Lameness in Pregnant Sows Alters Placental Stress Response
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Animals, Handling, and Locomotion Assessment
2.2. Experimental Data Collection
Intrauterine Growth Restriction and Placental Cortisol and Cortisone—Farm 2
2.3. Statistical Analysis
3. Results
3.1. Locomotion and Reproductive Measures
3.2. Placental Measures
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Parada, M.S.; Bernardino, T.; Tatemoto, P.; Polo, G.; Zanella, A.J. The In-Utero Experience of Piglets Born from Sows with Lameness Shapes Their Life Trajectory. Sci. Rep. 2021, 11, 13052. [Google Scholar] [CrossRef] [PubMed]
- Anil, S.S.; Anil, L.; Deen, J. Effect of Lameness on Sow Longevity. J. Am. Vet. Med. Assoc. 2009, 235, 734–738. [Google Scholar] [CrossRef] [PubMed]
- Dewey, C.E.; Friendship, R.M.; Wilson, M.R. Clinical and Postmortem Examination of Sows Culled for Lameness. Can. Vet. J. 1993, 34, 555–556. [Google Scholar] [PubMed]
- Heinonen, M.; Oravainen, J.; Orro, T.; Seppa-Lassila, L.; Ala-Kurikka, E.; Virolainen, J.; Tast, A.; Peltoniemi, O.A.T. Lameness and Fertility of Sows and Gilts in Randomly Selected Loose-Housed Herds in Finland. Vet. Rec. 2006, 159, 383–387. [Google Scholar] [CrossRef]
- Engblom, L.; Lundeheim, N.; Dalin, A.M.; Andersson, K. Sow Removal in Swedish Commercial Herds. Livest. Sci. 2007, 106, 76–86. [Google Scholar] [CrossRef]
- Ison, S.H.; Eddie Clutton, R.; Di Giminiani, P.; Rutherford, K.M.D. A Review of Pain Assessment in Pigs. Front. Vet. Sci. 2016, 3, 108. [Google Scholar] [CrossRef]
- Sneddon, L.U.; Elwood, R.W.; Adamo, S.A.; Leach, M.C. Defining and Assessing Animal Pain. Anim. Behav. 2014, 97, 201–212. [Google Scholar] [CrossRef]
- Pluym, L.M.; Maes, D.; Van Weyenberg, S.; Van Nuffel, A. Risk Factors for Development of Lameness in Gestating Sows within the First Days after Moving to Group Housing. Vet. J. 2017, 220, 28–33. [Google Scholar] [CrossRef]
- van Riet, M.M.J.; Millet, S.; Aluwé, M.; Janssens, G.P.J. Impact of Nutrition on Lameness and Claw Health in Sows. Livest. Sci. 2013, 156, 25–35. [Google Scholar] [CrossRef]
- Jensen, T.B.; Bonde, M.K.; Kongsted, A.G.; Toft, N.; Sørensen, J.T. The Interrelationships between Clinical Signs and Their Effect on Involuntary Culling among Pregnant Sows in Group-Housing Systems. Animal 2010, 4, 1922–1928. [Google Scholar] [CrossRef]
- Heinonen, M.; Peltoniemi, O.; Valros, A. Impact of Lameness and Claw Lesions in Sows on Welfare, Health and Production. Livest. Sci. 2013, 156, 2–9. [Google Scholar] [CrossRef]
- Dijkhuizen, A.A.; Krabbenborg, R.M.M.; Huirne, R.B.M. Sow Replacement: A Comparison of Farmers’ Actual Decisions and Model Recommendations. Livest. Prod. Sci. 1989, 23, 207–218. [Google Scholar] [CrossRef]
- Whay, H.R.; Main, D.C.J.; Greent, L.E.; Webster, A.J.F.; Green, L.E.; Webster, A.J.F. Animal-Based Measures for the Assessment of Welfare State of Dairy Cattle, Pigs and Laying Hens: Consensus of Expert Opinion. Anim. Welf. 2003, 12, 205–217. [Google Scholar] [CrossRef]
- Seckl, J.R.; Holmes, M.C. Mechanisms of Disease: Glucocorticoids, Their Placental Metabolism and Fetal “programming” of Adult Pathophysiology. Nat. Clin. Pract. Endocrinol. Metab. 2007, 3, 479–488. [Google Scholar] [CrossRef]
- McTernan, C.L.; Draper, N.; Nicholson, H.; Chalder, S.M.; Driver, P.; Hewison, M.; Kilby, M.D.; Stewart, P.M. Reduced Placental 11β-Hydroxysteroid Dehydrogenase Type 2 MRNA Levels in Human Pregnancies Complicated by Intrauterine Growth Restriction: An Analysis of Possible Mechanisms. J. Clin. Endocrinol. Metab. 2001, 86, 4979–4983. [Google Scholar] [CrossRef]
