Ultrasound Obstet Gynecol 2008; 31: 65–71 Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/uog.5231
Maternal cardiovascular function in pregnancies complicated by intrauterine growth restriction F. PREFUMO*, M. L. MUIESAN†, R. PERINI*, A. PAINI† B. BONZI† A. LOJACONO* E. AGABITI-ROSEI† and T. FRUSCA* *Maternal-Fetal Medicine Unit, Department of Obstetrics and Gynaecology and †Cardiovascular Ultrasound Laboratory, Department of Internal Medicine, University of Brescia, Brescia, Italy
K E Y W O R D S: blood pressure; cardiac function; intrauterine growth restriction; umbilical Doppler; uterine Doppler
ABSTRACT Objective To investigate maternal cardiovascular function in pregnancies complicated by intrauterine growth restriction (IUGR). Methods Maternal echocardiography and ambulatory blood pressure monitoring were performed in pregnancies complicated by IUGR (n = 12) and controls (n = 12), all of whom were normotensive at enrollment. Results Compared to controls, maternal blood pressure (P = 0.016) and total vascular resistance (P = 0.008) were higher in IUGR pregnancies. Heart rate was lower (P = 0.003), as was systolic function expressed by midwall fractional shortening (P = 0.04). No significant differences between the two groups were observed for left atrial or left ventricular dimensions, nor for left ventricular geometry. Assessment of diastolic function by means of transmitral Doppler flow measurements revealed a significantly longer isovolumetric relaxation time in pregnancies with IUGR (P = 0.006). Conclusions In normotensive pregnancies complicated by IUGR, as compared to controls, there is decreased diastolic and systolic maternal cardiac function, and a higher blood pressure. Copyright 2007 ISUOG. Published by John Wiley & Sons, Ltd.
INTRODUCTION Maternal cardiovascular function changes dramatically during pregnancy. Adaptations have been observed in cardiac output, heart rate, plasma volume, arterial compliance, ventricular morphology and systolic and diastolic
cardiac function1 – 6 . Although the exact mechanisms leading to these changes are not clear, the processes of placental development and trophoblast invasion are likely to have a role in them7 – 9 . Inadequate trophoblast invasion and placental development have been associated with intrauterine growth restriction (IUGR)10,11 . Maternal echocardiography has provided evidence that alterations in maternal cardiovascular function are present in this condition8,12 , and may even precede the onset of the full clinical syndrome13,14 . However, the pattern of maternal hemodynamic and echocardiographic alterations has not been unequivocally defined12,15 – 17 , probably owing to differences in case selection criteria and maternal assessment methodology. Moreover, it is also well known that there is a continuous inverse association between fetal growth and maternal blood pressure throughout the range seen in normal pregnancy18 and that increased blood pressure can be observed in IUGR19,20 . Therefore, the aim of our study was to evaluate maternal cardiovascular function by means of both echocardiography and ambulatory blood pressure monitoring in pregnancies complicated by IUGR.
PATIENTS AND METHODS Patients A case–control study was performed. Twelve consecutive pregnancies complicated by IUGR were enrolled between April 2003 and September 2004. Twelve uncomplicated pregnancies observed during the same period and matched for maternal and gestational age served as controls. Only singleton pregnancies were included. All the women were recruited from our IUGR clinic, receiving referrals from the Eastern Lombardy region. Women with a known medical condition (e.g. diabetes mellitus, connective tissue
Correspondence to: Dr F. Prefumo, Dipartimento di Ostetricia e Ginecologia, Universita` di Brescia, Piazzale Spedali Civili,1, 25123 Brescia, Italy (e-mail:
[email protected]) Accepted: 12 September 2007
Copyright 2007 ISUOG. Published by John Wiley & Sons, Ltd.
ORIGINAL PAPER
Prefumo et al.
66
disease, essential hypertension, renal or cardiovascular disease) or a history of recurrent miscarriage were excluded. None of the women received vasoactive medications during the study. Blood pressure was ≤ 140/90 mmHg in all cases at enrollment. Gestational age was calculated from the last menstrual period and confirmed by crown–rump length measurement. In all cases a careful search for fetal abnormalities was performed. All fetuses had normal chromosomes. Local ethical committee approval was obtained for this study, and all the women gave their written informed consent.
