Finding biomarkers of experience in animals.

Animal experience Animal welfare Biomarker Stress Welfare assessment

Journal

Journal of animal science and biotechnology
ISSN: 1674-9782
Titre abrégé: J Anim Sci Biotechnol
Pays: England
ID NLM: 101581293

Informations de publication

Date de publication:
20 Feb 2024
Historique:
received: 07 09 2023
accepted: 28 12 2023
medline: 20 2 2024
pubmed: 20 2 2024
entrez: 19 2 2024
Statut: epublish

Résumé

At a time when there is a growing public interest in animal welfare, it is critical to have objective means to assess the way that an animal experiences a situation. Objectivity is critical to ensure appropriate animal welfare outcomes. Existing behavioural, physiological, and neurobiological indicators that are used to assess animal welfare can verify the absence of extremely negative outcomes. But welfare is more than an absence of negative outcomes and an appropriate indicator should reflect the full spectrum of experience of an animal, from negative to positive. In this review, we draw from the knowledge of human biomedical science to propose a list of candidate biological markers (biomarkers) that should reflect the experiential state of non-human animals. The proposed biomarkers can be classified on their main function as endocrine, oxidative stress, non-coding molecular, and thermobiological markers. We also discuss practical challenges that must be addressed before any of these biomarkers can become useful to assess the experience of an animal in real-life.

Identifiants

pubmed: 38374201
doi: 10.1186/s40104-023-00989-z
pii: 10.1186/s40104-023-00989-z
doi:

Types de publication

Journal Article Review

Langues

eng

Pagination

28

Subventions

Organisme : Meat and Livestock Australia
ID : P.PSH.1232
Organisme : Australasian Pork Research Institute
ID : 5A-113

Informations de copyright

© 2024. The Author(s).

