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Fetal middle cerebral artery Doppler indices and clinical application at Korle Bu Teaching Hospital, Accra, Ghana
IJG-08671; No of Pages 5 International Journal of Gynecology and Obstetrics xxx (2016) xxx–xxx
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International Journal of Gynecology and Obstetrics journal homepage: www.elsevier.com/locate/ijgo
CLINICAL ARTICLE
Fetal middle cerebral artery Doppler indices and clinical application at Korle Bu Teaching Hospital, Accra, Ghana Joseph D. Seffah a,⁎, Alim Swarray-Deen b a b
Department of Obstetrics and Gynaecology, University of Ghana School of Medicine and Dentistry, Accra, Ghana Department of Obstetrics and Gynaecology, Korle Bu Teaching Hospital, Accra, Ghana
a r t i c l e
i n f o
Article history: Received 21 August 2015 Received in revised form 24 November 2015 Accepted 4 April 2016 Keywords: Accra Doppler indices Fetus Middle cerebral artery
a b s t r a c t Objective: To determine normal ranges for various Doppler flow velocity indices of the fetal middle cerebral artery (MCA) and their trends in normal pregnancies at Korle Bu Teaching Hospital, Accra, Ghana. Methods: A prospective cross-sectional study was conducted at Korle Bu Teaching Hospital in 2015. Included women had a singleton pregnancy of 20–40 weeks' duration, dated using an early ultrasonography scan, and normal fetal growth. Interviews were conducted to collect data on sociodemographic characteristics, followed by Doppler ultrasonography of the MCA. The resistive index, pulsatility index, systolic-to-diastolic ratio, and peak systolic velocity of the MCA were determined for all participants. Results: Overall, 458 pregnant women were recruited. The peak systolic velocity increased with advancing gestational age and a positive correlation of r = 0.725 (P b 0.001) was demonstrated between the peak systolic velocity and the gestational age. The resistive index, pulsatility index, and systolic-to-diastolic ratio of the MCA decreased with advancing gestational age in a parabolic pattern. Conclusion: The reference curve for the peak systolic velocity increases with gestational age, whereas the other indices decrease in a parabolic pattern. © 2016 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction Fetal surveillance in contemporary practice involves the use of Doppler ultrasonography of fetal vessels. Commonly used vessels include the umbilical vessels, the middle cerebral artery (MCA), the ductus venosus, and the uterine artery. These tests provide important information for the diagnosis and monitoring of fetal conditions that is not readily obtained from more routine tests of fetal well-being [1]. The umbilical artery is the most common vessel assessed by Doppler ultrasonography for the monitoring of the compromised fetus and to determine the timing of delivery. The role of the MCA is well established in the diagnosis of fetal anemia [2]. Some clinicians strongly support the use of MCA flow velocimetry to obtain information in conditions such as fetomaternal hemorrhage [3], fetal hypoxia, and adverse perinatal outcome [4]. With improved ultrasonography resolution and color Doppler imaging, Doppler assessment of the MCA has become the gold standard in the assessment of intracranial fetal vessels [5]. Normally, the fetal cerebral circulation is a continuous, forward, low flow with high impedance. In the presence of fetal hypoxemia secondary to placental insufficiency, the blood flow is redistributed to the brain, heart, and adrenal glands, with decreased resistance allowing ⁎ Corresponding author at: Department of Obstetrics and Gynaecology, University of Ghana School of Medicine and Dentistry, P.O. Box 4236, Accra, Ghana. Tel.: +233 243310011; fax: +233 302 663062. E-mail address: [email protected] (J.D. Seffah).
for increased blood flow and oxygen delivery to the brain [6]. Using Doppler studies, this decreased MCA impedance can manifest as the “brain-sparing reflex,” which has been proposed as an early indicator of autoregulation in cases of intrauterine growth restriction (IUGR) [7,8]. Despite the fact that ultrasonography was introduced relatively early in Africa (at the University of Cape Town, South Africa, in 1970) [9], Africa is the continent where the lowest number of obstetric and Doppler ultrasonography scans are performed. Although the commercialization of medical care has led to the excessive use of obstetric scans in some urban areas of Africa, pulsed-wave Doppler waveform analysis is not commonly done. This may be as a result of the high combined cost of equipment with pulsed-wave Doppler technology and of the training of healthcare workers in operating the units and interpreting results. For most lowincome countries, such technology is restricted to a few centers [10]. During the past 10 years, no fewer than 50 works on fetal Doppler ultrasonography from hospital groups and services from across Africa have been published in various national and specialist African journals [11]. Most of the studies have been related to assessment of the fetal MCA in patients with pre-eclampsia [12–14]. The MCA is the most studied fetal brain artery because it is simple to access. Numerous studies have been conducted to establish a normal reference range for common application [8–12]. However, studies from different parts of the world have indicated the possibility of loco-regional differences in the normal range, implying the need to construct local reference ranges and to follow the local range if it differs from published values.
http://dx.doi.org/10.1016/j.ijgo.2015.11.027 0020-7292/© 2016 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
Please cite this article as: Seffah JD, Swarray-Deen A, Fetal middle cerebral artery Doppler indices and clinical application at Korle Bu Teaching Hospital, Accra, Ghana, Int J Gynecol Obstet (2016), http://dx.doi.org/10.1016/j.ijgo.2015.11.027
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J.D. Seffah, A. Swarray-Deen / International Journal of Gynecology and Obstetrics xxx (2016) xxx–xxx
Table 1 Demographic information and Doppler indices of the middle cerebral artery by gestational age (n = 458).a Gestational age, wk
No.
