Advertisement

Growth of Cardiovascular Structures from the Fetus to the Young Adult

  • Frederic Dallaire
  • Taisto Sarkola
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1065)

Abstract

The size, hemodynamics, and function of cardiovascular structures change dramatically from the early fetal life to late adolescence. The principal determinants of cardiovascular dimensions are related to the blood flow needed to meet metabolic demands. This demand is in turn tightly related to body size and body composition, keeping in mind that various tissues may have different metabolic rates. There is no simple model that links cardiac dimensions with a single body size measurement. Consequently, despite abundant scientific literature, few studies have proposed pediatric reference values that efficiently and completely account for the effect of body size. Other factors influence cardiovascular size and function in children, including sex. The influence of sex is multifactorial and not fully understood, but differences in body size and body composition play an important role. We will first review the determinants of cardiovascular size and function in children. We then explore the evaluation and normalization of cardiovascular size and function in pediatric cardiology in relation to the growth of cardiovascular structures during childhood, with a particular focus on sex differences.

Keywords

Fetus Child Adolescent Growth Puberty Pediatric cardiology Sex Reference value Nomogram Indexing Blood pressure Echocardiography ECG Body composition Lean body mass Exercise testing Artery size Allometry Z score 

References

  1. 1.
    Prothero J. Heart weight as a function of body weight in mammals. Growth. 1979;43(3):139–50.PubMedGoogle Scholar
  2. 2.
    Graham TP Jr, Jarmakani JM, Canent RV Jr, Morrow MN. Left heart volume estimation in infancy and childhood. Reevaluation of methodology and normal values. Circulation. 1971;43(6):895–904.PubMedCrossRefGoogle Scholar
  3. 3.
    Graham TP Jr., Jarmakani MM, Canent RV Jr., Capp MP, Spach MS. Characterization of left heart volumes and mass in normal children and in infants with intrinsic myocardial disease. Circulation. 1968;38(5):826–37.PubMedCrossRefGoogle Scholar
  4. 4.
    Nevill AM, Bate S, Holder RL. Modeling physiological and anthropometric variables known to vary with body size and other confounding variables. Am J Phys Anthropol Suppl. 2005;41:141–53.CrossRefGoogle Scholar
  5. 5.
    Batterham AM, George KP, Whyte G, Sharma S, McKenna W. Scaling cardiac structural data by body dimensions: A review of theory, practice, and problems. Int J Sports Med. 1999;20(8):495–502.PubMedCrossRefGoogle Scholar
  6. 6.
    Dallaire F, Dahdah N. New equations and a critical appraisal of coronary artery z scores in healthy children. J Am Soc Echocardiogr. 2011;24(1):60–74.PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Gautier M, Detaint D, Fermanian C, Aegerter P, Delorme G, Arnoult F, Milleron O, Raoux F, Stheneur C, Boileau C, Vahanian A, Jondeau G. Nomograms for aortic root diameters in children using two-dimensional echocardiography. Am J Cardiol. 2010;105(6):888–94.PubMedCrossRefGoogle Scholar
  8. 8.
    Zilberman MV, Khoury PR, Kimball RT. Two-dimensional echocardiographic valve measurements in healthy children: Gender-specific differences. Pediatr Cardiol. 2005;26(4):356–60.PubMedCrossRefGoogle Scholar
  9. 9.
    Overbeek LI, Kapusta L, Peer PG, de Korte CL, Thijssen JM, Daniels O. New reference values for echocardiographic dimensions of healthy dutch children. Eur J Echocardiogr. 2006;7(2):113–21.PubMedCrossRefGoogle Scholar
  10. 10.
    Sluysmans T, Colan SD. Theoretical and empirical derivation of cardiovascular allometric relationships in children. J Appl Physiol. 2005;99(2):445–57.PubMedCrossRefGoogle Scholar
  11. 11.
    Blimkie CJ, Cunningham DA, Nichol PM. Gas transport capacity and echocardiographically determined cardiac size in children. J Appl Physiol Respir Environ Exerc Physiol. 1980;49(6):994–9.PubMedGoogle Scholar
  12. 12.
    Nevill AM, Holder RL, Baxter-Jones A, Round JM, Jones DA. Modeling developmental changes in strength and aerobic power in children. J Appl Physiol. 1998;84(3):963–70.PubMedCrossRefGoogle Scholar
  13. 13.
    Nevill AM, Winter EM, Ingham S, Watts A, Metsios GS, Stewart AD. Adjusting athletes’ body mass index to better reflect adiposity in epidemiological research. J Sports Sci. 2010;28(9):1009–16.PubMedCrossRefGoogle Scholar
  14. 14.
