Broiler welfare trade-off: A semi-quantitative welfare assessment for optimised welfare improvement based on an expert survey

Autoři: Marc B. M. Bracke aff001;  Paul Koene aff001;  Inma Estevez aff002;  Andy Butterworth aff004;  Ingrid C. de Jong aff001
Působiště autorů: Wageningen Livestock Research, Wageningen University & Research, Wageningen, The Netherlands aff001;  Neiker-Tecnalia Basque Institute for Agricultural Research and Development, Vitoria-Gasteiz, Spain aff002;  Ikerbasque, Basque Foundation for Science, Bilbao, Spain aff003;  School of Veterinary Sciences, University of Bristol, Bristol, England, United Kingdom aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article


In order to support decision making on how to most effectively improve broiler welfare an innovative expert survey was conducted based on principles derived from semantic modelling. Twenty-seven experts, mainly broiler welfare scientists (n = 20; and 7 veterinarians), responded (response rate 38%) by giving welfare scores (GWS, scale 0–10) to 14 benchmarking housing systems (HSs), and explaining these overall scores by selecting, weighing and scoring main welfare parameters, including both input and output measures. Data exploration followed by REML (Linear Mixed Model) and ALM (Automatic Linear Modelling) analyses revealed 6 clusters of HSs, sorted from high to low welfare, i.e. mean GWS (with superscripts indicating significant differences): 1. (semi-natural backyard) Flock (8.8a); 2. Nature (7.7ab), Label Rouge II (7.4ab), Free range EU (7.2ab), Better Life (7.2ab); 3. Organic EU (7.0bc), Freedom Food (6.2bc); 4. Organic US (5.8bcd), Concepts NL (5.6abcdef), GAP 2 (4.9bcd); 5. Conventional EU (3.7de), Conventional US (2.9ef), Modern cage (2.9abcdef); 6. Battery cage (1.3f). Mean weighting factors (WF, scale 0–10) of frequently (n> = 15) scored parameters were: Lameness (8.8), Health status (8.6), Litter (8.3), Density (8.2), Air quality (8.1), Breed (8.0), Enrichment (7.0) and Outdoor (6.6). These did not differ significantly, and did not have much added value in explaining GWS. Effects of Role (Scientist/Vet), Gender (M/F) and Region (EU/non-EU) did not significantly affect GWS or WF, except that women provided higher WF than men (7.2 vs 6.4, p<0.001). The contribution of welfare components to overall welfare has been quantified in two ways: a) using the beta-coefficients of statistical regression (ALM) analyses, and b) using a semantic-modelling type (weighted average) calculation of overall scores (CalcWS) from parameter level scores (PLS) and WF. GWS and CalcWS were highly correlated (R = ~0.85). CalcWS identified Lameness, Health status, Density, Breed, Air quality and Litter as main parameters contributing to welfare. ALM showed that the main parameters which significantly explained the variance in GWS based on all PLS, were the output parameter Health status (with a beta-coefficient of 0.38), and the input parameters (stocking) Density (0.42), Litter (0.14) and Enrichment (0.27). The beta-coefficients indicated how much GWS would improve from 1 unit improvement in PLS for each parameter, thus the potential impact on GWS ranged from 1.4 welfare points for Litter to 4.2 points for Density. When all parameters were included, 81% of the variance in GWS was explained (77% for inputs alone; 39% for outputs alone). From this, it appears that experts use both input and output parameters to explain overall welfare, and that both are important. The major conventional systems and modern cages for broilers received low welfare scores (2.9–3.7), well below scores that may be considered acceptable (5.5). Also, several alternatives like GAP 2 (4.9), Concepts NL (5.6), Organic US (5.8) and Freedom Food (6.2) are unacceptable, or at risk of being unacceptable due to individual variation between experts and farms. Thus, this expert survey provides a preliminary semi-quantified decision-support tool to help determine how to most effectively improve broiler welfare in a wide range of HSs.

Klíčová slova:

Article-level metrics – Food – Regression analysis – Scientists – Surveys – Welfare (social security) – Animal welfare – Air quality


1. EA. Introduction to Effective Altruism. The Centre for Effective Altruism (EA). 22 June 22 2016. Available from: Cited 15 March 2019.

2. Anonymous. Effective altruism. 2018. Available from: Cited 28 May 2018.

3. Bracke MBM, Spruijt BM, Metz JHM, Schouten WGP. Decision support system for overall welfare assessment in pregnant sows A: model structure and weighting procedure. J Anim Sci. 2002a;80(7):1819. doi: 10.2527/2002.8071819x 12162649.

