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Hormonal stress response of laboratory mice to conventional and minimally invasive bleeding techniques

Published online by Cambridge University Press:  01 January 2023

CC Voigt*
Affiliation:
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str 17, D-10315 Berlin, Germany Freie Universität, Takustr 3, D-14195 Berlin, Germany
P Klöckner
Affiliation:
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str 17, D-10315 Berlin, Germany Leibniz Institute for Farm Animal Biology, Wilhelm-Stahl-Allee 2, D-18196 Dummerstorf, Germany
C Touma
Affiliation:
Max Planck Institute of Psychiatry, Kraepelinstr 2-10, D-80804 Munich, Germany
C Neuschl
Affiliation:
Humboldt Universität Berlin, Invalidenstrasse 42, D-10115 Berlin, Germany
G Brockmann
Affiliation:
Humboldt Universität Berlin, Invalidenstrasse 42, D-10115 Berlin, Germany
F Göritz
Affiliation:
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str 17, D-10315 Berlin, Germany
R Palme
Affiliation:
Department of Biomedical Sciences/Biochemistry, University of Veterinary Medicine, Veterinärplatz 1, A-1210 Vienna, Austria
R Thomsen
Affiliation:
University of Leipzig, Talstr 33, D-04103 Leipzig, Germany
*
* Contact for correspondence and requests for reprints: voigt@izw-berlin.de

Abstract

Conventional bleeding of small laboratory animals is often associated with stress and injuries that can cause haematomas, inflammation and ultimately the death of animals under investigation. Here, we used faecal glucocorticoid metabolites as an indicator of stress imposed on laboratory mice (Mus musculus domesticus) when bled in three different ways: puncture of the tail vein following mechanical immobilisation; puncture of the retro-orbital plexus following chemical immobilisation; and a minimally invasive technique using blood-sucking bugs (Reduviidae, Heteroptera) without any immobilisation. We hypothesised that blood-sucking bugs provoke a lower hormonal stress response than conventional bleeding techniques because laboratory animals are not handled and because the mechanical stimulus of an insect sting is supposedly weak. Each of the 16 mice was bled using one of the three methods at a time in a random order with seven days of recovery between subsequent bleeding events. To monitor the stress hormones, we determined corticosterone metabolites in faecal samples of mice collected one day before, 8 h after and one day after the bleeding event. Concentrations of faecal glucocorticoid metabolites increased in all three treatment groups compared with baseline values. However, average concentration of stress hormone metabolites after bleeding was higher by a factor of about 1.5 when conventional bleeding techniques were applied than when bugs were used. We conclude that blood-sucking bugs may offer a gentle alternative for obtaining blood samples from small animals such as mice.

Type
Research Article
Copyright
© 2013 Universities Federation for Animal Welfare

