Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-17T18:29:51.889Z Has data issue: false hasContentIssue false
  • English
  • Français

Hair cortisol concentrations, as a measure of chronic activity within the hypothalamic-pituitary-adrenal axis, is elevated in dogs farmed for meat, relative to pet dogs, in South Korea

Published online by Cambridge University Press:  01 January 2023

NB Maxwell ,
CG Buchanan  and
NP Evans
NB Maxwell
Affiliation:
Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, University Avenue, Glasgow G12 8QQ, UK
CG Buchanan
Affiliation:
Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, University Avenue, Glasgow G12 8QQ, UK
NP Evans*
Affiliation:
Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, University Avenue, Glasgow G12 8QQ, UK
*
* Contact for correspondence: Neil.evans@glasgow.ac.uk
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Human consumption of dog meat continues in some countries as a result of tradition, ritual and claimed medical benefits. In South Korea, it is estimated that over 2,500,000 dogs (Canis familiaris) are eaten annually; however, dog farming is unregulated, as dogs are not classified as livestock, leading to animal welfare concerns. A key component of the physiological stress response is activation of the hypothalamic-pituitary-adrenal (HPA) axis. Cortisol released as a consequence of HPA axis activation is stably deposited in growing biological media, such as hair. Extraction and quantification of hair cortisol can provide a historical record of physiological stress experienced as the hair was growing. By comparison of hair cortisol concentrations in samples collected from dogs surrendered from meat farms with pet dogs, this study demonstrates that hair cortisol concentrations from dogs rescued from meat farms are over twice as high as pet dogs living in and close to Seoul. This difference was independent of sex, breed and coat colour. Within the farmed dogs there were no significant effects of farm identity, number of dogs per farm or dogs per cage. Within the Korean Jindos surrendered from meat farms, hair cortisol was significantly higher in white-compared to black-coated dogs but there were no significant differences within or between dogs of other coat colour variants (agouti, brown). These data provide quantitative evidence that dogs in meat farms are kept in conditions associated with poor welfare and identify the need for better welfare laws to protect farmed dogs.

Keywords

animal welfaredogdog meat farmshair cortisolSouth Koreastress
Type
Articles
Information
Animal Welfare , Volume 28 , Issue 4 , November 2019 , pp. 389 - 395
Copyright
© 2019 Universities Federation for Animal Welfare

References

Accorsi, PA, Carloni, E, Valsecchi, P, Viggiania, R, Gamberoni, M, Tamanini, C and Seren, E 2008 Cortisol determination in hair and faeces from domestic cats and dogs. General and Comparative Endocrinology 155: 398–402. https://doi.org/10.1016/j.ygcen.2007.07.002CrossRefGoogle ScholarPubMed
Assia, E, Epstein, Y, Magazanik, A, Shapiro, Y and Sohar, E 1989 Plasma-cortisol levels in experimental heatstroke in dogs. International Journal of Biometeorology 33: 85–88https://doi.org/10.1007/BF01686283CrossRefGoogle ScholarPubMed
Bates, DM 2010 Lme4: Mixed-Effects Modelling with R. Springer: New York USAGoogle Scholar
Bechshøft, TO, Sonne, C, Dietz, R, Born, EW, Novak, MA, Henchey, E and Meyer, JS 2011 Cortisol levels in hair of East Greenland polar bears. Science of the Total Environment 409: 831–834. https://doi.org/10.1016/j.scitotenv.2010.10.047CrossRefGoogle ScholarPubMed
