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Can biomarkers of biological age be used to assess cumulative lifetime experience?

Published online by Cambridge University Press:  01 January 2023

M Bateson  and
C Poirier
M Bateson
Affiliation:
Institute of Neuroscience and Centre for Behaviour and Evolution, Newcastle University, Newcastle-upon-Tyne, UK Contact for correspondence and requests for reprints: [email protected]
C Poirier
Affiliation:
Institute of Neuroscience and Centre for Behaviour and Evolution, Newcastle University, Newcastle-upon-Tyne, UK
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Abstract

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Objective methods for assessing the cumulative lifetime experience of non-human animals would be valuable. We develop the hypothesis that biological age is a common currency that integrates the overall quality of an animal's lifetime experience across a range of types of exposure. Ageing is the result of the accumulation of somatic damage, and its rate is determined by the balance between experiences that cause damage and experiences that mitigate damage or promote repair. Negative affective states are associated with somatic damage via both direct causal and indirect pathways. Based on these premises, we predict that individuals that are biologically old for their chronological age will, on average, have experienced worse lives than individuals that are biologically younger, both in terms of their overall health and affective experience. Biological age is, thus, an attractive measure of cumulative experience because it requires no subjective decisions either about how a given exposure impacts an animal, or about how different dimensions of welfare should be weighted in an overall assessment. Biological age can be measured objectively using biomarkers. We argue that two biomarkers, namely leukocyte telomere length and hippocampal volume, are valid biomarkers of cumulative experience in humans, with potential for use in non-human vertebrates. We discuss how these biomarkers could be used to assess cumulative experience in animals, highlighting some of the limitations. We conclude that biomarkers of biological age offer a viable objective solution to the assessment of cumulative experience and their application in an animal welfare context deserves further exploration.

Keywords

animal welfarebiological ageexposomehippocampuslifetime experiencetelomere length
Type
Articles
Information
Animal Welfare , Volume 28 , Issue 1 , February 2019 , pp. 41 - 56
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Copyright
© The Author(s), 2023. Published by Cambridge University Press on behalf of The Universities Federation for Animal Welfare

References

Arnone, D, Job, D, Selvaraj, S, Abe, O, Amico, F, Cheng, Y, Colloby, SJ, O’Brien, JT, Frodl, T, Gotlib, IH, Ham, BJ, Kim, MJ, Koolschijn, PCM, Périco, CAM, Salvadore, G, Thomas, AJ, Van Tol, MJ, van der Wee, NJA, Veltman, DJ, Wagner, G and McIntosh, AM 2016 Computational meta-analysis of sta-tistical parametric maps in major depression. Human Brain Mapping 37: 1393–1404. https://doi.org/10.1002/hbm.23108CrossRefGoogle Scholar
Astuti, Y, Wardhana, A, Watkins, J and Wulaningsih, W 2017 Cigarette smoking and telomere length: A systematic review of 84 studies and meta-analysis. Environmental Research 158: 480–489. https://doi.org/10.1016/j.envres.2017.06.038CrossRefGoogle ScholarPubMed
Aviv, A, Hunt, SC, Lin, J, Cao, X, Kimura, M and Blackburn, E 2011 Impartial comparative analysis of measurement of leukocyte telomere length/DNA content by Southern blots and qPCR. Nucleic Acids Research 39: e134. https://doi.org/10.1093/nar/gkr634CrossRefGoogle ScholarPubMed
Aviv, A, Valdes, AM and Spector, TD 2006 Human telomere biology: Pitfalls of moving from the laboratory to epidemiology. International Journal of Epidemiology 35: 1424–1429. https://doi.org/10.1093/ije/dyl169CrossRefGoogle ScholarPubMed