    Sarkola T, Manlhiot C, Slorach C, Bradley TJ, Hui W, Mertens L, Redington A, Jaeggi E. Evolution of the arterial structure and function from infancy to adolescence is related to anthropometric and blood pressure changes. Arterioscler Thromb Vasc Biol. 2012;32(10):2516–24.PubMedCrossRefGoogle Scholar
  15. 15.
    Doyon A, Kracht D, Bayazit AK, Deveci M, Duzova A, Krmar RT, Litwin M, Niemirska A, Oguz B, Schmidt BM, Sozeri B, Querfeld U, Melk A, Schaefer F, Wuhl E. Carotid artery intima-media thickness and distensibility in children and adolescents: reference values and role of body dimensions. Hypertension. 2013;62(3):550–6.PubMedCrossRefGoogle Scholar
  16. 16.
    Blais S, Berbari J, Counil FP, Dallaire F. A systematic review of reference values in pediatric cardiopulmonary exercise testing. Pediatr Cardiol. 2015;36(6):1316.CrossRefGoogle Scholar
  17. 17.
    Cawley RH, Mc KT, Record RG. Parental stature and birth weight. Am J Hum Genet. 1954;6(4):448–56.PubMedPubMedCentralGoogle Scholar
  18. 18.
    Ounsted M, Ounsted C. Maternal regulation of intra-uterine growth. Nature. 1966;212(5066):995–7.PubMedCrossRefGoogle Scholar
  19. 19.
    Lubchenco LO, Hansman C, Boyd E. Intrauterine growth in length and head circumference as estimated from live births at gestational ages from 26 to 42 weeks. Pediatrics. 1966;37(3):403–8.PubMedGoogle Scholar
  20. 20.
    Schwarzler P, Bland JM, Holden D, Campbell S, Ville Y. Sex-specific antenatal reference growth charts for uncomplicated singleton pregnancies at 15–40 weeks of gestation. Ultrasound Obstet Gynecol. 2004;23(1):23–9.PubMedCrossRefGoogle Scholar
  21. 21.
    Schneider C, McCrindle BW, Carvalho JS, Hornberger LK, McCarthy KP, Daubeney PE. Development of z-scores for fetal cardiac dimensions from echocardiography. Ultrasound Obstet Gynecol. 2005;26(6):599–605.PubMedCrossRefGoogle Scholar
  22. 22.
    Lee W, Riggs T, Amula V, Tsimis M, Cutler N, Bronsteen R, Comstock CH. Fetal echocardiography: Z-score reference ranges for a large patient population. Ultrasound Obstet Gynecol. 2010;35(1):28–34.PubMedCrossRefGoogle Scholar
  23. 23.
    Gagnon C, Bigras JL, Fouron JC, Dallaire F. Reference values and z scores for pulsed-wave doppler and m-mode measurements in fetal echocardiography. J Am Soc Echocardiogr. 2016;29:448–60.PubMedCrossRefGoogle Scholar
  24. 24.
    Perez-Cruz M, Cruz-Lemini M, Fernandez MT, Parra JA, Bartrons J, Gomez-Roig MD, Crispi F, Gratacos E. Fetal cardiac function in late-onset intrauterine growth restriction vs small-for-gestational age, as defined by estimated fetal weight, cerebroplacental ratio and uterine artery doppler. Ultrasound Obstet Gynecol. 2015;46(4):465–71.PubMedCrossRefGoogle Scholar
  25. 25.
    DeVore GR, Zaretsky M, Gumina DL, Hobbins JC. Abnormal Cardiovascular 24-Segment Sphericity Index of the Right and Left Ventricles in Fetuses with Growth Restriction. Ultrasound Obstet Gynecol. 2017 Jul 26. https://doi.org/10.1002/uog.18820. [Epub ahead of print] PubMed PMID: 28745414.
  26. 26.
    Cantinotti M, Scalese M, Murzi B, Assanta N, Spadoni I, Festa P, De Lucia V, Crocetti M, Marotta M, Molinaro S, Lopez L, Iervasi G. Echocardiographic nomograms for ventricular, valvular and arterial dimensions in caucasian children with a special focus on neonates, infants and toddlers. J Am Soc Echocardiogr. 2014;27(2):179–91. e172PubMedCrossRefGoogle Scholar
  27. 27.
    Kampmann C, Wiethoff CM, Wenzel A, Stolz G, Betancor M, Wippermann CF, Huth RG, Habermehl P, Knuf M, Emschermann T, Stopfkuchen H. Normal values of m-mode echocardiographic measurements of more than 2000 healthy infants and children in central europe. Heart. 2000;83(6):667–72.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Olander RF, Sundholm JK, Ojala TH, Andersson S, Sarkola T. Neonatal Arterial Morphology Is Related to Body Size in Abnormal Human Fetal Growth. Circ Cardiovasc Imaging. 2016;Sep;9(9). pii: e004657. https://doi.org/10.1161/CIRCIMAGING.116.004657. PubMed PMID: 27601367.
