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Abstract

A high systolic/diastolic (S/D) ratio of umbilical cord blood is a manifestation of intrauterine hypoxia. However, the clinical significance of a persistently decreased S/D ratio of umbilical cord blood has not been reported. We report eight cases of a persistently decreased S/D ratio of umbilical cord blood, with two cases of umbilical thrombus, five cases of excessive torsion, and one case of a true cord knot. Fetuses with a persistently decreased S/D ratio of umbilical cord blood may be at risk, and it may be an important indication of umbilical cord lesions.

Keywords

Systolic/diastolic ratio umbilical cord torsion thrombus true umbilical cord knot hypoxia case report

Introduction

A recent report on the causes of stillbirth showed that up to 19% of deaths are due to umbilical cord abnormalities, mainly including microcirculatory impairment in fetuses, umbilical cord compression, torsion and knots, and thrombosis of the umbilical vessels.¹ However, the detection rate of umbilical cord abnormalities is low with prenatal ultrasound. In suspected umbilical cord abnormalities, the umbilical systolic/diastolic (S/D) ratio or fetal electrocardiographic monitoring is often used to detect fetal intrauterine hypoxia. At present, the changes in umbilical cord blood flow mechanics caused by umbilical cord abnormalities, such as a cord knot, cord twist, and cord thrombosis, are unclear.² Ma et al analyzed the perinatal clinical symptoms of pregnant women with different S/D ratios and found that an S/D ratio >3 was a risk factor for fetal distress, low birth weight, and cesarean section.³ To date, little is known about the effect of a sustained decrease in the S/D ratio on fetal safety. In this study, we analyzed eight cases of adverse events associated with the umbilical cord, all of which presented with a sustained decrease in the S/D ratio. These cases raise concerns about the safety of a considerable decrease in the S/D ratio of cord blood flow.

Cases

All procedures performed in this study were in accordance with the ethical standards of the institution. Ethics approval was granted by the First Affiliated Hospital of Guangzhou University of Chinese Medicine Ethics Committee (approval number: ZYYECK2020-036-JT, 14 June 2020). All patients were exempted from signing informed consent because this was a retrospective analysis. The reporting of this study conforms to the CARE guidelines.⁴

We collected the clinical data of eight pregnant women with a decreased umbilical S/D ratio who were treated at our hospital between 2017 and 2019. Two women were diagnosed with thrombosis of the umbilical vessels, one was diagnosed with a true umbilical cord knot, and five were diagnosed with excessive torsion of the umbilical cord. No apparent structural or chromosomal abnormalities were observed in any of the eight fetuses. Umbilical blood flow is usually measured at the free segment of the umbilical cord. A series of segmental measurements were used to improve accuracy during the third trimester owing to incomplete imaging of the umbilical cord (Table 1).

Table 1.

Case details, prenatal findings, and pregnancy outcomes.

Case	Age (years)	Prenatal findings				Pregnancy outcomes
Case	Age (years)	GA (weeks + days)	Doppler S/D ratio (percentile)	Prenatal screening (heart)	History of gestation and other information	GA at birth (weeks + days), birth weight (kg), Apgar scores	Umbilical cord torsion, thrombus, a true knot	Placental pathology	Follow-up (3 months)
1	Early 30s	34 + 134 + 2	1.53 (0)1.3 (0)	Normal	G1P0A0, single umbilical artery, abnormal fetal heart monitoring	34 + 2,2.37,9-9-10	25, 3, 0	Mature placental tissue	PFO
2	Early 30s	38 + 3	1.85 (4.6)	Normal	G1A0P0, abnormal fetal heart monitoring	38 + 4, intrauterine death	0, 2, 0	None	None
3	Early 30s	24 + 438 + 1	2.14 (0.8)1.75 (1.4)	Normal	G1A0P0, FGR	38 + 2,1.92,10-10-10	38, 0, 0	Mature placental tissue	PFO
4	Early 30s	31 + 235 + 237 + 638 + 2	1.96 (1.9)1.79 (0.9)1.7 (0.6)1.68 (0.5)	Normal	G1A0P0, PT = 53 mm, maturity level III of the placenta, many spirals in the umbilical cord, GDM	38 + 2,2.69,10-10-10	40, 0, 0	None	None
5	Early 30s	24 + 332 + 237 + 3	2.16 (0.8)1.89 (1.3)2.0 (11.3)	Normal	G2P1S0, many spirals in the umbilical cord	37 + 3,3.07,10-10-10	40, 0, 0	None	Perinatal infection
6	Early 20s	36 + 639 + 239 + 6	1.99 (9.1)1.75 (2.1)1.57 (0.1)	Normal	G2A0P1, no other information	40 + 3,3.35, 10-10-10	30, 0, 0	None	Neonatal pneumonia, neonatal hyperbilirubinemia, PFO
7	Early 30s	37 + 440 + 3	1.68 (0.4)1.81 (6.)	Normal	G1A0P0, no other information	40 + 3,3.45, 10-10-10	32, 0, 0	None	Perinatal infection
8	Early 20s	33 + 339	1.7 (0.6)1.79 (3)	Normal	G1A0P0, suspicion of a cord knot	39 + 3,3.13,10-10-10	0, 0, 1	None	None

GA, gestational age; S/D, systolic to diastolic; G, gravida; P, para; A, abortion/miscarriage; PFO, patent foramen ovale; FGR, fetal growth restriction; PT, placental thickness, GDM, gestational diabetes.