Beerda, B, Schilder, MB, Janssen, NS and Mol, JA 1996 The use of saliva cortisol, urinary cortisol, and catecholamine meas-urements for a non-invasive assessment of stress responses in dogs. Hormones and Behavior 30: 272–279. https://doi.org/10.1006/hbeh.1996.0033CrossRefGoogle Scholar
Beerda, B, Schilder, MBH, van Hooff, JARAM and de Vries, HW 1997 Manifestations of chronic and acute stress in dogs. Applied Animal Behaviour Science 52: 307–319. https://doi.org/10.1016/S0168-1591(96)01131-8CrossRefGoogle Scholar
Bennett, A and Hayssen, V 2010 Measuring cortisol in hair and saliva from dogs: coat color and pigment differences. Domestic Animal Endocrinology 39: 171–180. https://doi.org/10.1016/j.domaniend.2010.04.003CrossRefGoogle ScholarPubMed
Buhler, HU, da Prada, M, Haefely, W and Picotti, GB 1978 Plasma adrendaline, noradrenaline and dopamine in man and dif-ferent animal species. Journal of Physiology 276: 311–320. https://doi.org/10.1113/jphysiol.1978.sp012235CrossRefGoogle Scholar
Burnett, TA, Madureira, AML, Silper, BF, Nadalin, A, Tahmasbi, A, Veira, DM and Cerri, RLA 2014 Short commu-nication: Factors affecting hair cortisol concentrations in lactating dairy cows. Journal of Dairy Science 97: 7685–7690. https://doi.org/10.3168/jds.2014-8444CrossRefGoogle Scholar
Carlsson, AM, Mastromonaco, G, Vandervalk, E and Kutz, S 2016 Parasites, stress and reindeer: infection with abomasal nematodes is not associated with elevated glucocorticoid levels in hair or faeces. Conservation and Physiology 4. https://doi.org/10.1093/conphys/cow058CrossRefGoogle Scholar
Czajkowski, C 2014 Dog meat trade in South Korea: A report on the current state of the trade and efforts to eliminate it. Animal Legislation 21: 30–52Google Scholar
Davenport, MD, Lutz, CK, Tiefenbacher, S, Novak, MA and Meyer, JS 2008 A rhesus monkey model of self-injury: Effects of relocation stress on behavior and neuroendocrine function. Biology Psychiatry 63: 990–996. https://doi.org/10.1016/j.biopsych.2007.10.025CrossRefGoogle ScholarPubMed
Diaz, SF, Torres, SM, Dunstan, RW and Lekcharoensuk, C 2004 An analysis of canine hair re-growth after clipping for a sur-gical procedure. Veterinary Dermatology 15: 25–30. https://doi.org/10.1111/j.1365-3164.2004.00356.xCrossRefGoogle Scholar
Diaz, SF, Torres, SM, Nogueira, SA, Gilbert, S and Jessen, CR 2006 The impact of body site, topical melatonin and brushing on hair regrowth after clipping normal Siberian Husky dogs. Veterinary Dermatology 17: 45–50. https://doi.org/10.1111/j.1365-3164.2005.00497.xCrossRefGoogle ScholarPubMed
Favarato, ES and Conceição, LG 2008 Hair cycle in dogs with different hair types in a tropical region of Brazil. Veterinary Dermatology 19: 15–20Google Scholar
Fraser, DG 2005 Animal welfare and the intensification of animal production: An alternative interpretation. Food and Agriculture Organisation of the UN-FAO: Rome, ItalyGoogle Scholar
Fujiwara, T, Cherrington, AD, Neal, DN and McGuinness, OP 1996 Role of cortisol in the metabolic response to stress hor-mone infusion in the conscious dog. Metabolism 45: 571–578. https://doi.org/10.1016/S0026-0495(96)90026-8CrossRefGoogle Scholar
González-de-la-Vara M del, R, Valdez, RA, Lemus-Ramirez, V, Vázquez-Chagoyán, JC, Villa-Godoy, A and Romano, MC 2011 Effects of adrenocorticotropic hormone challenge and age on hair cortisol concentrations in dairy cattle. Canadian Journal of Veterinary Research 75: 216–221Google ScholarPubMed
Gow, R, Thomson, S, Rieder, M, Van Uum, S and Koren, G 2010 An assessment of cortisol analysis in hair and its clinical applications. Forensic Science International 196: 32 37. https://doi.org/10.1016/j.forsciint.2009.12.040CrossRefGoogle Scholar