Ultrasound examination Ultrasound examinations were performed using HD11 (Advanced Technology Laboratories, Bothell, WA, USA) and Sequoia (Acuson, Mountain View, CA, USA) ultrasound systems with 3–7.5-MHz transabdominal probes. The ultrasound criteria for selecting pregnancies complicated by IUGR were: (a) fetal abdominal circumference below the 5th percentile by local reference values21 ; (b) umbilical artery pulsatility index (PI) more than two SDs above the gestational mean by local reference values; (c) mean uterine artery resistance index (RI) ≥ 0.65 and the presence of bilateral early diastolic notches22 . The controls all presented with a fetal abdominal circumference between the 10th and 90th percentiles, umbilical artery PI within two SDs of the mean and normal uterine artery resistance (RI < 0.65 and no notches). Fetal middle cerebral artery PI was also measured in all cases.
Blood pressure measurements Office blood pressure measurements were performed at the time of maternal echocardiography by a single operator using a mercury sphygmomanometer after a rest period of 10 min in the left lateral decubitus position. Systolic blood pressure (SBP) was measured at Korotkoff phase I, and diastolic blood pressure (DBP) at Korotkoff phase V. The average of three measurements was recorded. Mean arterial pressure (MAP) was calculated as (DBP + (SBP − DBP)/3). All the women had SBP ≤ 140 mmHg and DBP ≤ 90 mmHg. Ambulatory blood pressure monitoring (ABPM) was performed within 1 week of enrollment using an ABPM Spacelabs model 90207 device (SpaceLabs Inc., Redmond, WA, USA). The SBP and DBP of each of the study subjects were automatically monitored for 25 h, from 9 am to 10 am of the following day. Measurements were recorded every 20 min from 7 am to 11 pm, and every 30 min from 11 pm to 7 am, for a total of 67 measurements per subject, the cuff being worn on the non-dominant arm. ABPM was performed in addition to the women’s routine antenatal care, and no person was hospitalized during monitoring. Cuff size was determined by upper arm circumference at the time
Copyright 2007 ISUOG. Published by John Wiley & Sons, Ltd.
of each visit. During monitoring, each subject maintained a diary regarding information about their activity cycle, dietary consumption, physical activity, emotional state, and other external or internal stimuli that could possibly affect blood pressure. The device automatically discarded readings affected by artifacts (arm movements, noise). Automated analysis discarded isolated readings in case of differential blood pressure < 20 mmHg, DBP < 50 mmHg or SBP > 260 mmHg. ABPM recordings were considered technically satisfactory only if no more than 15% of the readings were discarded by applying the above criteria. The following values were calculated by ABPM: mean heart rate, SBP and DBP; daytime mean heart rate, SBP and DBP; night-time mean heart rate, SBP and DBP; MAP.
Maternal echocardiography A Sonos 5500 (Hewlett Packard, Andover, MA, USA) ultrasound machine with a 2.5-MHz probe was used. Examinations were performed after a rest period of 20 min in the left lateral decubitus position. Twodimensional measurements were performed as recommended by the American Society of Echocardiography23 . Left ventricular (LV) end-diastolic and end-systolic volumes were calculated with the Teichholz’s correction of the cube formula24 . As previously reported25,26 , LV systolic function was estimated by midwall fractional shortening (FS), calculated using the following equation: ((LVDd + PWTd /2 + IVSTd /2) − (LVDs + hs /2)) Midwall FS = (LVDd + PWTd /2 + IVSTd /2) where LVD = left ventricular diameter, PWT = posterior wall thickness, IVST = interventricular septum thickness, h = combined thickness of interventricular septum and posterior wall, and subscripts s and d indicate end-systole and end-diastole, respectively. Myocardial contractile efficiency is usually examined by the relationship of systolic shortening to end-systolic stress (ESS). In order to identify deviations from normal in contractile performance, observed midwall FS was expressed as a percentage of the value predicted from circumferential ESS with an equation derived from normal adults27,28 . Interobserver and intraobserver reproducibility of midwall FS in our laboratory were 4 and 4.5%, respectively29 . Cardiac output (CO) was calculated as the product of stroke volume multiplied by heart rate. Total vascular resistance (TVR) was calculated in dyne/s/cm5 according to the following formula: TVR = (MAP[mmHg]/CO[L/min]) × 80 LV mass (LVM) was calculated according to the Penn Convention30 , and the LVM index (LVMI) was obtained by normalization of LVM for height to the power 2.7 (LVMI = LVM/m2.7 , where m is the height of the woman in meters)28 . Transmitral inflow was recorded using pulsed wave Doppler recordings at the mitral valve
Ultrasound Obstet Gynecol 2008; 31: 65–71.
