect in the present study could be due to the lack of accuracy of the exercise history obtained from the owners, the fact that the training effect was not studied using a longitudinal model, or the unequal distribution of the studied horses into classesdmost of the horses (ie, 100) belonged to the no to light level of work class, and only a few of them belonged to the moderate or high level of work class (ie, 29 and 13, respectively). Although no significant effect of the training could be shown in this study, it cannot be excluded that training had some effect on echocardiographic parameters in some horses included in the study. The main limitations of this study are the limited number of animals investigated and the lack of inclusion of the effects of breed, sex, or growth in the statistical model. However, the objective of the study was not to establish reference values of echocardiographic parameters in horses. Rather, it focused on evaluating the best anthropometric variable and the most appropriate regression analysis that should be used to correct the body size effect on echocardiographic measurements in the equine species. The findings of this study could be used in future studies to evaluate, after inclusion of the body size effect using the most appropriate body size variable and mathematical model, the effect of other physiologic variables, such as sex or breed, on echocardiographic parameters, and to
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Table 2 Allometric equations between echocardiographic measurements and BW, BSA, and TC in 150 horses of different breeds, aged from 1 week to 17 years, and weighing 38-890 kg, and comparison with the allometric equations between echocardiographic measurements and BW reported in 68 growing Spanish foals aged from 22 to 394 days (Rovira et al. 2009)13 Echocardiographic measurements
BW Equations (Present Study)
BSA Equations (Present Study)
TC Equations (Present Study)
IVSd LVIDd LVFWd IVSs LVIDs LVFWs AO Pu LA
0.3 BW 0.36 0.99 BW 0.38 0.24 BW 0.36 0.47 BW 0.36 0.64 BW 0.37 0.39 BW 0.37 0.57 BW 0.42 0.47 BW 0.41 0.89 BW 0.4
1.01 BSA 0.54 3.71 BSA 0.57 0.83 BSA 0.54 1.59 BSA 0.53 2.29 BSA 0.55 1.38 BSA 0.55 2.37 BSA 0.62 1.93 BSA 0.61 3.5 BSA 0.6
0.01 0.04 0.01 0.02 0.03 0.02 0.02 0.01 0.03
TC TC TC TC TC TC TC TC TC
1.01 1.09 1.04 1.02 1.05 1.06 1.19 1.17 1.13
BW Equations (From Rovira et al. 2009)13 0.09 0.41 0.18 0.26 0.42 0.15 0.29 NR NR
BW BW BW BW BW BW BW
0.32 0.32 0.30 0.30 0.21 0.39 0.37
NR, not reported.
determine the normal echocardiographic measurements in healthy horses and ponies. These further studies could define the accurate predictive range of normal values for echocardiographic measurements in equines. Definition of such accurate predictive range of normal echocardiographic measurements is essential to allow differentiating abnormal from normal measurements in a given patient. Aiming at evaluating the relationship between cardiac measurements and body size, in veterinary as well as in human cardiology, several studies have been previously carried out on subjects of mixed age (including or not growing subjects), sex, or breed [5,7-9,15,20], and even on animals of different species [8], without taking into account the effect of those physiological variables on the model. In those studies, inclusion of growing subjects and/or of animals of various breeds or species with a large range of body size allowed to more closely document the relationship between echocardiographic measurements and body size. In humans, it has been shown that the degree of variance of the echocardiographic measurements explained by the subject size is much greater in the child than in the adult, because of the bigger variance in body size during growth [40]. However, the allometric exponents (ie, allometric scaling of a variable (Y) as function of another variable (X) using the power model: Y ¼ aXb) between cardiac dimensions and BW were shown to be similar in growing children and adults [40], which suggests that both growing and adult subjects can be included in studies on the relationship between cardiac measurements and body size. In the present study, the inclusion of growing animals, as well as the wide variation in somatotype of the breeds examined, broadened the range of body sizes investigated, which allowed better documentation of the relationship between cardiac measurements and body size in the equine species. Moreover, the statistical model has been applied not only in the whole group of studied animals (ie, simultaneously on growing and adult horses) but also within each of the two age-groups. In our study, as previously reported in humans [40], echocardiographic measurements showed a higher correlation with body size variables during the growth than in the adulthood. However, results obtained within the adult group suggest that the close and significant correlation between echocardiographic parameters and body size variables also exists after growth.
5. Conclusion This study suggests that in the equine species, dimensional echocardiographic reference values should be established with a correction for body size, especially during growth. The most accurate and straightforward method of performing this body size correction is to establish the allometric regression equations between cardiac dimensional measurements and body size expressed as TC or BW. Such body size correction should allow increasing the diagnostic value of quantitative echocardiography in horses, because of the more accurate definition of the normal values of echocardiographic measurements in this species. Acknowledgments This work was carried out at the Equine Teaching Hospital, Faculty of Veterinary Medicine, University of Liège, Belgium, and has partly been supported by the “Fonds Spéciaux pour la recherche” from the University of Liège. Also, the authors thank the owners of the horses for allowing their animals to be included in the study. References [1] Vörös K, Hetyey C, Reiczigel J, Czirok GN. M-mode and twodimensional echocardiographic reference values for three Hungarian dog breeds: Hungarian Vizsla, Mudi and Hungarian Greyhound. Acta veterinaria Hungarica 2009;57:217-27. [2] Boon JA. Evaluation of size, function, and hemodynamics. In: Boon JA, editor. Veterinary echocardiography. 2nd ed. Ames, IA: Wiley-Blackwell; 2011. p. 153-256. [3] Lauer MS, Larson MG, Levy D. Gender-specific reference M-mode values in adults: population-derived values with consideration of the impact of height. J Am Coll Cardiol 1995;26:1039-46. [4] Sisson D, Schaeffer D. Changes in linear dimensions of the heart, relative to body weight, as measured by M-mode echocardiography in growing dogs. Am J Vet Res 1991;52:1591-6. [5] Morrison SA, Moise NS, Scarlett J, Mohammed H, Yeager AE. Effect of breed and body weight on echocardiographic values in four breeds of dogs of differing somatotype. J Vet Intern Med 1992;6: 220-4. [6] Kampmann C, Wiethoff C, Wenzel A, Stolz G, Betancor M, Wippermann C-F, et al. Normal values of M mode echocardiographic measurements of more than 2000 healthy infants and children in central Europe. Heart 2000;83:667-72. [7] Gonçalves AC, Orton EC, Boon JA, Salman MD. Linear, logarithmic, and polynomial models of M-mode echocardiographic measurements in dogs. Am J Vet Res 2002;63:994-9.
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