- Kranendonk, G.; Hopster, H.; van Eerdenburg, F.; Van Reenen, K.; Fillerup, M.; De Groot, J.; Korte, M.; Taverne, M. Evaluation of Oral Administration of Cortisol as a Model for Prenatal Stress in Pregnant Sows. Am. J. Vet. Res. 2005, 66, 780–790. [Google Scholar] [CrossRef]
- Kramer, T.; Alberton, G.C. Prevalência de claudicação de porcas e condições Das Gaiolas de Gestação Em Granjas No Sul e Sudeste Do Brasil. In Proceedings of the VII Fórum Internacional de Suinocultura, Foz do Iguaçu, Brazil, 28–30 October 2014; pp. 331–332. [Google Scholar]
- Pluym, L.M.; Van Nuffel, A.; Dewulf, J.; Cools, A.; Vangroenweghe, F.; Van Hoorebeke, S.; Maes, D.; Van Nuffel, A.; Dewulf, J.; Cools, A.; et al. Prevalence and Risk Factors of Claw Lesions and Lameness in Pregnant Sows in Two Types of Group Housing. Vet. Med. (Praha) 2011, 56, 101–109. [Google Scholar] [CrossRef]
- Pluym, L.M.; Van Nuffel, A.; Van Weyenberg, S.; Maes, D. Prevalence of Lameness and Claw Lesions during Different Stages in the Reproductive Cycle of Sows and the Impact on Reproduction Results. Animal 2013, 7, 1174–1181. [Google Scholar] [CrossRef]
- Sobestiansky, J.; Wentz, I.; Souza da Silveira, P.R.; Munari, J.; Ribeiro de Freitas, A. Ocorrência e Caracterização Das Lesões Nos Cascos de Fêmeas Suínas Reprodutoras. Rev. Fac. Med. Vet. Zootec. Univ. São Paulo 1989, 26, 235–240. [Google Scholar] [CrossRef]
- D’Eath, R. Repeated Locomotion Scoring of a Sow Herd to Measure Lameness: Consistency over Time, the Effect of Sow Characteristics and Inter-Observer Reliability. Anim. Welf. 2012, 21, 219–231. [Google Scholar] [CrossRef]
- Hales, J.; Moustsen, V.A.; Nielsen, M.B.F.; Hansen, C.F. Individual Physical Characteristics of Neonatal Piglets Affect Preweaning Survival of Piglets Born in a Noncrated System. J. Anim. Sci. 2013, 91, 4991–5003. [Google Scholar] [CrossRef] [PubMed]
- Rettenbacher, S.; Möstl, E.; Hackl, R.; Ghareeb, K.; Palme, R. Measurement of Corticosterone Metabolites in Chicken Droppings. Br. Poult. Sci. 2004, 45, 704–711. [Google Scholar] [CrossRef] [PubMed]
- Palme, R.; Möstl, E. Measurement of Cortisol Metabolites in Faeces of Sheep as a Parameter of Cortisol Concentration in Blood. Int. J. Mammal. Biol. 1997, 62 (Suppl. 2), 192–197. [Google Scholar]
- Tatemoto, P.; Bernardino, T.; Alves, L.; Zanella, A.J. Sham-Chewing in Sows Is Associated With Decreased Fear Responses in Their Offspring. Front. Vet. Sci. 2019, 6, 390. [Google Scholar] [CrossRef]
- Bradford, M.M. A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Anal. Biochem. 1976, 72, 248–254. [Google Scholar] [CrossRef]
- RStudio Team. RStudio: Integrated Development Environment for R; RStudio Team: Vienna, Austria, 2020. [Google Scholar]
- Kuznetsova, A.; Brockhoff, P.B.; Christensen, R.H.B. LmerTest Package: Tests in Linear Mixed Effects Models. J. Stat. Softw. 2017, 82, 1–26. [Google Scholar] [CrossRef]
- Wickham, H. Jennifer Bryan Readxl: Read Excel Files. 2022. Available online: https://cran.r-project.org/web/packages/readxl/index.html (accessed on 17 May 2023).
- Wickham, H.; Averick, M.; Bryan, J.; Chang, W.; McGowan, L.; François, R.; Grolemund, G.; Hayes, A.; Henry, L.; Hester, J.; et al. Welcome to the Tidyverse. J. Open Source Softw. 2019, 4, 1686. [Google Scholar] [CrossRef]
- Kassambara, A. Rstatix: Pipe-Friendly Framework for Basic Statistical Tests. 2021. Available online: https://cran.r-project.org/web/packages/rstatix/index.html (accessed on 17 May 2023).