Aydinonat, D, Penn, DJ, Smith, S, Moodley, Y, Hoelzl, F, Knauer, F and Schwarzenberger, F 2014 Social isolation shortens telomeres in African Grey parrots (Psittacus erithacus erithacus). PLoS One 9: 2–6. https://doi.org/10.1371/journal.pone.0093839CrossRefGoogle ScholarPubMed
Barnard, CJ and Hurst, JL 1996 Welfare by design: The natural selection of welfare criteria. Animal Welfare 5: 405–433CrossRefGoogle Scholar
Bateson, M 2016 Cumulative stress in research animals: Telomere attrition as a biomarker in a welfare context? BioEssays 38: 201–212. https://doi.org/10.1002/bies.201500127CrossRefGoogle Scholar
Bateson, M, Aviv, A, Bendix, L, Benetos, A, Ben-Shlomo, Y, Bojesen, SE, Cooper, C, Cooper, R, Deary, IJ, Hägg, S, Harris, SE, Kark, JD, Kronenberg, F, Kuh, D, Labat, C, Martin-Ruiz, C, Meyer, C, Nordestgaard, BG, Penninx, BWJH, Pepper, G, Révész, D, Said, MA, Starr, JM, Syddall, H, Thomson, WM, van der Harst, P, Whooley, M, von Zglinicki, T, Willeit, P, Zhan, Y and Nettle, D undated Smoking does not accelerate leukocyte telomere attrition: a meta-analysis of 18 longitudinal cohorts. Royal Society Open Science. https://doi.org/10.5281/zenodo.1463971CrossRefGoogle Scholar
Bateson, M, Eisenberg, DTA and Nettle, D 2018 Controlling for baseline telomere length biases estimates of the rate of telom-ere attrition. Zenodo. http://doi.org/10.5281/zenodo.1009086CrossRefGoogle Scholar
Bateson, M and Nettle, D 2017 The telomere lengthening conundrum - it could be biology. Aging Cell 16(2): 312–319. https://doi.org/10.1111/acel.12555CrossRefGoogle ScholarPubMed
Bateson, M and Nettle, D 2018 Why are there associations between telomere length and behaviour? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 373:20160438. https://doi.org/10.1098/rstb.2016.0438CrossRefGoogle Scholar
Beirne, C, Delahay, R and Young, A 2015 Sex differences in senescence: The role of intra-sexual competition in early adult-hood. Proceedings of the Royal Society B: Biological Sciences 282:20151086. https://doi.org/10.1098/rspb.2015.1086CrossRefGoogle Scholar
Belsky, DW, Caspi, A, Houts, R, Cohen, HJ, Corcoran, DL, Danese, A, Harrington, H, Israel, S, Levine, ME, Schaefer, JD, Sugden, K, Williams, B, Yashin, AI, Poulton, R and Moffitt, TE 2015 Quantification of biological aging in young adults. Proceedings of the National Academy of Sciences 112: E4104–E4110. https://doi.org/10.1073/pnas.1506264112CrossRefGoogle ScholarPubMed
Bingman, VP, Salas, C and Rodriguez, F 2009 Evolution of the hippocampus. In: Binder, MD, Hirokawa, N and Winhorst, U (eds) Encyclopedia of Neuroscience pp 1356–1360. Springer-Verlag: Berlin, Heidelberg, Germany. https://doi.org/10.1007/978-3-540-29678-2_3158CrossRefGoogle Scholar
Carlson, LE, Beattie, TL, Giese-Davis, J, Faris, P, Tamagawa, R, Fick, LJ, Degelman, ES and Speca, M 2015 Mindfulness-based cancer recovery and supportive-expressive therapy maintain telom-ere length relative to controls in distressed breast cancer survivors. Cancer 121: 476–484. https://doi.org/10.1002/cncr.29063CrossRefGoogle ScholarPubMed
Clarkson, JM, Dwyer, DM, Flecknell, PA, Leach, MC and Rowe, C 2018 Handling method alters the hedonic value of reward in laboratory mice. Scientific Reports 8: 2448. https://doi.org/10.1038/s41598-018-20716-3CrossRefGoogle ScholarPubMed
Clubb, R, Rowcliffe, M, Lee, P, Mar, KU, Moss, C and Mason, GJ 2008 Compromised survivorship in zoo elephants. Science 322: 1649. https://doi.org/10.1126/science.1164298CrossRefGoogle ScholarPubMed
Cole, JH, Ritchie, SJ, Bastin, ME, Valdés Hernández, MC, Muñoz Maniega, S, Royle, N, Corley, J, Pattie, A, Harris, SE, Zhang, Q, Wray, NR, Redmond, P, Marioni, RE, Starr, JM, Cox, SR, Wardlaw, JM, Sharp, DJ and Deary, IJ 2018 Brain age predicts mortality. Molecular Psychiatry 23: 1385–1392CrossRefGoogle ScholarPubMed
Cronbach, LJ and Meehl, PE 1955 Construct validity in psycho-logical tests. Psychological Bulletin 52: 281–302. https://doi.org/10.1037/h0040957CrossRefGoogle Scholar
Dannlowski, U, Stuhrmann, A, Beutelmann, V, Zwanzger, P, Lenzen, T, Grotegerd, D, Domschke, K, Hohoff, C, Ohrmann, P, Bauer, J, Lindner, C, Postert, C, Konrad, C, Arolt, V, Heindel, W, Suslow, T and Kugel, H 2012 Limbic scars: Long-term conse-quences of childhood maltreatment revealed by functional and struc-tural magnetic resonance imaging. Biological Psychiatry 71: 286–293. https://doi.org/10.1016/j.biopsych.2011.10.021CrossRefGoogle Scholar