Références

Duncan IJH. Animal welfare: a brief history. In: Hild S, Schweitzer L, editors. Animal Welfare: from Science to Law. La Fondation Droit Animal: Éthique et Sciences. Paris; 2019. p. 13–9.
Cornish A, Wilson B, Raubenheimer D, McGreevy P. Demographics regarding belief in non-human animal sentience and emotional empathy with animals: a pilot study among attendees of an animal welfare symposium. Animals. 2018;8:174.
pubmed: 30287771 pmcid: 6210928 doi: 10.3390/ani8100174
Fraser D. The globalisation of farm animal welfare. Rev Sci Tech. 2014;33:33–8.
pubmed: 25000775 doi: 10.20506/rst.33.1.2267
Appleby M, Olsson I, Galindo F. Animal welfare. 3rd ed. Wallingford: CAB International; 2018.
doi: 10.1079/9781786390202.0000
Whittaker A, Marsh LE. The role of behavioural assessment in determining positive affective states. CAB Reviews. 2019;14:1–13.
doi: 10.1079/PAVSNNR201914010
Hemsworth PH, Mellor DJ, Cronin GM, Tilbrook AJ. Scientific assessment of animal welfare. New Zeal Vet J. 2015;63:24–30.
pubmed: 25263963 doi: 10.1080/00480169.2014.966167
Crump A, Arnott G, Bethell EJ. Affect-driven attention biases as animal welfare indicators: review and methods. Animals. 2018;8:136.
pubmed: 30087230 pmcid: 6115853 doi: 10.3390/ani8080136
Lawrence AB, Vigors B, Sandøe P. What is so positive about positive animal welfare?—a critical review of the literature. Animals. 2019;9:783.
pubmed: 31614498 pmcid: 6826906 doi: 10.3390/ani9100783
Mellor DJ. Positive animal welfare states and reference standards for welfare assessment. New Zeal Vet J. 2015;63:17–23.
pubmed: 24875152 doi: 10.1080/00480169.2014.926802
Radkowska I, Godyń D, Fic K. Stereotypic behaviour in cattle, pigs and horses-a review. Anim Sci Pap Rep. 2020;38:303–19.
Ridge EE, Foster MJ, Daigle CL. Effect of diet on non-nutritive oral behavior performance in cattle: a systematic review. Livest Sci. 2020;238:104063.
doi: 10.1016/j.livsci.2020.104063
Cronin GM, Glatz PC. Causes of feather pecking and subsequent welfare issues for the laying hen: a review. Anim Prod Sci. 2020;61:990–1005.
doi: 10.1071/AN19628
Dalton HA, Wood BJ, Torrey S. Injurious pecking in domestic turkeys: development, causes, and potential solutions. Worlds Poult Sci J. 2013;69:865–76.
doi: 10.1017/S004393391300086X
Sonoda L, Fels M, Oczak M, Vranken E, Ismayilova G, Guarino M, et al. Tail biting in pigs. Berl Munch Tierarztl Wochenschr. 2013;126:104–12.
pubmed: 23540192
Henry M, Jansen H, Amezcua M del R, O’sullivan TL, Niel L, Shoveller AK, et al. Tail-biting in pigs: a scoping review. Animals. 2021;11:2002.
Nicol CJ. Environmental choices of farm animals. BSAP Occasional Publication. 1997;20:35–43.
doi: 10.1017/S0263967X00043354
Miller LJ, Vicino GA, Sheftel J, Lauderdale LK. Behavioral diversity as a potential indicator of positive animal welfare. Animals. 2020;10(7):1211.
doi: 10.3390/ani10071211
Ahloy-Dallaire J, Espinosa J, Mason G. Play and optimal welfare: does play indicate the presence of positive affective states? Behav Process. 2018;156:3–15.
doi: 10.1016/j.beproc.2017.11.011
Held SDE, Špinka M. Animal play and animal welfare. Anim Behav. 2011;81:891–9.
doi: 10.1016/j.anbehav.2011.01.007
Daigle CL, Hubbard AJ, Grandin T. The use of traditional fear tests to evaluate different emotional circuits in cattle. J Vis Exp. 2020;158:e60641.
Forkman B, Boissy A, Meunier-Salaün MC, Canali E, Jones RB. A critical review of fear tests used on cattle, pigs, sheep, poultry and horses. Physiol Behav. 2007;92:340–74.
pubmed: 18046784 doi: 10.1016/j.physbeh.2007.03.016
Clegg ILK, Delfour F. Cognitive judgement bias is associated with frequency of anticipatory behavior in bottlenose dolphins. Zoo Biol. 2018;37:67–73.
pubmed: 29385270 doi: 10.1002/zoo.21400
Stamp Dawkins M. The science of animal welfare. Understanding what animals want. Oxford: Oxford University Press; 2021.
doi: 10.1093/oso/9780198848981.001.0001
Mattiello S, Battini M, de Rosa G, Napolitano F, Dwyer C. How can we assess positive welfare in ruminants? Animals. 2019;9:758.
pubmed: 31581658 pmcid: 6826499 doi: 10.3390/ani9100758
Roelofs S, Boleij H, Nordquist RE, van der Staay FJ. Making decisions under ambiguity: judgment bias tasks for assessing emotional state in animals. Front Behav Neurosci. 2016;10:119.
pubmed: 27375454 pmcid: 4899464 doi: 10.3389/fnbeh.2016.00119
Mendl M, Burman OHP, Parker RMA, Paul ES. Cognitive bias as an indicator of animal emotion and welfare: emerging evidence and underlying mechanisms. Appl Anim Behav Sci. 2009;118:161–81.
doi: 10.1016/j.applanim.2009.02.023
Baciadonna L, Mcelligott AG. The use of judgement bias to assess welfare in farm livestock. Anim Welf. 2015;24:81–91.
doi: 10.7120/09627286.24.1.081
Bethell EJ. A “how-to” guide for designing judgment bias studies to assess captive animal welfare. J Appl Anim Welf Sci. 2015;18:S18–42.
pubmed: 26440495 doi: 10.1080/10888705.2015.1075833
Ferguson D, Colditz I, Collins T, Matthews L, Hemsworth P. Assessing the welfare of farm animals-a review. Progress Report - APL Project No 2011/1036.421. Canberra: Australian Pork Limited; 2012.
Fleming PA, Clarke T, Wickham SL, Stockman CA, Barnes AL, Collins T, et al. The contribution of Qualitative Behavioural Assessment to appraisal of livestock welfare. Anim Prod Sci. 2016;56:1569–78.
doi: 10.1071/AN15101
Rose P, Riley L. The use of Qualitative Behavioural Assessment to zoo welfare measurement and animal husbandry change. J Zoo Aquar Res. 2019;7:150–61.
Patel F, Wemelsfelder F, Ward SJ. Using Qualitative Behaviour Assessment to investigate human-animal relationships in zoo-housed giraffes (Giraffa camelopardalis). Animals. 2019;9:381.
pubmed: 31234320 pmcid: 6616931 doi: 10.3390/ani9060381
Yon L, Williams E, Harvey ND, Asher L. Development of a behavioural welfare assessment tool for routine use with captive elephants. PLoS ONE. 2019;14:e0210783.
pubmed: 30726232 pmcid: 6364905 doi: 10.1371/journal.pone.0210783
Travnik IC, Sant’Anna AC. Do you see the same cat that I see? relationships between Qualitative Behaviour Assessment and indicators traditionally used to assess temperament in domestic cats. Anim Welf. 2021;30:211–23.
doi: 10.7120/09627286.30.2.211
Stubsjøen SM, Moe RO, Bruland K, Lien T, Muri K. Reliability of observer ratings: Qualitative Behaviour Assessments of shelter dogs using a fixed list of descriptors. Vet Anim Sci. 2020;10:100145.
pubmed: 33204895 pmcid: 7648176 doi: 10.1016/j.vas.2020.100145
Walker JK, Dale AR, D’Eath RB, Wemelsfelder F. Qualitative Behaviour Assessment of dogs in the shelter and home environment and relationship with quantitative behaviour assessment and physiological responses. Appl Anim Behav Sci. 2016;184:97–108.
doi: 10.1016/j.applanim.2016.08.012
Diaz-Lundahl S, Hellestveit S, Stubsjøen SM, Phythian CJ, Moe RO, Muri K. Intra- and inter-observer reliability of Qualitative Behaviour Assessments of housed sheep in Norway. Animals. 2019;9:569.
pubmed: 31426493 pmcid: 6719082 doi: 10.3390/ani9080569
Brscic M, Otten ND, Contiero B, Kirchner MK. Investigation of a standardized Qualitative Behaviour Assessment and exploration of potential influencing factors on the emotional state of dairy calves. Animals. 2019;9:757.
pubmed: 31581609 pmcid: 6826544 doi: 10.3390/ani9100757
Muri K, Stubsjøen SM, Vasdal G, Moe RO, Granquist EG. Associations between qualitative behaviour assessments and measures of leg health, fear and mortality in Norwegian broiler chicken flocks. Appl Anim Behav Sci. 2019;211:47–53.
doi: 10.1016/j.applanim.2018.12.010
Minero M, Dalla Costa E, Dai F, Canali E, Barbieri S, Zanella A, et al. Using qualitative behaviour assessment (QBA) to explore the emotional state of horses and its association with human-animal relationship. Appl Anim Behav Sci. 2018;204:53–9.
doi: 10.1016/j.applanim.2018.04.008
Descovich KA, Wathan J, Leach MC, Buchanan-Smith HM, Flecknell P, Farningham D, et al. Facial expression: an under-utilised tool for the assessment of welfare in mammals. Altex. 2017;34:409–29.
pubmed: 28214916
Lu Y, Mahmoud M, Robinson P. Estimating sheep pain level using facial action unit detection. In: Proceedings - 12th IEEE International Conference on Automatic Face and Gesture Recognition. Washington: Institute of Electrical and Electronics Engineers Inc; 2017. p. 394–9.
Proctor HS, Carder G. Looking into the eyes of a cow: Can eye whites be used as a measure of emotional state? Appl Anim Behav Sci. 2017;186:1–6.
doi: 10.1016/j.applanim.2016.11.005
Reefmann N, Bütikofer Kaszàs F, Wechsler B, Gygax L. Ear and tail postures as indicators of emotional valence in sheep. Appl Anim Behav Sci. 2009;118:199–207.
doi: 10.1016/j.applanim.2009.02.013
Laurijs KA, Briefer EF, Reimert I, Webb LE. Vocalisations in farm animals: a step towards positive welfare assessment. Appl Anim Behav Sci. 2021;236:105264.
doi: 10.1016/j.applanim.2021.105264
Adelman JS, Estes Z, Cossu M. Emotional sound symbolism: languages rapidly signal valence via phonemes. Cognition. 2018;175:122–30.
pubmed: 29510337 doi: 10.1016/j.cognition.2018.02.007
Briefer EF, Le Comber S. Vocal expression of emotions in mammals: mechanisms of production and evidence. J Zool. 2012;288:1–20.
doi: 10.1111/j.1469-7998.2012.00920.x
Tilbrook AJ, Ralph CR. Neurophysiological assessment of animal welfare. Anim Prod Sci. 2017;57:2370–5.
doi: 10.1071/AN17312
Tilbrook AJ, Ralph CR. Hormones, stress and the welfare of animals. Anim Prod Sci. 2018;58:408–15.
doi: 10.1071/AN16808
Ralph CR, Tilbrook AJ. Invited review: the usefulness of measuring glucocorticoids for assessing animal welfare. J Anim Sci. 2016;94:457–70.
