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Invited Review: The welfare of cull dairy cows

      ABSTRACT

      Purpose

      The purpose of this invited review was to identify and discuss (a) the welfare issues that can occur when cull dairy cows are sent for slaughter, (b) factors that can affect the occurrence and severity of these issues and how they relate to on-farm management decisions, (c) measures that can mitigate these issues, and (d) proposals to improve the welfare of cull dairy cows.

      Sources

      Peer-reviewed literature, book chapters, reports, and guidance documents were sources of information.

      Synthesis

      Severe welfare issues occur when some cull dairy cows that are not fit for the intended journey are transported to slaughter. These issues are even greater if compromised cows are sent to slaughter via an auction market. The decision to send a cull cow to slaughter needs to be made before the cow becomes unfit for the likely journey. If a cow becomes unfit for transport, it should be euthanized on the farm. Some cull cows arrive at slaughter plants and are observed at markets with distended udders, severe lameness, and disease. The numbers of cows with these severe welfare issues could be reduced by improved on-farm decision making about when and how to manage cows with health issues, when to euthanize sick or injured cows, and when a cow is fit for transport and for sale at a market. Dairy producers need to understand the welfare implications of how they manage their cull dairy cows, and that some changes in their management practices are required.

      Conclusions and Applications

      This review identified that research on the assessment of the fitness of cull dairy cows for transport and on the factors that influence their welfare during transport and marketing are required. Research about how to motivate dairy producers to incorporate the welfare implications of their management of cull cows into their culling decisions and how to increase their use of industry recommendations about the care of cull cows are priorities.

      Key words

      INTRODUCTION

      Aim of the Review

      The purpose of this review was to identify and discuss (a) the welfare issues that can occur when cull dairy cows are sent for slaughter, (b) research on factors that can affect the occurrence and severity of these welfare issues and how they relate to on-farm management decisions, (c) measures that have been proposed that can mitigate the occurrence and severity of these welfare issues, and (d) research that would increase understanding of how to improve the welfare of cull dairy cows.

      Complexity of Factors Affecting Culling Decisions

      This review will show how optimally managing the welfare of cull dairy cows requires an understanding of the interrelationships among many different issues (Figure 1). The literature discussed below indicates that some culling decisions are made at a herd level for efficiency reasons, and some are required for individual cows to reduce the risk of suffering. A key animal welfare issue is the fitness of cull dairy cows for transport to slaughter. The literature shows that the fitness of cull dairy cows for transport is influenced by (a) whether on-farm management procedures are adopted to reduce the risk factors for ill health, injury, and poor body condition and (b) whether the cows that develop ill health or injury are culled before their health and condition deteriorate to such an extent that they are no longer fit for transport. The individual circumstances that affect whether a cull cow is fit enough to be transported to slaughter or whether other options, such as (a) treatment for a disease or injury, (b) arrangement for on-farm slaughter, or (c) euthanasia, are preferable to reduce the risk of suffering will be discussed. In addition to an assessment of the health and condition of the cow in relation to fitness for transport, guidance documents suggest that consideration should also be given to whether any on-farm preparation is required before transport. This preparation should consider whether a lactating cow should be dried-off and whether a period of acclimatization to cold external conditions for cows that have been kept indoors would be beneficial. Research to support this guidance is evaluated. Public health literature on food safety issues that would affect the economic viability of transporting a cull cow to slaughter was consulted. This identified that in many cases, there was a risk of drug residues or condemnation of the carcass due to the pathology associated with the reason for culling. Surveys of the management and welfare of cull dairy cows, once they have left the farm, have shown that if a decision is made to send a cull cow to slaughter, the marketing route needs to be considered. Studies have shown that some compromised cull cows will only be fit enough to be transported on a short journey for local slaughter. Although some cull cows will be better able to cope with the journey to slaughter than others, research has shown that there are additional challenges faced by all cull dairy cows that are more severe than those experienced by many beef cattle. As most cull dairy cows are not in prime condition, they will be less able to cope with the stressors associated with transportation and auction markets. For example, cull dairy cows are vulnerable to bruising that is thought to occur from handling and from unsuitable vehicle design and operation. Surveys have shown that some cull cows pass through one or more auction markets or dealer premises before arriving at a slaughter plant, and this journey can sometimes take several days. The welfare implications from marketing cull cows through auction markets on long journeys to slaughter are discussed. The literature on the effects of fasting dairy cows for one or more days is considered because many cull cows sold through auction markets will likely be in a negative energy balance. Some cull cows will already be in poor body condition, and some compromised cows will have difficulty eating. In addition, cull dairy cows will not normally receive feed during a journey, and many will not be offered adequate feed while at an auction market. After several days of feed restriction, additional activity associated with prolonged standing and inadequate rest, the progression of disease processes, and their aggravation by transportation and handling, it is inevitable but preventable that some cull dairy cows will arrive at a slaughter plant in poor condition.
      Figure 1
      Figure 1Potential production, health, welfare, and food-safety issues that can influence culling decisions and the choice of marketing route when dairy cows are transported to slaughter. The diagram shows the range of potential production, health, welfare, and food-safety issues that can influence on-farm management decisions that are made by dairy producers when they cull a dairy cow (yellow); transport decisions (green) that should be influenced by the fitness of the cull cow; issues that can affect the welfare of cull cows at an auction market (gray); and potential negative outcomes at the time of slaughter (blue) that can be influenced by the health and condition of the cull cow. Red arrows indicate the potential marketing routes for cull cows on their journey to slaughter. Potential relationships between factors are shown by connecting black lines.

      Factors Affecting the Welfare of Cull Dairy Cows

      On the basis of the reported pathology associated with the reasons for condemnation of some carcasses as not fit for consumption, the review will contend that some cull dairy cows are not fit for transportation when they are sent for slaughter. It is suggested that the risk of cull cows suffering while still on the farm and during transportation to slaughter can vary considerably depending on the reasons for culling. On the basis of the likely associated pathophysiological changes, most cull cows that are not fit for transportation will be those that become sick or injured and are removed from the herd before they would have been removed due to a decline in their productivity. Research has shown that some cows culled for economic reasons such as reduced milk production or reduced fertility might also have chronic disease or be in poor physical condition. However, it will be asserted that their ability to cope with some journeys will still be better than those that are, for example, sick or severely lame. Cows culled while they are still in good health and good physical condition should be better able to cope with transportation and auction markets. Research on animal transportation has shown that if the conditions of transport, management, and handling are suboptimal, all types of cull cows can potentially experience welfare issues. The review considers the literature that identifies the main factors that affect the welfare of all cull dairy cows that are not experienced to the same extent by beef cattle. These include the potential susceptibility of cull dairy cows to thermal extremes; the type and frequency of handling; whether the cows have been dried-off or are still lactating and require milking; the duration of journeys; and time spent at markets and holding areas (where there might not be adequate opportunities to obtain feed, water, and rest).
      The review will assert that the risk of suffering in cull dairy cows is affected by on-farm management decisions. The factors that can reduce the risk of adverse welfare outcomes in cull dairy cows are procedures (a) for making early decisions on culling before the health and physical condition of cows deteriorate; (b) for assessing the fitness of cows for transportation; (c) for treatment and care or on-farm euthanasia of cows that are not fit for transport; (d) for assessing whether cows should be sent for slaughter if they are not likely to pass food safety requirements for human consumption due to drug residues or pathology; (e) for assessing the marketing route suitable for cull cows based on their health and condition; (f) for preparing cull cows for the journey to slaughter; and (g) for reducing the prevalence of conditions likely to make cull cows unfit for transportation.
      This review discusses the factors that influence the welfare of cull cows on farm and during their transport and marketing on route to slaughter and how these factors and the welfare of the cows are influenced by management decisions made by dairy producers. The literature cited on culling, euthanasia, fitness for transport, and transportation and marketing of dairy cows is listed in Table 1.
      Table 1Literature cited on culling, euthanasia, fitness for transport, and transportation and marketing of dairy cows
      CullingEuthanasiaFitness for transportTransportation and marketing
      • Armengol R.
      • Fraile L.
      Descriptive study for culling and mortality in five high-producing Spanish dairy cattle farms (2006–2016)..
      • Koralesky K.E.
      • Fraser D.
      Use of on-farm emergency slaughter for dairy cows in British Columbia..
      • Ahola J.K.
      • Foster H.A.
      • VanOverbeke D.L.
      • Jensen K.S.
      • Wilson R.L.
      • Glaze Jr., J.B.
      • Fife T.E.
      • Gray C.W.
      • Nash S.A.
      • Panting R.R.
      • Rimbey N.R.
      Survey of quality defects in market beef and dairy cows and bulls sold through livestock auction markets in the western United States: I. Incidence rates..
      ,
      • Ahola J.K.
      • Foster H.A.
      • VanOverbeke D.L.
      • Jensen K.S.
      • Wilson R.L.
      • Glaze Jr., J.B.
      • Fife T.E.
      • Gray C.W.
      • Nash S.A.
      • Panting R.R.
      • Rimbey N.R.
      Quality defects in market beef and dairy cows and bulls sold through livestock auction markets in the western United States: II. Relative effects on selling price..
      )
      • Bulitta S.F.
      • Aradom S.
      • Gebresenbet G.
      Effect of transport time of up to 12 hours on welfare of cows and bulls..
      • Bascom S.S.
      • Young A.J.
      A summary of the reasons why farmers cull cows..

      Shearer, J. K., and J. P. Reynolds. 2011. Euthanasia techniques for dairy cattle. Pages 331–339 in Dairy Production Medicine. C. A. Risco and P. M. Retamal, ed. John Wiley & Sons, NJ. 10.1002/9780470960554.ch25.

      • Akkina J.
      • Estberg L.
      Use of slaughter condemnation data to detect cattle health events in near real-time..
      • Edge M.K.
      • Barnett J.L.
      Development of animal welfare standards for the livestock transport industry: Process, challenges, and implementation..
      • Beaudeau F.
      • Seegers H.
      • Ducrocq V.
      • Fourichon C.
      • Bareille N.
      Effect of health disorders on culling in dairy cows: A review and a critical discussion..
      • Thomsen P.T.
      • Kjeldsen A.M.
      • Sørensen J.T.
      • Houe H.
      Mortality (including euthanasia) among Danish dairy cows (1990–2001)..

      American Association of Bovine Practitioners. 2019. Guidelines for Transportation and Fitness-To-Travel Recommendations for Cattle. Accessed Sep. 22, 2020. https://www.aabp.org/Resources/AABP_Guidelines/transportationguidelines-2019.pdf.

      Fisher, M., and B. Rothwell. 1999. Humane marketing and transportation of cull dairy cows. Adv. Dairy Technol. 11:135–139. https://wcds.ualberta.ca/2017/08/22/1999/.

      • Booth C.J.
      • Warnick L.D.
      • Gröhn Y.T.
      • Maizon D.O.
      • Guard C.L.
      • Janssen D.
      Effect of lameness on culling in dairy cows..
      • Turner P.V.
      • Doonan G.
      Developing on-farm euthanasia plans..
      • Cockram M.S.
      Fitness of animals for transport to slaughter..
      ,

      Cockram, M. 2020. Condition of animals on arrival at the abattoir and their management during lairage. Pages 49–77 in The Slaughter of Farmed Animals: Practical Ways of Enhancing Animal Welfare. T. Grandin and M. Cockram, ed. CABI Publ., Wallingford, Oxon, UK. 10.1079/9781789240573.0049.

      )
      • González L.A.
      • Schwartzkopf-Genswein K.
      • Bryan M.
      • Silasi R.
      • Brown F.
      Relationships between transport conditions and welfare outcomes during commercial long haul transport of cattle in North America..
      • Wagner B.K.
      • Cramer M.C.
      • Fowler H.N.
      • Varnell H.L.
      • Dietsch A.M.
      • Proudfoot K.L.
      • Shearer J.
      • Correa M.
      • Pairis-Garcia M.
      Determination of dairy cattle euthanasia criteria and analysis of barriers to humane euthanasia in the United States: The veterinarian perspective..
      • Dahl-Pedersen K.
      • Foldager L.
      • Herskin M.S.
      • Houe H.
      • Thomsen P.T.
      Lameness scoring and assessment of fitness for transport in dairy cows: Agreement among and between farmers, veterinarians and livestock drivers..
      ,
      • Dahl-Pedersen K.
      • Herskin M.S.
      • Houe H.
      • Thomsen P.T.
      Risk factors for deterioration of the clinical condition of cull dairy cows during transport to slaughter..
      ,
      • Dahl-Pedersen K.
      • Herskin M.S.
      • Houe H.
      • Thomsen P.T.
      A descriptive study of the clinical condition of cull dairy cows before transport to slaughter..
      )
      • Hong H.
      • Lee E.
      • Lee I.H.
      • Lee S.
      Effects of transport stress on physiological responses and milk production in lactating dairy cows..
      • Cha E.
      • Hertl J.A.
      • Schukken Y.H.
      • Tauer L.W.
      • Welcome F.L.
      • Gröhn Y.T.
      The effect of repeated episodes of bacteria-specific clinical mastitis on mortality and culling in Holstein dairy cows..
      • Edge M.K.
      • Barnett J.L.
      Development of animal welfare standards for the livestock transport industry: Process, challenges, and implementation..
      • Lambooij E.
      • van der Werf J.T.N.
      • Reimert H.G.M.
      • Hindle V.A.
      Compartment height in cattle transport vehicles..
      • Chiumia D.
      • Chagunda M.G.G.
      • MacRae A.I.
      • Roberts D.J.
      Predisposing factors for involuntary culling in Holstein-Friesian dairy cows..

      European Commission. (Directorate for Health and Food Audits and Analysis; Directorate-General for Health and Food Safety) 2016. Overview Report on Systems to Prevent the Transport of Unfit Animals in the European Union. Accessed Sep. 22, 2020. https://publications.europa.eu/en/publication-detail/-/publication/2bdfe42c-e33f-409e-8f02-4f0308205ede/language-en doi 10.2875/669512.

      Livestock Marketing Association. 2018. Guide to Animal Handling Employee Training for Livestock Auction Markets. Accessed Mar. 26, 2021. https://lmaweb.com/wp-content/uploads/2020/12/LMAhandlingprogram2018Edition.pdf.

