Original Research n Pediatric

Determining the Normal Aorta Size in Children1

Purpose:

To establish effective aorta diameter standards at multiple levels of the thoracic aorta, abdominal aorta, and common iliac arteries by using computed tomographic (CT) data in healthy children (infants, children, adolescents) through young adults (hereafter referred to collectively as “children”) of a wide range of sizes so that z scores may be calculated.

Materials and Methods:

This retrospective study was approved by the institutional review board. The effective diameter, the average of aortic anteroposterior and lateral diameters, was independently measured at multiple levels of the aorta and common iliac arteries by two radiologists using 1-mm–collimation double-oblique reconstructions. Ordinary least squares regression methods were used to investigate models with various functional forms that related effective diameters at each level to patient body surface area (BSA) and sex. The best model was selected by using R2, and formulas for deriving the expected diameter and estimates of the mean squared error (MSE) were generated.

Results:

Results from 88 thoracic and 110 abdominal contrast material–enhanced CT examinations were analyzed in children without known cardiovascular disease who ranged in age from 0 to 20 years (mean, 9.9 years; standard deviation, 5.7), with BSA ranging from 0.19 to 2.52 m2. Excellent interrater reliability was present (correlation coefficients ranged from 0.95 to 0.98). The best model was a polynomial regression model of the natural log transformation of the effective diameter that included linear, quadratic, and cubic BSA terms and a sex main effect as independent variables. The z scores were calculated by using the observed and expected effective diameters and the MSE.

Conclusion:

The range of normal effective diameters of the aorta at multiple levels and the common iliac arteries was determined for children of different sizes and both sexes. Measurements outside of the normal ranges are consistent with aneurysm or hypoplasia.

1

From the Department of Radiology, Section of Pediatric Radiology (S.V.H., S.B.G.), and Department of Biostatistics (S.Y.L.), Arkansas Children’s Hospital, University of Arkansas for Medical Sciences, 1 Children’s Way, Little Rock, AR 72202. Received February 27, 2014; revision requested March 31; final revision received July 2; accepted August 12; final version accepted August 20. Address correspondence to S.B.G. (e-mail: [email protected]).

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Online supplemental material is available for this article.

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Imaging

Shilpa V. Hegde, MBBS Shelly Y. Lensing, MS S. Bruce Greenberg, MD

PEDIATRIC IMAGING: Normal Aorta Size in Children

N

ormal standards for both the thoracic and abdominal aortic diameter at multiple levels have been established for adults and can be used to determine stenosis or aneurysm formation (1). Standards for infants (1 month to 1 year old), children (birth to 12 years old or 1–12 years old), adolescents (13–17 years old), and young adults (18–24 years old) (hereafter, individuals in these age groups will be referred to collectively as “children”) are not as well established. Echocardiography standards for the thoracic aorta rely on planar measurements rather than on transverse measurements. The planar image is created along the long axis of the aorta. As such, only one diameter can be measured at a given level of the aorta. An assumption is made that the plane precisely bisects the aorta and that the aorta is perfectly round. Cross-sectional imaging standards using computed tomography (CT) and magnetic resonance (MR) imaging of the thoracic aorta are limited in children, and no standards exist for the abdominal aorta (2–4). Determining diffuse aortic hypoplasia in conditions such as Williams syndrome or aneurysmal dilatation in children with Marfan disease is hampered by the lack of

Advances in Knowledge nn The normal ranges of effective aortic diameters in children (infants, children, adolescents) through young adults (collectively referred to as “children”) at multiple levels of the thoracic aorta, abdominal aorta, and common iliac arteries obtained with CT were established by measuring the effective diameter on doubleoblique reconstructions in children of varying sizes and analyzing the measurements by using the least squares regression method to determine the range of normal effective diameter. nn Aortic effective diameter measurements that are outside of the normal range can be considered aneurysmal or hypoplastic. 860

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reliable standards (1). Our purpose was to establish a set of standards for the effective aortic diameter, the mean of anteroposterior and transverse diameter measurements of the aorta at multiple levels of the thoracic aorta, abdominal aorta, and common iliac arteries in children of a wide range of sizes by using CT.