  29. 29.
    Lopez L, Colan SD, Frommelt PC, Ensing GJ, Kendall K, Younoszai AK, Lai WW, Geva T. Recommendations for quantification methods during the performance of a pediatric echocardiogram: a report from the pediatric measurements writing group of the american society of echocardiography pediatric and congenital heart disease council. J Am Soc Echocardiogr. 2010;23(5):465–95.Google Scholar
  30. 30.
    Colan SD. The why and how of z scores. J Am Soc Echocardiogr. 2013;26(1):38–40.PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Mawad W, Drolet C, Dahdah N, Dallaire F. A review and critique of the statistical methods used to generate reference values in pediatric echocardiography. J Am Soc Echocardiogr. 2013;26(1):29–37.CrossRefPubMedGoogle Scholar
  32. 32.
    Cantinotti M, Kutty S, Franchi E, Paterni M, Scalese M, Iervasi G, Koestenberger M. Pediatric echocardiographic nomograms: what has been done and what still needs to be done. Trends Cardiovasc Med. 2017;27(5):336–49.PubMedCrossRefGoogle Scholar
  33. 33.
    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):142–52.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Tanner JM. Fallacy of per-weight and per-surface area standards, and their relation to spurious correlation. J Appl Physiol. 1949;2(1):1–15.PubMedCrossRefGoogle Scholar
  35. 35.
    Gutgesell HP, Rembold CM. Growth of the human heart relative to body surface area. Am J Cardiol. 1990;65(9):662–8.PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    Neilan TG, Pradhan AD, King ME, Weyman AE. Derivation of a size-independent variable for scaling of cardiac dimensions in a normal paediatric population. Eur J Echocardiogr. 2009;10(1):50–5.PubMedCrossRefGoogle Scholar
  37. 37.
    Foster BJ, Mackie AS, Mitsnefes M, Ali H, Mamber S, Colan SD. A novel method of expressing left ventricular mass relative to body size in children. Circulation. 2008;117(21):2769–75.PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Buechel EV, Kaiser T, Jackson C, Schmitz A, Kellenberger CJ. Normal right- and left ventricular volumes and myocardial mass in children measured by steady state free precession cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2009;11:19.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Jones NL, Summers E, Killian KJ. Influence of age and stature on exercise capacity during incremental cycle ergometry in men and women. Am Rev Respir Dis. 1989;140(5):1373–80.PubMedCrossRefGoogle Scholar
  40. 40.
    Hansen JE, Sue DY, Wasserman K. Predicted values for clinical exercise testing. Am Rev Respir Dis. 1984;129(2 Pt 2):S49–55.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Sue DY, Hansen JE. Normal values in adults during exercise testing. Clin Chest Med. 1984;5(1):89–98.PubMedGoogle Scholar
  42. 42.
    Nes BM, Osthus IB, Welde B, Aspenes ST, Wisloff U. Peak oxygen uptake and physical activity in 13- to 18-year-olds: the young-hunt study. Med Sci Sports Exerc. 2013;45(2):304–13.PubMedCrossRefGoogle Scholar
  43. 43.
    Welsman JR, Armstrong N, Nevill AM, Winter EM, Kirby BJ. Scaling peak vo2 for differences in body size. Med Sci Sports Exerc. 1996;28(2):259–65.PubMedCrossRefGoogle Scholar
  44. 44.
    Sluysmans T, Colan SD. Structural measurements and adjustment for growth. In: Lai WW, Mertens LL, Cohen SC, Geva T, editors. Echocardiography in pediatric and congenital heart disease. West Sussex: Wiley-Blackwell; 2009. p. 52–62.Google Scholar
  45. 45.
    Dallaire F, Bigras JL, Prsa M, Dahdah N. Bias related to body mass index in pediatric echocardiographic z scores. Pediatr Cardiol. 2015;36(3):667–76.PubMedCrossRefGoogle Scholar
  46. 46.
    Bluemke DA, Kronmal RA, Lima JA, Liu K, Olson J, Burke GL, Folsom AR. The relationship of left ventricular mass and geometry to incident cardiovascular events: the mesa (multi-ethnic study of atherosclerosis) study. J Am Coll Cardiol. 2008;52(25):2148–55.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Brumback LC, Kronmal R, Heckbert SR, Ni H, Hundley WG, Lima JA, Bluemke DA. Body size adjustments for left ventricular mass by cardiovascular magnetic resonance and their impact on left ventricular hypertrophy classification. Int J Cardiovasc Imaging. 2010;26(4):459–68.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Chinali M, Emma F, Esposito C, Rinelli G, Franceschini A, Doyon A, Raimondi F, Pongiglione G, Schaefer F, Matteucci MC. Left ventricular mass indexing in infants, children, and adolescents: a simplified approach for the identification of left ventricular hypertrophy in clinical practice. J Pediatr. 2016;170:193–8.PubMedCrossRefGoogle Scholar
  49. 49.
