Pediatr Cardiol (2014) 35:315–322 DOI 10.1007/s00246-013-0778-1
ORIGINAL ARTICLE
Increased Regional Deformation of the Left Ventricle in Normal Children With Increased Body Mass Index: Implications for Future Cardiovascular Health David Black • Jen Bryant • Charles Peebles • Lucy Davies • Hazel Inskip • Keith Godfrey • Joseph Vettukattil • Mark Hanson
Received: 30 April 2013 / Accepted: 14 August 2013 / Published online: 29 August 2013 Ó Springer Science+Business Media New York 2013
Abstract The prevalence of obesity continues to increase in the developing world. The effects of obesity on the cardiovascular system include changes in systolic and diastolic function. More recently obesity has been linked with impairment of longitudinal myocardial deformation properties in children. We sought to determine the effect of increased body mass index (BMI) on cardiac deformation in a group of children taking part in the population-based Southampton Women’s Survey to detect early cardiovascular changes associated with increasing BMI before established obesity. Sixty-eight children at a mean age of 9.4 years old underwent assessment of longitudinal myocardial deformation in the basal septal segment of the left ventricle (LV) using twodimensional speckle tracking echocardiography. Parameters of afterload and preload, which may influence deformation, were determined from cardiac magnetic resonance imaging. BMI was determined from the child’s height and weight at the time of echocardiogram. Greater pediatric BMI was associated with greater longitudinal myocardial deformation or D. Black (&) J. Bryant H. Inskip K. Godfrey M. Hanson Institute of Developmental Sciences, Human Development and Health Academic Unit, University of Southampton, Southampton, UK e-mail:
[email protected] D. Black C. Peebles J. Vettukattil Pediatric Cardiology and Cardiothoracic Radiology, University Hospital Southampton NHS Foundation Trust, Southampton, UK J. Bryant L. Davies H. Inskip K. Godfrey M. Hanson MRC Lifecourse Epidemiology Unit, University of Southampton, Southampton, UK J. Bryant L. Davies H. Inskip K. Godfrey M. Hanson NIHR Southampton Biomedical Research Centre, University of Southampton and University Hospital Southampton NHS Foundation Trust, Southampton SO16 6YD, UK
strain in the basal septal segment of the LV (b = 1.6, p \ 0.001); however, this was not related to contractility or strain rate in this part of the heart (b = 0.001, p = 0.92). The end-diastolic volume of the LV increased with increasing BMI (b = 3.93, p \ 0.01). In young children, regional deformation in the LV increases with increasing BMI, whilst normal contractility is maintained. This effect may be explained by the increased preload of the LV associated with increased somatic growth. The long-term implications of this altered physiology need to be followed-up. Keywords BMI
Regional deformation Speckle tracking
Introduction Obesity leads to an expanded circulatory system with a resultant increase in cardiac mass, ventricular dimensions, and stroke volume [33]. In adult patients, this has ultimately led to both systolic and diastolic dysfunction and, over time, to congestive heart failure. Previous studies have shown preservation of ventricular function in obese children using standard echocardiographic measures for assessment [11]. Recently, however, evidence suggests that obesity in children has a significant impact on regional myocardial deformation with a decrease in longitudinal strain and strain rate (SR) [11, 21]. Many of these changes have been linked to duration of obesity [2, 9, 26]. It may be possible that early physiological changes in response to increased body mass index (BMI) could be detected using more sensitive methods, such as two-dimensional speckletracking echocardiography (2D STE). 2D STE has showed ability to detect subclinical myocardial dysfunction not detected using traditional echocardiographic parameters [6, 7, 31]. It has also been shown to be
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sensitive at detecting alterations in regional deformation early in the disease process [22]. More specifically, the basal septal segment of the left ventricle (LV) appears to be affected earliest, and regional deformation in this segment may be a sensitive marker for early changes in left-ventricular function [22]. In this study, we sought to determine whether we could detect any early changes in regional deformation of the basal septal segment of the LV in a group of normal children with increased BMI using 2D STE. This study focused specifically on this segment of the LV as a possible marker of early cardiovascular changes that could be routinely monitored in the assessment of children with obesity. Cardiac magnetic resonance imaging (CMRI) was used to determine the effect of increased BMI on cardiac structure and volumes and to provide information regarding loading conditions.
