Animal Reproduction (AR)
Animal Reproduction (AR)
Original Article

Colony aging affects the reproductive performance of Swiss Webster females used as recipients for embryo transfer

Geraldine Schlapp; Maria Noel Meikle; Cecilia Silva; Gabriel Fernandez-Graña; Alejo Menchaca; Martina Crispo

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Abstract: The objective was to evaluate the influence of colony aging in a Swiss Webster (SW) outbred stock used as recipients for embryo transfer. In the first study, a retrospective analysis was performed throughout several generations during a 38-month period in 2,398 embryos transferred to 108 SW recipients. A decrease in the percentage of live pups from transferred embryos was found at the end of the period. Impairment occurred due to the incidence of maternal cannibalism that increased from 0% to 67-100% (P<0.05), while pregnancy rate (pregnant/transferred recipients) and number of pups per delivered female were not affected throughout the period (P=NS). A following study was carried out to compare the reproductive performance of SW stock vs. B6D2F1 hybrid females in a 5-year interval. The study was conducted on a total of 893 embryos transferred to 40 females (20 SW and 20 B6D2F1) in Year #1, and 514 embryos transferred to 30 females (15 SW and 15 B6D2F1) in Year #5. No cases of maternal cannibalism were found on Year #1 in any of the strains (0/10 and 0/10). However, an incidence of 44,4% (4/9) was seen on Year #5 for SW, while for B6D2F1 the incidence was 0% (0/12) (P<0.05). Further examination of the uterus showed endometrial cysts and abnormal implantation sites in SW on Year #5 but not in B6D2F1 females. In conclusion, this study reports an impairment of the reproductive performance of an early aged SW outbred stock colony mainly due to the occurrence of maternal cannibalism. This finding has important implications for embryo transfer programs conducted in mouse facilities.


pre-implantation embryos, pregnancy failure, pseudopregnant females, foster, cannibalism


Berry M, Linder C. Breeding systems: considerations, genetic fundamentals, genetic background, and strain types. In: Fox JG, Barthold SW, Davisson MT, Christian Newcomer E, Quimby FW, Smith A, editors. The mouse in biomedical research, history, wild mice, and genetics. 2nd ed., Vol. 1. Burlington: Academic Press; 2006.

Byers SL, Payson SJ, Taft RA. Performance of ten inbred mouse strains following assisted reproductive technologies (ARTs). Theriogenology. 2006;65(9):1716-26. PMid:16271754.

Chia R, Achilli F, Festing MF, Fisher EM. The origins and uses of mouse outbred stocks. Nat Genet. 2005;37(11):1181-6. PMid:16254564.

Di Rienzo J, Casanoves F, Balzarini M, Gonzalez L, Tablada M, Robledo C. InfoStat versión 2020. Argentina: Centro de Transferencia InfoStat, Facultad de Ciencias Agropecuarias, Universidad Nacional de Córdoba; 2020.

Diercks A-K, Schwab A, Rittgen W, Kruspel A, Heuss E, Schenkel J. Environmental influences on the production of pre-implantation embryos. Theriogenology. 2010;73(9):1238-43. PMid:20171725.

Dorsch M, Wittur I, Garrels W. Success of embryo transfer in mice with freshly collected and cryopreserved two-cell embryos with different genetic backgrounds correlated with the number of transferred embryos: a 5-year retrospective analysis. Lab Anim. 2019;53(6):577-86. PMid:30866727.

Festing M. International index of laboratory animals. 6th ed. Newbury, England: 1993a.

Festing MF. FRAR course on laboratory approaches to aging. Genetic quality control in laboratory rodents. Aging (Milano). 1993b;5(4):309-15. PMid:8297934.

Gerlinskaya LA, Litvinova EA, Kontsevaya GV, Feofanova NA, Achasova KM, Anisimova MV, Maslennikova SO, Zolotykh MA, Moshkin YM, Moshkin MP. Phenotypic variations in transferred progeny due to genotype of surrogate mother. Mol Hum Reprod. 2019;25(2):88-99. PMid:30445548.

Hinrichs D, Meuwissen THE, Odegard J, Holt M, Vangen O, Woolliams JA. Analysis of inbreeding depression in the first litter size of mice in a long-term selection experiment with respect to the age of the inbreeding. Heredity (Edinb) 2007;99;81-8.

Jackson Laboratory. Breeding strategies for maintaining colonies of laboratory Mice: a Jackson Laboratory resource manual. Bar Harbor, ME: Jackson Laboratory; 2009.

Kolbe T, Palme R, Touma C, Rülicke T. Repeated use of surrogate mothers for embryo transfer in the mouse. Biol Reprod. 2012;86(1):1-6. PMid:21880946.

Lerch S, Tolksdorf G, Schütz P, Brandwein C, Dormann C, Gass P, Chourbaji S. Effects of embryo transfer on emotional behaviors in C57BL/6 mice. J Am Assoc Lab Anim Sci. 2016;55(5):510-9. PMid:27657704.