Darrow, SM, Verhoeven, JE, Révész, D, Lindqvist, D, Penninx, BW, Delucchi, KL, Wolkowitz, OM and Mathews, CA 2016 The association between psychiatric disorders and telomere length: A meta-analysis involving 14,827 persons. Psychosomatic Medicine 78: 776–787. https://doi.org/10.1097/PSY.0000000000000356CrossRefGoogle Scholar
Dawkins, MS 2006 A user's guide to animal welfare science. Trends in Ecology & Evolution 21: 77–82. https://doi.org/10.1016/j.tree.2005.10.017CrossRefGoogle ScholarPubMed
Dawkins, MS 2017 Animal welfare with and without conscious-ness. Journal of Zoology 301: 1–10. https://doi.org/10.1111/jzo.12434CrossRefGoogle Scholar
Ebner, K and Singewald, N 2017 Individual differences in stress susceptibility and stress inhibitory mechanisms. Current Opinion in Behavioral Sciences 14: 54–64. https://doi.org/10.1016/j.cobe-ha.2016.11.016CrossRefGoogle Scholar
Epel, ES, Blackburn, EH, Lin, J, Dhabhar, FS, Adler, NE, Morrow, JD and Cawthon, RM 2004 Accelerated telomere shortening in response to life stress. Proceedings of the National Academy of Sciences of the United States of America 101: 17312–17315. https://doi.org/10.1073/pnas.0407162101CrossRefGoogle ScholarPubMed
European Parliament and European Council 2010 Directive 2010/63/EU pp 33–79. EU: Brussels, BelgiumGoogle Scholar
Ezzati, A, Zimmerman, ME, Katz, MJ, Sundermann, EE, Smith, JL, Lipton, ML and Lipton, RB 2014 Hippocampal sub-fields differentially correlate with chronic pain in older adults. Brain Research 1573: 54–62. https://doi.org/10.1016/j.brain-res.2014.05.025CrossRefGoogle Scholar
Farm Animal Welfare Council (FAWC) 2009 Farm Animal Welfare in Great Britain: Past, Present and Future. FAWC: London, UKGoogle Scholar
Firth, J, Stubbs, B, Vancampfort, D, Schuch, F, Lagopoulos, J, Rosenbaum, S and Ward, PB 2018 Effect of aerobic exercise on hippocampal volume in humans: A systematic review and meta-analysis. NeuroImage 166: 230–238. https://doi.org/10.1016/j.neuroimage.2017.11.007CrossRefGoogle ScholarPubMed
Fjell, AM, Westlye, LT, Grydeland, H, Amlien, I, Espeseth, T, Reinvang, I, Raz, N, Holland, D, Dale, AM and Walhovd, KB 2013 Critical ages in the life course of the adult brain: Nonlinear subcortical aging. Neurobiology of Aging 34: 2239–2247. https://doi.org/10.1016/j.neurobiolaging.2013.04.006CrossRefGoogle ScholarPubMed
Fraser, D 1995 Science, values and animal welfare: exploring the ‘inextricable connection.’ Animal Welfare 4: 103–117CrossRefGoogle Scholar
Glass, J, Simon, RW and Andersson, MA 2016 Parenthood and happiness: Effects of work-family reconciliation policies in 22 OECD countries. American Journal of Sociology 122: 886–929. https://doi.org/10.1086/688892CrossRefGoogle ScholarPubMed
Gold, AL, Steuber, ER, White, LK, Pacheco, J, Sachs, JF, Pagliaccio, D, Berman, E, Leibenluft, E and Pine, DS 2017 Cortical thickness and subcortical gray matter volume in pediatric anxiety disorders. Neuropsychopharmacology 42: 2423–2433. https://doi.org/10.1038/npp.2017.83CrossRefGoogle ScholarPubMed
Gomes, NM, Ryder, OA, Houck, ML, Charter, SJ, Walker, W, Forsyth, NR, Austad, SN, Venditti, C, Pagel, M, Shay, JW and Wright, WE 2011 Comparative biology of mammalian telomeres: Hypotheses on ancestral states and the roles of telom-eres in longevity determination. Aging Cell 10: 761–768. https://doi.org/10.1111/j.1474-9726.2011.00718.xCrossRefGoogle Scholar
Gomes, NM, Shay, JW and Wright, WE 2010 Telomere biol-ogy in Metazoa. FEBS Letters 584: 3741–3751. https://doi.org/10.1016/j.febslet.2010.07.031CrossRefGoogle Scholar
Gottlieb, DH, Capitanio, JP and McCowan, B 2013 Risk fac-tors for stereotypic behavior and self-biting in rhesus macaques (Macaca mulatta): Animal's history, current environment, and per-sonality. American Journal of Primatology 75: 995–1008. https://doi.org/10.1002/ajp.22161CrossRefGoogle Scholar