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References

Arnold, JM, Oswald, SA, Voigt, CC, Palme, R, Braasch, A, Bauch, C and Becker, PH 2008 Taking the stress out of blood collection: comparison of field blood-sampling techniques for analysis of baseline corticosterone. Journal of Avian Biology 39: 588592. http://dx.doi.org/10.1111/j.0908-8857.2008.04265.xCrossRefGoogle Scholar
Becker, PH, Voigt, CC, Arnold, JM and Nagel, R 2005 A noninvasive technique to bleed incubating birds without trapping: a blood-sucking bug in a hollow egg. Journal of Ornithology 147: 115118. http://dx.doi.org/10.1007/s10336-005-0027-3CrossRefGoogle Scholar
Braun, BC, Frank, A, Dehnhard, M, Voigt, CC, Vargas, A, Göritz, F and Jewgenow, K 2009 Pregnancy diagnosis in urine of Iberian lynx (Lynx pardinus). Theriogenology 71: 754761. http://dx.doi.org/10.1016/j.theriogenology.2008.09.054CrossRefGoogle Scholar
Gärtner, K, Büttner, D, Döhler, K, Friedel, R, Lindena, J and Trautschold, I 1980 Stress response of rats to handling and experimental procedures. Laboratory Animals 14: 267274. http://dx.doi.org/10.1258/002367780780937454CrossRefGoogle ScholarPubMed
GV Solas Society for Laboratory Animal Science 2009 Recommendations for bleeding laboratory animals, expecially small sized animals. GV Solas Society for Laboratory Animal Science. www.gv-solas.deGoogle Scholar
Hoff, J 2000 Methods of blood collection in the mouse. Laboratory Animals 29(10): 4753Google Scholar
Holst, D 1998 The concept of stress and its relevance for animal behavior. Advances in the Study of Behavior 27: 1131. http://dx.doi.org/10.1016/S0065-3454(08)60362-9CrossRefGoogle Scholar
Klöckner, P, Stefanski, V and Voigt, CC 2013 Testing blood-sucking bugs (Triatominae, Heteroptera) as a blood-sampling technique to evaluate white blood cell subsets. In: Wibbelt, G and Schumann, A (eds) Proceedings of the International Conference on Diseases of Zoo and Wild Animals pp 146155. 8-11 May 2013, Vienna, AustriaGoogle Scholar
Kloet, ER, Oitzl, MS and Joels, M 1999 Stress and cognition: are corticosteroids good or bad guys? Trends in Neurosciences 22: 422426. http://dx.doi.org/10.1016/S0166-2236(99)01438-1CrossRefGoogle ScholarPubMed
Lehane, M 2005 The Biology of Blood-Sucking Insects. Cambridge University Press: Cambridge, UK. http://dx.doi.org/10.1017/CBO9780511610493CrossRefGoogle Scholar
Lent, H and Wygodzinsky, P 1979 Revision of the triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas’ Disease. Bulletin of the American Museum of Natural History 163: 123520Google Scholar
Marco, I and Lavin, S 1999 Effects of the method of capture on the haematology and blood chemistry of red deer (Cervus elaphus). Research in Veterinary Science 66: 8184. http://dx.doi.org/10.1053/rvsc.1998.0248CrossRefGoogle Scholar
Markvardsen, SN, Kjelgaard-Hansen, M, Ritz, C and SØrensen, DB 2012 Less invasive blood sampling in the animal laboratory: clinical chemistry and haematology of blood obtained by the Triatominae bug Dipetalogaster maximus. Laboratory Animals 46: 136141. http://dx.doi.org/10.1258/la.2011.011063CrossRefGoogle ScholarPubMed
Monash University Animal Welfare Committee(MUAWC) 2008 Blood Collection Guidelines. Monash University: Melbourne, VIC, AustraliaGoogle Scholar
Palme, R 2005 Measuring faecal steroids: Guidelines for practical application. Annals of the New York Academy of Sciences 1046: 7580. http://dx.doi.org/10.1196/annals.1343.007CrossRefGoogle ScholarPubMed
Parasuraman, S, Raveendran, R and Kesavan, R 2010 Blood sample collection in small laboratory animals. Journal of Pharmacology & Pharmacotherapeutics 1(2): 8793. http://dx.doi.org/10.4103/0976-500X.72350Google ScholarPubMed
Riley, V 1981 Psychoneuroendocrine influences on immunocompetence and neoplasia. Science 212: 11001109. http://dx.doi.org/10.1126/science.7233204CrossRefGoogle ScholarPubMed
Romero, LM and Reed, JM 2005 Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comparative Biochemistry and Physiology 140: 7379. http://dx.doi.org/10.1016/j.cbpb.2004.11.004Google ScholarPubMed