pubmed: 27065116 doi: 10.2527/jas.2015-9645
Manteuffel C, Spitschak M, Ludwig C, Wirthgen E. New perspectives in the objective evaluation of animal welfare, with focus on the domestic pig. J Appl Anim Welf Sci. 2023;26:518–29.
pubmed: 34727795 doi: 10.1080/10888705.2021.1998774
Boissy A, Manteuffel G, Jensen MB, Moe RO, Spruijt B, Keeling LJ, et al. Assessment of positive emotions in animals to improve their welfare. Physiol Behav. 2007;92:375–97.
pubmed: 17428510 doi: 10.1016/j.physbeh.2007.02.003
Turner AI, Rivalland ETA, Clarke IJ, Tilbrook AJ. Stressor specificity of sex differences in hypothalamo-pituitary-adrenal axis activity: cortisol responses to exercise, endotoxin, wetting, and isolation/restraint stress in gonadectomized male and female sheep. Endocrinology. 2010;151:4324–31.
pubmed: 20668025 doi: 10.1210/en.2010-0234
Tilbrook AJ. Effects of stress on reproduction in non-rodent mammals: the role of glucocorticoids and sex differences. Rev Reprod. 2017;5:105–13.
doi: 10.1530/ror.0.0050105
Parrott RF, Bradshaw RH, Lloyd DM, Goode JA. Effects of transport and indomethacin on telemetered body temperature and release of cortisol and prolactin in pre-pubertal pigs. Res Vet Sci. 1998;64:51–5.
pubmed: 9557806 doi: 10.1016/S0034-5288(98)90115-1
Dobson H, Fergani C, Routly JE, Smith RF. Effects of stress on reproduction in ewes. Anim Reprod Sci. 2012;130:135–40.
pubmed: 22325927 doi: 10.1016/j.anireprosci.2012.01.006
Morris MJ, Kaneko K, Walker SL, Jones DN, Routly JE, Smith RF, et al. Influence of lameness on follicular growth, ovulation, reproductive hormone concentrations and estrus behavior in dairy cows. Theriogenology. 2011;76:658–68.
pubmed: 21601262 pmcid: 3156299 doi: 10.1016/j.theriogenology.2011.03.019
Qu H, Ajuwon KM. Metabolomics of heat stress response in pig adipose tissue reveals alteration of phospholipid and fatty acid composition during heat stress. J Anim Sci. 2018;96:3184–95.
pubmed: 29961875 pmcid: 6095270
García-Bueno B, Madrigal JLM, Pérez-Nievas BG, Leza JC. Stress mediators regulate brain prostaglandin synthesis and peroxisome proliferator-activated receptor-γ activation after stress in rats. Endocrinology. 2008;149:1969–78.
pubmed: 18079203 doi: 10.1210/en.2007-0482
Morimoto A, Watanabe T, Morimoto K, Nakamori T, Murakami N. Possible involvement of prostaglandins in psychological stress-induced responses in rats. J Physiol. 1991;443:421–9.
pubmed: 1668342 pmcid: 1179849 doi: 10.1113/jphysiol.1991.sp018841
Cavallini D, Mammi LME, Buonaiuto G, Palmonari A, Valle E, Formigoni A. Immune-metabolic-inflammatory markers in Holstein cows exposed to a nutritional and environmental stressing challenge. J Anim Physiol Anim Nutr. 2021;105:42–55.
doi: 10.1111/jpn.13607
Eckersall D. Acute phase protein: biomarkers of disease in cattle and sheep. Cattle Pract. 2007;15:240–3.
Cywińska A, Szarska E, Górecka R, Witkowski L, Hecold M, Bereznowski A, et al. Acute phase protein concentrations after limited distance and long distance endurance rides in horses. Res Vet Sci. 2012;93:1402–6.
pubmed: 22390917 doi: 10.1016/j.rvsc.2012.02.008
Cerón JJ, Eckersall PD, Martínez-Subiela S. Acute phase proteins in dogs and cats: current knowledge and future perspectives. Vet Clin Pathol. 2005;34:85–99.
pubmed: 15902658 doi: 10.1111/j.1939-165X.2005.tb00019.x
Cray C, Watson T, Rodriguez M, Arheart KL. Application of galactomannan analysis and protein electrophoresis in the diagnosis of Aspergillosis in avian species. J Zoo Wildl Med. 2009;40:64–70.
pubmed: 19368241 doi: 10.1638/2007-0138.1
Yamamoto S, Motomura A, Akahoshi A, Takahashi K, Minami H. Immunoglobulin secretions in the mesenteric lymph node in stressed rats. J Nutr Sci Vitaminol. 2009;55:191–4.
pubmed: 19436147 doi: 10.3177/jnsv.55.191
Zoppi S, Madrigal JLM, Pérez-Nievas BG, Marín-Jiménez I, Caso JR, Alou L, et al. Endogenous cannabinoid system regulates intestinal barrier function in vivo through cannabinoid type 1 receptor activation. Am J Physiol Gastrointest Liver Physiol. 2012;302:565–71.
doi: 10.1152/ajpgi.00158.2011
Royo F, Lyberg K, Abelson K, Carlsson HE, Hau J. Effect of repeated confined single housing of young pigs on faecal excretion of cortisol and IgA. Scand J Clin Lab Invest. 2005;32:33–7.
Goshen I, Kreisel T, Ben-Menachem-Zidon O, Licht T, Weidenfeld J, Ben-Hur T, et al. Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression. Mol Psychiatry. 2008;13:717–28.
pubmed: 17700577 doi: 10.1038/sj.mp.4002055
Kubera M, Maes M, Holan V, Basta-Kaim A, Roman A, Shani J. Prolonged desipramine treatment increases the production of interleukin-10, an anti-inflammatory cytokine, in C57BL/6 mice subjected to the chronic mild stress model of depression. J Affect Disord. 2001;63:171–8.
pubmed: 11246093 doi: 10.1016/S0165-0327(00)00182-8
Sporer KRB, Xiao L, Tempelman RJ, Burton JL, Earley B, Crowe MA. Transportation stress alters the circulating steroid environment and neutrophil gene expression in beef bulls. Vet Immunol Immunopathol. 2008;121:300–20.
pubmed: 18061277 doi: 10.1016/j.vetimm.2007.10.010
Fustini M, Galeati G, Gabai G, Mammi LE, Bucci D, Baratta M, et al. Overstocking dairy cows during the dry period affects dehydroepiandrosterone and cortisol secretion. J Dairy Sci. 2017;100:620–8.
pubmed: 27837985 doi: 10.3168/jds.2016-11293
Schurr MJ, Fabian TC, Croce MA, Varnavas LE, Proctor KG. Dehydroepiandrosterone, an endogenous immune modulator, after traumatic shock. Shock. 1997;7:55–9.
pubmed: 8989837 doi: 10.1097/00024382-199701000-00007
Lanci A, Mariella J, Ellero N, Faoro A, Peric T, Prandi A, et al. Hair cortisol and DHEA-S in foals and mares as a retrospective picture of feto-maternal relationship under physiological and pathological conditions. Animals. 2022;12:1266.
pubmed: 35625111 pmcid: 9138058 doi: 10.3390/ani12101266
Whitham JC, Bryant JL, Miller LJ. Beyond glucocorticoids: integrating dehydroepiandrosterone (DHEA) into animal welfare research. Animals. 2020;10:1381.
pubmed: 32784884 pmcid: 7459918 doi: 10.3390/ani10081381
Coulon M, Nowak R, Peyrat J, Chandèze H, Boissy A, Boivin X. Do lambs perceive regular human stroking as pleasant? behavior and heart rate variability analyses. PLoS ONE. 2015;10:e0118617.
pubmed: 25714604 pmcid: 4340872 doi: 10.1371/journal.pone.0118617
Zupan M, Framstad T, Zanella AJ. Behaviour, heart rate, and heart rate variability in pigs exposed to novelty. Revista Brasileira de Zootecnia. 2016;45:121–9.
doi: 10.1590/S1806-92902016000300006
Clapp JB, Croarkin S, Dolphin C, Lyons SK. Heart rate variability: a biomarker of dairy calf welfare. Anim Prod Sci. 2015;55:1289.
doi: 10.1071/AN14093
Zupan M, Buskas J, Altimiras J, Keeling LJ. Assessing positive emotional states in dogs using heart rate and heart rate variability. Physiol Behav. 2016;155:102–11.
pubmed: 26631546 doi: 10.1016/j.physbeh.2015.11.027
Ille N, von Lewinski M, Erber R, Wulf M, Aurich J, Möstl E, et al. Effects of the level of experience of horses and their riders on cortisol release, heart rate and heart-rate variability during a jumping course. Anim Welf. 2013;22:457–65.
doi: 10.7120/09627286.22.4.457
Bergamasco L, Osella MC, Savarino P, Larosa G, Ozella L, Manassero M, et al. Heart rate variability and saliva cortisol assessment in shelter dog: human–animal interaction effects. Appl Anim Behav Sci. 2010;125:56–68.
doi: 10.1016/j.applanim.2010.03.002
Rashamol VP, Sejian V, Bagath M, Krishnan G, Archana PR, Bhatta R. Physiological adaptability of livestock to heat stress: an updated review. J Anim Behav Biometeorol. 2018;6:62–71.
doi: 10.31893/2318-1265jabb.v6n3p62-71
Berihulay H, Abied A, He X, Jiang L, Ma Y. Adaptation mechanisms of small ruminants to environmental heat stress. Animals. 2019;9:75.
pubmed: 30823364 pmcid: 6466405 doi: 10.3390/ani9030075
Caulfield MP, Cambridge H, Foster SF, McGreevy PD. Heat stress: a major contributor to poor animal welfare associated with long-haul live export voyages. The Vet J. 2014;199:223–8.
pubmed: 24157340 doi: 10.1016/j.tvjl.2013.09.018
Lopedote M, Valentini S, Musella V, Vilar JM, Spinella G. Changes in pulse rate, respiratory rate and rectal temperature in working dogs before and after three different field trials. Animals. 2020;10:733.
pubmed: 32340191 pmcid: 7222833 doi: 10.3390/ani10040733
Panksepp J. Affective neuroscience: the foundations of human and animal emotions. New York: Oxford University Press; 1998.
doi: 10.1093/oso/9780195096736.001.0001
LeDoux JE. Emotion: clues from the brain. Annu Rev Psychol. 1995;46:209–35.
pubmed: 7872730 doi: 10.1146/annurev.ps.46.020195.001233
Paul ES, Harding EJ, Mendl M. Measuring emotional processes in animals: the utility of a cognitive approach. Neurosci Biobehav Rev. 2005;29:469–91.
pubmed: 15820551 doi: 10.1016/j.neubiorev.2005.01.002
Kremer L, Klein Holkenborg SEJ, Reimert I, Bolhuis JE, Webb LE. The nuts and bolts of animal emotion. Neurosci Biobehav Rev. 2020;113:273–86.
pubmed: 31982603 doi: 10.1016/j.neubiorev.2020.01.028
Chincarini M, Qiu L, Spinelli L, Torricelli A, Minero M, Costa ED, et al. Evaluation of sheep anticipatory response to a food reward by means of functional near-infrared spectroscopy. Animals. 2019;9:11.
doi: 10.3390/ani9010011
Chincarini M, Dalla Costa E, Qiu L, Spinelli L, Cannas S, Palestrini C, et al. Reliability of fNIRS for noninvasive monitoring of brain function and emotion in sheep. Sci Rep. 2020;10:14726.
pubmed: 32895449 pmcid: 7477174 doi: 10.1038/s41598-020-71704-5
Iversen SD, Iversen LL. Dopamine: 50 years in perspective. Trends Neurosci. 2007;30:188–93.
