Abstract
As average human lifespans increase across the globe, companion animals, specifically dogs and cats, are also living longer with more age-related morbidities. However, a similar trend is not seen in mammalian livestock species. Cows, pigs, goats, and sheep, as well as more niche mammalian species raised across the world, have been primarily raised for their economic benefit to humans and are culled from the population once their production declines. To this end, we lack clear knowledge about the age-related morbidities and causes of death that afflict livestock animals due to natural aging, as well as detailed age-specific survival rates. Here, we review the current state of the field of agricultural mammal aging, as well as provide specific questions and directions that may provide novel resources for veterinarians and aging biologists. By raising awareness of the overall quality of life and ongoing health of individual livestock animals, we can potentially increase production into older life stages, leading to decreased costs to farmers and improved welfare for the animals themselves.
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Ahlman T, Berglund B, Rydhmer L, Strandberg E. Culling reasons in organic and conventional dairy herds and genotype by environment interaction for longevity. J Dairy Sci. 2011;94:1568–75. https://doi.org/10.3168/jds.2010-3483.
Albuquerque TAF, Drummond do Val L, Doherty A, de Magalhaes JP. From humans to hydra: patterns of cancer across the tree of life. Biol Rev Camb Philos Soc. 2018;93:1715–34. https://doi.org/10.1111/brv.12415.
Austad SN. Retarded senescence in an insular population of Virginia opossums. J Zool. 1993;229:695–708.
Austad SN, Fischer KE. Sex differences in lifespan. Cell Metab. 2016;23:1022–33. https://doi.org/10.1016/j.cmet.2016.05.019.
Austad SN, Hoffman JM. Is antagonistic pleiotropy ubiquitous in aging biology? Evol Med Public Health. 2018;2018:287–94. https://doi.org/10.1093/emph/eoy033.
Baker DJ, et al. Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature. 2011;479:232–6. https://doi.org/10.1038/nature10600.
Bartke A, Sun LY, Longo V. Somatotropic signaling: trade-offs between growth, reproductive development, and longevity. Physiol Rev. 2013;93:571–98. https://doi.org/10.1152/physrev.00006.2012.
Bellows J, et al. Aging in cats: common physical and functional changes. J Feline Med Surg. 2016a;18:533–50. https://doi.org/10.1177/1098612X16649523.
Bellows J, et al. Evaluating aging in cats: how to determine what is healthy and what is disease. J Feline Med Surg. 2016b;18:551–70. https://doi.org/10.1177/1098612X16649525.
Bieber A, et al. Production level, fertility, health traits, and longevity in local and commercial dairy breeds under organic production conditions in Austria, Switzerland, Poland, and Sweden. J Dairy Sci. 2019;102:5330–41. https://doi.org/10.3168/jds.2018-16147.
Biscarini F, Nicolazzi EL, Stella A, Boettcher PJ, Gandini G. Challenges and opportunities in genetic improvement of local livestock breeds. Front Genet. 2015;6:33. https://doi.org/10.3389/fgene.2015.00033.
Bonneau M, Weiler U. Pros and cons of alternatives to piglet castration: welfare, boar taint, and other meat quality traits. Animals (Basel). 2019;9. https://doi.org/10.3390/ani9110884.
Borghese A (2005) Buffalo production and research. REU Technical Series 67. FAO Regional Office for Europe
Brosnahan MM, Paradis MR. Assessment of clinical characteristics, management practices, and activities of geriatric horses. J Am Vet Med Assoc. 2003;223:99–103. https://doi.org/10.2460/javma.2003.223.99.
Brown DE, Dechow CD, Liu WS, Harvatine KJ, Ott TL. Hot topic: association of telomere length with age, herd, and culling in lactating Holsteins. J Dairy Sci. 2012;95:6384–7. https://doi.org/10.3168/jds.2012-5593.
Byun S (2010) Genes assoicated with variation in longevity and fecundity in sheep. Lincoln University
Byun SO, Zhou H, Frampton CM, Hickford JG. No association between variation in the ovine calpastatin gene and either longevity or fertility in sheep. Animal Genetics. 2010;41:223–4.
Byun SO, Zhou H, Hickford JG. Characterization of genetic variation in the Forkhead box class O3 gene (FOXO3) in sheep. DNA Cell Biol. 2011;30:449–52. https://doi.org/10.1089/dna.2010.1193.
Byun SO, Forrest RH, Frampton CM, Zhou H, Hickford JG. An association between lifespan and variation in insulin-like growth factor I receptor in sheep. J Anim Sci. 2012;90:2484–7. https://doi.org/10.2527/jas.2011-4148.
