Manual versus automated blood sampling: Impact of repeated blood sampling on stress parameters and behavior in male NMRI mice

Laboratory Animals

Volumn 48, Issue 4, 2014, Pages 278-291

  Teilmann, A Charlotte ^a   Kalliokoski, Otto ^a   Sørensen, Dorte B ^a   Hau, Jann ^a   Abelson, Klas S P ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Anxiety; Catheterization; Corticosterone; Reduction; Refinement

Indexed keywords

CORTICOSTERONE; GLUCOCORTICOID;

ANIMAL EXPERIMENT; ARTICLE; AUTOMATED BLOOD SAMPLING; BEHAVIOR; BLOOD SAMPLING; BODY WEIGHT; CAROTID ARTERY; CHEEK; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DYNAMICS; FACIAL VEIN PHLEBOTOMY; INTERMETHOD COMPARISON; INVESTIGATIVE PROCEDURES; MALE; MANUAL BLOOD SAMPLING; MOUSE; NONHUMAN; PHLEBOTOMY; STRESS; TAIL VEIN PHLEBOTOMY; ANIMAL; ANXIETY; BLOOD; CHEMISTRY; COMPARATIVE STUDY; FECES; METABOLISM; PHYSIOLOGICAL STRESS; PROCEDURES; TAIL;

MUS;

ANIMALS; ANXIETY; BODY WEIGHT; CHEEK; CORTICOSTERONE; FECES; MALE; MICE; PHLEBOTOMY; STRESS, PHYSIOLOGICAL; TAIL;

EID: 84913528139     PISSN: 00236772     EISSN: 17581117     Source Type: Journal    
DOI: 10.1177/0023677214541438     Document Type: Article

References (64)