      • De Vries A.
      Symposium review: Why revisit dairy cattle productive lifespan?.
      • Grandin T.
      Perspectives on transportation issues: The importance of having physically fit cattle and pigs..
      • Malena M.
      • Voslářová E.
      • Kozák A.
      • Bělobrádek P.
      • Bedáňová I.
      • Steinhauser L.
      • Večerek V.
      Comparison of mortality rates in different categories of pigs and cattle during transport for slaughter..
      • De Vries A.
      • Marcondes M.I.
      Review: Overview of factors affecting productive lifespan of dairy cows..
      • Harris M.K.
      • Eastwood L.C.
      • Boykin C.A.
      • Arnold A.N.
      • Gehring K.B.
      • Hale D.S.
      • Kerth C.R.
      • Griffin D.B.
      • Savell J.W.
      • Belk K.E.
      • Woerner D.R.
      • Hasty J.D.
      • Delmore Jr., R.J.
      • Martin J.N.
      • Lawrence T.E.
      • McEvers T.J.
      • VanOverbeke D.L.
      • Mafi G.G.
      • Pfeiffer M.M.
      • Schmidt T.B.
      • Maddock R.J.
      • Johnson D.D.
      • Carr C.C.
      • Scheffler J.M.
      • Pringle T.D.
      • Stelzleni A.M.
      National Beef Quality Audit–2016: Transportation, mobility, live cattle, and carcass assessments of targeted producer-related characteristics that affect value of market cows and bulls, their carcasses, and associated by-products..
      • Sánchez-Hidalgo M.
      • Bravo V.
      • Gallo C.
      Behavior and health indicators to assess cull cow’s welfare in livestock markets..
      • Deyrup C.L.
      • Southern K.J.
      • Cornett J.A.
      • Shultz C.E.
      • Cera D.A.
      Examining the occurrence of residues of flunixin meglumine in cull dairy cows by use of the flunixin cull cow survey..
      • Herskin M.S.
      • Hels A.
      • Anneberg I.
      • Thomsen P.T.
      Livestock drivers’ knowledge about dairy cow fitness for transport—A Danish questionnaire survey..
      • Schuetze S.J.
      • Schwandt E.F.
      • Maghirang R.G.
      • Thomson D.U.
      Review: Transportation of commercial finished cattle and animal welfare considerations..
      • Edwards-Callaway L.
      • Walker J.
      • Tucker C.B.
      Culling decisions and dairy cattle welfare during transport to slaughter in the United States..
      • Hoe F.G.H.
      • Ruegg P.L.
      Opinions and practices of Wisconsin dairy producers about biosecurity and animal well-being..
      • Strappini A.C.
      • Frankena K.
      • Metz J.H.M.
      • Gallo B.
      • Kemp B.
      Prevalence and risk factors for bruises in Chilean bovine carcasses..
      ,
      • Strappini A.C.
      • Metz J.H.M.
      • Gallo C.
      • Frankena K.
      • Vargas R.
      • De Freslon I.
      • Kemp B.
      Bruises in culled cows: When, where and how are they inflicted?.
      )
      • Esslemont R.J.
      • Kossaibati M.A.
      Culling in 50 dairy herds in England..
      • Ingham B.
      Abattoir survey of dental defects in cull cows..
      • Tarrant P.V.
      • Kenny F.J.
      • Harrington D.
      The effect of stocking density during 4 hour transport to slaughter on behaviour, blood constituents and carcass bruising in Friesian steers..
      • Fetrow J.
      • Nordlund K.V.
      • Norman H.D.
      Invited review: Culling: Nomenclature, definitions, and recommendations..
      • Magalhães-Sant’Ana M.
      • More S.J.
      • Morton D.B.
      • Hanlon A.J.
      Challenges facing the veterinary profession in Ireland: 3. Emergency and casualty slaughter certification..
      • Vogel K.D.
      • Claus J.R.
      • Grandin T.
      • Oetzel G.R.
      • Schaefer D.M.
      Effect of water and feed withdrawal and health status on blood and serum components, body weight loss, and meat and carcass characteristics of Holstein slaughter cows..
      • Hadley G.L.
      • Wolf C.A.
      • Harsh S.B.
      Dairy cattle culling patterns, explanations, and implications..
      • Moorman A.K.G.
      • Duffield T.F.
      • Godkin M.A.
      • Kelton D.F.
      • Rau J.
      • Haley D.B.
      Associations between the general condition of culled dairy cows and selling price at Ontario auction markets..
      • Haine D.
      • Cue R.
      • Sewalem A.
      • Wade K.
      • Lacroix R.
      • Lefebvre D.
      • Rushton J.
      • Arsenault J.
      • Bouchard É.
      • Dubuc J.
      Culling from the actors’ perspectives—Decision-making criteria for culling in Québec dairy herds enrolled in a veterinary preventive medicine program..
      ,
      • Haine D.
      • Delgado H.
      • Cue R.
      • Sewalem A.
      • Wade K.
      • Lacroix R.
      • Lefebvre D.
      • Arsenault J.
      • Bouchard É.
      • Dubuc J.
      Marginal structural cox model to estimate the causal effect of clinical mastitis on Québec dairy cow culling risk..
      )

      National Milk Producers Federation. 2020. Animal Care Reference Manual Version 4 2020–2022. Accessed Sep. 22, 2020. https://nationaldairyfarm.com/wp-content/uploads/2020/09/FARM_Animal-Care-4-Manual_Layout_FINAL_091520_SinglePages.pdf.

      • Langford F.M.
      • Stott A.W.
      Culled early or culled late: Economic decisions and risks to welfare in dairy cows..
      • Nicholson J.D.W.
      • Nicholson K.L.
      • Frenzel L.L.
      • Maddock R.J.
      • Delmore Jr., R.J.
      • Lawrence T.E.
      • Henning W.R.
      • Pringle T.D.
      • Johnson D.D.
      • Paschal J.C.
      • Gill R.J.
      • Cleere J.J.
      • Carpenter B.B.
      • Machen R.V.
      • Banta J.P.
      • Hale D.S.
      • Griffin D.B.
      • Savell J.W.
      Survey of transportation procedures, management practices, and health assessment related to quality, quantity, and value for market beef and dairy cows and bulls..
      • Lehenbauer T.W.
      • Oltjen J.W.
      Dairy cow culling strategies: Making economical culling decisions..

      Office International des Epizooties. 2011. Transport of animals by land. Chapter 7.3 in Terrestrial Animal Health Code. Accessed Sep. 22, 2020. https://www.oie.int/fileadmin/Home/eng/Health_standards/tahc/2018/en_chapitre_aw_land_transpt.htm.

      • McDougall S.
      • Bryan M.A.
      • Tiddy R.M.
      Effect of treatment with the nonsteroidal antiinflammatory meloxicam on milk production, somatic cell count, probability of re-treatment, and culling of dairy cows with mild clinical mastitis..
      • Rezac D.J.
      • Thomson D.U.
      • Siemens M.G.
      • Prouty F.L.
      • Reinhardt C.D.
      • Bartle S.J.
      A survey of gross pathologic conditions in cull cows at slaughter in the Great Lakes region of the United States..
      • Monti G.
      • Tenhagen B.-A.
      • Heuwieser W.
      Culling policies in dairy herds. A review..
      • Stojkov J.
      • Bowers G.
      • Draper M.
      • Duffield T.
      • Duivenvoorden P.
      • Groleau M.
      • Haupstein D.
      • Peters R.
      • Pritchard J.
      • Radom C.
      • Sillett N.
      • Skippon W.
      • Trépanier H.
      • Fraser D.
      Hot topic: Management of cull dairy cows—Consensus of an expert consultation in Canada..
      ,
      • Stojkov J.
      • von Keyserlingk M.A.G.
      • Duffield T.
      • Fraser D.
      Fitness for transport of cull dairy cows at livestock markets..
      ,
      • Stojkov J.
      • von Keyserlingk M.A.G.
      • Duffield T.
      • Fraser D.
      Management of cull dairy cows: Culling decisions, duration of transport, and effect on cow condition..
      )
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      • Klingborg D.J.
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      • Looper M.
      • Falk D.
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      DairyBeef: Maximizing quality and Profits—A consistent food safety message..
      • Warnock J.P.
      • Caple I.W.
      • Halpin C.G.
      • McQueen C.S.
      Metabolic changes associated with the ‘downer’ condition in dairy cows at abattoirs..
      • Oltenacu P.A.
      • Broom D.M.
      The impact of genetic selection for increased milk yield on the welfare of dairy cows..

      Western Dairy Science Inc. 2004. Humane handling of dairy cattle; Standards for the transportation of unfit cull animals. West. Dairy Sci. Inc. Accessed Sep. 22, 2020. http://www.agromedia.ca/HumaneHandling/HumaneHandling.pdf.

      • Orpin P.G.
      • Esslemont R.J.
      Culling and wastage in dairy herds: An update on incidence and economic impact in dairy herds in the UK..
      • White T.L.
      • Moore D.A.
      Reasons for whole carcass condemnations of cattle in the United States and implications for producer education and veterinary intervention..
      • Orpin P.G.
      • Sibley R.J.
      Counting the culls and costing the casualties—Not all cull cows are the same..
      • Overton M.W.
      • Dhuyvetter K.C.
      Symposium review: An abundance of replacement heifers: What is the economic impact of raising more than are needed?.
      • Pinedo P.J.
      • Daniels A.
      • Shumaker J.
      • De Vries A.
      Dynamics of culling for Jersey, Holstein, and Jersey × Holstein crossbred cows in large multibreed dairy herds..
      • Roche S.M.
      • Renaud D.L.
      • Genore R.
      • Shock D.A.
      • Bauman C.
      • Croyle S.
      • Barkema H.W.
      • Dubuc J.
      • Keefe G.P.
      • Kelton D.F.
      Canadian national dairy study: Describing Canadian dairy producer practices and perceptions surrounding cull cow management..
      • Rogers C.A.
      • Fitzgerald A.C.
      • Carr M.A.
      • Covey B.R.
      • Thomas J.D.
      • Looper M.L.
      On-farm management decisions to improve beef quality of market dairy cows..
      • Seegers H.
      • Beaudeau F.
      • Fourichon C.
      • Bareille N.
      Reasons for culling in French Holstein cows..
      • Shemeis A.R.
      • Liboriussen T.
      • Bech Andersen B.
      • Abdallah O.Y.
      Changes in carcass and meat quality traits of Danish Friesian cull cows with the increase of their age and body condition..
      • Stelzleni A.M.
      • Patten L.E.
      • Johnson D.D.
      • Calkins C.R.
      • Gwartney B.L.
      Benchmarking carcass characteristics and muscles from commercially identified beef and dairy cull cow carcasses for Warner-Bratzler shear force and sensory attributes..
      • Tsuruta S.
      • Misztal I.
      • Lawlor T.J.
      Changing definition of productive life in US Holsteins: Effect on genetic correlations..

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      • VanBaale M.J.
      • Galland J.C.
      • Hyatt D.R.
      • Milliken G.A.
      A survey of dairy producer practices and attitudes pertaining to dairy market beef food safety..
      • Walsh S.W.
      • Williams E.J.
      • Evans A.C.O.
      A review of the causes of poor fertility in high milk producing dairy cows..

      METHODS USED IN THE REVIEW

      Peer-reviewed publications on the culling of dairy cows were searched in Scopus and added to existing personal databases of publications on animal welfare, dairy cattle, and transportation. A Google and library search identified relevant book chapters, reports, and guidance documents. The reference section of each publication was used to find further publications and to identify topics that could potentially affect the welfare of cull dairy cows. A large number of publications on the culling of dairy cows were identified, and representative publications were consulted to inform understanding of the decision-making process affecting the culling of dairy cows and the reasons for culling. Relevant research on the welfare of cull dairy cows was identified, but much of this specific research was relatively recent and has not yet provided a comprehensive body of literature. Where reports and guidance documents on the management of cull dairy cows identified specific welfare issues that had not been comprehensively investigated, publications on these topics in dairy cows were examined to provide a basis for further research and interim recommendations on the management of the welfare of cull dairy cows. The selection of which publications to include, the relevance and significance of the information reported, and the extrapolation of existing research to this topic were value-related and academic judgments.

      CULLING

      Animal Welfare Significance of Culling Rate

      Culling is the removal of a cow from the dairy herd. It occurs when a producer considers that a cow has reached a point where she is no longer an economic asset, and it is preferable to replace her with a younger animal (such as a first-lactation heifer) that has greater potential productivity (
      • Hadley G.L.
      • Wolf C.A.
      • Harsh S.B.
      Dairy cattle culling patterns, explanations, and implications..
      ). Unfortunately, there is variation in the use of the term “culling,” and it has been used to refer to all cows that leave the herd regardless of the reason. As shown in Figure 2, dairy cows can leave the herd when they are transported alive from the farm: for sale at an auction market, direct to a place of slaughter, for salvage (rendered or used for purposes other than for human food), or for transfer to another dairy herd for breeding or milk production (
      • Fetrow J.
      • Nordlund K.V.
      • Norman H.D.
      Invited review: Culling: Nomenclature, definitions, and recommendations..
      ;

      USDA. 2018. Dairy 2014. Health and Management Practices on U.S. Dairy Operations, 2014. Accessed Sep. 22, 2020. https://www.aphis.usda.gov/animal_health/nahms/dairy/downloads/dairy14/Dairy14_dr_PartIII.pdf.

      ). The term “cull” can sometimes include those cows that die on the farm as a result of unassisted death (mortality), euthanasia, or on-farm slaughter (for family or employee consumption or where the carcass is sent to a slaughter establishment;
      • Fetrow J.
      • Nordlund K.V.
      • Norman H.D.
      Invited review: Culling: Nomenclature, definitions, and recommendations..
      ). From an animal welfare perspective, the cull dairy cows of most significance are those that are at greatest risk of suffering, i.e., those that are transported alive from the farm (and are not fit for transport or experience a prolonged and difficult journey to slaughter), those that have to be killed on the farm (euthanasia or on-farm slaughter) because they are suffering due to disease or injury, and those that die on the farm without their suffering having been ended by euthanasia (
      • Thomsen P.T.
      • Kjeldsen A.M.
      • Sørensen J.T.
      • Houe H.
      Mortality (including euthanasia) among Danish dairy cows (1990–2001)..
      ). When interpreting the welfare implications of culling, statistics that differentiate between these categories of culling are more useful than those that combine them into one category (
      • Orpin P.G.
      • Sibley R.J.
      Counting the culls and costing the casualties—Not all cull cows are the same..
      ). In addition, the welfare implications can be more readily assessed when recording systems provide an opportunity to record the primary, secondary, and sometimes the tertiary reasons why a cow has been selected for culling (
      • Bascom S.S.
      • Young A.J.
      A summary of the reasons why farmers cull cows..
      ). From an animal welfare perspective, an examination of the reasons for culling enables an assessment of the risk of suffering that might have been associated with specific diseases, injuries, and body condition, in relation to their management (
      • Edwards-Callaway L.
      • Walker J.
      • Tucker C.B.
      Culling decisions and dairy cattle welfare during transport to slaughter in the United States..
      ).
      Figure 2
      Figure 2Simplified diagram showing potential options for the management of cull dairy cows. The arrows indicate potential sequences in the culling of dairy cows depending on whether the culling decision was a planned removal from the herd or whether it was a consequence of disease or injury. If the removal of the cow from the herd was a planned decision and the cow was fit for transport, the options available for slaughter are indicated together with options for selling the cow at an auction market or directly to another farm. If the cow experiences disease or injury and does not die on farm before a management decision is made, the options, depending on the severity of the condition, are removal from the herd or treatment. If a decision is made to remove the cow from the herd and the cow is not fit for transport, then as indicated, it should be slaughtered or euthanized on farm. However, even if assessed as fit for transport, some cull cows will not be suitable to be sold at an auction market or transported on a long journey to slaughter and should only be sent for local slaughter.
      The herd culling rate is the percentage of the number of cows (milking and dry) culled over 12 mo divided by the average population of cows in the herd (milking and dry;
      • Fetrow J.
      • Nordlund K.V.
      • Norman H.D.
      Invited review: Culling: Nomenclature, definitions, and recommendations..
      ). In 2013, the percentage of cows removed from dairy herds in the USA (excluding cows that died) was 34% (

      USDA. 2018. Dairy 2014. Health and Management Practices on U.S. Dairy Operations, 2014. Accessed Sep. 22, 2020. https://www.aphis.usda.gov/animal_health/nahms/dairy/downloads/dairy14/Dairy14_dr_PartIII.pdf.

