Introduction
Sub-optimal housing and management pose risks for chronic stress in sows which negatively affects their welfare, health and productivity (Merlot et al. Reference Merlot, Quesnel and Prunier2013; Martinez-Miro et al. Reference Martinez-Miro, Tecles, Ramon, Escribano, Hernandez, Madrid, Orengo, Martinez-Subiela, Manteca and Ceron2016; Lagoda et al. Reference Lagoda, Marchewka, O’Driscoll and Boyle2022). Moreover, the detrimental effects of chronic stress can extend beyond the sow to compromise the welfare and resilience of her offspring through the process of prenatal stress (Braastad Reference Braastad1998; Parada Sarmiento et al. Reference Parada Sarmiento, Bernardino, Tatemoto, Polo and Zanella2021). Prenatally stressed piglets (for example, piglets born to sows subjected to social stress resulting from mixing with unfamiliar individuals; Rault et al. Reference Rault, Mack, Carter, Garner, Marchant-Forde, Richert and Lay2013) show impaired stress-coping ability and altered behaviour (i.e. longer latency to the first escape attempt) in contrast to non-prenatally stressed piglets (Weinstock Reference Weinstock1997; Rault et al. Reference Rault, Mack, Carter, Garner, Marchant-Forde, Richert and Lay2013). They also have reduced immunity, and are consequently more susceptible to disease (Tuchscherer et al. Reference Tuchscherer, Kanitz, Otten and Tuchscherer2002; Albernaz-Gonçalves et al. Reference Albernaz-Gonçalves, Olmos Antillón and Hötzel2022), particularly diarrhoea, both during the suckling and post-weaning periods (Friendship Reference Friendship2020). Diarrhoea is the main reason for antibiotic use in young pigs (Albernaz-Gonçalves et al. Reference Albernaz-Gonçalves, Olmos and Hötzel2021). As antimicrobial treatment for diarrhoea is applied to all piglets in the pen, it is a major contributor to antibiotic use in pig production (Campbell et al. Reference Campbell, Crenshaw and Polo2013; Xu et al. Reference Xu, Li, Yang, Li, Liang, Wu and Pu2018; Albernaz-Gonçalves et al. Reference Albernaz-Gonçalves, Olmos and Hötzel2021). This, combined with the on-farm prophylactic use of in-feed antibiotics, is a risk factor for the development of antimicrobial resistance (Koju et al. Reference Koju, Shrestha, Shrestha, Tamrakar, Rai, Shrestha, Madhup, Katuwal, Shrestha and Shrestha2022; O’Neill Reference O’Neill2022).
The threat of antimicrobial resistance generated interest in the development of ‘drug-free’ methods of improving immunity to optimise animal health (Xu et al. Reference Xu, Li, Yang, Li, Liang, Wu and Pu2018; Dawkins Reference Dawkins2019; Albernaz-Gonçalves et al. Reference Albernaz-Gonçalves, Olmos Antillón and Hötzel2022). Dawkins (Reference Dawkins2019) suggests the potential of good management and higher standards of welfare to act as preventative medicine. In line with this, van Dixhoorn et al. (Reference van Dixhoorn, Reimert, Middelkoop, Bolhuis, Wisselink, Groot Koerkamp, Kemp and Stockhofe-Zurwieden2016) showed that pigs housed in enriched pens (social and environmental enrichment) cleared viral PRRSV RNA from blood serum faster, developed fewer lung lesions, and had lower levels of pneumonia compared to pigs from barren pens. In addition, pigs in enriched pens showed less stress-related behaviour and differed immunologically and clinically from pigs in barren pens. Moreover, sows housed in larger pens with deep straw bedding maintained to a good standard of hygiene had lower granulocyte counts (Merlot et al. Reference Merlot, Pastorelli, Prunier, Pere, Louveau, Lefaucheur, Perruchot, Meunier-Salaun, Gardan-Salmon, Gondret and Quesnel2019), and lower concentrations of blood haptoglobin (Merlot et al. Reference Merlot, Calvar and Prunier2017), indicative of lower levels of microbial infection, inflammation and stress. These studies demonstrate the association between improved welfare and health (Fraser Reference Fraser2009).