1. Commision of the European Communities. Report from the commission to the council and the European Parliament: Sixth report on the statistics on the number of animal used for experimental and other scientific purposes in the member states of the European Union SEC (2012) 1107. Brussels: The European Commision, 2010.
2. Diehl KH, Hull R, Morton D, et al. A good practice guide to the administration of substances and removal of blood, including routes and volumes. J Appl Toxicol 2001; 21: 15–23.
3. van Herck H, Baumans V, Brandt CJWM, et al. Orbital sinus blood sampling in rats as performed by different animal technicians: the influence of technique and expertise. Lab Anim 1998; 32: 377–386.
4. Aynsley-Green A, Bicbuyck JF and Alberti KGMM. Anaesthesia and insulin secretion: the effects of diethyl ether, halothane, pentobarbitone sodium and ketamine hydrochloride on intravenous glucose tolerance and insulin secretion in the rat. Diabetologia 1973; 9: 274–281.
5. Umeda T and Inaba T. Effects of anesthetics on diphenylhydantoin metabolism in the rat: possible inhibition by diethyl ether. Can J Physiol Pharmacol 1977; 56: 241–244.
6. Forbes N, Brayton C, Grindle S, Shepherd S, Tyler B and Guarnieri M. Morbidity and mortality rates associated with serial bleeding from the superficial temporal vein in mice. Lab Anim (NY) 2010; 39: 236–240.
7. Abatan OI, Welch KB and Nemzek JA. Evaluation of saphenous venipuncture and modified tail-clip blood collection in mice. J Am Assoc Lab Anim Sci 2008; 47: 8–15.
8. Sorensen DB, Stub C, Jensen HE, et al. The impact of tail tip amputation and ink tattoo on C57BL/6JBomTac mice. Lab Anim 2007; 41: 19–29.
9. Fluttert M, Dalm S and Oitzl MS. A refined method for sequential blood sampling by tail incision in rats. Lab Anim 2000; 34: 372–378.
10. Sadler AM and Bailey SJ. Validation of a refined technique for taking repeated blood samples from juvenile and adult mice. Lab Anim 2013; 47: 316–319.
11. Balcombe JP, Barnard ND and Sandusky C. Laboratory routines cause animal stress. Contemp Top Lab Anim Sci 2004; 43: 42–51.
12. Tasker JG. Rapid glucocorticoid actions in the hypothalamus as a mechanism of homeostatic integration. Obesity 2006; 14: 259–265.
13. Tsigos C and Chrousos GP. Hypothalamic–pituitary–adrenal axis, neuroendocrine factors and stress. J Psychosom Res 2002; 53: 865–871.
14. Barr JE, Holmes DB, Ryan LJ and Sharpless SK. Techniques for the chronic cannulation of the jugular vein in mice. Pharmacol Biochem Behav 1979; 11: 115–118.
15. Bardelmeijer HA, Buckle T, Ouwehand M, Beijnen JH, Schellens JHM and Tellingen Ov. Cannulation of the jugular vein in mice: a method for serial withdrawal of blood samples. Lab Anim 2002; 37: 181–187.
16. Chistyakov VS and Tsibulsky VL. How to achieve chronic intravenous drug self-administration in mice. J Pharmacol Toxicol Methods 2006; 53: 117–127.
17. Sundbom R, Jacobsen KR, Kalliokoski O, Hau J and Abelson KSP. Postoperative corticosterone levels in plasma and feces of mice subjected to permanent catheterization and automated blood sampling. In Vivo 2011; 25: 335–342.
18. Teilmann AC, Jacobsen KR, Kalliokoski A, Hansen AK, Hau J and Abelson KSP. The effect of automated blood sampling on corticosterone levels, body weight and daily food intake in permanently catheterized male BALB/c mice. In Vivo 2012; 26: 577–582.
19. Abelson KSP, Adem B, Royo F, Carlsson HE and Hau J. High plasma corticosterone levels persist during frequent automatic blood sampling in rats. In Vivo 2005; 19: 815–819.
20. Siswanto H, Hau J, Carlsson HE, Goldkuhl R and Abelson KSP. Corticosterone concentrations in blood and excretion in faeces after ACTH administration in male Sprague-Dawley rats. In Vivo 2008; 22: 435–440.
21. Committee for the update of the Guide for the Care and Use of Laboratory Animals. Guide for the care and use of laboratory animals. Washington DC: National Academies Press, 2011, Report No. 8.
22. Beynen AC, Festing MFW and van Montfort MAJ. Design of animal experiments. In: Van Zutphen LFM, Baumans V and Beynen AC (eds) Principles of laboratory animal science, 2nd ed. Amsterdam: Elsevier, 2001, pp.219–249.
23. Hurst JL and West RS. Taming anxiety in laboratory mice. Nat Methods 2010; 7: 825–U1516.
24. Flecknell PA, Roughan JV and Stewart R. Use of oral buprenorphine (‘buprenorphine jello’) for postoperative analgesia in rats – a clinical trial. Lab Anim 1999; 33: 169–174.
25. Roughan JV and Flecknell PA. Buprenorphine: a reappraisal of its antinociceptive effects and therapeutic use in alleviating postoperative pain in animals. Lab Anim 2002; 36: 322–343.
26. Jacobsen KR, Kalliokoski O, Hau J and Abelson KSP. Voluntary ingestion of buprenorphine in mice. Anim Welfare 2011; 20: 591–596.
27. Kalliokoski O, Jacobsen KR, Hau J and Abelson KSP. Serum concentration of buprenorphine after oral and parenteral administration in male mice. Vet J 2009; 187: 251–254.
28. Abelson KSP, Jacobsen KR, Sundbom R, Kalliokoski O and Hau J. Voluntary ingestion of nut paste for administration of buprenorphine in rats and mice. Lab Anim 2012; 46: 349–351.
29. Bendtsen KMB, Krych L, Sørensen DB, et al. Gut microbiota composition is correlated to grid floor induced stress and behavior in the BALB/c mouse. PLoS One 2012; 7: 1–13.
30. Ottoni EB. EthoLog 2.2: a tool for the transcription and timing of behavior observation sessions. Behav Res Methods Instrum Comput 2000; 32: 446–449.
31. Holmberg A and Pelletier R. Automated blood sampling and the 3Rs. The National Centre for the Replacement Refinement and Reduction of Animals in Research. http://www.nc3rs.org.uk/news.asp?id¼1039 (2009, accessed 16 June 2014).