Caliebe A, Nebel A, Makarewicz C, Krawczak M, Krause-Kyora B. Insights into early pig domestication provided by ancient DNA analysis. Sci Rep. 2017;7:44550. https://doi.org/10.1038/srep44550.
Chen J, et al. Comprehensive transcriptional landscape of porcine cardiac and skeletal muscles reveals differences of aging. Oncotarget. 2018;9:1524–41. https://doi.org/10.18632/oncotarget.23290.
Chen J, et al. Comprehensive transcriptional profiling of aging porcine liver. Peer J. 2019a;7:e6949. https://doi.org/10.7717/peerj.6949.
Chen J, et al. Comprehensive transcriptional profiling of porcine brain aging. Gene. 2019b;693:1–9. https://doi.org/10.1016/j.gene.2019.01.019.
Clark S, Mora Garcia MB. A 100-year review: advances in goat milk research. J Dairy Sci. 2017;100:10026–44. https://doi.org/10.3168/jds.2017-13287.
Clutton-Brock TH, Isvaran K. Sex differences in ageing in natural populations of vertebrates. Proc Biol Sci. 2007;274:3097–104. https://doi.org/10.1098/rspb.2007.1138.
Cozzi B, Ballarin C, Mantovani R, Rota A. Aging and veterinary care of cats, dogs, and horses through the records of three university veterinary hospitals. Front Vet Sci. 2017;4:14. https://doi.org/10.3389/fvets.2017.00014.
Creevy KE, Austad SN, Hoffman JM, O'Neill DG, Promislow DE. The companion dog as a model for the longevity dividend cold spring. Harb Perspect Med. 2016;6:a026633. https://doi.org/10.1101/cshperspect.a026633.
de Magalhaes JP, et al. A reassessment of genes modulating aging in mice using demographic measurements of the rate of aging. Genetics. 2018;208:1617–30. https://doi.org/10.1534/genetics.118.300821.
Dohoo IR, DesCoteaux L, Leslie K, Fredeen A, Shewfelt W, Preston A, et al. A meta-analysis review of the effects of recombinant bovine somatotropin. 2. Effects on animal health, reproductive performance, and culling. Can J Vet Res. 2003a;67:252–64.
Dohoo IR, Leslie K, DesCoteaux L, Fredeen A, Dowling P, Preston A, et al. A meta-analysis review of the effects of recombinant bovine somatotropin. 1. Methodology and effects on production. Can J Vet Res. 2003b;67:241–51.
El Debaky HA, Kutchy NA, Ul-Husna A, Indriastuti R, Akhter S, Purwantara B, et al. Potential of water buffalo in world agriculture: challenges and opportunities. Appl Anim Sci. 2019;35:255–68.
Favier RP, Mol JA, Kooistra HS, Rijnberk A. Large body size in the dog is associated with transient GH excess at a young age. J Endocrinol. 2001;170:479–84.
Fleming JM, Creevy KE, Promislow DEL. Mortality in North American dogs from 1984 to 2004: an investigation into age-, size-, and breed-related causes of death. J Vet Intern Med. 2011;25:187–98. https://doi.org/10.1111/J.1939-1676.2011.0695.X.
Flisikowska T, Kind A, Schnieke A. The new pig on the block: modelling cancer in pigs. Transgenic Res. 2013;22:673–80. https://doi.org/10.1007/s11248-013-9720-9.
Fontana L, Partridge L, Longo VD. Extending healthy life span--from yeast to humans. Science. 2010;328:321–6. https://doi.org/10.1126/science.1172539.
Fowler ME. Health care of the geriatric llama and alpaca. Vet Clin North Am Food Anim Pract. 1994;10:391–9. https://doi.org/10.1016/s0749-0720(15)30571-5.
Gautam M, Stevenson MA, Lopez-Villalobos N, McLean V. Risk factors for culling, sales and deaths in New Zealand dairy goat herds, 2000–2009. Front Vet Sci. 2017;4:191. https://doi.org/10.3389/fvets.2017.00191.
Greer KA, Hughes LM, Masternak MM. Connecting serum IGF-1, body size, and age in the domestic dog. Age (Dordr). 2011;33:475–83. https://doi.org/10.1007/s11357-010-9182-4.
Hamidi Hay E, Roberts A. Genomic prediction and genome-wide association analysis of female longevity in a composite beef cattle breed. J Anim Sci. 2017;95:1467–71. https://doi.org/10.2527/jas.2016.1355.
Hamilton JB, Mestler GE. Mortality and survival: comparison of eunuchs with intact men and women in a mentally retarded population. J Gerontol. 1969;24:395–411. https://doi.org/10.1093/geronj/24.4.395.