Age, y
Pulsatility index
Resistive index
Peak systolic velocity, cm/s
S/D ratio
20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40
20 20 20 20 25 20 21 20 20 20 23 22 22 22 23 25 22 24 24 23 22
30.90 ± 6.40 28.30 ± 3.80 29.00 ± 6.30 29.20 ± 4.30 33.40 ± 4.30 28.40 ± 6.40 29.40 ± 6.20 30.40 ± 4.60 30.10 ± 3.50 30.70 ± 5.70 28.30 ± 6.90 30.00 ± 4.60 32.00 ± 6.60 34.60 ± 4.80 32.60 ± 3.90 30.60 ± 4.30 29.20 ± 5.10 30.50 ± 2.90 28.80 ± 6.20 30.10 ± 4.70 31.30 ± 3.60
1.48 ± 0.30 1.60 ± 0.35 1.81 ± 0.35 1.65 ± 0.41 1.46 ± 0.23 1.35 ± 0.46 1.59 ± 0.28 1.85 ± 0.40 1.80 ± 0.52 1.70 ± 0.41 1.83 ± 0.29 1.83 ± 0.24 1.69 ± 0.25 1.64 ± 0.40 1.53 ± 0.19 1.46 ± 0.34 1.45 ± 0.24 1.48 ± 0.29 1.29 ± 0.33 1.39 ± 0.38 0.99 ± 0.05
0.75 ± 0.06 0.75 ± 0.09 0.79 ± 0.05 0.77 ± 0.04 0.69 ± 0.20 1.03 ± 0.35 0.81 ± 0.06 0.82 ± 0.07 0.82 ± 0.10 0.79 ± 0.08 0.82 ± 0.05 0.82 ± 0.05 0.80 ± 0.08 0.80 ± 0.10 0.80 ± 0.03 0.77 ± 0.06 0.80 ± 0.07 0.78 ± 0.06 0.73 ± 0.08 0.74 ± 0.09 0.67 ± 0.05
23.30 ± 6.50 27.40 ± 7.40 30.00 ± 7.30 27.20 ± 7.90 27.10 ± 2.40 27.80 ± 7.40 29.40 ± 6.90 32.10 ± 12.10 34.60 ± 7.70 38.50 ± 11.50 44.60 ± 8.80 44.70 ± 9.80 47.30 ± 8.00 44.00 ± 11.10 48.40 ± 9.90 51.30 ± 8.40 51.70 ± 10.50 51.50 ± 11.10 48.90 ± 8.80 56.10 ± 15.60 53.70 ± 11.60
4.99 ± 1.64 5.36 ± 1.89 5.26 ± 2.03 5.25 ± 1.22 4.29 ± 0.75 5.61 ± 1.19 5.20 ± 1.29 9.95 ± 12.41 8.44 ± 1.79 7.21 ± 1.45 6.15 ± 1.45 6.41 ± 1.39 6.73 ± 1.59 5.97 ± 2.07 5.35 ± 1.21 4.48 ± 1.22 5.04 ± 1.40 5.11 ± 1.36 4.20 ± 1.68 4.13 ± 1.43 3.07 ± 0.63
Abbreviation: S/D, systolic to diastolic. a Values are given as mean ± SD unless indicated otherwise.
Therefore, the aim of the present study was to evaluate the range of normal local values at Korle Bu Teaching Hospital, Accra, Ghana. 2. Materials and methods The present study was a prospective cross-sectional study conducted between January 5 and May 30, 2015, at the maternity unit of the obstetrics department at Korle Bu Teaching Hospital, which is affiliated with the Medical School of the University of Ghana. The inclusion criteria were: a low-risk singleton pregnancy; a pregnancy duration of 20–40 weeks, with the pregnancy dated using early ultrasonography before 12 weeks of pregnancy; and normal fetal growth (growth curve between the 10th and 90th percentiles). The exclusion criteria were evidence of congenital or fetal structural anomaly on the sonogram; oligohydramnios as confirmed by an amniotic fluid index of less than 5; abnormal fetal biometry with an estimated fetal weight below the 10th percentile or above the 90th percentile (IUGR, small
for gestational age, or large for gestational age); a history of smoking and alcohol consumption during the index pregnancy; and chronic medical conditions (hypertension, diabetes mellitus, autoimmune disorders). The study aims were explained to the women and all participants were asked to provide written informed consent before any ultrasonography was performed. The study was approved by the Ethical and Protocol Review Committee of the College of Health Sciences, University of Ghana. Before the ultrasonography examination, participants were interviewed and a questionnaire was completed that included details of sociodemographic characteristics and obstetric history. All ultrasonography examinations were performed by J.D.S. and A.S-D, who had been trained in obstetric ultrasonography and Doppler imaging. The examinations were performed with the woman placed in a recumbent or semirecumbent position. Initially, greyscale ultrasonography was performed to evaluate for multiple pregnancies and to assess parameters related to the fetal anatomy and biophysical profile, including
Table 2 Percentile values for Doppler indices of the middle cerebral artery according to gestational age (n = 458). Gestational age, wk
20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40
Pulsatility index
Resistive index
Peak systolic velocity
S/D ratio
5th
50th
95th
5th
50th
95th
5th
50th
95th
5th
50th
95th
1.19 1.19 1.21 1.24 1.18 0.69 1.15 1.19 1.03 0.91 1.42 1.51 1.41 1.11 1.29 1.08 1.03 1.01 0.96 0.77 0.92
1.41 1.43 1.95 1.54 1.43 1.50 1.56 1.96 1.96 1.92 1.75 1.77 1.54 1.66 1.52 1.32 1.38 1.53 1.14 1.37 0.99
2.10 2.11 2.20 2.20 1.96 1.86 2.10 2.30 2.60 2.10 2.12 2.20 2.00 2.04 1.83 2.10 1.86 1.98 1.98 1.98 1.05
0.68 0.60 0.68 0.71 0.18 0.77 0.71 0.70 0.65 0.64 0.74 0.73 0.62 0.61 0.75 0.70 0.64 0.70 0.66 0.58 0.62
0.77 0.74 0.80 0.78 0.72 0.85 0.80 0.84 0.84 0.81 0.83 0.84 0.84 0.81 0.80 0.73 0.80 0.77 0.68 0.75 0.65
0.83 0.89 0.86 0.83 0.84 1.55 0.89 0.90 0.95 0.89 0.88 0.87 0.87 0.88 0.84 0.88 0.86 0.86 0.88 0.88 0.76
13.00 17.00 20.00 18.00 22.00 15.00 18.00 7.20 20.00 25.00 30.00 29.00 35.50 27.10 31.00 38.70 40.00 38.00 34.90 33.00 33.00
24.00 24.80 27.50 25.60 27.80 28.10 32.30 35.40 36.40 36.00 43.20 43.90 46.50 44.80 51.00 48.40 51.00 52.60 51.60 55.00 55.50
33.00 41.00 41.00 43.40 29.70 42.60 39.00 46.50 42.50 65.50 54.20 61.00 62.00 56.00 63.00 64.00 68.00 69.10 64.50 95.20 67.80
3.31 3.55 0.89 3.90 3.54 4.20 3.54 4.33 2.80 2.71 4.10 4.55 4.20 3.17 4.20 3.38 2.78 3.33 2.91 2.34 2.65
4.44 4.41 5.40 5.14 4.20 5.03 5.10 6.85 7.70 6.33 5.60 6.45 7.20 5.63 5.20 3.80 4.94 4.37 3.15 3.60 2.86
7.40 8.90 9.20 7.70 6.10 7.50 6.69 46.00 8.35 7.30 8.20 8.90 8.90 8.30 7.20 7.50 6.89 6.92 8.33 7.00 4.14
Abbreviation: S/D, systolic to diastolic.
