Lopez-Mendez et al.

BMC Research Notes 2013, 6:477

http://www.biomedcentral.com/1756-0500/6/477

RESEARCH ARTICLE Open Access

Doppler ultrasound evaluation in preeclampsia

Maria A Lopez-Mendez1,3, Victoria Martinez-Gaytan2, Raul Cortes-Flores2, Rene M Ramos-Gonzalez2,
Mauro A Ochoa-Torres2, Idalia Garza-Veloz3, Monica I Martinez-Acuña3, Jose I Badillo-Almaraz3
and Margarita L Martinez-Fierro3*

Abstract
Background: Worldwide preeclampsia (PE) is the leading cause of maternal death and affects 5 to 8% of pregnant
women. PE is characterized by elevated blood pressure and proteinuria. Doppler Ultrasound (US) evaluation has
been considered a useful method for prediction of PE; however, there is no complete data about the most
frequently altered US parameters in the pathology. The aim of this study was to evaluate the uterine, umbilical, and
the middle cerebral arteries using Doppler US parameters [resistance index (RI), pulsatility index (PI), notch (N),
systolic peak (SP) and their combinations] in pregnant women, in order to make a global evaluation of
hemodynamic repercussion caused by the established PE.
Results: A total of 102 pregnant Mexican women (65 PE women and 37 normotensive women) were recruited in a
cases and controls study. Blood velocity waveforms from uterine, umbilical, and middle cerebral arteries, in
pregnancies from 24 to 37 weeks of gestation were recorded by trans-abdominal examination with a Toshiba
Ultrasound Power Vision 6000 SSA-370A, with a 3.5 MHz convex transducer. Abnormal general Doppler US profile
showed a positive association with PE [odds ratio (OR) = 2.93, 95% confidence interval (CI) = 1.2 - 7.3, P = 0.021)], and a
specificity and predictive positive value of 89.2% and 88.6%, respectively. Other parameters like N presence, RI and PI of
umbilical artery, as well as the PI of middle cerebral artery, showed differences between groups (P values < 0.05).
Conclusion: General Doppler US result, as well as N from uterine vessel, RI from umbilical artery, and PI from umbilical
and middle cerebral arteries in their individual form, may be considered as tools to determine hemodynamic
repercussion caused by PE.
Keywords: Doppler velocimetry, Preeclampsia, Uterine artery, Umbilical artery, Middle cerebral artery