The S/D ratio of cord blood flow was determined by the average of three measurements at different positions. The percentile of the S/D ratio of umbilical cord blood flow was obtained from the “Pregnancy Calculation” program developed by Professor Sun Luming who is an expert in maternal-fetal medicine.

Case 1 had double umbilical arteries during the second trimester. At gestational week 34, only one umbilical artery was observed next to the bladder, with an atypical cross-sectional structure of the umbilical cord, which indicated umbilical artery embolism. Moreover, the S/D ratio was low and had a venous waveform, and fetal heart monitoring abnormalities were present. The patient underwent emergency cesarean section, and the fetus was found to have thrombosis of the umbilical vessels at three locations (Figures 1, 2). The neonatal Apgar score was 9 points at 1 minute (1 point loss in muscle strength), 9 points at 5 minutes (1 point loss in muscle strength), and 10 points at 10 minutes. Placental pathology showed no abnormalities.

Figure 1.

The S/D ratio measured by color ultrasound in case 1. (a) The S/D ratio at 31 + 1 weeks of gestation (S/D = 1.43) and (b) the S/D ratio on the following day. The S/D ratio progressively decreased and presented with a venous waveform. S/D, systolic/diastolic.

Figure 2.

Photograph showing the umbilical cord thrombus in case 1. White arrows indicate three areas of umbilical cord thrombosis.

Case 2 presented with fetal heart monitoring abnormalities and a low umbilical S/D ratio. The treating physician determined that the S/D ratio was not low enough to indicate severe intrauterine hypoxia. Unfortunately, the fetus died during observation. Two thrombi, one at the placental insertion point and the other at the abdominal wall insertion point, were found in vessels of the umbilical cord after the fetus was surgically removed.

Case 3 presented with a low umbilical S/D ratio starting in the second trimester. At 31 weeks of pregnancy, ultrasound showed fetal growth restriction (Z scores: biparietal diameter, −1.45; head circumference, −1.66; abdominal circumference, −2.6, femur length, 0.43; estimated fetal weight, −2.66). At gestational week 38, the umbilical S/D ratio was low, and the fetal weight was below the 10th quantile (Z scores: biparietal diameter, −1.33; head circumference, −1.74; abdominal circumference, −3.06; femur length, 0; estimated fetal weight, −2.89). Repeated observation of restricted fetal growth and development did not improve, and the S/D ratio of umbilical cord blood flow continued to be low. Therefore, fetal distress could not be ruled out. Consequently, obstetricians recommended early delivery by cesarean section. The fetus was later found to have umbilical cord torsion (approximately 38 twists) after being surgically removed.

Case 4 had a history of gestational diabetes. At gestational week 31, ultrasound showed that the placenta was considerably thickened (54 mm) compared with a previous measurement (31 mm at gestational week 24). There were many calcified spots and blood sinuses in the placenta, with a placental maturity of level III. After 31 weeks, the S/D ratio of fetal cord blood flow was persistently low. After 38 weeks of pregnancy, the electronic fetal monitoring pattern was grade II, which did not rule out the possibility of intrauterine hypoxia. Therefore, the obstetrician recommended early delivery by cesarean section. Eventually, the fetus was found to have severe umbilical cord torsion (40 twists) (Figure 3).

Figure 3.

Photograph showing the umbilical cord in case 4. The umbilical cord shows exaggerated torsion with up to 40 twists.

Cases 5, 6, and 7 had varying degrees of umbilical cord torsion (Figure 4). In these cases, a low S/D ratio of fetal cord blood flow appeared earlier as the umbilical cord torsion became more severe. Case 8 was found to have a decrease in the S/D ratio at gestational week 33, which lasted until week 39. The fetus was delivered naturally under strict electronic fetal monitoring and umbilical cord blood flow monitoring. A true knot was found in the umbilical cord after delivery.

Figure 4.

Spatio-temporal image correlation of the umbilical cord in case 5. The umbilical cord has many spirals and obvious entanglements.

