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DIAMETER DIFFERENCES IN FETAL UMBILICAL ARTERIES






















Abstract
Objective: This study aimed to investigate any differences between the pulsatility index (PI) and resistive index (RI) values at the common iliac arteries of fetuses demonstrating different umbilical artery diameters.
Patients and Methods: Doppler Ultrasonography (US) was performed on 165 pregnant women between 18 to 22 weeks of gestation and again between 27 to 37 weeks of gestation. The umbilical artery diameters and both common iliac artery flow parameters (PI and RI) were measured during these visits. 
Results: The incidence of diameter difference between the two umbilical arteries was found to be 6.7%. Eleven of the 165 patients demonstrated a diameter difference greater than 25% (95th percentile) between their two umbilical arteries at the 18th to 22nd gestational week measurement. Color Doppler US examination of these 11 cases showed that the RI values of the non-dominant common iliac artery were significantly higher than that of the dominant common iliac artery (p<0,001). 
Conclusions: RI values are higher in the non-dominant than the dominant common iliac artery in pregnant women whose two umbilical arteries demonstrate a significant difference in diameter.	
Key Words: Umbilical Artery, Diameter Difference, Color Doppler US, Common Iliac Artery










Introduction
The umbilical cord contains two arteries and one vein. Normally both umbilical arteries have a similar diameter. Studies have shown one umbilical artery to be smaller than the other in 0.7-1.4% of cases (1,2) . A hypoplastic umbilical artery is an artery whose diameter is smaller than the contralateral artery by 2 mm, 30% or 50% depending on the various authors (3, 4). In addition, differences in diameter between the two umbilical arteries have been shown to cause significant changes in blood flow parameters (2). Previous studies have shown conflicting results regarding the impact of diameter differences between the umbilical arteries on clinical outcomes. In some studies, hypoplastic umbilical artery has been found to correlate with umbilical cord hematoma, placental infarction, trisomy 18, polyhydramnios, congenital heart disease, intrauterine growth retardation (IUGR), and abnormal insertion of the umbilical cord (4,5,6,7).
In fetuses with single umbilical artery ( SUA), all the blood travels to the placenta via the vessel on the side of the umbilical artery. On the contralateral side, where the umbilical artery is absent, the common iliac artery can not participate in fetoplacental circulation and it carries the blood to the lower limb. Studies are available investigating the relationship between SUA and differences in diameter of the common iliac artery and related Doppler US parameters (8). Part of the conclusions of these studies is that the common iliac artery is hypoplastic on the side where the umbilical artery is absent. They also found RI to be higher compared with the contralateral side (8). However, a study investigating the flow parameters between the hypoplastic umbilical artery and the ipsilateral common iliac artery is not yet available in the literature.
Our aim in this study was to investigate the effect of differences in the diameter of the hypoplastic fetal umbilical artery on Doppler findings of the common iliac arteries and to investigate whether or not it is accompanied by placental or umbilical cord pathologies.