IUGR and cardiovascular function
67
leaflet tips in the apical four-chamber view. The peak velocity of early filling (E), peak velocity of atrial filling (A) and the deceleration time of the E wave were measured and the E/A ratio calculated. Isovolumetric relaxation time (IVRT) was measured as the interval between the aortic valve closure click and the start of mitral flow, using pulsed wave Doppler recordings of the LV outflow tract. The operator was blinded to the pregnancy characteristics of the women.
SPSS Inc., Chicago, IL, USA) and Prism (release 3.00, GraphPad Software Inc., San Diego, CA, USA) software packages. A power calculation based on the cardiac output values reported by Vasapollo et al.12 was performed with α = 0.05 and β = 0.2 using the Study Size software, ¨ version 2.0.1 (CreoStat HB, Frolunda, Sweden). On the basis of this calculation, differences in cardiac output 85% as large as those reported by Vasapollo et al. could be detected by studying 22 subjects in total (11 cases of IUGR and 11 controls).
Pregnancy outcome All pregnancy outcomes were obtained from the delivery suite database. Gestational hypertension was defined as a blood pressure ≥ 140/90 mmHg of new onset after 20 weeks’ gestation. Pre-eclampsia was defined as a blood pressure ≥ 140/90 mmHg and proteinuria of ≥ 300 mg in 24 h, or two readings of at least 2+ on dipstick analysis of midstream or catheter urine specimens if no 24-h urine collection was available. Cases were all confirmed to have a birth weight below the 10th percentile for gestational age, while controls had a birth weight between the 10th and 90th percentiles of the reference population31 .
Statistical analysis For inter-group comparisons, the Mann-Whitney, χ2 and Fisher’s exact tests were used as appropriate. All calculations were performed using the SPSS (release 11.5,
RESULTS The demographic and clinical characteristics of pregnancies complicated by IUGR and controls are shown in Table 1. All women were of Caucasian origin. Pregnancy outcomes are summarized in Table 2. Only one woman developed gestational hypertension, but not preeclampsia. There was one perinatal death due to placental abruption. Maternal hemodynamics data are displayed in Table 3. SBP, DBP, MAP and TVR were significantly higher in the IUGR group. Stroke volume and ejection fraction were similar in the two groups. Cardiac output was lower in the IUGR group, but the difference did not reach statistical significance. Maternal echocardiographic, anatomical and functional characteristics are shown in Table 4. No statistically significant differences between the two groups were observed for left atrial or left ventricular dimensions, nor for left ventricular geometry
Table 1 Demographic and clinical characteristics of the intrauterine growth restriction (IUGR) and control groups
Parameter Maternal age (years) Gestational age at assessment (weeks) Height (cm) Weight at assessment (kg) Body mass index at assessment (kg/m2 ) Mean uterine artery resistance index Mean uterine artery pulsatility index Umbilical artery pulsatility index Fetal middle cerebral artery pulsatility index
IUGR group (n = 12)
Controls (n = 12)
P
32 (25–39) 29.2 (26.2–33.4) 165 (150–173) 66 (51–90) 25 (19–36) 0.70 (0.65–0.77) 1.46 (1.13–1.73) 1.80 (1.61–2.00) 1.93 (1.13–2.05)
31 (28–42) 28.0 (25.5–32.4) 160 (156–171) 64 (54–79) 24 (22–28) 0.51 (0.38–0.57) 0.65 (0.40–1.04) 0.91 (0.74–1.13) 2.00 (1.95–2.10)
0.10 0.41 0.32 0.63 0.93 < 0.001 < 0.001 < 0.001 0.007
Values are given as median (range). Table 2 Pregnancy outcomes of the intrauterine growth restriction (IUGR) and control groups
Parameter Gestational hypertension Gestational age at delivery (weeks) Assessment to delivery interval (weeks) Birth weight (g) Delivery before 34 weeks Vaginal delivery Admission to neonatal intensive care unit Apgar score < 7 at 5 min Perinatal death
IUGR group (n = 12)
Controls (n = 12)
P
1 33.1 (29.5–39.6) 3.3 (1.4–6.6) 1285 (730–2500) 6 2 8 0 1
0 39.3 (37.0–41.1) 12.4 (6.9–13.5) 3250 (2630–3580) 0 9 0 0 0
1 < 0.001 < 0.001 < 0.001 0.01 0.01 0.001 1 1
Values are given as median (range) or n.
