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Eduard Gratacós a Fàtima Crispi a
a FetalMedicine Research Center, BCNatal – Barcelona Center for Maternal-Fetal and Neonatal Medicine
(Hospital Clínic and Hospital Sant Joan de Deu), Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS),
Universitat de Barcelona, and Centre for Biomedical Research on Rare Diseases (CIBER-ER), Barcelona, Spain;
b Pontificia Universidad Javeriana seccional Cali, Cali, Colombia; c Fetal Medicine Unit, Department of Obstetrics and
2D ultrasound
Tan et al. [29] 1992 Retrospective 100 Volunteer healthcare 18–40 Basal and longitudinal ventricular Different cardiac views depending on End-diastole
professionals diameters the measurement
Myocardial wall thicknesses End-systole
Atria width and length
Sharland et al. [31] 1992 Retrospective 100–337 High-risk pregnancies 16–40 Ventricular width (n = 337) Measurement below coapted End-diastole
(referred for fetal Longitudinal ventricular diameters atrioventricular valves
echocardiogram) (n = 100)
Shapiro et al. [12] 1998 637 Women at routine 14–40 Basal ventricular diameters Measured below the atrioventricular End-diastole Irregular volume of data
sonographic examination Atrial transverse diameters valves Maximal dilatation depending on GA (scarce
data over 28 weeks)
DOI: 10.1159/000494838
disease Atria width and length long-axis view and short-axis view)
Schneider et al. [13] 2005 Retrospective 130 High-risk pregnancies 15–39 Tricuspid and mitral valve Diastole Ventricular measurements
(referred for a fetal Ventricular inlet length not performed at end-
echocardiogram) Ventricular basal diameters diastole (atrioventricular
Ventricular area valves opened)
Chanthasenanont 2008 480 Pregnant women who 16–39 Left ventricular dimensions Diastole
et al. [34] routinely attended the Left and septal myocardial wall Diastole (left), systole
antenatal clinic thicknesses (right)
Lee et al. [32] 2010 Retrospective 2,735 Database of routine scans 17–41 Ventricular basal diameters Z-scores using menstrual age, BPD, End-diastole Study population initially
cross-sectional and FL as independent variables derived from a database
Li et al. [17] 2015 Cross-sectional 809 11–40 Transverse heart diameter End-diastole Exclusively Chinese
Heart length population
Heart circumference
Heart area
Gu et al. [15] 2016 Cross-sectional 4,396 20–34 Transverse cardiac diameter Below coapted atrioventricular valves End-diastole and Exclusively Chinese
Ventricular basal diameters end-systole population
Atrial transverse diameters
M-mode ultrasound
Allan et al. [3] 1981 Retrospective 178 18–40 Left and septal myocardial wall Short-axis view Not specified
thicknesses
Patchakapat et al. [35] 2006 410 Pregnant women who 32–35.6 Interventricular septal thickness Diastole and systole Exclusively Thai population
routinely attended the clinic
Gagnon et al. [16] 2016 Retrospective 104 High-risk pregnancies 18–39 Basal ventricular diameters Short-axis or 4-chamber view End-diastole and
(referred for a fetal end-systole
echocardiogram)
García-Otero et al.
GA, gestational age; BPD, biparietal diameter; FL, femur length.
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LCD
CA
MB
LV RV
LV RV
LATD
LA RA
TCD FO
LAA RAA
PV PV
FO PV
PV RALD RATD
a FO b LALD
LVWT
LVLD MB
RVLD
LV LV
LV RV SWT
LV RV LVMTD RVMTD RV
RV
d
RVWT
LVBD RVBD
PV
PV
c FO
Fig. 1. Fetal echocardiographic images illustrating the measure- area; RATD, left atrial transverse diameter; RALD, right atrial lon-
ment of cardiac diameters and area (a), atrial diameters and areas gitudinal diameter; RAA, right atrial area; LVBD, left ventricle bas-
(b), ventricular diameters and areas (c), and myocardial wall thick- al diameter; LVMTD, left ventricle midtransverse diameter; LVLD,
nesses (d). LV, left ventricle; RV, right ventricle; PV, pulmonary left ventricle longitudinal diameter; RVBD, right ventricle basal
veins; FO, fossa ovalis; MB, moderator band; TCD, transverse car- diameter; RVMTD, right ventricle midtransverse diameter; RVLD,
diac diameter; LCD, longitudinal cardiac diameter; CA, cardiac right ventricle longitudinal diameter; LVWT, left ventricular wall
area; LA, left atria; RA, right atria; LATD, left atrial transverse di- thickness; RVWT, right ventricle wall thickness; SWT, septal wall
ameter; LALD, left atrial longitudinal diameter; LAA, left atrial thickness.