Greco, BJ, Meehan, CL, Hogan, JN, Leighty, KA, Mellen, J, Mason, GJ and Mench, JA 2016 The days and nights of zoo ele-phants: Using epidemiology to better understand stereotypic behavior of African elephants (Loxodonta africana) and Asian ele-phants (Elephas maximus) in North American zoos. PLoS One 11:1–29. https://doi.org/10.1371/journal.pone.0144276CrossRefGoogle Scholar
Harshman, LG and Zera, AJ 2007 The cost of reproduction: the devil in the details. Trends in Ecology and Evolution 22: 80–86. https://doi.org/10.1016/j.tree.2006.10.008CrossRefGoogle ScholarPubMed
Hassett, AL, Epel, E, Clauw, DJ, Harris, RE, Harte, SE, Kairys, A, Buyske, S and Williams, D 2012 Pain is associated with short leukocyte telomere length in women with fibromyal-gia. Journal of Pain 13: 959–969. https://doi.org/10.1016/j.jpain.2012.07.003CrossRefGoogle Scholar
Heim, C and Nemeroff, CB 2001 The role of childhood trau-ma in the neurobiology of mood and anxiety disorders: preclini-cal and clinical studies. Biological Psychiatry 49: 1023–1039. https://doi.org/10.1016/S0006-3223(01)01157-XCrossRefGoogle Scholar
Hodel, AS, Hunt, RH, Cowell, RA, Van Den Heuvel, SE, Gunnar, MR and Thomas, KM 2015 Duration of early adversi-ty and structural brain development in post-institutionalized ado-lescents. NeuroImage 105: 112–119. https://doi.org/10.1016/j.neu-roimage.2014.10.020CrossRefGoogle Scholar
Hölzel, BK, Carmody, J, Vangel, M, Congleton, C, Yerramsetti, SM, Gard, T and Lazar, SW 2011 Mindfulness practice leads to increases in regional brain gray matter density. Psychiatry Research - Neuroimaging 191: 36–43. https://doi.org/10.1016/j.pscychresns.2010.08.006CrossRefGoogle ScholarPubMed
Honess, P and Wolfensohn, S 2010 The extended welfare assessment grid: A matrix for the assessment of welfare and cumulative suffering in experimental animals. ATLA Alternatives to Laboratory Animals 38: 205–212CrossRefGoogle ScholarPubMed
Huang, P, Zhou, J, Zhao, X, Chen, S, Zou, C and Li, J 2017 The association between obstructive sleep apnea and shortened telomere length: A systematic review and meta-analysis. Sleep Medicine 48: 107–112. https://doi.org/10.1016/j.sleep.2017.09.034CrossRefGoogle ScholarPubMed
Hurnik, JF and Lehmann, H 1985 The philosophy of farm ani-mal welfare: a contribution to the assessment of farm animal well-being. Second European Symposium on Poultry Welfare pp 256–266. Celle, GermanyGoogle Scholar
Jacka, FN, Cherbuin, N, Anstey, KJ, Sachdev, P and Butterworth, P 2015 Western diet is associated with a smaller hippocampus: a longitudinal investigation. BMC Medicine 13: 215. https://doi.org/10.1186/s12916-015-0461-xCrossRefGoogle ScholarPubMed
Jackowski, A, Perera, TD, Abdallah, CG, Garrido, G, Tang, CY, Martinez, J, Mathew, SJ, Gorman, JM, Rosenblum, LA, Smith, ELP, Dwork, AJ, Shungu, DC, Kaffman, A, Gelernter, J, Coplan, JD and Kaufman, J 2011 Early-life stress, corpus cal-losum development, hippocampal volumetrics, and anxious behav-ior in male nonhuman primates. Psychiatry Research - Neuroimaging 192: 37–44. https://doi.org/10.1016/j.pscychresns.2010.11.006CrossRefGoogle Scholar
Jia, L, Zhang, W and Chen, X 2017 Common methods of bio-logical age estimation. Clinical Interventions in Aging 12: 759–772. https://doi.org/10.2147/CIA.S134921CrossRefGoogle Scholar
Jylhava, J, Pedersen, NL and Hagg, S 2017 Biological age pre-dictors. EBioMedicine 21: 29–36. https://doi.org/10.1016/j.ebiom.2017.03.046CrossRefGoogle Scholar
Kaplanis, J, Gordon, A, Wahl, M, Gershowitz, M, Markus, B, Sheikh, M, Gymrek, M, Bhatia, G, MacArthur, DG, Price, A and Erlich, Y 2018 Quantitative analysis of population-scale fam-ily trees using millions of relatives. Science 360: 171–175. https://doi.org/10.1126/science.aam9309CrossRefGoogle Scholar
Kenyon, CJ 2010 The genetics of ageing. Nature 467: 504–512. https://doi.org/10.1038/nature08980CrossRefGoogle Scholar
Khan, SS, Singer, BD and Vaughan, DE 2017 Molecular and physiological manifestations and measurement of aging in humans. Aging Cell 16: 624–633. https://doi.org/10.1111/acel.12601CrossRefGoogle ScholarPubMed
