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Ultraschall Med 2018; 39(04): 413-421
DOI: 10.1055/s-0043-111590
Original Article
© Georg Thieme Verlag KG Stuttgart · New York

Endocardial Fibroelastosis of the Left Ventricle Affects Right Ventricular Performance in Fetuses with Hypoplastic Left Heart Syndrome: A Prospective Study Using M-Mode, PW- and Tissue Doppler Techniques

Auswirkungen einer linksventrikulären Endokardfibroelastose auf die Funktion des rechten Ventrikels bei Feten mit hypoplastischem Linksherzsyndrom: Eine prospektive Untersuchung mittels M-Mode, PW-Doppler und PW-TDI.
Oliver Graupner
1   Department of Obstetrics and Gynecology, Klinikum rechts der Isar, Technical University of Munich, Germany
,
Christian Enzensberger
2   Division of Prenatal Medicine, Department of Obstetrics and Gynecology, Justus-Liebig-University and UKGM, Giessen, Germany
,
Larissa Wieg
3   Department of Cardiology, Klinikum rechts der Isar, Technical University of Munich, Germany
,
Jan Degenhardt
2   Division of Prenatal Medicine, Department of Obstetrics and Gynecology, Justus-Liebig-University and UKGM, Giessen, Germany
,
Aline Wolter
2   Division of Prenatal Medicine, Department of Obstetrics and Gynecology, Justus-Liebig-University and UKGM, Giessen, Germany
,
Markus Khalil
4   Department of Paediatric Cardiology, Justus-Liebig-University and UKGM, Giessen, Germany
,
Dietmar Schranz
5   Paediatric Cardiology, Children's Hospital Giessen, Giessen, Germany
,
Can Yerebakan
6   Cardiovascular Surgery, Children’s National Heart Institute, George Washington University Medical Center, Washington, DC, USA
,
Astrid Doelle
7   Ultrasound, Toshiba Medical Systems, Neuss, Germany
,
Johannes Herrmann
8   IT Service Center, Statistical Consulting Service Unit, Justus-Liebig-University Giessen, Germany
,
Roland Axt-Fliedner
2   Division of Prenatal Medicine, Department of Obstetrics and Gynecology, Justus-Liebig-University and UKGM, Giessen, Germany
› Author Affiliations
Further Information

Publication History

16 October 2016

12 April 2017

Publication Date:
06 July 2017 (online)

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Abstract

Purpose Myocardial function (MF) of the systemic right ventricle (RV) influences the postnatal course of neonates with hypoplastic left heart syndrome (HLHS). Our study examines whether the presence of endocardial fibroelastosis of the left ventricle (LV EFE) influences MF of the RV in HLHS fetuses.

Materials and Methods A prospective study was conducted including 10 controls (group 1), 10 HLHS fetuses with (group 2) and 10 without LV EFE (group 3) – all matched for gestational age. M-mode was used to assess tricuspid plane systolic excursion (TAPSE) and the shortening fraction (SF). PW-Doppler-derived and PW-TDI-derived velocities were assessed. E/A, E/e', e'/a' ratios and the myocardial performance index (mpi’) were calculated.

Results The examination of MF revealed significantly lower s’ velocities (p < 0.05) and higher values for SF in group 2 compared to group 3. e’/a’ ratio, et’ (ejection time), E wave velocity, E/e’ and SF showed significantly higher values in group 2 compared to group 1. In group 2 a’ velocity increased significantly over gestational age. In group 3 but not in group 2, TAPSE increased during gestation.

Conclusion These significant differences in MF between the groups might lend support to the notion of negative ventricular-ventricular interaction in the case of HLHS with LV EFE possibly influencing surgical outcomes.

Zusammenfassung

Ziel Das Outcome von Kindern mit hypoplastischem Linksherzsyndrom (HLHS) wird durch die Myokardfunktion (MF) des rechten Ventrikels beeinflusst. Das Vorliegen einer Endokardfibroelastose im Bereich des linken Ventrikels (LV EFE) kann Auswirkungen auf die MF des rechten Ventrikels haben. Ziel dieser Untersuchung war es, mögliche Unterschiede in der rechtsventrikulären MF von HLHS-Feten mit und ohne LV EFE aufzuzeigen.