Discussion

Doppler ultrasound is widely used in clinical practice to detect the fetal umbilical S/D ratio, which reflects fetal–placental circulation and fetal blood supply. Li et al showed that resistance in the placental circulation and the umbilical arterial S/D ratio decreased with fetal development.⁵ However, in the case of abnormal umbilical arterial contraction, the S/D ratio increased, indicating low placental perfusion, abnormalities in fetal growth and development, and potential fetal distress. However, the eight pregnant women with severe umbilical cord adverse events in this study did not show the universally recognized manifestation of intrauterine hypoxia with an elevated S/D, but presented with a sustained low S/D ratio instead. There are two possible causes for this finding in our study as discussed below.

First, when severe vessel stenosis occurs, the flow rate and the resistance index increase at the stenosis and proximal to the stenosis. In contrast, the flow rate and the resistance index decrease distal to the stenosis (tardus parvus waveform on ultrasound). Therefore, severe cord thrombosis, cord knotting, and excessive cord torsion may lead to multiple stenoses, resulting in decreased lumen resistance and a low S/D ratio at the distal end of the stenosis. Wilke et al showed that the spirality of blood vessels reduced pressure in the arterial circulation.⁶ Cases 1 and 2 were diagnosed with umbilical cord thrombus, and the S/D ratio was lower with a larger number of thrombus sites. Cases 3, 4, 5, 6, and 7 had severe umbilical cord torsion and low S/D ratios, which are consistent with our first hypothesis.

Second, a low S/D ratio may be related to fetal thrombotic vasculopathy resulting from disorders of the fetal circulation. Studies have shown that umbilical cord abnormalities, especially umbilical cord torsion, are an important factor in fetal thrombotic vasculopathy.⁷ Machin et al⁸ reported that fetal death was the primary clinical outcome of excessive torsion of the umbilical cord, which is related to thrombosis of placental and villous vessels, umbilical vein thrombosis, and umbilical cord stricture. Pathological alterations in pregnant women include hypercoagulation, compressed umbilical cord vessels (as a result of the umbilical cord being twisted and crisscrossed to form multiple acute angles), vasospasm, vessel constriction, a large number of red blood cells in the vessels, endangiitis, and fibrin adherence to the intima (also known as fibrin pads). These conditions result in local slow and even stagnant blood flow, and subsequently lead to thrombosis. Lepais et al showed that fetal thrombotic vasculopathy may cause acute or intermittent obstruction of umbilical blood flow,⁹ which is related to fetal growth restriction and can lead to extraplacental umbilical cord and fetal thrombosis.¹⁰ Placental thrombosis may alter the entire umbilical circulation, which we believe is the cause of a low umbilical S/D ratio. In Case 4, the placenta was much thicker at gestational week 31 than a previous measurement, with many calcified spots and blood sinuses in the placenta, which were apparently inconsistent with normal placental maturity. Moreover, the S/D ratio began to decrease, and the patient had umbilical cord torsion (40 twists) after surgery. We speculate that severe umbilical cord torsion resulted in placental thrombosis and placental edema and thickening, while placental impairment further affected the umbilical S/D ratio. Unfortunately, placental pathology was not performed in this case to confirm this possibility.

Umbilical cord thrombosis is a rare obstetric complication. Vuong and Nguyen reported a special case of umbilical cord thrombosis combined with uterine torsion, and reviewed the literature on 10 cases of umbilical cord thrombosis.¹¹ They found that none of the cases had obvious clinical signs or ultrasound characteristics to predict umbilical cord thrombosis before birth. However, the parameters of cord blood flow mechanics were not mentioned in this previous study. With regard to umbilical cord torsion, researchers have paid attention to the measurement of the umbilical cord helix index to determine the degree of torsion, but rarely analyzed its hemodynamic characteristics. Japanese researchers found that, in cases of umbilical coil torsion with a length/diameter pitch value (L/R pitch) <2.0 coils/cm, the blood flow resistance index of the prime code was decreased and Doppler spectral fluctuation of the umbilical vein appeared,² which is similar to the hemodynamic changes in our case.

We believe that a continuous or severe decrease in the S/D ratio in umbilical cord blood flow may be an important manifestation of adverse events of the umbilical cord. We hope to make clinicians aware of this possibility from the findings of our case analysis. A multicenter, large-sample study is required to determine the exact effect of adverse events of the umbilical cord on umbilical cord blood flow mechanics and to clarify the meaning of a decrease in the S/D ratio.

Supplemental Material

sj-pdf-1-imr-10.1177_03000605241244763 - Supplemental material for A sustained decrease in the systolic/diastolic ratio may be a sign of severe adverse events in the umbilical cord: a report of eight cases

Supplemental material, sj-pdf-1-imr-10.1177_03000605241244763 for A sustained decrease in the systolic/diastolic ratio may be a sign of severe adverse events in the umbilical cord: a report of eight cases by Yan-Jing Zeng, Jun Zhang, Yan-Fang Li and Yu-Yi Chen in Journal of International Medical Research

Footnotes

Declaration of conflicting interest

The authors declare that there is no conflict of interest.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

ORCID iD

Yu-Yi Chen

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