Materials and Methods
This research study was approved by our institutional human ethics committee. Written informed consent was obtained from all of the subjects. Routine obstetric US was performed on 212 pregnant women with known dates of last menstruation during their 18th to 22nd gestational week, who were admitted to our clinic between January and July, 2010. 
Ultrasonography was performed via the transabdominal route using GE Logic 9 US equipment with a 3.5 to 5 MHz multi-frequency convex probe (Milwaukee, USA).
Inclusion criteria for this study were as follows: uniparity, gestational age between 18 and 22 weeks, intact membranes, 3-vessel cord, and living fetus. Patients with multiple pregnancies and inadequately imaged umbilical cords were excluded from the study. A detailed fetal anomaly scan was performed primarily via obstetric US. Umbilical cord structure and the presence of two arteries and one vein were carefully evaluated. Umbilical artery diameter was measured from the inner lumen of the artery under maximum magnification and the measurement was taken from the free section of the cord away from the fetus and the placenta. The percentage difference in diameter between the umbilical arteries (%AA) was calculated using the formula, %AA = (A1-A2) / A1. In this formula, A1 and A2, represent the largest and smallest diameters of the umbilical arteries, respectively (2). 
Iliac artery diameters were assessed by grey scala and color Doppler US; and larger iliac artery was accepted as dominant (8). Accordingly, dominant and non-dominant fetal common iliac arteries were examined just distal to the aortic bifurcation by color Doppler US, and the PI and RI measured. Fetal abdominal circumference, femur length, and biparietal diameter were measured and the average used to confirm gestational age. Control US�s were performed between gestational weeks 27 and 37 and repeat measurements of these parameters taken. Insonation angle between the umbilical cord vessels and Doppler waves were higher than 30-60� in all Doppler studies. Pulse Doppler gain was -10 to 10 dB, pulse gate was 2-4 mm and minimal wall filter was used.
Between gestational weeks 18 and 22 the percentage difference of umbilical artery diameter was calculated using the formula, %AA = (A1-A2) / A1 and according to this percentage two groups were formed: Group (A) Hypoplastic umbilical artery group: consisted of those with greater than 25% (>95 percentile) difference in umbilical artery diameters, and Group (B) Control group: consisted of those with less than a 25% (<95 percentile) difference in umbilical artery diameters. Any significant difference between these two groups in terms of age, gravidity, parity, placental and umbilical cord pathology , the quantity and quality of amniotic fluid, APGAR score, infant birth weight and birth route was investigated. In addition, the mean diameter for the large and small umbilical arteries in both gestational periods of 18-22 and 27-37 weeks for both Groups (A) and (B) were calculated. 
Group (A) patients between the 18th and 22nd gestational week were examined using color Doppler US to determine whether there was a relative dominance of one of the common iliac arteries (CIA) over the other.  Based on the iliac artery diameters, 11 patient were further divided into two sub-groups as (i) those demonstrating and (ii) those not demonstrating one CIA dominant over the other. PI and RI values were measured for both sub-groups (i) and (ii). Control US�s was performed between 27 and 37 gestational weeks and repeat measurements of these parameters taken. In addition, analysis of frequency of maternal gestational diabetes was carried out for all patients in Group (A).
Statistical analysis was performed using SPSS (Version 15.0, SPSS Chicago, IL, USA) computer software during this study. Bonferroni corrected Wilcoxon signed rank test was used for comparing intra-group averages for the left and right measurements, when the distribution was not normal. Mann-Whitney test was used for two-group and Kruskal-Wallis test for three-group comparisons of inter-group averages when normal distribution was lacking. Chi-square test was used to compare percentages between groups. Paired t-test was used for comparing dominant and non-dominant common iliac arteries RI values, when the distribution was normal.
Results
US was performed on 212 pregnant women between the 18th and 22nd week of gestation (second trimester US). Single umbilical artery was present in 5 women. Forty women were lost to follow up for the 27th to 37th gestational week US. Emergency evacuation was performed on one woman due to severe oligohydramnios. Hydrops fetalis was detected in the fetus and the baby was pronounced dead on birth. Therefore, a total of 47 cases were excluded from the study. A total of 165 patients met inclusion criteria for the study who also attended the 27th to 37th gestational week (third trimester) US. Of these, 11 demonstrated more than a 25% (95th percentile) difference in diameter between the two umbilical arteries at the second trimester US. The incidence of hypoplastic umbilical artery was therefore 6.7%.
The mean patient age in years was 27 (range: 17-32) in Group (A) and 25 (range: 19-40) in group (B). No significant age difference was found between groups (p=0.91). Mean gravidity and parity were 2 (range: 1-4) and 1 (range: 0-1) for Group (A), respectively, and 2 (range: 1-6) and 0 (range: 0-4) for Group B, respectively. There was no significant difference in gravidity or parity between the two groups (p=0.33 and p=0.82, respectively).
Group (A)�s second trimester US showed a mean right and left common iliac artery PI value of 1.31 (range: 1.05 to 1.76) and 1.60 (range: 1.01 to 2.89), respectively, and a right and left RI value of 0.81 (range: 0.70 to 0.85) and 0.85 (range: 0.66 to 0.91), respectively.
Group (B)�s second trimester US showed a mean right and left common iliac artery PI value of 1.59 (range: 0.90 to 2.80) and 1.58 (0.94 to 3.02), respectively, and a right and left RI value of 0.82 (range 0.66 to 0.93) and 0.83 (range: 0.64 to 0.96), respectively. Group (A)�s third trimester US showed a mean right and left common iliac artery PI value of 1.23 (range: 1.10 to 1.85) and 1.58 (range: 1.18 to 2.15), respectively, and a right and left RI value of 0.77 (range: 0.60 to 0.94) and 0.78 (0.56 to 0.93), respectively. Group (B)�s third trimester US showed a mean right and left common iliac artery PI value of 1.36 (range: 0.24 to 2.18) and 1.42 (range: 0.77 to 2.41), respectively, and a right and left RI value of 0.76 (range: 0.60 to 0.94) and 0.77 (range: 0.56 to 0.93), respectively.
Group (A)�s second trimester US showed the mean diameter of the large and small umbilical arteries to be 2mm (range: 1.6 to 2.6) and 1.2mm (range: 1.1 to 1.9), respectively. In group (B) these values were 1.8mm (range: 1.1 to 2.7) and 1.7mm (range 1.1 to 2.5), respectively. Group (A)�s third trimester US showed the mean diameter of the large and small umbilical artery to be 3.4mm (range: 2.7 to 4.5) and 2.7mm (range: 2.0 to 3.9), respectively. In Group (B) these values were 3.2mm (range: 2.2 to 5.0) and 3.0mm (range: 2.0 to 4.6), respectively (Table 1). 
Birth weight was 3060grams (range: 2700-3845) in Group (A) and 3185grams (range: 1700-4620) in Group (B). There was no significant difference in terms of fetal birth weight (p=0.90). There was no statistically significant difference between the two groups in terms of umbilical cord pathology, nuchal cord, 5th minute APGAR score, and the nature of the amniotic fluid (p>0.05).
Sub-group (ii) demonstrated a significantly higher mean RI value when compared with sub-group (i). The non-dominant iliac artery was found to have a significantly higher mean RI value than the dominant common iliac artery (p<0,001)  (Figure 1).
Group (A)�s third trimester US re-confirmed the diagnosis of hypoplastic umbilical artery detected from the second trimester in 9 of the 11 subjects (Figure 2: women 3 through 11). The remaining two women had resolution of their hypoplastic umbilical arteries showing umbilical artery diameters that were equivalent to one another (Figure 2: woman 1 and 2) .
In our study, no placental or umbilical cord pathology was detected in Group (A) (6.7% of patient population). Polyhydramnios was detected in 2 cases. Amniotic fluid was found to contain meconium in 4 cases. Nuchal cord was detected in 2 cases. No chromosomal defects, fetal anomalies or syndromes were detected. Finally, gestational diabetes was found in only 1 pregnant woman.