pubmed: 17368565 doi: 10.1016/j.tins.2007.03.002
Olguín HJ, Guzmán DC, García EH, Mejía GB. The role of dopamine and its dysfunction as a consequence of oxidative stress. Oxid Med Cell Longev. 2016;2016:9730467.
Alexander R, Aragón OR, Bookwala J, Cherbuin N, Gatt JM, Kahrilas IJ, et al. The neuroscience of positive emotions and affect: Implications for cultivating happiness and wellbeing. Neurosci Biobehav Rev. 2021;121:220–49.
pubmed: 33307046 doi: 10.1016/j.neubiorev.2020.12.002
Lürzel S, Bückendorf L, Waiblinger S, Rault JL. Salivary oxytocin in pigs, cattle, and goats during positive human-animal interactions. Psychoneuroendocrinology. 2020;115:104636.
pubmed: 32160578 doi: 10.1016/j.psyneuen.2020.104636
Busnelli M, Chini B. Molecular basis of oxytocin receptor signalling in the brain: what we know and what we need to know. In: Hurlemann R, Grinevich V, editors. Behavioral pharmacology of neuropeptides: Oxytocin. Cham: Springer; 2017. p. 3–29.
doi: 10.1007/7854_2017_6
Olazábal DE. Role of oxytocin in parental behaviour. J Neuroendocrinol. 2018;30:e12594.
pubmed: 29603440 doi: 10.1111/jne.12594
Cochran DM, Fallon D, Hill M, Frazier JA. The role of oxytocin in psychiatric disorders. Harv Rev Psychiatry. 2013;21:219–47.
pubmed: 24651556 pmcid: 4120070 doi: 10.1097/HRP.0b013e3182a75b7d
Morhenn V, Park J, Piper E, Zak P. Monetary sacrifice among strangers is mediated by endogenous oxytocin release after physical contact. Evol Hum Behav. 2008;29:375–83.
doi: 10.1016/j.evolhumbehav.2008.04.004
D’aniello B, Mastellone V, Pinelli C, Scandurra A, Musco N, Tudisco R, et al. Serum oxytocin in cows is positively correlated with caregiver interactions in the impossible task paradigm. Animals. 2022;12:276.
pubmed: 35158600 pmcid: 8833709 doi: 10.3390/ani12030276
Uvnäs-Moberg K, Arn I, Magnusson D. The psychobiology of emotion: the role of the oxytocinergic system. Int J Behav Med. 2005;12:59–65.
doi: 10.1207/s15327558ijbm1202_3
Tops M, van Peer JM, Korf J, Wijers AA, Tucker DM. Anxiety, cortisol, and attachment predict plasma oxytocin. Psychophysiology. 2007;44:444–9.
pubmed: 17371496 doi: 10.1111/j.1469-8986.2007.00510.x
Engert V, Koester AM, Riepenhausen A, Singer T. Boosting recovery rather than buffering reactivity: higher stress-induced oxytocin secretion is associated with increased cortisol reactivity and faster vagal recovery after acute psychosocial stress. Psychoneuroendocrinology. 2016;74:111–20.
pubmed: 27608360 doi: 10.1016/j.psyneuen.2016.08.029
Young Kuchenbecker S, Pressman SD, Celniker J, Grewen KM, Sumida KD, Jonathan N, et al. Oxytocin, cortisol, and cognitive control during acute and naturalistic stress. Stress. 2021;24:370–83.
pubmed: 33632072 doi: 10.1080/10253890.2021.1876658
Cardoso C, Ellenbogen MA, Orlando MA, Bacon SL, Joober R. Intranasal oxytocin attenuates the cortisol response to physical stress: a dose–response study. Psychoneuroendocrinology. 2013;38:399–407.
pubmed: 22889586 doi: 10.1016/j.psyneuen.2012.07.013
Yayou KI, Ito S, Kasuya E, Sutoh M, Ohkura S, Okamura H. Intracerebroventricularly administered oxytocin attenuated cortisol secretion, but not behavioral responses, during isolation in Holstein steers. J Vet Med Sci. 2008;70:665–71.
pubmed: 18685237 doi: 10.1292/jvms.70.665
Chen S, Sato S. Role of oxytocin in improving the welfare of farm animals — a review. Asian-Australas J Anim Sci. 2017;30:449.
pubmed: 26954194 doi: 10.5713/ajas.15.1058
Coria-Avila GA, Pfaus JG, Orihuela A, Domínguez-Oliva A, José-Pérez N, Hernández LA, et al. The neurobiology of behavior and its applicability for animal welfare: a review. Animals. 2022;12:928.
pubmed: 35405916 pmcid: 8997080 doi: 10.3390/ani12070928
Rault JL, van den Munkhof M, Buisman-Pijlman FTA. Oxytocin as an indicator of psychological and social well-being in domesticated animals: a critical review. Front Psychol. 2017;8:1521.
pubmed: 28955264 pmcid: 5601408 doi: 10.3389/fpsyg.2017.01521
LeRoith D, Holly JMP, Forbes BE. Insulin-like growth factors: ligands, binding proteins, and receptors. Mol Metab. 2021;52:101245.
pubmed: 33962049 pmcid: 8513159 doi: 10.1016/j.molmet.2021.101245
Mesotten D, van den Berghe G. Changes within the GH/IGF-I/IGFBP axis in critical illness. Crit Care Clin. 2006;22:17–28.
pubmed: 16399017 doi: 10.1016/j.ccc.2005.09.002
Lewitt MS, Boyd GW. The role of insulin-like growth factors and insulin-like growth factor–binding proteins in the nervous system. Biochem Insights. 2019;12:117862641984217.
doi: 10.1177/1178626419842176
Picillo M, Pivonello R, Santangelo G, Pivonello C, Savastano R, Auriemma R, et al. Serum IGF-1 is associated with cognitive functions in early, drug-naïve Parkinson’s disease. PLoS ONE. 2017;12:e0186508.
pubmed: 29065116 pmcid: 5655531 doi: 10.1371/journal.pone.0186508
Cassilhas RC, Antunes HKM, Tufik S, de Mello MT. Mood, anxiety, and serum IGF-1 in elderly men given 24 weeks of high resistance exercise. Percept Mot Skills. 2010;110:265–76.
pubmed: 20391891 doi: 10.2466/pms.110.1.265-276
Soto M, Cai W, Konishi M, Kahn CR. Insulin signaling in the hippocampus and amygdala regulates metabolism and neurobehavior. Proc Natl Acad Sci U S A. 2019;116:6379–84.
pubmed: 30765523 pmcid: 6442573 doi: 10.1073/pnas.1817391116
Wirthgen E, Kunze M, Goumon S, Walz C, Höflich C, Spitschak M, et al. Interference of stress with the somatotropic axis in pigs – lights on new biomarkers. Sci Rep. 2017;7:12055.
pubmed: 28935925 pmcid: 5608691 doi: 10.1038/s41598-017-11521-5
Bach LA. 40 years of IGF1: IGF-binding proteins. J Mol Endocrinol. 2018;61:T11-28.
pubmed: 29255001 doi: 10.1530/JME-17-0254
Allard JB, Duan C. IGF-binding proteins: why do they exist and why are there so many? Front Endocrinol. 2018;9:117.
doi: 10.3389/fendo.2018.00117
Murer MG, Yan Q, Raisman-Vozari R. Brain-derived neurotrophic factor in the control human brain, and in Alzheimer’s disease and Parkinson’s disease. Prog Neurobiol. 2001;63:71–124.
pubmed: 11040419 doi: 10.1016/S0301-0082(00)00014-9
Cattaneo A, Cattane N, Begni V, Pariante CM, Riva MA. The human BDNF gene: peripheral gene expression and protein levels as biomarkers for psychiatric disorders. Transl Psychiatry. 2016;6:e958.
pubmed: 27874848 pmcid: 5314126 doi: 10.1038/tp.2016.214
Yuluǧ B, Ozan E, Gönül AS, Kilic E. Brain-derived neurotrophic factor, stress and depression: a minireview. Brain Res Bull. 2009;78:267–9.
pubmed: 19111910 doi: 10.1016/j.brainresbull.2008.12.002
Chourbaji S, Brandwein C, Gass P. Altering BDNF expression by genetics and/or environment: Impact for emotional and depression-like behaviour in laboratory mice. Neurosci Biobehav Rev. 2011;35:599–611.
pubmed: 20621121 doi: 10.1016/j.neubiorev.2010.07.003
Murakami S, Imbe H, Morikawa Y, Kubo C, Senba E. Chronic stress, as well as acute stress, reduces BDNF mRNA expression in the rat hippocampus but less robustly. Neurosci Res. 2005;53:129–39.
pubmed: 16024125 doi: 10.1016/j.neures.2005.06.008
Nibuya M, Morinobu S, Duman RS. Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J Neurosci. 1995;15:7539–47.
pubmed: 7472505 pmcid: 6578063 doi: 10.1523/JNEUROSCI.15-11-07539.1995
Shirayama Y, Chen ACH, Nakagawa S, Russell DS, Duman RS. Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J Neurosci. 2002;22:3251–61.
pubmed: 11943826 pmcid: 6757539 doi: 10.1523/JNEUROSCI.22-08-03251.2002
Tyler WJ, Alonso M, Bramham CR, Pozzo-Miller LD. From acquisition to consolidation: on the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning. Learn Mem. 2002;9:224–37.
pubmed: 12359832 doi: 10.1101/lm.51202
Falkenberg T, Mohammed AK, Henriksson B, Kan Persson H, Winblad B, Lindefors N. Increased expression of brain-derived neurotrophic factor mRNA in rat hippocampus is associated with improved spatial memory and enriched environment. Neurosci Lett. 1992;138:153–6.
pubmed: 1407655 doi: 10.1016/0304-3940(92)90494-R
Ickes BR, Pham TM, Sanders LA, Albeck DS, Mohammed AH, Granholm AC. Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain. Exp Neurol. 2000;164:45–52.
pubmed: 10877914 doi: 10.1006/exnr.2000.7415
Gordon NS, Burke S, Akil H, Watson SJ, Panksepp J. Socially-induced brain “fertilization”: play promotes brain derived neurotrophic factor transcription in the amygdala and dorsolateral frontal cortex in juvenile rats. Neurosci Lett. 2003;341:17–20.
pubmed: 12676333 doi: 10.1016/S0304-3940(03)00158-7
Yamada K, Nabeshima T. Brain-derived neurotrophic factor/TrkB signaling in memory processes. J Pharmacol Sci. 2003;91:267–70.
pubmed: 12719654 doi: 10.1254/jphs.91.267
Klein AB, Williamson R, Santini MA, Clemmensen C, Ettrup A, Rios M, et al. Blood BDNF concentrations reflect brain-tissue BDNF levels across species. Int J Neuropsychopharmacol. 2011;14:347–53.
pubmed: 20604989 doi: 10.1017/S1461145710000738
Beeri MS, Sonnen J. Brain BDNF expression as a biomarker for cognitive reserve against Alzheimer disease progression. Neurology. 2016;86:702–3.
pubmed: 26819454 doi: 10.1212/WNL.0000000000002389
Mandel AL, Ozdener H, Utermohlen V. Brain-derived neurotrophic factor in human saliva: ELISA optimization and biological correlates. J Immunoassay Immunochem. 2011;32:18–30.
pubmed: 21253967 pmcid: 3046426 doi: 10.1080/15321819.2011.538625
Vrijen C, Schenk HM, Hartman CA, Oldehinkel AJ. Measuring BDNF in saliva using commercial ELISA: results from a small pilot study. Psychiatry Res. 2017;254:340–6.
pubmed: 28525789 doi: 10.1016/j.psychres.2017.04.034
Balietti M, Giuli C, Conti F. Peripheral blood brain-derived neurotrophic factor as a biomarker of Alzheimer’s disease: are there methodological biases. Mol Neurobiol. 2018;55:6661–72.
