Facilities of the Breeding Performance of BALB/с mice

DOI: 10.29296/2618723X-2020-01-04

M. Makarova, ORCID 0000-0003-3176-6386, M. Ilyinskaya, ORCID 0000-0001-8643-3613

St. Petersburg Institute of Pharmacy,

188663, Russia, Leningradskaya region, Vsevolozhskiy district, Kuzmolovskiy, Zavodskaya st., 3-245

Е-mail: [email protected]


Keywords: mice environment nesting ryonic mortality offspring livestock reproduction embryonic losses potential fertility reproductive function pre- and post-implantation death

For citation:

Makarova M.N., Ilyinskaya М.А. Facilities of the Breeding Performance of BALB/с mice. Laboratory Animals for Science. 2020; 1. https://doi.org/10.29296/2618723X-2020-01-04

Abstract

Balb/c mice are widely used in all areas of biomedical research. This is one of the oldest lines, which is considered noncancerous, despite the available data on the frequency of spontaneous neoplastic formations of the mammary glands, lungs and kidneys, which in some sublines can reach 40%. Many cell and tissue cultures that are widely used in biomedical experiments originate from balb/c mice. Breeding success among rodents kept in laboratory conditions consists of a combination of factors related to the health of the livestock, as well as the conditions of maintenance (population density, feeding, environmental parameters). The review considers and systematizes the influence of certain factors on the reproduction of balb/c mice.

Temperature affects mice mainly when they are kept at elevated values. The humidity of the environment significantly affects the health of mice. The data related to both a decrease and an increase in humidity are considered. Indicators of ventilation and air exchange also have a significant impact on the reproduction of the mice population. The most important indicator that affects the welfare of animals is considered to be the concentration of ammonia.

The intensity and duration of lighting affect behavior, physiology, and reproductive parameters of balb/c mice. The greatest danger is high intensity of lighting and changes in circadian cycles, which can cause phototoxic retinopathy and have a systemic effect, reducing reproductive function. It is impossible to exclude the influence of nutrition factors on reproductive function. It is shown that both the deficiency of nutrients and their redundancy have a negative effect on reproduction indicators.

Enrichment of the habitat with various elements, including nesting material, has a positive effect on the fertility of balb/c mice, while the type of enrichment and nesting material does not play a significant role.

The review concludes with recommendations from the Jackson Laboratory specialists for optimizing the reproduction of balb/c mice.