    Foster BJ, Khoury PR, Kimball TR, Mackie AS, Mitsnefes M. New reference centiles for left ventricular mass relative to lean body mass in children. J Am Soc Echocardiogr. 2016;29(5):441–7. e442PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Choudhry S, Salter A, Cunningham TW, Levy PT, Nguyen HH, Wallendorf M, Singh GK, Johnson MC. Normative left ventricular m-mode echocardiographic values in preterm infants up to 2 kg. J Am Soc Echocardiogr. 2017;30(8):781–9. e784PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Kobayashi T, Fuse S, Sakamoto N, Mikami M, Ogawa S, Hamaoka K, Arakaki Y, Nakamura T, Nagasawa H, Kato T, Jibiki T, Iwashima S, Yamakawa M, Ohkubo T, Shimoyama S, Aso K, Sato S, Saji T. A new z score curve of the coronary arterial internal diameter using the lambda-mu-sigma method in a pediatric population. J Am Soc Echocardiogr. 2016;29(8):794–801. e729PubMedCrossRefGoogle Scholar
  52. 52.
    Sharland GK, Allan LD. Normal fetal cardiac measurements derived by cross-sectional echocardiography. Ultrasound Obstet Gynecol. 1992;2(3):175–81.PubMedCrossRefGoogle Scholar
  53. 53.
    Tan J, Silverman NH, Hoffman JI, Villegas M, Schmidt KG. Cardiac dimensions determined by cross-sectional echocardiography in the normal human fetus from 18 weeks to term. Am J Cardiol. 1992;70(18):1459–67.PubMedCrossRefGoogle Scholar
  54. 54.
    Shapiro I, Degani S, Leibovitz Z, Ohel G, Tal Y, Abinader EG. Fetal cardiac measurements derived by transvaginal and transabdominal cross-sectional echocardiography from 14 weeks of gestation to term. Ultrasound Obstet Gynecol. 1998;12(6):404–18.PubMedCrossRefGoogle Scholar
  55. 55.
    McElhinney DB, Marshall AC, Wilkins-Haug LE, Brown DW, Benson CB, Silva V, Marx GR, Mizrahi-Arnaud A, Lock JE, Tworetzky W. Predictors of technical success and postnatal biventricular outcome after in utero aortic valvuloplasty for aortic stenosis with evolving hypoplastic left heart syndrome. Circulation. 2009;120(15):1482–90.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Lara DA, Morris SA, Maskatia SA, Challman M, Nguyen M, Feagin DK, Schoppe L, Zhang J, Bhatt A, Sexson-Tejtel SK, Lopez KN, Lawrence EJ, Andreas S, Wang Y, Belfort MA, Ruano R, Ayres NA, Altman CA, Aagaard KM, Becker J. Pilot study of chronic maternal hyperoxygenation and effect on aortic and mitral valve annular dimensions in fetuses with left heart hypoplasia. Ultrasound Obstet Gynecol. 2016;48(3):365–72.PubMedCrossRefGoogle Scholar
  57. 57.
    Lorenz CH. The range of normal values of cardiovascular structures in infants, children, and adolescents measured by magnetic resonance imaging. Pediatr Cardiol. 2000;21(1):37–46.PubMedCrossRefGoogle Scholar
  58. 58.
    Lorenz CH, Walker ES, Morgan VL, Klein SS, Graham TP Jr. Normal human right and left ventricular mass, systolic function, and gender differences by cine magnetic resonance imaging. J Cardiovasc Magn Reson. 1999;1(1):7–21.PubMedCrossRefGoogle Scholar
  59. 59.
    Robbers-Visser D, Boersma E, Helbing WA. Normal biventricular function, volumes, and mass in children aged 8 to 17 years. J Magn Reson Imaging. 2009;29(3):552–9.PubMedCrossRefGoogle Scholar
  60. 60.
    Sarikouch S, Peters B, Gutberlet M, Leismann B, Kelter-Kloepping A, Koerperich H, Kuehne T, Beerbaum P. Sex-specific pediatric percentiles for ventricular size and mass as reference values for cardiac MRI: assessment by steady-state free-precession and phase-contrast mri flow. Circ Cardiovasc Imaging. 2010;3(1):65–76.PubMedCrossRefGoogle Scholar
  61. 61.
    Schmitz L, Koch H, Bein G, Brockmeier K. Left ventricular diastolic function in infants, children, and adolescents. Reference values and analysis of morphologic and physiologic determinants of echocardiographic doppler flow signals during growth and maturation. J Am Coll Cardiol. 1998;32(5):1441–8.PubMedCrossRefGoogle Scholar
  62. 62.