Methods The Southampton Women’s survey contains a cohort of 9-year-old children who have been followed-up up since birth taking part in research related to maternal, foetal, and postnatal determinants of cardiovascular structure and function [18]. These children are normal with no history of cardiovascular disease. All children in whom CMRI and 2D transthoracic echocardiography (2D TTE) had been performed at the time of the study were included. CMRI and 2D TTE were performed on different occasions with the majority of studies occurring within 3 months of the first 2D TTE. All subjects had their blood pressure measured using an automated sphygmomanometer with an appropriate-sized cuff at the time of the CMRI scan. 2D TTE Echocardiography was performed using a Phillips IE33 ultrasound system (Philips Medical Systems). Images were acquired with either an X7-2 or S5 echocardiography probe (Philips). Apical four-chamber views were saved for off-line analysis using Philips QLAB version 8.1 cardiac motion quantification (CMQ) software. The longitudinal strain in the basal septal segment of the left-ventricular four-chamber apical view was analysed using CMQ. Values for strain and SR were determined using this method (Fig. 1). CMRI CMRI scans were performed on a 1.5-T MRI scanner (Avanto; Siemens Medical Systems, Erlangen, Germany) using a phased array spine coil in combination with a torso array coil. A short-axis stack of contiguous 7 mm—thick steady-state free-precession (SSFP) cine images was acquired. Scans were planned from an end-diastolic (ED)
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four-chamber SSFP image to cover from the base of the LV at the level of the mitral valve to the apex. Sequence parameters were as follows: repetition time (TR) 43.65, echo time (TE) 1.24, field of view (FOV) 280 mm, and flip angle 72°. Scans were acquired on an inspiratory breathhold and retrospectively electrocardiograph-gated. Images were analyzed using open source Osirix imaging analysis software. ED and end-systolic (ES) phases were identified at each slice position as those showing the largest and the smallest cavity area, respectively. LV endocardial and epicardial borders were manually traced at ED and ES for each slice position with endocardial trabecullae and papillary muscles included in the myocardial mass and excluded from the blood volume. The most basal image was selected as the image at ED and ES with myocardium extending over at least 50 % of the myocardial circumference. Using Simpson’s rule for measuring volumes, where a cavity volume is estimated by the sum of the cross-sectional area of multiple single slices multiplied by the slice thickness, ED (EDV) and ES volumes (ESVs) were obtained. LV ejection fraction (EF) was determined as (EDV–ESV)/EDV. Aortic Compliance Using three-chamber and LVOT SSFP cine views showing the aortic root, a single-slice high-resolution breath-hold SSFP cine acquisition was applied perpendicular to the long axis of the ascending aorta at the level of the pulmonary trunk. Sequence parameters were as follows: TR 41.8, TE 1.4, flip angle 52, FOV 280 mm, acquisition matrix 192 9 236, SLT 6 mm, pixel size 1.09 9 1.09, and cardiac phases 25. Brachial blood pressure was measured immediately after acquisition. The vessel lumen area was measured across the cardiac cycle in mm2 using an automated segmentation method described and validated by Jackson et al. [12] and implemented under Matlab (Mathworks, Inc., Natick, MA, USA). Compliance was calculated using the maximum vessel area (Amax) and minimum vessel area (Amin) corresponding to ES and ED area as follows: compliance (mm2/ mmHg) = Amax - Amin/PP [19]. Reproducibility Repeat measurements to assess intraobserver variability were performed in 20 subjects using CMQ. These measurements were performed at least 3 months after initial measurements with the observer blinded to initial results Statistics All data were analysed using STATA (version 11.1). Children’s BMI measurements (at the time of echo) were
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317
Fig. 1 Apical four-chamber view of the LV. CMQ was used to track the basal septal segment. The graphic display under the image shows longitudinal strain (–%) over time (s). The dot on this graphic display represents maximum longitudinal strain and corresponds to SRs (s-1). Other segments that were excluded from analysis for the purpose of this study remain labeled. MIS mid inferior septal, ApIS apical inferior septal, Apex, ApAL apical antero-lateral, MAL mid antero-lateral, BAL basal anterolateral
transformed into SD z-scores using the LMS method to obtain values standardised to each child’s sex and age [34]. Where appropriate, logarithmic transformation was applied to variables to satisfy assumptions of linearity. Univariate linear regression models were fitted using cardiovascular health measurements as the outcomes and BMI z-scores as the predictor. Regression models were then adjusted for potential confounders, including maternal qualification attainment, maternal prepregnancy smoking status, and maternal social class, in a multivariate analysis. Intraobserver variability was assessed for agreement by calculating the linear correlation, and reliability of the measurements was evaluated through the intraclass correlation coefficient (ICC). Bland–Altman plots were used to determine and evaluate the limits of agreement. Ethics This study was approved as part of the Southampton Women’s Survey and research into maternal, foetal, and postnatal determinants of cardiovascular structure and function in children.
Results A total of 88 children at a mean age of 9.4 years underwent CMRI and 2D TTE at the time of the study. Of these 68 (37 male and 31 female) were included in the study; 20 were excluded from final analysis due to poor image quality
(n = 7) and incorrect image acquisition (n = 13). Incorrect image acquisition was related to the use of an incorrect probe, i.e., S8 (Phillips), which is not compatible with the software required for analysis. Subject characteristics are listed in Table 1. In terms of general cardiovascular measurements, an increase in BMI was significantly associated with increased systolic blood pressure (b = 2.29, p = 0.04). This association remained when adjusting for maternal characteristics (b = 2.01, p = 0.08). There was also a significant association with increasing BMI and increasing heart rate (b = 2.45, p = 0.02). Diastolic blood pressure was not found to be associated with increased BMI (b = 1.1, p = 0.21) (Tables 2 and 3). STE and strain measurements identified a significant association with BMI. Longitudinal strain in the basal septal segment of the LV increased with increasing BMI (r = 0.41, p \ 0.001). SR rate was not significantly associated with children’s BMI (n = 53, b = 0.001, p = 0.92). An increase in BMI was significantly associated with an increase in LV EDV (b = 3.9, p = 0.008). There were also associations between increasing BMI and LV stroke volume (b = 2.3, p = 0.016) and LV ESV (b = 1.6, p = 0.029). Increasing BMI was found to be significantly associated with increasing cardiac output and remained significant when adjusting for heart rate (b = 0.31, p = 0.001). Increasing BMI was found to be associated with an increase in LV diastolic mass (b = 2.2, p = 0.035). Aortic compliance showed no significant association with BMI (b = 0.17, p = 0.22)