Full text avaliable in Russain only

References

  1. Бландова З.К., Душкин В.А., Малашенко А.М., Шмидт Д.Т. Линии лабораторных животных для медико-биологических исследований. М.: Наука, 1983, 190 с. [Blandova Z.K., Dushkin V.A., Malashenko A.M., Shmidt D.T. Linii laboratornykh zhivotnykh dlya mediko-biologicheskikh issledovanii. M.: Nauka, 1983, 190 p. (in Russ.)].
  2. The BALB/c Mouse Genetics and Immunology. Ed. by M. Potter, in book: Current Topics in Microbiology and Immunology. Springer-Verlag. 1985. 260 p. DOT: 10.1007/978-3-642-70740-7.
  3. Каркищенко В.Н., Шмидт Е.Ф., Брайцева Е.В. Исследователи предпочитают мышей BALB/c// Биомедицина. 2007; 6: 57–70. [Karkishchenko V.N., Shmidt E.F., Braitseva E.V. Issledovateli predpochitayut myshei BALB/c// Biomeditsina. 2007; 6: 57–70 (in Russ.).]
  4. Мамина В.П. Механизмы формирования эмбриональных потерь у мышевидных грызунов. Успехи современной биологии. 2010; 4: 426-32. [Mamina V.P. Mekhanizmy formirovaniya embrional'nykh poter' u myshevidnykh gryzunov. Uspekhi sovremennoi biologii. 2010; 4: 426–32 (in Russ.).]
  5. Strong L.C. The establishment of the "A" strain of inbred mice. J Heredity. 1963. Vol. 27: 21–4.
  6. MacDowell E.C., All en E.C., MacDowell C.G. The prenatal growth of the mouse. J. Gen. Physiol. 1927. Vol.11: 57–70.
  7. Yamauchi C., Fujita S., Obara T., Ueda T. Effects of room temperature on reproduction, body and organ weights, food and water intakes, and hematology in mice. Experimental Animal. 1983. Vol. 32 (1): 1–11.
  8. Gordon C.J., Becker P., Ali J.S. Behavioral thermoregulatory responses of single- and group-housed mice. Physiol Behav. 1998. Vol. 65 (2): 255–62.
  9. Gordon C.J. Effect of cage bedding on temperature regulation and metabolism of group-housed female mice. Comp Med. 2004. Vol. 54 (1): 63–8.
  10. Gordon C.J. Relationship between autonomic and behavioral thermoregulation in the mouse. Physiol Behav. 1985. Vol. 34 (5): 687–90.
  11. Gordon C.J. Temperature Regulation in Laboratory Rodents. Cambridge: Cambridge University Press. 1993: 276.
  12. Swoap S.J., Overton J.M., Garber G. Effect of ambient temperature on cardiovascular parameters in rats and mice: a comparative approach. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004. Vol. 287 (2): 391–6.
  13. Himms-Hagen J., Villemure C. Number of mice per cage influences uncoupling protein content of brown adipose tissue. Proceedings of the Society for Experimental Biology and Medicine. 1992. Vol. 200: 502–6.
  14. Prychodko W. Effect of aggregation of laboratory mice (Mus musculus) on food intake at different temperatures. Ecology. 1958. Vol. 39 (3): 500–3.
  15. Gordon C.J. Effect of cage bedding on temperature regulation and metabolism of group-housed female mice. Comp. Med. 2004. Vol. 54 (1): 63–8.
  16. Gaskill B.N., Rohr S.A., Pajor E.A. et al. Some like it hot: Mouse temperature preferences in laboratory housing. Applied Animal Behaviour Science. 2009; Vol. 116: 279–85.
  17. Gordon C.J. Temperature Regulation in Laboratory Rodents. Cambridge: Cambridge University Press. 1993: 296.
  18. Yamauchi C., Fujita S., Obara T., Ueda T. Effects of room temperature on reproduction, body and organ weights, food and water intakes, and hematology in mice. Experimental Animal. 1983. Vol. 32 (1): 1–11.
  19. Armstrong K.R., Clark T.R., Peterson M.R. Use of Corn-Husk Nesting Material to Reduce Aggression in Caged Mice. Contemp Top Lab Anim Sci. 1998. Vol. 37 (4): 64–6.
