Dietary fiber and weaning age affect stress and immune markers in saliva of sows and their offspring

Abstract

Diet, especially the intake of dietary fiber, and weaning practices may influence pig wellbeing. This study assessed changes in salivary stress and immune markers in sows and their offspring fed either hay (HAY) or sugar beet pulp (SBP), either fine (F) or coarse (C), during gestation and lactation. The effect of weaning age (conventional—CW, late—LW) on these markers was also evaluated. Saliva was analyzed for chromogranin A (CgA), cortisol, alpha-amylase, oxytocin, immunoglobulin A (IgA), and adenosine deaminase (ADA). CgA was higher at CW versus LW in sows fed SBP-F (P = 0.038). Alpha-amylase was higher in sows fed HAY-C at CW versus LW (P = 0.005) and in sows fed SBP-C at LW versus CW (P = 0.096). CgA and oxytocin were higher in sows fed SBP-F at CW versus LW (P = 0.038 and P = 0.017, respectively). ADA was higher in sows fed SBP-C versus HAY-C (P = 0.035) at LW and at LW versus CW in sows fed SBP-C (P = 0.002). Piglet salivary CgA was higher at CW versus LW in HAY-F (P = 0.002) and SBP-F (P = 0.031). Oxytocin was higher at CW versus LW in piglets fed HAY-F (P = 0.006). Piglet salivary IgA was higher in HAY-C versus HAY-F at CW (P = 0.010) and at LW versus CW in piglets fed HAY-F (P = 0.021). ADA was higher in piglets fed SBP-F versus HAY-F (P = 0.053) at CW and SBP-F versus SBP-C (P = 0.042) at LW. Dietary fiber type, weaning age, and to a lesser extent grinding degree affect stress and immune markers in pigs. These findings highlight the impact of diet and weaning practice on pig welfare.

This research highlights the importance of dietary fiber type and weaning age in reducing stress and enhancing immune function in pigs, suggesting that high-fermentable fiber and late weaning could improve overall pig health and wellbeing.

Introduction

Modern livestock production can be associated with various stress factors for the animals, which have to cope with challenging situations, for example, in relation to their development and the procedures within the production cycle. The transitions in early postnatal life, such as weaning, are particularly critical for pigs, and are associated with stress factors such as nursing environment, large litter size, weaning age, cross-fostering, diet shifts, sudden temperature changes, or animal relocations (Ott et al., 2014; Albernaz-Gonçalves et al., 2021; Lagoda et al., 2021). Stress, either acute or chronic, leads to the release of different signaling molecules to provoke certain types of reactions in the body. These molecules can be found in the body tissues such as brain, blood, or hair or in the fluids such as saliva or in the excrements such as urine, sweat, or feces (Behringer and Deschner, 2017). The stress markers include chromogranin A (CgA), oxytocin, cortisol, and cortisone. In addition, it has been described that stress situations can produce immune-related responses through an increased release of immunoglobulin A (IgA), adenosine deaminase (ADA), or alpha-amylase in saliva (Ott et al., 2014; Behringer and Deschner, 2017). Therefore, these analytes could be suitable as biomarkers for animal welfare.

Diet has a profound impact on animal physiology and health and nutritional strategies have been demonstrated to improve different aspects of animal health and wellbeing (Shang et al., 2019; Grześkowiak et al., 2023). Moreover, a growing body of evidence suggests the beneficial impact of dietary fiber on sows coping with stress (Do et al., 2023). Specifically, the satiating effect of fiber can prevent the development of hunger-related stress and reduce the occurrence of aggressive behavior due to competition for feed or low-feed amounts (Sapkota et al., 2016; Grześkowiak et al., 2023). While coarse fiber feeds promote gut motility, enhance microbial fermentation, and improve gut health, they may have lower digestibility and a higher environmental impact compared to fine fiber feeds (Vukmirović et al., 2017).