Kimura, M, Hjelmborg, JVB, Gardner, JP, Bathum, L, Brimacombe, M, Lu, X, Christiansen, L, Vaupel, JW, Aviv, A and Christensen, K 2008 Telomere length and mortality: A study of leukocytes in elderly Danish twins. American Journal of Epidemiology 167: 799–806. https://doi.org/10.1093/aje/kwm380CrossRefGoogle ScholarPubMed
King, KS, Kozlitina, J, Rosenberg, RN, Peshock, RM, McColl, RW and Garcia, CK 2014 Effect of leukocyte telomere length on total and regional brain volumes in a large population-based cohort.. JAMA Neurology 71(10): 1247–1254. https://doi.org/10.1001/jamaneurol.2014.1926CrossRefGoogle Scholar
Koolschijn, PCMP, van Haren, NEM, Lensvelt-Mulders, GJLM, Hulshoff Pol, HE and Kahn, RS 2009 Brain volume abnormalities in major depressive disorder: A meta-analysis of magnetic resonance imaging studies. Human Brain Mapping 30:3719–3735. https://doi.org/10.1002/hbm.20801CrossRefGoogle ScholarPubMed
Lemaître, JF, Gaillard, JM, Lackey, LB, Clauss, M and Müller, DWH 2013 Comparing free-ranging and captive populations reveals intra-specific variation in aging rates in large herbivores. Experimental Gerontology 48: 162–167. https://doi.org/10.1016/j.exger.2012.12.004CrossRefGoogle ScholarPubMed
Lendvai, Z, Giraudeau, M and Bo, V 2015 Within-individual plasticity explains age-related decrease in stress response in a short-lived bird. Biology Letters 11: 20150272. https://doi.org/10.1098/rsbl.2015.0272CrossRefGoogle Scholar
Li, Z, He, Y, Wang, D, Tang, J and Chen, X 2017 Association between childhood trauma and accelerated telomere erosion in adulthood: A meta-analytic study. Journal of Psychiatric Research 93:64–71. https://doi.org/10.1016/j.jpsychires.2017.06.002CrossRefGoogle ScholarPubMed
Lin, PY, Huang, YC and Hung, CF 2016 Shortened telomere length in patients with depression: A meta-analytic study. Journal of Psychiatric Research 76: 84–93. https://doi.org/10.1016/j.jpsy-chires.2016.01.015CrossRefGoogle ScholarPubMed
Luders, E, Toga, AW, Lepore, N and Gaser, C 2009 The underlying anatomical correlates of long-term meditation: Larger hippocampal and frontal volumes of gray matter. NeuroImage 45:672–678. https://doi.org/10.1016/j.neuroimage.2008.12.061CrossRefGoogle ScholarPubMed
Mason, GJ and Latham, NR 2004 Can't stop, won't stop: Is stereotypy a reliable animal welfare indicator? Animal Welfare 13: 57–69CrossRefGoogle Scholar
Mathur, MB, Epel, E, Kind, S, Desai, M, Parks, CG, Sandler, DP and Khazeni, N 2015 Perceived stress and telomere length: A systematic review, meta-analysis, and methodologic considerations for advancing the field. Brain, Behavior and Immunity 54: 158–169. https://doi.org/10.1016/j.bbi.2016.02.002CrossRefGoogle Scholar
McKinnon, MC, Yucel, K, Nazarov, A and MacQueen, GM 2009 A meta-analysis examining clinical predictors of hippocampal volume in patients with major depressive disorder. Journal of Psychiatry Neuroscience 3434: 41–54Google Scholar
Mendl, M, Burman, OHP, Parker, RMA and Paul, ES 2009 Cognitive bias as an indicator of animal emotion and welfare: Emerging evidence and underlying mechanisms. Applied Animal Behaviour Science 118: 161–181. https://doi.org/10.1016/j.applan-im.2009.02.023CrossRefGoogle Scholar
Mendl, M, Burman, OHP and Paul, ES 2010 An integrative and functional framework for the study of animal emotion and mood. Proceedings of the Royal Society B: Biological Sciences 277: 2895–2904. https://doi.org/10.1098/rspb.2010.0303CrossRefGoogle Scholar
Morozova, A, Zubkov, E, Strekalova, T, Kekelidze, Z, Storozeva, Z, Schroeter, CA, Bazhenova, N, Lesch, KP, Cline, BH and Chekhonin, V 2016 Ultrasound of alternating frequencies and variable emotional impact evokes depressive syndrome in mice and rats. Progress in Neuro-Psychopharmacology and Biological Psychiatry 68: 52–63. https://doi.org/10.1016/j.pnpbp.2016.03.003CrossRefGoogle ScholarPubMed
Morris, JR, Hurnik, JF, Friendship, RM and Evans, NM 1998 The effect of the Hurnik-Morris (HM) system on sow reproduction, attrition, and longevity. Journal of Animal Science 76: 2759–2762. https://doi.org/10.2527/1998.76112759xCrossRefGoogle ScholarPubMed