      ). Some people have attributed a high culling rate in dairy herds and the associated decreased cow longevity, fertility, and health to the genetic and management changes required to produce high milk yields in intensive dairy production (
      • Oltenacu P.A.
      • Broom D.M.
      The impact of genetic selection for increased milk yield on the welfare of dairy cows..
      ). A high and sustained culling rate could be an indicator of poor welfare status or management problems. However, it can be difficult to interpret a culling rate on its own as additional information is required to understand the factors affecting a specific herd. Each farm has its own culling policy, and the percentage of cows (a) that a producer plans to cull (sometimes referred to as voluntary culling); (b) that a producer did not originally intend to cull, but culling was necessary due to health or injury (sometimes referred to as involuntary culling); (c) euthanized; or (d) that die unassisted varies between farms (
      • Armengol R.
      • Fraile L.
      Descriptive study for culling and mortality in five high-producing Spanish dairy cattle farms (2006–2016)..
      ). A high planned or voluntary culling rate might indicate good management practice if it was undertaken to improve the genetic potential of the herd by replacing poor-performing cows with heifers with greater potential productivity (
      • Overton M.W.
      • Dhuyvetter K.C.
      Symposium review: An abundance of replacement heifers: What is the economic impact of raising more than are needed?.
      ). In contrast, a high culling rate undertaken for specific health reasons, such as mastitis and lameness, could indicate that there are farm management issues that need to be addressed. Alternatively, a high culling rate might also indicate a diligent early culling policy designed to arrange for the transport of cows to slaughter before they become unfit for transport. Therefore, without information on the specific reasons for culling, the overall culling rate for an individual farm can be difficult to interpret.

      Reasons for Culling

      Economic and Management Factors

      Culling is a complex management decision, and culling decisions vary from farm to farm depending on economics and the specific situation affecting the herd (
      • Lehenbauer T.W.
      • Oltjen J.W.
      Dairy cow culling strategies: Making economical culling decisions..
      ;
      • Monti G.
      • Tenhagen B.-A.
      • Heuwieser W.
      Culling policies in dairy herds. A review..
      ). Dairy cows are culled, i.e., removed from the herd, for several reasons, including low milk production, poor breeding performance, and health problems (
      • Bascom S.S.
      • Young A.J.
      A summary of the reasons why farmers cull cows..
      ). Some culling decisions taken by producers are planned or nonurgent decisions (sometimes referred to as voluntary culling) that are influenced by economics and strategic management decisions (
      • Monti G.
      • Tenhagen B.-A.
      • Heuwieser W.
      Culling policies in dairy herds. A review..
      ). These decisions are affected by factors such as milk price, cull cow value, replacement costs, housing capacity, and plans for genetic improvement and herd size (
      • Bascom S.S.
      • Young A.J.
      A summary of the reasons why farmers cull cows..
      ;
      • Beaudeau F.
      • Seegers H.
      • Ducrocq V.
      • Fourichon C.
      • Bareille N.
      Effect of health disorders on culling in dairy cows: A review and a critical discussion..
      ;
      • Langford F.M.
      • Stott A.W.
      Culled early or culled late: Economic decisions and risks to welfare in dairy cows..
      ;
      • Edwards-Callaway L.
      • Walker J.
      • Tucker C.B.
      Culling decisions and dairy cattle welfare during transport to slaughter in the United States..
      ). Unsatisfactory reproductive performance and low milk production are common primary causes of planned or nonurgent culling. In a survey of the reasons for culling cows from dairy herds enrolled on a milk recording program in Canada from 2014 to 2019, 21% of culls were due to reproduction issues and 9% to poor milk production (). Cows with low milk yield, poor fertility, and health issues that necessitate their early removal from the herd after only 1 or 2 lactations reduce the economic performance of a dairy herd (
      • Lehenbauer T.W.
      • Oltjen J.W.
      Dairy cow culling strategies: Making economical culling decisions..
      ;
      • De Vries A.
      Symposium review: Why revisit dairy cattle productive lifespan?.
      ). The longer that a producer can keep a cow that produces a calf each year, avoids mastitis and lameness, and produces good milk yields of sufficient quality, the greater the profitability that can be obtained from that animal (
      • Esslemont R.J.
      • Kossaibati M.A.
      Culling in 50 dairy herds in England..
      ). However, the average productive life of dairy cows in the USA tends to be less than 3 yr (
      • De Vries A.
      • Marcondes M.I.
      Review: Overview of factors affecting productive lifespan of dairy cows..
      ), with few cows reaching old age, i.e., older than 6 lactations (
      • Tsuruta S.
      • Misztal I.
      • Lawlor T.J.
      Changing definition of productive life in US Holsteins: Effect on genetic correlations..
      ). Cows in early lactation have high milk production, are profitable, and are less likely to be culled than cows in late lactation (

      USDA. 2018. Dairy 2014. Health and Management Practices on U.S. Dairy Operations, 2014. Accessed Sep. 22, 2020. https://www.aphis.usda.gov/animal_health/nahms/dairy/downloads/dairy14/Dairy14_dr_PartIII.pdf.

      ). If a cow with high milk production is removed in early lactation, it is likely to have been due to a serious health problem, such as mastitis or lameness (
      • Seegers H.
      • Beaudeau F.
      • Fourichon C.
      • Bareille N.
      Reasons for culling in French Holstein cows..
      ;
      • Pinedo P.J.
      • Daniels A.
      • Shumaker J.
      • De Vries A.
      Dynamics of culling for Jersey, Holstein, and Jersey × Holstein crossbred cows in large multibreed dairy herds..
      ).

      Sickness, Injury, and Lameness

      Some causes of culling are unplanned events (sometimes referred to as involuntary culling). They occur in extreme circumstances when ill health or injury becomes the main reason that it is no longer economical to keep a cow in the herd or the cow would continue to experience significant suffering if it remained in the herd (
      • Chiumia D.
      • Chagunda M.G.G.
      • MacRae A.I.
      • Roberts D.J.
      Predisposing factors for involuntary culling in Holstein-Friesian dairy cows..
      ). The decision to cull a cow with a health issue can be affected by the availability of heifer replacements, the amount of milk that the cow is producing, and whether it is pregnant (
      • Langford F.M.
      • Stott A.W.
      Culled early or culled late: Economic decisions and risks to welfare in dairy cows..
      ). Major health reasons for culling are those conditions that are not only painful but also affect reproductive performance and milk production (
      • Cha E.
      • Hertl J.A.
      • Schukken Y.H.
      • Tauer L.W.
      • Welcome F.L.
      • Gröhn Y.T.
      The effect of repeated episodes of bacteria-specific clinical mastitis on mortality and culling in Holstein dairy cows..
      ;
      • Haine D.
      • Delgado H.
      • Cue R.
      • Sewalem A.
      • Wade K.
      • Lacroix R.
      • Lefebvre D.
      • Arsenault J.
      • Bouchard É.
      • Dubuc J.
      Marginal structural cox model to estimate the causal effect of clinical mastitis on Québec dairy cow culling risk..
      ;
      • Petersson-Wolfe C.
      • Leslie K.E.
      • Swartz T.H.
      An update on the effect of clinical mastitis on the welfare of dairy cows and potential therapies..
      ), including mastitis (13% of culls), injury to the udder or teats (5% of culls), and those that affect the ability of the cows to walk, including feet and leg problems (8.6% of culls) and arthritis (0.4% of culls; ). Sickness is an important category of reasons for culling (6% of culls) with specific conditions, milk fever, pneumonia, and displaced abomasum, representing 0.5, 0.4, and 0.4% of culls, respectively (). Unfortunately, as discussed in the following, many cull cows with these types of conditions are not fit for transport to slaughter but are nevertheless sent to slaughter. Cows that are culled because they are sick, lame, weak, or injured will likely be suffering while on the farm and are more likely to suffer during transport than cull cows that are fitter (
      • Cockram M.S.
      Fitness of animals for transport to slaughter..
      ).

      Animal Welfare Significance of Culling Decisions

      Depending on the reasons for culling, dairy cows can be transported from the farm in various states of physical health and body condition, and this will affect their fitness for transport (
      • Cockram M.S.
      Fitness of animals for transport to slaughter..
      ). The condition of the animal should influence the options chosen for the marketing of cull cows, further treatment, or euthanasia. Proactive early culling can reduce the risk of cattle experiencing welfare issues on farm (
      • Orpin P.G.
      • Esslemont R.J.
      Culling and wastage in dairy herds: An update on incidence and economic impact in dairy herds in the UK..
      ) and during transport and marketing (
      • Walker J.B.
      • Roman-Muniz I.
      • Edwards-Callaway L.
      Timely euthanasia in the United States dairy industry—Challenges and a path forward..
      ). It avoids further loss of body condition (
      • Alawneh J.I.
      • Stevenson M.A.
      • Williamson N.B.
      • Lopez-Villalobos N.
      • Otley T.
      The effect of clinical lameness on liveweight in a seasonally calving, pasture-fed dairy herd..
      ) and increases in the severity of health conditions, such as lameness (
      • Leach K.A.
      • Tisdall D.A.
      • Bell N.J.
      • Main D.C.J.
      • Green L.E.
      The effects of early treatment for hindlimb lameness in dairy cows on four commercial UK farms..
      ). In addition, it will result in better meat quality (
      • Shemeis A.R.
      • Liboriussen T.
      • Bech Andersen B.
      • Abdallah O.Y.
      Changes in carcass and meat quality traits of Danish Friesian cull cows with the increase of their age and body condition..
      ) and a reduced risk of condemnation of the carcass as not fit for human consumption (
      • White T.L.
      • Moore D.A.
      Reasons for whole carcass condemnations of cattle in the United States and implications for producer education and veterinary intervention..
      ). Although chronic disease and poor body condition can be associated with poor fertility (
      • Walsh S.W.
      • Williams E.J.
      • Evans A.C.O.
      A review of the causes of poor fertility in high milk producing dairy cows..
      ) and low milk production (
      • Fourichon C.
      • Seegers H.
      • Bareille N.
      • Beaudeau F.
      Effects of disease on milk production in the dairy cow: A review..
      ), most dairy cows that are culled primarily for these production reasons will be fitter and better able to cope with transportation than those where the primary reason for culling is sickness or lameness (
      • Dahl-Pedersen K.
      • Herskin M.S.
      • Houe H.
      • Thomsen P.T.
      Risk factors for deterioration of the clinical condition of cull dairy cows during transport to slaughter..
      ).
      Many factors interact to affect the culling decisions made by dairy producers. Some are economic, but others are related to animal health, milk quality, and animal welfare (
      • De Vries A.
      • Marcondes M.I.
      Review: Overview of factors affecting productive lifespan of dairy cows..
      ). Further research is required to understand the priorities and motivations that result in a decision to cull a cow. For example, one study on the factors that influenced culling decisions in Québec, Canada (
      • Haine D.
      • Cue R.
      • Sewalem A.
      • Wade K.
      • Lacroix R.
      • Lefebvre D.
      • Rushton J.
      • Arsenault J.
      • Bouchard É.
      • Dubuc J.
      Culling from the actors’ perspectives—Decision-making criteria for culling in Québec dairy herds enrolled in a veterinary preventive medicine program..
      ) showed that dairy producers’ primary focus was on the quality of the milk produced, and secondary considerations were milk production and fertility. Farm advisers classified as having an economic focus considered the pregnancy status of the cow, fertility issues, and the stage of gestation. Other farm advisers also considered cow welfare and the withdrawal periods for milk and meat.

      JOURNEY TO SLAUGHTER

      Research on the factors that affect the welfare of beef cattle when they are transported to slaughter has been reviewed (
      • Schuetze S.J.
      • Schwandt E.F.
      • Maghirang R.G.
      • Thomson D.U.
      Review: Transportation of commercial finished cattle and animal welfare considerations..
      ), but other than considerations on fitness for transport, in comparison, less is known about the other factors affecting the welfare of cull dairy cows during transport. Further studies on how cull dairy cows behaviorally and physiologically respond to transportation and the various factors that influence the welfare implications of transport, including stocking density, deck height, thermal conditions, prolonged periods of feed and water restriction, road conditions and driving style, and journey duration are required.

      JOURNEY TO SLAUGHTER: FITNESS FOR TRANSPORT

      Potential for Adverse Animal Welfare Outcomes

      Transportation is stressful for dairy cows (
      • Hong H.
      • Lee E.
      • Lee I.H.
      • Lee S.
      Effects of transport stress on physiological responses and milk production in lactating dairy cows..
      ) and can, in some circumstances, represent significant challenges even for fit and healthy cull dairy cows (
      • Bulitta S.F.
      • Aradom S.
      • Gebresenbet G.
      Effect of transport time of up to 12 hours on welfare of cows and bulls..
      ). Health issues such as lameness, injury, and disease are major causes for the culling of dairy cows (
      • Hadley G.L.
      • Wolf C.A.
      • Harsh S.B.
      Dairy cattle culling patterns, explanations, and implications..
      ), and challenges associated with transportation are greater for cull cows that are weak, diseased, or injured (
      • Cockram M.S.
      Fitness of animals for transport to slaughter..
      ). Cows that are sick, injured, or lame are most likely already experiencing welfare issues, such as pain, before they are transported (

      Cockram, M. S., and B. O. Hughes. 2018. Health and disease. Pages 141–159 in Animal Welfare. 3rd ed. M. C. Appleby, I. A. S. Olsson, F. Galindo, ed. CABI, Wallingford, UK. 10.1079/9781786390202.0141.

      ). In this condition, they are less able to cope with the extra challenges associated with transport, such as getting on and off the vehicle, maintaining stability, and avoiding fatigue; feed and water restriction; and extreme thermal environments (
      • Cockram M.S.
      Fitness of animals for transport to slaughter..
      ,

      Cockram, M. 2020. Condition of animals on arrival at the abattoir and their management during lairage. Pages 49–77 in The Slaughter of Farmed Animals: Practical Ways of Enhancing Animal Welfare. T. Grandin and M. Cockram, ed. CABI Publ., Wallingford, Oxon, UK. 10.1079/9781789240573.0049.

      ). The specific reasons for culling a cow will affect its physical condition, and whether it is diseased or injured will affect its fitness for transport (
      • Cockram M.S.
      Fitness of animals for transport to slaughter..
      ). Dairy cows need to be culled before they become weak, debilitated, and not fit for transport to slaughter (
      • Stojkov J.
      • Bowers G.
      • Draper M.
      • Duffield T.
      • Duivenvoorden P.
      • Groleau M.
      • Haupstein D.
      • Peters R.
      • Pritchard J.
      • Radom C.
      • Sillett N.
      • Skippon W.
      • Trépanier H.
      • Fraser D.
      Hot topic: Management of cull dairy cows—Consensus of an expert consultation in Canada..
      ). Cull cows sent for slaughter with pre-existing conditions are more likely to die in transit, become nonambulatory, or be euthanized on arrival than those that are healthy (
      • Cockram M.S.
      Fitness of animals for transport to slaughter..
      ). In the Czech Republic,
      • Malena M.
      • Voslářová E.
      • Kozák A.
      • Bělobrádek P.
      • Bedáňová I.
      • Steinhauser L.
      • Večerek V.
      Comparison of mortality rates in different categories of pigs and cattle during transport for slaughter..
      recorded a mortality rate of cull dairy cows during transport or shortly after arrival at the slaughter plant of 0.04%. This was greater than that in fattened cattle (0.007%), and the mortality rate was greater in dairy cows from farms that were more than 100 km from the slaughter plant than in those that had been transported on a shorter journey. In the USA between 2005 and 2007, 0.8% of cull dairy cows sent to slaughter were condemned at ante mortem inspection, 62% of these cows were condemned because of mortality, and 35% of these condemnations were due to a nonambulatory or moribund condition (
      • White T.L.
      • Moore D.A.
      Reasons for whole carcass condemnations of cattle in the United States and implications for producer education and veterinary intervention..
      ).