The concept of cardiac remodeling – defined as chang- based on a selected high-risk population undergoing
es in size, shape, structure, and function of the heart in clinically prescribed echocardiography [12–14] (Table
order to adapt to an insult [4] – is now being applied in 1). Furthermore, the proposed methodology to assess
fetal life not only in CHD cases [5] but also in other pre- fetal cardiac dimensions frequently varied within and
natal conditions, such as fetal growth restriction (FGR) across studies, from 2D [15] to M-mode [16] with dis-
[6], the use of assisted reproductive techniques (ART) [7], similar cardiac views (transverse [17] vs. apical/basal
exposure to toxics [8], and pregestational diabetes [9]. An [13]) and moment of the cardiac cycle (at different points
adverse prenatal environment during the crucial period of the diastole in case of ventricular dimensions and
of in utero development might have a direct impact on without considering the closure of the AV valve as a land-
fetal cardiac structure and long-lasting consequences on mark to define the end-diastole [13, 15]), highlighting
health [10]. The use of echocardiography during fetal life the need for a well-defined methodology using stringent
enables the early identification of subtle or minor chang- criteria.
es in cardiac morphometry potentially useful for fetal The objective of the present study was to provide high-
monitoring and the prevention of cardiovascular conse- quality fetal cardiac dimension nomograms using a strin-
quences [11]. gent methodology on a low-risk population of fetuses
However, there is a lack of standardized reference val- throughout pregnancy. For that purpose, we specifically
ues for many cardiac morphometric parameters in fetal created a prospective cohort of low-risk singleton preg-
life. Most nomogram studies were performed in the 80s nancies from the 18th to the 41st weeks of gestational age
using relatively low-resolution equipment and usually (GA) to undergo comprehensive fetal echocardiography.
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Parameter Mean SD
c GA, weeks
Fig. 2. Scatterplots of the cardiac transverse (a) and longitudinal diameters (b) and cardiac area (c) plotted against
GA in the study population. Estimated 5th, 50th, and 95th centile curves are shown.
Fig. 3. Scatterplots of the left atrial transverse (a) and longitudinal diameters (b), left atrial area (c), right atrial
transverse (d) and longitudinal diameters (e), and right atrial area (f) plotted against GA in the study population.
Estimated 5th, 50th, and 95th centile curves are shown.
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Fig. 4. Scatterplots of the left ventricular basal (a), midtransverse (b), and longitudinal (c) diameters, the left ven-
tricular end-diastolic area (d), the right ventricular basal (e), midtransverse (f), and longitudinal diameters (g),
and the right ventricular end-diastolic area (h) plotted against GA in the study population. Estimated 5th, 50th,
and 95th centile curves are shown.
(Figure continued on next page.)
creased quadratically with GA, while their SD showed a whole-heart dimensions is relevant for describing cardio-
linear progression. These nomograms are mostly concor- megaly or cardiac compression.
dant with previously published data [17, 25]. Most previ-
ous studies coincide on the methodology for measuring Atrial Dimensions
cardiac area and longitudinal diameter but with a dissim- We have provided nomograms for fetal atrial diame-
ilar methodology for transverse diameters. While some ters and areas throughout pregnancy. Even though the
authors measured the transverse cardiac diameter at the accurate performance of this measurement could be chal-
level of atrioventricular valves [17, 26–28], we and others lenging [14], we showed high feasibility and reproducibil-
propose to measure it below the atrioventricular valves ity. Our results are in agreement with most previous data
[25] as it better corresponds to the mid-cardiac length [12, 14, 29], with slightly smaller longitudinal atrial diam-
reaching the maximal transverse diameter. These differ- eters than previously reported [14, 29], most likely ex-
ences in methodology may justify our values to be slight- plained by the inclusion of the atrioventricular valve an-
ly smaller than previously reported [17]. Assessment of nulus in other studies [29]. This is the first report on fetal
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atrial area normal values. Evaluation of atrial dimensions formed just below the atrioventricular valve instead of at
might be particularly relevant when studying cases with the level of the annulus, as recommended [22]. An accu-
volume or pressure overload – as atrial dilatation readily rate evaluation of ventricular dimensions is the key to de-
occurs in response to these insults due to the absence of scribing and monitoring ventricular remodeling.
muscular fibers and its hypertrophy inability.