Weaning is a critical and extremely stressful period for both the sow and her piglets. To allow for earlier inseminations of the sows and faster fattening of the piglets some current husbandry practices include short nursing periods which last less than 3 wk when piglets’ mean body weight is above 5 kg (Van Kerschaver et al., 2023). However, separating sows and their offspring too early leads to increased anxiety and aggression in sows (Prunier et al., 2019). In piglets, early weaning leads to nutritional, social, and immunological stress (Moeser et al., 2017; Cheng et al., 2022). Thus, either in sows or in their offspring, early weaning can have negative consequences on their health and welfare.

We hypothesized that fibers with different solubility properties in the gut can: 1) influence stress analytes as a function of weaning age and 2) mitigate the stress experienced by both sows and piglets to varying degrees. The objectives were to assess possible changes in salivary stress and immune markers in sows and their offspring due to the use of different diets and times of weaning. For this purpose, we fed gestating and lactating sows and their piglets with diets containing two different fiber sources (hay or sugar beet pulp, SBP) and with two particle sizes (fine or coarse). In addition, piglets were weaned at two different ages, that is, at 28 ± 2 and 42 ± 2 days of life, which corresponded to conventional and late weaning, respectively. To assess stress and immune-related markers, we measured salivary CgA, oxytocin, IgA, ADA, and alpha-amylase in sows and their offspring, and cortisol and cortisone in sow bristles.

Materials and Methods

Ethics approval

The institutional and national guidelines for the care and use of animals were followed, and the study was approved by the State Office of Health and Social Affairs “Landesamt für Gesundheit und Soziales Berlin” (LAGeSo, StN 014/22). This study was conducted in the experimental pig facilities of the Institute of Animal Nutrition at the Freie Universität Berlin, Berlin, Germany.

Animals and diets

Four feeding groups of nulliparous German Landrace sows were fed isocaloric and iso-nitrogenic experimental diets containing either 10% of hay (HAY) or sugar beet pulp (SBP) as fiber sources. The fiber particles were either finely (F; <1 mm) or coarsely (C; >1 mm) ground (Supplementary Table S1). The diets were formulated to meet or exceed the recommendations of gestating and lactating sows. Total dietary fiber was generally higher in gestating diets compared to lactating diets for sows to balance energy intake, control weight, and maintain gut health during gestation (GfE, 2006). Five sows were used in each of the HAY-F, HAY-C, and SBP-F groups, while six sows were used in the SBP-C group.

During gestation, the sows were housed in groups of five sows. Gestation diet was provided individually to each sow twice a day. One week before the estimated farrowing time, the sows were moved to the farrowing facility and were housed individually in pens until farrowing and kept in farrowing crates for the first 3 d post-partum. The sows were farrowed at the same time but weaned at different ages, as stated further.

The pen floor was covered with rubber mats and each pen was equipped with two piglet nests with infrared heating lamps. One day after farrowing, the sows received a lactation diet, which was provided three times a day. The body weight of the sows was recorded weekly during gestation and lactation.

Creep feed, with identical fiber type and particle size as in the maternal diet, was administered starting from day 14 of life and beyond (Supplementary Table S2). Water was available ad libitum to all animals.

The piglets were weaned at an age of 28 ± 2 d (conventional weaning, CW) and 42 ± 2 d (late weaning, LW) and their body weights were recorded.

Saliva and bristle collection

Saliva samples were collected before any other manipulations of the animals, that is, from the sows few hours after the end of parturition (the end of parturition was defined as the time point at which an amount of afterbirth corresponding to the litter size was expelled) and from the sows and their offspring in the early morning (07:00 a.m.) of the weaning days.

Saliva was collected from four piglets per sow (two males and two females; mean birth weight) at CW (two piglets) and LW (two piglets), just before the animals were separated from their dams and litters, using a standard saliva sampling kit (Salivette Cortisol, Sarstedt AG & CO. KG, Germany). Sows and piglets were offered a synthetic swab to chew on voluntarily (no fixation of animals) for approximately 1 (sows) or 2 (piglets) min. The samples were immediately placed on ice, centrifuged at 4 °C for 2 min at 1,000 × g and stored at −80 °C until analysis.