      Legal Regulations and Codes of Practice

      In many parts of the world, there are either legal regulations or codes of practice that are designed to prevent the transportation of animals that are not fit for the intended journey (
      • Edge M.K.
      • Barnett J.L.
      Development of animal welfare standards for the livestock transport industry: Process, challenges, and implementation..
      ). All countries that are members of the Office International des Epizooties have agreed to a code for the transport of animals that specifies the types of conditions that would make a cull dairy cow unfit for transport. These include cows that are sick, injured, weak, disabled, or fatigued; those that cannot bear weight on each leg; and those that cannot be moved without causing them additional suffering (

      Office International des Epizooties. 2011. Transport of animals by land. Chapter 7.3 in Terrestrial Animal Health Code. Accessed Sep. 22, 2020. https://www.oie.int/fileadmin/Home/eng/Health_standards/tahc/2018/en_chapitre_aw_land_transpt.htm.

      ). The

      American Association of Bovine Practitioners. 2019. Guidelines for Transportation and Fitness-To-Travel Recommendations for Cattle. Accessed Sep. 22, 2020. https://www.aabp.org/Resources/AABP_Guidelines/transportationguidelines-2019.pdf.

      guidelines for transportation and fitness-to-travel recommendations for cattle contain guidance not to transport animals with distended udders, ambulatory issues, or conditions that will not pass pre-slaughter inspection. “Special needs/compromised” cattle, such as those with mobility issues, low BCS, or suspected or confirmed disease issues, should be identified and provided with additional protection on the trailer and be loaded on the back of the trailer to make it easier for them to be unloaded first (

      American Association of Bovine Practitioners. 2019. Guidelines for Transportation and Fitness-To-Travel Recommendations for Cattle. Accessed Sep. 22, 2020. https://www.aabp.org/Resources/AABP_Guidelines/transportationguidelines-2019.pdf.

      ). Those that have conditions that increase the likelihood of becoming nonambulatory should not be transported, or if transported, they should be placed in a separate compartment without any other animal contact (

      American Association of Bovine Practitioners. 2019. Guidelines for Transportation and Fitness-To-Travel Recommendations for Cattle. Accessed Sep. 22, 2020. https://www.aabp.org/Resources/AABP_Guidelines/transportationguidelines-2019.pdf.

      ).

      Food Safety Requirements

      An important consideration for a producer when determining whether a cull cow should be transported to slaughter and potentially needlessly exposed to welfare issues is whether it will pass the food safety requirements at slaughter. There is a high risk that part of or the whole of the carcass of a cull dairy cow will be condemned as unfit for human consumption, and this risk is greater for cull dairy cows than for beef cattle. In the USA, in 2017, 1.7% of the cull dairy cows that were sent to slaughter were condemned as unfit for human consumption for the following main reasons: dead on arrival, moribund, emaciated, central nervous system disease, mastitis, pneumonia, pyrexia, and septicemia (
      • Akkina J.
      • Estberg L.
      Use of slaughter condemnation data to detect cattle health events in near real-time..
      ). Dairy cows should not be sent for slaughter and potentially exposed to the associated welfare issues if there is a reasonable risk that they will not pass the food safety requirements for withdrawal periods of medication or for pathological conditions (

      National Milk Producers Federation. 2020. Animal Care Reference Manual Version 4 2020–2022. Accessed Sep. 22, 2020. https://nationaldairyfarm.com/wp-content/uploads/2020/09/FARM_Animal-Care-4-Manual_Layout_FINAL_091520_SinglePages.pdf.

      ). However, the potential financial returns to the producer from sending cull cows to slaughter are such that they may not be concerned about the risk of having a cow condemned. Even if cull cows fail antemortem inspection, a dairy producer might profit from the sale of the hide and avoid the costs associated with the disposal of the body (
      • VanBaale M.J.
      • Galland J.C.
      • Hyatt D.R.
      • Milliken G.A.
      A survey of dairy producer practices and attitudes pertaining to dairy market beef food safety..
      ). A survey of Canadian dairy producers showed that 93% considered that drug withdrawal status was an important issue when making a decision on culling (
      • Roche S.M.
      • Renaud D.L.
      • Genore R.
      • Shock D.A.
      • Bauman C.
      • Croyle S.
      • Barkema H.W.
      • Dubuc J.
      • Keefe G.P.
      • Kelton D.F.
      Canadian national dairy study: Describing Canadian dairy producer practices and perceptions surrounding cull cow management..
      ). This is a relevant consideration as nonsteroidal anti-inflammatory drugs are used to control the pain, inflammation, and pyrexia associated with many of the health conditions that can lead to the culling of dairy cows (
      • McDougall S.
      • Bryan M.A.
      • Tiddy R.M.
      Effect of treatment with the nonsteroidal antiinflammatory meloxicam on milk production, somatic cell count, probability of re-treatment, and culling of dairy cows with mild clinical mastitis..
      ). The use of these drugs is beneficial for cow welfare while the cow is still on the farm, and there is a reasonable prospect of recovery. However, if the appropriate drug withdrawal period has not been followed, there is a risk that residues may still be present at the time of slaughter (
      • Deyrup C.L.
      • Southern K.J.
      • Cornett J.A.
      • Shultz C.E.
      • Cera D.A.
      Examining the occurrence of residues of flunixin meglumine in cull dairy cows by use of the flunixin cull cow survey..
      ).

      Cull Cows Unfit for Transport but Nevertheless Sent to Slaughter

      • Walker J.B.
      • Roman-Muniz I.
      • Edwards-Callaway L.
      Timely euthanasia in the United States dairy industry—Challenges and a path forward..
      estimated that each year more than half a million cull dairy cows that are unfit for transport are sent to slaughter in the USA. Surveys of the condition of cull cows at slaughter plants in the USA show the presence of pathological conditions in some cull cows that clearly indicate that they should not have been transported to slaughter. In one survey,
      • Nicholson J.D.W.
      • Nicholson K.L.
      • Frenzel L.L.
      • Maddock R.J.
      • Delmore Jr., R.J.
      • Lawrence T.E.
      • Henning W.R.
      • Pringle T.D.
      • Johnson D.D.
      • Paschal J.C.
      • Gill R.J.
      • Cleere J.J.
      • Carpenter B.B.
      • Machen R.V.
      • Banta J.P.
      • Hale D.S.
      • Griffin D.B.
      • Savell J.W.
      Survey of transportation procedures, management practices, and health assessment related to quality, quantity, and value for market beef and dairy cows and bulls..
      reported that 1% of the cull dairy cows arrived in a moribund condition (but this was not the case for fattened beef cattle). Five percent of the cull dairy cows examined antemortem had an extremely emaciated BCS, 2.7% were severely lame, 7% had foot abnormalities, 2% had an abscess in the knee/hock that was considered most likely caused by arthritis, 9% had mastitis, and 0.4% had either a tooth or jaw abscess or actinomycosis (lumpy jaw). Cull cows with these types of conditions would likely have had a reduced ability to obtain feed and water and respond to external events such as vehicle motion or interactions with other animals.
      In some cases, cull cows could arrive unfit at a slaughter plant because their health deteriorated during the journey. In Denmark,
      • Dahl-Pedersen K.
      • Herskin M.S.
      • Houe H.
      • Thomsen P.T.
      Risk factors for deterioration of the clinical condition of cull dairy cows during transport to slaughter..
      examined cull dairy cows on farm before loading and again at unloading at a slaughter plant and showed that the severity of lameness can increase and cows can be injured during a journey (mean duration 3 h, range 0.5–8.5 h). Some cows may have had pathology that was not readily apparent before loading, and they may not have had any obvious clinical signs of disease or injury for a competent stockperson or transporter to recognize. However,
      • Dahl-Pedersen K.
      • Herskin M.S.
      • Houe H.
      • Thomsen P.T.
      A descriptive study of the clinical condition of cull dairy cows before transport to slaughter..
      identified that 75% of the cull dairy cows that were transported to slaughter from 20 commercial Danish dairy herds had one or more signs of a clinical condition before transport. Many of the conditions recorded in cull cows at antemortem and postmortem inspection would have been present on the farm and would have been identifiable.

      Pathophysiology of Health Conditions in Cull Dairy Cows

      There has not been extensive research on how cows with different health issues respond to transportation. However, consideration of the pathophysiological implications of ill health and injury can identify the potential physical and physiological challenges that can occur during transportation and the potential for suffering (
      • Cockram M.S.
      Fitness of animals for transport to slaughter..
      ). The reasons reported for the postmortem condemnation of cull dairy cows show that many cull cows are transported to slaughter with major pathology that will have caused pain, systemic illness, or reduced physiological function, e.g., to respond to changes in environmental temperature and physical movement.
      • Rezac D.J.
      • Thomson D.U.
      • Siemens M.G.
      • Prouty F.L.
      • Reinhardt C.D.
      • Bartle S.J.
      A survey of gross pathologic conditions in cull cows at slaughter in the Great Lakes region of the United States..
      surveyed the prevalence and severity of gross lesions in cull dairy and beef cows (87% of the cows were Holsteins) that were slaughtered at a commercial abattoir in the USA. Almost 3% of the cows were condemned as not fit for human consumption. The causes of these condemnations included septicemia, abscess or pyemia, pericarditis, peritonitis, and pneumonia. They reported that 19% of the cull cows had a severe liver abscess and 10% had severe consolidation of a lung lobe or pleural adhesions to the thoracic cavity. Cull cows with severe metritis (inflammation of the uterus) can have clinical signs associated with a systemic illness (dullness, fever, and pain;
      • Sheldon I.M.
      • Lewis G.S.
      • LeBlanc S.
      • Gilbert R.O.
      Defining postpartum uterine disease in cattle..
      ;
      • Stojkov J.
      • von Keyserlingk M.A.G.
      • Marchant-Forde J.
      • Weary D.M.
      Assessment of visceral pain associated with metritis in dairy cows..
      ), thereby making the cow unfit for transport. Some cull dairy cows with cancer eye or ocular neoplasia are sent to auction markets and slaughter plants. If the condition is severe, these cows are not fit for transport, will likely be condemned as not fit for human consumption, will experience discomfort and pain (
      • Williams D.L.
      Welfare issues in farm animal ophthalmology..
      ), and should be euthanized rather than transported to slaughter (
      • Walker J.B.
      • Roman-Muniz I.
      • Edwards-Callaway L.
      Timely euthanasia in the United States dairy industry—Challenges and a path forward..
      ).

      Lameness

      Lameness can result in decreased milk production (
      • Warnick L.D.
      • Janssen D.
      • Guard C.L.
      • Gröhn Y.T.
      The effect of lameness on milk production in dairy cows..
      ) and lower reproductive performance (
      • Hernandez J.
      • Shearer J.K.
      • Webb D.W.
      Effect of lameness on the calving-to-conception interval in dairy cows..
      ) and is a common reason for culling. Depending on the stage of lactation and the type of lesion, there can be a delay between the recognition of lameness in a cow and culling (
      • Booth C.J.
      • Warnick L.D.
      • Gröhn Y.T.
      • Maizon D.O.
      • Guard C.L.
      • Janssen D.
      Effect of lameness on culling in dairy cows..
      ), and this could result in an increase in the severity of lameness. As most lameness is caused by pain (
      • Flower F.C.
      • Sedlbauer M.
      • Carter E.
      • von Keyserlingk M.A.G.
      • Sanderson D.J.
      • Weary D.M.
      Analgesics improve the gait of lame dairy cattle..
      ), severe lameness in cull dairy cows transported to slaughter (
      • Harris M.K.
      • Eastwood L.C.
      • Boykin C.A.
      • Arnold A.N.
      • Gehring K.B.
      • Hale D.S.
      • Kerth C.R.
      • Griffin D.B.
      • Savell J.W.
      • Belk K.E.
      • Woerner D.R.
      • Hasty J.D.
      • Delmore Jr., R.J.
      • Martin J.N.
      • Lawrence T.E.
      • McEvers T.J.
      • VanOverbeke D.L.
      • Mafi G.G.
      • Pfeiffer M.M.
      • Schmidt T.B.
      • Maddock R.J.
      • Johnson D.D.
      • Carr C.C.
      • Scheffler J.M.
      • Pringle T.D.
      • Stelzleni A.M.
      National Beef Quality Audit–2016: Transportation, mobility, live cattle, and carcass assessments of targeted producer-related characteristics that affect value of market cows and bulls, their carcasses, and associated by-products..
      ) or at an auction market (
      • Stojkov J.
      • von Keyserlingk M.A.G.
      • Duffield T.
      • Fraser D.
      Fitness for transport of cull dairy cows at livestock markets..
      ) is a serious welfare issue. Animals with painful foot lesions are more reluctant to bear weight on their feet than healthy animals (
      • Flower F.C.
      • Weary D.M.
      Gait assessment in dairy cattle..
      ), and pressure on a lesion causes additional pain (
      • Dyer R.M.
      • Neerchal N.K.
      • Tasch U.
      • Wu Y.
      • Dyer P.
      • Rajkondawar P.G.
      Objective determination of claw pain and its relationship to limb locomotion score in dairy cattle..
      ;
      • Flower F.C.
      • Sedlbauer M.
      • Carter E.
      • von Keyserlingk M.A.G.
      • Sanderson D.J.
      • Weary D.M.
      Analgesics improve the gait of lame dairy cattle..
      ). Therefore, walking during loading, unloading, and handling, and foot placements in response to vehicle movements during transport, will likely be painful. During transport, dairy cows have to adjust their footing at regular intervals to maintain their balance in response to vehicular movements and are at risk of falling over (
      • Bulitta S.F.
      • Aradom S.
      • Gebresenbet G.
      Effect of transport time of up to 12 hours on welfare of cows and bulls..
      ). The condition of lame animals during a journey is likely to deteriorate as exercise associated with prolonged standing and responses to other animals and vehicular movement to maintain stability have the potential to aggravate the lameness. As a lame cow is more likely to adopt a lying posture (
      • Ito K.
      • von Keyserlingk M.A.G.
      • LeBlanc S.J.
      • Weary D.M.
      Lying behavior as an indicator of lameness in dairy cows..
      ), but the other cattle on a vehicle are likely to remain standing, if it goes down, the cow will be susceptible to injury from trampling (
      • Tarrant P.V.
      • Kenny F.J.
      • Harrington D.
      The effect of stocking density during 4 hour transport to slaughter on behaviour, blood constituents and carcass bruising in Friesian steers..
      ).
      Although one study showed that producers, veterinarians, and livestock drivers were able to identify lame dairy cows to a similar extent, there were differences in assessment of whether the cows were fit for transport based on the severity of the lameness (
      • Dahl-Pedersen K.
      • Foldager L.
      • Herskin M.S.
      • Houe H.
      • Thomsen P.T.
      Lameness scoring and assessment of fitness for transport in dairy cows: Agreement among and between farmers, veterinarians and livestock drivers..
      ). In Denmark, an on-farm veterinary examination of cull dairy cows that had been selected by farmers for transport to slaughter classified more than 1% of these cows as not fit for transport because they were severely lame (i.e., obviously lame on one or more legs and unable, unwilling, or very reluctant to bear weight on the affected leg) and 31% were classified as lame (
      • Dahl-Pedersen K.
      • Herskin M.S.
      • Houe H.
      • Thomsen P.T.
      A descriptive study of the clinical condition of cull dairy cows before transport to slaughter..
      ). Severely lame cull cows that are not selected for treatment should be euthanized on farm rather than transported to slaughter, and no lame cows should be sent to an auction market. However, in a study of cull dairy cows sold through auction markets in Ontario, Canada, 73% were observed to be obviously lame with an unacceptable gait (
      • Moorman A.K.G.
      • Duffield T.F.
      • Godkin M.A.
      • Kelton D.F.
      • Rau J.
      • Haley D.B.
      Associations between the general condition of culled dairy cows and selling price at Ontario auction markets..
      ).
      • Stojkov J.
      • von Keyserlingk M.A.G.
      • Duffield T.
      • Fraser D.
      Fitness for transport of cull dairy cows at livestock markets..
      observed severe lameness in about 7% of cull dairy cows at markets in British Columbia, Canada.
      • Ahola J.K.
      • Foster H.A.
      • VanOverbeke D.L.
      • Jensen K.S.
      • Wilson R.L.
      • Glaze Jr., J.B.
      • Fife T.E.
      • Gray C.W.
      • Nash S.A.
      • Panting R.R.
      • Rimbey N.R.
      Survey of quality defects in market beef and dairy cows and bulls sold through livestock auction markets in the western United States: I. Incidence rates..
      reported that 4% of the cull dairy cows sold through several auction markets in the USA had a locomotion score that indicated that they were severely lame and “not capable of effectively navigating an auction market without tremendous increased risk of further injury and potentially becoming nonambulatory.”