- Lenth, R.V.; Buerkner, P.; Giné-Vázquez, I.; Herve, M.; Jung, M.; Love, J.; Miguez, F.; Riebl, H.; Singmann, H. Emmeans: Estimated Marginal Means, Aka Least-Squares Means. Repository CRAN. 2022. Available online: https://cran.r-project.org/web/packages/emmeans/index.html (accessed on 17 May 2023).
- Lüdecke, D.; Ben-Shachar, M.S.; Patil, I.; Wiernik, B.M.; Makowski, D. Easystats: Framework for Easy Statistical Modeling, Visualization, and Reporting. Repository CRAN. 2022. Available online: https://cran.r-project.org/web/packages/easystats/index.html (accessed on 17 May 2023).
- Cox, D.F. Survival and Gestation in Pig. Evolution 1967, 21, 195–196. [Google Scholar] [CrossRef]
- Kattesh, H.G.; Kornegay, E.T.; Knight, J.W.; Gwazdauskas, F.G.; Thomas, H.R.; Notter, D.R. Glucocorticoid Concentrations, Corticosteroid Binding Protein Characteristics and Reproduction Performance of Sows and Gilts Subjected to Applied Stress during Mid-Gestation. J. Anim. Sci. 1980, 50, 897–905. [Google Scholar] [CrossRef]
- Ashworth, C.J.; Hogg, C.O.; Hoeks, C.W.F.; Donald, R.D.; Duncan, W.C.; Lawrence, A.B.; Rutherford, K.M.D. Pre-Natal Social Stress and Post-Natal Pain Affect the Developing Pig Reproductive Axis. Reproduction 2011, 142, 907–914. [Google Scholar] [CrossRef]
- Seckl, J.R. Prenatal Glucocorticoids and Long-Term Programming. Eur. J. Endocrinol. Suppl. 2004, 151, 49–62. [Google Scholar] [CrossRef]
- Pairis-Garcia, M.D.; Karriker, L.A.; Johnson, A.K.; Kukanich, B.; Wulf, L.; Sander, S.; Millman, S.T.; Stalder, K.J.; Coetzee, J.F. Pharmacokinetics of Flunixin Meglumine in Mature Swine after Intravenous, Intramuscular and Oral Administration. BMC Vet. Res. 2013, 9, 165. [Google Scholar] [CrossRef]
- Schoos, A.; Devreese, M.; Maes, D.G. Use of Non-Steroidal Anti-Inflammatory Drugs in Porcine Health Management. Vet. Rec. 2019, 185, 172. [Google Scholar] [CrossRef]
- Hellhammer, D.H.; Wüst, S.; Kudielka, B.M. Salivary Cortisol as a Biomarker in Stress Research. Psychoneuroendocrinology 2009, 34, 163–171. [Google Scholar] [CrossRef]
- Pluym, L.; Van Nuffel, A.; Maes, D. Treatment and Prevention of Lameness with Special Emphasis on Claw Disorders in Group-Housed Sows. Livest. Sci. 2013, 156, 36–43. [Google Scholar] [CrossRef]
Score | Label | Description |
---|---|---|
0 | Normal | Even strides, rear end sways slightly while walking, pig is able to accelerate and change direction rapidly. Stands normally. |
1 | Stiff | Abnormal stride length, movements no longer fluent, pig appears stiff. Pig still able to accelerate and change direction. Stands normally. |
2 | Slight lameness | Shortened stride, lameness detected, swagger of rear end while walking, no hindrance in pig’s agility. Uneven posture while standing. |
3 | Lame | Pigs slow to get up (may dog sit), shortened stride, minimum weight-bearing on affected limb (standing on toes), swagger of rear end while walking. May still trot and gallop. |
4 | Limping | Pig reluctant to get up, holds limb off floor while standing, avoids placing affected limb on the floor while moving. |
5 | Downer | Pig unresponsive: does not move and struggles to stand when encouraged to do so. |
Groups | Number of Sows | Proportion (%) | |
---|---|---|---|
Farm 1 | NL | 224 | 56.4 |
L | 173 | 43.6 | |
Total | 397 | - | |
Farm 2 | G1 | 31 | 27.2 |
G2 | 59 | 51.8 | |
G3 | 24 | 21.1 | |
Total | 114 | - |