Materials and Methods The study was approved by the institutional review board (University of Arkansas for Medical Sciences, Little Rock, Ark). Informed consent was waived by the institutional review board. A retrospective study was performed to determine the normal effective diameter of the aorta at different levels in children of varying sizes. The inclusion criteria for children evaluated during a 6-month period between July and December 2012 included the following: (a) torso CT performed of the whole torso or chest or abdomen and pelvis with intravenous contrast material during a 6-month period between July and December 2012 at a tertiary care pediatric hospital (Arkansas Children’s Hospital, Little Rock, Ark), (b) patient height determined by length measurement using a paper tape measure in infants and toddlers and a stadiometer for older children, and (c) CT images archived using 0.5mm collimation. Exclusion criteria included the following: (a) history of cardiovascular disease; (b) patients without height determined by using a tape measure or stadiometer, which is necessary to calculate body surface area (BSA) (patient weight is always available because

Implication for Patient Care nn The range of normal effective diameters of the aorta at multiple levels and the common iliac arteries was determined for children of different sizes and both sexes; attention to these normal ranges may allow the radiologist to determine a diagnosis of aortic hypoplasia or aneurysm.

contrast material dose is based on patient weight); and (c) CT images archived using collimation of greater than 0.5 mm. Only the first CT scan was included in the study if multiple examinations were performed during the 6-month period. One hundred thirty-seven of 740 screened torso CT examinations met the study inclusion criteria. Of the 137 included CT studies, 88 included the chest and 110 included the abdomen and pelvis. Among the 603 excluded examinations, the criteria for exclusion included an examination for which the archived-collimation images were obtained with greater than 0.5mm collimation (n = 361), an examination with an absence of administration of intravenous contrast material (n = 101), the examination was a repeat examination during the study period (n = 52), an examination performed because the patient was suspected of having a vascular abnormality (n = 51), an examination that was a cardiac CT examination (n = 22), an examination that included only the pelvis at CT (n = 8), and an examination that included only the abdomen at CT (n = 8). The BSA for each patient was calculated by using the method of Haycock et al (5). This method was selected because a convenient BSA calculator is available for free on the Internet (http://www.

Published online before print 10.1148/radiol.14140500 Content codes: Radiology 2015; 274:859–865 Abbreviations: BSA = body surface area MSE = mean squared error SD = standard deviation Author contributions: Guarantors of integrity of entire study, S.V.H., S.B.G.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; agrees to ensure any questions related to the work are appropriately resolved, all authors; literature research, S.V.H., S.B.G.; clinical studies, S.V.H., S.B.G.; statistical analysis, S.Y.L.; and manuscript editing, all authors Conflicts of interest are listed at the end of this article.

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Figure 1

Figure 1: A, Sagittal oblique, B, coronal oblique multiplanar reconstructions obtained perpendicular to the aorta were created to determine cross section of the aorta at the level superior to the celiac axis. Arrows = planes used to create the true cross-sectional image, C. C, Effective diameter of abdominal aorta obtained superior to the celiac axis is 11.2 mm.

ultradrive.com/BSAc.htm) and has been used in our department for many years to determine BSA. All study examinations were performed with either of two CT scanners (Aquilion 64 or Aquilion One; Toshiba, Otawara-shi, Japan). The intravenous contrast material used for children who weighed less than 10 kg was iohexol (Omnipaque 240; GE Healthcare, Little Chalfont, Buckinghamshire, England), 240 mg of iodine per milliliter, at a dose of 3 mL per kilogram of body weight. For children who weighed more than 10 kg, iohexol (Omnipaque 300; GE Healthcare), 300 mg of iodine per milliliter, at a dose of 2 mL per kilogram, with a maximum dose of 100 mL, was used. Images were reconstructed by using axial 0.5-mm collimation. Multiplanar reformations were created by using a workstation (Vitrea FX; Vital Images, Minneapolis, Minn). All multiplanar reformations were double-oblique reconstructions obtained perpendicular to the aorta (Fig 1). The effective diameter at each level was determined by averaging the anteroposterior and lateral diameter measurements. The aortic levels at which measurements were obtained were as follows: aortic annulus, aorta at the sinuses, ascending aorta at the level of the right pulmonary artery, aortic arch, isthmus, proximal descending aorta (distal to the aortic arch where the descending

aorta obtains a cranial-caudal orientation), aorta at the diaphragm, aorta superior to the celiac axis, aorta at the level of the renal arteries, and superior to the descending aortic bifurcation. Right and left iliac artery effective diameters were measured midway between the aortic bifurcation and the common iliac artery bifurcation. Images from all studies were independently read by two pediatric radiologists (S.B.G., with 25 years of experience, and S.V.H., with 2 years of experience). Each radiologist independently created 1-mm-thick doubleoblique multiplanar reconstructions from the original axial data sets and used electronic calipers to measure anteroposterior and lateral diameters that were used to determine the effective diameter.

