Elsevier

Theriogenology

Volume 80, Issue 5, 15 September 2013, Pages 479-486
Theriogenology

Research article
Embryonic resorption in context to intragestational corpus luteum regression: A longitudinal ultrasonographic study in the European brown hare (Lepus europaeus PALLAS, 1778)

https://doi.org/10.1016/j.theriogenology.2013.05.010Get rights and content

Abstract

Embryonic resorption is frequently observed in polytocous mammals. Often it occurs as partial litter resorption affecting only single conceptuses of a whole litter. The aim of the study was to describe the incidence and morphology of embryonic resorption in the European brown hare (Lepus europaeus). In 154 pregnancies viable conceptuses, conceptuses undergoing resorption and CL of pregnancy were ultrasonographically monitored during the entire gestation period. Resorptions were classified into (1) “pre-implantation resorptions,” (2) “peri-implantation resorptions,” and (3) “post-implantation resorptions.” The incidence of resorption in the pre-implantation period was 9%, in the peri-implantation period 9%, and in the post-implantation period 24%. Post-implantation resorptions were found up to late pregnancy stages when fetal development was already in progress. The highest daily incidence of resorption was on Day 8 of the 42-day pregnancy. In 91% of the cases, the regression of one CL was observed, while an embryo was undergoing resorption at the same time. The number of resorptions did not significantly differ from the number of CL in regression during gestation, suggesting an interesting one-resorption-to-one-regression relationship. The ultrasonographic appearance of the luteal regression during pregnancy was similar to the morphology characteristic for postpartal luteolysis.

Introduction

Embryonic resorption is a widespread phenomenon among polytocous species [1], [2]. It often affects only single conceptuses of the litter, whereas others continue to develop until term [3], [4], [5]. This is referred to as “partial litter resorption” [6], whereas resorption of the whole litter is referred to as “total litter resorption” [7]. Incidences of embryonic resorptions in polytocous species are generally based on the difference between the mean number of CL and mean number of embryos, placental scars, and the young [2], [3], [7], [8]. The release of the ovum from the mature follicle results in the autonomous formation of a CL. However, so far there has been no evidence of a correlation between the number of embryos and the number of CL [9], [10]. The reason for this is that studies describing the incidence or morphology of embryonic resorptions are usually performed post mortem or after ovariohysterectomy [9], [10], [11], [12], which explains why it has been not possible to demonstrate intragestational changes of the luteal morphology in the context of embryos undergoing resorption. Moreover, the exact day of embryonic death is usually unknown, and the time course of the resorption process cannot therefore be described. Often, detection of the dead conceptus is difficult because it is already in a late stage of resorption and almost completely decomposed. The establishment of ultrasound as diagnostic tool in reproduction medicine facilitated in vivo longitudinal monitoring of the macroscopic process of embryonic resorptions [4], [13], [14]. However, in small mammals, such as rodents and rabbits, used for experimental studies on a regular basis, descriptions of the resorption process are still based on post mortem studies [15], [16], [17].

In the European brown hare (Lepus europaeus), hereafter referred to as the hare, regular ultrasonographic monitoring of embryonic development showed that resorptions occur on a regular basis [5], [18]. However, detailed studies of the incidence and morphology of embryonic resorptions have not been conducted so far. Based on the recently established parameters for prenatal development in the hare [19], the present study is a longitudinal ultrasonographic investigation of the incidence and morphology of embryonic resorption coupled with ovarian dynamics specifically tracing the development of CL of pregnancy.

Section snippets

Animals

Hares were housed in specific hare breeding cages (type Nitra) on the field research station of the Leibniz Institute of Zoo and Wildlife Research (IZW). Each cage had an area of 2 m2 and comprised a front part where hares had free access to food and drinking water and a back retreat area with fresh hay. Hares were fed ad libitum with a customized hare pellet diet and fresh hay. All hares were kept under natural weather conditions.

The study included 44 females and 38 males. One hundred and

Classification, incidence, and morphology of embryonic resorptions

In 154 pregnancies (n = 44 females), 259 offspring were born healthy at term (1–6 offspring per litter). The overall mean litter size was 2.44 ± 1.08 offspring. A significant difference in mean litter size was detected between animals with (including total litter resorption: 1.33 ± 1.39 offspring; excluding total litter resorption: 2.23 ± 1.09) and without resorption (2.72 ± 1.00 offspring) (paired sample t-test, including total litter resorption: P < 0.0001, excluding total litter resorption:

Discussion

In this study, embryonic resorption and CL regression were monitored for the first time over the complete course of pregnancy in a small polytocous mammal, the European brown hare.

The resorption process in the hare was characterized by an initial increase in the mean diameter before a size reduction was observed. This might be due to a massive influx of maternal blood into the resorption site as shown in the previous resorption studies on hares [5]. Continuous ultrasonographic imaging of the

Acknowledgments

The authors acknowledge our animal keepers Baerbel Baumann, Mathias Otto, Robert Schilke, Steffen Zeise, and Béla Harting from our research station for their help in handling, treating, and maintaining the hare population. The authors also thank their colleagues Dr Claudia Szentiks, Dr Alexandre Courtiol, Luis Eduardo Flores Landaverde, Ina Buentjen, and Mirjam Becker, as well as their technical assistants Angelika Kissmann, Jette Dierich, and Nga Nguyen for their support.

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