in

Regular outdoor access decreases stress with positive effects on the health of growing pigs raised on a conventional farm


Abstract

Conventional pig production systems are characterized by fully slatted floors and space restrictions, hindering pigs from foraging and roaming. In contrast, providing pigs with outdoor access allows them to express a wide range of behaviors, but might challenge their health. In this context, we hypothesized that giving pigs regular outdoor access might lower stress exposure with positive impacts for health and welfare. A total of 145 male and 148 female pigs, housed in a conventional barn, were provided (OUT) or not (IN) with access to a grassy paddock twice a week from the age of 77 days to slaughter. The OUT pigs had lower salivary cortisol levels than the IN pigs. Regular access to a pasture also lowered the severity of body lesions. While it had no consequences on animal growth, it was associated with a reduced frequency of diarrhea in pigs. Despite lower leukocytes counts in the OUT pigs compared to the IN ones, higher proportion of the OUT pigs developed humoral response against L. intracellularis. Thus, providing regular access to a paddock for growing pigs had positive impacts on their health and welfare, with no consequence on their performance.

Data availability

The data generated and analyzed in the current study are available in Supplementary Table 1.

References

  1. Sato, P., Hötzel, M. J. & Von Keyserlingk, M. A. G. American citizens’ views of an ideal pig farm. Animals 7, 64. https://doi.org/10.3390/ani7080064 (2017).

    Google Scholar 

  2. Thorslund, C. A. H., Aaslyng, M. D. & Lassen, J. Perceived importance and responsibility for market-driven pig welfare: literature review. Meat Sci. 125, 37–45. https://doi.org/10.1016/j.meatsci.2016.11.008 (2017).

    Google Scholar 

  3. Towaza, A., Tanaka, S. & Sato, S. The effects of components of grazing system on welfare of fattening Pigs, Asian Australas. J. Anim. Sci. 29, 428–435. https://doi.org/10.5713/ajas.15.0190 (2016).

    Google Scholar 

  4. Stolba, A. & Wood-Gush, D. G. M. The behaviour of pigs in a semi-natural environment. Anim. Sci. 48, 419–425. https://doi.org/10.1017/S0003356100040411 (1989).

    Google Scholar 

  5. Stäbler, R., Patzkéwitsch, D., Reese, S., Erhard, M. & Hartmannsgruber, S. Behavior of domestic pigs under near-natural forest conditions with ad libitum supplementary feeding. J. Veterinary Behav. 48, 20–35. https://doi.org/10.1016/j.jveb.2021.10.011 (2022).

    Google Scholar 

  6. Park, H. S., Min, B. & Oh, S. H. Research trends in outdoor pig production: A review. Asian-Australas J. Anim. Sci. 30, 1207–1214. https://doi.org/10.5713/ajas.17.0330 (2017).

    Google Scholar 

  7. Mateos, G. G., Corrales, N. L., Talegón, G. & Aguirre, L. Pig meat production in the European Union-27: current status, challenges, and future trends. Anim. Biosci. 37, 755–774. https://doi.org/10.5713/ab.23.0496 (2024).

    Google Scholar 

  8. Bellini, S. The pig sector in the European Union. In Understanding and Combatting African Swine Fever 183–195 (Wageningen Academic, 2021). https://doi.org/10.3920/978-90-8686-910-7_7.

    Google Scholar 

  9. Kittawornrat, A. & Zimmerman, J. J. Toward a better understanding of pig behavior and pig welfare. Anim. Health Res. Reviews 12, 25–32. https://doi.org/10.1017/S1466252310000174 (2011).

    Google Scholar 

  10. Studnitz, M., Jensen, M. B. & Pedersen, L. J. Why do pigs root and in what will they root? A review on the exploratory behaviour of pigs in relation to environmental enrichment. Appl. Anim. Behav. Sci. 107, 183–197. https://doi.org/10.1016/j.applanim.2006.11.013 (2007).

    Google Scholar 

  11. EFSA Panel on Animal Health and Welfare et al. Welfare of pigs on farm. EFSA J. 20, e07421. https://doi.org/10.2903/j.efsa.2022.7421 (2022).

    Google Scholar 

  12. Brajon, S., Tallet, C., Merlot, E. & Lollivier, V. Barriers and drivers of farmers to provide outdoor access in pig farming systems: a qualitative study. Animal 18, 101138. https://doi.org/10.1016/j.animal.2024.101138 (2024).