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318 Table 1 Subject characteristics by male versus female sex for all parameters measured during the study
n number of subject measurements taken a
Difference between sexes
b
Geometric mean (SD) is given
Table 2 Children’s BMI British Growth Foundation zscores as a predictor of cardiovascular health at 9 years of age
Pediatr Cardiol (2014) 35:315–322
Characteristics
N Age at MRI (y)
33
Height at MRI (cm)
37
pa
Female Mean (SD)
N
9.4 (0.16)
30
135.7 (5.9)
31
Mean (SD) 9.4 (0.17)
0.92
133.8 (6.0)
0.2
Weight at MRI (kg)
37
32.1 (5.8)
31
33.0 (6.7)
0.55
BMI at MRI (kg/cm2)
37
17.3 (2.1)
31
18.3 (3.0)
0.10
Age at echo (y)
37
Height at echo (cm)
37
9.2 (0.11)
31
135.1 (5.7)
31
9.2 (0.12)
0.25
133.4 (6.1)
0.26
Weight at echo (kg)
37
30.4 (5.3)
31
31.5 (6.0)
0.44
BMI at echo (kg/cm2)
37
16.4 (1.1)b
31
17.4 (1.1)b
0.067
Cardiac strain (% shortening)
37
17.6 (3.3)
31
19.6 (4.6)
0.049
SR (s-1)
27
0.41 (0.04)
26
0.41 (0.02)
0.38
Systolic blood pressure (mmHg) Diastolic blood pressure (mmHg)
33 33
98.1 (7.9) 57.6 (6.6)
30 30
99.9 (10.4) 59.8 (7.6)
0.44 0.23
Mean arterial blood pressure (mmHg)
26
71.3 (7.2)
30
77.0 (7.8)
0.003
Heart rate (bpm)
36
70.3 (7.8)
31
76.8 (9.6)
0.003
Aortic compliance score
28
2.7 (1.4)b
28
2.8 (1.0)b
0.94
Left-ventricular EDV
31
75.6 (12.1)
29
66.5 (10.9)
0.003
Left-ventricular ESV
31
27.3 (6.4)
29
23.0 (5.0)
0.005
Left-ventricular stroke volume
31
48.3 (7.9)
29
43.5 (7.3)
0.017
Left-ventricular EF
31
64.1 (4.9)
29
65.5 (4.0)
0.22
Left-ventricular cardiac output
31
Left-ventricular systolic mass
31
55.3 (7.9)
29
49.0 (8.5)
0.003
Left-ventricular diastolic mass
30
56.7 (7.3)
26
50.9 (8.3)
0.007
Parameter
N
3.6 (1.2)b
29
b
r
3.4 (1.2)b
95 % CI
0.29
p
0.74, 2.47
\0.001
-0.01, 0.01
0.916
Cardiac strain (% shortening)
68
0.41
1.60
SR (s-1)
53
0.01
0.001
Systolic blood pressure (mmHg)
63
0.27
2.29
0.16, 4.42
0.035
Diastolic blood pressure (mmHg)
63
0.16
1.08
-0.63, 2.78
0.211
Mean arterial blood pressure (mmHg)
66
0.18
1.37
-0.47, 3.21
0.143
Heart rate (bpm)
67
0.28
2.45
0.36, 4.53
0.022
Aortic compliance score
56
0.13
0.04
-0.05, 0.91
0.341
Left-ventricular EDV
60
0.34
3.93
1.07, 6.80
0.008
Left-ventricular ESV
60
0.28
1.63
0.17, 3.08
0.029 0.016
Left-ventricular stroke volume
60
0.31
Left-ventricular EF
60
-0.104
Left-ventricular cardiac output
60
0.43
2.31
0.45, 4.17
-0.44
-1.54, 0.67
0.431
0.08
0.04, 0.13
\0.001
Left-ventricular systolic mass
60
0.21
1.64
-0.41, 3.68
0.115
Left-ventricular diastolic mass
56
0.28
2.21
0.16, 4.26
0.035
Reproducibility Levels of reliability (ICC r = 0.77, 95 % CI [0.56, 0.91]) and agreement (Pearson’s r = 0.77, p \ 0.001) were good between intraobserver variability measurements. Figure 2
123
Male
suggests that the differences between the measurements observed were dispersed around the mean and stayed within the limits of agreement (-4.7 to 6.0). The mean difference between the two measurements was not found to be statistically significant (mean difference 0.66, p = 0.31).