Romero, LM and Romero, RC 2002 Corticosterone responses in wild birds: the importance of rapid initial sampling. Condor 104: 129135. http://dx.doi.org/10.1650/0010-5422(2002)104[0129:CRIWBT]2.0.CO;2CrossRefGoogle Scholar
Sheriff, MJ, Dantzer, B, Delehanty, B, Palme, R and Boonstra, R 2011 Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166: 869887. http://dx.doi.org/10.1007/s00442-011-1943-yCrossRefGoogle ScholarPubMed
Stefanski, V 1998 Social stress in loser rats: opposite immunological effects in submissive and subdominant males. Physiology & Behaviour 63: 605613. http://dx.doi.org/10.1016/S0031-9384(97)00492-7Google ScholarPubMed
Thomsen, R and Voigt, CC 2006 Non-invasive blood sampling from primates using laboratory-bred blood-sucking bugs (Dipetalogester maximus; Reduviidae, Heteroptera). Primates 47: 397400. http://dx.doi.org/10.1007/s10329-006-0194-8CrossRefGoogle Scholar
Touma, C and Palme, R 2005 Measuring faecal glucocorticoid metabolites in mammals and birds: the importance of validation. Annals of the New York Academy of Sciences 1046: 5474. http://dx.doi.org/10.1196/annals.1343.006CrossRefGoogle ScholarPubMed
Touma, C, Palme, R and Sachser, N 2004 Analyzing corticosterone metabolites in faecal samples of mice: a non-invasive technique to monitor stress hormones. Hormones and Behavior 45: 1022. http://dx.doi.org/10.1016/j.yhbeh.2003.07.002CrossRefGoogle Scholar
Touma, C, Sachser, N, Möstl, E and Palme, R 2003 Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. General and Comparative Endocrinology 130: 267278. http://dx.doi.org/10.1016/S0016-6480(02)00620-2CrossRefGoogle ScholarPubMed
Vahl, TP, Ulrich-Lai, YM, Ostrander, MM, Dolgas, CM, Elfers, EE, Seeley, RJ, D’Alessio, DA and Herman, JP 2005 Comparative analysis of ACTH and corticosterone sampling methods in rats. American Journal of Physiology Endocrinology and Metabolism 289: E823E828. http://dx.doi.org/10.1152/ajpendo.00122.2005CrossRefGoogle ScholarPubMed
Voigt, CC, Faßbender, M, Dehnhard, M, Wibbelt, G, Jewgenow, K, Hofer, H and Schaub, GA 2004 Validation of a minimally invasive blood-sampling technique for the analysis of hormones in domestic rabbits, Oryctolagus cuniculus (Lagomorpha). General and Comparative Endocrinology 135: 100107. http://dx.doi.org/10.1016/j.ygcen.2003.08.005CrossRefGoogle ScholarPubMed
Voigt, CC, Michener, R, Wibbelt, G, Kunz, TH and von Helversen, O 2005 Blood-sucking bugs as a gentle method for blood-collection in water budget studies using doubly labelled water. Comparative Biochemistry and Physiology 142A: 318324CrossRefGoogle Scholar
Voigt, CC, Peschel, U, Wibbelt, G and Frölich, K 2006 An alternative, less invasive blood sample collection technique for serologic studies utilizing Triatomine bugs (Heteroptera; Insecta). Journal of Wildlife Diseases 42: 466469CrossRefGoogle Scholar
Voigt, CC, von Helversen, O, Michener, RH and Kunz, TH 2003 Validation of a non-invasive blood-sampling technique for doubly-labelled water experiments. Journal of Experimental Zoology 296A: 8797. http://dx.doi.org/10.1002/jez.a.10121Google Scholar
von Helversen, O and Reyer, HU 1984 Nectar intake and energy expenditure in a flower-visiting bat. Oecologia 63: 178184. http://dx.doi.org/10.1007/BF00379875CrossRefGoogle Scholar
von Helversen, O, Volleth, M and Núnez, J 1986 A new method for obtaining blood from a small mammal without injuring the animal: use of Triatomid bugs. Experientia 42: 809810. http://dx.doi.org/10.1007/BF01941531Google Scholar
Vos, AC, Mueller, T, Neubert, L and Voigt, CC 2010 Validation of a less invasive blood sampling technique in rabies serology using reduviid bugs (Triatominae, Hemiptera). Journal of Zoo and Wildlife Medicine 41: 6368. http://dx.doi.org/10.1638/2009-0103.1CrossRefGoogle Scholar
Wells, RMG, Tetens, V and Devries, AL 1984 Recovery from stress following capture and anaesthesia of antarctic fish: haematology and blood chemistry. Journal of Fish Biology 25: 567576. http://dx.doi.org/10.1111/j.1095-8649.1984.tb04903.xCrossRefGoogle Scholar