      Low BCS

      In the US National Beef Quality Audit 2016, 9% of the cull dairy cows sent for slaughter were classified as thin with a BCS of 1 or 1.5 (
      • Harris M.K.
      • Eastwood L.C.
      • Boykin C.A.
      • Arnold A.N.
      • Gehring K.B.
      • Hale D.S.
      • Kerth C.R.
      • Griffin D.B.
      • Savell J.W.
      • Belk K.E.
      • Woerner D.R.
      • Hasty J.D.
      • Delmore Jr., R.J.
      • Martin J.N.
      • Lawrence T.E.
      • McEvers T.J.
      • VanOverbeke D.L.
      • Mafi G.G.
      • Pfeiffer M.M.
      • Schmidt T.B.
      • Maddock R.J.
      • Johnson D.D.
      • Carr C.C.
      • Scheffler J.M.
      • Pringle T.D.
      • Stelzleni A.M.
      National Beef Quality Audit–2016: Transportation, mobility, live cattle, and carcass assessments of targeted producer-related characteristics that affect value of market cows and bulls, their carcasses, and associated by-products..
      ) and the percentages of cull dairy cows sold through several auction markets in the USA with a BCS of 1 or 1.5 were 1.7 and 12%, respectively (
      • Ahola J.K.
      • Foster H.A.
      • VanOverbeke D.L.
      • Jensen K.S.
      • Wilson R.L.
      • Glaze Jr., J.B.
      • Fife T.E.
      • Gray C.W.
      • Nash S.A.
      • Panting R.R.
      • Rimbey N.R.
      Survey of quality defects in market beef and dairy cows and bulls sold through livestock auction markets in the western United States: I. Incidence rates..
      ).
      • Stojkov J.
      • von Keyserlingk M.A.G.
      • Duffield T.
      • Fraser D.
      Management of cull dairy cows: Culling decisions, duration of transport, and effect on cow condition..
      recorded that 9% of the cull dairy cows studied on Canadian farms had a BCS ≤2 but nevertheless were sent to a market. Whether they were sent to a market was influenced by the veterinary practice that provided advice to the farm.
      A high-producing dairy cow uses its body fat reserves as well as the energy in its feed to meet the energy demands of lactation. If a cow does not fully regain the body fat that is lost during lactation, there is a cumulative decrease in body fat reserves during subsequent lactations. The net effect is that by the time that a dairy cow is culled from the herd, it can have a low BCS that reflects the low body fat reserves. A low BCS may also occur following health issues (
      • Bewley J.M.
      • Schutz M.M.
      An interdisciplinary review of body condition scoring for dairy cattle..
      ). Most dairy producers do not have a specific additional feeding protocol for cull dairy cows before sending them to slaughter so that the carcass characteristics are improved. Although additional feeding can improve the quality of the meat (
      • Stelzleni A.M.
      • Patten L.E.
      • Johnson D.D.
      • Calkins C.R.
      • Gwartney B.L.
      Benchmarking carcass characteristics and muscles from commercially identified beef and dairy cull cow carcasses for Warner-Bratzler shear force and sensory attributes..
      ), the economic returns on the additional feed costs to improve body condition and the value of the carcass have not been demonstrated (
      • Rogers C.A.
      • Fitzgerald A.C.
      • Carr M.A.
      • Covey B.R.
      • Thomas J.D.
      • Looper M.L.
      On-farm management decisions to improve beef quality of market dairy cows..
      ). However, if there was sufficient financial incentive, some dairy producers have reported that they would consider extra feeding of cows before they left their farm to improve body condition (
      • VanBaale M.J.
      • Galland J.C.
      • Hyatt D.R.
      • Milliken G.A.
      A survey of dairy producer practices and attitudes pertaining to dairy market beef food safety..
      ).
      The evidence that a low BCS compromises animal welfare is not strong, but thinness may increase the risk of discomfort in cold environments (
      • Roche J.R.
      • Friggens N.C.
      • Kay J.K.
      • Fisher M.W.
      • Stafford K.J.
      • Berry D.P.
      Body condition score and its association with dairy cow productivity, health, and welfare..
      ). Thin animals are also more likely to be injured or bruised during transport and have an increased risk of becoming nonambulatory (
      • Grandin T.
      Perspectives on transportation issues: The importance of having physically fit cattle and pigs..
      ;
      • Strappini A.C.
      • Frankena K.
      • Metz J.H.M.
      • Gallo B.
      • Kemp B.
      Prevalence and risk factors for bruises in Chilean bovine carcasses..
      ). More evidence is required on the welfare implications of transporting and marketing emaciated/thin cows, including the implications of body condition on their stability, weakness and vigor, and response to periods of feed restriction and exposure to cold conditions.

      Potential for Deterioration of Pre-Existing Conditions when Cull Cows Are Sold at Auction Markets

      If compromised dairy cows are sent to an auction market or transported on long journeys to slaughter, they are likely to continue to experience pain and discomfort, there is a risk of deterioration of the animal during the journey, and pre-existing conditions are likely to be aggravated by transportation. They are frequently sent to a market because the economic returns from selling cull cows at a market can be high (
      • Moorman A.K.G.
      • Duffield T.F.
      • Godkin M.A.
      • Kelton D.F.
      • Rau J.
      • Haley D.B.
      Associations between the general condition of culled dairy cows and selling price at Ontario auction markets..
      ;

      USDA. 2018. Dairy 2014. Health and Management Practices on U.S. Dairy Operations, 2014. Accessed Sep. 22, 2020. https://www.aphis.usda.gov/animal_health/nahms/dairy/downloads/dairy14/Dairy14_dr_PartIII.pdf.

      ). However, cull dairy cows that are severely lame or obviously sick are often sold at a discounted price (
      • Ahola J.K.
      • Foster H.A.
      • VanOverbeke D.L.
      • Jensen K.S.
      • Wilson R.L.
      • Glaze Jr., J.B.
      • Fife T.E.
      • Gray C.W.
      • Nash S.A.
      • Panting R.R.
      • Rimbey N.R.
      Quality defects in market beef and dairy cows and bulls sold through livestock auction markets in the western United States: II. Relative effects on selling price..
      ). These authors suggested that this was “probably associated with the likelihood of an animal dying or becoming non-ambulatory before slaughter, being condemned, or yielding a poor quality carcass at slaughter.” To ensure humane handling and transportation,

      Fisher, M., and B. Rothwell. 1999. Humane marketing and transportation of cull dairy cows. Adv. Dairy Technol. 11:135–139. https://wcds.ualberta.ca/2017/08/22/1999/.

      proposed that producers should deliver their compromised cull cows directly to slaughter. Where there is no local slaughter facility for cull cows, it was suggested that dairy producers should cooperate to assemble a load of cull cows for direct transport to the nearest slaughter plant.

      Reasons for Sending Unfit Cows to Slaughter

      Further research is required on how dairy producers incorporate the welfare implications of their actions in their management of cull cows and how to increase their use of industry recommendations on the care of cull cows. The potential reasons why unfit cull cows are transported to slaughter and what measures could reduce the numbers of cows that arrive at slaughter plants in poor condition have been considered in several publications, including those by
      • White T.L.
      • Moore D.A.
      Reasons for whole carcass condemnations of cattle in the United States and implications for producer education and veterinary intervention..
      , the

      European Commission. (Directorate for Health and Food Audits and Analysis; Directorate-General for Health and Food Safety) 2016. Overview Report on Systems to Prevent the Transport of Unfit Animals in the European Union. Accessed Sep. 22, 2020. https://publications.europa.eu/en/publication-detail/-/publication/2bdfe42c-e33f-409e-8f02-4f0308205ede/language-en doi 10.2875/669512.

      ,
      • Edwards-Callaway L.
      • Walker J.
      • Tucker C.B.
      Culling decisions and dairy cattle welfare during transport to slaughter in the United States..
      , and
      • Walker J.B.
      • Roman-Muniz I.
      • Edwards-Callaway L.
      Timely euthanasia in the United States dairy industry—Challenges and a path forward..
      . These issues are listed and discussed below.

      a. Lack of Awareness that It Is a Problem

      (
      • White T.L.
      • Moore D.A.
      Reasons for whole carcass condemnations of cattle in the United States and implications for producer education and veterinary intervention..
      ). The focus of the dairy industry is on milk production rather than on the beef produced by cull dairy cows (
      • Douphrate D.I.
      • Hagevoort G.R.
      • Nonnenmann M.W.
      • Lunner Kolstrup C.
      • Reynolds S.J.
      • Jakob M.
      • Kinsel M.
      The dairy industry: A brief description of production practices, trends, and farm characteristics around the world..
      ;
      • Britt J.H.
      • Cushman R.A.
      • Dechow C.D.
      • Dobson H.
      • Humblot P.
      • Hutjens M.F.
      • Jones G.A.
      • Ruegg P.S.
      • Sheldon I.M.
      • Stevenson J.S.
      Invited review: Learning from the future—A vision for dairy farms and cows in 2067..
      ). In one survey in the USA, less than 15% of the dairy producers had visited an establishment where cull cows are slaughtered (
      • VanBaale M.J.
      • Galland J.C.
      • Hyatt D.R.
      • Milliken G.A.
      A survey of dairy producer practices and attitudes pertaining to dairy market beef food safety..
      ). Unlike the poultry, swine, and beef sectors, where there can be a degree of vertical integration between the farm of production and the slaughter plant (

      Martinez, S. W. 1999. Vertical coordination in the pork and broiler industries: Implications for pork and chicken products. Agricultural Economic Report No. 777. USDA. Accessed Mar. 26, 2021. https://www.ers.usda.gov/publications/pub-details/?pubid=41010.

      ;
      • Mulrony B.R.
      • Chaddad F.R.
      Strategic alliances in the US beef supply chain..
      ), dairy producers do not normally obtain feedback on the condition of their own animals at slaughter (

      Lowe, M., and G. Gereffi. 2009. A value chain analysis of the US beef and dairy industries. Center on Globalization, Governance & Competitiveness, Duke University. Pages 1–55. Accessed Mar. 26, 2021. https://gvcc.duke.edu/cggclisting/a-value-chain-analysis-of-the-u-s-beef-and-dairy-industries/.

      ). This is unfortunate as this might influence how they manage their cull cows (
      • Moore D.A.
      • Kirk J.H.
      • Klingborg D.J.
      • Garry F.
      • Wailes W.
      • Dalton J.
      • Busboom J.
      • Sams R.W.
      • Poe M.
      • Payne M.
      • Marchello J.
      • Looper M.
      • Falk D.
      • Wright T.
      DairyBeef: Maximizing quality and Profits—A consistent food safety message..
      ). Increased communication is required between relevant stakeholders, e.g., veterinarians, producers, farm advisers, transporters, and meat producers, and their respective associations of the results of various audits on the prevalence of health and welfare concerns, the implications of marketing routes, and the treatment of cull cows on route to slaughter (
      • White T.L.
      • Moore D.A.
      Reasons for whole carcass condemnations of cattle in the United States and implications for producer education and veterinary intervention..
      ). This will assist in the identification of training needs of the relevant stakeholders (

      European Commission. (Directorate for Health and Food Audits and Analysis; Directorate-General for Health and Food Safety) 2016. Overview Report on Systems to Prevent the Transport of Unfit Animals in the European Union. Accessed Sep. 22, 2020. https://publications.europa.eu/en/publication-detail/-/publication/2bdfe42c-e33f-409e-8f02-4f0308205ede/language-en doi 10.2875/669512.

      ).

      b. Lack of Financial Incentives and Disincentives to Change Practices

      (
      • VanBaale M.J.
      • Galland J.C.
      • Hyatt D.R.
      • Milliken G.A.
      A survey of dairy producer practices and attitudes pertaining to dairy market beef food safety..
      ;
      • White T.L.
      • Moore D.A.
      Reasons for whole carcass condemnations of cattle in the United States and implications for producer education and veterinary intervention..
      ;
      • Edwards-Callaway L.
      • Walker J.
      • Tucker C.B.
      Culling decisions and dairy cattle welfare during transport to slaughter in the United States..
      ). A survey of US dairy producers by
      • VanBaale M.J.
      • Galland J.C.
      • Hyatt D.R.
      • Milliken G.A.
      A survey of dairy producer practices and attitudes pertaining to dairy market beef food safety..
      reported that the income that producers received from the slaughter of cull dairy cows was important, but the authors concluded that as it only represented a small proportion of a dairy producer’s total income, their financial incentive to change their practices was limited. The main motivating factors that could change their practices in relation to the sending of cull cows to slaughter were the introduction of premiums or deductions from slaughter establishments and subsidies for euthanizing sick or injured cows (
      • VanBaale M.J.
      • Galland J.C.
      • Hyatt D.R.
      • Milliken G.A.
      A survey of dairy producer practices and attitudes pertaining to dairy market beef food safety..
      ). In the USA, there is no significant disincentive for selling or purchasing compromised cull dairy cows. A producer might not experience a financial penalty from the slaughter plant for sending a cull cow to slaughter that is subsequently condemned (
      • VanBaale M.J.
      • Galland J.C.
      • Hyatt D.R.
      • Milliken G.A.
      A survey of dairy producer practices and attitudes pertaining to dairy market beef food safety..
      ;
      • Edwards-Callaway L.
      • Walker J.
      • Tucker C.B.
      Culling decisions and dairy cattle welfare during transport to slaughter in the United States..
      ). Producers balance the potential financial return from transporting an animal that is not in good health with the potential risk of suffering to the animal, financial loss from mortality, partial or total condemnation of the carcass for human consumption, and any regulatory enforcement or poor public perception of their practices (
      • Magalhães-Sant’Ana M.
      • More S.J.
      • Morton D.B.
      • Hanlon A.J.
      Challenges facing the veterinary profession in Ireland: 3. Emergency and casualty slaughter certification..
      ;
      • Cockram M.S.
      Fitness of animals for transport to slaughter..
      ). Certification schemes (
      • Main D.C.J.
      • Mullan S.
      • Atkinson C.
      • Cooper M.
      • Wrathall J.H.M.
      • Blokhuis H.J.
      Best practice framework for animal welfare certification schemes..
      ) and industry codes of practice (

      National Milk Producers Federation. 2020. Animal Care Reference Manual Version 4 2020–2022. Accessed Sep. 22, 2020. https://nationaldairyfarm.com/wp-content/uploads/2020/09/FARM_Animal-Care-4-Manual_Layout_FINAL_091520_SinglePages.pdf.