When the piglets were weaned late, bristles from the sows were obtained by razor cutting of a piece of entire hair (about 100 individual entire hairs) from cranial, dorsal, and caudal sides of the sow back. Collected bristles were stored frozen at −80 °C until analysis.

Determination of salivary CgA, alpha-amylase, oxytocin, IgA, and ADA

CgA concentration was measured in the saliva samples of sows and piglets using a time-resolved immunofluorometric assay, as described previously (Escribano et al., 2013). Alpha-amylase and ADA activities were measured by a spectrophotometric automated assay, previously validated (Contreras-Aguilar et al., 2019). Oxytocin concentration was measured by an AlphaLISA assay using a monoclonal antibody, previously validated in saliva of pigs (López-Arjona et al., 2021). IgA concentration was measured by an ELISA assay, as described elsewhere (Cerón et al., 2022).

Determination of cortisol in saliva, and cortisol and cortisone in bristles

The cortisol and cortisone concentrations in sow and piglet saliva or in sow bristles were measured by two AlphaLISA assays, as validated and described previously (López-Arjona et al., 2020).

Statistical analysis

Data was analyzed and reported as mean and standard error (SE). Body weight of the sows and their offspring were analyzed by the multivariate ANOVA with fiber source, fiber particle size, and weaning age as factors. Data on the salivary stress and immune markers and on the bristle stress markers were not normally distributed and thus they were analyzed using Kruskal–Wallis test (comparison of sow or piglet of different dietary groups) with Mann–Whitney U post hoc test, where applicable, univariate analysis of covariance (ANCOVA) test (litter size as a cofactor for age comparisons for sows) and Mann–Whitney U test (comparison of piglet groups of different weaning ages). Significance was considered at P ≤ 0.005. Data were analyzed using IBM SPSS Statistics Version 27.

Results

Body weight

None of the fiber diets had an impact on the body weight of the sows during gestation and lactation. The body weight of the piglets at CW was as follows: 6.3 kg in the HAY-F, 6.0 kg in the HAY-C, 6.0 kg in the SBP-F, and 6.8 kg in the SBP-C groups (SEM 0.11, P = 0.040 for fiber type × particle size). At LW, body weight of the piglets was as follows: 10.2 kg in the HAY-F, 9.2 kg in the HAY-C, 9.7 kg in the SBP-F, and 10.6 kg in the SBP-C groups (SEM 0.02, P = 0.042 for fiber type × particle size).

Changes in markers of wellbeing or stress: salivary CgA, cortisol, alpha-amylase and oxytocin, and bristle cortisol and cortisone in sows

After parturition, a trend for higher alpha-amylase activity in sows fed SBP-F as compared to other diets was observed (P = 0.098) while CgA, cortisol, and oxytocin concentrations were not affected by the diet (Table 1).

Table 1.

Salivary chromogranin A, cortisol, alpha-amylase, oxytocin, immunoglobulin A, and adenosine deaminase levels (mean ± SE) in sows fed diets enriched in either hay-fine, hay-coarse, sugar beet pulp-fine, and sugar beet pulp-coarse fibers, collected few hours after the farrowing has ended

	HAY-F	HAY-C	SBP-F	SBP-C	P1
CgA, µg/mL	0.43 ± 0.15	0.25 ± 0.07	0.55 ± 0.14	0.47 ± 0.13	0.267
Cortisol, ng/mL	418 ± 101	185 ± 118	262 ± 104	172 ± 18.2	0.183
Alpha-amylase, U/L	469 ± 154	823 ± 351	1,872 ± 162	732 ± 196	0.098
Oxytocin, ng/mL	1.81 ± 0.84	1.88 ± 0.69	2.84 ± 1.70	3.83 ± 1.15	0.278
IgA, µg/mL	101 ± 21.2	80.0 ± 25.6	139 ± 30.4	143 ± 16.1	0.204
ADA, U/L	9,704 ± 910	7,561 ± 2,592	10,991 ± 4,897	15,052 ± 3,081	0.430

¹ Kruskal–Wallis test for the comparison of dietary groups.

