Direct compression
A simple model of umbilical cord occlusion is to provide transverse pressure on the cord until blood flow stops. This is the most common experimental model in the sheep with an inflatable occluder cuff placed around the umbilical cord. These experiments suggest that there is a simple answer to the question: “How much external pressure is needed to occlude the umbilical vein?”. However, after reviewing a large stack of ovine umbilical occlusion studies, I was unable to find out how much pressure was needed to stop flow. Typically, a silicon rubber occluder 16mm heavy duty was put around the cord and filled with 3-5 ml of saline until flow stopped. The occluders were made by In Vivo Metric, so I asked the company in an email if they knew how much pressure was being applied to the cord. Surprisingly, they did not know.
An estimate of the occlusion pressure was published using an vitro system, in which umbilical vein flow was reduced usually below 50% with 200 g on a 5-cm2 plate, although not completely occluded[1]. In this experiment, arterial pressures were at 60 mmHg and venous pressure at 20 mmHg, which is equivalent to 27 cm of water. If the pressure of the plate is acting over a cord segment 5 cm long and approximately 1 cm side, that would 5 cm2 so the 200 g of mass would be divided by 5 suggesting that 40 grams / cm2 is sufficient pressure to occlude flow (grams are a unit of mass not weight, but it is still a reasonable sense of the statics.) That is not much force.
Another in vitro experiment with umbilical cords, wrapped them one and a half times around a 4 cm cylinder and then applied increasing weight to one end until venous flow (maintained with 40 mmHg of pressure) stopped[2]. The range was wide with 250 to 1400 grams needed to stop flow. If one assumes that the cord did not slip, then the occlusion was due to compression of the vein as it rounded the back of the cylinder. The authors found an inverse relationship between the coiling index and the weight required which as they note could have been due to differences in how the vein contacted the cylinder since more coils were in contact in the highly coiled cords. In any case, the tug needed to stop flow is not massive if one thinks about the force needed to lift even 1400 grams, the equivalent of a 30 week gestation infant.
This experimental evidence supports anatomic studies that show that the umbilical cord anatomy may not protect the vessels. The vessels do not move freely in Wharton’s jelly but are enmeshed in the helical collagen structure as can be readily demonstrated after delivery. If they were free in the jelly, a direct external force could for example displace the vein between the more rigid arteries. After delivery, the encasing Wharton’s jelly appears to be protective, like packing china in shrink-wrap. However, this plentiful Wharton’s jelly is much thinner before delivery when the vessels are distended by blood, as was demonstrated in 1952 by Reynolds who clamped still pulsating cords simultaneously at 2 points in a Cesarean delivery and in several vaginal deliveries[3]. This finding has been repeatedly confirmed by ultrasound examination of the umbilical cord in situ.
The anatomical structure does suggest that the helical collagen attachment may favor patency of the vein lumen, since after delivery the empty umbilical vein typically has a wide-open lumen. Also possible, but as far as I can find still unproven, is that in vivo the umbilical cord surface over the rigid scaffold of the distended circulation can protect the vein from compression. Another possibility is that the helical structure of the cord helps deflect a compressive force. However unless new evidence is produced, the experimental evidence shows that the umbilical cord is susceptible to compression by relatively weak forces.
Fetal heart rate evidence of cord umbilical cord compression
Building on the innovative work of Dr. Roberto Caldeyro-Barcia and colleagues, Dr. Edward Hon published some important early reports of continuous fetal heart rate tracing in relationship to contractions[4-6]. In one of the early studies, the umbilical cord blood gases at delivery were compared to the fetal heart rate tracing for the half hour prior to the delivery. Not surprisingly severe late decelerations were associated with the heighted base deficits, but interestingly severe variable decelerations (intermittent cord compression) showed the largest umbilical artery to vein difference[7]. This was indirect evidence of umbilical cord compression. This can be understood as follows: In the situation of late decelerations, caused by loss of placental gas exchange (uterine contractions with reduced placental gas exchange capacity, or premature placental separation), the fetus will become hypoxic and then acidotic and the fetal blood entering the placenta via the umbilical arteries will not become oxygenated in the placenta. As a result, both the umbilical artery and vein will have similar low oxygen, high lactate (base deficit) levels. In the scenario of cord compression, the flow of fetal blood through the placenta is impeded, but maternal perfusion of the placenta continues. Repetitive deep decelerations can reflect intermittent cord compression that results in fetal hypoxia, oxygen debt and acidosis. This will be reflected in the fetal arterial blood that traverses the umbilical arteries to the placenta. In the still functioning placenta that arterial blood will become well oxygenated which will be reflected in the venous outflow and into the umbilical vein. At delivery, the vein blood will have a higher pO2 and lower lactate than the arterial blood. In general, Dr. Hon’s observations reflected the state of the art in my one-year of obstetrical internship (1975-76), namely we recognized late decelerations as fetal hypoxia and variable decelerations as umbilical cord compression. I don’t recall thinking in detail about the underlying anatomic causes of the fetal heart rate tracings. That approach for me came later as a pathologist, and will be addressed in the following sections.