    Google Scholar 

  13. Spooner, J. M., Schuppli, C. A. & Fraser, D. Attitudes of Canadian pig producers toward animal welfare. J. Agric. Environ. Ethics. 27, 569–589. https://doi.org/10.1007/s10806-013-9477-4 (2014).

    Google Scholar 

  14. Delsart, M. et al. Descriptive epidemiology of the main internal parasites on alternative pig farms in France. J. Parasitol. 108, 306–321. https://doi.org/10.1645/21-126 (2022).

    Google Scholar 

  15. Lindgren, K., Gunnarsson, S., Höglund, J., Lindahl, C. & Roepstorff, A. Nematode parasite eggs in pasture soils and pigs on organic farms in Sweden. Org. Agr. 10, 289–300. https://doi.org/10.1007/s13165-019-00273-3 (2020).

    Google Scholar 

  16. Gebreyes, W. A., Bahnson, P. B., Funk, J. A., McKean, J. & Patchanee, P. Seroprevalence of Trichinella, Toxoplasma, and Salmonella in antimicrobial-free and conventional swine production systems. Foodborne Pathog. Dis. 5, 199–203. https://doi.org/10.1089/fpd.2007.0071 (2008).

    Google Scholar 

  17. Etterlin, P. E. et al. Effects of free-range and confined housing on joint health in a herd of fattening pigs. BMC Vet. Res. 10, 208. https://doi.org/10.1186/s12917-014-0208-5 (2014).

    Google Scholar 

  18. Pandolfi, F., Kyriazakis, I., Stoddart, K., Wainwright, N. & Edwards, S. A. The real welfare scheme: identification of risk and protective factors for welfare outcomes in commercial pig farms in the UK. Prev. Vet. Med. 146, 34–43. https://doi.org/10.1016/j.prevetmed.2017.07.008 (2017).

    Google Scholar 

  19. Leeb, C. et al. Effects of three husbandry systems on health, welfare and productivity of organic pigs. Animal 13, 2025–2033. https://doi.org/10.1017/S1751731119000041 (2019).

    Google Scholar 

  20. Düpjan, S. & Dawkins, M. S. Animal welfare and resistance to disease: Interaction of affective states and the immune system. Front. Vet. Sci. https://doi.org/10.3389/fvets.2022.929805 (2022).

    Google Scholar 

  21. Millet, S., Moons, C. P., Van Oeckel, M. J. & Janssens, G. P. Welfare, performance and meat quality of fattening pigs in alternative housing and management systems: a review. J. Sci. Food. Agric. 85, 709–719. https://doi.org/10.1002/jsfa.2033 (2005).

    Google Scholar 

  22. Patience, J. F., Rossoni-Serão, M. C. & Gutiérrez, N. A. A review of feed efficiency in swine: biology and application. J. Anim. Sci. Biotechnol. 6, 33. https://doi.org/10.1186/s40104-015-0031-2 (2015).

    Google Scholar 

  23. Hervé, J. et al. Pathogen exposure influences immune parameters around weaning in pigs reared in commercial farms. BMC Immunol. 23, 61. https://doi.org/10.1186/s12865-022-00534-z (2022).

    Google Scholar 

  24. Gavaud, S. et al. Effects of improved early-life conditions on health, welfare, and performance of pigs raised on a conventional farm. Animal 17, 100810. https://doi.org/10.1016/j.animal.2023.100810 (2023).

    Google Scholar 

  25. Jacobson, M., Wallgren, P., Nordengrahn, A., Merza, M. & Emanuelson, U. Evaluation of a blocking ELISA for the detection of antibodies against Lawsonia intracellularis in pig sera. Acta Vet. Scand. 53, 23. https://doi.org/10.1186/1751-0147-53-23 (2011).

    Google Scholar 

  26. Carroll, G. A. et al. Identifying physiological measures of lifetime welfare status in pigs: exploring the usefulness of haptoglobin, C- reactive protein and hair cortisol sampled at the time of slaughter. Ir. Veterinary J. 71, 8. https://doi.org/10.1186/s13620-018-0118-0 (2018).