^a,bDifferent superscripts indicate significantly different values within parameter (post hoc Mann–Whitney U test).

HAY-F, hay-fine; HAY-C, hay-coarse; SBP-F, sugar beet pulp-fine; SBP-C, sugar beet pulp-coarse; CgA, chromogranin A; IgA, immunoglobulin; ADA, adenosine deaminase.

Weaning age had an impact on CgA and oxytocin concentrations which were higher at CW versus LW post-partum in sows fed SBP-F diet (0.57 ± 0.08 vs. 0.26 ± 0.03 µg/mL, P = 0.038 and 0.54 ± 0.26 vs. 0.23 ± 0.21 ng/mL, P = 0.017, respectively). Also, alpha-amylase was higher at CW versus LW in sows fed HAY-C diet (758 ± 574 vs. 386 ± 142 U/L, P = 0.005) (Table 2).

Table 2.

Salivary chromogranin A, cortisol, alpha-amylase, alpha-amylase, oxytocin, immunoglobulin A, and adenosine deaminase levels (mean ± SE) in sows fed diets enriched in either hay-fine, hay-coarse, sugar beet pulp-fine, and sugar beet pulp-coarse fibers, measured at conventional and late weaning of piglets

	HAY-F	HAY-C	SBP-F	SBP-C	P1
CgA, µg/mL
CW	0.56 ± 0.11	0.35 ± 0.08	0.57 ± 0.08	0.43 ± 0.11	0.329
LW	0.23 ± 0.04	0.25 ± 0.05	0.26 ± 0.03	0.40 ± 0.05	0.124
P2	0.135	0.798	0.038	0.347
Cortisol, ng/mL
CW	12.8 ± 5.28	39.8 ± 19.2	30.7 ± 19.2	11.3 ± 5.1	0.586
LW	54.3 ± 35.0	123 ± 70.0	82.6 ± 50.7	21.3 ± 7.6	0.870
P2	0.275	0.377	0.276	0.384
Alpha-amylase, U/L
CW	174 ± 7	758 ± 574	335 ± 50	221 ± 87	0.222
LW	264 ± 43	386 ± 142	418 ± 210	352 ± 124	0.946
P2	0.106	0.005	0.912	0.096
Oxytocin, ng/mL
CW	0.39 ± 0.09	0.59 ± 0.14	0.54 ± 0.26	0.55 ± 0.15	0.625
LW	0.92 ± 0.32	0.87 ± 0.26	0.23 ± 0.21	0.57 ± 0.05	0.151
P2	0.252	0.923	0.017	0.254
IgA, µg/mL
CW	18.3 ± 4.74	25.5 ± 3.41	36.6 ± 3.29	22.3 ± 6.44	0.115
LW	36.5 ± 11.0	42.8 ± 16.1	42.0 ± 10.3	31.0 ± 4.23	0.976
P2	0.171	0.611	0.457	0.150
ADA, U/L
CW	3,639 ± 1,475	2,292 ± 368	5,067 ± 970	3,169 ± 978	0.243
LW	5,788 ± 1,226a,b	4,594 ± 616b	9,098 ± 2,040a,b	10,258 ± 677a	0.027
P2	0.965	0.389	0.185	0.002

¹ Kruskal–Wallis test for the comparison of dietary groups.

² Univariate ANCOVA (cofactor: litter size).

^a,bDifferent superscripts indicate significantly different values within parameter (post hoc Mann–Whitney U test).