Statistical Methods Intraclass correlation coefficients were computed for evaluating the interrater reliability of diameter measurements from two readers (6). These two measurements were then averaged for further analysis. Ordinary least squares regression models were fit to describe the relationship between aortic diameter at a particular level (dependent variable) and independent variables defined by BSA. Following the approach and using models described in two studies that modeled aortic diameter measured with an echocardiogram (3,4), three sets of

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models were initially evaluated by using R2 to determine the functional form with the best fit, as shown in the examples for the aortic annulus (AA) that follow: AA = b0 + b1· BSA + b2 · BSA2+ b3 · BSA3,(1) loge (AA) = b0 + b1· BSA + b2 · BSA2+ b3 · BSA3,

(2)

and loge (AA) = b0 + b1 · loge (BSA), (3) where b0 is the intercept and b1–b3 are the slopes estimated by the model for linear, quadratic, and cubic terms; BSA is used to predict loge of the aortic annulus (ie, natural log of the aortic annulus). After the best model was identified, the effect of sex was investigated by adding a sex main effect and interactions with the BSA terms in the model. Age was not included in the model because the effect of age is confounded by BSA, as the two are highly correlated (Spearman correlation, 0.93). Finally, outliers were identified as being observations with studentized residuals greater than three or less than negative three. The models were then refitted without outliers, consistent with studies performed in patients in whom echocardiograms were obtained (7,8). From these models’ slope estimates, formulas were specified for the predicted diameters, 861

PEDIATRIC IMAGING: Normal Aorta Size in Children

Table 1

0–2 3–5 6–11 12–16 17–20 Total

and that all polynomial terms remained significant. The equations, MSEs, and R2 for the final models may be found in Table 3. These equations can be used to calculate the predicted diameter of the aorta at various levels. To calculate a z score, we first obtained the predicted natural log of the diameter of the aorta at various levels by using the patient’s BSA and sex in the formulas. Then, we calculated the natural log of the observed diameters. The z score, z, at a particular level could then be calculated thus:

Table 2

Age According to Sex Age (y)

Hegde et al

No. of Male No. of Female Patients Patients All 11 (15) 12 (16) 14 (19) 20 (27) 18 (24) 75

9 (15) 12 (19) 12 (19) 22 (35) 7 (11) 62

20 (15) 24 (18) 26 (19) 42 (31) 25 (18) 137

Note.—Numbers in parentheses are percentages.

and estimates of the mean squared error (MSE) were obtained, so that the z scores could be calculated. Analyses were performed by using software (SAS 9.3; SAS Institute, Cary, NC).

Intraclass Correlation at Different Aortic Levels as Measured by Two Radiologists

Aortic Level Annulus Sinus of Valsalva Sinotubular junction Mid ascending aorta Arch Isthmus Proximal descending aorta At the diaphragm Superior to the celiac axis Level of renal arteries Above the bifurcation Right common iliac artery Left common iliac artery

Intraclass Correlation Coefficient 0.95 0.98 0.98 0.98 0.98 0.98 0.97 0.97 0.96 0.96 0.97 0.95 0.96