Occult umbilical cord prolapse
A clinical event that mimics the direct in vitro model of umbilical cord compression is occult cord prolapse. This is manifested by a loop of umbilical cord caught between the pelvis and the presenting fetal part, usually the skull. The cord does not cross the cervical os, and therefore cannot be palpated as in a complete umbilical cord prolapse in which the delivery of the umbilical cord precedes that of the presenting fetal part. In early clinical case reports the diagnosis, when not inferred, was made by direct observation at Cesarean section for fetal distress (distress in the 1950’s was defined as thick meconium and fetal bradycardia auscultated with a fetoscope, a type of stethoscope strapped over the head that was still being used during my training in 1975) [8, 9]. Some of the reports of occult cord prolapse are demonstrations of cord presentation in vulnerable fetuses such as those in transverse or breech lie who would then be vulnerable to cord prolapse following rupture of the membranes. In one such report demonstrated that manually pushing the fetal part against the pelvic inlet by fundal or suprapubic pressure could cause fetal bradycardia[10]. There was no indication of how much pressure was used, but in principle this proves that physiologic levels of pressure could occlude the cord.
In the Perinatal Collaborative study the incidence of occult cord prolapse was 0.35%, but as they noted determining the incidence clinically is quite difficult[11]. The study found an increase in perinatal mortality in mature infants with occult prolapse but otherwise no consequential poor outcome.
During the labor of one of my daughters, the fetal heart rate developed a pattern of repetitive deep decelerations that on ultrasound examination demonstrated that the umbilical cord that was alongside the fetal head was being compressed with each contraction. The maternal fetal medicine physician said this was not going to get any better with continued labor, and recommended a Cesarean delivery to avoid potential hypoxic ischemic brain injury. The outcome was successful. Certainly one case proves nothing, but the logic seems very compelling. If the cause of an abnormal fetal heart rate tracing can be determined, a rational decision can be made as to when and how to intervene. At least one case report of occult prolapse suggests this approach[12], but I could not find large prospective studies of it. I think the potential value of this approach will become more obvious in the further sections about the mechanisms of fetal asphyxia.
Umbilical cord prolapse
Umbilical cord prolapse occurs when the cord slips by the presenting part and presents over or through the cervical os. There are many papers on the risk factors for cord prolapse, basically situations in which the presenting part is not obstructing the cervical os, such as malpresentation, polyhydramnios, and premature rupture of membranes. The prolapsed cord might be compromised by contractions compressing the cord against the fetus similar to occult prolapse, but few studies have examined what is specifically happening to the cord, except that trying to put it back in does not solve the problem[13].
Interestingly in one of Dr. Hon’s early studies he demonstrated the effects of manually compressing a prolapsed umbilical cord for 25 and 40 seconds, and the fetal heart rate decelerations produced resembled those produced by natural contractions with an onset just after compression, and then a compounded late deceleration[4].
The ability to recognize umbilical cord presentation (the cord in front of the fetal presenting part) by ultrasound has been documented, but the value of the finding is controversial since many of the patients do not go on to have cord prolapse, and most of those that do, already had a known high risk for prolapse such as an abnormal lie, either transverse or breech[14, 15]. The cord in these studies was often identified by normal ultrasound without Doppler studies, suggesting that the location of the cord over the cervical os could potentially be seen even without blood flow as in a stillborn infant[10, 15]. Conceivably, a trapped umbilical cord across the internal os of the uterine cervix could lead to cord compression and fetal death prior to delivery perhaps from uterine contractions or even by gravity. While umbilical cord prolapse is not a common cause of stillbirth, in one study of 17,265 deliveries there were 6 in which cord prolapse was diagnosed before or at the time of fetal death[16].
Fetal grasping of the umbilical cord
An unexpected cause of umbilical cord compression is that reported due to fetal grasping of the cord, due to the fetal grasp reflex. The early reports correlated fetal grasping with variable fetal heart rate decelerations[17, 18]. Others subsequently reported cases that appeared to have persistent fetal grasping of the cord with evidence of increased umbilical vascular resistance and fetal hypoxia[19-21]. In one series of 7 such cases one infant had “dystonia syndrome and mild motor deficit as a sign of peripartal hypoxia”[20]. While the wording of the report is not completely clear, this was likely the infant who persisted in grasping his cord through labor and even after delivery. These observations raise the question how much pressure can the fetal hand generate. As an approximate guide, a newborn infant can support its own weight, so we are looking at a force that could exceed 4 lbs.