Copyright 2007 ISUOG. Published by John Wiley & Sons, Ltd.
Ultrasound Obstet Gynecol 2008; 31: 65–71.
Prefumo et al.
68 Table 3 Maternal hemodynamics of the intrauterine growth restriction (IUGR) and control groups
Parameter Heart rate (beats per min) Office systolic blood pressure (mmHg) Office diastolic blood pressure (mmHg) Office mean arterial pressure (mmHg) Total vascular resistance (dyne/s/cm5 ) Stroke volume (mL) Cardiac output (L/min) Ejection fraction (%)
IUGR group (n = 12)
Controls (n = 12)
P
70 (63–88) 125 (115–139) 87 (80–89) 99 (92–117) 1623 (1287–3125) 69 (36–81) 5.40 (4.4–7.0) 69 (64–83)
78 (52–102) 110 (100–120) 70 (70–80) 86 (80–93) 1163 (944–1785) 67 (57–86) 6.1 (4.0–8.1) 71 (65–79)
0.22 0.003 < 0.001 < 0.001 0.008 0.95 0.08 0.59
Values are given as median (range). Table 4 Maternal echocardiographic anatomical and functional characteristics of the intrauterine growth restriction (IUGR) and control groups IUGR group (n = 12)
Controls (n = 12)
P
3.3 (2.8–4.0) 2.8 (2.4–3.1) 107 (75–166) 28.4 (18.8–42.8) 0.28 (0.20–0.44) 118 (94–126) 99 (56–111) 65 (58–84) 1.4 (0.9–1.7) 181 (146–225) 78 (50–90)
3.3 (3.1–3.9) 2.8 (2.5–3.3) 101 (80–136) 27.8 (21.4–32.9) 0.27 (0.25–0.33) 122 (106–140) 85 (62–120) 63 (47–81) 1.4 (0.9–1.9) 174 (123–243) 60 (45–75)
0.98 0.76 0.38 0.63 0.84 0.04 0.80 0.22 0.35 0.80 0.006
Parameter Left atrial diameter (cm) Aortic root diameter (cm) Left ventricular mass (g) Left ventricular mass index (g/m2.7 ) Relative wall thickness Midwall fractional shortening (% of predicted value) Peak velocity of the E-wave (cm/s) Peak velocity of the A-wave (cm/s) E/A ratio Deceleration time of the E-wave (ms) Isovolumetric relaxation time (ms) Values are given as median (range).
Table 5 Ambulatory blood pressure monitoring findings of the intrauterine growth restriction (IUGR) and control groups
Parameter 24 h Heart rate (beats per min) Systolic blood pressure (mmHg) Diastolic blood pressure (mmHg) Mean arterial pressure (mmHg) Daytime Heart rate (beats per min) Systolic blood pressure (mmHg) Diastolic blood pressure (mmHg) Mean arterial pressure (mmHg) Night-time Heart rate (beats per min) Systolic blood pressure (mmHg) Diastolic blood pressure (mmHg) Mean arterial pressure (mmHg)
IUGR group (n = 12)
Controls (n = 12)
P
74 (61–82) 117 (104–136) 75 (65–88) 87 (79–104)
79 (76–92) 106 (101–121) 66 (56–73) 79 (72–87)
0.003 0.031 0.012 0.016
79 (64–86) 120 (105–140) 79 (69–90) 91 (81–108)
82 (79–95) 114 (103–123) 72 (58–77) 85 (75–89)
0.031 0.038 0.010 0.016
63 (55–75) 112 (98–130) 66 (57–83) 81 (72–98)
75 (66–84) 98 (92–116) 58 (53–71) 70 (68–85)
0.001 0.025 0.031 0.025
Values are given as median (range).
(expressed by relative wall thickness). Systolic function, as expressed by midwall FS, was lower in the IUGR group. Assessment of diastolic function by means of transmitral Doppler flow measurements revealed a significantly longer IVRT in pregnancies complicated by IUGR. Finally, ABPM measurements confirmed the pattern observed at conventional blood pressure measurements, with higher
Copyright 2007 ISUOG. Published by John Wiley & Sons, Ltd.
blood pressure values and lower heart rates in complicated pregnancies compared with controls (Table 5).