Background of PE and it can be detected by Doppler ultrasound

Worldwide pre-eclampsia (PE) is the first cause of maternal (US). The latter has been considered a useful method
mortality, intrauterine growth retardation (IUGR), and fetal for prediction of PE and adverse pregnancy outcome
prematurity [1,2]. PE affects 5-10% of pregnancies and is [8,9]. Uterine artery is the most studied vessel in the
clinically manifested after 20 weeks of gestation (GW) [3,4]. Doppler evaluation in PE, because it represents the
The etiology of PE is still unknown, although an excessive maternal vascular condition, through the pulsatility and
maternal systemic inflammatory response and an imbalance resistance index (PI and RI respectively) and the presence
between circulating angiogenic and anti-angiogenic factors of early diastolic notch (N) [10,11]. Although there are
have been described [5,6]. The pathophysiology of PE is some studies including the umbilical artery as a relevant
based on the incapability of the trophoblast to invade vessel in the PE evaluation, traditionally this artery is taken
properly the myometrium causing a limited remodeling of together with the middle cerebral artery in the fetus status
spiral arteries [7]. The impaired placental perfusion caused evaluation [12-15]. In PE evaluation using Doppler US,
by vascular abnormalities precedes clinical manifestations there is no complete data about the most frequently altered
US parameters in their individual or combined form for
* Correspondence: margaritamf@uaz.edu.mx each artery. In this study we evaluate the uterine, umbilical,
3
Molecular Medicine Laboratory, Unidad Academica de Medicina Humana y and the middle cerebral arteries using several Doppler
Ciencias de la Salud, Universidad Autonoma de Zacatecas, Carretera
Zacatecas-Guadalajara Km. 6, C.P. 98160 Zacatecas, Mexico
US parameters (RI, PI, N, SP and their combinations)
Full list of author information is available at the end of the article in order to make a global evaluation of hemodynamic
© 2013 Lopez-Mendez et al.; licensee BioMed Central Ltd. This is an open access article distributed under the terms of the
Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.
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repercussion caused by the established PE, in a cases percentile standardized for the gestational age were consid-
and controls study. ered abnormal for the uterine and umbilical arteries, and
below the 10th percentile for the middle cerebral artery
Methods [20,21]. Alterations in any of the uterine artery parameters
Patients were interpreted as an abnormal result of this artery and
The patients were recruited from the high risk consult consequently an abnormal general Doppler result was re-
of the Unidad Medica de Alta Especialidad (UMAE) # ported. In the umbilical vessel, alterations in the individual
23 of the Instituto Mexicano del Seguro Social (IMSS) or combined RI and PI values were reported as an abnor-
in Monterrey, Mexico, between September 2009 and mal artery result. Decreases of individual RI or PI values,
June 2010.Women from 15 to 40 years old, with singleton as well as their combination in the middle cerebral artery
pregnancy between the 24–37 GW were included and were considered as an abnormal artery result. For umbilical
divided in cases and controls groups. The cases group and middle cerebral vessels only their combination with
consisted by diagnosed PE women according to the another abnormal artery was considered to report an
guidelines of the International Society for the Study of abnormal general Doppler result.
Hypertension in Pregnancy [16]. Most of the patients
were not on any treatment at the time of examination, Statistical analysis
the patients from the cases group with treatment, had Chi-square or Fisher’s exact test was used to analyze
been on it for less than 2 days. Medical therapy of these categorical variables. Unpaired t-test and Mann–Whitney
patients was selected according to the Mexican Technical Rank Sum test were used for continuous variables; P values
Guideline for Prevention, Diagnosis, and Management were corrected by maternal age using a multiple logistic
of Preeclampsia-Eclampsia [17]. Normotensive women regression analysis. Sensitivity, specificity, predictive positive
from the control group did not have any hypo tensor (PPV) and negative (NPV) values were calculated according
treatment at the moment of the US, nor did they have to the Bayes theorem. Statistically, P values < 0.05 were
co-morbidities associated to IUGR. Multiple pregnancies, considered significant. Statistical analysis was performed
pregnancies with structural or chromosomal fetus mal- using the SigmaPlot software v11.
formations, no feasibility to undergo the Doppler US test
(obesity, oligohydramnios, etc.) were excluded from the Results
study. The protocol was approved by the Institutional A total of 102 Mexican women were recruited and
Review Board (ID number R-2010-1905-17). All patients sub-divided in two groups: 65 formed the cases group
provided written informed consent for their participation. (38 mild and 27 severe PE) and 37 were the control group.
56.9% of the cases were diagnosed with PE before 34 GW
Doppler US evaluation (early PE) and the remaining 43.1% had a late onset of
To determine the Doppler US pattern, only one exam disease (34–37 GW). General characteristics of the
on each patient was carried out at the recruitment time. study population are shown in Table 1. The median of GW
The Doppler US was performed by trans-abdominal was 34 for the cases (ranging from 24.5 to 37 GW) and 32
examination with a Toshiba Power Vision 6000 SSA- (ranging from 24 to 37 GW) for controls, respectively.
370A model, with a 3.5 MHz convex transducer. The Maternal age, was the only characteristic with statistical
examination included one uterine artery from the difference among groups (29.1 for the cases and 26.1 for
placental side or the mean if there was a symmetrical the controls, P = 0.019). There were no differences in risk
placenta, the umbilical artery, and one middle cerebral factors such as past personal or familial history of PE, pri-
artery (indistinct hemisphere) [18,19]. Umbilical artery mipaternity and nulliparity, among study groups (Table 1).
measures were taken in a free umbilical cord loop. In Table 2 summarizes the ultrasound findings classified
order to register the values, four out of five spectral by artery and its comparison between cases and controls.
continuous and identical waves were considered, after The proportion of patients with PE and an abnormal
verification of regular maternal and fetal cardiac frequency, Doppler US for the uterine artery was statistically significant
without breath and/or fetal movement interference. The (OR = 2.6, 95% CI = 1.01 – 6.68, P = 0.047). The N presence
Doppler insonation angle was maintained below 60 degrees. was restricted only for the cases group in a proportion of
All the US evaluations were performed by a gynecologist 20% (OR = 9.0, 95% CI = 1.127 - 71.887, P = 0.032). The
with maternal-fetal medicine experience. The results medians of RI and PI parameters of the uterine artery
were documented on a record sheet designed for the showed a close gap between the study groups and therefore
study, as well as in the clinical record of each patient. they were not associated to PE (P values > 0.05). The me-
The abnormality in the wave morphology was considered dian of umbilical RI and PI were 0.59 and 0.91 for the cases
as the presence of a protodiastolic N after the 24 GW in group and 0.51 and 0.78 for the control group, respectively.
the uterine artery [20]. RI and PI values above the 95th There was a positive association between individual values
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Table 1 Comparison of general characteristics between study groups