CW, conventional weaning; LW, late weaning; HAY-F, hay-fine; HAY-C, hay-coarse; SBP-F, sugar beet pulp-fine; SBP-C, sugar beet pulp-coarse; CgA, chromogranin A; IgA, immunoglobulin; ADA, adenosine deaminase.

There was no statistical difference in bristle cortisol; however, cortisone concentration was significantly lower in the bristles of sows fed HAY-F and HAY-C, as compared to those fed SBP-F and SBP-C diets (P = 0.002), all sampled at the LW time point (Table 3).

Table 3.

Bristle cortisol and cortisone levels (mean ± SE) in sows fed diets enriched in either hay-fine, hay-coarse, sugar beet pulp-fine, and sugar beet pulp-coarse fibers, measured at conventional and late weaning of their piglets

	HAY-F	HAY-C	SBP-F	SBP-C	P1
Cortisol, pg/mg	119.9 ± 10.2	142.6 ± 14.4	144.5 ± 6.3	154.0 ± 19.9	0.287
Cortisone, pg/mg	2.71 ± 0.09b	2.49 ± 0.31b	216.8 ± 14.2a	203.4 ± 27.4a	0.002

¹ Kruskal–Wallis test for the comparison of dietary groups.

^a,bDifferent superscripts indicate significantly different values within parameter (post hoc Mann–Whitney U test).

HAY-F, hay-fine; HAY-C, hay-coarse; SBP-F, sugar beet pulp-fine; SBP-C, sugar beet pulp-coarse.

Changes in markers of the immune system: IgA and ADA in sows

After parturition, IgA and ADA were not statistically affected by the diet (Table 1). However, at LW post-partum, the ADA activity was significantly higher in sows fed SBP-C versus HAY-C diets (10,258 ± 677 vs. 4,594 ± 616 U/L, post hoc Bonferroni corrected P = 0.035) (Table 2). Weaning age had an impact on ADA activity which was higher at LW versus CW post-partum in sows fed SBP-C diet (10,258 ± 677 vs. 3,169 ± 978 U/L, P = 0.002) (Table 2).

Changes in markers of wellbeing or stress: CgA, cortisol, alpha-amylase, and oxytocin in piglets

In piglets, salivary CgA concentration was higher at CW versus LW in groups fed HAY-F (1.21 ± 0.08 vs. 0.82 ± 0.06 µg/mL, P = 0.002) and SBP-F (1.25 ± 0.16 vs. 0.76 ± 0.10 µg/mL, P = 0.031) diets. In addition, oxytocin concentration was higher at CW versus LW in piglets fed HAY-F diet (2.58 ± 0.43 ng/mL vs. 1.04 ± 0.25 ng/mL, P = 0.006) (Table 4).

Table 4.

Salivary chromogranin A, alpha-amylase, oxytocin, immunoglobulin A, and adenosine deaminase levels (mean ± SE) in piglets fed diets enriched in either hay-fine, hay-coarse, sugar beet pulp-fine, and sugar beet pulp-coarse fibers, measured at conventional and late weaning of piglets

	HAY-F	HAY-C	SBP-F	SBP-C	P1
CgA, µg/mL
CW	1.21 ± 0.08	0.93 ± 0.10	1.25 ± 0.16	0.93 ± 0.16	0.148
LW	0.82 ± 0.06	0.89 ± 0.13	0.76 ± 0.10	0.97 ± 0.11	0.344
P2	0.002	0.393	0.031	0.720
Alpha-amylase, U/L
CW	1,204 ± 433	1,062 ± 292	757 ± 140	753 ± 298	0.834
LW	1,359 ± 464	981 ± 221	719 ± 196	2,366 ± 587	0.056
P2	0.797	0.859	0.573	0.112
Oxytocin, ng/mL
CW	2.58 ± 0.43	2.03 ± 0.27	2.11 ± 0.95	1.90 ± 0.40	0.880
LW	1.04 ± 0.25	1.67 ± 0.29	2.23 ± 0.90	1.67 ± 0.18	0.172
P2	0.006	0.408	1.000	0.282
IgA, µg/mL
CW	6.09 ± 1.67b	17.7 ± 1.44a	13.8 ± 3.09a,b	10.1 ± 2.46a,b	0.016
LW	14.1 ± 2.28	13.1 ± 2.71	16.2 ± 2.46	15.2 ± 4.14	0.835
P2	0.021	0.518	0.463	0.562
ADA, U/L
CW	4,107 ± 1,110b	6,488 ± 772a,b	8,768 ± 802a	4,313 ± 492a,b	0.039
LW	4,426 ± 692a,b	5,421 ± 587a,b	8,496 ± 1,459a	4,298 ± 602b	0.039
P2	0.731	0.435	0.755	0.727