Grigg, EK, Nibblett, BM, Robinson, JQ and Smits, JE 2017 Evaluating pair versus solitary housing in kennelled domestic dogs (Canis familiaris) using behaviour and hair cortisol: a pilot study. The Veterinary Record Open 4. https://doi.org/10.1136/vetreco-2016-000193CrossRefGoogle Scholar
Gunaratnam, P and Wilkinson, GT 1983 A study of normal hair growth in the dog, Journal of Small Animal Practice 24: 445–453. https://doi.org/10.1111/j.1748-5827.1983.tb00384.xCrossRefGoogle Scholar
Heimbürge, S, Kanitz, E and Otten, W 2019 The use of hair cortisol for the assessment of stress in animals. General and Comparative Endocrinology 270: 10–17. https://doi.org/10.1016/j.ygcen.2018.09.016CrossRefGoogle ScholarPubMed
Herman, JP, McKlveen, JM, Ghosal, S, Kopp, B, Wulsin, A, Makinson, R, Scheimann, J and Myers, B 2016 Regulation of the hypothalamic-pituitary-adrenocortical stress response. Comprehensive Physiology 6: 603–621. https://doi.org/10.1002/cphy.c150015CrossRefGoogle ScholarPubMed
Hume, DM and Egdahl, RH 1959 Effect of hypothermia and of cold exposure on adrenal cortical and medullary secretion. Annuls New York Academy of Science 80: 435–444. https://doi.org/10.1111/j.1749-6632.1959.tb49221.xCrossRefGoogle ScholarPubMed
Ibraheem, M, Galbraith, H, Scaife, J and Ewen, S 1994 Growth of secondary hair follicles of the Cashmere goat in vitro and their response to prolactin and melatonin. Journal of Anatomy 185: 135–142. https://doi.org/10.1017/S0308229600027628Google ScholarPubMed
Kelly, AM and Vitousek, MN 2017 Dynamic modulation of sociality and aggression: an examination of plasticity within endocrine and neuroendocrine systems. Philosophical Transactions of the Royal Society of London B, Biological Sciences 372: https://doi.org/10.1098/rstb.2016.0243CrossRefGoogle Scholar
Kenagy, GJ and Place, NJ 2000 Seasonal changes in plasma glu-cocorticosteroids of free-living female yellow-pine chipmunks: effects of reproduction and capture and handling. Endocrinology 117: 189–199. https://doi.org/10.1006/gcen.1999.7397Google ScholarPubMed
Kiddie, J and Collins, L 2015 Identifying environmental and man-agement factors that may be associated with the quality of life of kennelled dogs (Canis familiaris). Applied Animal Behaviour Science 167: 43–55. https://doi.org/10.1016/j.applanim.2015.03.007CrossRefGoogle Scholar
Kim, RE 2008 Dog meat in Korea: A socio-legal challenge. Animal Law Review 14. https://doi.org/10.2139/ssrn.1325574CrossRefGoogle Scholar
Kim, TK, Jo, MH, Park, MN, Jo, EJ, Nam, TS, Son, SK and Heo, JH 2009 Prevalence of heartworm infection among dogs on breeding farms in southern Gyeongnam area. Korean Journal of Veterinary Services 32: 369–375Google Scholar
Knowles, TG, Warriss, PD, Brown, SN and Edwards, JE 1988 Effects of stocking density on lambs being transported by road. The Veterinary Record 142: 503–509. https://doi.org/10.1136/vr.142.19.503CrossRefGoogle Scholar
Kremenak, CR 1969 Dental eruption chronology in dogs: decid-uous tooth gingival emergence. Journal of Dental Research 48:1177–1184. https://doi.org/10.1177/00220345690480061501CrossRefGoogle ScholarPubMed
Kuhn, G, Lichtwald, K, Hardegg, W and Abel, HH 1991 The effect of transportation stress on circulating corticosteroids, enzyme activities and haematological values in laboratory dogs. Journal of Experimental Animal Science 34: 99–104Google ScholarPubMed
LeMay, L, Vander, AJ and Kluger, M 1990 The effects of psy-chological stress on plasma interleukin-6 activity in rats. Physiology and Behaviour 47: 957–961. https://doi.org/10.1016/0031-9384(90)90024-XCrossRefGoogle Scholar
Livestock Products Sanitary Control Act (Republic of South Korea) 2010 Source: Statutes of the Republic of Korea. http://elaw.klri.re.kr/eng_service/main.doGoogle Scholar