Litvinova EA, Kontsevaya GV, Kozhevnikova EN, Achasova KM, Gerlinskaya LA, Feofanova NA, Moshkin MP. Modification of fecal bacteria counts and blood immune cells in the offspring of BALB/c and C57BL/6 mice obtained through interstrain mouse embryo transfer. J Am Assoc Lab Anim Sci. 2020;59(4):401-10. PMid:32517848.

Lutz C, Linder C, Davisson M. Strains, stocks and mutant mice. In: Hedrich HJ, editor. The laboratory mouse. 2nd ed. Burlington: Academic Press; 2012, p. 37-56.

McCallum ML, Pru CA, Niikura Y, Yee S-P, Lydon JP, Peluso JJ, Pru JK. Conditional ablation of progesterone receptor membrane component 1 results in subfertility in the female and development of endometrial cysts. Endocrinology. 2016;157(9):3309-19. PMid:27309940.

Meikle MN, Schlapp G, Menchaca A, Crispo M. Minimum volume Spatula MVD vitrification method improves embryo survival compared to traditional slow freezing, both for in vivo and in vitro produced mice embryos. Cryobiology. 2018;84:77-81. PMid:30040919.

Mir F, Fontaine E, Albaric O, Greer M, Vannier F, Schlafer DH, Fontbonne A. Findings in uterine biopsies obtained by laparotomy from bitches with unexplained infertility or pregnancy loss: an observational study. Theriogenology. 2013;79(2):312-22. PMid:23178080.

Nagy A, Gertsenstein M, Vintersten K, Behringer R. Surgical procedures. Manipulating the mouse embryo, a laboratory manual. 3rd ed. New York: Cold Spring Harbour Laboratory Press; 2003, p. 251–87.

National Research Council. Committee for the Update of the Guide for the Care and Use of Laboratory Animals. Guide for the care and use of laboratory animals. 8th ed. Washington: National Academies Press; 2011.

Nomura T, Yonezawa K. A comparison of four systems of group mating for avoiding inbreeding. Genet Sel Evol. 1996;28(2):141-59.

Pritchett K, Taft R. Reproductive biology of the laboratory mouse. In: Fox JG, Barthold SW, Davisson MT, Christian Newcomer E, Quimby FW, Smith A, editors. The mouse in biomedical research, history, wild mice, and genetics. 2nd ed., Vol. 3. Burlington: Academic Press; 2006.

Rapp KG. HAN-rotation, a new system for rigorous outbreeding. Z Versuchstierkd. 1972;14(3):133-42. PMid:5077749.

Rasmussen S, Glickman G, Norinsky R, Quimby FW, Tolwani RJ. Construction noise decreases reproductive efficiency in mice. J Am Assoc Lab Anim Sci. 2009;48(4):363-70. PMid:19653943.

Rose C, Schwegler H, Hanke J, Yilmazer-Hanke DM. Pregnancy rates, prenatal and postnatal survival of offspring, and litter sizes after reciprocal embryo transfer in DBA/2JHd, C3H/HeNCrl and NMRI mice. Theriogenology. 2012;77(9):1883-93. PMid:22401828.

Schlapp G, Fernández-Graña G, Arévalo AP, Crispo M. Establishment of an environmental microbiological monitoring program in a mice barrier facility. An Acad Bras Cienc. 2018;90(3):3155-64. PMid:30304242.

Schlapp G, Goyeneche L, Fernández G, Menchaca A, Crispo M. Administration of the nonsteroidal anti-inflammatory drug tolfenamic acid at embryo transfer improves maintenance of pregnancy and embryo survival in recipient mice. J Assist Reprod Genet. 2015;32(2):271-5. PMid:25561155.

Stringfellow DA, Seidel SM, International Embryo Transfer Society. Manual of the International Embryo Transfer Society : a procedural guide and general information for the use of embryo transfer technology emphasizing sanitary procedures. Savory, Ill: International Embryo Transfer Society; 2007.

Sztein J, Kastenmayer R, Perdue K. Pathogen-free mouse rederivation by IVF, natural mating and hysterectomy. In: Pease S, Saunders T, editors. Advanced protocols for animal transgenesis : an ISTT manual. New York: Springer; 2011, p. 615-42.

Tannus RJ, Thun R. Influence of endometrial cysts on conception rate of mares. Zentralbl Veterinärmed A. 1995;42(4):275-83. PMid:7495166.

Van Keuren ML, Saunders TL. Rederivation of transgenic and gene-targeted mice by embryo transfer. Transgenic Res. 2004;13(4):363-71. PMid:15517995.

Weber E, Olsson I. Maternal behaviour in Mus musculus sp.: an ethological review. Appl Anim Behav Sci. 2008;114(1-2):1-22.

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