pubmed: 29330839 pmcid: 6061178 doi: 10.1007/s12035-017-0866-y
Foltran RB, Diaz SL. BDNF isoforms: a round trip ticket between neurogenesis and serotonin? J Neurochem. 2016;138:204–21.
pubmed: 27167299 doi: 10.1111/jnc.13658
Gejl AK, Enevold C, Bugge A, Andersen MS, Nielsen CH, Andersen LB. Associations between serum and plasma brain-derived neurotrophic factor and influence of storage time and centrifugation strategy. Sci Rep. 2019;9:9655.
pubmed: 31273250 pmcid: 6609657 doi: 10.1038/s41598-019-45976-5
Wessels JM, Agarwal RK, Somani A, Verschoor CP, Agarwal SK, Foster WG. Factors affecting stability of plasma brain-derived neurotrophic factor. Sci Rep. 2020;10:20232.
pubmed: 33214644 pmcid: 7677545 doi: 10.1038/s41598-020-77046-6
Sargin D. The role of the orexin system in stress response. Neuropharmacology. 2019;154:68–78.
pubmed: 30266600 doi: 10.1016/j.neuropharm.2018.09.034
Peyron C, Tighe DK, van den Pol AN, de Lecea L, Heller HC, Sutcliffe JG, et al. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci. 1998;18:9996–10015.
pubmed: 9822755 pmcid: 6793310 doi: 10.1523/JNEUROSCI.18-23-09996.1998
Seigneur E, de Lecea L. Hypocretin (orexin) replacement therapies. Med Drug Discov. 2020;8:100070.
doi: 10.1016/j.medidd.2020.100070
Jacobson LH, Hoyer D, Lecea L. Hypocretins (orexins): the ultimate translational neuropeptides. J Intern Med. 2022;291:533–56.
pubmed: 35043499 doi: 10.1111/joim.13406
Yeoh JW, Campbell EJ, James MH, Graham BA, Dayas CV. Orexin antagonists for neuropsychiatric disease: progress and potential pitfalls. Front Neurosci. 2014;8:36.
pubmed: 24616658 pmcid: 3934415 doi: 10.3389/fnins.2014.00036
Giardino WJ, de Lecea L. Hypocretin (orexin) neuromodulation of stress and reward pathways. Curr Opin Neurobiol. 2014;29:103–8.
pubmed: 25050887 doi: 10.1016/j.conb.2014.07.006
Hopf FW. Recent perspectives on orexin/hypocretin promotion of addiction-related behaviors. Neuropharmacology. 2020;168:108013.
pubmed: 32092435 doi: 10.1016/j.neuropharm.2020.108013
Allard JS, Tizabi Y, Shaffery JP, Ovid Trouth C, Manaye K. Stereological analysis of the hypothalamic hypocretin/orexin neurons in an animal model of depression. Neuropeptides. 2004;38:311–5.
pubmed: 15464197 doi: 10.1016/j.npep.2004.06.004
Chung HS, Kim JG, Kim JW, Kim HW, Yoon BJ. Orexin administration to mice that underwent chronic stress produces bimodal effects on emotion-related behaviors. Regul Pept. 2014;194–195:16–22.
pubmed: 25450574 doi: 10.1016/j.regpep.2014.11.003
Lindström M, Schinkelshoek M, Tienari PJ, Kukkonen JP, Renkonen R, Fronczek R, et al. Orexin-A measurement in narcolepsy: a stability study and a comparison of LC-MS/MS and immunoassays. Clin Biochem. 2021;90:34–9.
pubmed: 33539807 doi: 10.1016/j.clinbiochem.2021.01.009
Kukkonen JP. What do I talk about when I talk about measuring CNS orexin-A? Considerations of orexin-A measurements in clinical and preclinical setting. Med Drug Discov. 2021;11:100101.
doi: 10.1016/j.medidd.2021.100101
McLaughlin RJ, Hill MN, Gorzalka BB. A critical role for prefrontocortical endocannabinoid signaling in the regulation of stress and emotional behavior. Neurosci Biobehav Rev. 2014;42:116–31.
pubmed: 24582908 doi: 10.1016/j.neubiorev.2014.02.006
van der Stelt M, Hansen HH, Veldhuis WB, Bär PR, Nicolay K, Veldink GA, et al. Biosynthesis of endocannabinoids and their modes of action in neurodegenerative diseases. Neurotox Res. 2003;5:183–200.
pubmed: 12835123 doi: 10.1007/BF03033139
Finn DP, Haroutounian S, Hohmann AG, Krane E, Soliman N, Rice ASC. Cannabinoids, the endocannabinoid system, and pain: a review of preclinical studies. Pain. 2021;162:S5–25.
pubmed: 33729211 pmcid: 8819673 doi: 10.1097/j.pain.0000000000002268
deRoon-Cassini TA, Stollenwerk TM, Beatka M, Hillard CJ. Meet your stress management professionals: the endocannabinoids. Trends Mol Med. 2020;26:953–68.
pubmed: 32868170 pmcid: 7530069 doi: 10.1016/j.molmed.2020.07.002
Petrie GN, Nastase AS, Aukema RJ, Hill MN. Endocannabinoids, cannabinoids and the regulation of anxiety. Neuropharmacology. 2021;195:108626.
pubmed: 34116110 doi: 10.1016/j.neuropharm.2021.108626
Rahman SMK, Uyama T, Hussain Z, Ueda N. Roles of endocannabinoids and endocannabinoid-like molecules in energy homeostasis and metabolic regulation: a nutritional perspective. Annu Rev Nutr. 2021;41:177–202.
pubmed: 34115519 doi: 10.1146/annurev-nutr-043020-090216
Hillard CJ. Circulating endocannabinoids: from whence do they come and where are they going? Neuropsychopharmacology. 2018;43:155–72.
pubmed: 28653665 doi: 10.1038/npp.2017.130
Ye Q, Zeng X, Cai S, Qiao S, Zeng X. Mechanisms of lipid metabolism in uterine receptivity and embryo development. Trends Endocrinol Metab. 2021;32:1015–30.
pubmed: 34625374 doi: 10.1016/j.tem.2021.09.002
Zachut M, Kra G, Moallem U, Livshitz L, Levin Y, Udi S, et al. Characterization of the endocannabinoid system in subcutaneous adipose tissue in periparturient dairy cows and its association to metabolic profiles. PLoS ONE. 2018;13:e0205996.
pubmed: 30403679 pmcid: 6221292 doi: 10.1371/journal.pone.0205996
Myers MN, Zachut M, Tam J, Contreras GA. A proposed modulatory role of the endocannabinoid system on adipose tissue metabolism and appetite in periparturient dairy cows. J Anim Sci Biotechnol. 2021;12:21.
doi: 10.1186/s40104-021-00549-3
Kuhla B, Kaever V, Tuchscherer A, Kuhla A. Involvement of plasma endocannabinoids and the hypothalamic endocannabinoid system in increasing feed intake after parturition of dairy cows. Neuroendocrinology. 2020;110:246–57.
pubmed: 31141804 doi: 10.1159/000501208
Iannotti FA, Di Marzo V. The gut microbiome, endocannabinoids and metabolic disorders. J Endocrinol. 2021;248:83–97.
doi: 10.1530/JOE-20-0444
Celi P. Biomarkers of oxidative stress in ruminant medicine. Immunopharmacol Immunotoxicol. 2011;33:233–40.
pubmed: 20849293 doi: 10.3109/08923973.2010.514917
Ursini F, Maiorino M, Forman HJ. Redox homeostasis: The golden mean of healthy living. Redox Biol. 2016;8:205–15.
pubmed: 26820564 pmcid: 4732014 doi: 10.1016/j.redox.2016.01.010
Valacchi G, Virgili F, Cervellati C, Pecorelli A. OxInflammation: from subclinical condition to pathological biomarker. Front Physiol. 2018;9:858.
pubmed: 30038581 pmcid: 6046448 doi: 10.3389/fphys.2018.00858
Niedzielska E, Smaga I, Gawlik M, Moniczewski A, Stankowicz P, Pera J, et al. Oxidative stress in neurodegenerative diseases. Mol Neurobiol. 2016;53:4094–125.
pubmed: 26198567 doi: 10.1007/s12035-015-9337-5
Liu Z, Ren Z, Zhang J, Chuang CC, Kandaswamy E, Zhou T, et al. Role of ROS and nutritional antioxidants in human diseases. Front Physiol. 2018;9:477.
pubmed: 29867535 pmcid: 5966868 doi: 10.3389/fphys.2018.00477
Wei C, Sun Y, Chen N, Chen S, Xiu M, Zhang X. Interaction of oxidative stress and BDNF on executive dysfunction in patients with chronic schizophrenia. Psychoneuroendocrinology. 2020;111:104473.
pubmed: 31655452 doi: 10.1016/j.psyneuen.2019.104473
Forlenza MJ, Miller GE. Increased serum levels of 8-hydroxy-2′-deoxyguanosine in clinical depression. Psychosom Med. 2006;68:1–7.
pubmed: 16449405 doi: 10.1097/01.psy.0000195780.37277.2a
Yoshihara K, Hiramoto T, Sudo N, Kubo C. Profile of mood states and stress-related biochemical indices in long-term yoga practitioners. Biopsychosoc Med. 2011;5:6.
pubmed: 21635790 pmcid: 3125330 doi: 10.1186/1751-0759-5-6
Quesnel H, Père MC, Louveau I, Lefaucheur L, Perruchot MH, Prunier A, et al. Sow environment during gestation: part II. Influence on piglet physiology and tissue maturity at birth. Animal. 2019;13:1440–7.
pubmed: 30442216 doi: 10.1017/S1751731118003087
Sahoo A, Paul RK, Thirumurgan P, Sharma S, Kumawat PK, De K. Immunological and plasma antioxidant response following protection of newborn lambs from cold by umbrella-type housing and lamb-jacket in winter. Biol Rhythm Res. 2019;52:726–33.
doi: 10.1080/09291016.2019.1603688
Gatellier P, Mercier Y, Renerre M. Effect of diet finishing mode (pasture or mixed diet) on antioxidant status of Charolais bovine meat. Meat Sci. 2004;67:385–94.
pubmed: 22061512 doi: 10.1016/j.meatsci.2003.11.009
Rubio CP, Contreras-Aguilar MD, Quiles A, López-Arjona M, Cerón JJ, Martínez-Subiela S, et al. Biomarkers of oxidative stress in saliva of sheep: analytical performance and changes after an experimentally induced stress. Res Vet Sci. 2019;123:71–6.
pubmed: 30592995 doi: 10.1016/j.rvsc.2018.12.015
Apak R. Current issues in antioxidant measurement. J Agric Food Chem. 2019;67:9187–202.
pubmed: 31259552 doi: 10.1021/acs.jafc.9b03657
McBean GJ, Aslan M, Griffiths HR, Torrão RC. Thiol redox homeostasis in neurodegenerative disease. Redox Biol. 2015;5:186–94.
pubmed: 25974624 pmcid: 4434181 doi: 10.1016/j.redox.2015.04.004
Klimiuk A, Maciejczyk M, Choromańska M, Fejfer K, Waszkiewicz N, Zalewska A. Salivary redox biomarkers in different stages of dementia severity. J Clin Med. 2019;8:840.
pubmed: 31212834 pmcid: 6617318 doi: 10.3390/jcm8060840
Lim ZX, Duong MN, Boyatzis AE, Golden E, Vrielink A, Fournier PA, et al. Oxidation of cysteine 34 of plasma albumin as a biomarker of oxidative stress. Free Radic Res. 2020;54:91–103.
pubmed: 31903812 doi: 10.1080/10715762.2019.1708347
Al-Mshhdani B, Terrill J, Grounds M, Arthur P. Plasma albumin thiol oxidation as a biomarker of muscle damage and inflammation. Neuromuscul Disord. 2019;29:S157–8.
doi: 10.1016/j.nmd.2019.06.422
Woolley LD, Pilmer LW, Stephens FJ, Lim ZX, Arthur PG, GholipourKanani H, et al. The effect of hydrogen peroxide concentration and water temperature on yellowtail kingfish Seriola lalandi in a repeated bathing treatment. Aquaculture. 2022;560:738545.
