Abstract
Umbilical cord accident [UCA] occurs when umbilical blood flow is compromised to a degree where fetal stress, injury or death follows. There are various types of UCA's, including true knots, nuchal cord [loops of cord around the neck] and body coils. The latter is a condition in which the umbilical cord is coiled around a part of the fetus other than the neck, and is caused by movement of the fetus through, or around, a loop of cord. It is associated with excessively long cords [ELUC], a recognised risk factor for fetal malformation and stillbirth.1 In humans, long cords have been significantly associated with maternal systemic disease, increased maternal age, cord entanglement, fetal distress during labour and respiratory distress at delivery.2 Prolonged cord constriction in utero, or compression during labour, can lead to fetal heart decelerations and eventual death.
UCA's are not uncommon in some mammals1,3, however, to the best of our knowledge, this condition has not been reported in dolphins. This presentation describes four cases of ELUC/UCA in two bottlenose dolphins [Tursiops truncatus] and one beluga [Delphinapterus leucas].
Case 1. Female 1, a T. truncatus, with an estimated age of 20 years and an unknown obstetric history, exhibited raised serum progesterone levels in mid-June 2004. Pregnancy was confirmed by ultrasonography in July 2004 and parturition was estimated between May and June 2005. The animal was known to be 'nervous and aggressive'. On February 4th 2005 she exhibited an 'aggressive episode' and the following day aborted a macerated, female fetus. The umbilical cord was looped at least twice around the peduncle, and was congested and flattened. The peduncle showed distinct compression marks from the cord. The cord length was not measured, but staff remember it as being "too long". The calf was 83cm in length; the body weight was not recorded. From the condition of the fetal tissues, it was estimated that intrauterine death had occurred 24-48 hours prior to abortion. Final diagnosis--preterm intrauterine fetal death [IUFD] and abortion secondary to UCA.
Case 2. This case occurred in the same female as in Case 1. Increased serum progesterone levels were again noted in mid-May 2005, three months after the first abortion, and pregnancy was confirmed by ultrasonography one month later. Parturition was initially estimated for May 2006, but later revised to March 2006. Routine ultrasonography on February 7th 2006 showed no fetal heartbeat and the following day Female 1 aborted a macerated, male calf. The calf was 103cm in length and weighed 13.6kg. The umbilical cord was wrapped [again clockwise] four times around the peduncle, which was compressed and wasted. The cord was 51 cm in length. From the condition of the fetal tissues, it was estimated that IUFD had occurred up to 5 days prior to abortion. The cord and membranes showed congestion, edema and haemorrhage, consistent with prolonged compression. No other pathology was found. Final diagnosis--preterm IUFD and abortion secondary to UCA/ELUC.
Case 3. Female 2, a T. truncatus, with an estimated age of 13-15 years, had delivered a healthy, male calf in 2004. She became pregnant again at the end of February 2006. Ultrasonography in August 2006 demonstrated a fetus with marked hydrops and hydrocephaly. It was also noted at this time that the umbilical cord was wrapped around the peduncle, which was small and deformed. Fetal measurements were consistent with a gestational age of 18-20 weeks, although this could not be absolute due to fetal abnormalities. Ultrasonographic examination was repeated regularly to monitor the rapidly increasing fetal diameter. On 5.8.06, the fetal heartbeat [FHB] was slow and difficult to monitor. On 7.8.06 it was not possible to demonstrate a FHB, and on 9.8.06, Female 3 aborted a severely hydropic, macerated, female fetus. The peduncle bore compression marks from the cord and was markedly wasted. The full cord was not recovered due to autolysis and fragmentation, therefore measurement was not possible. The calf was 34cm in length and weighed 1.5kg. Final diagnosis--Preterm IUFD and abortion of fetus with hydrocephalus, hydrops fetalis and compression of the umbilical cord.
Case 4. Female 3, a 20 y.o. D. leucas, with a history of one previous, healthy calf (head-first delivery) in 1999, conceived around 5.6.05. At 17.17h on 8.9.06, she presented with flukes protruding; the calf was out as far as the genital slit by 17.49h and fluke movements were noted. At this time, some 'dark tissue' was visible above the genital slit and around the peduncle. The calf was last seen to move at 20.15h. Female 3 was moved to a back pool and examined at 20.36h. The tissue was seen to be a single loop of umbilical cord, wrapped tightly around the top of the peduncle. Intravenous administration of 140 units of Oxytocin was performed at 20.48h and a stillborn, female calf was expelled a minute later. Resuscitation was unsuccessful. The calf was 155cm in length and weighed 64.5kg, consistent with a term gestation (with a gestation length of 460 days) and the average size of other beluga calves born at this facility. The umbilical cord was wrapped once around the peduncle, in a clockwise direction. The cord was excessively long, at 123cm in length. Otherwise there was no abnormality. There were no cord impressions and no wasting of the peduncle. Final diagnosis--Stillbirth secondary to UCA/ELUC.
The average cord length of T. truncatus is 25-45cm (K. Benirschke, unpublished) and for D. leucas is 91cm (L. Dalton, unpublished). In cases 1, 2 and 4 the umbilical cord was longer than average, with multiple coils around the tail. In cases 1-3, the coils had been tight enough to cause compression and wasting of the peduncle, and eventual death of the fetus; in case 4, cord compression and fetal death occurred during parturition.
It is possible to identify cord abnormalities antenatally using B-mode and Colour Doppler ultrasound and we recommend close examination of the cord be included in all prenatal examinations. Although antenatal treatment may not be possible in dolphins, it would be useful to have forewarning of a potential UCA to encourage earlier intervention during parturition. UCA's also tend to repeat in the same mother4, as Cases 1 and 2 may indicate, therefore it is further recommended that female dolphins with this history should be monitored closely during pregnancy.
Acknowledgements
The authors would like to thank all colleagues at L'Oceanografic, Dolphin Adventures, and SeaWorld San Antonio involved in the care of these cases. Thanks also to Dr Nimal Fernando and Ocean Park Corporation for allowing the use of some ultrasound images.
References
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2. Sornes T, T Bakke. 1989. Uterine size, parity and umbilical cord length. Acta Obstet Gynecol Scand 68:439-441.
3. Whitwell KE. 1975. Morphology and pathology of the equine umbilical cord. J. Reprod Fertil Suppl. 23:599-603.
4. Baergen RN, Malicki D, Behling C, K Benirschke. 2001. Morbidity, mortality and placental pathology in excessively long umbilical cords: Retrospective study. Pediat and Develop Path. 4:144-153.