    Eidem BW, McMahon CJ, Cohen RR, Wu J, Finkelshteyn I, Kovalchin JP, Ayres NA, Bezold LI, O'Brian Smith E, Pignatelli RH. Impact of cardiac growth on doppler tissue imaging velocities: a study in healthy children. J Am Soc Echocardiogr. 2004;17(3):212–21.PubMedCrossRefGoogle Scholar
  63. 63.
    Cui W, Roberson DA, Chen Z, Madronero LF, Cuneo BF. Systolic and diastolic time intervals measured from doppler tissue imaging: normal values and z-score tables, and effects of age, heart rate, and body surface area. J Am Soc Echocardiogr. 2008;21(4):361–70.PubMedCrossRefGoogle Scholar
  64. 64.
    Roberson DA, Cui W. Right ventricular tei index in children: effect of method, age, body surface area, and heart rate. J Am Soc Echocardiogr. 2007;20(6):764–70.PubMedCrossRefGoogle Scholar
  65. 65.
    Roberson DA, Cui W, Chen Z, Madronero LF, Cuneo BF. Annular and septal doppler tissue imaging in children: normal z-score tables and effects of age, heart rate, and body surface area. J Am Soc Echocardiogr. 2007;20(11):1276–84.PubMedCrossRefGoogle Scholar
  66. 66.
    Harada K, Rice MJ, Shiota T, Ishii M, McDonald RW, Reller MD, Sahn DJ. Gestational age- and growth-related alterations in fetal right and left ventricular diastolic filling patterns. Am J Cardiol. 1997;79(2):173–7.PubMedCrossRefGoogle Scholar
  67. 67.
    Harada K, Suzuki T, Tamura M, Ito T, Shimada K, Takada G. Effect of aging from infancy to childhood on flow velocity patterns of pulmonary vein by doppler echocardiography. Am J Cardiol. 1996;77(2):221–4.PubMedCrossRefGoogle Scholar
  68. 68.
    Cantinotti M, Lopez L. Nomograms for blood flow and tissue doppler velocities to evaluate diastolic function in children: a critical review. J Am Soc Echocardiogr. 2013;26(2):126–41.PubMedCrossRefGoogle Scholar
  69. 69.
    Cantinotti M, Giordano R, Scalese M, Murzi B, Assanta N, Spadoni I, Crocetti M, Marotta M, Molinaro S, Kutty S, Iervasi G. Nomograms for mitral inflow doppler and tissue doppler velocities in caucasian children. J Cardiol. 2016;68(4):288–99.PubMedCrossRefGoogle Scholar
  70. 70.
    Dallaire F, Slorach C, Hui W, Sarkola T, Friedberg MK, Bradley T, Jaeggi E, Dragulescu A, Har RLH, Cherney DZI, Mertens L (2015) Reference values for pulse wave doppler and tissue doppler imaging in pediatric echocardiography. Circ Cardiovasc Imaging 8 (2):e002167. doi:10.002110.001161/CIRCIMAGING.002114.002167Google Scholar
  71. 71.
    Weidemann F, Eyskens B, Jamal F, Mertens L, Kowalski M, D'Hooge J, Bijnens B, Gewillig M, Rademakers F, Hatle L, Sutherland GR. Quantification of regional left and right ventricular radial and longitudinal function in healthy children using ultrasound-based strain rate and strain imaging. J Am Soc Echocardiogr. 2002;15(1):20–8.PubMedCrossRefGoogle Scholar
  72. 72.
    Marcus KA, Mavinkurve-Groothuis AM, Barends M, van Dijk A, Feuth T, de Korte C, Kapusta L. Reference values for myocardial two-dimensional strain echocardiography in a healthy pediatric and young adult cohort. J Am Soc Echocardiogr. 2011;24(6):625–36.PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Kaku K, Takeuchi M, Tsang W, Takigiku K, Yasukochi S, Patel AR, Mor-Avi V, Lang RM, Otsuji Y. Age-related normal range of left ventricular strain and torsion using three-dimensional speckle-tracking echocardiography. J Am Soc Echocardiogr. 2014;27(1):55–64.PubMedCrossRefGoogle Scholar
  74. 74.
    Al-Naami GH. Torsion of young hearts: a speckle tracking study of normal infants, children, and adolescents. Eur J Echocardiogr. 2010;11(10):853–62.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    Takahashi K, Al Naami G, Thompson R, Inage A, Mackie AS, Smallhorn JF. Normal rotational, torsion and untwisting data in children, adolescents and young adults. J Am Soc Echocardiogr. 2010;23(3):286–93.PubMedCrossRefGoogle Scholar
  76. 76.