Material und Methode Das Patientenkollektiv dieser prospektiven Studie besteht aus 10 gesunden Kontrollfeten (Gruppe 1), 10 HLHS-Feten mit (Gruppe 2) und ohne LV EFE (Gruppe 3). Alle Gruppen wurden in Bezug auf das Schwangerschaftsalter gematched. Die systolische Trikuspidalklappenringauslenkung (TAPSE) und die Verkürzungsfraktion (SF) wurden mittels M-Mode bestimmt. Systolische und diastolische Geschwindigkeiten wurden mittels PW-Doppler und PW-TDI bestimmt. Anschließend wurden die E/A-, die e ́/a ́-, die E/e ́-Ratio sowie der Myokardiale Perfomance Index (mpi’) berechnet.

Ergebnisse Die Untersuchung der MF ergab signifikant niedrigere s’-Geschwindigkeiten (p < 0,05) und höhere Werte für die SF in Gruppe 2 verglichen mit Gruppe 3. Die e ́/a ́- Ratio, die Ejektionszeit (et ́), die E-Geschwindigkeit sowie die E/e’- Ratio und die SF zeigten signifikant höhere Werte in Gruppe 2 im Vergleich zur Gruppe 1. Die a ́-Geschwindigkeit zeigte in Gruppe 2 einen signifikanten Anstieg mit zunehmendem Schwangerschaftsalter. In Gruppe 3 nicht aber in Gruppe 2 kam es zu einem signifikanten Anstieg der TAPSE im Laufe der Schwangerschaft.

Schlussfolgerung Die beobachteten Unterschiede in der MF zwischen den Gruppen können als Zeichen der eingeschränkten ventrikulären Interaktion bei HLHS-Feten mit LV EFE verstanden werden. Dies hat möglicherweise einen Einfluss auf das chirurgische Outcome betroffener HLHS-Kinder.

Key Words

hypoplastic left heart syndrome - fetal cardiac function - tissue Doppler imaging

Ergänzendes Material/Supplementary material

 

