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Behavioral and physiological performance of different gilt breeds during lactation

ABSTRACT

We evaluated the maternal behavior, physiology, and reproductive performance of both Damin (Min-pig × Large White) and Large White gilts to identify the advantages hybrid sows offer with regard to stress relieve and improvement of the welfare level of sows during late lactation. First-parity Damin gilts (n = 40) and first-parity Large White gilts (n = 40) were farrowed in individual pens. Video surveillance was used to monitor the occurrence of lateral recumbency and compare it to other postures, such as ventral recumbency, defecation, urination, tail posture, sham-chewing, and bar-biting behaviors. Monitoring was conducted from 07:00 to 09:00 h and from 13:00 to 15:00 h on days 3 and 6 of each week from the third to the fifth week post-parturition. In addition, the concentrations of tumor necrosis factor-α, interleukin-6, and salivary α-amylase were assessed. During the fourth week postpartum, Damin gilts showed a higher frequency of postural changes from lateral recumbency to other postures and less ventral recumbency, sham-chewing, and bar-biting behavior compared with Large White gilts. However, no significant differences were found between Damin and Large White gilts with regard to urination, defecation, tail wagging, and “tail low” behaviors. The concentrations of serum interleukin-6, salivary α-amylase, and serum tumor necrosis factor-α were higher in Damin gilts than in Large White gilts during the fifth week postpartum. Damin gilts partly achieve lower stress levels during late lactation and better animal welfare than purebred Large White gilts.

breed; gilt; lactation; physiology; welfare

1. Introduction

In recent years, welfare considerations have increased the interest in loose-housing systems (large individual house for breeding) for parturient and lactating sows ( Damm et al., 2005Damm, B. I.; Forkman, B. and Pedersen, L. J. 2005. Lying down and rolling behaviour in sows in relation to piglet crushing. Applied Animal Behaviour Science 90:3-20. https://doi.org/10.1016/j.applanim.2004.08.008
https://doi.org/10.1016/j.applanim.2004....
). Growing evidence indicates that a barren environment during lactation negatively impacts sows, and environmental enrichment might be a useful procedure to improve their welfare ( Jarvis et al., 2006Jarvis, S.; D’Eath, R. B.; Robson, S. K. and Lawrence, A. B. 2006. The effect of confinement during lactation on the hypothalamic-pituitary-adrenal axis and behaviour of primiparous sows. Physiology and Behavior 87:345-352. https://doi.org/10.1016/j.physbeh.2005.10.004
https://doi.org/10.1016/j.physbeh.2005.1...
; Van de Weerd and Day, 2009Van de Weerd, H. A. and Day, J. E. L. 2009. A review of environmental enrichment for pigs housed in intensive housing systems. Applied Animal Behaviour Science 116:1-20. https://doi.org/10.1016/j.applanim.2008.08.001
https://doi.org/10.1016/j.applanim.2008....
). Stress reduction is an important aspect to improve welfare of gilts during late lactation.

This study compares the stress level of two gilt breeds during lactation. The Min pig, a local breed that can be commonly found in north-eastern China, displays good maternal instincts ( Cui et al., 2011Cui, S. Q.; Chen, D. H.; Li, J. H.; Li, X.; Yin, G. A. and Bao, J. 2011. A comparison of postural changes and maternal responsiveness during early lactation in Landrace and Minpig sows. Applied Animal Behaviour Science 131:40-47. https://doi.org/10.1016/j.applanim.2011.01.011
https://doi.org/10.1016/j.applanim.2011....
; Liu et al., 2013Liu, H. G.; Wang, C.; Lv, J.; Yu, Y. Q.; Zhang, J. L. and Bao, J. 2013. Behavior and performance in primiparous sows of two Min pig hybrid breeds in outdoor housing systems. Applied Animal Behaviour Science 146:37-44. https://doi.org/10.1016/j.applanim.2013.03.010
https://doi.org/10.1016/j.applanim.2013....
). The majority of relevant research has focused on common commercial pig breeds (such as the Large White), and far less is known about how traditional breeds may cope in these intensive production systems. Thus, utilizing maternal advantages, Damin gilts (Large White × Min gilts) were used to evaluate the behavioral and physiological animal welfare of gilts during late lactation.