4. Bracke MBM, Spruijt BM, Metz JHM, Schouten WGP. Decision support system for overall welfare assessment in pregnant sows. B. Validation by expert opinion. J Anim Sci. 2002b;8:1835–8812. doi: 10.2527/2002.8071835x

5. Bracke MBM. Modelling of animal welfare: The development of a decision support system to assess the welfare status of pregnant sows. PhD Thesis, Wageningen University and Research. Available from:

6. Bracke MBM, Hulsegge B, Keeling L, Blokhuis HJ. Decision support system with semantic model to assess the risk of tail biting in pigs: 1. Modelling. Appl Anim Behav Sci. 2004a;87(1): 31–44. doi: 10.1016/j.applanim.2003.12.005

7. Bracke MBM, Hulsegge B, Keeling L, Blokhuis HJ. Decision support system with semantic model to assess the risk of tail biting in pigs: 2. ‘Validation’. Appl Anim Behav Sci. 2004b;87(1): 45–54. doi: 10.1016/j.applanim.2003.12.006

8. Bracke MBM. Richpig: a semantic model to assess enrichment materials for pigs. Anim Welfare. 2008;17(3): 289–7286.

9. De Mol RM, Schouten W, Evers E, Drost H, Houwers H, Smits A. A computer model for welfare assessment of poultry production systems for laying hens. Neth J Agric Sci. 2006;54(2): 157–68.

10. Ursinus W, Schepers F, De Mol R, Bracke M, Metz J, Koerkamp PG. COWEL: a decision support system to assess welfare of husbandry systems for dairy cattle. Anim Welfare. 2009;18(4): 545–52.

11. Bracke MBM, Edwards SA, Engel B, Buist WG, Algers B. Expert opinion as 'validation' of risk assessment applied to calf welfare. Acta Vet Scand. 2008b;50(1): 29. doi: 10.1186/1751-0147-50-29 18625048.

12. Stien LH, Bracke MBM, Folkedal O, Nilsson J, Oppedal F, Torgersen T, et al. Salmon Welfare Index Model (SWIM 1.0): a semantic model for overall welfare assessment of caged Atlantic salmon: review of the selected welfare indicators and model presentation. Rev Aquacult. 2013;5(1): 33–57. doi: 10.1111/j.1753-5131.2012.01083.x

13. Pettersen JM, Bracke MBM, Midtlyng PJ, Folkedal O, Stien LH, Steffenak H, et al. Salmon welfare index model 2.0: an extended model for overall welfare assessment of caged Atlantic salmon, based on a review of selected welfare indicators and intended for fish health professionals. Rev Aquacult. 2014;6(3): 162–179. doi: 10.1111/raq.12039

14. Folkedal O, Pettersen J, Bracke M, Stien L, Nilsson J, Martins C, et al. On-farm evaluation of the Salmon Welfare Index Model (SWIM 1.0): theoretical and practical considerations. Anim Welfare. 2016;25(1): 135–49.

15. Bollard L. Initial grants to support corporate cage-free reforms. Open Philanthropy Project. 31 March 2016.Available from: Cited 28 May 2018.

16. Cotra A. How will hen welfare be impacted by the transition to cage-free housing? Open Philanthropy Project. 15 Sept 2017. Available from: Cited 28 May 2018.

17. EC. Commission Regulation (EC) No 889/2008 of 5 September 2008 laying down detailed rules for the implementation of Council Regulation (EC) No 834/2007 on organic production and labelling of organic products with regard to organic production, labelling and control. Official Journal of the European Union. 2008;250: 1–84.

18. SCAHAW. The welfare of chickens kept for meat production (broilers). Report from the Scientific Committee on Animal Health and Animal Welfare (SCAHAW). Brussels: European Commission. 2000. Available from: Cited 12 Feb 2018.

19. Ellen H, Leenstra F, Van Emous R, Groenestein K, Van Harn J, Van Horne P, et al. Vleeskuikenproductiesystemen in Nederland—Vergelijkende studie. [Broiler Production Systems in The Netherlands—Comparative study]. Report 619. Lelystad: Wageningen Livestock Research. 2012. Available from: Cited 29 June 2016.

20. EFSA. Scientific opinion on the influence of genetic parameters on the welfare and the resistance to stress of commercial broilers. EFSA Journal. 2010;8: 1666. doi: 10.2903/j.efsa.2010.1666

21. De Jong I, Berg C, Butterworth A, Estevéz I. Scientific report updating the EFSA opinions on the welfare of broilers and broiler breeders. 2012. Available from: doi: 10.2903/sp.efsa.2012.EN-295

22. Gocsik É, Brooshooft SD, de Jong IC, Saatkamp HW. Cost-efficiency of animal welfare in broiler production systems: A pilot study using the Welfare Quality® assessment protocol. Agr Syst. 2016;146: 55–69. doi: 10.1016/j.agsy.2016.04.001

23. Buijs S, Ampe B, Tuyttens F. Sensitivity of the Welfare Quality® broiler chicken protocol to differences between intensively reared indoor flocks: which factors explain overall classification? Animal. 2017;11(2): 244–253. doi: 10.1017/S1751731116001476 27416919.

24. Anonymous. Scientists' Assessment of the Impact of Housing and Management on Animal Welfare. J Appl Anim Welf Sci. 2001;4(1): 3–52. doi: 10.1207/S15327604JAWS0401_2

25. Bracke M, Spruijt B, Metz J. Overall animal welfare assessment reviewed. Part 1: Is it possible? Neth J Agric Sci. 1999a;47(3): 279–91. Available from:

26. Blokhuis H, Veissier I, Miele M, Jones B. The Welfare Quality® project and beyond: Safeguarding farm animal well-being. Acta Agric Scand Section A. 2010;60(3): 129–40. doi: 10.1080/09064702.2010.523480

27. Bracke M. Animal-based parameters are no panacea for on-farm monitoring of animal welfare. Anim Welfare. 2007;16(2): 229–31.