  20. Setchell B.P., Ekpe G., Zupp J.L., Surani M.A. Transient retardation in embryo growth in normal female mice made pregnant by males whose testes had been heated. Hum Reprod. 1998. Vol. 13 (2): 342–7.
  21. Yamamoto S., Ando M., Suzuki E. High-temperature effects on antibody response to viral antigen in mice. Exp Anim. 1999. Vol. 48 (1): 9-–4.
  22. Harakai N., Tomogane K., Miyamoto M. et al. Dynamic response to acute heat stress between 34 degrees celcius and 38.5 degrees celcius, and characteristics of heat stress response in mice. Biol. Pharm. Bull. 2003. Vol. 26 (5): 701–8.
  23. Yaeram J., Setchell B.P., Maddocks S. Effect of heat stress on the fertility of male mice in vivo and in vitro. Reprod Fertil Dev. 2006. Vol 18 (6): 647–53.
  24. Edwards M.J. Congenital defects due to hyperthermia. Advances in Veterinary Science and Comparative Medicine. 1978. Vol 22: 29–52.
  25. Reeb C.K., Jones R.B., Bearg D.W., Bedigian H., Paigen B. Impact of Room Ventilation Rates on Mouse Cage Ventilation and Microenvironment. Contemp Top Lab Anim Sci. 1997. Vol. 36 (1): 74–9.
  26. Clough G. Environmental effects on animals used in biomedical research. Biological Review. 1982. Vol. 57: 487–523.
  27. Donnelly H. Effects of humidity on breeding success in laboratory mice. Laboratory Animal Welfare Research: Rodents. Proceedings of a symposium organized by the Universities Federation for Animal Welfare, held at Royal Holloway and Bedford New College, University of London, Egham, Surrey, UK, 22 April, 1988. Potters Bar, UK: Universities Federation for Animal Welfare. 1989: 17–24.
  28. Lipman N.S., Perkins S.E. Factors that may affect animal research. In: Fox JG, Anderson L.C., Loew F.M., Quimby F.W., eds. Laboratory Animal Medicine. Second ed. San Diego. Academic Press (Elsevier Science). 2002.
  29. DePass L.R., Weil C.S., Ballantyne B., et al. Influence of housing conditions for mice on the results of a dermal oncogenicity bioassay. Fundam Appl Toxicol. 1986; Vol. 7 (4): 601–8.
  30. Barabino S., Rolando M., Chen L., Dana M.R. Exposure to a dry environment induces strain-specific responses in mice. Exp. Eye Res. 2007. Vol. 84 (5): 973–7.
  31. Raut C.G., Gengaje B.B. Ringtail in mice. Indian Veterinary Journal. 1998. Vol. 75 (10): 920–1.
  32. Hosoi J., Hariya T., Denda M., Tsuchiya T. Regulation of the cutaneous allergic reaction by humidity. Contact Dermatitis. 2000. Vol. 42 (2): 81– 4.
  33. Hessler J.R., Leary S.L. Design and management of animal facilities. In: Fox JG, Anderson LC, Loew FM, Quimby FW, eds. Laboratory Animal Medicine. Second ed. San Diego. Academic Press (Elsevier Science). 2002.
  34. Reeb-Whitaker C.K., Paigen B., Beamer W.G., et al. The impact of reduced frequency of cage changes on the health of mice housed in ventilated cages. Lab Anim. 2001. Vol. 35 (1): 58–73.
  35. Whitaker J.W., Moy S.S., Pritchett-Corning K.R., Fletcher C.A. Effects of Enrichment and Litter Parity on Reproductive Performance and Behavior in BALB/c and 129/Sv Mice. J. Am. Assoc. Lab. Anim. Sci. 2016. Vol. № 55 (4): 387–99.
  36. Perkins S.E., Lipman N.S. Evaluation of microenvironmental conditions and noise generation in three individually ventilated rodent caging systems and static isolator cages. Contemp Top Lab Anim Sci. 1996. Vol. 35 (2): 61–5.
  37. Memarzadeh F. Ventilation Design Handbook on Animal Research Facilities Using Static Microisolators. Bestheda, Maryland. National Institutes of Health, Division of Engineering Sciences. 1998.
  38. Clough G. Suggested guidelines for the housing and husbandry of rodents for aging studies. Neurobiology of Aging. 1991. Vol. 12 (6): 653–8.
