Evaluation of infrared thermography findings in pseudopregnant rabbit

Abstract

The effectiveness of infrared thermography (IRT) in the diagnosis of pseudopregnant rabbits, the change of these images in the pseudopregnancy process, and its relationship with serum progesterone (P4) level was investigated. Fourteen healthy female rabbits of New Zealand breed were divided into two study groups. Pseudopregnancy induction was performed in the first study group with GnRH injection (0.2 ml Buserelin acetate, intramuscularly) on the 0th day of the study (Group 1, n=7). The second group (Group 2, n=7) was given placebo (0.2 ml 0.9% NaCl, intramuscularly). Rectal temperature was taken from all rabbits on days 0-5-10 and 15, eye, nasal tip, and vulvar IRT were applied, and serum P4 valueswere measured by Enzyme-linked immunosorbent assay (ELISA) method. In the pseudopregnant group, the temperatures of the eyes, nose, and vulva were higher on the 10th day (p<0.05). While time-dependent eye, nose, vulva, and rectal temperature changes were observed in the pseudopregnant group (p<0.05), it was not observed in the control group (p>0.05). The increase in rectal temperature was only on the 15th day in the pseudopregnant group (p<0.001). Serum P4 value was high on day 0 in Group 1 (p<0.05), but no change was observed in both groups over time (p>0.05). A low negative correlation (-0.04) was observed between serum P4 value and IRT and rectal measurements, and the highest correlation was observed between nasal temperature and rectal temperature (0.28). Infrared thermography applications in rabbits are useful in non-invasive and rapid body temperature monitoring and can determine the temperature increase in the eyes, nose, and vulva on the 10th day of pseudopregnancy.

Keywords

• Progesterone
• pseudopregnancy
• rabbit
• thermography

Supporting Institution

Aydın Adnan Menderes University Scientific Research Projects Unit

Project Number

VTF-19013

Thanks

The authors would like to thank Aydın Adnan Menderes University Scientific Research Projects Unit for funding this research project numbered VTF-19013.

References

1. Bekyürek, T. (2010). Laboratuvar Hayvanlarında Üreme ve Sorunları. In: Alaçam E (ed), Evcil Hayvanlarda Doğum ve İnfertilite (pp. 355-381). Ankara: Medisan.
2. Bell, D.J. (1999). The European wild rabbit. In: Poole T (ed). The UFAW Handbook on the Care and Management of Laboratory Animals 7th edition (pp. 389-394). Oxford: Blackwell Publishing.
3. Carter, C.L., Adams, J.K., Czarra, J.A., & Coan, P.N. (2016). An incidence of pseudopregnancy associated with the social enrichment of rabbits (Oryctolagus cuniculi). Journal of the American Association for Laboratory Animal Science, 55(1), 98-99.
4. Dal Bosco, A., Rebollar, P.G., Boiti, C., Zerani, M., & Castellini, C. (2011). Ovulation induction in rabbit does: current knowledge and perspectives. Animal Reproduction Science, 129(3-4), 106-117. https://doi.org/10.1016/j.anireprosci.2011.11.007
5. De Freitas, A.C.B., Vega, W.H.O., Quirino, C.R., Junior, A.B., David, C.M.G., Geraldo, A. T., & Dias, A.J.B. (2018). Surface temperature of ewes during estrous cycle measured by infrared thermography. Theriogenology, 119, 245-251. https://doi.org/10.1016/j.theriogenology.2018.07.015
6. De Ruediger, F.R., Yamada, P.H., Barbosa, L.G.B., Chacur, M.G.M., Ferreira, J.C.P., de Carvalho, N.A.T., & Oba, E. (2018). Effect of estrous cycle phase on vulvar, orbital area and muzzle surface temperatures as determined using digital infrared thermography in buffalo. Animal Reproduction Science, 197, 154-161. https://doi.org/10.1016/j.anireprosci.2018.08.023
7. Donnelly, T.M. (2013). Pseudopregnancy. J. Mayer (Ed.): Clinical Veterinary Advisor Birds and Exotic Pets (pp. 411-412). Saint Louis: W.B. Saunders.
8. Dugré, F.J., Lambert, R.D., Bélanger, A. & Fortier, M.A. (1989). Relationship between steroid levels in peripheral serum and uterine tissue during pseudopregnancy in rabbit. Theriogenology, 31(2), 353-360. https://doi.org/10.1016/0093-691X(89)90541-4