Interest for the animal welfare of farm animals is increasing to achieve an improvement of our understanding of both animal welfare and health ( Mendl and Paul, 2004Mendl, M. and Paul, E. S. 2004. Consciousness, emotion and animal welfare: insights from cognitive science. Animal Welfare 13:17-25. ; Boissy et al., 2007Boissy, A.; Manteuffel, G.; Jensen, M. B.; Moe, R. O.; Spruijt, B.; Keeling, L. J.; Winckler, C.; Forkman, B.; Dimitrov, I.; Langbein, J.; Bakken, M.; Veissier, I. and Aubert, A. 2007. Assessment of positive emotions in animals to improve their welfare. Physiology & Behavior 92:375-397. https://doi.org/10.1016/j.physbeh.2007.02.003
https://doi.org/10.1016/j.physbeh.2007.0...
). So far, researchers in this field have focused on sham-chewing ( Mason, 1993Mason, G. J. 1993. Forms of stereotypic behaviour. In: Stereotypic animal behaviour: fundamentals and applications to welfare. CAB International, Wallingford. ), bar-biting ( Lawrence and Terlouw, 1993Lawrence, A. B. and Terlouw, E. M. C. 1993. A review of behavioral factors involved in the development and continued performance of stereotypic behaviors in pigs. Journal of Animal Science 71:2815-2825. https://doi.org/10.2527/1993.71102815x
https://doi.org/10.2527/1993.71102815x...
), and excessive excretion ( Mendl et al., 1997Mendl, M.; Erhard, H. W.; Haskell, M.; Wemelsfelder, F. and Lawrence, A. B. 1997. Experience in substrate-enriched and substrate-impoverished environments affects behaviour of pigs in a T-maze task. Behaviour 134:643-659. https://www.jstor.org/stable/4535463
https://www.jstor.org/stable/4535463...
; Mendl and Paul, 2004Mendl, M. and Paul, E. S. 2004. Consciousness, emotion and animal welfare: insights from cognitive science. Animal Welfare 13:17-25. ; Zupan et al., 2016Zupan, M.; Framstad, T. and Zanella, A. J. 2016. Behaviour, heart rate, and heart rate variability in pigs exposed to novelty. Revista Brasileira de Zootecnia 45:121-129. https://doi.org/10.1590/S1806-92902016000300006
https://doi.org/10.1590/S1806-9290201600...
). The results indicated that these behaviors are closely associated with negative emotions ( Mendl et al., 1997Mendl, M.; Erhard, H. W.; Haskell, M.; Wemelsfelder, F. and Lawrence, A. B. 1997. Experience in substrate-enriched and substrate-impoverished environments affects behaviour of pigs in a T-maze task. Behaviour 134:643-659. https://www.jstor.org/stable/4535463
https://www.jstor.org/stable/4535463...
). Numerous studies have shown that tail postures are indicators of behavioral and psychological responses ( Forkman et al., 2007Forkman, B.; Boissy, A.; Meunier-Salaün, M. C.; Canali, E. and Jones, R. B. 2007. A critical review of fear tests used on cattle, pigs, sheep, poultry and horses. Physiology & Behavior 92:340-374. https://doi.org/10.1016/j.physbeh.2007.03.016
https://doi.org/10.1016/j.physbeh.2007.0...
; Reefmann et al., 2009Reefmann, N.; Kaszàs, F. B.; Wechsler, B. and Gygax, L. 2009. Ear and tail postures as indicators of emotional valence in sheep. Applied Animal Behaviour Science 118:199-207. https://doi.org/10.1016/j.applanim.2009.02.013
https://doi.org/10.1016/j.applanim.2009....
; Boissy et al., 2011Boissy, A.; Aubert, A.; Désiré, L.; Greiveldinger, L.; Delval, E. and Veissier, I. 2011. Cognitive sciences to relate ear postures to emotions in sheep. Animal Welfare 20:47-56. ; Jones and Boissy, 2011Jones, B. and Boissy, A. 2011. Fear and other negative emotions. p.78-97. In: Animal welfare. 2nd ed. Appleby, M. C.; Mench, J. A.; Olsson, I. A. S. and Hughes, B. O., eds. CAB International, Wallingford. ; Marcet-Rius et al., 2019Marcet-Rius, M.; Fàbrega, E.; Cozzi, A.; Bienboire-Frosini, C.; Descout, E.; Velarde, A. and Pageat, P. 2019. Are tail and ear movements indicators of emotions in tail-docked pigs in response to environmental enrichment? Animals 9:449. https://doi.org/10.3390/ani9070449
https://doi.org/10.3390/ani9070449...
).