Myocardial Wall Thicknesses
Ventricular Dimensions Finally, normal values for septal and lateral myocar-
Ventricular diameters and areas were rigorously mea- dial wall thicknesses are also reported both in 2D (main
sured demonstrating a high feasibility and reproducibili- document) and M-mode (online suppl. material), show-
ty, as previously reported [30]. Methodological variability ing a progressive increase throughout gestation with ex-
for measuring ventricular dimensions among previous cellent feasibility and consistency with previous studies,
studies, using different cardiac views and points of refer- although methodological heterogeneity used in previous
ence throughout the diastolic phase, limits the compari- studies [16, 29, 33–35] hampers the direct comparison of
son of data [12, 13, 29, 31, 32] even though they are most- results. An accurate measurement of ventricular wall
ly consistent. The only exception comes from Shapiro et thicknesses is essential to assess myocardial hypertrophy
al. [12], who reported slightly smaller ventricular basal di- as a common response to pressure/volume overload or
ameters, most likely due to the measurement being per- toxicity.
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c GA, weeks
Fig. 5. Scatterplots of the left (a), right (b), and septal (c) wall thicknesses plotted against GA in the study popu-
lation. Estimated 5th, 50th, and 95th centile curves are shown.
References
1 Kleinman CS, Hobbins JC, Jaffe CC, Lynch 11 Rodriguez-Lopez M, Osorio L, Acosta-Rojas 19 Hadlock FP, Shah YP, Kanon DJ, Lindsey JV.
DC, Talner NS. Echocardiographic studies of R, Figueras J, Cruz-Lemini M, Figueras F, et Fetal crown-rump length: reevaluation of re-
the human fetus: prenatal diagnosis of con- al. Influence of breastfeeding and postnatal lation to menstrual age (5-18 weeks) with
genital heart disease and cardiac dysrhyth- nutrition on cardiovascular remodeling in- high-resolution real-time US. Radiology.
mias. Pediatrics. 1980 Jun;65(6):1059–67. duced by fetal growth restriction. Pediatr Res. 1992 Feb;182(2):501–5.
2 Crawford CS. Antenatal diagnosis of fetal car- 2016 Jan;79(1-1):100–6. 20 Carvalho JS, Allan LD, Chaoui R, Copel JA,
diac abnormalities. Ann Clin Lab Sci. 1982 12 Shapiro I, Degani S, Leibovitz Z, Ohel G, Tal DeVore GR, Hecher K, et al.; International
Mar-Apr;12(2):99–105. Y, Abinader EG. Fetal cardiac measurements Society of Ultrasound in Obstetrics and Gy-
3 Allan LD, Tynan M, Campbell S, Anderson derived by transvaginal and transabdominal necology. ISUOG Practice Guidelines (updat-
RH. Normal fetal cardiac anatomy—a basis cross-sectional echocardiography from 14 ed): sonographic screening examination of
for the echocardiographic detection of abnor- weeks of gestation to term. Ultrasound Obstet the fetal heart. Ultrasound Obstet Gynecol.
malities. Prenat Diagn. 1981 Apr;1(2):131–9. Gynecol. 1998 Dec;12(6):404–18. 2013 Mar;41(3):348–59.