    Google Scholar 

  27. Calderón Díaz, J. A., Fahey, A. G. & Boyle, L. A. Effects of gestation housing system and floor type during lactation on locomotory ability; body, limb, and claw lesions; and lying-down behavior of lactating sows1. J. Anim. Sci. 92, 1675–1685. https://doi.org/10.2527/jas.2013-6279 (2014).

    Google Scholar 

  28. R Core Team. R: A language and environment for statistical computing (2022). https://www.R-project.org/

  29. Cerón, J. J. et al. Basics for the potential use of saliva to evaluate stress, inflammation, immune system, and redox homeostasis in pigs. BMC Vet. Res. 18, 81. https://doi.org/10.1186/s12917-022-03176-w (2022).

    Google Scholar 

  30. Boissy, A. et al. Assessment of positive emotions in animals to improve their welfare. Physiol. Behav. 92, 375–397. https://doi.org/10.1016/j.physbeh.2007.02.003 (2007).

    Google Scholar 

  31. Foury, A. et al. Alternative rearing systems in pigs: consequences on stress indicators at slaughter and meat quality. Animal 5, 1620–1625. https://doi.org/10.1017/S1751731111000784 (2011).

    Google Scholar 

  32. Levallois, P. et al. Hair cortisol concentration in finishing pigs on commercial farms: variability between pigs, batches, and farms. Front. Vet. Sci. https://doi.org/10.3389/fvets.2023.1298756 (2024).

    Google Scholar 

  33. Dostálová, A., Svitáková, A., Bureš, D., Vališ, L. & Volek, Z. Effect of an outdoor access system on the growth performance, carcass characteristics, and Longissimus lumborum muscle meat quality of the Prestice black-pied pig breed. Animals 10, 1244. https://doi.org/10.3390/ani10081244 (2020).

    Google Scholar 

  34. EdwardsS.A. Intake of nutrients from pasture by pigs. Proc. Nutr. Soc. 62, 257–265. https://doi.org/10.1079/PNS2002199 (2003).

    Google Scholar 

  35. Buijs, S., McFarland, C., Olave, R. & Muns, R. Health and performance of fattening pigs reared in grassland and agroforestry systems in a temperate maritime climate. Animal 19, 101616. https://doi.org/10.1016/j.animal.2025.101616 (2025).

    Google Scholar 

  36. Etterlin, P. E. et al. Osteochondrosis, but not lameness, is more frequent among free-range pigs than confined herd-mates. Acta Vet. Scand. 57, 63. https://doi.org/10.1186/s13028-015-0154-7 (2015).

    Google Scholar 

  37. Wallander, C. et al. Pasture is a risk factor for Toxoplasma gondii infection in fattening pigs. Vet. Parasitol. 224, 27–32. https://doi.org/10.1016/j.vetpar.2016.05.005 (2016).

    Google Scholar 

  38. Brewer, M. T. & Greve, J. H. Internal Parasites. In Diseases of Swine 1028–1040 (Wiley, 2019). https://doi.org/10.1002/9781119350927.ch67.

    Google Scholar 

  39. Lindsay, D. S., Dubey, J. P. & Santín-Durán, M. Coccidia and Other Protozoa. In Diseases of Swine 1015–1027 (Wiley, 2019). https://doi.org/10.1002/9781119350927.ch66.

    Google Scholar 

  40. van Dixhoorn, Ingrid, I. et al. Stockhofe-Zurwieden, enriched housing reduces disease susceptibility to co-Infection with Porcine reproductive and respiratory virus (PRRSV) and Actinobacillus pleuropneumoniae (A. pleuropneumoniae) in young pigs. PLOS ONE 11, e0161832. https://doi.org/10.1371/journal.pone.0161832 (2016).

    Google Scholar 

  41. Campillo, M., Smith, S. H., Gaily, D. L. & Opriessnig, T. Review of methods for the detection of lawsonia intracellularis infection in pigs. J. Vet. Diagn. Invest. 33, 621–631. https://doi.org/10.1177/10406387211003551 (2021).

    Google Scholar 

  42. Glaser, R. & Kiecolt-Glaser, J. K. Stress-induced immune dysfunction: implications for health. Nat. Rev. Immunol. 5, 243–251. https://doi.org/10.1038/nri1571 (2005).