    Sato Y, Maruyama A, Ichihashi K. Myocardial strain of the left ventricle in normal children. J Cardiol. 2012;60(2):145–9.PubMedCrossRefGoogle Scholar
  77. 77.
    Kutty S, Deatsman SL, Nugent ML, Russell D, Frommelt PC. Assessment of regional right ventricular velocities, strain, and displacement in normal children using velocity vector imaging. Echocardiography. 2008;25(3):294–307.PubMedCrossRefGoogle Scholar
  78. 78.
    Lorch SM, Ludomirsky A, Singh GK. Maturational and growth-related changes in left ventricular longitudinal strain and strain rate measured by two-dimensional speckle tracking echocardiography in healthy pediatric population. J Am Soc Echocardiogr. 2008;21(11):1207–15.PubMedCrossRefGoogle Scholar
  79. 79.
    Zhang L, Gao J, Xie M, Yin P, Liu W, Li Y, Klas B, Sun J, Balluz R, Ge S. Left ventricular three-dimensional global systolic strain by real-time three-dimensional speckle-tracking in children: feasibility, reproducibility, maturational changes, and normal ranges. J Am Soc Echocardiogr. 2013;26(8):853–9.PubMedCrossRefGoogle Scholar
  80. 80.
    Forsey J, Friedberg MK, Mertens L. Speckle tracking echocardiography in pediatric and congenital heart disease. Echocardiography. 2013;30(4):447–59.PubMedCrossRefGoogle Scholar
  81. 81.
    Cantinotti M, Kutty S, Giordano R, Assanta N, Murzi B, Crocetti M, Marotta M, Iervasi G. Review and status report of pediatric left ventricular systolic strain and strain rate nomograms. Heart Fail Rev. 2015;20(5):601–12.PubMedCrossRefGoogle Scholar
  82. 82.
    Dallaire F, Slorach C, Bradley T, Hui W, Sarkola T, Friedberg MK, Jaeggi E, Dragulescu A, Mahmud FH, Daneman D, Mertens L. Pediatric reference values and z score equations for left ventricular systolic strain measured by two-dimensional speckle-tracking echocardiography. J Am Soc Echocardiogr. 2016;29(8):786–93. e788PubMedCrossRefGoogle Scholar
  83. 83.
    Davignon A, Rautaharju P, Boisselle E, Soumis F, Megelas M, Choguette A. Normal ECG standards for infants and children. Pediatr Cardiol. 1979;1:123–31.CrossRefGoogle Scholar
  84. 84.
    Macfarlane PW, McLaughlin SC, Devine B, Yang TF. Effects of age, sex, and race on ecg interval measurements. J Electrocardiol. 1994;27(Suppl):14–9.PubMedCrossRefGoogle Scholar
  85. 85.
    Rijnbeek PR, Witsenburg M, Schrama E, Hess J, Kors JA. New normal limits for the paediatric electrocardiogram. Eur Heart J. 2001;22(8):702–11.PubMedCrossRefGoogle Scholar
  86. 86.
    Palhares DMF, Marcolino MS, Santos TMM, da Silva JLP, Gomes PR, Ribeiro LB, Macfarlane PW, Ribeiro ALP. Normal limits of the electrocardiogram derived from a large database of Brazilian primary care patients. BMC Cardiovasc Disord. 2017;17(1):152.Google Scholar
  87. 87.
    Pearl W. Effects of gender, age, and heart rate on qt intervals in children. Pediatr Cardiol. 1996;17(3):135–6.PubMedCrossRefGoogle Scholar
  88. 88.
    Mason JW, Ramseth DJ, Chanter DO, Moon TE, Goodman DB, Mendzelevski B. Electrocardiographic reference ranges derived from 79,743 ambulatory subjects. J Electrocardiol. 2007;40(3):228–34.PubMedCrossRefGoogle Scholar
  89. 89.
    Semizel E, Ozturk B, Bostan OM, Cil E, Ediz B. The effect of age and gender on the electrocardiogram in children. Cardiol Young. 2008;18(1):26–40.PubMedCrossRefGoogle Scholar
  90. 90.
    Silvetti MS, Drago F, Ragonese P. Heart rate variability in healthy children and adolescents is partially related to age and gender. Int J Cardiol. 2001;81(2-3):169–74.PubMedCrossRefGoogle Scholar
  91. 91.
    Rogowski MP, Guilkey JP, Stephens BR, Cole AS, Mahon AD. The influence of maturation on the oxygen uptake efficiency slope. Pediatr Exerc Sci. 2012;24(3):347–56.PubMedCrossRefGoogle Scholar
  92. 92.
    Wasserman K, Hensen JE, Sue DY, Stringer WW, Sietsema KE, Sun X-G, Whipp BJ. Normal values. In: Principles of exercise testing and interpretation : Including pathophysiology and clinical applications. 5th ed. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2012. p. 154–80.Google Scholar
  93. 93.