¹ Kruskal–Wallis test for the comparison of dietary groups.

² Wilcoxon test for the weaning age comparison.

^a,bDifferent superscripts indicate significantly different values within parameter (post hoc Mann–Whitney U test).

CW, conventional weaning; LW, late weaning; HAY-F, hay-fine; HAY-C, hay-coarse; SBP-F, sugar beet pulp-fine; SBP-C, sugar beet pulp-coarse; CgA, chromogranin A; IgA, immunoglobulin; ADA, adenosine deaminase.

Changes in markers of the immune system: IgA and ADA in piglets

The salivary IgA concentration was higher in piglets fed HAY-C versus HAY-F diet when sampled at CW (17.7 ± 1.44 vs. 6.09 ± 1.67 µg/mL, post hoc Bonferroni corrected P = 0.010). The LW versus CW age increased the concentration of IgA in piglets from the HAY-F diet (14.1 ± 2.28 vs. 6.09 ± 1.67, P = 0.021). The ADA activity was higher in piglets fed SBP-F versus HAY-F diet when sampled at CW (8,768 ± 802 vs. 4,107 ± 1,110 U/L, post hoc Bonferroni corrected P = 0.053) and in piglets fed SBP-F versus SBP-C diet when sampled at LW (8,496 ± 1,459 vs. 4,298 ± 602 U/L, post hoc Bonferroni corrected P = 0.042) (Table 4).

Discussion

Awareness of farm animal welfare and the number of studies on animal stress and behavior are constantly increasing. Farrowing is an extremely stressful period with effects on the behavior, immune system, and physiology of sows (Jarvis et al., 2002). In this line, dietary strategies offer promising possibilities for stress management in intensive pork production (Do et al., 2023). Through a process known as “early programming,” providing sows with diets enriched in specific dietary fibers during gestation and lactation can potentially impact the gut microbiota, immune system, and behavior of the offspring (Shang et al., 2019; Grześkowiak et al., 2022). This signaling mechanism, known as the “gut–brain axis,” was demonstrated in a recent study using carbon-labeled tracers (Murray et al., 2023). The study reported that metabolites produced during intestinal protein fermentation, including amino acid precursors like tyrosine, can be detected in the brain. Consequently, these metabolites could potentially influence brain function in pigs (Murray et al., 2023). Additionally, reports indicate that a later weaning age may benefit the behavior, digestive physiology, immune system, and overall performance of pigs (Moeser et al., 2017; Faccin et al., 2020).

In this study, we observed a trend toward high alpha-amylase activity in sows fed SBP-F diets a few hours after farrowing, which could be related to the higher digestible carbohydrates in SBP compared to hay (Grześkowiak et al., 2023). Further, salivary alpha-amylase was higher at conventional, as compared to late weaning in sows fed HAY-C diet. In pigs, stress has been reported to affect salivary alpha-amylase activity. Short-term acute stress might be associated with an increase in salivary alpha-amylase activity in pigs but that needs to be still verified (Fuentes et al., 2011; Contreras-Aguilar et al., 2018). This increase is part of the fight-or-flight response, preparing the body for energy production and nutrient mobilization. In this line, the surge in salivary alpha-amylase activity aids in carbohydrate breakdown, providing readily available energy.