Results Patient Characteristics The age and sex distributions are summarized in Table 1. For 137 children, the median age was 10 years 11 months, and age ranged from 2 months to 20 years 11 months (mean, 9.9 years; standard deviation [SD], 5.7 years). The mean BSA was 1.23 m2 ± 0.62 (SD) for the thorax and 1.22 m2 ± 0.57 for the abdomen; BSA for both ranged from 0.19 to 2.52 m2. The most common clinical indication for a CT scan was oncology follow-up (n = 57, 42%). No tumor compression or other mass compression of the aorta occurred in our study. Other common indications were pain (n = 22, 16%), trauma (n = 14, 10%), and infection (n = 12, 9%). Interrater Reliability There was excellent interrater reliability between the two readers, indicating that the method to determine the effective diameter was reproducible (Table 2). Intraclass correlation coefficients ranged from 0.95 to 0.98 (Table 2). Regression Models The best model was the polynomial regression model of natural log of the effective diameter that included linear, 862

quadratic, and cubic terms as independent variables (Eq [2]). The R2 was the highest for this model for all levels; the R2 for this model versus Equation (1) and Equation (3) was higher by a median of 0.023 (range, 0.014–0.036) and 0.005 (range, 0.002–0.034), respectively. For all levels, the intercept and linear, quadratic, and cubic terms were significant (all P , .05). The effect of sex was investigated and was found to be significant as a main effect for Valsalva sinus, isthmus, proximal descending aorta, aorta at the diaphragm, and right common iliac artery (all P , .05). This factor indicated that the curves were shifted higher (ie, had a larger intercept) for male children as compared with female children. For consistency, a sex main effect was included in all models. Interactions between sex and linear, quadratic, and cubic BSA terms all were not significant. Outliers were deleted for five levels: Three levels had one outlier, and two had two outliers; the remaining levels had no outliers. For the models with outliers removed, it was verified that the cubic model for the log of the diameter remained the best model, as compared with the other two models

z=

log e( D obs) —log e( D pred) ,(4) MSE

where Dobs is observed diameter and Dpred is predicted diameter. Note that the formulas in Table 3 already give the predicted values on the natural log scale, so once the formulas are applied, there is no need to natural log transform the calculated value. The z scores are approximately normally distributed, with a mean of 0 and SD of 1. The z scores represent how many SDs above or below the predicted regression line (or mean) an observation is. For example, a measurement with a z score of 2 means that the value for the subject is 2 SDs above what would be estimated for the mean; whereas a z score of 22 would indicate that the value for the subject is 2 SDs below what would be expected. Also, given the theoretical normal distribution, it is expected that values for 68.3% of the population are within the mean 6 1 SD, those for 95.4% of the population are within the mean 6 2 SDs, and those for 99.7% of the population are within the mean 6 3 SDs. The same information can be displayed in the form of a graph that does not require calculations. An example for the aortic annulus level is included (Fig 2). Graphs of all aortic levels and the common iliac arteries are included in Appendix E1 (online).

Discussion A prerequisite for identifying abnormal is to first determine normal. The normal range of aortic effective diameters

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Table 3 Formulae to Calculate the Predicted Diameter on a Natural Log Scale Aortic Level Annulus Sinus of Valsalva Sinotubular junction Mid ascending aorta Arch Isthmus Proximal descending aorta At the diaphragm Superior to the celiac axis Level of renal arteries Above the bifurcation Right common iliac artery Left common iliac artery

Formula

Sample Size*

loge(ED) = 2.049 + 0.022 · M + 1.359 · BSA 2 0.614 · BSA2 + 0.112 · BSA3 loge(ED) = 2.145 + 0.061· M + 1.519 · BSA 2 0.724 · BSA2 + 0.134 · BSA3 loge(ED) = 1.761 + 0.0081· M + 1.930 · BSA 2 0.977 · BSA2 + 0.189 · BSA3 loge(ED) = 1.747 2 0.016 · M + 2.053 · BSA 2 1.044 · BSA2 + 0.195 · BSA3 loge(ED) = 1.519 + 0.038 · M + 2.047 · BSA 2 1.006 · BSA2 + 0.187 · BSA3 loge(ED) = 1.295 + 0.058 · M + 2.396 · BSA 2 1.276 · BSA2 + 0.245 · BSA3 loge(ED) = 1.467 + 0.080 · M + 1.880 · BSA 2 0.937 · BSA2 + 0.176 · BSA3 loge(ED) = 1.492 + 0.058 · M + 1.593 · BSA 2 0.739 · BSA2 + 0.132 · BSA3 loge(ED) = 1.499 + 0.023 · M + 1.454 · BSA 2 0.663 · BSA2 + 0.123 · BSA3 loge(ED) = 1.205 + 0.043 · M + 1.555 · BSA 2 0.658 · BSA2 + 0.115 · BSA3 loge(ED) = 1.021 + 0.042 · M + 1.826 · BSA 2 0.812 · BSA2 + 0.138 · BSA3 loge(ED) = 0.388 + 0.079 · M + 2.475 · BSA 2 1.272 · BSA2 + 0.233 · BSA3 loge(ED) = 0.417 + 0.062 · M + 2.486 · BSA 2 1.323 · BSA2 + 0.252 · BSA3