Haskell MJ, Rennie LJ, Bowell VA, Bell MJ, Lawrence AB. Housing system, milk production, and zero-grazing effects on lameness and leg injury in dairy cows. J Dairy Sci. 2006;89:4259-66. https://doi.org/10.3168/jds.S0022-0302(06)72472-9.
Heise J, Liu Z, Stock KF, Rensing S, Reinhardt F, Simianer H. The genetic structure of longevity in dairy cows. J Dairy Sci. 2016;99:1253–65. https://doi.org/10.3168/jds.2015-10163.
Hickson LJ, et al. Senolytics decrease senescent cells in humans: Preliminary report from a clinical trial of Dasatinib plus Quercetin in individuals with diabetic kidney disease. EBioMedicine. 2019;47:446–56. https://doi.org/10.1016/j.ebiom.2019.08.069.
Hinrichs A, et al. Growth hormone receptor-deficient pigs resemble the pathophysiology of human Laron syndrome and reveal altered activation of signaling cascades in the liver. Mol Metab. 2018;11:113–28. https://doi.org/10.1016/j.molmet.2018.03.006.
Hoffman JM, Creevy KE, Franks A, O'Neill DG, Promislow DEL. The companion dog as a model for human aging and mortality. Aging Cell. 2018a;17:e12737. https://doi.org/10.1111/acel.12737.
Hoffman JM, O’Neill DG, Creevy KE, Austad SN. Do female dogs age differently than male dogs? J Gerontol A Biol Sci Med Sci. 2018b;73:150–6. https://doi.org/10.1093/gerona/glx061.
Hoffman JM, et al. Tryptophan metabolism is differently regulated between large and small dogs. Geroscience. 2019. https://doi.org/10.1007/s11357-019-00114-x.
Horn M, Knaus W, Kirner L, Steinwidder A. Economic evaluation of longevity in organic dairy cows. Organic Agric. 2012;2:127–43.
Ireland JL, McGowan CM, Clegg PD, Chandler KJ, Pinchbeck GL. A survey of health care and disease in geriatric horses aged 30 years or older. Vet J. 2012;192:57–64. https://doi.org/10.1016/j.tvjl.2011.03.021.
Jimenez AG, Winward J, Beattie U, Cipolli W. Cellular metabolism and oxidative stress as a possible determinant for longevity in small breed and large breed dogs. Plos One. 2018;13:e0195832. https://doi.org/10.1371/journal.pone.0195832.
Justice JN, et al. Senolytics in idiopathic pulmonary fibrosis: results from a first-in-human, open-label, pilot study. EBioMedicine. 2019;40:554–63. https://doi.org/10.1016/j.ebiom.2018.12.052.
Kaeberlein M, Creevy KE, Promislow DE. The dog aging project: translational geroscience in companion animals. Mamm Genome. 2016;27:279–88. https://doi.org/10.1007/s00335-016-9638-7.
Kennedy BK, et al. Geroscience: linking aging to chronic disease. Cell. 2014;159:709–13. https://doi.org/10.1016/j.cell.2014.10.039.
Kennedy U, Sharma A, Phillips CJC. The sheltering of unwanted cattle, experiences in India and implications for cattle industries elsewhere. Animals (Basel). 2018;8. https://doi.org/10.3390/ani8050064.
Kern G, Kemper N, Traulsen I, Henze C, Stamer E, Krieter J. Analysis of different effects on longevity in four sheep breeds of northern Germany. Small Ruminant Res. 2010;90:71–4. https://doi.org/10.1016/j.smallrumres.2010.01.005.
Kilbride AL, Gillman CE, Green LE. A cross-sectional study of the prevalence of lameness in finishing pigs, gilts and pregnant sows and associations with limb lesions and floor types on commercial farms in England. Anim Welf. 2009;18:215–24.
Klein B. Cunningham’s textbook of veterinary physiology. 6th ed: Saunders; 2019.
Korec E, et al. Genus Bison has the biggest sex-related difference in longevity among mammals. Approaches Poult Dairy Vet Sci. 2019;5:1–4. https://doi.org/10.31031/APDV.2019.05.000620.
Kraus WE, et al. 2 years of calorie restriction and cardiometabolic risk (CALERIE): exploratory outcomes of a multicentre, phase 2, randomised controlled trial. Lancet Diabetes Endocrinol. 2019;7:673–83. https://doi.org/10.1016/S2213-8587(19)30151-2.