Please cite this article as: Seffah JD, Swarray-Deen A, Fetal middle cerebral artery Doppler indices and clinical application at Korle Bu Teaching Hospital, Accra, Ghana, Int J Gynecol Obstet (2016), http://dx.doi.org/10.1016/j.ijgo.2015.11.027
J.D. Seffah, A. Swarray-Deen / International Journal of Gynecology and Obstetrics xxx (2016) xxx–xxx
abdominal circumference, head circumference, femur length, and biparietal diameter. The fetal weight was estimated using the Hadlock formulas [15]. Furthermore, the amniotic fluid volume and the placental grade were evaluated. This preliminary examination lasted 5–15 min. Thereafter, Doppler examination was performed using a Philips ClearVue 350 (Philips, Andover, MA, USA) ultrasonography machine with a 3.5-MHz curvilinear transducer. Color flow mapping was used to identify the circle of Willis and the proximal MCA, which is easily identified along the lesser wing of the sphenoid at the level of cerebral peduncles. The pulsed-wave Doppler gate was then placed at the proximal third of the MCA, within 1 cm of the origin of the MCA. The angle between the ultrasound beam and direction of blood flow was kept below 30°. The waveforms were quantified immediately after freezing the image using 3–10 consecutive waveforms. The peak systolic velocity (PSV), defined as the highest point of the waveform, was measured using manual calipers, and the resistive index (RI), pulsatility index (PI), and systolic-to-diastolic (S/D) ratio were calculated. Care was taken to apply minimal pressure to the maternal abdomen to avoid fetal head compression [16]. During the study period, all women who met the inclusion criteria were recruited. The sample size was calculated using the formula: n = Z [2] × (P) × (1 – P)/C2, assuming P = 0.5 (maximum variability), C = confidence interval of 95%, and Z = 1.96 (margin of random error). To correct for subgroup variability, 20% was added to the sample size. A minimum of 20 participants was to be recruited for each week of pregnancy (weeks 20–40). The collected data were entered into an Excel 2013 (Microsoft, Redmond, WA, USA) spreadsheet and the statistical analysis was performed using SPSS version 22 (IBM, Amonk, NY, USA). The t test was used as a test of significance, with P b 0.05 considered statistically significant. Pearson correlation and regression analyses were used to evaluate the correlation between the ultrasonography indices and the gestational age. Reference ranges (5th, 50th, and 95th percentiles) and their 95% confidence intervals were constructed for each parameter. The percentile values of the ultrasonography indices were calculated and compared with those from published international studies. 3. Results A total of 788 women attending the prenatal clinic at Korle Bu Teaching Hospital underwent an ultrasonography examination during the study period, but only 470 met the inclusion criteria. No woman declined the scan, but for 12 women, no MCA Doppler scan could be attained because of technical difficulties. Therefore, 458 women were included. The MCA indices were measured successfully for the 458 women, and the entire process took 5–15 min per woman. The mean age of the study participants was 30.4 ± 5.3 years. Overall, 375 (81.9%) women had a parity of two or less, and 158 (34.5%) were nulliparous. The Doppler results obtained from the women are tabulated in Table 1 and the reference nomograms of the Doppler indices are shown in Table 2 and Figs. 1–4. The PSV of the MCA ranged from 7.2 cm/s to 95.2 cm/s, with a mean of 40.5 cm/s, a median of 29.6 cm/s, and a standard deviation of 14.0 cm/s. There was a strong positive correlation between the PSV and gestational age (r = 0.725, P b 0.001) indicating that the PSV increases with increasing gestational age. The reference curve of the PI, RI, and S/D ratio had a parabolic shape with a decrease after the 28th week of pregnancy for the RI and after the 30th week for PI and S/D ratio (Figs. 1, 2, and 4). A negative linear correlation between the gestational age and the PI (r = −0.260, P b 0.001) and between the gestational age and the S/D ratio (r = − 0.123, P b 0.001) was also seen. There was a strong positive linear correlation between the RI and the PI (r = 0.284, P = 0.006), between the RI and the S/D ratio (r = 0.323, P b 0.001), and between the PI and the S/D ratio (r = 0.432, P b 0.001).