      ) can provide market incentives to improve the management of cull dairy cows.

      c. Lack of Regulatory Enforcement

      (

      European Commission. (Directorate for Health and Food Audits and Analysis; Directorate-General for Health and Food Safety) 2016. Overview Report on Systems to Prevent the Transport of Unfit Animals in the European Union. Accessed Sep. 22, 2020. https://publications.europa.eu/en/publication-detail/-/publication/2bdfe42c-e33f-409e-8f02-4f0308205ede/language-en doi 10.2875/669512.

      ). Legal regulations on the fitness of animals for transport and their enforcement, on farm, in transit, at markets, and at slaughter can reduce the risk of suffering in cull cows (

      European Commission. (Directorate for Health and Food Audits and Analysis; Directorate-General for Health and Food Safety) 2016. Overview Report on Systems to Prevent the Transport of Unfit Animals in the European Union. Accessed Sep. 22, 2020. https://publications.europa.eu/en/publication-detail/-/publication/2bdfe42c-e33f-409e-8f02-4f0308205ede/language-en doi 10.2875/669512.

      ). In the absence of legal regulations and their effective enforcement, a producer might decide to risk transporting a compromised cull cow to attempt to obtain the maximum financial return and avoid the costs of undertaking on-farm euthanasia and subsequent carcass disposal (
      • Walker J.B.
      • Roman-Muniz I.
      • Edwards-Callaway L.
      Timely euthanasia in the United States dairy industry—Challenges and a path forward..
      ). In many countries, if an unfit animal arrives at a slaughter plant, there are procedures for the collection of evidence and the investigation of suspected breaches of welfare legislation with the possibility of penalties imposed on the producer and transporter (

      European Commission. (Directorate for Health and Food Audits and Analysis; Directorate-General for Health and Food Safety) 2016. Overview Report on Systems to Prevent the Transport of Unfit Animals in the European Union. Accessed Sep. 22, 2020. https://publications.europa.eu/en/publication-detail/-/publication/2bdfe42c-e33f-409e-8f02-4f0308205ede/language-en doi 10.2875/669512.

      ).

      d. No Economic Alternatives Other than to Send Cull Cows to Slaughter

      (
      • White T.L.
      • Moore D.A.
      Reasons for whole carcass condemnations of cattle in the United States and implications for producer education and veterinary intervention..
      ;

      European Commission. (Directorate for Health and Food Audits and Analysis; Directorate-General for Health and Food Safety) 2016. Overview Report on Systems to Prevent the Transport of Unfit Animals in the European Union. Accessed Sep. 22, 2020. https://publications.europa.eu/en/publication-detail/-/publication/2bdfe42c-e33f-409e-8f02-4f0308205ede/language-en doi 10.2875/669512.

      ). There are often very limited options for on-farm slaughter with the transport of the carcass to a slaughter plant, but where this option is available, it is likely to reduce some of the dilemmas associated with decisions on fitness for transport and economics (
      • Magalhães-Sant’Ana M.
      • More S.J.
      • Morton D.B.
      • Hanlon A.J.
      Challenges facing the veterinary profession in Ireland: 3. Emergency and casualty slaughter certification..
      ;
      • Koralesky K.E.
      • Fraser D.
      Use of on-farm emergency slaughter for dairy cows in British Columbia..
      ).

      e. Inadequate Evaluation of Fitness for Transport

      (

      European Commission. (Directorate for Health and Food Audits and Analysis; Directorate-General for Health and Food Safety) 2016. Overview Report on Systems to Prevent the Transport of Unfit Animals in the European Union. Accessed Sep. 22, 2020. https://publications.europa.eu/en/publication-detail/-/publication/2bdfe42c-e33f-409e-8f02-4f0308205ede/language-en doi 10.2875/669512.

      ). The number of animals that arrive at slaughter plants in poor condition would be reduced if there was a more effective assessment of the fitness of animals before they are loaded on the journey to be sent to slaughter (
      • Dahl-Pedersen K.
      • Herskin M.S.
      • Houe H.
      • Thomsen P.T.
      A descriptive study of the clinical condition of cull dairy cows before transport to slaughter..
      ). There are detailed guidelines to assess the fitness for transport of cull cows (

      American Association of Bovine Practitioners. 2019. Guidelines for Transportation and Fitness-To-Travel Recommendations for Cattle. Accessed Sep. 22, 2020. https://www.aabp.org/Resources/AABP_Guidelines/transportationguidelines-2019.pdf.

      ), but different stakeholders can have different views on the criteria that would make an animal unfit for transport (
      • Herskin M.S.
      • Hels A.
      • Anneberg I.
      • Thomsen P.T.
      Livestock drivers’ knowledge about dairy cow fitness for transport—A Danish questionnaire survey..
      ;
      • Dahl-Pedersen K.
      • Foldager L.
      • Herskin M.S.
      • Houe H.
      • Thomsen P.T.
      Lameness scoring and assessment of fitness for transport in dairy cows: Agreement among and between farmers, veterinarians and livestock drivers..
      ). A survey of Wisconsin dairy producers showed that 12% did not examine cull cows before transport and routinely shipped sick cows. Forty percent of producers visually examined cull cows before transport and shipped some sick cows (
      • Hoe F.G.H.
      • Ruegg P.L.
      Opinions and practices of Wisconsin dairy producers about biosecurity and animal well-being..
      ). A recent survey showed that the percentages of Canadian dairy producers who considered that BCS and the ability of a cow to stand and stay standing were of little importance/unimportant when making a decision on culling were 23 and 2%, respectively (
      • Roche S.M.
      • Renaud D.L.
      • Genore R.
      • Shock D.A.
      • Bauman C.
      • Croyle S.
      • Barkema H.W.
      • Dubuc J.
      • Keefe G.P.
      • Kelton D.F.
      Canadian national dairy study: Describing Canadian dairy producer practices and perceptions surrounding cull cow management..
      ).

      f. Inadequate Evaluation of Need and Procedures for Euthanasia of Cows that Are Not Fit for Transport

      (

      European Commission. (Directorate for Health and Food Audits and Analysis; Directorate-General for Health and Food Safety) 2016. Overview Report on Systems to Prevent the Transport of Unfit Animals in the European Union. Accessed Sep. 22, 2020. https://publications.europa.eu/en/publication-detail/-/publication/2bdfe42c-e33f-409e-8f02-4f0308205ede/language-en doi 10.2875/669512.

      ;
      • Edwards-Callaway L.
      • Walker J.
      • Tucker C.B.
      Culling decisions and dairy cattle welfare during transport to slaughter in the United States..
      ;
      • Walker J.B.
      • Roman-Muniz I.
      • Edwards-Callaway L.
      Timely euthanasia in the United States dairy industry—Challenges and a path forward..
      ). For cull cows that are either experiencing suffering that cannot be mitigated, are not fit for transport, have no reasonable prospect of economic recovery, or are not fit for human consumption, on-farm euthanasia is the preferred option. Producers should be encouraged to develop an on-farm euthanasia plan that is part of their health and welfare plan developed in consultation with the herd veterinarian (
      • Turner P.V.
      • Doonan G.
      Developing on-farm euthanasia plans..
      ). This should include clinical endpoints, decision trees, training of staff, and appropriate methods of euthanasia.

      Shearer, J. K., and J. P. Reynolds. 2011. Euthanasia techniques for dairy cattle. Pages 331–339 in Dairy Production Medicine. C. A. Risco and P. M. Retamal, ed. John Wiley & Sons, NJ. 10.1002/9780470960554.ch25.

      provide examples of conditions that often result in on-farm euthanasia. Euthanasia guidelines, protocols, trained personnel, and effective equipment for euthanasia should be available on-farm (
      • Turner P.V.
      • Doonan G.
      Developing on-farm euthanasia plans..
      ), at auction markets (

      Livestock Marketing Association. 2018. Guide to Animal Handling Employee Training for Livestock Auction Markets. Accessed Mar. 26, 2021. https://lmaweb.com/wp-content/uploads/2020/12/LMAhandlingprogram2018Edition.pdf.

      ), and for transporters. However,
      • Walker J.B.
      • Roman-Muniz I.
      • Edwards-Callaway L.
      Timely euthanasia in the United States dairy industry—Challenges and a path forward..
      suggested that written guidelines for treatment and euthanasia were not present on most US dairy farms and that many producers did not make the decision to euthanize a cow soon enough to prevent avoidable or unnecessary suffering. A survey of Wisconsin dairy producers showed that 32% had not undertaken euthanasia of a sick animal during the previous 3 yr (
      • Hoe F.G.H.
      • Ruegg P.L.
      Opinions and practices of Wisconsin dairy producers about biosecurity and animal well-being..
      ). A survey in the USA showed that of the dairy cows that died on dairy farms, 40% died unassisted, and the remainder were euthanized (

      USDA. 2018. Dairy 2014. Health and Management Practices on U.S. Dairy Operations, 2014. Accessed Sep. 22, 2020. https://www.aphis.usda.gov/animal_health/nahms/dairy/downloads/dairy14/Dairy14_dr_PartIII.pdf.

      ). If a high percentage of cows in a herd die unassisted, this would suggest that the welfare of the cows in that herd was poor (
      • Alvåsen K.
      • Thomsen P.T.
      • Sandgren C.H.
      • Mörk M.J.
      • Emanuelson U.
      Risk factors for unassisted on-farm death in Swedish dairy cows..
      ). Unless the cows that died unassisted died rapidly, they likely experienced a period of suffering and distress before death (
      • Alvåsen K.
      • Thomsen P.T.
      • Sandgren C.H.
      • Mörk M.J.
      • Emanuelson U.
      Risk factors for unassisted on-farm death in Swedish dairy cows..
      ;
      • Walker J.B.
      • Roman-Muniz I.
      • Edwards-Callaway L.
      Timely euthanasia in the United States dairy industry—Challenges and a path forward..
      ). Alternatively, a high percentage of euthanized cows may be a consequence of a reduced threshold for a decision to euthanize a cow compared with treating it or sending it for slaughter (
      • Thomsen P.T.
      • Kjeldsen A.M.
      • Sørensen J.T.
      • Houe H.
      Mortality (including euthanasia) among Danish dairy cows (1990–2001)..
      ;
      • Alvåsen K.
      • Thomsen P.T.
      • Sandgren C.H.
      • Mörk M.J.
      • Emanuelson U.
      Risk factors for unassisted on-farm death in Swedish dairy cows..
      ). A reduced threshold for euthanasia is preferable from an animal welfare perspective as this would avoid suffering associated with a prolonged illness or transportation in a compromised condition (
      • Alvåsen K.
      • Thomsen P.T.
      • Sandgren C.H.
      • Mörk M.J.
      • Emanuelson U.
      Risk factors for unassisted on-farm death in Swedish dairy cows..
      ). However, most producers will only undertake euthanasia in extreme circumstances. They are reluctant to undertake on-farm euthanasia because of the costs involved in undertaking euthanasia, the cost for disposal of the body, the loss of carcass value (
      • Langford F.M.
      • Stott A.W.
      Culled early or culled late: Economic decisions and risks to welfare in dairy cows..
      ;
      • Edwards-Callaway L.
      • Walker J.
      • Tucker C.B.
      Culling decisions and dairy cattle welfare during transport to slaughter in the United States..
      ), and the difficulty in finding a competent person and suitable equipment to undertake euthanasia (

      European Commission. (Directorate for Health and Food Audits and Analysis; Directorate-General for Health and Food Safety) 2016. Overview Report on Systems to Prevent the Transport of Unfit Animals in the European Union. Accessed Sep. 22, 2020. https://publications.europa.eu/en/publication-detail/-/publication/2bdfe42c-e33f-409e-8f02-4f0308205ede/language-en doi 10.2875/669512.

      ).

      g. Inadequate Early Recognition of Disease or Disability, the Scope for Improved Preventive Measures, and the Need for a Culling Policy

      (
      • White T.L.
      • Moore D.A.
      Reasons for whole carcass condemnations of cattle in the United States and implications for producer education and veterinary intervention..
      ). The National Dairy Farm Program (

      National Milk Producers Federation. 2020. Animal Care Reference Manual Version 4 2020–2022. Accessed Sep. 22, 2020. https://nationaldairyfarm.com/wp-content/uploads/2020/09/FARM_Animal-Care-4-Manual_Layout_FINAL_091520_SinglePages.pdf.

      ) advises that dairy producers should have an effective written protocol for common diseases that sets out procedures for the rapid diagnosis and quick decision making on necessary treatment and care of sick or injured cows. A delay in undertaking these procedures can result in avoidable suffering. Whether a cow is treated for a disease and how soon it is treated are dependent on several factors. For example, it can depend on whether and how soon the disease is recognized, the severity of the clinical signs, the effectiveness of any treatment, and the potential for drug residues in the milk or meat (
      • Roberson J.R.
      Treatment of clinical mastitis..
      ). Another major issue is the economics of treatment, e.g., drug and veterinary costs. These are considered in relation to the effects of the disease on milk production and reproduction, and the economic consequences of culling the cow and sending it for slaughter (
      • Cha E.
      • Hertl J.A.
      • Bar D.
      • Gröhn Y.T.
      The cost of different types of lameness in dairy cows calculated by dynamic programming..
      ,
      • Cha E.
      • Bar D.
      • Hertl J.A.
      • Tauer L.W.
      • Bennett G.
      • González R.N.
      • Schukken Y.H.
      • Welcome F.L.
      • Gröhn Y.T.
      The cost and management of different types of clinical mastitis in dairy cows estimated by dynamic programming..
      ;
      • Liang D.
      • Arnold L.M.
      • Stowe C.J.
      • Harmon R.J.
      • Bewley J.M.
      Estimating US dairy clinical disease costs with a stochastic simulation model..
      ). These are difficult individual decisions that are conducted each time a cow is sick or injured (
      • Wagner B.K.
      • Cramer M.C.
      • Fowler H.N.
      • Varnell H.L.
      • Dietsch A.M.
      • Proudfoot K.L.
      • Shearer J.
      • Correa M.
      • Pairis-Garcia M.
      Determination of dairy cattle euthanasia criteria and analysis of barriers to humane euthanasia in the United States: The veterinarian perspective..
      ). Further research would be beneficial to understand how these decisions are made by producers and how they balance treatment, euthanasia, and culling options. The length of time between a decision by Canadian dairy producers to cull a cow and the actual time that the cow leaves the farm can be several weeks (
      • Roche S.M.
      • Renaud D.L.
      • Genore R.
      • Shock D.A.
      • Bauman C.
      • Croyle S.
      • Barkema H.W.
      • Dubuc J.
      • Keefe G.P.
      • Kelton D.F.
      Canadian national dairy study: Describing Canadian dairy producer practices and perceptions surrounding cull cow management..
      ). In a recent survey, the percentages of producers that stated that a lame cow and a sick cow could remain on their farm for longer than 6 wk after a decision had been taken to cull them was 10 and 5%, respectively, and for less than 3 d, it was 16 and 30%, respectively (
      • Roche S.M.
      • Renaud D.L.
      • Genore R.
      • Shock D.A.
      • Bauman C.
      • Croyle S.
      • Barkema H.W.
      • Dubuc J.
      • Keefe G.P.
      • Kelton D.F.
      Canadian national dairy study: Describing Canadian dairy producer practices and perceptions surrounding cull cow management..
      ). The duration that a cow experiences a condition such as a foot lesion and the severity of the lesion will affect the welfare impact on the cow (
      • Bruijnis M.R.N.
      • Beerda B.
      • Hogeveen H.
      • Stassen E.N.
      Assessing the welfare impact of foot disorders in dairy cattle by a modeling approach..
      ). Further research on the reasons and circumstances for delays between a decision to cull a cow and the time that the cow leaves the farm would be beneficial to highlight whether the delays are due to specific economic factors that are putting the welfare of cull cows at risk.
      Early culling of cows with health conditions can avoid the development of significant animal welfare issues on the farm and during transport to slaughter. Culling procedures should form part of a written farm health and welfare plan developed in consultation with the unit’s veterinarian (

      National Milk Producers Federation. 2020. Animal Care Reference Manual Version 4 2020–2022. Accessed Sep. 22, 2020. https://nationaldairyfarm.com/wp-content/uploads/2020/09/FARM_Animal-Care-4-Manual_Layout_FINAL_091520_SinglePages.pdf.