Müezzinler, A, Zaineddin, KA and Brenner, H 2013 A sys-tematic review of leukocyte telomere length and age in adults. Ageing Research Reviews 12: 509–519. https://doi.org/10.1016/j.arr.2013.01.003CrossRefGoogle Scholar
Munafò, MR and Smith, GD 2018 Repeating experiments is not enough. Nature 553: 399–401. https://doi.org/10.1038/d41586-018-01023-3CrossRefGoogle Scholar
Mundstock, E, Zatti, H, Louzada, FM, Oliveira, SG, Guma, FTCR, Paris, MM, Rueda, AB, Machado, DG, Stein, RT, Jones, MH, Sarria, EE, Barbé-Tuana, FM and Mattiello, R 2015 Effects of physical activity in telomere length: Systematic review and meta-analysis. Ageing Research Reviews 22: 72–80. https://doi.org/10.1016/j.arr.2015.02.004CrossRefGoogle ScholarPubMed
Nettle, D, Andrews, C, Reichert, S, Bedford, T, Kolenda, C, Parker, C, Martin-Ruiz, C, Monaghan, P and Bateson, M 2017 Early-life adversity accelerates cellular ageing and affects adult inflammation: Experimental evidence from the European starling. Scientific Reports 7: 40794. https://doi.org/10.1038/srep40794CrossRefGoogle ScholarPubMed
Nettle, D and Bateson, M 2012 The evolutionary origins of mood and its disorders. Current Biology 22: R712–721. https://doi.org/10.1016/j.cub.2012.06.020CrossRefGoogle ScholarPubMed
Niddam, DM, Lee, S-H, Su, Y-T and Chan, R-C 2017 Brain structural changes in patients with chronic myofascial pain. European Journal of Pain 21: 148–158. https://doi.org/10.1002/ejp.911CrossRefGoogle ScholarPubMed
Nilsonne, G, Tamm, S, Månsson, KNT, Åkerstedt, T and Lekander, M 2015 Leukocyte telomere length and hippocampus volume: a meta-analysis. F1000 Research 4: 1073. https://doi.org/10.12688/f1000research.7198.1CrossRefGoogle ScholarPubMed
Nussey, DH, Baird, D, Barrett, E, Boner, W, Fairlie, J, Gemmell, N, Hartmann, N, Horn, T, Haussmann, M, Olsson, M, Turbill, C, Verhulst, S, Zahn, S and Monaghan, P 2014 Measuring telomere length and telomere dynamics in evolutionary biology and ecology. Methods in Ecology and Evolution 5:299–310. https://doi.org/10.1111/2041-210X.12161CrossRefGoogle ScholarPubMed
Nussey, DH, Froy, H, Lemaitre, JF, Gaillard, JM and Austad, SN 2013 Senescence in natural populations of animals: Widespread evidence and its implications for bio-gerontology. Ageing Research Reviews 12: 214–225. https://doi.org/10.1016/j.arr.2012.07.004CrossRefGoogle ScholarPubMed
Nussey, DH, Kruuk, LEB, Donald, A, Fowlie, M and Clutton-Brock, TH 2006 The rate of senescence in maternal performance increases with early-life fecundity in red deer. Ecology Letters 9:1342–1350. https://doi.org/10.1111/j.1461-0248.2006.00989.xCrossRefGoogle ScholarPubMed
O’Doherty, DCM, Chitty, KM, Saddiqui, S, Bennett, MR and Lagopoulos, J 2015 A systematic review and meta-analysis of magnetic resonance imaging measurement of structural volumes in post-traumatic stress disorder. Psychiatry Research -Neuroimaging 232: 1–33. https://doi.org/10.1016/j.pscy-chresns.2015.01.002CrossRefGoogle Scholar
Paquola, C, Bennett, MR and Lagopoulos, J 2016 Understanding heterogeneity in grey matter research of adults with childhood maltreatment. A meta-analysis and review. Neuroscience and Biobehavioral Reviews 69: 299–312. https://doi.org/10.1016/j.neubiorev.2016.08.011CrossRefGoogle ScholarPubMed
Park, M, Verhoeven, JE, Cuijpers, P, Reynolds, CF and Penninx, BWJH 2015 Where you live may make you old: The association between perceived poor neighborhood quality and leukocyte telomere length. PLoS One 10: 1–13. https://doi.org/10.1371/journal.pone.0128460Google ScholarPubMed
Paul, ES, Harding, EJ and Mendl, M 2005 Measuring emotional processes in animals: the utility of a cognitive approach. Neuroscience and Biobehavioral Reviews 29: 469–491. https://doi.org/10.1016/j.neubiorev.2005.01.002CrossRefGoogle ScholarPubMed
Pechtel, P and Pizzagalli, DA 2011 Effects of early life stress on cognitive and affective function: An integrated review of human literature. Psychopharmacology 214: 55–70. https://doi.org/10.1007/s00213-010-2009-2CrossRefGoogle ScholarPubMed
Pepper, GV, Bateson, M and Nettle, D 2018 Telomeres as integrative markers of exposure to stress and adversity: A sys-tematic review and meta-analysis. Royal Society Open Science. http://rsos.royalsocietypublishing.org/content/5/8/180744CrossRefGoogle Scholar