Variable | No Lame N = 16 | Lame N = 14 | Effect p-Value | ||||
---|---|---|---|---|---|---|---|
Mean | SEM | Mean | SEM | Locomotion Group | Parity | Litter Size | |
Gestation length (days) | 115.6 | 0.47 | 114.5 | 0.24 | 0.06 t | 0.68 | 0.18 |
Average litter weight (kg) | 18.9 | 1.12 | 18.8 | 0.97 | 0.90 | 0.01 | <0.01 |
Average piglet weight (kg) | 1.60 | 0.09 | 1.50 | 0.07 | 0.16 | 0.18 | <0.01 |
Number of male piglets | 6.00 | 0.69 | 6.90 | 0.65 | 0.17 | <0.05 | <0.01 |
Number of female piglets | 6.70 | 0.59 | 6.20 | 0.65 | 0.44 | 0.60 | <0.01 |
Total number of piglets | 13.6 | 1.01 | 14.2 | 0.97 | 0.65 | 0.57 | - |
Number of live piglets | 12.7 | 0.95 | 13.1 | 0.89 | 0.32 | <0.01 | <0.01 |
Number of mummified piglets | 0.20 | 0.19 | 0.30 | 0.16 | 0.70 | 0.74 | <0.05 |
Number of stillborn piglets | 0.70 | 0.34 | 0.80 | 0.25 | 0.82 | 0.54 | 0.36 |
Variable | G1 N = 12 | G2 N = 13 | G3 N = 14 | Effect p-Value | Tukey Adjusted p-Value | |||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Mean | SEM | Mean | SEM | Mean | SEM | Locomotion Group | Parity | Litter Size | G1–G2 | G1–G3 | G2–G3 | |
Gestation length (days) | 116.1 | 0.33 | 114.6 | 0.49 | 115.3 | 0.40 | 0.06 t | 0.29 | 0.95 | 0.14 | 0.93 | 0.29 |
Average litter weight (kg) | 18.1 | 1.22 | 18.8 | 1.27 | 18.7 | 0.94 | 0.92 | 0.91 | <0.05 | 0.94 | 0.94 | 0.77 |
Average piglet weight (kg) | 1.50 | 0.08 | 1.40 | 0.06 | 1.30 | 0.07 | 0.19 | 0.66 | <0.001 | 0.87 | 0.59 | 0.85 |
Number of male piglets | 6.20 | 0.64 | 7.10 | 0.75 | 7.20 | 0.66 | 0.49 | 0.41 | <0.01 | 0.78 | 0.84 | 0.99 |
Number of female piglets | 6.10 | 0.87 | 6.40 | 0.87 | 6.80 | 0.54 | 0.79 | 0.46 | 0.02 | 0.98 | 0.99 | 0.95 |
Total number of piglets | 15.0 | 0.75 | 15.8 | 1.10 | 16.4 | 0.88 | 0.60 | 0.82 | - | 0.98 | 0.79 | 0.87 |
Number of live piglets | 12.7 | 0.87 | 14.2 | 1.01 | 14.3 | 0.58 | 0.02 | 0.14 | <0.001 | 0.25 | 0.99 | 0.21 |
Number of mummified piglets | 0.60 | 0.26 | 0.30 | 0.13 | 0.90 | 0.38 | 0.22 | 0.08 t | 0.08 t | 0.85 | 0.47 | 0.19 |
Number of stillborn piglets | 1.70 | 0.45 | 1.30 | 0.47 | 1.20 | 0.32 | 0.60 | <0.01 | 0.11 | 0.24 | 0.68 | 0.71 |
Number of piglets dead in the 1st week | 1.20 | 0.28 | 2.50 | 0.67 | 2.20 | 0.74 | 0.25 | 0.44 | <0.001 | 0.22 | 0.52 | 0.83 |
Placental cortisol/cortisone ratio | 0.77 | 0.08 | 1.17 | 0.15 | 0.78 | 0.09 | 0.03 | 0.47 | 0.16 | 0.05 | 0.93 | 0.02 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Parada Sarmiento, M.; Lanzoni, L.; Sabei, L.; Chincarini, M.; Palme, R.; Zanella, A.J.; Vignola, G. Lameness in Pregnant Sows Alters Placental Stress Response. Animals 2023, 13, 1722. https://doi.org/10.3390/ani13111722
Parada Sarmiento M, Lanzoni L, Sabei L, Chincarini M, Palme R, Zanella AJ, Vignola G. Lameness in Pregnant Sows Alters Placental Stress Response. Animals. 2023; 13(11):1722. https://doi.org/10.3390/ani13111722
Chicago/Turabian StyleParada Sarmiento, Marisol, Lydia Lanzoni, Leandro Sabei, Matteo Chincarini, Rupert Palme, Adroaldo José Zanella, and Giorgio Vignola. 2023. "Lameness in Pregnant Sows Alters Placental Stress Response" Animals 13, no. 11: 1722. https://doi.org/10.3390/ani13111722
APA StyleParada Sarmiento, M., Lanzoni, L., Sabei, L., Chincarini, M., Palme, R., Zanella, A. J., & Vignola, G. (2023). Lameness in Pregnant Sows Alters Placental Stress Response. Animals, 13(11), 1722. https://doi.org/10.3390/ani13111722