Furthermore, maternal and prenatal stress are linked, so improving sow welfare during gestation could reduce prenatal stress levels acting on developing offspring in utero (Tuchscherer et al. Reference Tuchscherer, Kanitz, Otten and Tuchscherer2002; Kranendonk et al. Reference Kranendonk, Mulder, Parvizi and Taverne2008), translating into improved health and resilience of piglets early (Rault et al. Reference Rault, Mack, Carter, Garner, Marchant-Forde, Richert and Lay2013), and potentially later (Jarvis et al. Reference Jarvis, Moinard, Robson, Baxter, Ormandy, Douglas, Seckl, Russell and Lawrence2006; Merlot et al. Reference Merlot, Calvar and Prunier2017, Reference Merlot, Pastorelli, Prunier, Pere, Louveau, Lefaucheur, Perruchot, Meunier-Salaun, Gardan-Salmon, Gondret and Quesnel2019) in life. For instance, sows on deep straw bedding and in larger pens (Merlot et al. Reference Merlot, Calvar and Prunier2017; Quesnel et al. Reference Quesnel, Pere, Louveau, Lefaucheur, Perruchot, Prunier, Pastorelli, Meunier-Salaun, Gardan-Salmon, Merlot and Gondret2019a), or provided with enrichment (Quesnel et al. Reference Quesnel, Peuteman, Pere, Louveau, Lefaucheur, Perruchot, Prunier, Meunier-Salaun, Gardan-Salmon, Gondret and Merlot2019b) produced offspring with better health. Quesnel et al. (Reference Quesnel, Pere, Louveau, Lefaucheur, Perruchot, Prunier, Pastorelli, Meunier-Salaun, Gardan-Salmon, Merlot and Gondret2019a) demonstrated compromised tissue maturity (lighter gut and lower glycogen content of the longissimus muscle) in piglets born to sows from conventional, non-enriched pens, compared to piglets born to sows from enriched pens. In addition, Quesnel et al. (Reference Quesnel, Pere, Louveau, Lefaucheur, Perruchot, Prunier, Pastorelli, Meunier-Salaun, Gardan-Salmon, Merlot and Gondret2019a) and Merlot et al. (Reference Merlot, Calvar and Prunier2017) recorded lower mortality 12 h after birth, and lower pre-weaning mortality for litters of sows housed in enriched pens during pregnancy (compared to barren pens). However, these findings should be interpreted with caution, as in some instances prenatal stress can be advantageous by preparing offspring for their future environment. For instance, prenatal stress resulting from inadequate maternal nutrition can improve offspring resilience by modifying their metabolic phenotype to better use available resources later in life, and thus ensure greater resilience and survivability (Gonzalez-Bulnes et al. Reference Gonzalez-Bulnes, Astiz, Ovilo, Lopez-Bote, Torres-Rovira, Barbero, Ayuso, Garcia-Contreras and Vazquez-Gomez2016).
Although additional space or deep straw bedding certainly improves sow welfare (Merlot et al. Reference Merlot, Calvar and Prunier2017; Quesnel et al. Reference Quesnel, Pere, Louveau, Lefaucheur, Perruchot, Prunier, Pastorelli, Meunier-Salaun, Gardan-Salmon, Merlot and Gondret2019a,Reference Quesnel, Peuteman, Pere, Louveau, Lefaucheur, Perruchot, Prunier, Meunier-Salaun, Gardan-Salmon, Gondret and Merlotb), such approaches are potentially disruptive to the management or operation of the farm (Winkel et al. Reference Winkel, von Meyer-Höfer and Heise2020; Lagoda et al. Reference Lagoda, O’Driscoll, Galli, Marchewka and Boyle2023). In our sister paper (Lagoda et al. Reference Lagoda, O’Driscoll, Galli, Marchewka and Boyle2023), we demonstrated that the implementation of a number of smaller, incremental improvements to conventional gestation housing (rubber mats, manila ropes and foraging substrates provided in rooting towers) can improve sow welfare. In addressing psychological and physical stressors experienced by pregnant sows, levels of oral stereotypies and tear-stain scores were lower, which is likely indicative of reduced chronic stress.
Chronic stress compromises immune function, and potentially contributes to a chronic inflammatory response (Salak-Johnson & McGlone Reference Salak-Johnson and McGlone2007; Xiong et al. Reference Xiong, Cao, Xiao, Wu, Yi, Jiang and Wang2022). Levels of acute phase proteins, such as haptoglobin, are increased during systemic inflammation, and hence can be used as stress markers (Wang et al. Reference Wang, Kinzie, Berger, S-K and Baumann2001), in addition to traditional measures of cortisol. Specifically, haptoglobin in pigs is a ‘moderate slow’ acute phase protein which can be used to assess the immune status, and thus chronic stress under different conditions, over a prolonged period (Millet et al. Reference Millet, Cox, Buyse, Goddeeris and Janssens2005; Murata Reference Murata2007; Cerón et al. Reference Cerón, Contreras-Aguilar, Escribano, Martínez-Miró, López-Martínez, Ortín-Bustillo, Franco-Martínez, Rubio, Muñoz-Prieto and Tvarijonaviciute2022). For example, pigs housed in an organic production system showed lower haptoglobin levels at slaughter, indicating more stress resistance compared to pigs from a conventional production system (Millet et al. Reference Millet, Cox, Buyse, Goddeeris and Janssens2005). Thus, haptoglobin can reflect levels of chronic stress (Millet et al. Reference Millet, Cox, Buyse, Goddeeris and Janssens2005).