    Cooper DM, Weiler-Ravell D, Whipp BJ, Wasserman K. Aerobic parameters of exercise as a function of body size during growth in children. J Appl Physiol. 1984;56(3):628–34.PubMedCrossRefGoogle Scholar
  94. 94.
    Cooper DM, Weiler-Ravell D, Whipp BJ, Wasserman K. Growth-related changes in oxygen uptake and heart rate during progressive exercise in children. Pediatr Res. 1984;18(9):845–51.PubMedCrossRefGoogle Scholar
  95. 95.
    Ten Harkel AD, Takken T, Van Osch-Gevers M, Helbing WA. Normal values for cardiopulmonary exercise testing in children. Eur J Cardiovasc Prev Rehabil. 2011;18(1):48–54.PubMedCrossRefGoogle Scholar
  96. 96.
    Loftin M, Sothern M, Abe T, Bonis M. Expression of VO2 peak in children and youth, with special reference to allometric scaling. Sports Med. 2016;46(10):1451–60.PubMedCrossRefGoogle Scholar
  97. 97.
    Cooper DM, Weiler-Ravell D. Gas exchange response to exercise in children. Am Rev Respir Dis. 1984;129(2 Pt 2):S47–8.PubMedCrossRefGoogle Scholar
  98. 98.
    Wang X, Xu X, Su S, Snieder H. Familial aggregation and childhood blood pressure. Curr Hypertens Rep. 2015;17(1):509.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics. 2004;114(2 Suppl 4th Report):555–76.Google Scholar
  100. 100.
    Xi B, Zong X, Kelishadi R, Hong YM, Khadilkar A, Steffen LM, Nawarycz T, Krzywinska-Wiewiorowska M, Aounallah-Skhiri H, Bovet P, Chiolero A, Pan H, Litwin M, Poh BK, Sung RY, So HK, Schwandt P, Haas GM, Neuhauser HK, Marinov L, Galcheva SV, Motlagh ME, Kim HS, Khadilkar V, Krzyzaniak A, Romdhane HB, Heshmat R, Chiplonkar S, Stawinska-Witoszynska B, El Ati J, Qorbani M, Kajale N, Traissac P, Ostrowska-Nawarycz L, Ardalan G, Parthasarathy L, Zhao M, Zhang T. Establishing international blood pressure references among nonoverweight children and adolescents aged 6 to 17 years. Circulation. 2016;133(4):398–408.PubMedCrossRefGoogle Scholar
  101. 101.
    Wuhl E, Witte K, Soergel M, Mehls O, Schaefer F. Distribution of 24-h ambulatory blood pressure in children: normalized reference values and role of body dimensions. J Hypertens. 2002;20(10):1995–2007.PubMedCrossRefGoogle Scholar
  102. 102.
    Whincup PH, Nightingale CM, Owen CG, Rapala A, Bhowruth DJ, Prescott MH, Ellins EA, Donin AS, Masi S, Rudnicka AR, Sattar N, Cook DG, Deanfield JE. Ethnic differences in carotid intima-media thickness between UK children of black african-caribbean and white European origin. Stroke. 2012;43(7):1747–54.PubMedCrossRefGoogle Scholar
  103. 103.
    Chowdhury SM, Henshaw MH, Friedman B, Saul JP, Shirali GS, Carter J, Levitan BM, Hulsey T. Lean body mass may explain apparent racial differences in carotid intima-media thickness in obese children. J Am Soc Echocardiogr. 2014;27(5):561–7.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Yoo BW. Epidemiology of congenital heart disease in boys and girls. Adv Exp Med Biol. 2018;162:191–3.Google Scholar
  105. 105.
    Schaefer F, Doyon A, Azukaitis K, Bayazit A, Canpolat N, Duzova A, Niemirska A, Sozeri B, Thurn D, Anarat A, Ranchin B, Litwin M, Caliskan S, Candan C, Baskin E, Yilmaz E, Mir S, Kirchner M, Sander A, Haffner D, Melk A, Wuhl E, Shroff R, Querfeld U. Cardiovascular phenotypes in children with CKD: The 4c study. Clin J Am Soc Nephrol. 2017;12(1):19–28.PubMedCrossRefGoogle Scholar
  106. 106.
    Gao Z, Khoury PR, McCoy CE, Shah AS, Kimball TR, Dolan LM, Urbina EM. Adiposity has no direct effect on carotid intima-media thickness in adolescents and young adults: use of structural equation modeling to elucidate indirect & direct pathways. Atherosclerosis. 2016;246:29–35.PubMedCrossRefGoogle Scholar
  107. 107.