It is generally assumed that long-term stress exerts an inhibitory effect on the immune system ( Groot et al., 2000Groot, J.; Jong, I. C.; Prelle, I. T. and Koolhaas, J. M. 2000. Immunity in barren and enriched housed pigs differing in baseline cortisol concentration. Physiology & Behavior 71:217-223. https://doi.org/10.1016/S0031-9384 (00)00336-X
https://doi.org/10.1016/S0031-9384 (00)0...
). Therefore, IFN-γ (interferon gamma), TNF-α (tumor necrosis factor alpha; which mediates cellular immunity), as well as IL-10 (interleukin) and IgG (immunoglobulin G), both of which mediate humoral immunity, are immune factors that can be used for the evaluation whether animals are in a state of infection or chronic stress. To evaluate the advantages of hybrid sows, this study assessed the behavior and physiology of both Damin and Large White sows during the late lactation period.

2. Material and Methods

All procedures used for the present study were approved by the local Institutional Animal Care and Use Committee (case no. IACECNEAU20121013). This study was performed in Harbin, Heilongjiang Province, China (45°31'12" E longitude, 126°57'11" N latitude, and 126 m altitude).

Eighty first-parity gilts (40 Damin and 40 Large White gilts) that had been mated with Duroc (Canadian) males, were selected. No significant differences were found between both breeds (Damin vs. Large White) with regard to backfat and weight when gilts were mated at an age of 7-8 months (backfat: 18.99±1.22 vs 19.06±0.91; weight: 113.39±6.10 vs 115.99±5.01 kg, respectively). Both groups were housed in identical pens (5.5 m width, 5.6 m length), each containing 10 pregnant gilts, a sow feeder, a water nipple drinker, and concrete flooring with straw. A heating pad was set up in the lying area to automatically heat; the gas environment was controlled by an automatic detection system to prevent harmful gases from exceeding standards; and average temperature and humidity were maintained at 24 ℃ and 65%, respectively. Sows were transferred to parturition pens seven days before the expected due date. Each gilt was randomly assigned to a parturition house. The litter sizes of Damin and Large White gilts were 14.0±1.4 and 12.3±1.5, respectively (P = 0.018), and their survival rates were 91.80 and 89.69%, respectively (P = 0.08).

The structure of an enriched farrowing pen was used in this study ( Figure 1 ). A wall partitioned the parturition area and piglet activity area in each parturition pen; however, a space between the wall and the floor allowed piglets free access. Each parturition pen held one sow and was made of galvanized tubes with an inset straw board, which was divided into lying and excreting areas. Two drinkers were provided at different heights so that both sows and piglets had convenient access to water. The concrete floor had a slope of 18°. All parturition pens contained straw as litter material (with a thickness of 0.05 m), which was supplemented after cleaning every morning.

Figure 1
Structure of the enriched farrowing pen.

Gilts were fed twice daily (at 07:30 and 16:00 h) in their parturition pens. The health of piglets was assessed, and sick piglets were removed from parturition pens at 06:30 h each morning. Approximately 2 cm of bedding was added to parturition pen floors at 07:30 h each weekend. All gilts were restrictively fed 3 kg of complete feed per day, which contained the following constituents per kg: 12.9 MJ ME, 185.0 g crude protein, 50.0 g crude fat, 80.0 g crude ash, and 12.0 g lysine. During the study period, both the temperature and relative humidity of the interior and exterior of the parturition pens were measured daily using a hygrothermograph (Kestrel 4000 Pocket Weather Tracker; Kestrel, Santa Cruz, CA, USA). Daily temperature and humidity inside the parturition pens in August were 21.6 ℃ and 58.7%, respectively, while in September, the values were 14.7 ℃ and 51.3%, respectively. Piglets were weaned on day 35 after birth, and neither tails nor teeth were docked.

Behaviors of gilts were recorded with a video surveillance system (DS-IT5, Hangzhou Hikvision Digital Technology Co., Ltd., Hangzhou, China) to prevent artificially delimited observation times from impacting the test results. From the third to the fifth post-parturition weeks, all behaviors were recorded on video via focal sampling continuous recording from 07:00 to 09:00 h and 13:00 to 15:00 h on days 3 and 6 of each week; this could avoid stockman feeding time and sow sleeping time, and the observation interval twice a week was to increase the behavior of sows at each observation and then prevent the observer’s subjective judgment from affecting sow behavior statistics, in addition to avoiding man-made disturbance of sow behavior caused by the noise from cleaning the outside walls and corridors of the farm every Sunday. The behaviors were observed via instantaneous sampling (20-s interval) for the statistics of status behavior in a more accurate and less demanding manner. Data of continuous behaviors were converted into percentages of the total observation time, and aggregated data of behaviors were recorded as the number of their occurrence. The parameters and their definitions are presented in Table 1 .