The objective of this study was to determine if improvements to welfare associated with less chronic stress during gestation would translate into a reduced inflammatory response in sows in late pregnancy, and whether this, in turn, could improve reproductive performance and contribute to better health of the offspring.
Materials and methods
Ethical approval
Experimental work was authorised by the Teagasc Animal Ethics Committee (Approval no TAEC 2020-266, and TAEC 2020-267). No invasive measures were employed in this farm-based trial. Experimental animals were monitored twice daily by farm staff and researchers, and any sick or injured sows or piglets were treated immediately or, if necessary, removed from the trial.
Assignment of animals to trial, housing and management
Details regarding the assignment of animals to trial, housing and management, as well as results for the effects of improved gestation housing on chronic stress and welfare indicators are described in Lagoda et al. (Reference Lagoda, O’Driscoll, Galli, Marchewka and Boyle2023). In summary, the study took place on a 2,000-sow commercial farrow-to-finish farm in County Cork, Ireland, between July 2021 and April 2022. Sows went on trial over two three-week periods (period 1: 2–16 August 2021; period 2: 15–29 November 2021), whereby 40 served sows were enrolled in the study every week, with 20 sows assigned to conventional (CONTROL) and 20 to treatment (IMPROVED) pens. In total, the study used 240 sows of parity 1 to 5 (mean [± SD]; 2.4 [± 1.03]) in six replicates.
The experiment started on the day sows were mixed into the gestation pens (day 28.9 [± 0.37] post-insemination). Thereafter, the composition of each group was stable. Each pen had 20 individual, free-access feeding/lying stalls (2.30 × 0.55 m; length ×width), and sows were free to move around the remainder of the pen (7.3 × 7.2 m; roaming area between two rows of feeding stalls: 7.3 × 2.7 m). CONTROL pens had fully slatted concrete floors, two blocks of wood and two chains suspended in the loose area. In replicates four to six, pens also had a rubber toy (Astro 200, EasyFix Rubber Products, Ballinasloe, County Galway, Ireland) suspended from a chain. IMPROVED pens were the same, but with the addition of a length of natural fibre rope (1-m manila rope; Marine Suppliers & Co Ltd, Howth, Co Dublin; replenished every two weeks throughout gestation) suspended from the feed trough within each feeding stall, and straw provided (replenished daily) in three custom-made structures (two straw racks at each end of the pen, and a rooting tower in the middle of the roaming area; Figure 1). Additionally, in the IMPROVED treatment, the slats in each feeding stall, as well as in front of the rooting tower, were covered with rubber mats (EasyFix Rubber Products, Ballinasloe, Co Galway, Ireland).
Diagram of the layout and set-up of the IMPROVED pen for pregnant sows.
Sows were fed a liquid diet twice per day and had ad libitum access to water via three nipple drinkers at one end of the pen. Sows were transferred into conventional farrowing crates (2.2 × 0.6 m) with fully slatted cast-iron floors and a heated pad for piglets one week prior to farrowing. Piglets were cross-fostered within treatment only, and within the first 24 h of life, after piglet measures (birth weight, intra-uterine growth restriction, IUGR, and vitality) were recorded. Piglets were weaned at approximately 28 days post-farrowing (26 [± 2.3] days).
All measures were performed by a single observer who practiced prior to the beginning of the study until 90% intra-observer repeatability was achieved. The observer was blind to treatments for the measures carried out in the farrowing rooms.
Sow measures
Salivary haptoglobin
A single saliva sample was collected from each sow on day 79.7 (± 1.21) of pregnancy, between 0800 and 0900h (Kováč et al. Reference Kováč, Tothova, Nagy and Seidel2008) by allowing her to chew on a 5 × 2 × 2 cm (length × width × breadth) polypropylene sponge (Esponja Marina, La Griega E Koronis, Madrid, Spain) clipped to a metal rod for approximately 1 min, until thoroughly moist. Moist sponges were placed inside Salivette tubes (Salimetrics) and centrifuged for 5 min at 3,000 rpm. Saliva samples were frozen at –20°C pending analysis in a professional biomarker laboratory (Interdisciplinary Laboratory of Clinical Analysis of the University of Murcia, Spain). Haptoglobin was measured using an in-house assay based on alphaLISA technology and a method described by Ortín-Bustillo et al. (Reference Ortín-Bustillo, Escribano, López-Arjona, Botia, Fuentes, Martínez-Miró, Rubio, García-Manzanilla, Franco-Martínez and Pardo-Marín2022), with intra- and inter-assay coefficient of variation (CV) < 15%.
Hair cortisol
Sows were restrained in the free-access stalls on day 25 of gestation, and then again in late pregnancy (day 109) to collect hair samples. An electric razor was used to shave hair from the dorso-lumbar region, identified by measuring 6.5 cm left and right from the mid-point at the spine marked by the position of the last rib. Hair samples were placed into plastic zip-lock bags, and frozen at −20°C until hair cortisol analysis. Samples of re-grown hair collected in late pregnancy (day 109) were analysed for cortisol concentration.