Pickard, J 2013 Review of the assessment of cumulative severity and lifetime experience in non-human primates used in neuroscience research. http://www.gov.uk/government/uploads/system/uploads/attachment_data/file/261687/cs_nhp_review_FINAL_2013_cor-rected.pdfGoogle Scholar
Poirier, C and Bateson, M 2017 Pacing stereotypies in labora-tory rhesus macaques: implications for animal welfare and the validity of neuroscientific findings. Neuroscience and Biobehavioral Reviews 83: 508–515. https://doi.org/10.1016/j.neu-biorev.2017.09.010CrossRefGoogle Scholar
Poirier, C, Bateson, M, Gualtieri, F, Armstrong, EA, Laws, GC, Boswell, T and Smulders, TV 2018 Validation of a cumulative affective experience biomarker: hippocampal plasticity (Version1). Zenodo. http://doi.org/10.5281/zenodo.2445798CrossRefGoogle Scholar
Puterman, E, Lin, J, Krauss, J, Blackburn, EH and Epel, ES 2015 Determinants of telomere attrition over 1 year in healthy older women: stress and health behaviors matter. Molecular Psychiatry 20: 529–535. https://doi.org/10.1038/mp.2014.70CrossRefGoogle ScholarPubMed
Rafie, N, Golpour Hamedani, S, Barak, F, Safavi, SM and Miraghajani, M 2017 Dietary patterns, food groups and telom-ere length: A systematic review of current studies. European Journal of Clinical Nutrition 71: 151–158. https://doi.org/10.1038/ejcn.2016.149CrossRefGoogle ScholarPubMed
Rahman, MM, Callaghan, CK, Kerskens, CM, Chattarji, S and O’Mara, SM 2016 Early hippocampal volume loss as a mark-er of eventual memory deficits caused by repeated stress. Scientific Reports 6: 1–15. https://doi.org/10.1038/srep29127CrossRefGoogle Scholar
Ralph, CR and Tilbrook, AJ 2016 The usefulness of measuring glucocorticoids for assessing animal welfare. Journal of Animal Science 94: 457–470. https://doi.org/10.2527/jas.2015-9645CrossRefGoogle ScholarPubMed
Rolls, ET 2013 What are emotional states, and why do we have them? Emotion Review 5: 241–247. https://doi.org/10.1177/1754073913477514CrossRefGoogle Scholar
Schutte, NS and Malouff, JM 2015 The association between depression and leukocyte telomere length: a meta-analysis. Depression and Anxiety 32: 229–238. https://doi.org/10.1002/da.22351CrossRefGoogle ScholarPubMed
Seeker, LA, Ilska, JJ, Psifidi, A, Wilbourn, RV, Underwood, SL, Fairlie, J, Holland, R, Froy, H, Salvo-Chirnside, E, Bagnall, A, Whitelaw, B, Coffey, MP, Nussey, DH and Banos, G 2018 Bovine telomere dynamics and the association between telomere length and productive lifespan. Scientific Reports 8: 12748CrossRefGoogle ScholarPubMed
Selye, H 1956 The Stress of Life. McGraw-Hill: New York, NY, USAGoogle Scholar
Sforza, E, Celle, S, Saint-Martin, M, Barthélémy, JC and Roche, F 2016 Hippocampus volume and subjective sleepiness in older people with sleep-disordered breathing: A preliminary report. Journal of Sleep Research 25: 190–193. https://doi.org/10.1111/jsr.12367CrossRefGoogle ScholarPubMed
Smith, EL, Greenwood, VJ, Goldsmith, AR and Cuthill, IC 2005 Effect of repetitive visual stimuli on behaviour and plasma corticosterone of European starlings. Animal Biology 55: 245–258. https://doi.org/10.1163/1570756054472827CrossRefGoogle Scholar
Solomon, Z, Tsur, N, Levin, Y, Uziel, O, Lahav, M and Ohry, A 2017 The implications of war captivity and long-term psy-chopathology trajectories for telomere length. Psychoneuroendocrinology 81: 122–128. https://doi.org/10.1016/j.psyneuen.2017.04.004CrossRefGoogle Scholar
Spencer, KA, Evans, NP and Monaghan, P 2009 Postnatal stress in birds: a novel model of glucocorticoid programming of the hypothalamic-pituitary-adrenal axis. Endocrinology 150: 1931–1934. https://doi.org/10.1210/en.2008-1471CrossRefGoogle ScholarPubMed
Staffaroni, AM, Tosun, D, Lin, J, Elahi, FM, Casaletto, KB, Wynn, MJ, Patel, N, Neuhaus, J, Walters, SM, Epel, ES, Blackburn, EH and Kramer, JH 2018 Telomere attrition is associated with declines in medial temporal lobe volume and white matter microstructure in functionally independent older adults. Neurobiology of Aging 69: 68–75. https://doi.org/10.1016/j.neurobiolaging.2018.04.021CrossRefGoogle ScholarPubMed