Characteristic PE Controls P value
(n = 65) (n = 37)
Maternal age years, mean (range) 29.1 (15–42) 26.1 (17–36) 0.019*
Gestational age weeks, median (range) 34 (24.5-37) 32 (24–37) 0.084
Number of pregnancies, median (range) 2 (1–9) 2 (1–6) 0.608
Past history of PE, n (%) 10 (15.4) 1 (2.7) 0.098
Familial history of PE, n (%) 9 (13.8) 1 (2.7) 0.141
Primipaternity n (%) 24 (36.9) 11 (29.7) 0.604
Nulliparous, n (%) 26 (40.0) 11 (29.7) 0.410
Blood pressure systolic, median (range) 140 (130–179) 100 (90–122) < 0.001
Blood pressure diastolic, median (range) 90 (50–120) 70 (50–80) < 0.001
*
Statistical significance.

of abnormal umbilical RI or PI and PE (OR = 30.63, In the umbilical artery the most frequent altered parameter
95% CI = 1.47 – 639.71, P = 0.027, and OR = 10.82, 95% was the RI (17% in the cases group and 4% for the controls).
CI = 2.19 – 53.58, P = 0.004, respectively); however, The combination of abnormal RI + PI was detected in
considering the general Doppler result for this artery, 65.2% of the cases with abnormal Doppler US for this
differences between proportions of abnormal umbil- artery versus 8.7% of the control pregnancies. Considering
ical Doppler US in the study groups were not observed the abnormal middle cerebral artery results, 53.8% of
(P = 0.107). An abnormal PI was the only middle cerebral women showed altered PI and SP individual parameters
artery parameter associated to PE (OR = 0.243, 95% in the cases group; this condition was present only in
CI = 0.08 – 0.70, P = 0.009). 3.2% of the controls.
Figure 1 shows the frequencies of the most common Table 3 displays the Doppler US parameters ability to
abnormal US findings, including the parameters combina- classify the study groups. The general Doppler result had
tions for each artery. In the uterine artery, the most frequent the most representative values with specificity and PPV
abnormal parameter in its individual form and the most fre- of 75.7% and 78.6%, respectively. The sensitivity and the
quent abnormal combination for both the cases and con- NPV for the general US examination were calculated in
trols were the RI (17% for cases and 6.9% for controls) and 50.8% and 46.7%, respectively.
the RI + PI (31% for cases and 3.4% for controls) respect-
ively. The N presence and its combination with altered RI Discussion
(RI + N) and the combination between abnormal RI, PI and Most of reports related to PE evaluation by Doppler US
N (RI + PI + N), only had representation in the cases group. have been focused on the study of the uterine artery and

Table 2 Classification of Doppler US findings by artery in the study groups

PE Controls
Artery Ultrasound finding P value†
(n = 65) (n = 37)
RI, median (range) 0.54 (0.2-1) 0.51 (0.31-0.62) 0.131
PI, median (range) 0.84 (0.42-1.7) 0.79 (0.44-1.9) 0.510
Uterine
Notch proportion (%) 20 0.0 0.032*
Uterine abnormal Doppler US proportion (%) 44.6 21.6 0.047*
RI, median (range) 0.59 (0.31-1.1) 0.51 (0.28-0.76) 0.027*
Umbilical PI, median (range) 0.91 (0.42-1.9) 0.78 (0.35-1.26) 0.004*
Umbilical abnormal Doppler US proportion (%) 49.2 29.7 0.107
RI, median (range) 0.76 (0.5-1) 0.83 (0.4-1.3) 0.500
PI, median (range) 1.4 (0.9-2.66) 1.815 (1.11-2.81) 0.009*
Middle cerebral
SP, mean (range) 0.462 (0.22-0.80) 0.434 (0.18-0.60) 0.218
Cerebral abnormal Doppler US proportion (%) 23.1 18.9 0.911
Proportion of Abnormal Doppler US (%) 47.7 24.3 0.021*
†
P value adjusted by maternal age. *Statistical significance.
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Figure 1 Proportions of the most common abnormal US findings and their combinations for each artery.

its parameters [22-24]; there are descriptive trials about the more informative and accurate report [32-35]. In this study,
hemodynamic changes during pregnancy [25], studies to we report a full Doppler US vision about PE induced vascu-
determine the normality ranges of the Doppler US values lar changes in the mother, reflected as vascular changes in
in some populations [26,27], and reports in which the aim the uterine artery, and in the fetus, considered as alter-
has been to get a spectral pattern of Doppler US to predict ations in umbilical and middle cerebral artery parameters;
which pregnancies will evolve to PE [28-31]. Only a few additionally, these abnormal Doppler US measurements
papers provide an extended description of other vessels in were disaggregated for each examined vessel.
PE evaluation, and even fewer have shown the combination In our study, maternal age was the only known PE risk
of two or more arteries with the objective of establishing a factor with differences among groups [36,37]. Despite

