Urinary estrogens as a non-invasive biomarker of viable pregnancy in the giant panda (Ailuropoda melanoleuca)

Kirsten S Wilson,Hemin Zhang,Desheng Li,Ruth Andrew,Mick T Rae,Jella Wauters,Forbes Howie,Iain Valentine,William Colin Duncan,Rengui Li,Simon Girling,Alan Mcneilly

doi:10.1038/s41598-019-49288-6

Abstract

Female giant pandas show complex reproductive traits, being seasonally monoestrus, displaying a variable length embryonic diapause and exhibiting pseudopregnancy. Currently, there is no confirmatory non-invasive biomarker of blastocyst implantation or pregnancy. This study aimed to monitor urinary estrogens across gestation in pregnancy (n = 4), pseudopregnancy (n = 4) and non-birth cycles (n = 5) in the giant panda. A pregnancy-specific profile of estrogens corrected for urinary specific gravity was identified during the gestation period. Pregnant females showed increasing concentrations of estrogens for 29 days until birth, no increase was observed during pseudopregnancy and the two profiles were distinguishable from each other for the final 2 weeks of the cycle suggesting the estrogens are of placental origin. This allowed a nomogram, starting at a known fixed point during the cycle, to be created and tested with cycles of known outcome, and cycles which were inseminated but did not result in a birth. Non-birth profiles showed deviations from that of pregnancy. We believe these deviations indicate the point of failure of the placenta to support a developing cub. Non-invasive longitudinal monitoring of estrogen concentrations therefore has the potential to be developed as a panda pregnancy test to predict viable cub development.

Highlights

Conservation success recently downgraded giant pandas from endangered to vulnerable[1], there are fewer than 2000 giant pandas (Ailuropoda melanoleuca) in the wild throughout China
P4 and estrogen concentrations did not correlate across the luteal phase of the cycle (r = −0.25, P = 0.43)
Our study clearly illustrates that the measurement of urinary estrogens corrected for urinary specific gravity (USpG) provides noteworthy potential as a non-invasive biomarker of ongoing pregnancy in the giant panda

Summary

Introduction

Conservation success recently downgraded giant pandas from endangered to vulnerable[1], there are fewer than 2000 giant pandas (Ailuropoda melanoleuca) in the wild throughout China. The captive breeding programme has facilitated conservation and succeeded in increasing the global population of giant pandas[2], which includes over 500 pandas in captivity. It has been vital in aiding understanding of their complex reproductive physiology. The peak P4 in the secondary rise is associated with a prostaglandin surge and there is a marked spike of urinary 13,14,dihydro-15-keto- prostaglandin F2α (PGFM) in the urine[7]. Giant pandas undergo pseudopregnancy; the luteal phase of all ovulating female pandas displays the same biphasic P4 profile and urinary PGFM surge during the secondary rise, independent to pregnancy[6]. During the secondary P4 rise, PGFM can be used as a predictive marker for the timing of birth[7]

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Conclusion