DISCUSSION In normotensive pregnancies complicated by IUGR, we observed an increase in total vascular resistance and in
Ultrasound Obstet Gynecol 2008; 31: 65–71.
IUGR and cardiovascular function maternal blood pressure, measured in the clinic and by 24-h ambulatory monitoring, and a decrease in heart rate compared with controls. From the early stages of normal pregnancy, a fall in systemic vascular tone and expansion of plasma volume lead to a compensatory increase in heart rate and to an overall increase in cardiac output3,32 . Duvekot et al. examined, at between 5 and 8 weeks of gestation, ten women who subsequently had normal pregnancies and four women who subsequently developed IUGR (birth weight < 10th percentile), showing a smaller left atrial diameter and a failure of cardiac output increase in complicated pregnancies13 . Left atrial diameter is an index of preload, which is related to plasma volume expansion. Veille et al. examined 19 pregnancies with IUGR (defined as birth weight below two SDs of the mean) and 79 controls, at an average of 2–4 weeks before delivery15 . They found no significant differences in left ventricular size, cardiac output, blood pressure or TVR. Vasapollo et al. examined 21 pregnancies complicated by IUGR at 25–36 weeks’ gestation, and 21 matched controls12 . The criteria for case selection included not only birth weight (< 10th percentile), but also an umbilical artery PI more than two SDs above the mean. They found heart rate to be slightly lower in the growth-restricted group, whereas blood pressure and total vascular resistance were higher compared with the control subjects. End-diastolic volume, stroke volume and CO were lower in the complicated pregnancies. The growth-restricted group had smaller left atrial maximal dimensions and greater left atrial minimal areas compared with the control subjects. Left atrial function was depressed. A smaller left ventricular mass was also present, and IVRT was prolonged in the women with growth-restricted fetuses compared with controls. The IVRT is the time interval between the end of LV systolic ejection and the opening of the mitral valve, when LV pressure decreases while LV volume remains constant. A prolonged IVRT results from high residual atrial preload and normal left atrial contractility, or from increased afterload33 . Bamfo et al. compared 107 uncomplicated pregnancies with 20 pregnancies complicated by IUGR at 25–37 weeks’ gestation16 . In the complicated group, maternal assessment was carried out within 10 days prior to delivery in order to correlate findings with the maximum degree of fetal disease. The criteria for case selection included an estimated fetal weight less than the 3rd centile, fetal asymmetry (defined as the ratio of head circumference to abdominal circumference above the 95th centile), cerebral redistribution (defined as the ratio of umbilical artery to middle cerebral artery PI greater than the 95th centile) and oligohydramnios (defined as amniotic fluid index below the 5th centile). CO, stroke volume and LV long-axis shortening were lower in the growth-restricted group than in controls. Heart rate was lower in pregnancies complicated by IUGR, while the E/A ratio was similar between the two groups. MAP was also similar between the two groups, while TVR was higher in the IUGR group than in the normal group.
Copyright 2007 ISUOG. Published by John Wiley & Sons, Ltd.