Hair sample preparation and cortisol extraction were based on the procedure described by Davenport et al. (Reference Davenport, Tiefenbacher, Lutz, Novak and Meyer2006), with certain modifications described by Lagoda et al. (Reference Lagoda, O’Driscoll, Marchewka, Foister, Turner and Boyle2021). In brief, hair samples were defrosted for 1 h prior to preparation procedures, then washed by placing 300 mg of hair into a 10 mL polypropylene tube along with 5 mL of isopropanol, and mixing gently on a shaker for 3 min. This was repeated using fresh isopropanol for the second wash. Washed hair samples were left inside the wash tubes and placed inside a protected fume hood to dry overnight. Samples prepared in this way were then individually ground into a fine powder using a Retsch mixing mill (MM200; 10 mL stainless steel grinding jars, single 12-mm stainless steel grinding ball) for 4 min at 25 Hz. Approximately 50 mg of ground hair was weighed and placed in a 2 mL tube along with 1 mL of methanol, which was incubated for 24 h at room temperature with constant gentle agitation (approximately 95 rpm) for cortisol extraction. Following the 24-h incubation period, we removed 0.6 mL of the cortisol extract in methanol (taking care not to disturb the settled hair powder at the bottom of the tube) using an Eppendorf pipette and transferred to a clean 1.5 mL tube for methanol evaporation, which was performed using a stream of nitrogen gas at 38°C. Cortisol extracts were frozen at −20°C pending EIA analysis. Extracted samples of cortisol were analysed using Salimetrics® Expanded Range, High Sensitivity Salivary Cortisol EIA kit. Frozen extract samples along with the EIA kit were brought to room temperature 1.5 h prior to being reconstituted with 0.4 mL of phosphate buffer (assay diluent) provided with the EIA kit. Reconstituted extracts (n = 159) were analysed for cortisol concentration levels in duplicate using five assays, following the protocol provided with the EIA kit. Inter- and intra-assay CV were 11.5 and 15.9%, respectively.
Tear staining (Chromodacryorrhea)
We scored the area of tear staining for the left and right eye when sows were in mid lactation and at weaning, according to a scale (Table 1) developed by DeBoer et al. (Reference DeBoer, Garner, McCain, Lay, Eicher and Marchant-Forde2015).
Description of the scores, developed by DeBoer et al. (Reference DeBoer, Garner, McCain, Lay, Eicher and Marchant-Forde2015) used in the assessment of tear staining in sows
Reproductive performance
Sow reproductive performance was recorded by the research team and included the following measures: number of piglets born alive, born dead, mummified, and total born.
Offspring measures
Birth weight, vitality and intra-uterine growth restriction (IUGR)
Piglets were weighed and scored for vitality and IUGR at birth. Vitality was scored according to criteria shown in Table 2, modified from Schmitt et al. (Reference Schmitt, Baxter, Lawlor, Boyle and O’Driscoll2019) and Rooney et al. (Reference Rooney, O’Driscoll, O’Doherty and Lawlor2020). The summation of scores for each criterion yielded a total vitality score, with the maximum (best) possible score of three per piglet. The degree of IUGR was estimated by visually scoring the presence/absence of nose wrinkles, cone-shaped head, and bulging eyes, based on a method from Hales et al. (Reference Hales, Moustsen, Nielsen and Hansen2013). For all three measures, a piglet scored 0 if the trait was absent, and 1 if it was present; therefore, the maximum (worst) total IUGR score a piglet could receive was 3.
Vitality scoring system used for piglets at birth (Schmitt et al. Reference Schmitt, Baxter, Lawlor, Boyle and O’Driscoll2019; Rooney et al. Reference Rooney, O’Driscoll, O’Doherty and Lawlor2020)
Diarrhoea
Presence of diarrhoea in the farrowing pen was scored approximately every second day throughout lactation (always starting on the Monday after farrowing, until the day of weaning; n = 10 scores per litter). This allowed us to distinguish fresh faeces from those present on the previous scoring day, according to criteria shown in Table 3, based on a method from Casey et al. (Reference Casey, Gardiner, Casey, Bradshaw, Lawlor, Lynch, Leonard, Stanton, Ross and Fitzgerald2007) and Marquardt et al. (Reference Marquardt, Jin, Kim, Fang, Frohlich and Baidoo1999) (0 = normal faeces, to 3 = severe diarrhoea). Scores were summed to yield a total diarrhoea score (TDS) per pen per sow per litter throughout lactation.