    Google Scholar 

  43. Bane, D. P., Neumann, E., Gebhart, C. J., Gardner, I. A. & Norby, B. Porcine proliferative enteropathy: a case-control study in swine herds in the united States. J. Swine Health Prod. 9, 155–158 (2001). https://www.swinevet.com/shap/issues/v9n4/v9n4p155.html

    Google Scholar 

  44. Steinerová, K. et al. Rearing pigs with play opportunities: the effects on disease resilience in pigs experimentally inoculated with PRRSV. Front. Vet. Sci. https://doi.org/10.3389/fvets.2024.1460993 (2024).

    Google Scholar 

  45. Reimert, I., Rodenburg, T. B., Ursinus, W. W., Kemp, B. & Bolhuis, J. E. Selection based on indirect genetic effects for growth, environmental enrichment and coping style affect the immune status of pigs. PLoS ONE 9, e108700. https://doi.org/10.1371/journal.pone.0108700 (2014).

    Google Scholar 

  46. Bacou, E. et al. Acute social stress-induced immunomodulation in pigs high and low responders to ACTH. Physiol. Behav. 169, 1–8. https://doi.org/10.1016/j.physbeh.2016.11.012 (2017).

    Google Scholar 

  47. ter Horst, R. et al. Seasonal and nonseasonal longitudinal variation of immune function. J. Immunol. 207, 696–708. https://doi.org/10.4049/jimmunol.2000133 (2021).

    Google Scholar 

  48. Moeser, A. J., Roney, A., Fardisi, M. & Thelen, K. Biological sex: an understudied factor driving disease susceptibility in pigs. J. Anim. Sci. 100, skac146. https://doi.org/10.1093/jas/skac146 (2022).

    Google Scholar 

  49. Ruckli, A. K. et al. Access to bedding and outdoor runs for growing-finishing pigs: is it possible to improve welfare without increasing environmental impacts? Animal 18, 101155. https://doi.org/10.1016/j.animal.2024.101155 (2024).

    Google Scholar 

  50. Wimmler, C., Vermeer, H. M., Leeb, C., Salomon, E. & Andersen, H. M. L. Review: concrete outdoor runs for organic growing-finishing pigs – a legislative, ethological and environmental perspective. Animal 16, 100435. https://doi.org/10.1016/j.animal.2021.100435 (2022).

    Google Scholar 

  51. Bartlett, H. et al. Trade-offs in the externalities of pig production are not inevitable. Nat. Food. 5, 312–322. https://doi.org/10.1038/s43016-024-00921-2 (2024).

    Google Scholar 

Download references

Acknowledgements

We sincerely thank Charline Niort and Grégory Khelifi from the GenESI research facility as well as Morgane Rémond, the veterinarian of the farm. We also gratefully acknowledge everyone at IECM, particularly the interns for their work on sample analyses, as well as Laboniris for technical support. We express our deep gratitude to INRAE, especially the SANBA Metaprogram, for supporting this work. We acknowledge Labocea (Ploufragan, France) for the rapid analyses of L. intracellularis in feces using PCR.

Funding

AJ was supported by the INRAE through her PhD fellowship. The study was funded by the INRAE Metaprogram SANBA through the PANORAMA project, supervised by CT and JH.

Author information

Authors and Affiliations

Authors

Contributions

BL, CT, and JH designed the experiment. CT and JH supervised the project. AJ, FG, JL, SG, KH, TT, SF, BL, and JH conducted the experiments. AJ, JL, KH, BL, and JH analyzed the results. AJ, BL, and JH interpreted the results and wrote the main manuscript text. All authors have read and approved the submitted version of the manuscript.

Corresponding author

Correspondence to
Julie Hervé.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary Material 1

Supplementary Material 2

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.

Reprints and permissions

About this article

Cite this article

Jahoui, A., Lion, J., Guiraud, F. et al. Regular outdoor access decreases stress with positive effects on the health of growing pigs raised on a conventional farm.
Sci Rep (2026). https://doi.org/10.1038/s41598-026-38461-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41598-026-38461-3

Keywords

  • Outdoor access
  • Pig
  • Health
  • Cortisol
  • Immunity


Source: Ecology - nature.com

Enhancing the classification of spectrally similar land use/land cover classes using transfer learning in arid regions

A novel hybrid model for species distribution prediction of soil-transmitted helminthiasis (STH) under soil temperature conditions using Random Forest and Particle Swarm Optimization Algorithm

Back to Top