  • References

  • 1 Allan LD, Sharland GK, Milburn A. et al. Prospective diagnosis of 1006 consecutive cases of congenital heart disease in the fetus. J Am Coll Cardiol 1994; 23: 1452-1458
    CrossrefPubMedGoogle Scholar
  • 2 Hoffman JIE. Incidence of congenital heart disease: II. Prenatal incidence. Pediatr Cardiol 1995; 16: 155-165
    PubMedGoogle Scholar
  • 3 Hoffman JIE, Kaplan S. The incidence of congenital heart disease. J Am Coll Cardiol 2002; 39: 1890-1900
    CrossrefPubMedGoogle Scholar
  • 4 Ferencz C, Rubin JD, McCarter RJ. et al. Congenital heart disease: prevalence at livebirth. The Baltimore-Washington infant study. Am J Epidemiol 1985; 121: 31-36
    CrossrefPubMedGoogle Scholar
  • 5 Fyler DC, Buckley LP, Hellenbrand WE. et al. Report of the New England Regional Infant Cardiac care Program. Pediatrics 1980; 65: 375-461
    PubMedGoogle Scholar
  • 6 Freedom RM. Atresia or hypoplasia of the left atrioventricular and/or ventriculoarterial junction. In: Anderson RH, McCartney FJ, Shinebourne EA. et al. eds Paediatric Cardiology. Vol. 2. Edinburgh, London, Melbourne, New York: Churchill, Livingstone; 1987: 737-765
    Google Scholar
  • 7 Allan LD, Anderson RH, Cook AC. Atresia or absence of the left-sided atrioventricular connection in the fetus: echocardiographic diagnosis and outcome. Ultrasound Obstet Gynecol 1996; 8: 295-302
    CrossrefPubMedGoogle Scholar
  • 8 Axt-Fliedner R, Enzensberger C, Fass N. et al. Fetal diagnosis of hypoplastic left heart, associations and outcomes in the current era. Ultraschall in Med 2012; 33: E51-E56
    Article in Thieme ConnectPubMedGoogle Scholar
  • 9 Sellers FJ, Keith JD, Manning JA. The diagnosis of primary endocardial fibroelastosis. Circulation 1964; 29: 49-59
    CrossrefPubMedGoogle Scholar
  • 10 Moller JH, Lucas Jr RV, Adams Jr P. et al. Endocardial fibroelastosis. A clinical and anatomic study of 47 patients with emphasis on its relationship to mitral insufficiency. Circulation 1964; 30: 759-782
    CrossrefPubMedGoogle Scholar
  • 11 Ni J, Bowles NE, Kim YH. et al. Viral infection of the myocardium in endocardial fibroelastosis: molecular evidence . Circulation 1997; 95: 133-139
    CrossrefPubMedGoogle Scholar
  • 12 Dincsoy MY, Dincsoy HP, Kessler AD. et al. Generalized glycogenosis and associated endocardial fibroelastosis. Report of 3 cases with biochemical studies. The Journal of Pediatrics 1965; 67: 728-740
    CrossrefPubMedGoogle Scholar
  • 13 Andersen DH, Kelly J. Endocardial fibroelastosis. I. Endocardial fibro-elastosis associated with congenital malformations of the heart. Pediatrics 1956; 18: 513-538
    PubMedGoogle Scholar
  • 14 Ursell PC, Neill CA, Anderson RH. et al. Endocardial fibroelastosis and hypoplasia of the left ventricle in neonates without significant aortic stenosis. British Heart Journal 1984; 51: 492-497
    CrossrefPubMedGoogle Scholar
  • 15 Sharland GK, Chita SK, Fagg NLK. et al. Left ventricular dysfunction in the fetus: Relation to aortic valve anomalies and endocardial fibroelastosis. Br Heart J 1991; 66: 419
    CrossrefPubMedGoogle Scholar
  • 16 Natarajan S, Szwast A, Tian Z. et al. Right ventricular mechanics in the fetus with hypoplastic left heart syndrome. J Am Soc Echocardiogr 2013; 26: 515-520
    CrossrefPubMedGoogle Scholar
  • 17 Axt-Fliedner R, Tenzer A, Kawecki A. et al. Prenatal assessment of ventriculocoronary connections and ventricular endocardial fibroelastosis in hypoplastic left heart. Ultraschall in Med 2014; 35: 357-363
    Article in Thieme ConnectPubMedGoogle Scholar
  • 18 Szwast A, Tian Z, McCann M. et al. Right ventricular performance in the fetus with hypoplastic left heart syndrome. Ann Thorac Surg 2009; 87: 1214-1219
    CrossrefPubMedGoogle Scholar
  • 19 Kaltman JR, Di H, Tian Z. et al. Impact of congenital heart disease on cerebrovascular blood flow dynamics in the fetus. Ultrasound Obstet Gynecol 2005; 25: 32-36
    CrossrefPubMedGoogle Scholar