Table 1
Behavioral parameters and their definitions 1

Blood samples of each sow were collected at the 7th day of weeks 3, 4, and 5 of lactation. Immediately after the collection of blood from the ear vein, serum was prepared. The concentrations of IL-6 and TNF-α in serum were measured with a commercial porcine ELISA kit (Nanjing Jiancheng Bioengineering Institute, Nanjing, China). Concentrations of salivary α-amylase in the saliva were assayed using a commercial porcine ELISA kit (Nanjing Jiancheng Bioengineering Institute) ( Cook et al., 1996Cook, N. J.; Schaefer, A. L.; Lepage, P. and Morgan Jones, S. 1996. Salivary vs. serum cortisol for the assessment of adrenal activity in swine. Canadian Journal of Animal Science 76:329-335. https://doi.org/10.4141/cjas96-049
https://doi.org/10.4141/cjas96-049...
). The sponge block was wrapped in sterile gauze before both sides of the sponge were fastened with sterile ribbon gauze. Then, both sides of the ribbon gauze were connected with a 0.1 m elastic rubber hose. All equipment was disinfected after use.

All dependent variables were examined for normal distribution, using PROC UNIVARIATE of SAS (Statistical Analysis System, version 9.0), considering skewness, kurtosis, the Shapiro-Wilks test (for normality), and a normal probability plot. A GLM procedure of SAS was used to test behavioral differences between both breeds and time-dependent observations. The model for behavioral analysis after parturition included the following effects:

Y i j k = μ + Breed i + Time j + Breed i × Time j + e i j

in which μ represents the overall average, Breed i represents the effect of breed on behavior data, Time j represents the effect of the number of weeks after parturition (W 3 , W 4 , and W 5 ) on behavior data, and Breed i × Time j indicates the interaction between breeds and observation time. All data are presented as mean ± standard errors.

3. Results

There were no significant differences in behaviors between Damin and Large White gilts during weeks 3 and 4, with the exception of tail curling in the fourth week (P>0.05); however, significant differences were found between Damin and Large White gilts with regard to movement from lateral recumbency to other postures, such as ventral recumbency, sham-chewing, and bar-biting behavior in week 4 (P = 0.030, P = 0.007, P = 0.004). During the study period, no differences were found between Damin and Large White gilts with regard to urination, defecation, tail wagging, and “tail low” behavior (P>0.05). The frequency of movements from lateral recumbency to other postures gradually increased in Damin and Large White gilts over extended lactation ( Table 2 ).

Table 2
Observations of behavioral differences and changes in two different breeds of gilts kept in the same environment for 3 to 5 weeks after farrowing

No significant differences were found between both breeds of gilts in serum concentrations of TNF-α and IL-6 during the third and fourth weeks after parturition (P>0.05). The concentration of salivary α-amylase in the third and fourth weeks after parturition also did not significantly differ between both breeds (P>0.05); however, significant differences were found between both breeds in the fifth week in concentrations of TNF-α, IL-6, and salivary α-amylase (P = 0.028, P = 0.035, and P = 0.022, respectively). During extended lactation period, concentrations of TNF-α and salivary α-amylase decreased progressively. Serum concentration of IL-6 in Damin gilts followed an increasing tendency. The concentration of IL-6 of Large White gilts initially followed an increasing trend and then decreased ( Table 3 ).

Table 3
Effect of breed on the physiological indices of gilts at different stages

