Introduction
Nuclear transfer of somatic cells and other biotechnologies
applied to embryo production in vitro yield very few em-
bryos that are competent to become live offspring. Multiple
factors can cumulatively impinge on embryonic compe-
tence, including methods for the induction of ovulation,
in vitro maturation (IVM), fertilization, culture, nuclear
transfer, gene injection, cryopreservation and transfer. In
general, minimization of in vitro handling associated with
these procedures is likely to be beneficial to subsequent
development. This is especially true for pig gametes and
embryos, as the techniques are less well developed for this
species (Nagashima et al., 1995; Wang et al., 1998, 1999;
Dobrinsky et al., 2000).
Several groups have reported the production of viable
piglets after nuclear transfer of somatic cells (Betthauser
et al., 2000; Onishi et al., 2000; Polejaeva et al., 2000).
Interestingly, all of these groups transferred cloned embryos
to final recipients before embryonic compaction. Although
piglets were produced, the proportion of embryonic loss
directly due to early transfer is unknown. In early studies in
mice and sheep, transfer of precompacted embryos with
disrupted zonae pellucidae resulted in embryonic loss
(Modlinski, 1970; Bronson and McClaren, 1970; Trounson
and Moore, 1974). Transfer of zona pellucida-free rabbit
blastomeres also results in embryonic loss (Moore et al.,
1968). However, nuclear transfer rabbit embryos can
survive immediate oviductal transfer (Collas and Robl,
1990; Stice and Robl, 1998). The mechanism by which
embryos are lost remains unclear, although it has been
speculated that the loss reflects immunological attack
(Moore et al., 1968). The objective of the first experiment in
Reproduction (2002) 123, 507–515
Research
Embryo transfer and pregnancy maintenance strategies in
pigs were evaluated with reference to situations in which
limited numbers of viable embryos or micromanipulated
embryos are available, such as pig cloning. Development
of embryos with compromised zona pellucida was com-
pared with development of embryos with intact zona
pellucida. Micromanipulation had no effect on blastocyst
production rates after development in vivo or in vitro, but
development in vivo improved the number of embryos
reaching the blastocyst stage. Transfer of embryos with
compromised zona pellucida resulted in live piglets.
Several hormone treatments to maintain pregnancy were
tested in a model in which three embryos were transferred
into unmated recipient gilts, compared with transfer of
three embryos into mated recipients. None of the hormonal
treatments resulted in pregnancy rates of more than 25%
at term and no more than 9% of transferred embryos
survived, in comparison with 50% of the mated recipients
successfully carrying 25% of transferred embryos. Lastly,
the developmental potential of parthenogenetic embryos
was assessed and 62% of transferred embryos resulted in
pregnancies, none of which continued beyond day 55 of
gestation. After co-transfer of three fertilized embryos
with 55–60 parthenogenetic embryos into each of six
recipients, two live piglets were delivered. The results from
the present study indicate that transfer of zona pellucida
compromised embryos can yield litters of normal piglets.
In addition, it was demonstrated in a model system involving
the transfer of three fertilized embryos into mature gilts
that hormonal pregnancy maintenance strategies support a
low proportion of embryos to term. Lastly, the present
study shows for the first time a comparably effective but
novel alternative for pregnancy maintenance in the pig
involving the co-transfer of parthenote embryos.
© 2002 Society for Reproduction and Fertility
1470-1626/2002
Embryo development and establishment of pregnancy after
embryo transfer in pigs: coping with limitations in the
availability of viable embryos
T. J. King
1
, J. R. Dobrinsky
2
, J. Zhu
1
, H. A. Finlayson
1
, W. Bosma
1
,
L. Harkness
1
, W. A. Ritchie
1
, A. Travers
1
, C. McCorquodale
1
,
B. N. Day
3
, A. Dinnyés
1
, P. A. De Sousa
1
and I. Wilmut
1
*
1
Department of Gene Expression and Development, Roslin Institute (Edinburgh), Roslin,
Midlothian, Edinburgh EH25 9PS, UK;
2
Germplasm & Gamete Physiology Laboratory, ARS,
US Department of Agriculture, Beltsville, MD 20705, USA; and
3
Animal Science Unit,
University of Missouri, College of Agriculture, Animal Sciences Centre, Columbia,
MO 65211, USA
*Correspondence
Email: Ian.Wilmut@bbsrc.ac.uk