Scoring system used for pen diarrhoea level assessment throughout lactation, adapted from Marquardt et al. (Reference Marquardt, Jin, Kim, Fang, Frohlich and Baidoo1999) and Casey et al. (Reference Casey, Gardiner, Casey, Bradshaw, Lawlor, Lynch, Leonard, Stanton, Ross and Fitzgerald2007)
Statistical analysis
SAS v9.4 was used for all statistical analyses (SAS Inst Inc, Cary, NC, USA) with sow as the experimental unit. Differences were reported when P ≤ 0.05. Residuals were checked for normality by examination of histograms, quantile-quantile and normal distribution plots using the univariate procedure. Degrees of freedom were estimated using the Kenward-Rogers adjustment, and P-values adjusted using the Tukey-Kramer adjustment where mixed models were used. Data are presented as least square (LS) means and standard errors (SE).
All general linear models included the fixed effects of treatment and replicate, and pen as a random effect. The model for piglet birth weight also included the interactive effect of treatment and piglet sex, the repeated effect of piglet to allow for repeated measures, and sow as the subject. Covariance structure was selected on the basis of best fit, using the minimum finite-sample corrected Akaike Information Criteria (AIC).
Salivary haptoglobin, hair cortisol, piglet birth weight, total diarrhoea score, the number of piglets born alive, and the total number born were analysed using general linear models (PROC MIXED), while the number of piglets born dead and mummified were analysed using PROC GLIMMIX (with Poisson set as the distribution, and no offset command).
The Mann-Whitney test (PROC Npar1Way) was used to compare tear stains for both the right and left eyes of sows from CONTROL and IMPROVED pens, in mid lactation and at weaning. Right and left eyes were analysed separately, as previous work showed differences in tear staining for both eyes in response to stressors (DeBoer et al. Reference DeBoer, Garner, McCain, Lay, Eicher and Marchant-Forde2015). P-values were adjusted post hoc using the Bonferroni adjustment to account for multiple comparisons. The Mann-Whitney test (PROC Npar1Way) was also used to compare vitality scores, while a Chi-squared test was used to compare IUGR scores of piglets born to sows from CONTROL and IMPROVED pens.
Results
Effect of treatment on sow measures
There were higher concentrations of haptoglobin in the saliva of CONTROL compared to IMPROVED sows (P = 0.007; Table 4). There was no effect of treatment on concentrations of cortisol in the hair (P = 0.438; Table 4).
Differences (least square means (± SE]) in saliva haptoglobin, hair cortisol, and reproductive performance of 240 sows housed in either conventional (CONTROL; n = 120) or IMPROVED (n = 120) pens, as well as differences in the measures recorded for their offspring (birth weight, diarrhoea score)
Sows in the IMPROVED pens had lower (mean [± SD]) tear-stain scores in mid lactation (Right eye: 1.4 [± 0.91]; Left eye: 1.4 [± 0.94]) and at weaning (Right eye: 1.7 [± 1.07]; Left eye: 1.6 [± 1.13]) compared to CONTROL sows (Mid lactation, right eye: 2.0 [± 1.16], left eye: 2.0 [± 1.22]; Weaning, right eye: 2.3 [± 1.14], left eye: 2.2 [± 1.28]; All P ≤ 0.005; Figure 2).
The number of sows per tear-stain score category around the (a) right and (b) left eyes in mid lactation and at weaning, for the two treatment groups.
While there was no effect of treatment on the number of piglets born alive, born dead and the total number born, CONTROL sows gave birth to more mummified piglets compared to IMPROVED sows (P = 0.013; Table 4).
Effect of treatment on offspring measures
Piglets born to CONTROL sows tended to have lower weights at birth compared to those born to IMPROVED sows (P = 0.069; Table 4). There was no effect of treatment on piglet vitality at birth (P > 0.05), however there was an effect of treatment on IUGR scores. Piglets born to CONTROL sows had higher IUGR scores compared to those born to IMPROVED sows (P = 0.007; Table 5).
Number of piglets per intra-uterine growth restriction (IUGR) score category at birth
Finally, there was an effect of treatment on farrowing pen diarrhoea scores during the suckling period. Pens of piglets born to CONTROL sows had higher total diarrhoea scores compared to pens of piglets born to IMPROVED sows (P < 0.001; Table 4). Table 6 shows the number of farrowing pens that received a score of ≥ 2 in each treatment, along with the range in scores per day of lactation on which the pens were scored. Only one farrowing pen was scored 3 throughout the entire study.
Number of farrowing pens scored ≥ 2 in each treatment with the range in scores per day of lactation on which they were scored
Discussion
There is growing evidence that chronic stress experienced by pregnant sows in conventional housing systems contributes to prenatal stress, which can be detrimental to their offspring (Braastad Reference Braastad1998; Albernaz-Gonçalves et al. Reference Albernaz-Gonçalves, Olmos Antillón and Hötzel2022). Improving sow welfare is therefore an important step towards ensuring good health and resilience of piglets (Kapoor et al. Reference Kapoor, Dunn, Kostaki, Andrews and Matthews2006). Our findings support this hypothesis with improved sow welfare during pregnancy (described in Lagoda et al. Reference Lagoda, O’Driscoll, Galli, Marchewka and Boyle2023) translating to piglets with a tendency towards higher birth weights, significantly lower IUGR scores, and less diarrhoea during the suckling period.