Mack, Z and Fokidis, HB 2017 A novel method for assessing chronic cortisol concentrations in dogs using the nail as a source. Domestic Animal Endocrinology 59: 53–57. https://doi.org/10.1016/j.domaniend.2016.11.003CrossRefGoogle ScholarPubMed
Mahut, H 1958 Breed differences in the dog's emotional behav-iour. Canadian Journal of Psychology 12: 35–44. https://doi.org/10.1037/h0083722CrossRefGoogle Scholar
Mastromonaco, GF, Gunn, K, McCurdy-Adams, H, Edwards, DB and Schulte-Hostedde, AI 2014 Validation and use of hair cortisol as a measure of chronic stress in eastern chip-munks (Tamias striatus). Conservation Physiology 2: https://doi.org/10.1093/conphys/cou055CrossRefGoogle Scholar
McCurley, JL, Mills, PJ, Roesch, SC, Carnethon, M, Giacinto, RE, Isasi, CR and Gallo, LC 2015 Chronic stress, inflammation, and glucose regulation in US Hispanics from the HCHS/SOL soci-ocultural ancillary study. Psychophysiology 52: 1071–1079. https://doi.org/10.1111/psyp.12430CrossRefGoogle ScholarPubMed
Mesarcova, L, Kottferova, J, Skurkova, L, Leskova, L and Kmecova, N 2017 Analysis of cortisol in dog hair – a potential biomarker of chronic stress: a review. Veterinarni Medicina 62:363–376. https://doi.org/10.17221/19/2017-VETMEDCrossRefGoogle Scholar
Nejad, G, Kim, BW, Lee, BH and Sung, KI 2017 Coat and hair color: hair cortisol and serotonin levels in lactating Holstein cows under heat stress conditions. Journal of Animal Science 88: 190–194. https://doi.org/10.1111/asj.12662CrossRefGoogle Scholar
Öhlin, B, Nilsson, PM, Nilsson, J-Å and Berglund, G 2004 Chronic psychosocial stress predicts long-term cardiovascular morbidity and mortality in middle-aged men. European Heart Journal 25: 867–873. https://doi.org/10.1016/j.ehj.2004.03.003CrossRefGoogle ScholarPubMed
Palazzolo, DL and Quadri, SK 1987 Plasma thyroxine and cor-tisol under basal conditions and during cold stress in the aging dog. Proceedings of the Society for Experimental Biology and Medicine 185: 305–311. https://doi.org/10.3181/00379727-185-42549CrossRefGoogle ScholarPubMed
Papafotiou, C, Christaki, E, van den Akker, EL, Wester, VL, Apostolakou, F, Papassotiriou, I and Pervanidou, P 2017 Hair cortisol concentrations exhibit a positive association with salivary cortisol profiles and are increased in obese prepubertal girls. Stress 20: 217–222. https://doi.org/10.1080/10253890.2017.1303830CrossRefGoogle ScholarPubMed
Pickering, T 2007 Stress inflammation and hypertension. Journal of Clinical Hypertension 9: 567–571. https://doi.org/10.1111/j.1524-6175.2007.06301.xCrossRefGoogle ScholarPubMed
Podberscek, AL 2007 Encyclopedia of Human-Animal Relationships: A Global Exploration of our Connections with Animals pp 24–34. Greenwood Press: Westport, CT, USAGoogle Scholar
Podberscek, AL 2009 Good to pet and eat: The keeping and consuming of dogs in South Korea. Journal of Social Issues 65: 615–632. https://doi.org/10.1111/j.1540-4560.2009.01616.xCrossRefGoogle Scholar
Protopopova, A 2016 Effects of sheltering on physiology, immune function, behavior, and the welfare of dogs. Journal of Physiology and Behavior 15: 95–103. https://doi.org/10.1016/j.phys-beh.2016.03.020CrossRefGoogle Scholar
Radosevich, PM, Nash, JA, Brooks, D, Lacy, C, O’Donovan, PE, Williams, and Abumrad, NN 1989 Effects of low- and high-intensity exercise on plasma and cerebrospinal fluid levels of ir-β-endorphin, ACTH, cortisol, norepinephrine and glucose in the conscious dog. Brain Research 498: 89–98. https://doi.org/10.1016/0006-8993(89)90402-2CrossRefGoogle ScholarPubMed