Liang JB, Paengkoum P. Current status, challenges and the way forward for dairy goat production in Asia - conference summary of dairy goats in Asia Asian-Australas. J Anim Sci. 2019;32:1233–43. https://doi.org/10.5713/ajas.19.0272.
Lim MY, Song EJ, Kang KS, Nam YD. Age-related compositional and functional changes in micro-pig gut microbiome. Geroscience. 2019;41:935–44. https://doi.org/10.1007/s11357-019-00121-y.
Lunney JK. Advances in swine biomedical model genomics. Int J Biol Sci. 2007;3:179–84. https://doi.org/10.7150/ijbs.3.179.
Macfadyen MA, Daniel Z, Kelly S, Parr T, Brameld JM, Murton AJ, et al. The commercial pig as a model of spontaneously-occurring osteoarthritis. BMC Musculoskelet Disord. 2019;20:70. https://doi.org/10.1186/s12891-019-2452-0.
Malher X, Seegers H, Beaudeau F. Culling and mortality in large dairy goat herds managed under intensive conditions in western France. Livest Prod Sci. 2001;71:75–86.
Mattison JA, et al. Caloric restriction improves health and survival of rhesus monkeys. Nat Commun. 2017;8:14063. https://doi.org/10.1038/ncomms14063.
Millikan LE, Boylon JL, Hook RR, Manning PJ. Melanoma in Sinclair swine: a new animal model. J Invest Dermatol. 1974;62:20–30. https://doi.org/10.1111/1523-1747.ep12676714.
Min KJ, Lee CK, Park HN. The lifespan of Korean eunuchs. Curr Biol. 2012;22:R792–3. https://doi.org/10.1016/j.cub.2012.06.036.
Mirzaei H, Suarez JA, Longo VD. Protein and amino acid restriction, aging and disease: from yeast to humans. Trends Endocrinol Metab. 2014;25:558–66. https://doi.org/10.1016/j.tem.2014.07.002.
Morrow LD, et al. Retrospective analysis of post-mortem findings in 1,444 aged donkeys. J Comp Pathol. 2011;144:145–56. https://doi.org/10.1016/j.jcpa.2010.08.005.
Muller DWH, Gaillard JM, Lackey LB, Hatt JM, Clauss M. Comparing life expectancy of three deer species between captive and wild populations. Eur J Wildl Res. 2010;56:205–8.
Munoz CA, Campbell AJD, Hemsworth PH, Doyle RE. Evaluating the welfare of extensively managed sheep. PLoS One. 2019;14:e0218603. https://doi.org/10.1371/journal.pone.0218603.
Nicholatos JW, et al. Cellular energetics and mitochondrial uncoupling in canine aging. Geroscience. 2019;41:229–42. https://doi.org/10.1007/s11357-019-00062-6.
Noppibool U, Koonawootrittriron S, Elzo MA, Suwanasopee T. Factors affecting length of productive life and lifetime production traits in a commercial swine herd in Northern Thailand. Agric Nat Resour. 2016;50:71–4.
Nussey DH, Wilson AJ, Brommer JE. The evolutionary ecology of individual phenotypic plasticity in wild populations. J Evol Biol. 2007;20:831–44. https://doi.org/10.1111/j.1420-9101.2007.01300.x.
O’Neill DG, Church DB, McGreevy PD, Thomson PC, Brodbelt DC. Longevity and mortality of owned dogs in England. Vet J. 2013;198:638–43. https://doi.org/10.1016/j.tvjl.2013.09.020.
Olshansky SJ, Perry D, Miller RA, Butler RN. Pursuing the longevity dividend: scientific goals for an aging world. Ann N Y Acad Sci. 2007;1114:11–3. https://doi.org/10.1196/annals.1396.050.
O'Neill DG, Church DB, McGreevy PD, Thomson PC, Brodbelt DC. Longevity and mortality of cats attending primary care veterinary practices in England. J Feline Med Surg. 2015;17:125–33. https://doi.org/10.1177/1098612X14536176.
Pinnapureddy AR, Stayner C, McEwan J, Baddeley O, Forman J, Eccles MR. Large animal models of rare genetic disorders: sheep as phenotypically relevant models of human genetic disease. Orphanet J Rare Dis. 2015;10:107. https://doi.org/10.1186/s13023-015-0327-5.
Prescott JHD, Lamming GE. The effects of castration on meat production in cattle, sheep and pigs. J Agric Sci. 1964;63:341–57.
Raziq A, Younas M, Kakar MA. Camel- a potential dairy animal in difficult environment. Pakistan J Agric Sci. 2008;45:263–7.