3
Fig. 1. Pulsatility index in the middle cerebral artery (n = 458). Individual measurements (circles) and calculated reference ranges (lines) are shown; the reference boundaries include 95% of the sample population (P b 0.001). Abbreviations: GA, gestational age; PI, pulsatility index.
4. Discussion The present study has demonstrated that the PSV of the MCA increases continuously with advancing gestational age. The reference curves of the other ultrasonography indices (PI, RI, S/D ratio) had a parabolic shape with an overall decrease after the 28th week of pregnancy. Most of the published studies on Doppler indices of the MCA identified a similar pattern, albeit with reference ranges that can vary considerably. Potential reasons for such differences include the experience or skill of the sonographer, the techniques used, and the statistical tools applied. The present percentile distribution of the MCA PSV was compared with results from Iran [17], Brazil [18], and India [19]. These studies demonstrated a continuous increase in the PSV from 20 weeks of pregnancy to 40 weeks [17], from 23 weeks to 35 weeks [18], and from 12 weeks to 39 weeks [19]. Despite some differences in the actual PSV values, the present reference ranges were overall in good agreement with previously reported ranges [8,17,20].
Fig. 2. Resistive index in the middle cerebral artery (n = 458). Individual measurements (circles) and calculated reference ranges (lines) are shown; the reference boundaries include 95% of the sample population (P ≤ 0.006). Abbreviations: GA, gestational age; RI, resistive index.
Please cite this article as: Seffah JD, Swarray-Deen A, Fetal middle cerebral artery Doppler indices and clinical application at Korle Bu Teaching Hospital, Accra, Ghana, Int J Gynecol Obstet (2016), http://dx.doi.org/10.1016/j.ijgo.2015.11.027
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J.D. Seffah, A. Swarray-Deen / International Journal of Gynecology and Obstetrics xxx (2016) xxx–xxx
Fig. 3. Peak systolic velocity in the middle cerebral artery (n = 458). Individual measurements (circles) and calculated reference ranges (lines) are shown; the reference boundaries include 95% of the sample population (P b 0.001). Abbreviations: GA, gestational age; PSV, peak systolic velocity.
The nomogram for the RI was compared with results from the USA [9] and Germany [20]. The present reference curves had a parabolic shape (RI at 20 weeks: 0.75; RI at 28 weeks: 0.82; RI at 40 weeks: 0.67) similar to that seen in the other studies, but with some differences in the actual reference values. The present values were closest to those reported for the USA [8]. When compared with the RI reference curves published by Tarzamni et al. in Iran [17], the present curves showed an almost identical parabolic pattern for the period of 20–40 weeks of pregnancy. Most previous studies have demonstrated a parabolic shape for the reference curves of the MCA PI, usually with a fall after the 28th week of pregnancy. This fall has been attributed to a decreasing vascular impedance with increasing gestational age [21]. We compared the present values with the reference ranges published by Baschat et al. [7] and Tarzamni et al. [17]. The parabolic patterns of the previously published reference curves were similar to those in the present study, but the PI values in both studies were higher. A possible reason for this discrepancy may be pressure exerted by the ultrasonography probe on the fetal
head, which can lead to extremely low end-diastolic flow velocities resulting in higher PI values. Most previous Doppler studies of the fetal MCA were performed for the detection of fetal anemia resulting from Rhesus isoimmunization or parvovirus infection, both of which are rare occurrences in the Sub-Saharan population (the frequency of the Rhesus-negative allele in Africans is approximately 3%). Doppler assessment of the MCA also plays an important part in the identification of IUGR and is based on blood flow redistribution associated with fetal hypoxia. The West African subregion alone accounts for 11.4% of all infants with a low birth weight worldwide, with most cases being related to IUGR [22]. The major determinants of such growth retardation in utero are related to maternal nutritional deficiencies (iron-deficiency anemia), malaria, sickle cell disease, and the high rate of maternal HIV infection in this region. The ratio of MCA PI to the umbilical artery PI (i.e. cerebroplacental ratio) has been shown to be a good measure of redistribution of cardiac output to the cerebral vessels and it is predictive of adverse perinatal outcome in both growth-restricted fetuses and appropriate-forgestational-age fetuses [23]. Several studies have reported that the cerebroplacental ratio is a better predictor of adverse outcome than are the MCA or umbilical artery Doppler indices alone [23–25]. Even with the introduction of affordable ultrasonography hardware, medical ultrasonography machines with added color Doppler and pulsed-wave functions come at a very high price. Most healthcare facilities with an ultrasonography device can only perform standard two-dimensional scans. Another potential limitation to the use of Doppler assessment of the fetal MCA is the fact that there are very few trained individuals who can offer a level 2 or 3 obstetric scan and even fewer who are trained in fetal medicine. Therefore, even in clinical scenarios when a Doppler study of the MCA is indicated, the low awareness, added cost, and accessibility of such services serve as major deterrents. The present reference curves for Doppler indices of the MCA demonstrated a similar pattern to the ones reported in other regions. Because Doppler assessment of the MCA represents a rapid, reproducible, simple, and reliable method with minimal interobserver and intraobserver variability, it can be used in fetal monitoring for highrisk pregnancies—especially those complicated by IUGR—at Korle Bu Teaching Hospital.
Conflict of interest The authors have no conflicts of interest.
References
Fig. 4. Systolic-to-diastolic ratio in the middle cerebral (n = 458). Individual measurements (circles) and calculated reference ranges (lines) are shown; the reference boundaries include 95% of the sample population (P b 0.009). Abbreviations: GA, gestational age; S/D ratio, systolic-to-diastolic ratio.