69
Some of the differences between earlier and later reports may be explained by different criteria for the definition of IUGR. In particular, the studies by Duvekot et al.13 and Veille et al.15 only relied on birth weight, while Vasapollo et al.12 and Bamfo et al.16 included Doppler ultrasound signs of placental dysfunction. Recently, Bamfo et al. also suggested that a pattern of reduced CO and increased TVR may help in differentiating growth-restricted fetuses from small-for-gestational-age fetuses with no signs of placental impairment17 . In our study we used very strict criteria for the identification of complicated cases, including not only abnormal fetal growth and umbilical flow as in the previous papers, but also abnormal uterine artery blood flow patterns. Therefore, our results apply to a wellcharacterized group of cases of IUGR due to placental dysfunction. Interestingly, while Bamfo et al.16 found no difference in maternal blood pressure values, our data and those of Vasapollo et al.12 demonstrated an increase in office measurements of SBP, DBP and MAP. In order to further characterize the relationship between maternal cardiac function and blood pressure, we employed for the first time ABPM in combination with maternal echocardiography to characterize maternal cardiovascular function in pregnancies complicated by IUGR. ABPM reduces the errors in measuring blood pressure, and 24h monitoring reliably records the actual blood pressure variations during ordinary daily life34 . ABPM has been confirmed to be a reliable technique for measuring blood pressure in pregnancy35 – 37 , and has been shown to be more clinically predictive than office blood pressure measurements in hypertensive complications of pregnancy38 – 40 . Using ABPM we were able to confirm an increase in maternal blood pressure in pregnancies complicated by IUGR, although the readings were still within the normotensive range. This finding is in accordance with previous studies using ABPM18,20 , suggesting that increased blood pressure may have a role in IUGR, either as an etiological factor or as a compensatory mechanism. As this increase in blood pressure is accompanied by a decrease in heart rate, it can be concluded that the raised blood pressure is not dependent on heightened adrenergic activity, but it should rather be related to a real increase in peripheral vascular resistance. It is interesting to observe that in our series and in that of Vasapollo et al.12 the increase in blood pressure seems to be a major determinant of TVR changes, and is paralleled by an increase in IVRT. On the other hand, Bamfo et al.16 observed no differences in blood pressure or IVRT between cases and controls. Therefore, most of the increase in TVR they observed in growth-restricted fetuses must be ascribed to impaired LV systolic function and to a consequent decrease in cardiac output, or alternatively to reduced hemodilution and increased blood viscosity. Whether the different ethnic composition of the study populations (Caucasian in the two Italian studies, multiethnic in the English study), and the different intervals between maternal assessment and delivery, have a role in explaining these discrepancies, remains to be clarified.
Ultrasound Obstet Gynecol 2008; 31: 65–71.
70
In our series, one woman with a growth-restricted fetus developed gestational hypertension later in pregnancy. However, even excluding this case from the analysis, the conclusions were unaffected (data not shown). One of the limitations of our study was the small size of the study population (12 women in each group), which may have limited our ability to observe differences in LV systolic performance measured at the endocardium between pregnancies complicated by IUGR and controls, and may have influenced to some extent the significance of the findings reported. However, the sample size was adequate to detect a difference in ambulatory heart rate, office and ambulatory blood pressure, TVR, and an early impairment of systolic contractility and diastolic relaxation. In conclusion, we found that in pregnancies complicated by IUGR, as compared to controls, a number of alterations in maternal cardiovascular function can be observed by means of both echocardiography and ABPM. When compared to previous studies with similar selection criteria, our results suggest that a higher blood pressure in IUGR may be a more relevant factor in determining changes in maternal cardiovascular function than previously suspected. Further research is needed to clarify the relative significance of echocardiographic and bloodpressure findings for the pathogenesis of uteroplacental insufficiency and growth restriction, and to define their possible roles in the clinical management of these pregnancies.
REFERENCES 1. Capeless EL, Clapp JF. Cardiovascular changes in early phase of pregnancy. Am J Obstet Gynecol 1989; 161: 1449–1453. 2. Hunter S, Robson SC. Adaptation of the maternal heart in pregnancy. Br Heart J 1992; 68: 540–543. 3. Duvekot JJ, Cheriex EC, Pieters FA, Menheere PP, Peeters LH. Early pregnancy changes in hemodynamics and volume homeostasis are consecutive adjustments triggered by a primary fall in systemic vascular tone. Am J Obstet Gynecol 1993; 169: 1382–1392. 4. Poppas A, Shroff SG, Korcarz CE, Hibbard JU, Berger DS, Lindheimer MD, Lang RM. Serial assessment of the cardiovascular system in normal pregnancy. Role of arterial compliance and pulsatile arterial load. Circulation 1997; 95: 2407–2415. 5. Mesa A, Jessurun C, Hernandez A, Adam K, Brown D, Vaughn WK, Wilansky S. Left ventricular diastolic function in normal human pregnancy. Circulation 1999; 99: 511–517. 6. Simmons LA, Gillin AG, Jeremy RW. Structural and functional changes in left ventricle during normotensive and preeclamptic pregnancy. Am J Physiol Heart Circ Physiol 2002; 283: H1627–H1633. 7. Carbillon L, Uzan M, Uzan S. Pregnancy, vascular tone, and maternal hemodynamics: a crucial adaptation. Obstet Gynecol Surv 2000; 55: 574–581. 8. Valensise H, Vasapollo B, Novelli GP, Larciprete G, Romanini ME, Arduini D, Galante A, Romanini C. Maternal diastolic function in asymptomatic pregnant women with bilateral notching of the uterine artery waveform at 24 weeks’ gestation: a pilot study. Ultrasound Obstet Gynecol 2001; 18: 450–455. 9. Prefumo F, Sharma R, Brecker SJ, Gaze DC, Collinson PO, Thilaganathan B. Maternal cardiac function in early pregnancies with high uterine artery resistance. Ultrasound Obstet Gynecol 2007; 29: 58–64.