Table 3 Effectiveness of Doppler US in PE discrimination: accuracy of general Doppler US result by artery and
their combinations
Artery Parameter Sensitivity (%) Specificity (%) PPV† (%) PNV‡ (%)
RI 7.7 94.6 71.4 36.8
N 6.2 100.0 100.0 37.8
RI + PI 13.8 97.3 90.0 39.1
Uterine
RI + N 4.6 100.0 100.0 37.4
RI + PI + N 7.7 100.0 100.0 38.1
Abnormal Doppler US of uterine artery 44.6 78.4 78.4 44.6
RI 1.5 100.0 100.0 36.6
PI 6.2 97.3 80.0 37.1
Umbilical
RI + PI 23.1 94.6 88.2 41.2
Abnormal Doppler US of umbilical artery 49.2 70.3 74.4 44.1
RI 10.8 100.0 100.0 38.9
SP 10.8 97.3 87.5 38.3
PI + SP 6.2 97.3 80.0 37.1
Middle Cerebral
RI + PI 1.5 91.9 25.0 34.7
SP + RI + PI 3.1 100.0 100.0 37.0
Abnormal Doppler US of cerebral artery 23.1 81.1 68.2 37.5
Abnormal Doppler US 50.8 75.7 78.6 46.7
†
PPV: Predictive positive value. ‡PNV: Predictive negative value.
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the fact that nulliparity, personal history and/or family of Conclusion

PE have been supported as PE risk factors in several studies General Doppler US result, as well as N from uterine
[38,39], our results showed no association between these vessel, RI from umbilical artery, and PI from umbilical
characteristics and PE; however, these data should be and middle cerebral arteries in their individual form,
cautiously interpreted due to the small number of patients may be considered as tools to determine hemodynamic
included in the study. repercussion caused by PE.
Considering the Doppler US findings for motherhood
Abbreviations
status, from individual parameters evaluated in the uterine PE: Preeclampsia; US: Ultrasound; RI: Resistance index; PI: Pulsatility index;
artery, N showed to be the most meaningful (but not the N: Notch; SP: Systolic peak; IUGR: Intrauterine growth retardation; GW: Weeks
most frequent) individual finding, due to the fact that its of gestation; PPV: Predictive positive value; NPV: Negative predictive value.
presence was restricted to the cases group. These results
Competing interests
are similar to those reported previously, where the N is The authors declare that they have no competing interests. The authors are
considered as a relevant parameter in the uterine artery responsible for the content and writing of the research paper.
study [40,41]. Although PI and RI are considered funda-
mental values in the uterine artery evaluation, we did Authors’ contributions
MALM, MLMF, drafted the manuscript. MALM, VMG, RCF, RMRG, MAOT, and
not find differences in these parameters among the study MLMF, participated in the design of the study and in the coordination
groups. It could be because the reference values considered of the patients’ recruitment. MALM, VMG, RCF, RMRG, MAOT, IGV, MIMA, and
in previous studies consisted of standardized measures for JIBA, participated in data acquisition, data analysis and interpretation,
they participated in manuscript review. MLMF conceived of the study, and
each population, and the abnormality limits of these values participated in its design and coordination, and performed the statistical
may differ between populations [40]. analysis. All authors read and approved the final manuscript.
In the fetal condition, the umbilical artery has been
Acknowledgments
related typically to pregnancy outcome, while the middle We thank all the study participants. Also, the authors gratefully acknowledge
cerebral artery has been considered as a fetal circulation the critical reading and correction of this manuscript by María Guadalupe
marker and a useful non-invasive tool in risk assessment Ramos del Hoyo, M.E. This study was funded by FOMIX CONACyT-Gobierno
del Estado de Zacatecas Grant (ID number: 121535).
for fetal anemia [42-45]. In our study, as individual
measurements, abnormal RI from umbilical artery, and Author details
1
altered PI from umbilical and middle cerebral arteries, Departamento de Radiologia e Imagen, Unidad Medica de Alta Especialidad
No. 25 Instituto Mexicano del Seguro Social, Monterrey, Mexico. 2Unidad
were associated to PE; however, considering all the pa- Medica Materno-Fetal del Noreste, Unidad Medica de Alta Especialidad No.
rameters reviewed in these arteries, the general results 23 Instituto Mexicano del Seguro Social, Monterrey, Mexico. 3Molecular
for each vessel did not show a difference between Medicine Laboratory, Unidad Academica de Medicina Humana y Ciencias de
la Salud, Universidad Autonoma de Zacatecas, Carretera
groups, suggesting that these individual parameters, but Zacatecas-Guadalajara Km. 6, C.P. 98160 Zacatecas, Mexico.
not the general Doppler US for these arteries, could be
considered as indicators to evaluate the specific PE Received: 2 August 2013 Accepted: 15 November 2013
Published: 19 November 2013
vascular alterations.
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