At farrowing, a trend for slightly higher saliva CgA concentrations, which is a biomarker of stress was noted in sows fed SBP-enriched diets compared to low-fermentable fibers. Thus, low-fermentable fibers seem to lower the acute stress in sows at farrowing. The reason for this observation could be that low-fermentable fiber has a bulking effect, leading to greater satiety and longer resting periods between meals. Chewing and manipulating fibrous feed can help alleviate boredom, reduce stress, and possibly also the occurrence of undesirable behaviors such as tail biting or aggression in sows (Sapkota et al., 2016; Grześkowiak et al., 2023). We also found that the weaning age impacted CgA concentration, which was higher at conventional weaning compared to late weaning in sows from all dietary groups, especially those fed the SBP-F diet. Interestingly, the abovementioned alpha-amylase levels were higher also at conventional, as compared to late offspring weaning in sows, which may indicate similar dynamics of these two salivary markers which are associated to acute stress. CgA and its derived peptides are involved in regulating inflammatory processes, including the modulation of immune cell function, cytokine release, and the interaction between the immune and nervous systems during stress and inflammation (Giacomello et al., 2020).

Weaning is a very challenging period for piglets in relation to behavior, immunity, and gut physiology. Interestingly, salivary CgA levels were higher in conventionally weaned piglets compared to late-weaned piglets across all feeding groups, with significant differences observed for the HAY-F and SBP-F diets. Thus, later weaning age seems to lower the CgA level in piglets, just as it does for their dams and therefore decrease stress. In our report, piglets, especially those from the HAY-F group and weaned early, had higher levels of oxytocin in their saliva, than their late-weaned littermates, which could indicate that the younger the offspring are, the stronger the bond to their dam is (Nagasawa et al., 2012).

In contrast, salivary cortisol did not differ between dietary groups or sampling ages of sows. Previous studies also found no effect of high-fiber diets on salivary or circulating cortisol levels in sows (Holt et al., 2016; Loisel et al., 2013). Thus, cortisol may not be a reliable marker for acute stress in sows on fiber diets. Hair cortisol, which accumulates over time, can be used for assessing chronic stress (López-Arjona et al., 2020; Morgan et al., 2021). Chronic stress can affect natural defence mechanisms leading to increased susceptibility to infections or reduced animal performance (Valros et al., 2003; Morgan et al., 2021). In this study, bristle cortisone was higher in sows fed SBP-enriched diets than in those fed hay-enriched diets at late weaning, while bristle cortisol levels were similar across groups. Increased cortisone in hair has been detected in some stress situations such as heat stress (Escribano et al., 2023). Thus, it could be postulated that in our report, the increase in cortisone in hair in sows fed SBP-enriched diets could be a reflect of an increased stress.

We found that oxytocin levels were slightly higher in sows fed SBP diets when sampled just after farrowing. Oxytocin is crucial for facilitating maternal behaviors in pigs, promoting uterine contractions during parturition, and stimulating milk ejection post-partum (Renfrew et al., 2000). Moreover, oxytocin can be detected in sow’s milk, thus it can directly affect the offspring. It also contributes to the formation of the maternal bonds between sows and their piglets or between individuals within a group of pigs (Gimsa et al., 2022). High-fermentable SBP fiber in the sow’s diet may have contributed to numerically higher oxytocin levels at parturition as compared to low-fermentable hay fiber diets, which are known for its bulking effects, higher satiety, and longer resting periods (Sapkota et al., 2016; Grześkowiak et al., 2023). SBP is readily fermented in the gut, leading to the production of SCFA and other metabolites (Pieper et al., 2014; Grześkowiak et al., 2022). These fermentation products may positively affect gut physiology, potentially enhancing overall wellbeing, and triggering higher oxytocin release. Additionally, oxytocin was higher at conventional weaning, as compared to late weaning in sows fed the SBP-F diet. The release of oxytocin, the “bonding hormone,” is triggered by positive, longer sow-offspring interactions, while stress-related hormone CgA levels decreased.