4. Discussion

Ventral recumbency and movement from lateral recumbency to other postures represent two important indicators of a gilt’s refusal to lactate ( Gonyou et al., 1998Gonyou, H. W.; Beltranena, E.; Whittington, D. L. and Patience, J. F. 1998. The behaviour of pigs weaned at 12 and 21 days of age from weaning to market. Canadian Journal of Animal Science 78:517-523. https://doi.org/10.4141/A98-023
https://doi.org/10.4141/A98-023...
; Valros et al., 2003Valros, A.; Rundgren, M.; Špinka, M.; Saloniemi, H.; Rydhmer, L.; Hultén, F.; Uvnäs-Moberg, K.; Tománek, M.; Krejcı́, P. and Algers, B. 2003. Metabolic state of the sow, nursing behaviour and milk production. Livestock Production Science 79:155-167. https://doi.org/10.1016/S0301-6226 (02)00154-9
https://doi.org/10.1016/S0301-6226 (02)0...
). In the present study, observations of ventral recumbency at weeks 3-5 postpartum showed that both breeds gradually refused to lactate. This trend toward this type of behavior may indicate that the use of more maternal gilt breeds (i.e., Damin pigs) might still not eliminate the resulting effects on piglets. However, at the fifth week after parturition, Damin gilts spent markedly less time in ventral recumbency than Large White gilts. This might indicate that Damin gilts had particular advantages when dealing with late lactation under stress conditions, and may have a genetically favorable maternal ability and inherited tolerance traits of the Min pig breed ( Liu et al., 2013Liu, H. G.; Wang, C.; Lv, J.; Yu, Y. Q.; Zhang, J. L. and Bao, J. 2013. Behavior and performance in primiparous sows of two Min pig hybrid breeds in outdoor housing systems. Applied Animal Behaviour Science 146:37-44. https://doi.org/10.1016/j.applanim.2013.03.010
https://doi.org/10.1016/j.applanim.2013....
).

Excessive excretion has been reported to be closely related to negative animal welfare and stress being experienced by the animals ( Jones and Boissy, 2011Jones, B. and Boissy, A. 2011. Fear and other negative emotions. p.78-97. In: Animal welfare. 2nd ed. Appleby, M. C.; Mench, J. A.; Olsson, I. A. S. and Hughes, B. O., eds. CAB International, Wallingford. ); however, in this study, both defecation and urination behaviors of both gilt breeds were neither directly affected by late lactation environment nor by piglets. This may be related to the enriched farrowing environments that were used for both gilt breeds in the present study. Results of both gilt breeds were derived from conditions in which the gilts were not sufficiently stressed during the late lactation phase. Nevertheless, other authors have found that excessive excretion might be caused by severe environmental constraints. For example, excessive excretion has been reported for sows that were kept in restricted spaces ( Chapinal et al., 2010Chapinal, N.; Ruiz de la Torre, J. L.; Cerisuelo, A.; Gasa, J.; Baucells, M. D.; Coma, J.; Vidal, A. and Manteca, X. 2010. Evaluation of welfare and productivity in pregnant sows kept in stalls or in 2 different group housing systems. Journal of Veterinary Behavior 5:82-93. https://doi.org/10.1016/j.jveb.2009.09.046
https://doi.org/10.1016/j.jveb.2009.09.0...
).

In the present study, the frequency of tail wagging decreased gradually under conditions of extended lactation. This indicates that tail wagging may be a very useful index for animal emotional behavior; however, the association between tail wagging and positive animal welfare still requires a more formal verification ( Newberry et al., 1988Newberry, R. C.; Wood-Gush, D. G. M. and Hall, J. W. 1988. Playful behavior of piglets. Behavioural Processes 17:205-216. https://doi.org/10.1016/0376-6357 (88)90004-6
https://doi.org/10.1016/0376-6357 (88)90...
; Kleinbeck and McGlone, 1993Kleinbeck, S. N. and McGlone, J. J. 1993. Pig tail posture: a measure of stress. Texas Tech University Agricultural Science Technical Report No. T-5-327. p.47-48. ; Terlouw and Porcher, 2005Terlouw, E. M. C. and Porcher, J. 2005. Repeated handling of pigs during rearing. I. Refusal of contact by the handler and reactivity to familiar and unfamiliar humans. Journal of Animal Science 83:1653-1663. https://doi.org/10.2527/2005.8371653x
https://doi.org/10.2527/2005.8371653x...
). In the present study, the tail low position occurred more often during the fourth and fifth weeks than during the third week after parturition. This indicates that the tail low position may represent a potentially novel indicator of negative emotional expression in pigs. The expression of tail curling did not appear to follow any particular rule in both breeds during the experimental period. Therefore, it cannot be used as an indicator of animal welfare (with an acceptable standard of accuracy) and, therefore, does not seem to be useful when determining late-lactation behavior and welfare of sows.

Large White gilts exhibited more sham-chewing and bar-biting behaviors during the fourth and fifth weeks postpartum than Damin gilts. This indicates that Large White gilts had a more negative emotional state during late lactation than Damin gilts, which is consistent with previously published observations ( Chapinal et al., 2010Chapinal, N.; Ruiz de la Torre, J. L.; Cerisuelo, A.; Gasa, J.; Baucells, M. D.; Coma, J.; Vidal, A. and Manteca, X. 2010. Evaluation of welfare and productivity in pregnant sows kept in stalls or in 2 different group housing systems. Journal of Veterinary Behavior 5:82-93. https://doi.org/10.1016/j.jveb.2009.09.046
https://doi.org/10.1016/j.jveb.2009.09.0...
). Furthermore, we propose abnormal behaviors, such as sham-chewing and bar-biting, to be valuable indicators of negative animal welfare in late-lactating sows.