  39. Broderson J.R., Lindsey J.R., Crawford J.E. The role of environmental ammonia in respiratory mycoplasmosis of rats. Am. J. Pathol. 1976. Vol. 85 (1): 115–30.
  40. Schoeb T.R., Davidson M.K., Lindsey J.R. Intracage ammonia promotes growth of Mycoplasma pulmonis in the respiratory tract of rats. Infect Immun. 1982. Vol. 38 (1): 212–7.
  41. Green A.R., Wathes C.M., Demmers T.G., Clark J.M., Xin H. Development and application of a novel environmental preference chamber for assessing responses of laboratory mice to atmospheric ammonia. J. Am..Assoc. Lab. Anim. Sci. 2008. Vol. 47 (2): 49–56.
  42. Smith A.L., Mabus S.L., Stockwell J.D., Muir C. Effects of housing density and cage floor space on C57BL/6J mice. Comp. Med. 2004. Vol. 54 (6): 656–63.
  43. Clement Y., Chapouthier G. Biological bases of anxiety. Neurosci Biobehav Rev. Sep 1998. Vol. 22 (5): 623–33.
  44. Hascoet M., Bourin M., Dhonnchadha B.A. The mouse light-dark paradigm: a review. Prog Neuropsychopharmacol Biol Psychiatry. 2001. Vol. 25 (1): 141–66.
  45. Weihe W.H., Schidlow J., Strittmatter J. The effect of light intensity on the breeding and development of rats and golden hamsters. Int. J. Biometeorol. 1969. Vol. 13 (1): 69–79.
  46. Greenman D.L., Bryant P., Kodell R.L., Sheldon W. Influence of cage shelf level on retinal atrophy in mice. Lab. Anim. Sci. 1982. Vol. 32 (4): 353–6.
  47. LaVail M.M., Gorrin G.M., Repaci M.A. Strain differences in sensitivity to light-induced photoreceptor degeneration in albino mice. Curr. Eye Res. 1987. Vol. 6 (6): 825–34.
  48. Clough G. Light intensity influences the oestrous cycle of LACA mice. In: Welfare UFfA, ed. Standards in Laboratory Animal Management. Hertfordshire. Universities Federation for Animal Welfare. 1984.
  49. Bronson F.H. Light intensity and reproduction in wild and domestic house mice. Biol Reprod. 1979. Vol. 21 (1): 235–9.
  50. Porter G., Lane-Petter W., Horne N. Effects of strong light on breeding mice. Journal of Animal Tech. Ass. 1963. Vol. 14: 117–9.
  51. Lucas R.J., Freedman M.S., Lupi D. et al. Identifying the photoreceptive inputs to the mammalian circadian system using transgenic and retinally degenerate mice. Behav Brain Res. 2001. Vol. 125 (1-2): 97–102.
  52. Perreault M.L., Rollo C.D. Transgenic growth hormone mice exposed to lifetime constant illumination:gender-specific effects. Canadian Journal of Zoology. 2004. Vol. 82 (6): 950–65.
  53. Drickamer L.C. Daylength and sexual maturation in female house mice. Dev Psychobiol. 1975. Vol. 8 (6): 561–70.
  54. Cameron M.A., Barnard A.R., Lucas R.J. The electroretinogram as a method of studying circadian rhythms in the mammalian retina. Journal of Genetics. 2008. Vol. 87 (5): 459–66.
  55. Sakellaris P.C., Peterson A., Goodwin A., Winget C.M., Vernikos-Danellis J. Response of mice to repeated photoperiod shifts: susceptibility to stress and barbiturates. Proc Soc Exp Biol Med. 1975. Vol. 149 (3): 677–80.
  56. Jiang Z., Liu Y., Wan C., et al. Different light-dark cycles affect growth rate and food intake of mice. Biological Rhythm Research. 2006. Vol. 37 (1): 11–9.
  57. Campuzano A., Cambras T., Vilaplana J., Canal M.M., Carulla M., Diez-Noguera A. Period length of the light-dark cycle influences the growth rate and food intake in mice. Physiol Behav. 1999. Vol. 67 (5): 791–7.
  58. Filipski E., Innominato P.F., Wu M, et al. Effects of light and food schedules on liver and tumor molecular clocks in mice. J Natl Cancer Inst. 2005. Vol. 97 (7): 507–17.