88 88 87 88 88 88 88 88 110 109 109 108 108

MSE

0.084 0.095 0.106 0.116 0.109 0.095 0.103 0.095 0.102 0.118 0.109 0.130 0.120

R2 0.912 0.896 0.898 0.875 0.908 0.928 0.904 0.905 0.872 0.870 0.874 0.860 0.872

Note.—ED = effective diameter, loge = natural log, M = male, MSE = square root of the MSE; male = 1 when patient is male and male = 0 when patient is female. * Sample size for final model after removing 0–2 outliers.

in the aortic root, thoracic aorta, abdominal aorta, and iliac arteries in children were determined in a wide range of child sizes in our study. The regression equations derived from the measurements allow for the calculation of z scores. A z score calculator using a spreadsheet (Excel; Microsoft, Redmond, Wash) is now used at our institution (Arkansas Children’s Hospital), with only the patient BSA, sex, and effective diameter at the level of interest entered to determine the z score. The range of normal effective diameters of the aorta at multiple levels and of the common iliac arteries was determined for children of different sizes and both sexes. Measurements outside of the normal ranges are consistent with aneurysm or hypoplasia. Echocardiography is the standard method for determining the size of the thoracic aorta in children. A recent review of echocardiographic methods showed a general lack of standardization in technique (9). The current guideline is to obtain measurements perpendicular to the axis of blood flow at reproducible landmarks. The aortic diameter is measured in a single plane from a planar image. The aorta is not always round, leading to an error in effective diameter. The limited available ultrasonography (US)

windows frequently fetter the ability to accurately determine aortic effective diameter. In our experience, echocardiographic standards are especially poor in larger children. Measurements of aortic diameter should be taken at reproducible anatomic landmarks perpendicular to the axis of blood flow (10). CT and MR imaging three-dimensional data sets are ideal for creating multiplanar reconstructions perpendicular to the aorta for accurate measurements of the aortic diameter (11). Axial reconstructions introduce error in measuring the true aortic effective diameter because of the normal oblique course of the aorta. If the patient is suspected of having an aneurysm or hypoplasia, a doubleoblique reconstruction should be created. Few reports of the normal thoracic aorta size in children determined by using CT or MR exist. Fitzgerald et al (2) correlated axial CT measurements of the thoracic aorta with patient age in children. The study was limited by the use of 5–10-mm-thick axial sections, which do not allow for multiplanar reconstructions perpendicular to the aorta. The authors failed to relate aortic diameter to patient size. Akay et al (3) correlated thoracic aortic diameter to thoracic vertebral diameter. The researchers in that study also

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failed to relate aortic diameter with patient size. Both studies were limited to the thoracic aorta. Wolak et al (12) used CT to relate the ascending and descending thoracic aortic diameter to patient age, sex, and BSA but only included adults in their study. Kaiser et al (4) used contrast material–enhanced MR angiography studies to measure aortic diameters in children. The study utilized double-oblique measurements perpendicular to the aorta and related effective diameter measurements to BSA. The youngest child in the study was 2 years of age, and the smallest BSA was greater than one-half of a square meter. Hence, the study had no information in regard to infants. Our study included newborns to 20-year-old patients who ranged in size from 0.19 to 2.52 m2. Our study identified sex differences in aortic effective diameter. Gautier et al (13), in an echocardiographic study limited to the aortic root, also identified sex differences in the aortic root diameter. The study of Gautier et al focused on determining normal standards to help determine aneurysmal dilatation in older children with Marfan syndrome and was weighted toward older children and teenagers. No standards for the normal size of the abdominal aorta in children, 863

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Figure 2

Figure 2: Effective diameter of the aorta at aortic annulus versus BSA in, A, male and, B, female patients. Dotted lines = z scores, which denote the number of SDs above and below the mean (solid line), ○ = patients.