32. Macloed JN and Shapiro BH. Repetitive blood sampling in unrestrained and unstressed mice using a chronic indwelling right atrial catheterization apparatus. Lab Anim Sci 1988; 38: 603–608.
33. Royo F, Bjork N, Carlsson W, Mayo S and Hau J. Impact of chronic catheterization and automated blood sampling (Accusampler) on serum corticosterone and fecal immunoreactive corticosterone metabolites and immunoglobulin A in male rats. J Endocrinol 2004; 180: 145–153.
34. Dürschlag M, Wurbel H, Stauffacher M and Von Holst D. Repeated blood collection in the laboratory mouse by tail incision – modification of an old technique. Physiol Behav 1996; 60: 1565–1568.
35. Hui Y, Huang NH, Ebbert L, et al. Pharmacokinetic comparisons of tail-bleeding with cannula- or retro-orbital bleeding techniques in rats using six marketed drugs. J Pharmacol Toxicol Methods 2007; 56: 256–264.
36. Grouzmann E, Cavadas C, Grand D, et al. Blood sampling methodology is crucial for precise measurement of plasma catecholamines concentrations in mice. Pflugers Arch 2003; 447: 254–258.
37. McGuill MW and Rowan AN. Biological effects of blood loss: implications for sampling volume and techniques. ILAR News 1989; 31: 5–20.
38. Desborough JP. The stress response to trauma and surgery. Br J Anaesth 2000; 85: 109–117.
39. Jacobsen KR, Kalliokoski O, Teilmann AC, Hau J and Abelson KSP. Postsurgical food and water consumption, fecal corticosterone metabolites, and behavior assessment as noninvasive measures of pain in vasectomized BALB/c mice. J Am Assoc Lab Anim Sci 2012; 51: 69–75.
40. Blaha MD and Leon LR. Effects of indomethacin and buprenorphine analgesia on the postoperative recovery of mice. J Amer Assoc Lab Anim Sci 2008; 47: 8–19.
41. The European Parliament and the Council. Directive 2010/63/EU on the protection of animals used for scientific purposes. Official J EU 2010; 276: 33–79.
42. Kohn DF, Martin TE, Foley PL, et al. Guidelines for the assessment and management of pain in rodents and rabbits. J Am Assoc Lab Anim Sci 2007; 46: 97–108.
43. Goldkuhl R, Carlsson HE, Hau J and Abelson KSP. Effect of subcutaneous injection and oral voluntary ingestion of buprenorphine on postoperative serum corticosterone levels in male rats. Eur Surgi Res 2008; 41: 272–278.
44. Goldkuhl R, Hau J and Abelson KSP. Effects of voluntarily-ingested buprenorphine on plasma corticosterone levels, body weight, water intake, and behaviour in permanently catheterised rats. In Vivo 2010; 24: 131–135.
45. de Kloet ER, Karst H and Joe¨ ls M. Corticosteroid hormones in the central stress response: quick-and-slow. Front Neuroendocrinol 2007; 29: 268–72.
46. Spackman DH and Riley V. Corticosterone concentrations in mouse. Science 1978; 200: 87.
47. Kannan Y. The handbook of experimental animals. The laboratory mouse, 1st ed. Amsterdam: Elsevier Academic Press, 2004.
48. Touma C, Palme R and Sachser N. Analyzing corticosterone metabolites in fecal samples of mice: a noninvasive technique to monitor stress hormones. Horm Behav 2004; 45: 10–22.
49. Thanos PK, Cavigelli SA, Michaelides M, et al. A noninvasive method for detecting the metabolic stress response in rodents: characterization and disruption of the circadian corticosterone rhythm. Physiological Res 2009; 58: 219–228.
50. Kalliokoski O, Hau J, Jacobsen KR, Schumacher- Petersen C and Abelson KSP. Distribution and time course of corticosterone excretion in faeces and urine of female mice with varying systemic concentrations. Gen Comp Endocrinol 2010; 168: 450–454.
51. Barriga C, Martin MI, Tabla R, Ortega E and Rodriguez AB. Circadian rhythm of melatonin, corticosterone and phagocytosis: effect of stress. J Pineal Res 2001; 30: 180–187.
52. Kalliokoski O, Jacobsen KR, Teilmann AC, Hau J and Abelson KSP. Quantitative effects of diet on fecal corticosterone metabolites in two strains of laboratory mice. In Vivo 2012; 26: 213–221.
53. Goymann W. On the use of non-invasive hormone research in uncontrolled, natural environments: the problem with sex, diet, metabolic rate and the individual. Methods Ecol Evol 2012; 3: 757–765.
54. Pihl L and Hau J. Faecal corticosterone and immunoglobulin A in young adult rats. Lab Anim 2003; 37: 166–171.
55. Archer J. Tests for emotionality in rats and mice – review. Anim Behav 1973; 21: 205–235.
56. Crabbe JC, Wahlsten D and Dudek BC. Genetics of mouse behavior: interactions with laboratory environment. Science 1999; 284: 1670–1672.
57. Holmes A, Yang RJ, Lesch KP, Crawley JN and Murphy DL. Mice lacking the serotonin transporter exhibit 5-HT1A receptor-mediated abnormalities in tests for anxiety-like behavior. Neuropsychopharmacology 2003; 28: 2077–2088.
58. Trullas R and Skolnick P. Differences in Fear motivated behaviors among inbred mouse strains. Psychopharmacology 1993; 111: 323–331.
59. Fraser LM, Brown RE, Hussin A, et al. Measuring anxiety-and locomotion-related behaviours in mice: a new way of using old tests. Psychopharmacology 2010; 211: 99–112.
60. Ramos A, Pereira E, Martins GC, Wehrmeister TD and Izidio GS. Integrating the open field, elevated plus maze and light/dark box to assess different types of emotional behaviors in one single trial. Behav Brain Res 2008; 193: 277–288.
61. Bertoglio LJ and Carobrez AP. Previous maze experience required to increase open arms avoidance in rats submitted to the elevated plus-maze model of anxiety. Behav Brain Res 2000; 108: 197–203.
62. Ramos A. Animal models of anxiety: do I need multiple tests? Trends Pharmacol Sci 2008; 29: 493–498.
63. Popesko P, Rajtová V and Horák J. A colour atlas of anatomy of small laboratory animals, 1st ed. London: Wolfe Publishing Ltd, 1990.
64. Russell WMS and Burch RL. The principles of humane experimental technique. Available at: http://altweb.jhsph.edu/pubs/books/humane_exp/addendum. London, Methuen, 1959.