Pediatr Cardiol (2014) 35:315–322 Table 3 Child BMI BGF z-scores as a predictor of cardiovascular health at 9 years of age adjusted for maternal qualification attainment, maternal prepregnancy smoking status, and maternal social class
319
Parameter
N
b
95 % CI
Cardiac strain (% shortening)
67
1.42
SR (s-1)
52
0.003
p
0.52, 2.31
0.002
-0.01, 0.01
0.498
Systolic blood pressure (mmHg)
62
2.01
-0.23, 4.26
0.078
Diastolic blood pressure (mmHg)
62
0.39
-1.38, 2.16
0.664
Mean arterial blood pressure (mmHg)
65
1.09
-0.89, 3.08
0.275
Heart rate (bpm)
66
1.63
-0.44, 3.70
0.120
Aortic compliance score
55
0.05
-0.04, 0.15
0.269
Left-ventricular EDV
59
4.21
1.07, 7.35
0.009
Left-ventricular ESV
59
1.52
-0.06, 3.10
0.060
Left-ventricular stroke volume
59
2.69
0.67, 4.71
0.010
Left-ventricular EF
59
-0.20
-1.39, 1.00
0.745
Left-ventricular cardiac output
59
0.08
0.04, 0.13
\0.001
Left-ventricular systolic mass
59
1.57
-0.67, 3.81
0.165
Left-ventricular diastolic mass
55
2.21
-0.04, 4.45
0.054
Fig. 2 Bland–Altman plot for intraobserver variability of measurements derived using CMQ in the basal septal segment of the LV
Discussion Obesity and its Cardiovascular Effects Significant changes in the cardiovascular system can be attributed to obesity both due to generation of a hyperdynamic state and metabolic derangements [33]. Obese children are more likely to develop hypertension, peripheral vascular dysfunction, and atherosclerosis [4, 10]. Endothelial dysfunction plays a key role in the progression of this process [4]. In our study, children with increased BMI already demonstrate a significant increase in blood pressure compared with their peers. Obesity is an anabolic state with consequent increase in lean body mass, acceleration of linear growth, enhanced skeletal maturation, and advanced sexual development
[33]. As can be seen from our results, children with increased BMI were significantly taller. The consequence of this increase in lean body tissue is increased plasma volume and larger circulatory system. The myocardium hypertrophies, and cardiac chambers enlarge in response to such. Obese children have been noted to have larger, thicker hearts with greater stroke volumes and cardiac outputs [13, 24, 32]. Our data show a trend to increased LV mass and stroke volume in patients with increased BMI. These changes are likely to become more significant with the duration and severity of weight increase. Changes in adults and children with obesity have been linked to duration and severity [9, 26]. Differences in LV size related to obesity are greater when comparing adult groups versus childhood groups; this is presumed to be a reflection of disease progression with duration of obesity [2]. Cardiac function appears to be preserved in the early stages of obesity with maintenance of functional reserve [16]. There is evidence, however, that over time a degree of myocardial dysfunction develops. This is believed to be due to a combination of volume load and other metabolic factors, such as insulin resistance and the role of leptins [28, 30]. Earlier studies in children showed preservation of cardiac function using traditional echocardiographic measures [11]. Other echocardiographic studies have showed a decrease in LV shortening fraction with progressively increasing BMI and increased tissue Doppler E/e’ suggesting mildly increased left-ventricular filling pressure from diastolic dysfunction [20, 27, 29]. A number of studies using strain and SR rate imaging have showed a decrease in both systolic and diastolic function in obese children [15, 23, 35]. Recently a study by Giovanni et al. using SR imaging suggested that despite apparent maintenance of normal EF, longitudinal deformation and contractility are decreased in obese children [11].