Steenstrup, T, Hjelmborg, JVB, Kark, JD, Christensen, K and Aviv, A 2013 The telomere lengthening conundrum: Artifact or biology? Nucleic Acids Research 41: 1–7. https://doi.org/10.1093/nar/gkt370CrossRefGoogle ScholarPubMed
Strandberg, TE, Strandberg, A, Saijonmaa, O, Tilvis, RS, Pitkälä, KH and Fyhrquist, F 2012 Association between alcohol consumption in healthy midlife and telomere length in older men. The Helsinki Businessmen Study. European Journal of Epidemiology 27: 815–822. https://doi.org/10.1007/s10654-012-9728-0CrossRefGoogle ScholarPubMed
Trochim, WMK, Donnelly, JP and Arora, K 2015 Research Methods: The Essential Knowledge Base, Second Edition. Wadsworth Publishing: Belmont, CA, USAGoogle Scholar
UK Government 2012 The Animals (Scientific Procedures) Act 1986 Amendment Regulations 2012. https://www.legislation.gov.uk/ukdsi/2012/9780111530313Google Scholar
Walker, M, Duggan, G, Roulston, N, Van Slack, A and Mason, G 2012 Negative affective states and their effects on mor-bidity, mortality and longevity. Animal Welfare 21: 497–509. https://doi.org/10.7120/09627286.21.4.497CrossRefGoogle Scholar
Weich, S, Patterson, J, Shaw, R and Stewart-Brown, S 2009 Family relationships in childhood and common psychiatric disor-ders in later life: systematic review of prospective studies. British Journal of Psychiatry 194: 392–398. https://doi.org/10.1192/bjp.bp.107.042515CrossRefGoogle Scholar
Welfare Quality® 2009 Welfare Quality® assessment protocol for poultry (broilers, laying hens). Welfare Quality®: Lelystad, The Netherlands.Google Scholar
Wilbourn, RV, Moatt, JP, Froy, H, Walling, CA, Nussey, DH and Boonekamp, JJ 2018 The relationship between telomere length and mortality risk in non-model vertebrate systems: A meta-analysis. Philosophical Transactions of the Royal Society B: Biological Sciences 373: 20160447. https://doi.org/10.1098/rstb.2016.0447CrossRefGoogle ScholarPubMed
Wild, CP 2005 Complementing the genome with an ‘exposome’: The outstanding challenge of environmental exposure measure-ment in molecular epidemiology. Cancer Epidemiology Biomarkers and Prevention 14: 1847–1850. https://doi.org/10.1158/1055-9965.EPI-05-0456CrossRefGoogle Scholar
Wild, CP 2012 The exposome: From concept to utility. International Journal of Epidemiology 41: 24–32. https://doi.org/10.1093/ije/dyr236CrossRefGoogle ScholarPubMed
Wise, T, Radua, J, Via, E, Cardoner, N, Abe, O, Adams, TM, Amico, F, Cheng, Y, Cole, JH, de Azevedo Marques Périco, C, Dickstein, DP, Farrow, TFD, Frodl, T, Wagner, G, Gotlib, IH, Gruber, O, Ham, BJ, Job, DE, Kempton, MJ, Kim, MJ, Koolschijn, PCMP, Malhi, GS, Mataix-Cols, D, McIntosh, AM, Nugent, AC, O’Brien, JT, Pezzoli, S, Phillips, ML, Sachdev, PS, Salvadore, G, Selvaraj, S, Stanfield, AC, Thomas, AJ, van Tol, MJ, van der Wee, NJA, Veltman, DJ, Young, AH, Fu, CH, Cleare, AJ and Arnone, D 2017 Common and distinct patterns of grey-matter volume alteration in major depression and bipolar disorder: evidence from voxel-based meta-analysis. Molecular Psychiatry 22(10): 1455–1463. https://doi.org/10.1038/mp.2016.72CrossRefGoogle ScholarPubMed
Wojcicki, JM, Medrano, R, Lin, J and Epel, E 2018 Increased cel-lular aging by 3 years of age in Latino, preschool children who con-sume more sugar-sweetened beverages: A pilot study. Childhood Obesity 14(3): 149–157. https://doi.org/10.1089/chi.2017.0159CrossRefGoogle Scholar
Woon, FL, Sood, S and Hedges, DW 2010 Hippocampal vol-ume deficits associated with exposure to psychological trauma and posttraumatic stress disorder in adults: A meta-analysis. Progress in Neuro-Psychopharmacology and Biological Psychiatry 34:1181–1188. https://doi.org/10.1016/j.pnpbp.2010.06.016CrossRefGoogle Scholar
Zimmerman, ME, Ezzati, A, Katz, MJ, Lipton, ML, Brickman, AM, Sliwinski, MJ and Lipton, RB 2016 Perceived stress is differentially related to hippocampal subfield volumes among older adults. PLoS One 11: e0154530. https://doi.org/10.1371/journal.pone.0154530CrossRefGoogle ScholarPubMed