    Vatanen A, Sarkola T, Ojala TH, Turanlahti M, Jahnukainen T, Saarinen-Pihkala UM, Jahnukainen K. Radiotherapy-related arterial intima thickening and plaque formation in childhood cancer survivors detected with very-high resolution ultrasound during young adulthood. Pediatr Blood Cancer. 2015;62(11):2000–6.PubMedCrossRefGoogle Scholar
  108. 108.
    Litwin M, Niemirska A, Sladowska-Kozlowska J, Wierzbicka A, Janas R, Wawer ZT, Wisniewski A, Feber J. Regression of target organ damage in children and adolescents with primary hypertension. Pediatr Nephrol. 2010;25(12):2489–99.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Braamskamp M, Langslet G, McCrindle BW, Cassiman D, Francis GA, Gagne C, Gaudet D, Morrison KM, Wiegman A, Turner T, Miller E, Kusters DM, Raichlen JS, Martin PD, Stein EA, Kastelein JJP, Hutten BA. Effect of rosuvastatin on carotid intima-media thickness in children with heterozygous familial hypercholesterolemia: the Charon study (hypercholesterolemia in children and adolescents taking rosuvastatin open label). Circulation. 2017;136(4):359–66.Google Scholar
  110. 110.
    Cantinotti M, Giordano R, Scalese M, Murzi B, Assanta N, Spadoni I, Maura C, Marco M, Molinaro S, Kutty S, Iervasi G. Nomograms for two-dimensional echocardiography derived valvular and arterial dimensions in caucasian children. J Cardiol. 2017;69(1):208–15.PubMedCrossRefGoogle Scholar
  111. 111.
    Hashimoto I, Watanabe K, Ichida F. Right to left ventricular diameter ratio >/=0.42 is the warning flag for suspecting atrial septal defect in preschool children: age- and body surface area-related reference values determined by m-mode echocardiography. Pediatr Cardiol. 2016;37(4):704–13.PubMedCrossRefPubMedCentralGoogle Scholar
  112. 112.
    Koestenberger M, Burmas A, Ravekes W, Avian A, Gamillscheg A, Grangl G, Grillitsch M, Hansmann G. Echocardiographic reference values for right atrial size in children with and without atrial septal defects or pulmonary hypertension. Pediatr Cardiol. 2016;37(4):686–95.PubMedCrossRefGoogle Scholar
  113. 113.
    Koestenberger M, Nagel B, Ravekes W, Avian A, Burmas A, Grangl G, Cvirn G, Gamillscheg A. Reference values and calculation of z-scores of echocardiographic measurements of the normal pediatric right ventricle. Am J Cardiol. 2014;114(10):1590–8.PubMedCrossRefGoogle Scholar
  114. 114.
    Zhang YQ, Chen SB, Huang GY, Zhang HY, Huang MR, Wang SS, Wu LP, Hong WJ, Shen R, Liu YQ, Zhu JX, Lu ZH. Coronary artery indexed diameter and z score regression equations in healthy Chinese Han children. J Clin Ultrasound. 2015;43(1):39–46.Google Scholar
  115. 115.
    Laser KT, Houben BA, Korperich H, Haas NA, Kelter-Klopping A, Barth P, Burchert W, DallaPozza R, Kececioglu D, Herberg U. Calculation of pediatric left ventricular mass: validation and reference values using real-time three-dimensional echocardiography. J Am Soc Echocardiogr. 2015;28(3):275–83.PubMedCrossRefGoogle Scholar
  116. 116.
    Cantinotti M, Scalese M, Murzi B, Assanta N, Spadoni I, De Lucia V, Crocetti M, Cresti A, Gallotta M, Marotta M, Tyack K, Molinaro S, Iervasi G. Echocardiographic nomograms for chamber diameters and areas in Caucasian children. J Am Soc Echocardiogr. 2014;27(12):1279–92.CrossRefGoogle Scholar
  117. 117.
    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):159–64.PubMedCrossRefGoogle Scholar
  118. 118.
    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):922–34.PubMedCrossRefGoogle Scholar
  119. 119.
    Kaldararova M, Balazova E, Tittel P, Stankovicova I, Brucknerova I, Masura J. Echocardiographic measurements of the aorta in normal children and young adults. Bratisl Lek Listy. 2007;108(10-11):437–41.PubMedGoogle Scholar
  120. 120.
    Bonatto RC, Fioretto JR, Okoshi K, Matsubara BB, Padovani CR, Manfrin TC, Gobbi Mde F, Martino RS, Bregagnollo EA. Percentile curves of normal values of echocardiographic measurements in normal children from the central-southern region of the state of Sao Paulo, Brazil. Arq Bras Cardiol. 2006;87(6):711–21.Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Université de SherbrookeSherbrookeCanada
  2. 2.University of Helsinki, the Helsinki University Central Hospital/Children’s HospitalHelsinkiFinland

Personalised recommendations