  59. Kolaczkowska E., Chadzinska M., Seljelid R., Plytycz B. Strain differences in some immune parameters can be obscured by circadian variations and laboratory routines: studies of male C57BL/6J, Balb/c and CB6 F1 mice. Laboratory Animals Ltd. 2000. Vol. 35: 91–100.
  60. Dauchy R.T., Sauer L.A., Blask D.E., Vaughan G.M. Light contamination during the dark phase in "photoperiodically controlled" animal rooms: effect on tumor growth and metabolism in rats. Lab Anim Sci. 1997. Vol. 47 (5): 511–8.
  61. Lalitha R., Suthanthirarajan N., Namasivayam A. Effect of flickering light stress on certain biochemical parameters in rats. Indian J Physiol Pharmacol. 1988. Vol. 32 (3): 182–6.
  62. Семенов Χ.X., Малашенко Α.Μ. Цитологическое исследование ранней эмбриональной смертности у лабораторных мышей. Бюл. эксперим. биологии и медицины. 1975. 80: 107. [Semenov Χ.X., Malashenko Α.Μ. Tsitologicheskoe issledovanie rannei embrional'noi smertnosti u laboratornykh myshei // Byul. eksperim. biologii i meditsiny . 1975. Vol. 80: 107 (in Russ.).]
  63. Danny L.В., Keith Υ. Е. Factors influencing peri- and early postnatal calf mortality. J . Anim. Sci. 1973. Vol. 37: 1092.
  64. Penn D., Potts W.K. Chemical signals and parasite-mediated sexual selection. Trends Ecol. Evol. 1998. Vol. 13 (10): 391.
  65. Осадчук Л.В., Межлинейные различия в формировании генеративной функции в период полового созревания у самцов мышей//Онтогенез. 2010; 3: 213–20. [Osadchuk L.V., Mezhlineinye razlichiya v formirovanii generativnoi funktsii v period polovogo sozrevaniya u samtsov myshei. Ontogenez. 2010; 3: 213–20 (in Russ.)].
  66. Hillman N., Nadijcka M. A comparative study of spermiogenesis in wild-type and T:t-bearing mice. Embryol. exp. Morph. 1978. Vol. 44: 243–61.
  67. Dewsbury D.A. Dominance rank, copulatory behavior, and differential reproduction. Quart. Rev. Biol. 1982. Vol. 57: 135.
  68. Lenington S., Coopersmith C., Williams J. Genetic basis of mating preferences in wild house mice. Amer. Zool. 1992. V. 32: 40.
  69. Герлинская Л.А. Механизмы поддержания гетерогенного воспроизводства в популяциях млекопитающих: Автореф. дис. докт. биол. наук. Новосибирск: НИИ физиологии СО РАМН, 2008: 34 с. [Gerlinskaya L.A. Mekhanizmy podderzhaniya geterogennogo vosproizvodstva v populyatsiyakh mlekopitayushchikh: Avtoref. dis. d-ra biol. nauk. Novosibirsk: GU NII fiziologii SO RAMN, 2008: 34 р. (in Russ.)].
  70. Morozova A.Y., Zubkov E.A. Behavioral Patterns and Expression of Genes Coding Serotonin Receptors in Rats with Ultrasound Induced Depression. British Journal of Medicine & Medical Research. 2013. Vol. 3 (4): 2107–18.
  71. Pleasants J.R., Johnson M.H., Wostmann B.S. Adequacy of chemically defined, water-soluble diet for germfree BALB/c mice through successive generations and litters. J Nutr. 1986. Vol. 116 (10): 49–64.
  72. Berger A., German J.B., Chiang B.L., Ansari A.A. et al. Influence of feeding unsaturated fats on growth and immune status of mice. 1993. Vol. 123 (2): 25–33.
  73. Bianconi S., Santillán M.E., Solís M.D.R., Martini A.C. et al. Effects of dietary omega-3 PUFAs on growth and development: Somatic, neurobiological and reproductive functions in a murine model. J Nutr Biochem. 2018. Vol. 61: 82–90.
  74. Palsdottir V., Mansson J.E., Blomqvist M., Egecioglu E., Olsson B. Long-term effects of perinatal essential fatty acid deficiency on anxiety-related behavior in mice. Behav Neurosci. 2012. Vol. 126 (2): 361–9. DOI: 10.1037/a0027161.
  75. Mukerjee S., Zhu Y., Zsombok A. et al. Perinatal Exposure to Western Diet Programs Autonomic Dysfunction in the Male Offspring. Cell Mol Neurobiol. 2018. Vol. 38 (1): 233–42. DOI: 10. 1007/s10571-017-0502-4.