Reimers, TJ, Lawler, DF, Sutaria, PM, Correa, MT and Erb, HN 1990 Effects of age, sex, and body size on serum concentrations of thyroid and adrenocortical hormones in dogs. American Journal Veterinary Research 51: 454–457Google ScholarPubMed
Romero, LM, Meister, CJ, Cyr, NE, Kenagy, GJ and Wingfield, JC 2008 Seasonal glucocorticoid responses to capture in wild free-living mammals. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 294: 614–622. https://doi.org/10.1152/ajpregu.00752.2007CrossRefGoogle ScholarPubMed
Sandri, M, Colussi, A, Perrotta, MG and Stefanon, B 2015 Salivary cortisol concentration in healthy dogs is affected by size, sex, and housing context. Journal of Veterinary Behaviour 10: 302–306. https://doi.org/10.1016/j.jveb.2015.03.011CrossRefGoogle Scholar
Schipper, LL, Vinke, CM, Schilder, MBH and Spruijt, BM 2008 The effect of feeding enrichment toys on the behaviour of kennelled dogs (Canis familiaris). Applied Animal Behaviour Science 114: 182–195. https://doi.org/10.1016/j.applanim.2008.01.001CrossRefGoogle Scholar
Schubert, C, Lambertz, M, Nelesen, RA, Bardwell, W, Choi, JB and Dimsdale, JE 2009 Effects of stress on heart rate com-plexity: A comparison between short-term and chronic stress. Biological Psychology. 80: 325–332. https://doi.org/10.1016/j.biopsy-cho.2008.11.005CrossRefGoogle Scholar
Slater, JDH, Barbour, BH, Henderson, HH, Casper, AGT and Bartter, FC 1963 Influence of the pituitary and the renin-angiotensin system on the secretion of aldosterone, cortisol and corticosterone. Journal of Clinical Investigation 42: 1504–1520. https://doi.org/10.1172/JCI104835CrossRefGoogle ScholarPubMed
Storengen, LM and Lingaas, F 2015 Noise sensitivity in 17 dog breeds: Prevalence, breed risk and correlation with fear in other situations. Applied Animal Behaviour Science 171: 152–160. https://doi.org/10.1016/j.applanim.2015.08.020CrossRefGoogle Scholar
Stubsjøen, SM, Bohlin, J, Dahl, E, Knappe-Poindecker, M, Fjeldaas, T, Lepschy, M, Palme, R, Langbein, J and Ropstad, E 2015 Assessment of chronic stress in sheep (part I): The use of cortisol and cortisone in hair as non-invasive biological markers. Small Ruminant Research 132: 25–31. https://doi.org/10.1016/j.smallrumres.2015.09.015CrossRefGoogle Scholar
Tallo-Parra, O, Lopez-Bejar, M, Carbajal, A, Monclús, L, Manteca, X and Devant, M 2017 Acute ACTH-induced elevations of circulating cortisol do not affect hair cortisol concentrations in calves. General Comparative Endocrinology 240: 138–142. https://doi.org/10.1016/j.ygcen.2016.10.007CrossRefGoogle Scholar
Tarrant, PV, Kenny, FJ, Harrington, D and Murphy, M 1992 Long distance transportation of steers to slaughter: effect of stocking density on physiology, behaviour and carcass quality. Livestock Production Science 30: 223–238. https://doi.org/10.1016/S0301-6226(06)80012-6CrossRefGoogle Scholar
Welle, MM and Wiener, DJ 2016 The hair follicle: A comparative review of canine hair follicle anatomy and physiology. Toxicologic Pathology 44: 564–574. https://doi.org/10.1177/0192623316631843CrossRefGoogle ScholarPubMed
Wosu, AC, Valdimarsdóttir, U, Shields, AE, Williams, DR and Williams, MA 2013 Correlates of cortisol in human hair: Implications for epidemiologic studies on health effects of chron-ic stress. Annals of Epidemiology 23: 797–811. https://doi.org/10.1016/j.annepidem.2013.09.006CrossRefGoogle Scholar
Yamanashi, Y, Morimura, N, Mori, Y, Hayashi, M and Suzuki, J 2013 Cortisol analysis of hair of captive chimpanzees (Pan troglodyes). General and Comparative Endocrinology 194: 55–63. https://doi.org/10.1016/j.ygcen.2013.08.013CrossRefGoogle Scholar
Yelland, T and Whelan, F 2011 An introduction to handling aggressive patients. The Veterinary Nurse 2: 568–576. https://doi.org/10.12968/vetn.2011.2.10.568CrossRefGoogle Scholar