Cardiac dysfunction and cell damage across clinical
stages of severity in growth-restricted fetuses
Fatima Crispi, MD; Edgar Hernandez-Andrade, MD; Maurice M.A.L. Pelsers, PhD; Walter Plasencia, MD;
Jesus Andres Benavides-Serralde, MD; Elisenda Eixarch, MD; Ferdinand Le Noble, PhD;
Asif Ahmed, PhD; Jan F.C. Glatz, PhD; Kypros H. Nicolaides, MD; Eduard Gratacos, MD
OBJECTIVE: The purpose of this study was to assess cardiac function
and cell damage in intrauterine growth-restricted (IUGR) fetuses across
clinical Doppler stages of deterioration.
STUDY DESIGN: One hundred twenty appropriate-for-gestational-age and
81 IUGR fetuses were classified in stages 1/2/3 according umbilical artery
present/absent/reversed end-diastolic blood flow, respectively. Cardiac
function was assessed by modified-myocardial performance index, early-
to-late diastolic filling ratios, cardiac output, and cord blood B-type natri-
uretic peptide; myocardial cell damage was assessed by heart fatty acid–
binding protein, troponin-I, and high-sensitivity C-reactive protein.
RESULTS: Modified-myocardial performance index, blood B-type na-
triuretic peptide, and early-to-late diastolic filling ratios were increased
in a stage-dependent manner in IUGR fetuses, compared with appro-
priate-for-gestational-age fetuses. Heart fatty acid– binding protein lev-
els were higher in IUGR fetuses at stage 3, compared with control fe-
tuses. Cardiac output, troponin-I, and high-sensitivity C-reactive
protein did not increase in IUGR fetuses at any stage.
CONCLUSION: IUGR fetuses showed signs of cardiac dysfunction from
early stages. Cardiac dysfunction deteriorates further with the progres-
sion of fetal compromise, together with the appearance of biochemical
signs of cell damage.
Key words: cardiac function, Doppler ultrasound, heart fatty acid–
binding protein, intrauterine growth restriction, myocardial damage
Cite this article as: Crispi F, Hernandez-Andrade E, Pelsers MMAL, et al. Cardiac dysfunction and cell damage across clinical stages of severity in growth-
restricted fetuses. Am J Obstet Gynecol 2008;199:254.e1-254.e8.
S
evere intrauterine growth restric-
tion (IUGR) because of placental
insufficiency affects 1% of pregnancies
and contributes to 30% of total perina-
tal loss and severe morbidity.
1
The
heart is a central organ in the fetal
adaptive mechanisms to placental in-
sufficiency and hypoxia. Elevated fetal
levels of atrial and B-type natriuretic
peptides and significant differences in
echocardiographic parameters have
been reported in small-for-date ba-
bies.
2-6
Monitoring of cardiac function
is proposed as an adjunct to current
methods to predict adverse outcome
and death in IUGR
7
; however, suitable
parameters remain to be established.
Furthermore, fetal cardiac dysfunction
might have important consequences in
fetal programming of postnatal cardiac
disease later in adulthood. Epidemio-
logic studies and animal models have
established that low-birthweight ba-
bies have an increased risk of cardio-
vascular disease later in life.
8,9
Clinically, IUGR fetuses are stratified
in stages of severity, according to the se-
quential deterioration of fetoplacental
Doppler patterns.
1,10
However, the onset
and progression of fetal cardiac dysfunc-
tion across stages of severity in IUGR
have not been established. Recently,
Girsen et al
6
evaluated cord blood atrial
and B-type natriuretic peptides in fetuses
at different stages of Doppler deteriora-
tion and suggested that subclinical car-
diac dysfunction might constitute an
early event in the course of the disease.
Aside from cardiac function, it is un-
known whether myocardial cell damage
occurs at any stage of fetal deterioration.
From the Department of Maternal-Fetal Medicine, Institut Clínic de Ginecologia, Obstetrícia
i Neonatologia; the Fetal and Perinatal Medicine Research Group, Institut d’Investigacions
Biomèdiques August Pi i Sunyer; and Centro de Investigación Biomédica en Red de
Enfermedades Raras (CIBERER), Instituto de Salud Carlos III, Hospital Clinic-University of
Barcelona, Barcelona, Spain (Drs Crispi, Hernandez-Andrade, Benavides-Serralde, Eixarch,
and Gratacos); the Department of Reproductive and Vascular Biology, University of
Birmingham Medical School, Edgbaston, Birmingham, West Midlands, UK (Drs Crispi and
Ahmed); the Department of Clinical Chemistry, University Hospital Maastricht, Maastricht,
the Netherlands (Dr Pelsers); the Cardiovascular Research Institute Maastricht, Maastricht
University, Maastricht, The Netherlands (Dr Glatz); Harris Birthright Research Centre for
Fetal Medicine, King’s College Hospital Medical School, Denmark Hill, London, UK (Drs
Plasencia and Nicolaides); and the Max Delbrueck Center for Molecular Medicine,
Laboratory for Angiogenesis and Cardiovascular Pathology, Berlin, Germany (Dr Le Noble).
This research was presented at the 28th Annual Meeting of the Society for Maternal–Fetal
Medicine, Dallas, TX, Jan. 28-Feb. 2, 2008.
Received Jan. 2, 2008; accepted June 18, 2008
Reprints: Eduard Gratacos, Department of Maternal-Fetal Medicine (ICGON), Hospital Clinic,
Sabino de Arana 1, 08028, Barcelona, Spain. egratacos@clinic.ub.es.
Supported by grants from the Fondo the Investigación Sanitaria (PI0600347); Cerebra Foundation
for the Brain Injured Child, Carmarthen, Wales, UK; Thrasher Research Fund (Salt Lake City, UT);
and the Medical Research Council (grants G0601295 and G0700288 [A.A.; E.G.]).
0002-9378/$34.00 • © 2008 Mosby, Inc. All rights reserved. • doi: 10.1016/j.ajog.2008.06.056
SMFM Papers www. AJOG.org
254.e1 American Journal of Obstetrics & Gynecology SEPTEMBER 2008