  76. Skaznik-Wikiel M.E., Swindle D.C., Allshouse A.A., Polotsky A.J., McManaman J.L. High-Fat Diet Causes Subfertility and Compromised Ovarian Function Independent of Obesity in Mice. Biol Reprod. 2016. Vol. 94 (5): 108. DOI: 10.1095/biolreprod.115.137414.
  77. Kubandová J., Fabian D., Burkuš J., Cikoš Š. et al. Two-generation diet-induced obesity model producing mice with increased amount of body fat in early adulthood. Physiol Res. 2014. Vol. 63 (1): 103–13.
  78. Da Silva V.C., Fernandes L., Haseyama E.J., Agamme A.L. et al. Effect of vitamin B deprivation during pregnancy and lactation on homocysteine metabolism and related metabolites in brain and plasma of mice offspring. PLoS One. 2014. Vol. 9 (4): 72–83. DOI: 10.1371/journal.pone.0092683.
  79. Tarín J.J., Pérez-Albalá S., Pertusa J.F., Cano A. Oral administration of pharmacological doses of vitamins C and E reduces reproductive fitness and impairs the ovarian and uterine functions of female mice. Theriogenology. 2002. Vol. 57 (5): 39–50.
  80. Cederroth C.R., Zimmermann C., Beny J.L., Schaad O. et al. Potential detrimental effects of a phytoestrogen-rich diet on male fertility in mice. Mol Cell Endocrinol. 2010. Vol. 321 (2): 52–60. DOI: 10.1016/j.mce.2010.02.011.
  81. Jung E.Y., Lee B.J., Yun Y.W. et al. Effects of exposure to genistein and estradiol on reproductive development in immature male mice weaned from dams adapted to a soy-based commercial diet. J Vet Med Sci. 2004. Vol. 66 (11): 47–54.
  82. Wang H., Tranguch S., Xie H. et al. Variation in commercial rodent diets induces disparate molecular and physiological changes in the mouse uterus. Proc Natl Acad Sci USA. 2005. Vol. 102 (28). DOI: 10.1073/pnas.0501632102
  83. Sayed A.A., Ali A.A., Mohamed H.R.H. Fertility enhancing efficacy of Cicer arietinum in male albino mice. Cell Mol Biol (Noisy-le-grand). 2018; Vol. 64 (4): 29–38.
  84. Utsugi C., Miyazono S., Osada K., Sasajima H., Noguchi T., Matsuda M., Kashiwayanagi M. Hard-diet feeding recovers neurogenesis in the subventricular zone and olfactory functions of mice impaired by soft-diet feeding. PLoS One. 2014. Vol. 9 (5). DOI: 10.1371/journal.pone.0097309.
  85. Noguchi T., Utsugi C., Kashiwayanagi M. Soft-diet feeding impairs neural transmission between mitral cells and interneurons in the mouse olfactory bulb. Arch Oral Biol. 2017: 209–13. DOI: 10.1016/j.archoralbio.
  86. Brain P. Understanding the behaviour of feral species may facilitate design of optimal living conditions for common laboratory rodents. Animal Technology. 1992. Vol. 43: 99–105.
  87. Sherwin C.M. Observations on the prevalence of nest-building in nonbreeding TO strain mice and their use of two nesting materials. Lab Anim. 1997. Vol. 31 (2): 125–132.
  88. Olsson I.A., Dahlborn K. Improving housing conditions for laboratory mice: a review of "environmental enrichment". Lab Anim. 2002. Vol. 36 (3): 243–70.
  89. Roper T.J. Nest material and food as reinforcers for fixed-ratio responding in mice. Learning and Motivation. 1975. Vol. 6: 327–43.
  90. Roper T.J. Self-sustaining activities and reinforcement in the nest building behaviour of mice. Behaviour. 1975. Vol. 59: 40–57.
  91. Roper T.J. Diurnal rhythms in the nest-building behaviour of female mice. Behaviour. 1975. Vol. 52: 95–103.
  92. Roper T.J. Diurnal rhythms in the nest-building behaviour of female mice. Behaviour. 1975. Vol. 52: 95–103.
  93. Sherwin C.M., Nicol C.J. Changes in meal patterning by mice measure the cost imposed by natural obstacles. Applied Animal Behaviour Science. 1995. Vol. 43: 291–300.