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Please cite this article as: Seffah JD, Swarray-Deen A, Fetal middle cerebral artery Doppler indices and clinical application at Korle Bu Teaching Hospital, Accra, Ghana, Int J Gynecol Obstet (2016), http://dx.doi.org/10.1016/j.ijgo.2015.11.027
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International Journal of Gynecology and Obstetrics journal homepage: www.elsevier.com/locate/ijgo
CLINICAL ARTICLE
Fetal middle cerebral artery Doppler indices and clinical application at Korle Bu Teaching Hospital, Accra, Ghana Joseph D. Seffah a,⁎, Alim Swarray-Deen b a b
Department of Obstetrics and Gynaecology, University of Ghana School of Medicine and Dentistry, Accra, Ghana Department of Obstetrics and Gynaecology, Korle Bu Teaching Hospital, Accra, Ghana
a r t i c l e
i n f o
Article history: Received 21 August 2015 Received in revised form 24 November 2015 Accepted 4 April 2016 Keywords: Accra Doppler indices Fetus Middle cerebral artery
a b s t r a c t Objective: To determine normal ranges for various Doppler flow velocity indices of the fetal middle cerebral artery (MCA) and their trends in normal pregnancies at Korle Bu Teaching Hospital, Accra, Ghana. Methods: A prospective cross-sectional study was conducted at Korle Bu Teaching Hospital in 2015. Included women had a singleton pregnancy of 20–40 weeks' duration, dated using an early ultrasonography scan, and normal fetal growth. Interviews were conducted to collect data on sociodemographic characteristics, followed by Doppler ultrasonography of the MCA. The resistive index, pulsatility index, systolic-to-diastolic ratio, and peak systolic velocity of the MCA were determined for all participants. Results: Overall, 458 pregnant women were recruited. The peak systolic velocity increased with advancing gestational age and a positive correlation of r = 0.725 (P b 0.001) was demonstrated between the peak systolic velocity and the gestational age. The resistive index, pulsatility index, and systolic-to-diastolic ratio of the MCA decreased with advancing gestational age in a parabolic pattern. Conclusion: The reference curve for the peak systolic velocity increases with gestational age, whereas the other indices decrease in a parabolic pattern. © 2016 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction Fetal surveillance in contemporary practice involves the use of Doppler ultrasonography of fetal vessels. Commonly used vessels include the umbilical vessels, the middle cerebral artery (MCA), the ductus venosus, and the uterine artery. These tests provide important information for the diagnosis and monitoring of fetal conditions that is not readily obtained from more routine tests of fetal well-being [1]. The umbilical artery is the most common vessel assessed by Doppler ultrasonography for the monitoring of the compromised fetus and to determine the timing of delivery. The role of the MCA is well established in the diagnosis of fetal anemia [2]. Some clinicians strongly support the use of MCA flow velocimetry to obtain information in conditions such as fetomaternal hemorrhage [3], fetal hypoxia, and adverse perinatal outcome [4]. With improved ultrasonography resolution and color Doppler imaging, Doppler assessment of the MCA has become the gold standard in the assessment of intracranial fetal vessels [5]. Normally, the fetal cerebral circulation is a continuous, forward, low flow with high impedance. In the presence of fetal hypoxemia secondary to placental insufficiency, the blood flow is redistributed to the brain, heart, and adrenal glands, with decreased resistance allowing ⁎ Corresponding author at: Department of Obstetrics and Gynaecology, University of Ghana School of Medicine and Dentistry, P.O. Box 4236, Accra, Ghana. Tel.: +233 243310011; fax: +233 302 663062. E-mail address: [email protected] (J.D. Seffah).
for increased blood flow and oxygen delivery to the brain [6]. Using Doppler studies, this decreased MCA impedance can manifest as the “brain-sparing reflex,” which has been proposed as an early indicator of autoregulation in cases of intrauterine growth restriction (IUGR) [7,8]. Despite the fact that ultrasonography was introduced relatively early in Africa (at the University of Cape Town, South Africa, in 1970) [9], Africa is the continent where the lowest number of obstetric and Doppler ultrasonography scans are performed. Although the commercialization of medical care has led to the excessive use of obstetric scans in some urban areas of Africa, pulsed-wave Doppler waveform analysis is not commonly done. This may be as a result of the high combined cost of equipment with pulsed-wave Doppler technology and of the training of healthcare workers in operating the units and interpreting results. For most lowincome countries, such technology is restricted to a few centers [10]. During the past 10 years, no fewer than 50 works on fetal Doppler ultrasonography from hospital groups and services from across Africa have been published in various national and specialist African journals [11]. Most of the studies have been related to assessment of the fetal MCA in patients with pre-eclampsia [12–14]. The MCA is the most studied fetal brain artery because it is simple to access. Numerous studies have been conducted to establish a normal reference range for common application [8–12]. However, studies from different parts of the world have indicated the possibility of loco-regional differences in the normal range, implying the need to construct local reference ranges and to follow the local range if it differs from published values.
http://dx.doi.org/10.1016/j.ijgo.2015.11.027 0020-7292/© 2016 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
Please cite this article as: Seffah JD, Swarray-Deen A, Fetal middle cerebral artery Doppler indices and clinical application at Korle Bu Teaching Hospital, Accra, Ghana, Int J Gynecol Obstet (2016), http://dx.doi.org/10.1016/j.ijgo.2015.11.027
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J.D. Seffah, A. Swarray-Deen / International Journal of Gynecology and Obstetrics xxx (2016) xxx–xxx
Table 1 Demographic information and Doppler indices of the middle cerebral artery by gestational age (n = 458).a Gestational age, wk
No.