Copyright 2007 ISUOG. Published by John Wiley & Sons, Ltd.
Prefumo et al. 10. Brosens I, Dixon HG, Robertson WB. Fetal growth retardation and the arteries of the placental bed. Br J Obstet Gynaecol 1977; 84: 656–663. 11. Brosens IA, Robertson WB, Dixon HG. The role of the spiral arteries in the pathogenesis of pre-eclampsia. J Pathol 1970; 101: Pvi. 12. Vasapollo B, Valensise H, Novelli GP, Larciprete G, Di Pierro G, Altomare F, Casalino B, Galante A, Arduini D. Abnormal maternal cardiac function and morphology in pregnancies complicated by intrauterine fetal growth restriction. Ultrasound Obstet Gynecol 2002; 20: 452–457. 13. Duvekot JJ, Cheriex EC, Pieters FAA, Peeters LLH. Severely impaired fetal growth is preceded by maternal hemodynamic maladaptation in very early pregnancy. Acta Obstet Gynecol Scand 1995; 74: 693–697. 14. Vasapollo B, Valensise H, Novelli GP, Altomare F, Galante A, Arduini D. Abnormal maternal cardiac function precedes the clinical manifestation of fetal growth restriction. Ultrasound Obstet Gynecol 2004; 24: 23–29. 15. Veille JC, Morton MJ, Paul MS. Maternal left ventricular dimension in pregnancies complicated by fetal growth retardation. Obstet Gynecol 1991; 78: 265–269. 16. Bamfo JEAK, Kametas NA, Turan O, Khaw A, Nicolaides KH. Maternal cardiac function in fetal growth restriction. BJOG 2006; 113: 784–791. 17. Bamfo JEAK, Kametas NA, Chambers JB, Nicolaides KH. Maternal cardiac function in fetal growth-restricted and nongrowth-restricted small-for-gestational age pregnancies. Ultrasound Obstet Gynecol 2007; 29: 51–57. 18. Churchill D, Perry IJ, Beevers D. Ambulatory blood pressure in pregnancy and fetal growth. Lancet 1997; 349: 7–10. 19. Koenen SV, Franx A, Mulder EJ, Bruinse HW, Visser GH. Fetal and maternal cardiovascular diurnal rhythms in pregnancies complicated by pre-eclampsia and intrauterine growth restriction. J Matern Fetal Neonatal Med 2002; 11: 313–320. 20. Tranquilli AL, Giannubilo SR. Blood pressure is elevated in normotensive pregnant women with intrauterine growth restriction. Eur J Obstet Gynecol Reprod Biol 2005; 122: 45–48. 21. Nicolini U, Todros T, Ferrazzi E, Zorzoli A, Groli C, Zucca S, Tinti A, Dodero D, Destro F, Ceccarello P, Paroni M. Curve trasversali dell’accrescimento fetale. Studio multicentrico. Minerva Ginecol 1986; 38: 873–887. 22. Bower S, Bewley S, Campbell S. Improved prediction of preeclampsia by two-stage screening of uterine arteries using the early diastolic notch and color Doppler imaging. Obstet Gynecol 1993; 82: 78–83. 23. Schiller NB, Shah PM, Crawford M, DeMaria A, Devereux R, Feigenbaum H, Gutgesell H, Reichek N, Sahn D, Schnittger I, Silverman NH, Tajik AJ. Recommendations for quantitation of the left ventricle by two-dimensional echocardiography. American Society of Echocardiography Committee on Standards, Subcommittee on Quantitation of Two-Dimensional Echocardiograms. J Am Soc Echocardiogr 1989; 2: 358–367. 24. Teichholz LE, Kreulen T, Herman MV, Gorlin R. Problems in echocardiographic volume determinations: echocardiographicangiographic correlations in the presence or absence of asynergy. Am J Cardiol 1976; 37: 7–11. 25. Devereaux RB, Roman MJ. Evaluation of cardiac and vascular structure by echocardiography and other noninvasive techniques. In Hypertension: pathophysiology, diagnosis, treatment, Laragh JH, Brenner BM (eds). Raven Press: New York, 1995; 1969–1985. 26. Muiesan ML, Lupia M, Salvetti M, Grigoletto C, Sonino N, Boscaro M, Rosei EA, Mantero F, Fallo F. Left ventricular structural and functional characteristics in Cushing’s syndrome. J Am Coll Cardiol 2003; 41: 2275–2279. 27. de Simone G, Devereux RB, Koren MJ, Mensah GA, Casale PN, Laragh JH. Midwall left ventricular mechanics. An independent predictor of cardiovascular risk in arterial hypertension. Circulation 1996; 93: 259–265.