  • 20 Donofrio MT, Bremer YA, Schieken RM. et al. Autoregulation of cerebral blood flow in the fetus with congential heart disease: the brain sparing effect. Pediatr Cardiol 2003; 24: 436-443
    CrossrefPubMedGoogle Scholar
  • 21 Miller SP, McQuillen PS, Hamrick S. et al. Abnormal brain development in newborns with congenital heart disease. N Engl J Med 2007; 357: 1928-1938
    CrossrefPubMedGoogle Scholar
  • 22 Brooks PA, Khoo NS, Mackie AS. et al. Right ventricular function in fetal hypoplastic left heart syndrome. J Am Soc Echocardiogr 2012; 25: 1068-1074
    CrossrefPubMedGoogle Scholar
  • 23 Axt-Fliedner R, Graupner O, Kawecki A. et al. Fetal Cardiac Imaging Research Group, Germany. Evaluation of right ventricular function in fetuses with hypoplastic left heart syndrome using tissue Doppler techniques. Ultrasound Obstet Gynecol 2015; 45: 670-677
    CrossrefPubMedGoogle Scholar
  • 24 Graupner O, Enzensberger C, Wieg L. et al. Evaluation of right ventricular function in fetal hypoplastic left heart syndrome by colour tissue Doppler imaging. Ultrasound Obstet Gynecol 2016; 47: 732-738
    CrossrefPubMedGoogle Scholar
  • 25 Furck AK, Uebing A, Hansen JH. et al. Outcome of the norwood operation in patients with hypoplastic left heart syndrome: a 12 year single-center survey. J Thorac Cardiovasc Surg 2010; 139: 359-365
    CrossrefPubMedGoogle Scholar
  • 26 Sugiyama H, Yutani C, Iida K. et al. The relation between right ventricular function and left ventricular morphology in hypoplastic left heart syndrome: angiographic and pathological studies. Pediatr Cardiol 1999; 20: 422-427
    CrossrefPubMedGoogle Scholar
  • 27 McElhinney DB, Vogel M, Benson CB. et al. Assessment of left ventricular endocardial fibroelastosis in fetuses with aortic stenosis and evolving hypoplastic left heart syndrome. Am J Cardiol 2010; 106: 1792-1797
    CrossrefPubMedGoogle Scholar
  • 28 Schneider C, McCrindle BW, Carvalho JS. et al. Development of Z-scores for fetal cardiac dimensions from echocardiography. Ultrasound Obstet Gynecol 2005; 26: 599-605
    CrossrefPubMedGoogle Scholar
  • 29 Nagueh SF, Middleton KJ, Kopelen HA. et al. Doppler tissue imaging: a non invasive technique for evaluation of left ventricular relaxation and estimation of filling pressures. J am Coll Cardiol 1997; 30: 1527-1533
    CrossrefPubMedGoogle Scholar
  • 30 Sohn DW, Chai IH, Lee DJ. et al. Assessment of mitral annulus velocity by Doppler tissue imaging in the evaluation of left ventricular diastolic function. J Am Coll Cardiol 1997; 30: 474-480
    CrossrefPubMedGoogle Scholar
  • 31 Ommen SR, Nishimura RA, Appleton CP. et al. Clinical utility of Doppler echocardiography and tissue Doppler imaging in the estimation of left ventricular filling pressures: A comparative simultaneous Doppler-cathererization study. Circulation 2000; 102: 1788-1794
    CrossrefPubMedGoogle Scholar
  • 32 Tei C, Nishimura RA, Seward JB. et al. Noninvasive Doppler-derived myocardial performance index: correlation with simultaneous measurements of cardiac catheterization measurements. J Am Soc Echocardiogr 1997; 10: 169-178
    CrossrefPubMedGoogle Scholar
  • 33 Godfrey ME, Messing B, Cohen SM. et al. Functional assessment of the fetal heart: a review. Ultrasound Obstet Gynecol 2012; 39: 131-144
    CrossrefPubMedGoogle Scholar
  • 34 Comas M, Crispi F, Cruz-Martinez R. et al. Usefulness of myocardial tissue Doppler vs conventional echocardiography in the evaluation of cardiac dysfunction in early-onset intrauterine growth restriction. Am J Obstet Gynecol 2010; 203: 45e41-47
    PubMedGoogle Scholar
  • 35 Carvalho JS, O´Sullivan C, Shinebourne EA. et al. Right and left ventricular long-axis function in the fetus using angular M-Mode. Ultrasound Obstet Gynecol 2001; 18: 619-622
    CrossrefPubMedGoogle Scholar
  • 36 DeVore GR. Assessing fetal cardiac ventricular function. Semin Fetal Neonatal Med 2005; 10: 515-541
    CrossrefPubMedGoogle Scholar