As a likely consequence of the lower levels of chronic stress during gestation (Wang et al. Reference Wang, Kinzie, Berger, S-K and Baumann2001), sows in the improved pens had lower concentrations of salivary haptoglobin in late pregnancy. Saliva samples were taken on day 80 of pregnancy, encompassing seven weeks of exposure to the different housing systems for the sows in each treatment. This was obviously a sufficient amount of time for haptoglobin levels to diverge between the two treatments. This divergence indicates lower levels of systemic inflammation and disease in sows in the improved pens (Wang et al. Reference Wang, Kinzie, Berger, S-K and Baumann2001), and suggests improved health and better stress-coping abilities (Millet et al. Reference Millet, Cox, Buyse, Goddeeris and Janssens2005; Murata Reference Murata2007; Cerón et al. Reference Cerón, Contreras-Aguilar, Escribano, Martínez-Miró, López-Martínez, Ortín-Bustillo, Franco-Martínez, Rubio, Muñoz-Prieto and Tvarijonaviciute2022). This is in line with previous work, whereby finisher pigs housed in an organic system had lower haptoglobin levels compared to pigs housed in a conventional system (Millet et al. Reference Millet, Cox, Buyse, Goddeeris and Janssens2005). Similarly, growing pigs kept in enriched housing had lower levels of haptoglobin and were less affected by stress induced by a regrouping test compared to pigs housed in barren pens (Reimert et al. Reference Reimert, Rodenburg, Ursinus, Kemp and Bolhuis2014).
It is possible that the consumption of straw also had a positive impact on the digestive/gut health of sows in the improved pens, protecting against inflammation, and contributing to lower haptoglobin levels. Indeed, Kobek-Kjeldager et al. (Reference Kobek-Kjeldager, Schönherz, Canibe and Pedersen2022) hypothesised that certain dietary fibres stimulate beneficial gut microbiota that protect against inflammation and improve stress resilience. Although we cannot discern the extent of the contribution made by the different enrichment substrates or the rubber mats to sow welfare, it is likely that straw played a major role. This is based on the relevance of this enrichment type to highly motivated sow behaviours, as well as the benefits it provides for gut health and satiety (Tuyttens Reference Tuyttens2005; Stewart et al. Reference Stewart, O’Connell and Boyle2008). Moreover, chewing straw or ropes may influence saliva production, and therefore improve dental/buccal health (as described in humans; Haigh et al. Reference Haigh, Stewart, Whelan, Barnett, Smolenski and Wheeler2010). This could also have contributed to the reduction seen in haptoglobin levels in the improved sows.
We found no difference in the concentration of hair cortisol between treatments. This is contrary to our findings on haptoglobin, tear staining, and stereotypical behaviour which all point to reduced stress in sows in improved pens (Lagoda et al. Reference Lagoda, O’Driscoll, Galli, Marchewka and Boyle2023). It is possible that the methodology we employed was flawed or inaccurate, that hair cortisol does not accurately reflect chronic stress, or that the levels of stress were simply not divergent enough between the two treatments to cause a difference. We employed the shave/re-shave method (first shave on day 30, then re-shave performed in late pregnancy), as it more accurately determines cortisol concentrations, and thus stress corresponding to approximately the last two-thirds of the pregnancy. The collection site can impact on concentrations of cortisol found in hair (Heimbürge et al. 2019; Lagoda et al. Reference Lagoda, O’Driscoll, Marchewka, Foister, Turner and Boyle2021). Therefore, based on previous research, we selected the dorso-lumbar region as the most appropriate site for hair collection to ensure adequate measurement of cortisol concentrations (Casal et al. Reference Casal, Manteca, Peña, Bassols and Fàbrega2017; Otten, et al. Reference Otten, Heimbürge, Kanitz and Tuchscherer2020; Lagoda et al. Reference Lagoda, O’Driscoll, Marchewka, Foister, Turner and Boyle2021). Nevertheless, cortisol concentrations in hair are also influenced by cleanliness (Davenport et al. Reference Davenport, Tiefenbacher, Lutz, Novak and Meyer2006; Meyer & Novak Reference Meyer and Novak2012; Heimburge et al. Reference Heimburge, Kanitz and Otten2019). For instance, endogenous hair cortisol concentrations may be altered by exogenous cortisol entering the hair shaft by diffusion from urine, faeces and saliva, which commonly contaminate the outside of sow hair in on-farm settings (Otten et al. Reference Otten, Heimbürge, Kanitz and Tuchscherer2020). Working within the limits of a commercial farm it was not possible to control for cleanliness of sow hair during gestation.