Anhydramnios and the umbilical cord
Another suspected manner of causing umbilical cord compression is the loss of the protective surrounding amniotic fluid. Normally the cord is suspended in the fluid, and like someone scuba diving in water, because the pressure is surrounding on all sides, pressure from uterine contractions do not cause umbilical cord compression. If fluid is absent, the cord is more likely to be compressed by a solid part of the fetus during a uterine contraction. Absent amniotic fluid can be a consequence of failed urine production, the source of the amniotic fluid. This can occur with absent kidneys, obstruction of urinary tract outflow or some intrinsic renal diseases. Indeed such infants may have an increased incidence of stillbirth. In my autopsy database of infants with lethal renal related oligohydramnios, 99 were liverborn, and 16 were stillborn. Given the usual incidence of 1 stillbirth in 250 live births, this appears to be excessive, consistent with the idea that oligohydramnios in itself increases the incidence of stillbirth, perhaps from cord compression.
More commonly, the loss of amniotic fluid is the consequence of ruptured fetal membranes. In early studies of fetal blood pH, the artificial rupture of membranes did produce a transient acidemia in some infants, but only a minority of these had a concurrent bradycardia to suggest cord compression[22]. A decrease of utero-placental perfusion from accommodation to the loss of intrauterine volume seemed the more likely cause[23]. In 1976 Gabbe and colleagues published a paper in rhesus monkeys that described variable fetal heart rate decelerations with ruptured membranes that could be reduced by restoring the amniotic fluid volume[24]. Subsequently amniotic fluid infusion became a part of obstetrical practice. A review by the Cochrane Pregnancy and Childbirth Group’s Trials Register demonstrated some efficacy of the practice[25]. The authors concluded: “The use of amnioinfusion for potential or suspected umbilical cord compression may be of considerable benefit to mother and baby by reducing the occurrence of variable FHR decelerations, improving short-term measures of neonatal outcome, reducing maternal postpartum endometritis and lowering the use of caesarean section, although there were methodological limitations to the trials reviewed here. In addition, the trials are too small to address the possibility of rare but serious maternal adverse effects of amnioinfusion. More research is needed to confirm the findings, assess longer-term measures of fetal outcome, and to assess the impact on caesarean section rates when the diagnosis of fetal distress is more stringent. Trials should assess amnioinfusion in specific clinical situations, such as FHR decelerations, oligohydramnios or prelabour rupture of membranes.” The mechanism behind the success of amnioinfusion has been less studied. One study looking at umbilical artery Doppler waveforms found no differences in the waveforms between amnioinfusion that was successful versus unsuccessful in maintaining adequate amniotic fluid[26]. This would suggest that the improvement is not because of the intrauterine pressure on fetal blood flow. If the salutary effect is to prevent acute umbilical cord compression, the anatomic details are still unclear.
Pathologic findings in umbilical cord compression
As a pathologist, proving that a stillbirth is from cord compression is very difficult. One rare observation is focal acute inflammation in a vessel of the umbilical cord without other evidence of intrauterine inflammation. Logically, a severe but partial or intermittent pressure on the cord might induce inflammation in the underlying umbilical cord vessel. I have step sectioned entire umbilical cords from fetal lambs that had been asphyxiated by umbilical cord occlusion and could find no microscopic lesion. The cords were kindly provided by Dr. Laura Bennet, at the Research Centre for Developmental Medicine and Biology, New Zealand. As an aside the United States Department of Agriculture Animal and Plant Health Inspection Services required that I purchase an import permit to receive the formalin fixed cords. Unfortunately, I did not know where the cord occluder had been placed on the cord, and the cords were days to weeks from the actual compression. I am not aware that anyone has looked at the immediate local effects of an experimental cord occluder.
Another suspicious autopsy lesion that sometimes correlates with suspected cord occlusion is pallor of a segment of the cord. Below are some case examples. If an umbilical cord of a living fetus were compressed, there would be backpressure on either side of the compressed area keeping the vessels filled with blood. However, with death, the backpressure would be lost, and portions of an umbilical cord could show less blood depending on the passive placental and fetal blood pressures. If a large segment of the umbilical cord were directly being compressed, that area might remain bloodless after fetal death. As a fetus is retained in the uterus after death, hemoglobin eventually diffuses from red blood cells in the umbilical vessels turning the umbilical cord red. If blood is absent in a portion of the cord, the cord in that area will be appear pale compared to adjacent areas. Below are some case examples.
Case examples:
See short case reviews 9-1, 9-2, 9-3.
References
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2. Georgiou, H.M., et al., The effect of vascular coiling on venous perfusion during experimental umbilical cord encirclement. Am J Obstet Gynecol, 2001. 184(4): p. 673-8.
3. Reynolds, S.R., The proportion of Wharton’s jelly in the umbilical cord in relation to distention of the umbilical arteries and vein, with observations on the folds of Hoboken. Anat Rec, 1952. 113(3): p. 365-77.
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25. Hofmeyr, G.J. and T.A. Lawrie, Amnioinfusion for potential or suspected umbilical cord compression in labour.Cochrane Database Syst Rev, 2012. 1: p. CD000013.
26. Fisk, N.M., et al., Relief of presumed compression in oligohydramnios: amnioinfusion does not affect umbilical artery Doppler waveforms. Fetal Diagn Ther, 1992. 7(3-4): p. 180-5.
obstetrical pathology 