9. Durrant B.S., Schwede T., & Spady T.J. (2004). The potential utility of thermography to differentiate pregnancy and pseudopregnancy in bears. Proceedings, 15th International Conference on Bear Research and Management. San Diego, CA.
10. Durrant, B.S., Ravida, N., Spady, T., & Cheng, A. (2006). New technologies for the study of carnivore reproduction. Theriogenology, 66(6-7), 1729-1736. https://doi.org/10.1016/j.theriogenology.2006.02.046
11. Façanha, D.A.E., Peixoto, G.C.X., Ferreira, J.B., de Souza, J.E.R., Paiva, R.D.M., & Ricarte, A.R.F. (2018). Detecting estrus in Canindé goats by two infrared thermography methods. Acta Veterinaria Brasilica, 12(2). https://doi.org/10.21708/avb.2018.12.2.7243
12. Fragalà, S., Medica, P., Grande, F., Vazzana, I., & Fazio, E. (2015). Evaluation of seasonal changes of serum and plasma estradiol-17β, progesterone and testosterone in dolphins (Tursiops truncatus) by chemiluminescence. Veterinary World, 8(8), 977. doi: 10.14202/vetworld.2015.977-982
13. Harris, M.A., & Kesel, M.L. (1990). An improved method for accurately timed mating in rats. Laboratory Animal Science, 40(4), 424-425.
14. Hilsberg-Merz, S. (2008). Infrared thermography in zoo and wild animals. In Fowler, M.E. & Miller, R.E. (eds) Zoo and Wild Animal Medicine. Current Therapy, 6th edn. Philadelphia: Saunders.
15. Hurnik, J.F., Webster, A.B., & De Boer, S. (1985). An investigation of skin temperature differentials in relation to estrus in dairy cattle using a thermal infrared scanning technique. Journal of Animal Science, 61(5), 1095-1102. https://doi.org/10.2527/jas1985.6151095x
16. Huynh, M. (2019). Smartphone-based device in exotic pet medicine. Veterinary Clinics: Exotic Animal Practice, 22(3), 349-366. https://doi.org/10.1016/j.cvex.2019.05.001
17. Johnson, S.R., Rao, S., Hussey, S.B., Morley, P.S., & Traub-Dargatz, J.L. (2011). Thermographic eye temperature as an index to body temperature in ponies. Journal of Equine Veterinary Science, 31(2), 63-66. https://doi.org/10.1016/j.jevs.2010.12.004
18. Jones, M., Denson, A., Williams, E., Dos Santos, A., Graves, K., Kouba, A., & Willard, S. (2005). Assessing pregnancy status using digital infrared thermal imaging in Holstein heifers. Journal of Dairy Science 88, 40-41.
19. Ludwig, N., Gargano, M., Luzi, F., Carenzi, C., & Verga, M. (2007). Applicability of infrared thermography as a noninvasive measurements of stress in rabbit. World Rabbit Science, 15(4). https://doi.org/10.4995/wrs.2007.588
20. Maranesi, M., Petrucci, L., Leonardi, L., Piro, F., Rebollar, P.G., Millán, P., & Zerani, M. (2018). New insights on a NGF-mediated pathway to induce ovulation in rabbits (Oryctolagus cuniculus). Biology of Reproduction, 98(5), 634-643. https://doi.org/10.1093/biolre/ioy041
21. Marcinkiewicz, J.L., Moy, E.S., & Bahr, J.M. (1992). Change in responsiveness of rabbit corpus luteum to prostaglandin F-2α during pregnancy and pseudopregnancy. Reproduction, 94(2), 305-310. https://doi.org/10.1530/jrf.0.0940305
22. McNitt, J.I., Lukefahr, S.D., Cheeke, P.R., Patton, N.M. (2013). Rabbit Reproduction, 9th ed In: Rabbit Production (pp. 144-159). USA.
23. Orstead, M. K., Hess, D.L., & Spies, H.G. (1988). Pulsatile patterns of gonadotropins and ovarian steroids during estrus and pseudopregnancy in the rabbit. Biology of Reproduction, 38(4), 733-743. https://doi.org/10.1095/biolreprod38.4.733
24. Olğaç, K.T., Akçay, E., Çil, B., Uçar, B.M., & Daşkın, A. (2017). The use of infrared thermography to detect the stages of estrus cycle and ovulation time in anatolian shepherd dogs. Journal of Animal Science and Technology, 59(1), 1-6. https://doi.org/10.1186/s40781-017-0146-4