Age, y
Pulsatility index
Resistive index
Peak systolic velocity, cm/s
S/D ratio
20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40
20 20 20 20 25 20 21 20 20 20 23 22 22 22 23 25 22 24 24 23 22
30.90 ± 6.40 28.30 ± 3.80 29.00 ± 6.30 29.20 ± 4.30 33.40 ± 4.30 28.40 ± 6.40 29.40 ± 6.20 30.40 ± 4.60 30.10 ± 3.50 30.70 ± 5.70 28.30 ± 6.90 30.00 ± 4.60 32.00 ± 6.60 34.60 ± 4.80 32.60 ± 3.90 30.60 ± 4.30 29.20 ± 5.10 30.50 ± 2.90 28.80 ± 6.20 30.10 ± 4.70 31.30 ± 3.60
1.48 ± 0.30 1.60 ± 0.35 1.81 ± 0.35 1.65 ± 0.41 1.46 ± 0.23 1.35 ± 0.46 1.59 ± 0.28 1.85 ± 0.40 1.80 ± 0.52 1.70 ± 0.41 1.83 ± 0.29 1.83 ± 0.24 1.69 ± 0.25 1.64 ± 0.40 1.53 ± 0.19 1.46 ± 0.34 1.45 ± 0.24 1.48 ± 0.29 1.29 ± 0.33 1.39 ± 0.38 0.99 ± 0.05
0.75 ± 0.06 0.75 ± 0.09 0.79 ± 0.05 0.77 ± 0.04 0.69 ± 0.20 1.03 ± 0.35 0.81 ± 0.06 0.82 ± 0.07 0.82 ± 0.10 0.79 ± 0.08 0.82 ± 0.05 0.82 ± 0.05 0.80 ± 0.08 0.80 ± 0.10 0.80 ± 0.03 0.77 ± 0.06 0.80 ± 0.07 0.78 ± 0.06 0.73 ± 0.08 0.74 ± 0.09 0.67 ± 0.05
23.30 ± 6.50 27.40 ± 7.40 30.00 ± 7.30 27.20 ± 7.90 27.10 ± 2.40 27.80 ± 7.40 29.40 ± 6.90 32.10 ± 12.10 34.60 ± 7.70 38.50 ± 11.50 44.60 ± 8.80 44.70 ± 9.80 47.30 ± 8.00 44.00 ± 11.10 48.40 ± 9.90 51.30 ± 8.40 51.70 ± 10.50 51.50 ± 11.10 48.90 ± 8.80 56.10 ± 15.60 53.70 ± 11.60
4.99 ± 1.64 5.36 ± 1.89 5.26 ± 2.03 5.25 ± 1.22 4.29 ± 0.75 5.61 ± 1.19 5.20 ± 1.29 9.95 ± 12.41 8.44 ± 1.79 7.21 ± 1.45 6.15 ± 1.45 6.41 ± 1.39 6.73 ± 1.59 5.97 ± 2.07 5.35 ± 1.21 4.48 ± 1.22 5.04 ± 1.40 5.11 ± 1.36 4.20 ± 1.68 4.13 ± 1.43 3.07 ± 0.63
Abbreviation: S/D, systolic to diastolic. a Values are given as mean ± SD unless indicated otherwise.
Therefore, the aim of the present study was to evaluate the range of normal local values at Korle Bu Teaching Hospital, Accra, Ghana. 2. Materials and methods The present study was a prospective cross-sectional study conducted between January 5 and May 30, 2015, at the maternity unit of the obstetrics department at Korle Bu Teaching Hospital, which is affiliated with the Medical School of the University of Ghana. The inclusion criteria were: a low-risk singleton pregnancy; a pregnancy duration of 20–40 weeks, with the pregnancy dated using early ultrasonography before 12 weeks of pregnancy; and normal fetal growth (growth curve between the 10th and 90th percentiles). The exclusion criteria were evidence of congenital or fetal structural anomaly on the sonogram; oligohydramnios as confirmed by an amniotic fluid index of less than 5; abnormal fetal biometry with an estimated fetal weight below the 10th percentile or above the 90th percentile (IUGR, small
for gestational age, or large for gestational age); a history of smoking and alcohol consumption during the index pregnancy; and chronic medical conditions (hypertension, diabetes mellitus, autoimmune disorders). The study aims were explained to the women and all participants were asked to provide written informed consent before any ultrasonography was performed. The study was approved by the Ethical and Protocol Review Committee of the College of Health Sciences, University of Ghana. Before the ultrasonography examination, participants were interviewed and a questionnaire was completed that included details of sociodemographic characteristics and obstetric history. All ultrasonography examinations were performed by J.D.S. and A.S-D, who had been trained in obstetric ultrasonography and Doppler imaging. The examinations were performed with the woman placed in a recumbent or semirecumbent position. Initially, greyscale ultrasonography was performed to evaluate for multiple pregnancies and to assess parameters related to the fetal anatomy and biophysical profile, including
Table 2 Percentile values for Doppler indices of the middle cerebral artery according to gestational age (n = 458). Gestational age, wk
20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40
Pulsatility index
Resistive index
Peak systolic velocity
S/D ratio
5th
50th
95th
5th
50th
95th
5th
50th
95th
5th
50th
95th
1.19 1.19 1.21 1.24 1.18 0.69 1.15 1.19 1.03 0.91 1.42 1.51 1.41 1.11 1.29 1.08 1.03 1.01 0.96 0.77 0.92
1.41 1.43 1.95 1.54 1.43 1.50 1.56 1.96 1.96 1.92 1.75 1.77 1.54 1.66 1.52 1.32 1.38 1.53 1.14 1.37 0.99
2.10 2.11 2.20 2.20 1.96 1.86 2.10 2.30 2.60 2.10 2.12 2.20 2.00 2.04 1.83 2.10 1.86 1.98 1.98 1.98 1.05
0.68 0.60 0.68 0.71 0.18 0.77 0.71 0.70 0.65 0.64 0.74 0.73 0.62 0.61 0.75 0.70 0.64 0.70 0.66 0.58 0.62
0.77 0.74 0.80 0.78 0.72 0.85 0.80 0.84 0.84 0.81 0.83 0.84 0.84 0.81 0.80 0.73 0.80 0.77 0.68 0.75 0.65
0.83 0.89 0.86 0.83 0.84 1.55 0.89 0.90 0.95 0.89 0.88 0.87 0.87 0.88 0.84 0.88 0.86 0.86 0.88 0.88 0.76
13.00 17.00 20.00 18.00 22.00 15.00 18.00 7.20 20.00 25.00 30.00 29.00 35.50 27.10 31.00 38.70 40.00 38.00 34.90 33.00 33.00
24.00 24.80 27.50 25.60 27.80 28.10 32.30 35.40 36.40 36.00 43.20 43.90 46.50 44.80 51.00 48.40 51.00 52.60 51.60 55.00 55.50
33.00 41.00 41.00 43.40 29.70 42.60 39.00 46.50 42.50 65.50 54.20 61.00 62.00 56.00 63.00 64.00 68.00 69.10 64.50 95.20 67.80
3.31 3.55 0.89 3.90 3.54 4.20 3.54 4.33 2.80 2.71 4.10 4.55 4.20 3.17 4.20 3.38 2.78 3.33 2.91 2.34 2.65
4.44 4.41 5.40 5.14 4.20 5.03 5.10 6.85 7.70 6.33 5.60 6.45 7.20 5.63 5.20 3.80 4.94 4.37 3.15 3.60 2.86
7.40 8.90 9.20 7.70 6.10 7.50 6.69 46.00 8.35 7.30 8.20 8.90 8.90 8.30 7.20 7.50 6.89 6.92 8.33 7.00 4.14
Abbreviation: S/D, systolic to diastolic.