Discussion
Hypoplastic umbilical artery (HUA) is accepted as an incomplete form of SUA (4). Although its etiology is unknown this condition has been found to be associated with various pathologies such as trisomy 18, polyhydramnios, congenital heart disease, IUGR, placental infarction, umbilical cord hematoma, and abnormal umbilical cord insertion (5-7). Dolkart et al. studied umbilical artery diameters and found a 2mm difference in 6 cases measured in the 2nd and 3rd trimesters. One of the 6 cases was accompanied by preterm birth and another suffered death due to neonatal liver failure 3 months after birth. No clinical pathology was reported in the other 4 cases (9).
In another study by Predanic et al, no pathological findings were detected in the examination of placental and umbilical cords of 6 pregnancies demonstrating 1-3mm differences in umbilical artery diameters (2). Conversely, Raio et al demonstrated abnormal cord insertions (marginal, velamentous and eccentric) in 8 of 14 cases with more than 1mm differences between umbilical artery diameters. Placental abnormalities were detected in the remaining 7 cases (3 placental infarctions, 2 bipartite placentas, 1 plasenta succentriata, 1 corangioma and the absence of Hyrtl anastomosis) (7).
Petrikovsky and Schneider detected hypoplastic umbilical artery using prenatal US in 12 patients. They found 1 of these cases to be associated with trisomy 18, 3 with polyhydroamniosis, 1 with congenital heart disease, and 2 with IUGR. They also found maternal diabetes in 4 cases (4). In our study of patients with hypoplastic umbilical arteries, no placental or umbilical cord pathology was detected. However, 2 cases demonstrated polyhydroamniosis and amniotic fluid with meconium was found in 4 cases. In addition, gestational diabetes was found in one pregnant woman.
Sepulveda et al examined blood flow patterns in the common iliac artery in 15 cases of SUA. They found that PI values on the side not attending the fetoplacental circulation were higher (8). In our study, the hypoplastic umbilical artery group US�s performed during the 18th to the 22nd gestational week demonstrated PI and RI values of the common iliac arteries that were higher on the non-dominant side as compared with the dominant side. The higher RI value may be due to the smaller diameter of the common iliac artery on the side of the hypoplastic umbilical artery in early gestational stages.
In a study of 8 cases of SUA from birth to 4 years of age, Meyer et al reported significant anatomical and histological differences between the common iliac arteries. Whereas normal muscular structure was detected in the smaller common iliac artery, a calcified pattern was detected in the larger common iliac artery. Also interestingly, early atherosclerotic lesions were identified in this larger vessel. It has been thought that this may reduce blood flow especially in the dominant vessel resulting in vessel wall remodeling after clamping of the cord (10).
Some limitations of our study include the small sample size and the lack of macroscopic examination of placental and umbilical cord pathologies. The effect of hypoplastic fetal umbilical artery on prognosis is difficult to judge definitively due to the small sample size. It is known however that fetal prognosis is better in hypoplastic umbilical artery as compared with SUA. More extensive studies are needed to determine the affect of hypoplastic fetal umbilical artery on fetal prognosis. 
Another limitation for this study was the subjective evaluation criteria for dominant and non-dominant fetal common iliac arteries.
Our study revealed  that RI values of the non-dominant common iliac artery at the hypoplastic umbilical artery group  were higher than that of the contralateral dominant common iliac artery. However, there was no negative affect of these values on fetal prognosis.




