      ). Keeping detailed records of cull cows and the reasons for culling will assist a veterinarian in offering advice to the dairy producer (
      • Orpin P.G.
      • Sibley R.J.
      Counting the culls and costing the casualties—Not all cull cows are the same..
      ). An annual culling audit of the detailed analysis of culling and the reasons for culling can form part of proactive health planning in dairy herds (
      • Orpin P.G.
      • Esslemont R.J.
      Culling and wastage in dairy herds: An update on incidence and economic impact in dairy herds in the UK..
      ). Veterinary involvement is vital for early detection and appropriate treatment of disease conditions. Farm staff should be trained on the recognition of disease, provision of effective treatment, when to obtain veterinary advice, and how to assess improvement or deterioration in health (
      • White T.L.
      • Moore D.A.
      Reasons for whole carcass condemnations of cattle in the United States and implications for producer education and veterinary intervention..
      ). An effective health plan; regular health monitoring; and veterinary advice on preventive measures, biosecurity, and treatment protocols should improve the health and fitness of the animals and reduce the number of animals on a farm that need to be culled prematurely (
      • LeBlanc S.J.
      • Lissemore K.D.
      • Kelton D.F.
      • Duffield T.F.
      • Leslie K.E.
      Major advances in disease prevention in dairy cattle..
      ). Improvements to the welfare of lactating dairy cows by reducing the prevalence of health issues will also provide economic returns by increasing the longevity of cows in the herd and milk production, and reducing the costs associated with unplanned culling (
      • Langford F.M.
      • Stott A.W.
      Culled early or culled late: Economic decisions and risks to welfare in dairy cows..
      ). Regular on-farm health assessments, including gait scoring (
      • Schlageter-Tello A.
      • Bokkers E.A.M.
      • Koerkamp P.W.G.G.
      • Van Hertem T.
      • Viazzi S.
      • Romanini C.E.B.
      • Halachmi I.
      • Bahr C.
      • Berckmans D.
      • Lokhorst K.
      Manual and automatic locomotion scoring systems in dairy cows: A review..
      ) and body condition scoring (
      • Roche J.R.
      • Dillon P.G.
      • Stockdale C.R.
      • Baumgard L.H.
      • VanBaale M.J.
      Relationships among international body condition scoring systems..
      ), will assist in identifying cows suitable for culling before they become unfit for transport. Attention to the management of cows that are at increased risk from culling (e.g., those that are recently calved, lame, with a high BCS at calving, or in estrus) and areas where the risk of injury is increased (e.g., slippery concrete, inadequate feed and water space, and congested areas) would also be beneficial (
      • Orpin P.G.
      • Sibley R.J.
      Counting the culls and costing the casualties—Not all cull cows are the same..
      ).
      The ability of a dairy producer to improve the health and welfare of their cows is affected by many factors, including the managerial skills of the producer, herd size, facilities, training and experience of stock people, and the ratio of stock people to the number of cows (
      • Barkema H.W.
      • von Keyserlingk M.A.G.
      • Kastelic J.P.
      • Lam T.J.G.M.
      • Luby C.
      • Roy J.
      • LeBlanc S.J.
      • Keefe G.P.
      • Kelton D.F.
      Invited review: Changes in the dairy industry affecting dairy cattle health and welfare..
      ). Although they tend to be complex multifactorial conditions, the main causes of unplanned culling are amenable to control measures. Many of the risk factors are understood, and these can form the basis for specific control protocols designed for individual farms (
      • Orpin P.G.
      • Sibley R.J.
      Counting the culls and costing the casualties—Not all cull cows are the same..
      ). Veterinary herd health management programs are available to dairy producers to monitor herd health and provide preventive advice to enable the producer to achieve their farm performance goals (
      • Noordhuizen J.P.T.M.
      • Wentink G.H.
      Epidemiology: Developments in veterinary herd health programmes on dairy farms: A review..
      ;
      • Sibley R.
      Developing health plans for the dairy herd..
      ;
      • Derks M.
      • van Werven T.
      • Hogeveen H.
      • Kremer W.D.J.
      Associations between farmer participation in veterinary herd health management programs and farm performance..
      ). However, dairy producers adopt varying degrees of interaction with their herd veterinarian and participate at different levels in herd health schemes (
      • Derks M.
      • van Werven T.
      • Hogeveen H.
      • Kremer W.D.J.
      Veterinary herd health management programs on dairy farms in the Netherlands: Use, execution, and relations to farmer characteristics..
      ,
      • Derks M.
      • van Werven T.
      • Hogeveen H.
      • Kremer W.D.J.
      Associations between farmer participation in veterinary herd health management programs and farm performance..
      ). In a study in the Netherlands, producers who chose the minimal level of participation in a health scheme had a lower culling rate, and their cows were older at culling than those who participated fully in a health scheme. Producers who participated at an intermediate level had a greater culling rate, and their cows were older at culling than those who participated fully in a health scheme. Although further research on the specific reasons for culling is required, it is possible that the veterinarians advised producers to cull their sick or problem cows earlier than the producer otherwise would have culled the cows (
      • Derks M.
      • van Werven T.
      • Hogeveen H.
      • Kremer W.D.J.
      Associations between farmer participation in veterinary herd health management programs and farm performance..
      ). An increased understanding of how veterinary advice on the treatment and control of the common health conditions in dairy cows can be used to improve the management decisions made by dairy producers would be beneficial in reducing the numbers of cull cows with severe health and welfare issues.

      FACTORS THAT AFFECT THE RISK OF SUFFERING DURING MARKETING AND TRANSPORT

      In addition to issues related to fitness for transport, there are several factors during marketing and transport that are not faced to the same extent by other types of cattle, and these can interact with the condition of the cow and increase the risk of suffering in cull dairy cows (

      Western Dairy Science Inc. 2004. Humane handling of dairy cattle; Standards for the transportation of unfit cull animals. West. Dairy Sci. Inc. Accessed Sep. 22, 2020. http://www.agromedia.ca/HumaneHandling/HumaneHandling.pdf.

      ;
      • Strappini A.C.
      • Frankena K.
      • Metz J.H.M.
      • Gallo B.
      • Kemp B.
      Prevalence and risk factors for bruises in Chilean bovine carcasses..
      ;
      • Stojkov J.
      • Bowers G.
      • Draper M.
      • Duffield T.
      • Duivenvoorden P.
      • Groleau M.
      • Haupstein D.
      • Peters R.
      • Pritchard J.
      • Radom C.
      • Sillett N.
      • Skippon W.
      • Trépanier H.
      • Fraser D.
      Hot topic: Management of cull dairy cows—Consensus of an expert consultation in Canada..
      ,
      • Stojkov J.
      • von Keyserlingk M.A.G.
      • Duffield T.
      • Fraser D.
      Management of cull dairy cows: Culling decisions, duration of transport, and effect on cow condition..
      ).

      Lactation, Udder Distention, and Edema

      In a survey in the USA, 20% of the cows that were removed from the herd were in early lactation, 24% were removed during mid-lactation, and 7% of removals from the herd were dry cows (

      USDA. 2018. Dairy 2014. Health and Management Practices on U.S. Dairy Operations, 2014. Accessed Sep. 22, 2020. https://www.aphis.usda.gov/animal_health/nahms/dairy/downloads/dairy14/Dairy14_dr_PartIII.pdf.

      ). If a lactating cull dairy cow is not milked at regular intervals after it has left the farm, milk will accumulate in the udder, causing increased intramammary pressure, and this can result in tissue damage, discomfort, and potentially pain (
      • Bertulat S.
      • Fischer-Tenhagen C.
      • Suthar V.
      • Möstl E.
      • Isaka N.
      • Heuwieser W.
      Measurement of fecal glucocorticoid metabolites and evaluation of udder characteristics to estimate stress after sudden dry-off in dairy cows with different milk yields..
      ;
      • Vilar M.J.
      • Rajala-Schultz P.
      Dry-off and dairy cow udder health and welfare: Effects of different milk cessation methods..
      ).
      • Dahl-Pedersen K.
      • Herskin M.S.
      • Houe H.
      • Thomsen P.T.
      Risk factors for deterioration of the clinical condition of cull dairy cows during transport to slaughter..
      observed more cull cows with milk leakage after transport to slaughter than on farm before loading. The risk of milk leakage increased with journey distances greater than 100 km and in cows in early lactation.
      • Stojkov J.
      • von Keyserlingk M.A.G.
      • Duffield T.
      • Fraser D.
      Fitness for transport of cull dairy cows at livestock markets..
      ,
      • Stojkov J.
      • von Keyserlingk M.A.G.
      • Duffield T.
      • Fraser D.
      Management of cull dairy cows: Culling decisions, duration of transport, and effect on cow condition..
      ) observed that 9% of the cull dairy cows on dairy farms in British Columbia, Canada, had udder edema, but they were still sent to an auction market; 10% of cull cows at markets had an engorged udder, and 3% had a swollen or inflamed udder. A lactating cow that has not been milked regularly can be identified by milk leaking from the teats and by udder edema (that likely occurs due to inflammation and reduced venous drainage;
      • Balmer M.
      • Alsaaod M.
      • Boesiger M.
      • Studer E.
      • O’Brien R.
      • Schuepbach-Regula G.
      • Steiner A.
      Risk factors for sonographically detectable udder edema in overbagged cows at dairy shows..
      ). Cows with signs of edema can have a reduced feed intake (
      • Bareille N.
      • Beaudeau F.
      • Billon S.
      • Robert A.
      • Faverdin P.
      Effects of health disorders on feed intake and milk production in dairy cows..
      ). A lactating dairy cow that is transported to slaughter should be milked to reduce potential udder discomfort (

      National Milk Producers Federation. 2020. Animal Care Reference Manual Version 4 2020–2022. Accessed Sep. 22, 2020. https://nationaldairyfarm.com/wp-content/uploads/2020/09/FARM_Animal-Care-4-Manual_Layout_FINAL_091520_SinglePages.pdf.

      ); slaughtered within 24 h of leaving the farm; or preferably dried off about 3 wk before transport by a gradual cessation of milking over several days before the final milking so that their udder is involuted by the time of transport (

      Western Dairy Science Inc. 2004. Humane handling of dairy cattle; Standards for the transportation of unfit cull animals. West. Dairy Sci. Inc. Accessed Sep. 22, 2020. http://www.agromedia.ca/HumaneHandling/HumaneHandling.pdf.

      ;
      • Vilar M.J.
      • Rajala-Schultz P.
      Dry-off and dairy cow udder health and welfare: Effects of different milk cessation methods..
      ).

      Thermal Environment

      In some climates, cull cows are transported in cold conditions, e.g., <2°C (
      • Goldhawk C.
      • Janzen E.
      • González L.A.
      • Crowe T.
      • Kastelic J.
      • Kehler C.
      • Siemens M.
      • Ominski K.
      • Pajor E.
      • Schwartzkopf-Genswein K.S.
      Trailer temperature and humidity during winter transport of cattle in Canada and evaluation of indicators used to assess the welfare of cull beef cows before and after transport..
      ). Cull dairy cows are susceptible to thermal discomfort (

      European Food Safety Authority. 2004. Opinion of the Scientific Panel on Animal Health and Welfare on a request from the Commission related to the Standards for the microclimate inside animal road transport vehicles. EFSA J. 122:1–25. 10.2903/j.efsa.2004.122.

      ) if they are exposed to environments that are colder than those to which they have been acclimatized during housing. Exposed udders are also susceptible to frostbite at a market or during transportation (

      Fisher, M., and B. Rothwell. 1999. Humane marketing and transportation of cull dairy cows. Adv. Dairy Technol. 11:135–139. https://wcds.ualberta.ca/2017/08/22/1999/.

      ). In cold climates, dairy producers have been advised that they may need to give cull cows an opportunity to grow a winter coat by acclimating them to cold conditions for at least 2 wk before transport, or they should ensure that they are only transported locally (

      Western Dairy Science Inc. 2004. Humane handling of dairy cattle; Standards for the transportation of unfit cull animals. West. Dairy Sci. Inc. Accessed Sep. 22, 2020. http://www.agromedia.ca/HumaneHandling/HumaneHandling.pdf.

      ). This advice is supported by the estimates made by

      Webster, A. J. F. 1974. Heat loss from cattle with particular emphasis on the effects of cold. Pages 205–231 in Heat Loss from Animals and Man. J. L. Monteith and L. E. Mount, ed. Butterworth-Heinemann, Oxford, UK. 10.1016/B978-0-408-70652-0.50016-0.

      that a nonlactating dairy cow that had been kept indoors could have a lower critical temperature of 2°C, which increases to 14°C when exposed to an air movement of 4 m/s. Therefore, if during transport or at a market a cull cow was exposed to an air temperature of <2°C, or an air temperature of <14°C and air movement, it would need to attempt to increase its metabolic heat production and conserve heat loss by vasoconstriction, piloerection, and changes in behavior (

      European Food Safety Authority. 2004. Opinion of the Scientific Panel on Animal Health and Welfare on a request from the Commission related to the Standards for the microclimate inside animal road transport vehicles. EFSA J. 122:1–25. 10.2903/j.efsa.2004.122.