Please cite this article as: Seffah JD, Swarray-Deen A, Fetal middle cerebral artery Doppler indices and clinical application at Korle Bu Teaching Hospital, Accra, Ghana, Int J Gynecol Obstet (2016), http://dx.doi.org/10.1016/j.ijgo.2015.11.027
J.D. Seffah, A. Swarray-Deen / International Journal of Gynecology and Obstetrics xxx (2016) xxx–xxx
abdominal circumference, head circumference, femur length, and biparietal diameter. The fetal weight was estimated using the Hadlock formulas [15]. Furthermore, the amniotic fluid volume and the placental grade were evaluated. This preliminary examination lasted 5–15 min. Thereafter, Doppler examination was performed using a Philips ClearVue 350 (Philips, Andover, MA, USA) ultrasonography machine with a 3.5-MHz curvilinear transducer. Color flow mapping was used to identify the circle of Willis and the proximal MCA, which is easily identified along the lesser wing of the sphenoid at the level of cerebral peduncles. The pulsed-wave Doppler gate was then placed at the proximal third of the MCA, within 1 cm of the origin of the MCA. The angle between the ultrasound beam and direction of blood flow was kept below 30°. The waveforms were quantified immediately after freezing the image using 3–10 consecutive waveforms. The peak systolic velocity (PSV), defined as the highest point of the waveform, was measured using manual calipers, and the resistive index (RI), pulsatility index (PI), and systolic-to-diastolic (S/D) ratio were calculated. Care was taken to apply minimal pressure to the maternal abdomen to avoid fetal head compression [16]. During the study period, all women who met the inclusion criteria were recruited. The sample size was calculated using the formula: n = Z [2] × (P) × (1 – P)/C2, assuming P = 0.5 (maximum variability), C = confidence interval of 95%, and Z = 1.96 (margin of random error). To correct for subgroup variability, 20% was added to the sample size. A minimum of 20 participants was to be recruited for each week of pregnancy (weeks 20–40). The collected data were entered into an Excel 2013 (Microsoft, Redmond, WA, USA) spreadsheet and the statistical analysis was performed using SPSS version 22 (IBM, Amonk, NY, USA). The t test was used as a test of significance, with P b 0.05 considered statistically significant. Pearson correlation and regression analyses were used to evaluate the correlation between the ultrasonography indices and the gestational age. Reference ranges (5th, 50th, and 95th percentiles) and their 95% confidence intervals were constructed for each parameter. The percentile values of the ultrasonography indices were calculated and compared with those from published international studies. 3. Results A total of 788 women attending the prenatal clinic at Korle Bu Teaching Hospital underwent an ultrasonography examination during the study period, but only 470 met the inclusion criteria. No woman declined the scan, but for 12 women, no MCA Doppler scan could be attained because of technical difficulties. Therefore, 458 women were included. The MCA indices were measured successfully for the 458 women, and the entire process took 5–15 min per woman. The mean age of the study participants was 30.4 ± 5.3 years. Overall, 375 (81.9%) women had a parity of two or less, and 158 (34.5%) were nulliparous. The Doppler results obtained from the women are tabulated in Table 1 and the reference nomograms of the Doppler indices are shown in Table 2 and Figs. 1–4. The PSV of the MCA ranged from 7.2 cm/s to 95.2 cm/s, with a mean of 40.5 cm/s, a median of 29.6 cm/s, and a standard deviation of 14.0 cm/s. There was a strong positive correlation between the PSV and gestational age (r = 0.725, P b 0.001) indicating that the PSV increases with increasing gestational age. The reference curve of the PI, RI, and S/D ratio had a parabolic shape with a decrease after the 28th week of pregnancy for the RI and after the 30th week for PI and S/D ratio (Figs. 1, 2, and 4). A negative linear correlation between the gestational age and the PI (r = −0.260, P b 0.001) and between the gestational age and the S/D ratio (r = − 0.123, P b 0.001) was also seen. There was a strong positive linear correlation between the RI and the PI (r = 0.284, P = 0.006), between the RI and the S/D ratio (r = 0.323, P b 0.001), and between the PI and the S/D ratio (r = 0.432, P b 0.001).