Previous authors consider hair a suitable medium for quantifying levels of chronic stress in cattle and sheep (Salaberger et al. Reference Salaberger, Millard, El Makarem, Mostl, Grunberger, Krametter-Frotscher, Wittek and Palme2016; Heimburge et al. Reference Heimburge, Kanitz, Tuchscherer and Otten2020) due to the long-term accumulation of cortisol within the shaft (Davenport et al. Reference Davenport, Tiefenbacher, Lutz, Novak and Meyer2006; Meyer & Novak Reference Meyer and Novak2012; Heimbürge et al. 2019). However, in pigs, the value of hair cortisol is less clear (Lagoda et al. Reference Lagoda, O’Driscoll, Marchewka, Foister, Turner and Boyle2021). For instance, following a period of ACTH injections in cattle and pigs, there were differences in hair cortisol between treatments for cattle, but not for pigs (Heimburge et al. Reference Heimburge, Kanitz, Tuchscherer and Otten2020). It is possible that this is due to a lower systemic cortisol response following an ACTH challenge, or a faster rate at which ACTH is metabolised in pigs (Heimburge et al. Reference Heimburge, Kanitz, Tuchscherer and Otten2020).
Sows kept in the improved housing environment during pregnancy also had somewhat better reproductive performance, with lower numbers of piglets born mummified. However, as this difference was small, its biological significance is questionable. Nonetheless, it further supports our hypothesis of improved health status of those sows (evidenced by lower haptoglobin levels), and is in accordance with Lewis et al. (Reference Lewis, Torremorell, Galina-Pantoja and Bishop2009) who also found improved reproductive performance in healthier sows. In that study, sows infected with PRRSV gave birth to more mummified piglets (Lewis et al. Reference Lewis, Torremorell, Galina-Pantoja and Bishop2009). It is also in line with Hartnett et al. (Reference Hartnett, Boyle and O’Driscoll2020) who found fewer piglets born dead to sows reared in female-only groups as gilts. These sows also had lower salivary cortisol concentration, indicating lower stress levels resulting from a more optimal rearing environment, with carry-over benefits for their future performance (Hartnett et al. Reference Hartnett, Boyle and O’Driscoll2020). It is likely that healthy, less-stressed sows redirect fewer energy and metabolic resources away from developmental and maintenance processes such as pregnancy, towards processes aimed at ensuring survival, e.g. to fight off infection (Einarsson et al. Reference Einarsson, Brandt, Lundeheim and Madej2008, Kick et al. Reference Kick, Tompkins and Almond2011).
Formation of the skeleton of the pig foetus (calcification) takes place around day 38 to 45 of gestation, and any foetus that dies in utero prior to this undergoes reabsorption by the sow (Flowers Reference Flowers2019, Reference Flowers2020). The greater number of mummified piglets born to sows in the control treatment suggests that sows continued to redirect energy and metabolic resources away from the reproductive process in mid gestation. In addition to their reduced health status as reflected in the higher levels of haptoglobin, this could also reflect the higher levels of stress experienced by these sows during gestation (Lagoda et al. Reference Lagoda, O’Driscoll, Galli, Marchewka and Boyle2023). It is also in line with the findings of Lagoda et al. (Reference Lagoda, O’Driscoll, Marchewka, Foister, Turner and Boyle2021) who reported a similar negative effect of mid- to late-gestation stress (induced by sustained aggression) in sows on the numbers of mummified piglets.
The improved gestation environment enhanced the welfare of the sows and, in accordance with Dawkins (Reference Dawkins2019), led to the sows having better health outcomes which extended to their offspring. Piglets born to sows kept in the improved environment during pregnancy tended to be heavier at birth and to have significantly lower IUGR scores compared to piglets born to sows from control pens. This suggests those piglets received more resources from their mother in utero (Costa et al. Reference Costa, Marques, de Campos, Saraiva, Guimarães and Guimarães2019; Rooney et al. Reference Rooney, O’Driscoll, O’Doherty and Lawlor2020). Perhaps there were more resources available for the reproductive process as a by-product of better health and welfare of the mothers (Kick et al. Reference Kick, Tompkins and Almond2011; He et al. Reference He, Guo, Zheng, Xue, Zhao and Yao2019). Indeed Lagoda et al. (Reference Lagoda, O’Driscoll, Marchewka, Foister, Turner and Boyle2021) found higher IUGR scores in piglets born to sows that suffered higher levels of chronic stress resulting from sustained aggression, while Rooney et al. (Reference Rooney, O’Driscoll, O’Doherty and Lawlor2020) found the same in piglets born to sows fed low energy diets in late gestation. These findings suggest that maternal stress can have the same impact as protein or energy intake deficits when it comes to foetal development.