Grinman E, Espadas I, Puthanveettil SV. Emerging roles for long noncoding RNAs in learning, memory and associated disorders. Neurobiol Learn Mem. 2019;163:107034.
pubmed: 31176693 doi: 10.1016/j.nlm.2019.107034
Wang J, Liu Y, Xia Q, Xia Q, Wang B, Yang C, et al. Potential roles of telomeres and telomerase in neurodegenerative diseases. Int J Biol Macromol. 2020;163:1060–78.
pubmed: 32673712 doi: 10.1016/j.ijbiomac.2020.07.046
Zhan Y, Clements MS, Roberts RO, Vassilaki M, Druliner BR, Boardman LA, et al. Association of telomere length with general cognitive trajectories: a meta-analysis of four prospective cohort studies. Neurobiol Aging. 2018;69:111–6.
pubmed: 29870951 pmcid: 6064381 doi: 10.1016/j.neurobiolaging.2018.05.004
Codocedo JF, Inestrosa NC. Environmental control of microRNAs in the nervous system: Implications in plasticity and behavior. Neurosci Biobehav Rev. 2016;60(121–38):121–38.
pubmed: 26593111 doi: 10.1016/j.neubiorev.2015.10.010
Lee GS, Conine CC. The transmission of intergenerational epigenetic information by sperm microRNAs. Epigenomes. 2022;6:12.
pubmed: 35466187 pmcid: 9036291 doi: 10.3390/epigenomes6020012
Narayanan R, Schratt G. MiRNA regulation of social and anxiety-related behaviour. Cell Mol Life Sci. 2020;77:4347–64.
pubmed: 32409861 doi: 10.1007/s00018-020-03542-7
Issler O, Haramati S, Paul ED, Maeno H, Navon I, Zwang R, et al. MicroRNA 135 is essential for chronic stress resiliency, antidepressant efficacy, and intact serotonergic activity. Neuron. 2014;83:344–60.
pubmed: 24952960 doi: 10.1016/j.neuron.2014.05.042
Haramati S, Navon I, Issler O, Ezra-Nevo G, Gil S, Zwang R, et al. MicroRNA as repressors of stress-induced anxiety: the case of amygdalar miR-34. J Neurosci. 2011;31:14191–203.
pubmed: 21976504 pmcid: 6623664 doi: 10.1523/JNEUROSCI.1673-11.2011
Baudry A, Mouillet-Richard S, Schneider B, Launay JM, Kellermann O. MiR-16 targets the serotonin transporter: a new facet for adaptive responses to antidepressants. Science. 2010;329:1537–41.
pubmed: 20847275 doi: 10.1126/science.1193692
Tavares GA, Torres A, de Souza JA. Early life stress and the onset of obesity: proof of microRNAs’ involvement through modulation of serotonin and dopamine systems’ homeostasis. Front Physiol. 2020;11:925.
pubmed: 32848865 pmcid: 7399177 doi: 10.3389/fphys.2020.00925
Roy B, Ochi S, Dwivedi Y. Potential of circulating miRNAs as molecular markers in mood disorders and associated suicidal behavior. Int J Mol Sci. 2023;24:4664.
pubmed: 36902096 pmcid: 10003208 doi: 10.3390/ijms24054664
Kozomara A, Birgaoanu M, Griffiths-Jones S. MiRBase: from microRNA sequences to function. Nucleic Acids Res. 2019;47:155–62.
doi: 10.1093/nar/gky1141
Raza SHA, Wijayanti D, Pant SD, Abdelnour SA, Hashem NM, Amin A, et al. Exploring the physiological roles of circular RNAs in livestock animals. Res Vet Sci. 2022;152:726–35.
pubmed: 36270182 doi: 10.1016/j.rvsc.2022.09.036
Miretti S, Lecchi C, Ceciliani F, Baratta M. MicroRNAs as biomarkers for animal health and welfare in livestock. Front Vet Sci. 2020;7:578193.
pubmed: 33392281 pmcid: 7775535 doi: 10.3389/fvets.2020.578193
Kos MZ, Puppala S, Cruz D, Neary JL, Kumar A, Dalan E, et al. Blood-based miRNA biomarkers as correlates of brain-based miRNA expression. Front Mol Neurosci. 2022;15:817290.
pubmed: 35392269 pmcid: 8981579 doi: 10.3389/fnmol.2022.817290
Wiegand C, Savelsbergh A, Heusser P. MicroRNAs in psychological stress reactions and their use as stress-associated biomarkers, especially in human saliva. Biomed Hub. 2017;2:1–15.
pubmed: 31988918 pmcid: 6945927 doi: 10.1159/000481126
Wang N, Zhang J, Xiao B, Sun X, Xie R, Chen A. Recent advances in the rapid detection of microRNA with lateral flow assays. Biosens Bioelectron. 2022;211:114345.
pubmed: 35576723 doi: 10.1016/j.bios.2022.114345
Bond CS, Fox AH. Paraspeckles: nuclear bodies built on long noncoding RNA. J Cell Biol. 2009;186:637–44.
pubmed: 19720872 pmcid: 2742191 doi: 10.1083/jcb.200906113
Fox AH, Nakagawa S, Hirose T, Bond CS. Paraspeckles: where long noncoding RNA meets phase separation. Trends Biochem Sci. 2018;43:124–35.
pubmed: 29289458 doi: 10.1016/j.tibs.2017.12.001
Chujo T, Hirose T. Nuclear bodies built on architectural long noncoding RNAs: unifying principles of their construction and function. Mol Cells. 2017;40:889–96.
pubmed: 29276943 pmcid: 5750707
An H, Williams NG, Shelkovnikova TA. NEAT1 and paraspeckles in neurodegenerative diseases: a missing lnc found? Noncoding RNA Res. 2018;3:243–52.
pubmed: 30533572 pmcid: 6257911 doi: 10.1016/j.ncrna.2018.11.003
Wang Y, Hu SB, Wang MR, Yao RW, Wu D, Yang L, et al. Genome-wide screening of NEAT1 regulators reveals cross-regulation between paraspeckles and mitochondria. Nat Cell Biol. 2018;20:1145–58.
pubmed: 30250064 doi: 10.1038/s41556-018-0204-2
Barry G, Briggs JA, Hwang DW, Nayler SP, Fortuna PRJ, Jonkhout N, et al. The long non-coding RNA NEAT1 is responsive to neuronal activity and is associated with hyperexcitability states. Sci Rep. 2017;7:40127.
pubmed: 28054653 pmcid: 5214838 doi: 10.1038/srep40127
Kukharsky MS, Ninkina NN, An H, Telezhkin V, Wei W, de Meritens CR, et al. Long non-coding RNA Neat1 regulates adaptive behavioural response to stress in mice. Transl Psychiatry. 2020;10:1–19.
doi: 10.1038/s41398-020-0854-2
Boros FA, Maszlag-Török R, Vécsei L, Klivényi P. Increased level of NEAT1 long non-coding RNA is detectable in peripheral blood cells of patients with Parkinson’s disease. Brain Res. 2020;1730:146672.
pubmed: 31953211 doi: 10.1016/j.brainres.2020.146672
Simchovitz A, Hanan M, Niederhoffer N, Madrer N, Yayon N, Bennett ER, et al. NEAT1 is overexpressed in Parkinson’s disease substantia nigra and confers drug-inducible neuroprotection from oxidative stress. FASEB J. 2019;33:11223–34.
pubmed: 31311324 pmcid: 6766647 doi: 10.1096/fj.201900830R
Bu F, Wang A, Zhu Y, You H, Zhang Y, Meng X, et al. LncRNA NEAT1: shedding light on mechanisms and opportunities in liver diseases. Liver Int. 2020;40:2612–26.
pubmed: 32745314 doi: 10.1111/liv.14629
Dong P, Xiong Y, Yue J, Hanley SJB, Kobayashi N, Todo Y, et al. Long Non-coding RNA NEAT1: a novel target for diagnosis and therapy in human tumors. Front Genet. 2018;9:471.
pubmed: 30374364 pmcid: 6196292 doi: 10.3389/fgene.2018.00471
Varki A. Biological roles of glycans. Glycobiology. 2017;27:3–49.
pubmed: 27558841 doi: 10.1093/glycob/cww086
Flynn RA, Pedram K, Malaker SA, Batista PJ, Smith BAH, Johnson AG, et al. Small RNAs are modified with N-glycans and displayed on the surface of living cells. Cell. 2021;184:3109–24.
pubmed: 34004145 pmcid: 9097497 doi: 10.1016/j.cell.2021.04.023
Disney MD. A glimpse at the glycoRNA world. Cell. 2021;184:3080–1.
pubmed: 34115968 doi: 10.1016/j.cell.2021.05.025
Flynn R, Smith B, Johnson A, Pedram K, George B, Malaker S, et al. Mammalian Y RNAs are modified at discrete guanosine residues with N-glycans. bioRxiv. 2019;787614:1–30.
Kowalski MP, Krude T. Functional roles of non-coding Y RNAs. Int J Biochem Cell Biol. 2015;66:20–9.
pubmed: 26159929 pmcid: 4726728 doi: 10.1016/j.biocel.2015.07.003
Lünemann JD, von Gunten S, Neumann H. Targeting sialylation to treat central nervous system diseases. Trends Pharmacol Sci. 2021;42:998–1008.
pubmed: 34607695 doi: 10.1016/j.tips.2021.09.002
Blackburn EH. Structure and function of telomeres. Nature. 1991;350:569–73.
pubmed: 1708110 doi: 10.1038/350569a0
Levy MZ, Allsopp RC, Futcher AB, Greider CW, Harley CB. Telomere end-replication problem and cell aging. J Mol Biol. 1992;225:951–60.
pubmed: 1613801 doi: 10.1016/0022-2836(92)90096-3
Reichert S, Criscuolo F, Verinaud E, Zahn S, Massemin S. Telomere length correlations among somatic tissues in adult zebra finches. PLoS ONE. 2013;8:e81496.
pubmed: 24349076 pmcid: 3857187 doi: 10.1371/journal.pone.0081496
Bateson M, Poirier C. Can biomarkers of biological age be used to assess cumulative lifetime experience? Anim Welf. 2019;28:41–56.
doi: 10.7120/09627286.28.1.041
Oliveira BS, Zunzunegui MV, Quinlan J, Fahmi H, Tu MT, Guerra RO. Systematic review of the association between chronic social stress and telomere length: a life course perspective. Ageing Res Rev. 2016;26:37–52.
pubmed: 26732034 doi: 10.1016/j.arr.2015.12.006
Rentscher KE, Carroll JE, Mitchell C. Psychosocial stressors and telomere length: a current review of the science. Annu Rev Public Health. 2020;41:223–45.
pubmed: 31900099 doi: 10.1146/annurev-publhealth-040119-094239
Koliada AK, Krasnenkov DS, Vaiserman AM. Telomeric aging: mitotic clock or stress indicator? Front Genet. 2015;5:82.
Denham J. Telomere regulation: lessons learnt from mice and men, potential opportunities in horses. Anim Genet. 2020;51:3–13.
pubmed: 31637754 doi: 10.1111/age.12870
Uchino BN, Cawthon RM, Smith TW, Light KC, McKenzie J, Carlisle M, et al. Social relationships and health: is feeling positive, negative, or both (ambivalent) about your social ties related to telomeres? Health Psychol. 2012;31:789–96.
pubmed: 22229928 pmcid: 3378918 doi: 10.1037/a0026836
Lin X, Zhou J, Dong B. Effect of different levels of exercise on telomere length: A systematic review and meta-analysis. J Rehabil Med. 2019;51:473–8.
pubmed: 31093683 doi: 10.2340/16501977-2560
Schutte NS, Palanisamy SKA, McFarlane JR. The relationship between positive psychological characteristics and longer telomeres. Psychol Health. 2016;31:1466–80.
pubmed: 27616348 doi: 10.1080/08870446.2016.1226308