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Fig. 1. Pulsatility index in the middle cerebral artery (n = 458). Individual measurements (circles) and calculated reference ranges (lines) are shown; the reference boundaries include 95% of the sample population (P b 0.001). Abbreviations: GA, gestational age; PI, pulsatility index.
4. Discussion The present study has demonstrated that the PSV of the MCA increases continuously with advancing gestational age. The reference curves of the other ultrasonography indices (PI, RI, S/D ratio) had a parabolic shape with an overall decrease after the 28th week of pregnancy. Most of the published studies on Doppler indices of the MCA identified a similar pattern, albeit with reference ranges that can vary considerably. Potential reasons for such differences include the experience or skill of the sonographer, the techniques used, and the statistical tools applied. The present percentile distribution of the MCA PSV was compared with results from Iran [17], Brazil [18], and India [19]. These studies demonstrated a continuous increase in the PSV from 20 weeks of pregnancy to 40 weeks [17], from 23 weeks to 35 weeks [18], and from 12 weeks to 39 weeks [19]. Despite some differences in the actual PSV values, the present reference ranges were overall in good agreement with previously reported ranges [8,17,20].
Fig. 2. Resistive index in the middle cerebral artery (n = 458). Individual measurements (circles) and calculated reference ranges (lines) are shown; the reference boundaries include 95% of the sample population (P ≤ 0.006). Abbreviations: GA, gestational age; RI, resistive index.
Please cite this article as: Seffah JD, Swarray-Deen A, Fetal middle cerebral artery Doppler indices and clinical application at Korle Bu Teaching Hospital, Accra, Ghana, Int J Gynecol Obstet (2016), http://dx.doi.org/10.1016/j.ijgo.2015.11.027
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J.D. Seffah, A. Swarray-Deen / International Journal of Gynecology and Obstetrics xxx (2016) xxx–xxx
Fig. 3. Peak systolic velocity in the middle cerebral artery (n = 458). Individual measurements (circles) and calculated reference ranges (lines) are shown; the reference boundaries include 95% of the sample population (P b 0.001). Abbreviations: GA, gestational age; PSV, peak systolic velocity.
The nomogram for the RI was compared with results from the USA [9] and Germany [20]. The present reference curves had a parabolic shape (RI at 20 weeks: 0.75; RI at 28 weeks: 0.82; RI at 40 weeks: 0.67) similar to that seen in the other studies, but with some differences in the actual reference values. The present values were closest to those reported for the USA [8]. When compared with the RI reference curves published by Tarzamni et al. in Iran [17], the present curves showed an almost identical parabolic pattern for the period of 20–40 weeks of pregnancy. Most previous studies have demonstrated a parabolic shape for the reference curves of the MCA PI, usually with a fall after the 28th week of pregnancy. This fall has been attributed to a decreasing vascular impedance with increasing gestational age [21]. We compared the present values with the reference ranges published by Baschat et al. [7] and Tarzamni et al. [17]. The parabolic patterns of the previously published reference curves were similar to those in the present study, but the PI values in both studies were higher. A possible reason for this discrepancy may be pressure exerted by the ultrasonography probe on the fetal
head, which can lead to extremely low end-diastolic flow velocities resulting in higher PI values. Most previous Doppler studies of the fetal MCA were performed for the detection of fetal anemia resulting from Rhesus isoimmunization or parvovirus infection, both of which are rare occurrences in the Sub-Saharan population (the frequency of the Rhesus-negative allele in Africans is approximately 3%). Doppler assessment of the MCA also plays an important part in the identification of IUGR and is based on blood flow redistribution associated with fetal hypoxia. The West African subregion alone accounts for 11.4% of all infants with a low birth weight worldwide, with most cases being related to IUGR [22]. The major determinants of such growth retardation in utero are related to maternal nutritional deficiencies (iron-deficiency anemia), malaria, sickle cell disease, and the high rate of maternal HIV infection in this region. The ratio of MCA PI to the umbilical artery PI (i.e. cerebroplacental ratio) has been shown to be a good measure of redistribution of cardiac output to the cerebral vessels and it is predictive of adverse perinatal outcome in both growth-restricted fetuses and appropriate-forgestational-age fetuses [23]. Several studies have reported that the cerebroplacental ratio is a better predictor of adverse outcome than are the MCA or umbilical artery Doppler indices alone [23–25]. Even with the introduction of affordable ultrasonography hardware, medical ultrasonography machines with added color Doppler and pulsed-wave functions come at a very high price. Most healthcare facilities with an ultrasonography device can only perform standard two-dimensional scans. Another potential limitation to the use of Doppler assessment of the fetal MCA is the fact that there are very few trained individuals who can offer a level 2 or 3 obstetric scan and even fewer who are trained in fetal medicine. Therefore, even in clinical scenarios when a Doppler study of the MCA is indicated, the low awareness, added cost, and accessibility of such services serve as major deterrents. The present reference curves for Doppler indices of the MCA demonstrated a similar pattern to the ones reported in other regions. Because Doppler assessment of the MCA represents a rapid, reproducible, simple, and reliable method with minimal interobserver and intraobserver variability, it can be used in fetal monitoring for highrisk pregnancies—especially those complicated by IUGR—at Korle Bu Teaching Hospital.
Conflict of interest The authors have no conflicts of interest.
References
Fig. 4. Systolic-to-diastolic ratio in the middle cerebral (n = 458). Individual measurements (circles) and calculated reference ranges (lines) are shown; the reference boundaries include 95% of the sample population (P b 0.009). Abbreviations: GA, gestational age; S/D ratio, systolic-to-diastolic ratio.
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Please cite this article as: Seffah JD, Swarray-Deen A, Fetal middle cerebral artery Doppler indices and clinical application at Korle Bu Teaching Hospital, Accra, Ghana, Int J Gynecol Obstet (2016), http://dx.doi.org/10.1016/j.ijgo.2015.11.027