In our study, sows fed SBP-enriched diets also showed a trend for higher concentrations of salivary IgA. Previous studies demonstrated that sows fed SBP, as compared to wheat bran-enriched diets had higher IgA in milk obtained 3 wk after farrowing (Shang et al., 2019). Here, the IgA was slightly higher in sows sampled late, as compared to early offspring weaning. In addition, salivary IgA level was higher in piglets when the animals were weaned late, especially in those fed the HAY-F diets. Previously, others have noted higher intestinal IgA levels in piglets whose dams were fed SBP, as compared to wheat bran diets (Shang et al., 2019).

Similarly, when ADA, the other marker of immune system was evaluated in our report, sows fed SBP-enriched diets showed slightly higher ADA activity compared to those fed hay. ADA was significantly higher in sows fed SBP-C compared to HAY-C at late weaning. Weaning age also impacted ADA, with higher levels at late weaning in sows fed SBP-C diet. Piglets fed SBP-F had the highest ADA activity in saliva at both weaning ages. The specific influence of fiber on ADA activity in pigs is not well-studied, but ADA is crucial for the development and function of the immune cells and reflects the status of lymphocyte function (Contreras-Aguilar et al., 2020); therefore, higher values of ADA in pigs with later weaning and fed high-fermentable fiber diets could indicate a better immune function that could be also reflected with higher values of IgA. Therefore, it could be postulated that the combination of reduced stress from later weaning, and the beneficial effects of high-fermentable fibers can significantly enhance the immune function of sows.

The results demonstrate that SBP-rich diets improved immune function by increasing salivary IgA, ADA. Conversely, hay-rich diets reduced stress markers CgA and alpha-amylase at farrowing. These effects could potentially lower stress levels and enhance immune protection in the offspring due to the close sow-piglet association. Better immune function in piglets may offer protection against environmental challenges such as pathogenic Escherichia coli among others (Raskova Kafkova et al., 2021).

Conclusions

High-fermentable SBP fiber appears to support better the immune function, potentially offering a dietary strategy to improve the health and wellbeing of sows and their offspring. Late weaning improves stress and immune biomarkers. Overall, our findings suggest that dietary fiber type and weaning age significantly influence the stress and immune markers in both sows and piglets. Further research is warranted to explore the long-term impacts of these dietary interventions on animal health and productivity.

Glossary

Abbreviations

ADA

adenosine deaminase

C

coarse

CgA

chromogranin A

CW

conventional weaning

F

fine

IgA

immunoglobulin A

HAY

hay

LW

late weaning

SBP

sugar beet pulp

SCFA

short-chain fatty acids

Author Contributions

Lukasz Grzeskowiak (Conceptualization, Data curation, Methodology, Writing—original draft), Jose Cerón (Data curation, Methodology, Writing—review & editing), Marina Lopez-Arjona (Data curation, Methodology, Writing—review & editing), Beatriz Martinez Vallespin (Conceptualization, Methodology, Writing—review & editing), Johannes Schulze Holthausen (Conceptualization, Methodology, Writing—review & editing), Philip Krüsselmann (Methodology, Writing—review & editing), Cornelia Metges (Conceptualization, Writing—review & editing), Bjoern Kuhla (Conceptualization, Writing—review & editing), Wilfried Vahjen (Conceptualization, Methodology, Writing—review & editing), Jürgen Zentek (Conceptualization, Methodology, Writing—review & editing), and Eva-Maria Saliu (Conceptualization, Methodology, Writing—review & editing)

Conflict of interest statement

The authors declare no real or perceived conflicts of interest.

Data Availability

The data that support the study findings are available to reviewers, or available from the authors upon reasonable request.