  • 37 DeVore GR, Siassi B, Platt LD. Fetal echocardiography. IV. M-mode assessment of ventricular size and contractility during the second and third trimesters of pregnancy in the normal fetus. Am J Obstet Gynecol 1984; 150: 981-988
    CrossrefPubMedGoogle Scholar
  • 38 Enzensberger C, Tenzer A, Degenhardt J. et al. Assessment of fetal cardiac function-established and novel methods. Z Geburtshilfe Neonatol 2014; 218: 56-63
    Article in Thieme ConnectPubMedGoogle Scholar
  • 39 Hsieh YY, Chang FC, Tsai HD. et al. Longitudinal survey of fetal ventricular ejection and shortening fraction throughout pregnancy. Ultrasound Obstet Gynecol 2000; 16: 46-48
    PubMedGoogle Scholar
  • 40 Park YS, Park JH, Ahn KT. et al. Usefulness of mitral annular systolic velocity in the detection of left ventricular systolic dysfunction: comparison with three dimensional echocardiographic data. J Cardiovasc Ultrasound 2010; 18: 1-5
    CrossrefPubMedGoogle Scholar
  • 41 Watanabe S, Hashimoto I, Saito K. et al. Characterization of ventricular myocardial performance in the fetus by tissue Doppler imaging. Circ J 2009; 73: 943-947
    CrossrefPubMedGoogle Scholar
  • 42 Pettersen E, Helle-Valle T, Edvardsen T. et al. Contraction pattern of the systemic right ventricle shift from longitudinal to circumferential shortening and absent global ventricular torsion. J Am Coll Cardiol 2007; 49 (25) 2450-2456
    CrossrefPubMedGoogle Scholar
  • 43 Clur SA, van der Wal AC, Ottenkamp J. et al. Echocardiographic evaluation of fetal cardiac function: clinical and anatomical correlations in two cases of endocardial fibroelastosis. Fetal Diagn Ther 2010; 28: 51-57
    CrossrefPubMedGoogle Scholar
  • 44 Vorisek C, Shimada S, Axt-Fliedner R. et al. Inhibition of endocardial fibroelastosis in unborn children with hypoplastic left heart in the cell culture model. Z Geburtshilfe Neonatol 2015; 219-P08_7
    PubMedGoogle Scholar
  • 45 Schranz D, Bauer A, Reich B. et al. Fifteen-year single center experience with the "Giessen Hybrid" approach for hypoplastic left heart and variants: current strategies and outcomes. Pediatr Cardiol 2015; 36: 365-373
    CrossrefPubMedGoogle Scholar
  • 46 Yerebakan C, Murray J, Valeske K. et al. Long-term results of biventricular repair after initial Giessen hybrid approach for hypoplastic left heart variants. J Thorac Cardiovasc Surg 2015; 149: 1112-1120
    CrossrefPubMedGoogle Scholar
  • 47 Husain N, Gokhale J, Nicholson L. et al. Noninvasive estimation of ventricular filling pressures in patients with single right ventricles. J Am Soc Echocardiogr 2013; 26: 1330-1336
    CrossrefPubMedGoogle Scholar
  • 48 Bellsham-Revell HR, Tibby SM, Bell AJ. et al. Tissue Doppler time intervals and derived indices in hypoplastic left heart syndrome. Eur Heart J Cardiovasc Imaging 2012; 13: 400-407
    CrossrefPubMedGoogle Scholar
  • 49 Menon SC, Gray R, Tani LY. Evaluation of ventricular filling pressures and ventricular function by Doppler echocardiography in patients with functional single ventricle: correlation with simultaneous cardiac catheterization. J Am Soc Echocardiogr 2011; 24: 1220-1225
    CrossrefPubMedGoogle Scholar
  • 50 Yu CM, Fung JW, Zhang Q. et al. Tissue Doppler echocardiographic evidence of atrial mechanical dysfunction in coronary artery disease. Int J Cardiol 2005; 105: 178-185
    CrossrefPubMedGoogle Scholar
  • 51 Hernandez-Andrade E, Benavides-Serralde JA, Cruz-Martinez R. et al. Evaluation of conventional Doppler fetal cardiac function parameters: E/A ratios, outflow tracts, and myocardial performance index. Fetal Diagn Ther 2012; 32: 22-29
    CrossrefPubMedGoogle Scholar
  • 52 Rojo EC, Rodrigo JL, Pérez de Isla L. et al. Disagreement between tissue Doppler imaging and conventional pulsed wave Doppler in the measurement of myocardial performance index. Eur J Echocardiogr 2006; 7: 356-364
    CrossrefPubMedGoogle Scholar
  • 53 Bijnens B, Cikes M, Butakoff C. et al. Myocardial motion and deformation: What does it tell us and how does it relate to function?. Fetal Diagn Ther 2012; 32: 5-16
    CrossrefPubMedGoogle Scholar