Ultrasound Obstet Gynecol 2008; 31: 65–71.
IUGR and cardiovascular function 28. de Simone G, Devereux RB, Daniels SR, Koren MJ, Meyer RA, Laragh JH. Effect of growth on variability of left ventricular mass: assessment of allometric signals in adults and children and their capacity to predict cardiovascular risk. J Am Coll Cardiol 1995; 25: 1056–1062. 29. Muiesan ML, Salvetti M, Monteduro C, Rizzoni D, Corbellini C, Castellano M, Porteri E, Agabiti-Rosei E. Changes in midwall systolic performance and cardiac hypertrophy reduction in hypertensive patients. J Hypertens 2000; 18: 1651–1656. 30. Devereux RB, Reichek N. Echocardiographic determination of left ventricular mass in man. Anatomic validation of the method. Circulation 1977; 55: 613–618. 31. Parazzini F, Cortinovis I, Bortolus R, Fedele L, Recarli A. Weight at birth by gestational age in Italy. Hum Reprod 1995; 10: 1862–1863. 32. Valensise H, Novelli GP, Vasapollo B, Borzi M, Arduini D, Galante A, Romanini C. Maternal cardiac systolic and diastolic function: relationship with uteroplacental resistances. A Doppler and echocardiographic longitudinal study. Ultrasound Obstet Gynecol 2000; 15: 487–497. 33. Naqvi TZ. Diastolic function assessment incorporating new techniques in Doppler echocardiography. Rev Cardiovasc Med 2003; 4: 81–99. 34. Bergel E, Carroli G, Althabe F. Ambulatory versus conventional methods for monitoring blood pressure during pregnancy. Cochrane Database Syst Rev 2002, Issue 2, CD001231.
Copyright 2007 ISUOG. Published by John Wiley & Sons, Ltd.
71 35. Brown MA, Buddle ML, Bennett M, Smith B, Morris R, Whitworth JA. Ambulatory blood pressure in pregnancy: comparison of the Spacelabs 90207 and Accutracker II monitors with intraarterial recordings. Am J Obstet Gynecol 1995; 173: 218–223. 36. Brown MA, Robinson A, Bowyer L, Buddle ML, Martin A, Hargood JL, Cario GM. Ambulatory blood pressure monitoring in pregnancy: what is normal? Am J Obstet Gynecol 1998; 178: 836–842. 37. Pang TC, Brown MA. Accuracy of ambulatory blood pressure monitors in routine clinical practice. Am J Hypertens 2006; 19: 801–809. 38. Penny JA, Halligan AW, Shennan AH, Lambert PC, Jones DR, de Swiet M, Taylor DJ. Automated, ambulatory, or conventional blood pressure measurement in pregnancy: which is the better predictor of severe hypertension? Am J Obstet Gynecol 1998; 178: 521–526. 39. Waugh J, Perry IJ, Halligan AW, De Swiet M, Lambert PC, Penny JA, Taylor DJ, Jones DR, Shennan A. Birth weight and 24-hour ambulatory blood pressure in nonproteinuric hypertensive pregnancy. Am J Obstet Gynecol 2000; 183: 633–637. 40. Tranquilli AL, Giannubilo SR, Dell’Uomo B, Corradetti A. Prediction of gestational hypertension or intrauterine fetal growth restriction by mid-trimester 24-h ambulatory blood pressure monitoring. Int J Gynaecol Obstet 2004; 85: 126–131.
Ultrasound Obstet Gynecol 2008; 31: 65–71.