4 Opie LH, Commerford PJ, Gersh BJ, Pfeffer 13 Schneider C, McCrindle BW, Carvalho JS, 21 Lopez L, Colan SD, Frommelt PC, Ensing GJ,
MA. Controversies in ventricular remodel- Hornberger LK, McCarthy KP, Daubeney PE. Kendall K, Younoszai AK, et al. Recommen-
ling. Lancet. 2006 Jan;367(9507):356–67. Development of Z-scores for fetal cardiac dations for quantification methods during the
5 Guirado L, Crispi F, Masoller N, Bennasar M, dimensions from echocardiography. Ultra- performance of a pediatric echocardiogram:
Marimon E, Carretero J, et al. Biventricular sound Obstet Gynecol. 2005 Nov; 26(6): 599– a report from the Pediatric Measurements
impact of mild to moderate fetal pulmonary 605. Writing Group of the American Society of
valve stenosis. Ultrasound Obstet Gynecol. 14 Firpo C, Hoffman JI, Silverman NH. Evalua- Echocardiography Pediatric and Congenital
2018 Mar;51(3):349–56. tion of fetal heart dimensions from 12 weeks Heart Disease Council. J Am Soc Echocar-
6 Crispi F, Bijnens B, Figueras F, Bartrons J, to term. Am J Cardiol. 2001 Mar; 87(5): 594– diogr. 2010 May;23(5):465–95.
Eixarch E, Le Noble F, et al. Fetal growth re- 600. 22 Lang RM, Badano LP, Mor-Avi V, Afilalo J,
striction results in remodeled and less effi- 15 Gu X, He Y, Zhang Y, Sun L, Zhao Y, Han J, Armstrong A, Ernande L, et al. Recommenda-
cient hearts in children. Circulation. 2010 et al. Fetal echocardiography: reference values tions for cardiac chamber quantification by
Jun;121(22):2427–36. for the Chinese population. J Perinat Med. echocardiography in adults: an update from
7 Valenzuela-Alcaraz B, Crispi F, Bijnens B, 2017 Feb;45(2):171–9. the American Society of Echocardiography
Cruz-Lemini M, Creus M, Sitges M, et al. As- 16 Gagnon C, Bigras JL, Fouron JC, Dallaire F. and the European Association of Cardiovas-
sisted reproductive technologies are associ- Reference values and Z scores for pulsed- cular Imaging. J Am Soc Echocardiogr. 2015
ated with cardiovascular remodeling in utero wave Doppler and M-mode measurements in Jan;28(1):1–39.e14.
that persists postnatally. Circulation. 2013 fetal echocardiography. J Am Soc Echocar- 23 Royston P, Wright EM. How to construct
Sep;128(13):1442–50. diogr. 2016 May;29(5):448–60.e9. ‘normal ranges’ for fetal variables. Ultrasound
8 García-Otero L, López M, Gómez O, Goncé 17 Li X, Zhou Q, Huang H, Tian X, Peng Q. Z- Obstet Gynecol. 1998 Jan;11(1):30–8.
A, Bennasar M, Martínez JM, et al. Zidovu- score reference ranges for normal fetal heart 24 McAuliffe FM, Trines J, Nield LE, Chitayat D,
dine treatment in HIV-infected pregnant sizes throughout pregnancy derived from Jaeggi E, Hornberger LK. Early fetal echocar-
women is associated with fetal cardiac remod- fetal echocardiography. Prenat Diagn. 2015 diography—a reliable prenatal diagnosis tool.
elling. AIDS. 2016 Jun;30(9):1393–401. Feb;35(2):117–24. Am J Obstet Gynecol. 2005 Sep; 193(3 Pt 2):
9 Pauliks LB. The effect of pregestational diabe- 18 Hadlock FP, Harrist RB, Carpenter RJ, Deter 1253–9.
tes on fetal heart function. Expert Rev Cardio- RL, Park SK. Sonographic estimation of fetal 25 Luewan S, Yanase Y, Tongprasert F, Srisu-
vasc Ther. 2015 Jan;13(1):67–74. weight. The value of femur length in addition pundit K, Tongsong T. Fetal cardiac dimen-
10 Barker DJ, Winter PD, Osmond C, Margetts to head and abdomen measurements. Radiol- sions at 14-40 weeks’ gestation obtained using
B, Simmonds SJ. Weight in infancy and death ogy 1984;150:535–40. cardio-STIC-M. Ultrasound Obstet Gynecol.
from ischaemic heart disease. Lancet. 1989 2011 Apr;37(4):416–22.
Sep;2(8663):577–80.
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