      ). Whereas, if it had been acclimatized to outdoor conditions before transport, it would have greater external insulation from a longer, thicker hair coat and thicker skin insulation, and it could have a lower critical temperature of −10°C and be better able to cope with cold temperatures and air movement during transportation or while at a market. However, if in poor body condition, a dairy cow would be at even greater risk of thermal discomfort due to reduced tissue insulation, and its lower critical temperature could be 6°C, rising to 16°C if exposed to air movement (

      Webster, A. J. F. 1974. Heat loss from cattle with particular emphasis on the effects of cold. Pages 205–231 in Heat Loss from Animals and Man. J. L. Monteith and L. E. Mount, ed. Butterworth-Heinemann, Oxford, UK. 10.1016/B978-0-408-70652-0.50016-0.

      ).
      Whether cull dairy cows that have been housed experience thermal discomfort when exposed to cold conditions during transport and marketing and how cull dairy cows respond to high humidity and temperature during transport and marketing are important topics for research.
      • González L.A.
      • Schwartzkopf-Genswein K.
      • Bryan M.
      • Silasi R.
      • Brown F.
      Relationships between transport conditions and welfare outcomes during commercial long haul transport of cattle in North America..
      reported that the risk of mortality of cattle during long journeys increased when the temperature was less than 0°C and especially when it was below −15°C. The risk of mortality also increased when the temperature was greater than 20°C and especially when it was greater than 35°C.

      Bruising

      Cull dairy cows are at greater risk of bruising than fattened cattle (
      • Strappini A.C.
      • Frankena K.
      • Metz J.H.M.
      • Gallo B.
      • Kemp B.
      Prevalence and risk factors for bruises in Chilean bovine carcasses..
      ). Some of this bruising has been attributed to handling on farm and during the preslaughter period (
      • Strappini A.C.
      • Metz J.H.M.
      • Gallo C.
      • Frankena K.
      • Vargas R.
      • De Freslon I.
      • Kemp B.
      Bruises in culled cows: When, where and how are they inflicted?.
      ). In a survey of cull cows at slaughter in the USA,
      • Rezac D.J.
      • Thomson D.U.
      • Siemens M.G.
      • Prouty F.L.
      • Reinhardt C.D.
      • Bartle S.J.
      A survey of gross pathologic conditions in cull cows at slaughter in the Great Lakes region of the United States..
      recorded some degree of bruising on over half of the carcasses of cull dairy cows, and 12% of the carcasses had at least one severe bruise. Bruising was observed in the hip region of 37% of the carcasses and on the back of 24% of the carcasses. The authors speculated that many of the Holstein cows were too tall to avoid hitting either their hips or backs within the types of trailers used to transport them to slaughter.
      • Lambooij E.
      • van der Werf J.T.N.
      • Reimert H.G.M.
      • Hindle V.A.
      Compartment height in cattle transport vehicles..
      observed that adult dairy cows with a withers height of about 1.4 m required a ceiling height during transport of greater than 20 cm above the withers to avoid a raised head from touching the ceiling.

      Prolonged Marketing Route and Potential for Inadequate Feed Intake

      An important aspect of the culling decision is the marketing route chosen for the cows. Cull cows are often sent for slaughter via auction markets as this has the potential to maximize financial returns (
      • Edwards-Callaway L.
      • Walker J.
      • Tucker C.B.
      Culling decisions and dairy cattle welfare during transport to slaughter in the United States..
      ). In a survey of dairy herds in the USA in 2013, 92% of dairy operations sent cull cows to a market, auction, or stockyard, and 37% sent cows directly to a packer or slaughter plant (

      USDA. 2018. Dairy 2014. Health and Management Practices on U.S. Dairy Operations, 2014. Accessed Sep. 22, 2020. https://www.aphis.usda.gov/animal_health/nahms/dairy/downloads/dairy14/Dairy14_dr_PartIII.pdf.

      ). In the USA, 63% of shipments of cull cows made to a market, auction, or stockyard were transported 10 to 49 miles (16–79 km) and 22% for 50 to 249 miles (80–400 km) from the farm of origin. Forty-three percent of the shipments of cull cows direct to slaughter were transported 10 to 49 miles, 38% were sent 50 to 249 miles, and 11% were sent 250 or more miles from the farm of origin (

      USDA. 2018. Dairy 2014. Health and Management Practices on U.S. Dairy Operations, 2014. Accessed Sep. 22, 2020. https://www.aphis.usda.gov/animal_health/nahms/dairy/downloads/dairy14/Dairy14_dr_PartIII.pdf.

      ).
      • Stojkov J.
      • von Keyserlingk M.A.G.
      • Duffield T.
      • Fraser D.
      Management of cull dairy cows: Culling decisions, duration of transport, and effect on cow condition..
      identified that the journey of some cull dairy cows to a slaughter plant from dairy farms in British Columbia, Canada, can be long, e.g., 1,000 km, whereas other cows were transported on local journeys e.g., 60 km. The average duration between a cow leaving a dairy farm and arriving at a slaughter plant was over 3 d. Some of the time was spent at auctions or assembly yards. Five percent of the cull cows were slaughtered within 1 d, 43% within 2 to 3 d, 41% in 4 to 5 d, 8% in 5 to 7 d, and 3% in 8 to 16 d of leaving the farm. The journey to slaughter and the total time between leaving the farm and slaughter are affected by the location and availability of slaughter plants that slaughter cull dairy cows and the limited slaughter capacity at some establishments (
      • Stojkov J.
      • von Keyserlingk M.A.G.
      • Duffield T.
      • Fraser D.
      Management of cull dairy cows: Culling decisions, duration of transport, and effect on cow condition..
      ). Delays can also occur when dealers and transporters obtain small numbers of cull cows from various farms and markets to assemble a large load before traveling a long distance to a remote slaughter plant (
      • Stojkov J.
      • Bowers G.
      • Draper M.
      • Duffield T.
      • Duivenvoorden P.
      • Groleau M.
      • Haupstein D.
      • Peters R.
      • Pritchard J.
      • Radom C.
      • Sillett N.
      • Skippon W.
      • Trépanier H.
      • Fraser D.
      Hot topic: Management of cull dairy cows—Consensus of an expert consultation in Canada..
      ). A recent survey showed that 32% of Canadian dairy producers considered that the duration of the journey to slaughter was of little importance/unimportant when making a decision on culling (
      • Roche S.M.
      • Renaud D.L.
      • Genore R.
      • Shock D.A.
      • Bauman C.
      • Croyle S.
      • Barkema H.W.
      • Dubuc J.
      • Keefe G.P.
      • Kelton D.F.
      Canadian national dairy study: Describing Canadian dairy producer practices and perceptions surrounding cull cow management..
      ).
      After a producer has delivered a cull cow to an auction market, the cow may not receive the same standard of care for the provision of feed, water, shelter, and handling that it received while on the farm (
      • Moorman A.K.G.
      • Duffield T.F.
      • Godkin M.A.
      • Kelton D.F.
      • Rau J.
      • Haley D.B.
      Associations between the general condition of culled dairy cows and selling price at Ontario auction markets..
      ;
      • Sánchez-Hidalgo M.
      • Bravo V.
      • Gallo C.
      Behavior and health indicators to assess cull cow’s welfare in livestock markets..
      ). It is also possible that the cow will be transferred between multiple owners, involving multiple journeys over several days before it is slaughtered. Therefore, “only healthy, non-compromised cull dairy cows should enter the market system” (

      Fisher, M., and B. Rothwell. 1999. Humane marketing and transportation of cull dairy cows. Adv. Dairy Technol. 11:135–139. https://wcds.ualberta.ca/2017/08/22/1999/.

      ). Sending a compromised cull animal to an auction market can increase the journey duration; and expose the animal to extra handling (
      • Sánchez-Hidalgo M.
      • Bravo V.
      • Gallo C.
      Behavior and health indicators to assess cull cow’s welfare in livestock markets..
      ), novel environments, restricted availability of feed and water, cold or hot environments, provide reduced opportunities for rest, and more opportunity for any existing health conditions to deteriorate.
      Cull dairy cows will not have access to feed and water during transport, and it is traditional practice to withhold feed during the preslaughter period. If the marketing process is prolonged, it can result in a loss of BW (
      • Arp T.S.
      • Carr C.C.
      • Johnson D.D.
      • Thrift T.A.
      • Warnock T.M.
      • Schaefer A.L.
      Effects of preslaughter electrolyte supplementation on the hydration and meat quality of cull dairy cows..
      ) and body condition (
      • Stojkov J.
      • von Keyserlingk M.A.G.
      • Duffield T.
      • Fraser D.
      Management of cull dairy cows: Culling decisions, duration of transport, and effect on cow condition..
      ) and signs of dehydration (
      • Vogel K.D.
      • Claus J.R.
      • Grandin T.
      • Oetzel G.R.
      • Schaefer D.M.
      Effect of water and feed withdrawal and health status on blood and serum components, body weight loss, and meat and carcass characteristics of Holstein slaughter cows..
      ). If feed intake is inadequate during this period, the cow will have to use its body energy reserves and protein (
      • Chowdhury S.A.
      • Ørskov E.R.
      Implications of fasting on the energy metabolism and feed evaluation in ruminants..
      ). When a lactating cow is fasted, it can show metabolic changes within 24 h (
      • Baird G.D.
      • Heitzman R.J.
      • Hibbitt K.G.
      Effects of starvation on intermediary metabolism in the lactating cow: A comparison with metabolic changes occurring during bovine ketosis..
      ), with most of the required energy obtained from body fat (
      • Chowdhury S.A.
      • Ørskov E.R.
      Implications of fasting on the energy metabolism and feed evaluation in ruminants..
      ). Plasma free fatty acid concentrations increase (
      • Athanasiou V.N.
      • Phillips R.W.
      Effect of fasting on plasma metabolites and hormones in lactating dairy cows..
      ), and glucose is obtained from carbohydrate stores such as liver glycogen (
      • Reid I.M.
      • Harrison R.D.
      • Collins R.A.
      Fasting and refeeding in the lactating dairy cow: 2. The recovery of liver cell structure and function following a six-day fast..
      ) and from gluconeogenesis of AA (
      • Chowdhury S.A.
      • Ørskov E.R.
      Implications of fasting on the energy metabolism and feed evaluation in ruminants..
      ). Some cows can become hypoglycemic after 24 h (
      • Athanasiou V.N.
      • Phillips R.W.
      Effect of fasting on plasma metabolites and hormones in lactating dairy cows..
      ), whereas others do not become hypoglycemic until 6 d of fasting (
      • Baird G.D.
      • Heitzman R.J.
      • Hibbitt K.G.
      Effects of starvation on intermediary metabolism in the lactating cow: A comparison with metabolic changes occurring during bovine ketosis..
      ). During gluconeogenesis, free fatty acids can be used in the liver to create ketone bodies, and plasma β-hydroxybutyrate concentration increases (
      • Baird G.D.
      • Heitzman R.J.
      • Hibbitt K.G.
      Effects of starvation on intermediary metabolism in the lactating cow: A comparison with metabolic changes occurring during bovine ketosis..
      ;
      • Athanasiou V.N.
      • Phillips R.W.
      Effect of fasting on plasma metabolites and hormones in lactating dairy cows..
      ;
      • Chowdhury S.A.
      • Ørskov E.R.
      Implications of fasting on the energy metabolism and feed evaluation in ruminants..
      ). Reduced feed intake and fasting can cause hunger, weakness, increased susceptibility to cold conditions, ketosis (sometimes with clinical signs associated with sickness,
      • Schultz L.H.
      Ketosis in dairy cattle..
      ), and in lactating cows, hypocalcemia and hypomagnesemia (
      • Robertson A.
      • Paver H.
      • Barden P.
      • Marr T.G.
      Fasting metabolism of the lactating cow..
      ), with an increased risk of becoming nonambulatory (
      • Warnock J.P.
      • Caple I.W.
      • Halpin C.G.
      • McQueen C.S.
      Metabolic changes associated with the ‘downer’ condition in dairy cows at abattoirs..
      ). If a cull cow is already in a negative energy balance because of early lactation or reduced feed intake due to a health issue, such as metritis, ketosis, mastitis, lameness, and oral pathology, their condition is likely to further deteriorate during prolonged marketing (
      • Herdt T.H.
      Ruminant adaptation to negative energy balance: Influences on the etiology of ketosis and fatty liver..
      ;
      • Ingham B.
      Abattoir survey of dental defects in cull cows..
      ;
      • Bareille N.
      • Beaudeau F.
      • Billon S.
      • Robert A.
      • Faverdin P.
      Effects of health disorders on feed intake and milk production in dairy cows..
      ;
      • Esposito G.
      • Irons P.C.
      • Webb E.C.
      • Chapwanya A.
      Interactions between negative energy balance, metabolic diseases, uterine health and immune response in transition dairy cows..
      ;
      • Norring M.
      • Häggman J.
      • Simojoki H.
      • Tamminen P.
      • Winckler C.
      • Pastell M.
      Short communication: Lameness impairs feeding behavior of dairy cows..
      ). The management of cull dairy cows when they are at auction markets and in prolonged marketing chains needs further investigation. Relevant animal welfare outcomes should be monitored at intervals during this process. Benchmarking studies are required to provide surveillance on the clinical and metabolic condition and pathology observed when cull cows are sent for slaughter. Industry standards and practices change over time, and these studies would monitor progress in improving the welfare of cull dairy cows.

      CONCLUSIONS

      This review identified reasons why welfare issues occur in cull dairy cows and the proposals that have been made for the mitigation of these welfare issues. As with several other welfare issues in production animals, there are broad economic and societal issues that influence their occurrence. The main factors influencing the welfare issues in cull cows are known, and dairy producers have access to the necessary advice and recommendations. However, as shown above, in relation to the numbers of cull dairy cows that arrive at slaughter plants in poor health and physical condition, a proportion of producers do not follow that guidance. Dairy producers need to understand the welfare implications of how they manage their cull dairy cows, and if the welfare of cull cows is to be improved, some need to change their management practices. Research on how dairy producers incorporate the welfare implications of their actions in their management of cull cows and how to increase their use of industry recommendations on the care of cull cows are priorities. An increased understanding of how to improve utilization of the veterinary advice provided to dairy producers on the treatment and control of the common health conditions in dairy cows would be expected to reduce the numbers of cull cows with severe health and welfare issues. Further research on the assessment of the fitness of cull dairy cows for transport and on the factors that influence their welfare during transport and marketing is required.

      APPLICATIONS

      Literature was reviewed to improve understanding of the welfare issues affecting cull dairy cows. The welfare implications of sending a cow to slaughter depend on its fitness for transport, the characteristics of the journey, and the standards of care provided. Cows sent to slaughter via auction markets are exposed to additional welfare risks. Cows culled for production reasons that are otherwise in good health and physical condition are better able to cope with transportation and marketing than cows culled because of ill health or injury. There has not been extensive research on how cull dairy cows with different health issues respond to transportation. However, consideration of the pathophysiological implications of ill health and injury can identify potential physical and physiological challenges that can occur during transportation. Surveys at markets and at slaughter plants, together with pathology identified postmortem, indicate that a proportion of cull dairy cows sent to slaughter should not have been transported, and inappropriate on-farm culling decisions likely resulted in unnecessary suffering. The reasons why this occurs have been discussed. They include a focus on economics and inadequate awareness of the welfare implications of culling decisions; lack of legal regulations and their enforcement; lack of financial and market incentives to change practices; practical and financial difficulties with euthanasia; inadequate evaluation of fitness for transport; and inadequate use of health plans that would prevent some issues, identify problems earlier, and cull cows before their condition deteriorates to such an extent that they are no longer fit for transport.

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