25. Osawa T., Tanaka M., Morimatsu M., Hashizume K., & Syuto B. (2004). Use of infrared thermography to detect the change in the body surface temperature with estrus in the cow. Proceedings from the 2004 SFT/ACT Annual Conference & Symposium. Kentucky-USA.
26. Polit, M., Rząsa, A., Rafajłowicz, W., & Niżański, W. (2018). Infrared technology for estrous detection in Chinchilla lanigera. Animal Reproduction Science, 197, 81-86. https://doi.org/10.1016/j.anireprosci.2018.08.012
27. Ptaszynska, M. (2001). Reproduction in the Rabbit. In: Ptaszynska (Ed). Compendium of Animal Reproduction (pp. 243-256). International Intervet Publisher.
28. Radigonda, V.L., Pereira, G.R., da Cruz Favaro, P., Júnior, F.A.B., Borges, M.H.F., Galdioli, V.H.G., & Júnior, C. K. (2017). Infrared thermography relationship between the temperature of the vulvar skin, ovarian activity, and pregnancy rates in Braford cows. Tropical Animal Health and Production, 49(8), 1787-1791. https://doi.org/10.1007/s11250-017-1378-5
29. Redaelli, V., Ludwig, N., Cosat, L.N., Crosta, L., Riva, J., & Luzi, F. (2014). Potential application of thermography (IRT) in animal production ad for animal welfare. A case report of working dogs. Annali dell’Istituto Superiore di Sanita, 50(2), 147-152.
30. Regidor, P.A. (2014). Progesterone in peri-and postmenopause: a review. Geburtshilfe und Frauenheilkunde, 74(11), 995. doi: 10.1055/s-0034-1383297
31. Rommers, J.M., Boiti, C., De Jong, I., & Brecchia, G. (2006). Performance and behaviour of rabbit does in a group-housing system with natural mating or artificial insemination. Reproduction Nutrition Development, 46(6), 677-687. https://doi.org/10.1051/rnd:2006038
32. Scolari, S.C., Clark, S.G., Knox, R.V., & Tamassia, M.A. (2011). Vulvar skin temperature changes significantly during estrus in swine as determined by digital infrared thermography. Journal of Swine Health and Production. 19(3), 151-155.
33. Sykes, D., Chromiak, A., Couvillion, S., Gerard, P., Crenshaw, M., Willard, S., & Ryan, P. (2006). Estrus detection in gilts using digital infrared thermal imaging. Journal of Animal Science, 84, 1.
34. Sykes, D.J., Couvillion, J.S., Cromiak, A., Bowers, S., Schenck, E., Crenshaw, M., & Ryan, P.L. (2012). The use of digital infrared thermal imaging to detect estrus in gilts. Theriogenology, 78(1), 147-152. https://doi.org/10.1016/j.theriogenology.2012.01.030
35. Talukder, S., Kerrisk K. L., Ingenhoff L., Thomson P.C., Garcia S. C., & Celi P. (2014). Infrared technology for estrus detection and as a predictor of time of ovulation in dairy cows in a pasture-base system. Theriogenology, 81(7), 925-935. https://doi.org/10.1016/j.theriogenology.2014.01.009
36. Talukder, S., Thomson, P.C., Kerrisk, K.L., Clark, C.E.F., & Celi, P. (2015). Evaluation of infrared thermography body temperature and collar-mounted accelerometer and acoustic technology for predicting time of ovulation of cows in a pasture-based system. Theriogenology, 83(4), 739-748. https://doi.org/10.1016/j.theriogenology.2014.11.005
37. Willard, S.T., Vinson, M.C., & Godfrey, R.W. (2006). Digital infrared thermal imaging of the eye as correlated to rectal and vaginal temperature measurements in the ewe. Journal of Animal Science, 84, 434-434.
38. Zavos, P.M., Correa, J.R. , Panayota, N,. Zarmakoupis-Zavos, M.D. (1998). Assessment of a tablet drug delivery system incorporating nonoxynol-9 coprecipitated with polyvinylpyrrolidone in preventing the onset of pregnancy in rabbits. Fertility and Sterility, 69, 4,768-773. https://doi.org/10.1016/S0015-0282(98)00004