Moreover, although there were fewer IUGR piglets born to improved sows, there was no treatment effect on vitality scores. Other research indicates that survivability of IUGR piglets is compromised (Baxter et al. Reference Baxter, Jarvis, D’Eath, Ross, Robson, Farish, Nevison, Lawrence and Edwards2008) which could be reflected in vitality scores at birth. Indeed, allometric measurements of the piglet body parts in addition to IUGR scores is a more objective method of determining IUGR (Baxter et al. Reference Baxter, Jarvis, D’Eath, Ross, Robson, Farish, Nevison, Lawrence and Edwards2008) and should be employed in future studies.
Pens of piglets born to sows from the improved environment showed lower diarrhoea scores throughout the suckling period. This likely reflects improved immune function, resilience and health, and provides evidence for the beneficial impact of improved sow welfare and lower chronic stress levels during gestation on offspring outcomes (Albernaz-Gonçalves et al. Reference Albernaz-Gonçalves, Olmos Antillón and Hötzel2022). This is in line with studies by Merlot et al. (Reference Merlot, Calvar and Prunier2016, Reference Merlot, Pastorelli, Prunier, Pere, Louveau, Lefaucheur, Perruchot, Meunier-Salaun, Gardan-Salmon, Gondret and Quesnel2019, Reference Merlot, Meunier-Salaün, Peuteman, Père, Louveau, Perruchot, Prunier, Gardan-Salmon, Gondret and Quesnel2022) and Quesnel et al. (Reference Quesnel, Pere, Louveau, Lefaucheur, Perruchot, Prunier, Pastorelli, Meunier-Salaun, Gardan-Salmon, Merlot and Gondret2019a) that showed improved piglet immune function and tissue maturity, and consequently lower mortality during the suckling period when pregnant sows were provided with wood and straw pellets, or a larger pen with deep straw bedding. Specifically in relation to the potential carry-over benefits to offspring of maternal straw consumption, Cheng et al. (Reference Cheng, Wei, Xu, Xie, Jiang and Peng2018) and Bernardino et al. (Reference Bernardino, Tatemoto, Morrone, Mazza Rodrigues and Zanella2016) demonstrated that piglets born to sows fed high fibre diets during pregnancy have altered intestinal microbiota and reduced intestinal permeability, with fewer skin lesions prior to weaning suggesting less agonistic interactions. This is evidence for a longer-term carry-over benefit of improved maternal diet, and hence welfare, on the offspring.
Lactating sows from improved gestation housing had lower tear-stain scores in mid lactation and at weaning, suggesting a beneficial carry-over effect of the gestation housing environment during housing in farrowing crates. This is in agreement with Espejo-Beristain et al. (Reference Espejo-Beristain, Ahuja-Aguirre, Carrasco-García, Hernandez-Cruz and Paredes-Ramos2022) where sows from enriched pens had lower levels of cortisol in hair in late pregnancy, and displayed behaviours indicative of better coping ability during and after farrowing, compared to sows from non-enriched pens. The benefits of the improved gestation housing environment clearly overrode any potential stress arising for the improved sows from the sudden transition from rubber mats to lie on and an enriched environment to barren farrowing crates with cast-iron floors. Straw consumption during pregnancy may have improved digestive health and reduced stress as reflected in the lower tear stains recorded for improved sows during lactation. In turn, less-stressed sows could have contributed to improved piglet health. Kinane et al. (Reference Kinane, Butler and O’Driscoll2022, Reference Kinane, Butler and O’Driscoll2021) found that sows kept in free-lactation crates had lower tear-stain scores at weaning than those kept in standard crates. Their piglets performed fewer damaging behaviours during suckling and grew faster post-weaning compared to piglets from standard crates, and the authors hypothesised that the reduced maternal stress, even post-farrowing, was a contributing factor.
Animal welfare implications and conclusion
Overall, these results emphasise the cumulative effectiveness of improvements to the housing environment in addressing both physical and psychological stressors experienced by pregnant sows, with associated benefits for the health and resilience of their offspring. If implemented on-farm, our findings could not only improve sow and piglet welfare but contribute to a reduction in antibiotic use to treat diarrhoea in piglets during the suckling period. This would, in turn, reduce the risk of antimicrobial resistance development and improve economic returns for the farmer resulting from reduced veterinary/medication costs and improved pig performance.
Acknowledgements
MEL was funded by the Teagasc Walsh Scholarship Programme. The work was conducted as part of a Teagasc funded grant-in-aid project, ‘Effects of chronic stress on sow welfare and performance, and on the resilience of their offspring (SowWeanWel)’ ref 0370. The authors would like to thank the farm owner and his staff for facilitating the work. The authors would also like to thank L Markland, M Harrison, and L Serai for their help with data collection, and MJ López-Martínez for help with saliva sample processing.
Competing interest
None.
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