Schneper LM, Brooks-Gunn J, Notterman DA, Suomi SJ. Early-life experiences and telomere length in adult rhesus monkeys: an exploratory study. Psychosom Med. 2016;78:1066–71.
pubmed: 27763985 pmcid: 5097005 doi: 10.1097/PSY.0000000000000402
Bateson M. Cumulative stress in research animals: telomere attrition as a biomarker in a welfare context? BioEssays. 2016;38:201–12.
pubmed: 26645576 doi: 10.1002/bies.201500127
Pepper GV, Bateson M, Nettle D. Telomeres as integrative markers of exposure to stress and adversity: a systematic review and meta-analysis. R Soc Open Sci. 2018;5: 180744.
pubmed: 30225068 pmcid: 6124068 doi: 10.1098/rsos.180744
Badmus KA, Idrus Z, Meng GY, Mamat-Hamidi K. Telomere length, apoptotic, and inflammatory genes: novel biomarkers of gastrointestinal tract pathology and meat quality traits in chickens under chronic stress (Gallus gallus domesticus). Animals. 2021;11:3276.
pubmed: 34828008 pmcid: 8614256 doi: 10.3390/ani11113276
Lai TP, Wright WE, Shay JW. Comparison of telomere length measurement methods. Proc R Soc B Biol Sci. 2018;373:20160451.
Refinetti R. Circadian rhythmicity of body temperature and metabolism. Temperature. 2020;7:321–62.
doi: 10.1080/23328940.2020.1743605
Brown SA, Zumbrunn G, Fleury-Olela F, Preitner N, Schibler U. Rhythms of mammalian body temperature can sustain peripheral circadian clocks. Curr Biol. 2002;12:1574–83.
pubmed: 12372249 doi: 10.1016/S0960-9822(02)01145-4
Refinetti R. The circadian rhythm of body temperature. Front Biosci. 2010;15:564–94.
doi: 10.2741/3634
Maloney SK, Goh G, Fuller A, Vesterdorf K, Blache D. Amplitude of the circadian rhythm of temperature in homeotherms. CAB Reviews. 2019;14:1–30.
doi: 10.1079/PAVSNNR201914019
Refinetti R, Piccione G. Intra- and inter-individual variability in the circadian rhythm of body temperature of rats, squirrels, dogs, and horses. J Therm Biol. 2005;30:139–46.
doi: 10.1016/j.jtherbio.2004.09.003
Palacios C, Plaza J, Abecia JA. A high cattle-grazing density alters circadian rhythmicity of temperature, heart rate, and activity as measured by implantable bio-loggers. Front Physiol. 2021;12:707222.
pubmed: 34483961 pmcid: 8414586 doi: 10.3389/fphys.2021.707222
Lamont EW, Legault-Coutu D, Cermakian N, Boivin DB. The role of circadian clock genes in mental disorders. Dialogues Clin Neurosci. 2007;9:333–42.
pubmed: 17969870 doi: 10.31887/DCNS.2007.9.3/elamont
Elmore SK, Dahl K, Avery DH, Savage MV, Brengelmann GL. Body temperature and diurnal type in women with seasonal affective disorder. Health Care Women Int. 1993;14:17–26.
pubmed: 8454523 doi: 10.1080/07399339309516023
Souetre E, Salvati E, Wehr TA, Sack DA, Krebs B, Darcourt G. Twenty-four-hour profiles of body temperature and plasma TSH in bipolar patients during depression and during remission and in normal control subjects. Am J Psychiatry. 1988;145:1133–7.
pubmed: 3414857 doi: 10.1176/ajp.145.9.1133
Volicer L, Harper DG, Manning BC, Goldstein R, Satlin A. Sundowning and circadian rhythms in Alzheimer’s disease. A J Psychiatry. 2001;158:704–11.
doi: 10.1176/appi.ajp.158.5.704
Nikitopoulou G, Crammer JL. Change in diurnal temperature rhythm in manic-depressive illness. BMJ. 1976;1:1311–4.
pubmed: 944610 pmcid: 1640287 doi: 10.1136/bmj.1.6021.1311
Mota-Rojas D, Miranda-Cortés A, Casas-Alvarado A, Mora-Medina P, Boscato-Funes L, Hernández-Ávalos I. Neurobiology and modulation of stress-induced hyperthermia and fever in animal. Abanico veterinario. 2021;11:1–17.
Oka T. Stress-induced hyperthermia and hypothermia. Handb Clin Neurol. 2018;157:599–621.
pubmed: 30459027 doi: 10.1016/B978-0-444-64074-1.00035-5
Blache D, Maloney SK. New physiological measures of the biological cost of responding to challenges. In: Ferguson DM, Lee C, Fisher F, editors. Advances in Sheep Welfare. Sawston: Woodhead Publishing; 2017. p. 73–104.
doi: 10.1016/B978-0-08-100718-1.00005-4
Meyer LCR, Fick L, Matthee A, Mitchell D, Fuller A. Hyperthermia in captured impala (Aepyceros melampus): a fright not flight response. J Wildl Dis. 2008;44:404–16.
pubmed: 18436672 doi: 10.7589/0090-3558-44.2.404
Pedernera-Romano C, Ruiz de la Torre J, Badiella L, Manteca X. ssociations between open-field behavior and stress-induced hyperthermia in two breeds of shee. Anim Welf. 2011;20:339–46.
doi: 10.1017/S0962728600002906
Dallmann R, Steinlechner S, von Hörsten S, Karl T. Stress-induced hyperthermia in the rat: comparison of classical and novel recording methods. Lab Anim. 2006;40:186–93.
pubmed: 16600078 doi: 10.1258/002367706776319015
Sanger ME, Doyle RE, Hinch GN, Lee C. Sheep exhibit a positive judgement bias and stress-induced hyperthermia following shearing. Appl Anim Behav Sci. 2011;131:94–103.
doi: 10.1016/j.applanim.2011.02.001
Lees AM, Salvin HE, Colditz IG, Lee C. The influence of temperament on body temperature response to handling in angus cattle. Animals. 2020;10:172.
pubmed: 31968606 pmcid: 7023438 doi: 10.3390/ani10010172
Adriaan Bouwknecht J, Olivier B, Paylor RE. The stress-induced hyperthermia paradigm as a physiological animal model for anxiety: a review of pharmacological and genetic studies in the mouse. Neurosci Biobehav Rev. 2007;31:41–59.
pubmed: 16618509 doi: 10.1016/j.neubiorev.2006.02.002
Watanabe S. Social factors modulate restraint stress induced hyperthermia in mice. Brain Res. 2015;1624:134–9.
pubmed: 26232073 doi: 10.1016/j.brainres.2015.07.019
Keeney AJ, Hogg S, Marsden CA. Alterations in core body temperature, locomotor activity, and corticosterone following acute and repeated social defeat of male NMRI mice. Physiol Behav. 2001;74:177–84.
pubmed: 11564466 doi: 10.1016/S0031-9384(01)00541-8
Travain T, Valsecchi P. Infrared thermography in the study of animals’ emotional responses: a critical review. Animals. 2021;11:2510.
pubmed: 34573476 pmcid: 8464846 doi: 10.3390/ani11092510
Barbini B, Benedetti F, Colombo C, Guglielmo E, Campori E, Smeraldi E. Perceived mood and skin body temperature rhythm in depression. Eur Arch Psychiatry Clin Neurosci. 1998;248:157–60.
pubmed: 9728735 doi: 10.1007/s004060050033
Rushen J. Changing concepts of farm animal welfare: bridging the gap between applied and basic research. Appl Anim Behav Sci. 2003;81:199–214.
doi: 10.1016/S0168-1591(02)00281-2
Richter SH, Hintze S. From the individual to the population – and back again? emphasising the role of the individual in animal welfare science. Appl Anim Behav Sci. 2019;212:1–8.
doi: 10.1016/j.applanim.2018.12.012
Morgan L, Raz T. Providing meaningful environmental enrichment and measuring saliva cortisol in pigs housed on slatted flooring. J Vis Exp. 2019;151: e60070.
Heimbürge S, Kanitz E, Tuchscherer A, Otten W. Is it getting in the hair? – cortisol concentrations in native, regrown and segmented hairs of cattle and pigs after repeated ACTH administrations. Gen Comp Endocrinol. 2020;295:113534.
pubmed: 32540492 doi: 10.1016/j.ygcen.2020.113534
Weaver SJ, Hynd PI, Ralph CR, Hocking Edwards JE, Burnard CL, Narayan E, et al. Chronic elevation of plasma cortisol causes differential expression of predominating glucocorticoid in plasma, saliva, fecal, and wool matrices in sheep. Domest Anim Endocrinol. 2021;74:106503.
pubmed: 32846373 doi: 10.1016/j.domaniend.2020.106503
Cheong Y, Oh C, Lee K, Cho KH. Survey of porcine respiratory disease complex-associated pathogens among commercial pig farms in Korea via oral fluid method. J Vet Sci. 2017;18:283–9.
pubmed: 27586468 pmcid: 5639080 doi: 10.4142/jvs.2017.18.3.283
Fels M, Rauterberg S, Schwennen C, Ligges U, Herbrandt S, Kemper N, et al. Cortisol/dehydroepiandrosterone ratio in saliva: endocrine biomarker for chronic stress in pigs? Livest Sci. 2019;222:21–4.
doi: 10.1016/j.livsci.2019.01.022
Nakagawa Y, To M, Saruta J, Yamamoto Y, Yamamoto T, Shimizu T, et al. Effect of social isolation stress on saliva BDNF in rat. J Oral Sci. 2019;61:516–20.
pubmed: 31631095 doi: 10.2334/josnusd.18-0409
Heimbürge S, Kanitz E, Otten W. The use of hair cortisol for the assessment of stress in animals. Gen Comp Endocrinol. 2019;270:10–7.
pubmed: 30287191 doi: 10.1016/j.ygcen.2018.09.016
Kovács L, Jurkovich V, Bakony M, Szenci O, Póti P, Tå’Zsér J. Welfare implication of measuring heart rate and heart rate variability in dairy cattle: literature review and conclusions for future research. Animal. 2014;8:316–30.
Camerlink I, Coulange E, Farish M, Baxter EM, Turner SP. Facial expression as a potential measure of both intent and emotion. Sci Rep. 2018;8:17602.
pubmed: 30514964 pmcid: 6279763 doi: 10.1038/s41598-018-35905-3
Seidl R. A functional-dynamic reflection on participatory processes in modeling projects. Ambio. 2015;44:750–65.
pubmed: 25999270 pmcid: 4646859 doi: 10.1007/s13280-015-0670-8
Nowotny H. Democratising expertise and socially robust knowledge. Sci Public Policy. 2003;30:151–6.
doi: 10.3152/147154303781780461
Fiorino D. Citizen participation and environmental risk: a survey of institutional mechanisms. Sci Technol Human Values. 1990;15:226–43.
doi: 10.1177/016224399001500204
Stauffacher M, Flüeler T, Krütli P, Scholz RW. Analytic and dynamic approach to collaboration: a transdisciplinary case study on sustainable landscape development in a swiss prealpine region. Syst Pract Action Res. 2008;21:409–22.
doi: 10.1007/s11213-008-9107-7
Fröhlich H, Balling R, Beerenwinkel N, Kohlbacher O, Kumar S, Lengauer T, et al. From hype to reality: data science enabling personalized medicine. BMC Med. 2018;16:1–15.
doi: 10.1186/s12916-018-1122-7
Fernandes JN, Hemsworth PH, Coleman GJ, Tilbrook AJ. Costs and benefits of improving farm animal welfare. Agriculture. 2021;11(2):104.
doi: 10.3390/agriculture11020104