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Koopman et al. [21] showed decreased systolic and diastolic deformation in obese children with lower STEderived LV systolic longitudinal strain values (-18 ± –2 % vs. -21 ± –2 %, p \ .001), and lower STE-derived LV early diastolic SR values (1.7 ± -0.3 vs. 2.5 ± -0.4, p \ .001). Reassuringly, Ingul et al. [17] showed an improvement in cardiac function, as evaluated by strain and SR, in obese adolescents after a training program. This would suggest that early intervention is paramount in curbing the disease process. Our study looked more specifically at regional deformation in the basal septal segment of the LV and showed an increase in longitudinal deformation in this region. We propose that this is an early response to the hyperdynamic state that accompanies obesity with an increase in preload. Increased left-ventricular EDV, and therefore preload, was significantly associated with increasing BMI in our study. The preservation of SR, and therefore contractility, at this stage suggests that myocardial function is well preserved and that metabolic factors involved in the later pathophysiology of myocardial dysfunction are not yet at play. The trend is toward increased cardiac mass, stroke volume, and EDV, which may increase with time and severity of weight gain. Effect of Cardiac Load on Deformation When analysing our data, it is important to consider the impact of both afterload and preload on cardiac deformation [8, 17]. An increase in afterload has been shown to result in a decrease in deformation in both studies of the right and LV. In right-ventricular studies performed on patients after pulmonary valve replacement for severe pulmonary stenosis and consequently increased RV afterload, there was a significant increase in both strain and SR with RV unloading [25]. This pathophysiology has also been shown in patients with aortic stenosis who demonstrate decreased longitudinal strain and SR, which progresses with disease severity [1, 36]. Even with milder increases in afterload, as seen in hypertension, studies have showed a decrease in regional longitudinal deformation [3, 22]. A combination of fibre orientation and radius of curvature in the base of the heart versus the apex results in an increase in local wall stress, and hence hypertrophy, in the basal segment. One may assume that in obesity, the associated hypertension may cause a similar effect. In our study population, there was a significant increase in systolic and mean blood pressure with increasing BMI. Although significant, this increase in blood pressure did not meet the criteria for hypertension in these children. The studies described earlier in the text relate to adults with longstanding hypertension, and we do not believe that the children in our study would have had significant effects related to blood pressure. The blood pressure measurements
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were also taken on a single occasion and with one cuff size. It would be important for repeated measurements to be taken in the future to monitor the effect of blood pressure on these subjects. Another marker used for afterload in our study was aortic compliance with our hypothesis being that increased BMI and obesity may lead to decreased aortic compliance related to the peripheral vascular dysfunction these patients experience. There was, however, no association between increasing aortic compliance and increasing BMI. It may be that this occurs early in the disease process when peripheral vascular disease has not yet developed. The increase in afterload does not explain the difference in longitudinal strain in the basal septal segment of the LV seen in our study; based on the previous studies mentioned, this would have had the opposite effect. Preload also has a significant effect on deformation. Right ventricle (RV) longitudinal strain is decreased after percutaneous closure of atrial septal defect due to a decrease in RV preload [5]. In the context of obesity with an increase in lean body mass and organ size, the consequent expanded circulatory system, and the subsequent increase in preload to the LV, we suggest that this is an explanation for the finding of increased deformation in the basal septal segment of the LV. This segment has been shown to be sensitive to early changes in LV load, and this may be the first indicator of altered cardiovascular physiology in these patients. Children with increased BMI had greater LV EDVs. This may continue to increase as the duration and severity of weight gain continues, which would potentially be associated with cardiac dysfunction. SR is considered to be a marker of contractility and appears to be less affected by loading conditions [5]. SR in our study did not differ between groups and this possibly reflects a preservation of contractility in patients with a increased BMI.
Limitations Analysis of the echocardiographic images was performed on a retrospective basis. A number of patients were excluded from the study due to poor image quality or image acquisition with an incorrect probe. The quality of image acquisition has been highlighted as a area of importance when applying STE, and in our study this was no different [12, 14]. We believe that looking specifically at the basal septal segment increases the number of images suitable for analysis because this is not affected by poor tracking of the LV apex and free wall, which is often problematic. Although strain and SR measurements in other segments may have been useful, the aim of the study was to look specifically at regional deformation in the basal septal
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segment of the LV. We believe that this method is both sensitive and simple to perform and may be useful in the ongoing monitoring of specific patients as has previously been suggested in patients with hypertension [22].
Conclusion Normal children with increased BMI have with an increase in regional deformation of the basal septal segment of the LV, whilst maintaining normal contractility. Increased longitudinal deformation of the basal septal segment of the LV is an early marker of an increased preload in these children and is an early indicator of an altered cardiovascular system. Early intervention is required for children with increased BMI to prevent the significant consequences of obesity. Using CMQ of a specific region may be an easy and sensitive method of monitoring these children with increased weight gain.
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