to our knowledge, exist. In a single study (14), the researchers evaluated the diameter of the abdominal aorta in children by using B-mode US, but the study was limited to the infrarenal 864

abdominal aorta and the iliac arteries. The study was further limited by measuring diameters in only the anteroposterior dimension. The effective diameter of the abdominal aorta was

measured at multiple levels in our study. We are unaware of any existing study about CT or MR imaging measurements of the effective diameter of the abdominal aorta or the iliac arteries in children. A limitation of our study was that electrocardiographic gating is not routinely performed for torso CT imaging. As such, the measurement reflects neither end-systolic nor end-diastolic measurements. An intermediate effective diameter, rather than a true maximum or minimum aortic diameter, is measured. The range for the measured diameters will include this variation and may slightly increase the SD at each level. However, this is also true of the technique most likely to be used when performing torso imaging. Another limitation of the study was the number of patients included in the study. The study included 88 thoracic and 110 abdominal studies. Although the formulas apply to most pediatric patients that a clinician is likely to encounter, the formulas are only valid for the range of data analyzed here. We limited the models that we evaluated to three that had been described in the literature (7,8) for aortic diameter measured with an echocardiogram; other better-fitting models may exist that are better justified. It should be kept in mind that the 13 levels for each patient are correlated, so it is not surprising that the best model is the same in functional form for all levels. Also, consistent with others (7,8), we refitted the model after removing outliers; this procedure can reduce the estimated variability around the fitted line, resulting in the estimated MSE being slightly underestimated. Also, a small percentage (roughly 5%) of a healthy population will have values outside of 2 SDs, so although a reading is beyond 2 SDs, it could still be a true normal finding, but having objective data for a healthy population gives important context for further clinical evaluation. Disclosures of Conflicts of Interest: S.V.H. disclosed no relevant relationships. S.Y.L. disclosed no relevant relationships. S.B.G. disclosed no relevant relationships.

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References 1. Rogers IS, Massaro JM, Truong QA, et al. Distribution, determinants, and normal reference values of thoracic and abdominal aortic diameters by computed tomography (from the Framingham Heart Study). Am J Cardiol 2013;111(10):1510–1516. 2. Fitzgerald SW, Donaldson JS, Poznanski AK. Pediatric thoracic aorta: normal measurements determined with CT. Radiology 1987;165(3):667–669. 3. Akay HO, Ozmen CA, Bayrak AH, et al. Diameters of normal thoracic vascular structures in pediatric patients. Surg Radiol Anat 2009;31(10):801–807. 4. Kaiser T, Kellenberger CJ, Albisetti M, Bergsträsser E, Valsangiacomo Buechel ER. Normal values for aortic diameters in children and adolescents: assessment in vivo by contrast-enhanced CMR-angiography. J Cardiovasc Magn Reson 2008 (Dec 5);10:56. 5. Haycock GB, Schwartz GJ, Wisotsky DH. Geometric method for measuring body surface area: a height-weight formula validated in infants, children, and adults. J Pediatr 1978;93(1):62–66.

6. Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol Bull 1979;86(2):420–428. 7. Olivieri L, Arling B, Friberg M, Sable C. Coronary artery Z score regression equations and calculators derived from a large heterogeneous population of children undergoing echocardiography. J Am Soc Echocardiogr 2009;22(2):159–164. 8. Pettersen MD, Du W, Skeens ME, Humes RA. Regression equations for calculation of z scores of cardiac structures in a large cohort of healthy infants, children, and adolescents: an echocardiographic study. J Am Soc Echocardiogr 2008;21(8):922–934. 9. Cantinotti M, Scalese M, Molinaro S, Murzi B, Passino C. Limitations of current echocardiographic nomograms for left ventricular, valvular, and arterial dimensions in children: a critical review. J Am Soc Echocardiogr 2012;25(2):142–152. 10. Hiratzka LF, Bakris GL, Beckman JA, et al. 2010 ACCF/AHA/AATS/ACR/ASA/SCA/SCAI/ SIR/STS/SVM guidelines for the diagnosis and management of patients with thoracic aortic disease: executive summary—a report of the American College of Cardiology Foundation/

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