References
Weissman A, Drugan A. Sonographic Findings of the Umbilical Cord: Implications for the Risk of Fetal Chromosomal Anomalies. Ultrasound Obstet Gynecol 2001;17:536-41.
Predanic M, Perni SC. Antenatal Assessment of Discordant Umbilical Arteries in Singleton Pregnancies. Croat Med J 2006;47:701-8.
Sepulveda W, Flack NJ, Bower S, Fisk NM. The Value of Color Doppler Ultrasound in the Prenatal Diagnosis of Hypoplastic Umbilical Artery. Ultrasound Obstet Gynecol 1994;4:143-6.
Petrikovsky B, Schneider E. Prenatal Diagnosis and Clinical Significance of Hypoplastic Umbilical Artery. Prenat Diagn 1996;16:938-40.
Sepulveda W, Shennan Ah, Bower S, Fisk NM. Discordant Umbilical Artery Flow Velocity Waveforms in Spontaneous Umbilical Cord Hematoma. J Clinic Ultrasound 1995;23:330-2.
Harper MA, MurnaghanGA. Discordant Umbilical Artery Flow Velocity Waveforms and Pregnancy Outcome. Br J Obstet Gynaecol 1989;96:1449-50.
Raio L, Ghezzi F, Di Naro E, Gomez R, Saile G, et al. The Clinical Significance of Antenatal Detection of Discordant Umbilical Arteries. Obstet Gynecol 1998;91:86-91.
Sepulveda W, Nicolaidis P, Bower S, Ridout DA, Fisk NM. Comman Iliac Artery Flow Velocity Waveforms in Fetuses with a Single Umbilical Artery: A Longitudinal Study. Br J Obstet Gynaecol�1996;103:660-3.
Dolkart LA, Reimers FT, Kuonen CA. Discordant Umbilical Arteries: Ultrasonographic and Doppler Analysis. Obstet Gynecol 1992;79:59-63
Meyer WW, Lind J. Iliac Arteries in Children with a Single Umbilical Artery. Structure, Calcifications, and Early Atherosclerotic Lesions. Arch Dis Child 1974;49:671-9.











































Table 1:

GroupsHypoplastic Umbilical Artery Group (Group A)Control Group (Group B)Birth Weight (gr)3060   (2700-3845)3185   (1700-4620)Mean Age27 (17-32)25 (19-40)Gravidity2 (1-4)2 (1-6)Parity1 (0-1)0 (0-4)Mean Right Common Iliac Artery PI 2. Trimerter1.31 (1.05-1.76)1.59 (0.90-2.80)3. Trimester1.23 (1.10-1.85)1.36 (0.24-2.18)Mean Left Common Iliac Artery PI 2. Trimerter1.60 (1.01-2.89)1.58 ( 0.94-3.02)3. Trimester1.58 (1.18-2.15)1.42 (0.77-2.41)Mean Right Common Iliac Artery RI 2. Trimerter0.81 (0.70-0.85)0.82 (0.66-0.93)3. Trimester0.77 (0.60-0.94)0.76 (0.60-0.94)Mean Left Common Iliac Artery RI2. Trimerter0.85 (0.66-0.91)0.83 (0.64-0.96)3. Trimester0.78 (0.56-0.93)0.77 (0.56-0.93)Mean Large UA (mm)2. Trimerter2 (1.6-2.6)1.8 (1.1-2.7)3. Trimester3.4 (2.7-4.5)3.2 (2.2-5)Mean Small UA (mm)2. Trimerter1.2 (1.1-1.9)1.7 (1.1-2.5)3. Trimester2.7 (2-3.9)3 (2-4.6)
























Table Legend:

Table 1; The mean values for the hypoplastic umbilical artery (Group A) and the control groups (Group B)














































Figure Legends

Figure 1a; Longitudinal view of the umbilical cord showing size difference between umbilical arteries.
Figure 1b;  Dominant common iliac artery flow waveforms at 20 weeks and 1 day of gestation in a fetus demonstrating a lower RI value.
Figure 1c; Non-dominant common iliac artery flow waveforms at 20 weeks and 1 day of gestation in a fetus demonstrating a higher RI.
Figure 2a; Transverse view of an umbilical cord showing the size difference between the umbilical arteries. 
Figure 2b; The difference in umbilical artery size at 30 weeks and 6 days of gestation in a fetus.
Figure 2c: Non-dominant common iliac artery flow waveforms at 30 weeks and 6 days of gestation in a fetus demonstrating a higher RI value.












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