28. NCC. Animal welfare guidelines and autit checklist for broilers. Available from: Cited 3 Feb 2018. Washington DC: National Chicken Council, 2017.

29. Vissers L, De Jong IC, Van Horne PLM, Saatkamp HW. Global prospects of the cost-efficiency of broiler welfare in middle-segment production systems. Animals. 2019;9(7): 473. doi: 10.3390/ani9070473 31340587.

30. Smithers R. Animal welfare groups call for higher standards for farmed chickens. The Guardian. 13 Jan 2018. Available from: Cited 25 June 2018.

31. Nunnally CJJ. Introduction to psychological measurement. New York: McGraw-Hill; 1970.

32. Koene P. Leeftijd van zelfstandig eten bij papegaaien [Weaning ages in parrot species]. Report 771. Wageningen: Wageningen Livestock Research. 2014. Available from: Cited 6 Feb 2019.

33. Koene P, De Mol R, Ipema B. Behavioral ecology of captive species: Using bibliographic information to assess pet suitability of mammal species. Front Vet Sci. 2016;20(3): 35. doi: 10.3389/fvets.2016.00035

34. SPSS. IBM SPSS Statistics for Windows (Version Version 23.0). Armonk, NY: IBM Corp; 2013.

35. Bracke MBM, Zonderland JJ, Bleumer EJB. Expert judgement on enrichment materials for pigs validates preliminary RICHPIG model. Appl Anim Behav Sci. 2007a;104(1–2): 1–13. doi: 10.1016/j.applanim.2006.05.005

36. Bracke MBM, Zonderland JJ, Bleumer EJB. Expert consultation on weighting factors of criteria for assessing environmental enrichment materials for pigs. Appl Anim Behav Sci. 2007b;104(1–2): 14–23. doi: 10.1016/j.applanim.2006.05.006

37. Widowski TM, Duncan IJH. Working for a dustbath: are hens increasing pleasure rather than reducing suffering? Appl Anim Behav Sci. 2000;68(1): 39–53. doi: 10.1016/S0168-1591(00)00088-5 10771314

38. Bilgili S, Hess J, Blake J, Macklin K, Saenmahayak B, Sibley J. Influence of bedding material on footpad dermatitis in broiler chickens. J Appl Poultry Res. 2009;18(3): 583–589. doi: 10.3382/japr.2009-00023

39. de Jong IC, Gunnink H, Van Harn J. Wet litter not only induces footpad dermatitis but also reduces overall welfare, technical performance, and carcass yield in broiler chickens. J Appl Poultry Res. 2014;23(1): 51–58. doi: 10.3382/japr.2013-00803

40. Bracke MBM, Koene P. Expert opinion on metal chains and other indestructible objects as proper enrichment for intensively-farmed pigs. PLOS ONE. 2019. Available from: doi: 10.1371/journal.pone.0212610 30794640.

41. Opengart K, Bilgili S, Warren G, Baker K, Moore J, Dougherty S. Incidence, severity, and relationship of broiler footpad lesions and gait scores of market-age broilers raised under commercial conditions in the southeastern United States. J Appl Poultry Res. 2018; 27(3): 424–432. doi: 10.3382/japr/pfy002

42. Collins L, Part C. Modelling Farm Animal Welfare. Animals. 2013;3(2): 416–441. doi: 10.3390/ani3020416 26487411

43. De Oliveira Souza AP, Sans ES, Müller BR, Molento CM. Broiler chicken welfare assessment in GLOBALGAP (R) certified and non-certified farms in Brazil. Anim Welfare. 2015;24: 45–54.

44. Federici J, Vanderhasselt R, Sans E, Tuyttens F, Souza A, Molento C. Assessment of Broiler Chicken Welfare in Southern Brazil. Available from: Braz J Poultry Sci (Rev Bras Cienc Avic). 2015;18(1).

45. Tuyttens FAM, Federici JF, Vanderhasselt RF, Goethals K, Duchateau L, Sans ECO, et al. Assessment of welfare of Brazilian and Belgian broiler flocks using the Welfare Quality protocol Poultry Sci. Poultry Science. 2015;94(8): 1758–66. doi: 10.3382/ps/pev167 26049803

46. Vasdal G, Moe RO, Jong ICd, Granquist EG. The relationship between measures of fear of humans and lameness in broiler chicken flocks. Animal. 2017;12(2): 334–339. doi: 10.1017/S1751731117001434 28683840.

47. Van Emous R. SMP-18004 Introduction of innovative broiler houses in Indonesia for a healthier future. Wageningen: Wageningen UR. Available from: Cited 11 March 2019.

48. JPE. The BroMaxx broiler housing system [BroMaxx vleeskuiken huisvestingssysteem]. No date. Available from: Cited 30 Nov 2018.

49. Naturalness Yeates J. and Welfare Animal. Animals. 2018;8(4): 53. doi: 10.3390/ani8040053 29621140

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