Scholtens MR, Lopez-Villalobos N, Garrick DJ, Blair HT. Heritability of longevity in New Zealand dairy goats. N Z J Anim Sci Prod. 2018;78:11–5.
Seeker LA, et al. Bovine telomere dynamics and the association between telomere length and productive lifespan. Sci Rep. 2018;8:12748. https://doi.org/10.1038/s41598-018-31185-z.
Sharma A, Phillips CJC. Lameness in sheltered cows and its association with cow and shelter attributes. Animals (Basel). 2019;9. https://doi.org/10.3390/ani9060360.
Smith JA. Noninfectious diseases, metabolic diseases, toxicities, and neoplastic diseases of South American camelids. Vet Clin North Am Food Anim Pract. 1989;5:101–43. https://doi.org/10.1016/s0749-0720(15)31006-9.
Steri R, Moioli B, Catillo G, Galli A, Buttazzoni L. Genome-wide association study for longevity in the Holstein cattle population. Animal. 2019;13:1350–7. https://doi.org/10.1017/S1751731118003191.
Tacutu R, et al. Human ageing genomic resources: new and updated databases. Nucleic Acids Res. 2018;46:D1083-D1090. https://doi.org/10.1093/nar/gkx1042.
Tapprest J, et al. Fallen stock data: an essential source of information for quantitative knowledge of equine mortality in France. Equine Vet J. 2017;49:596–602. https://doi.org/10.1111/evj.12664.
Thomas MG, Bennett-Wimbush K, Keisler DH, Loch WE. Plasma concentrations of growth hormone and insulin-like growth factor-I in prepuberal quarter horses and ponies. J Equine Vet Sci. 1998;18:52–5.
Urfer SR, Kaeberlein M. Desexing dogs: a review of the current literature. Animals (Basel). 2019:9. https://doi.org/10.3390/ani9121086.
Urfer SR, Kaeberlein TL, Mailheau S, Bergman PJ, Creevy KE, Promislow DEL, et al. A randomized controlled trial to establish effects of short-term rapamycin treatment in 24 middle-aged companion dogs. Geroscience. 2017;39:117–27. https://doi.org/10.1007/s11357-017-9972-z.
Vaarst M, Roderick S, Lund V, Lockeretz W (2003) Animal health and welfare in organic agriculture. CABI
Valentine BA, Martin JM. Prevalence of neoplasia in llamas and alpacas (Oregon State University, 2001–2006). J Vet Diagn Invest. 2007;19:202–4. https://doi.org/10.1177/104063870701900213.
Wang Y, Zhou J, Wang G, Cai S, Zeng X, Qiao S. Advances in low-protein diets for swine. J Anim Sci Biotechnol. 2018;9:60. https://doi.org/10.1186/s40104-018-0276-7.
Weigl R (2005) Longevity of mammals in captivity: from the living collections of the world. A list of mammalian longevity in captivity. Schweizerbart'sche, E.
Welsh CE, Duz M, Parkin TDH, Marshall JF. Prevalence, survival analysis and multimorbidity of chronic diseases in the general veterinarian-attended horse population of the UK. Prev Vet Med. 2016;131:137–45. https://doi.org/10.1016/j.prevetmed.2016.07.011.
Xu M, et al. Senolytics improve physical function and increase lifespan in old age. Nat Med. 2018;24:1246–56. https://doi.org/10.1038/s41591-018-0092-9.
Youssef G, Wallace WA, Dagleish MP, Cousens C, Griffiths DJ. Ovine pulmonary adenocarcinoma: a large animal model for human lung cancer. Ilar J. 2015;56:99–115. https://doi.org/10.1093/ilar/ilv014.
Zhang Q, Guldbrandtsen B, Thomasen JR, Lund MS, Sahana G. Genome-wide association study for longevity with whole-genome sequencing in 3 cattle breeds. J Dairy Sci. 2016;99:7289–98. https://doi.org/10.3168/jds.2015-10697.
Acknowledgments
We would like to thank all the organizers and attendants of the 14th International Symposium on Neurobiology and Neuroendocrinology of Aging, especially Holly Brown-Borg and Kurt Borg which allowed us to meet and begin our collaboration. Special thanks to Steven Austad for critical reading of the manuscript. We would also like to thank the two reviewers for their insightful comments.
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JMH is supported by the National Institutes of Health K99AG059920.
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Hoffman, J.M., Valencak, T.G. A short life on the farm: aging and longevity in agricultural, large-bodied mammals. GeroScience 42, 909–922 (2020). https://doi.org/10.1007/s11357-020-00190-4
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DOI: https://doi.org/10.1007/s11357-020-00190-4