Auteurs

Sarah Babington (S)

School of Agriculture and Environment, The University of Western Australia, Crawley, WA, 6009, Australia.

Alan J Tilbrook (AJ)

Centre for Animal Science, The Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St Lucia, QLD, 4072, Australia.
School of Veterinary Science, The University of Queensland, Gatton, QLD, 4343, Australia.

Shane K Maloney (SK)

School of Human Sciences, The University of Western Australia, Crawley, WA, 6009, Australia.

Jill N Fernandes (JN)

School of Veterinary Science, The University of Queensland, Gatton, QLD, 4343, Australia.

Tamsyn M Crowley (TM)

School of Medicine, Deakin University, Geelong, VIC, 3217, Australia.
Poultry Hub Australia, University of New England, Armidale, NSW, 2350, Australia.

Luoyang Ding (L)

School of Agriculture and Environment, The University of Western Australia, Crawley, WA, 6009, Australia.
College of Animal Science and Technology, Yangzhou University, Yangzhou, 225009, China.

Archa H Fox (AH)

School of Human Sciences, The University of Western Australia, Crawley, WA, 6009, Australia.

Song Zhang (S)

School of Human Sciences, The University of Western Australia, Crawley, WA, 6009, Australia.

Elise A Kho (EA)

Centre for Animal Science, The Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St Lucia, QLD, 4072, Australia.

Daniel Cozzolino (D)

Centre for Nutrition and Food Sciences, The Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St Lucia, QLD, 4072, Australia.

Timothy J Mahony (TJ)

Centre for Animal Science, The Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St Lucia, QLD, 4072, Australia.

Dominique Blache (D)

School of Agriculture and Environment, The University of Western Australia, Crawley, WA, 6009, Australia. dominique.blache@uwa.edu.au.
College of Animal Science and Technology, Yangzhou University, Yangzhou, 225009, China. dominique.blache@uwa.edu.au.

Classifications MeSH