  94. Weerd H.A. van de, Loo PLP van, Zutphen LFM van et al. Strength of preference for nesting material as environmental enrichment for laboratory mice. Applied Animal Behaviour Science. 1998. Vol. 55 (3/4): 369–82.
  95. Sherwin C.M. Preferences of individually housed TO strain laboratory mice for loose substrate or tubes for sleeping. Lab Anim. 1996. Vol. 30 (3): 245–51.
  96. Weerd H.A. van de, Loo P.L. van, Zutphen L.F. van et al. Preferences for nesting material as environmental enrichment for laboratory mice. Lab Anim. 1997. Vol 31 (2): 133–43.
  97. Weerd H.A. van de, Baumans V., Koolhaas J.M., Zutphen L.F. van. Strain specific behavioural response to environmental enrichment in the mouse. J Exp Anim Sci. 1994. Vol. 36 (4-5): 117–127.
  98. Loo PLP van, Meer E. van der, Kruitwagen C.L. et al. Long-term effects of husbandry procedures on stress-related parameters in male mice of two strains. Laboratory Animals. 2004. Vol. 38 (2): 169–77.
  99. Loo P.L.P. van, Blom H.J.M., Meijer M.K, Baumans V. Assessment of the use of two commercially available environmental enrichments by laboratory mice by preference testing. Laboratory Animals. 2005. Vol. 39 (1): 58–67.
  100. Watson D.S. Evaluation of inanimate objects on commonly monitored variables in preclinical safety studies for mice and rats. Lab Anim Sci. 1993. Vol. 43 (4): 378–80.
  101. Loo P.L.P. van, Meer E. van der, Kruitwagen C.L. et al. Long-term effects of husbandry procedures on stress-related parameters in male mice of two strains. Laboratory Animals. 2004. Vol. 38 (2): 169–77.
  102. Dahlborn K., Gils BAA van, Weerd H.A. van de, Dijk J. van, Baumanns V. Evaluation of long-term environmental enrichment in the mouse. Scandinavian Journal of Laboratory Animal Science. 1996. Vol. 23: 97–106.
  103. Loo P.L.P. van, Meer E. van der, Kruitwagen C.L. et al. Strain-specific aggressive behaviour of male mice submitted to different husbandry procedures. Aggressive Behaviour. 2003. Vol. 29: 69–80.
  104. Mulder J.B. Bedding preferences of pregnant laboratory-reared mice. Behaviour Research Methods and Instrumentation. 1975. Vol. 7 (1): 21–2.
  105. Oortmerssen G.A. van. Biological significance, genetics and evolutionary origin of variability in behaviour within and between inbred strains of mice (Mus musculus). A behaviour genetic study. Behaviour. 1971. Vol. 38 (1): 1–92.
  106. Eskola S., Kaliste E. Nesting material and number of females per cage: effects on mouse productivity in BALB/c, C57BL/6J, DBA/2 and NIH/S mice. Article in Laboratory Animals. 1999. Vol. 33 (2): 108–12.
  107. Moreira V.B, Mattaraia V.G.M., Moura A.S. Lifetime Reproductive Efficiency of BALB/c Mouse Pairs after an Environmental Modification at 3 Mating Ages. J Am Assoc Lab Anim Sci. 2015. Vol. 54 (1): 29–34.
  108. Walker M/, Fureix C/, Palme R. et al. Mixed-strain housing for female C57BL/6, DBA/2, and BALB/c mice: validating a split-plot design that promotes refinement and reduction. BMC Med Res Methodol. 2016. Vol. 16: 11. DOI: 10.1186/s12874-016-0113-7.
  109. Kavaliers M., Colwell D.D., Choleris E. Analgesic responses of male mice exposed to the odors of parasitized females: effects of male sexual experience and infection status. Behav. Neurosci. 1998. Vol. 112 (4): 1001.
  110. Kavaliers M., Colwell, D.D., Braun W.J., Choleris E. Brief exposure to the odour of a parasitized male alters the subsequent mate odour responses of female mice. Anim. Behav. 2003. Vol. 65: 59–68.

You may be interested