The concentration of salivary α-amylase tended to gradually decrease during extended lactation, which is consistent with psychological observations in humans. Thus, it is possible that the decrease in salivary α-amylase concentration is regulated by chronic stress ( Grigoriev et al., 2003Grigoriev, I. V.; Nikolaeva, L. V. and Artamonov, I. D. 2003. Protein content of human saliva in various psycho-emotional states. Biochemistry 68:405-406. ; Wolf et al., 2008Wolf, J. M.; Nicholls, E. and Chen, E. 2008. Chronic stress, salivary cortisol, and α-amylase in children with asthma and healthy children. Biological Psychology 78:20-28. https://doi.org/10.1016/j.biopsycho.2007.12.004
https://doi.org/10.1016/j.biopsycho.2007...
). In the present study, the decrease in salivary α-amylase concentration might indicate sustained stress in both gilt breeds during the late lactation period. Therefore, salivary α-amylase can be considered as a valuable indicator for assessment of psychological state of gilts.

Serum concentration of IL-6 was significantly higher in Damin gilts than in Large White gilts during the fifth week after parturition. The major reason for this observed difference might be the dual function of IL-6 as a cytokine that displays both pro- and anti-inflammatory properties ( Zaldivar et al., 2006Zaldivar, F.; Wang-Rodriguez, J.; Nemet, D.; Schwindt, C.; Galassetti, P.; Mills, P. J.; Wilson, L. D. and Cooper, D. M. 2006. Constitutive pro- and anti-inflammatory cytokine and growth factor response to exercise in leukocytes. Journal of Applied Physiology 100:1124-1133. https://doi.org/10.1152/japplphysiol.00562.2005
https://doi.org/10.1152/japplphysiol.005...
). Thus, the insensitivity of serum IL-6 levels to stress, which was observed in the present study, may be associated with the anti-inflammatory action of IL-6. The exposure of Damin gilts to continuous stress during the fifth week might have caused them to adapt to the environment during the late lactation period via a compensatory increase of the levels of beneficial inflammatory cytokines ( Chrousos, 2000Chrousos, G. P. 2000. Stress, chronic inflammation, and emotional and physical well-being: concurrent effects and chronic sequelae. Journal of Allergy & Clinical Immunology 106:S275-S291. https://doi.org/10.1067/mai.2000.110163
https://doi.org/10.1067/mai.2000.110163...
; Marshall Jr. and Agarwal, 2000). However, during the fifth week of lactation, the ability of Large White gilts to adapt to environmental stress decreased, which might have led to a decline in the production of immunological factors. Combined with observations of the abovementioned behaviors, this outcome might also indicate that Damin gilts had a higher capacity to adjust to late lactation stress and a superior level of psychological health compared with Large White gilts. With extended lactation period, the serum concentration of IL-6 in Damin gilts increased significantly, while that in Large White gilts increased briefly before following a decreasing trend. These observations were consistent with previously reported results (DeRijk, et al., 1997; Tuchscherer et al., 2009Tuchscherer, M.; Kanitz, E.; Puppe, B.; Tuchscherer, A. and Viergutz, T. 2009. Changes in endocrine and immune responses of neonatal pigs exposed to a psychosocial stressor. Research in Veterinary Science 87:380-388. https://doi.org/10.1016/j.rvsc.2009.04.010
https://doi.org/10.1016/j.rvsc.2009.04.0...
). Such changes might also reflect the psychological component of the stressor, which has been characterized by an uncontrolled and unpredictable appearance of anxiety in animals ( Mormede et al., 1988Mormede, P.; Dantzer, R.; Michaud, B.; Kelley, K. W. and Le Moal, M. 1988. Influence of stressor predictability and behavioral control on lymphocyte reactivity, antibody responses and neuroendocrine activation in rats. Physiology & Behavior 43:577-583. https://doi.org/10.1016/0031-9384 (88)90211-9
https://doi.org/10.1016/0031-9384 (88)90...
; Brosschot et al., 1998Brosschot, J. F.; Godaert, G. L. R.; Benschop, R. J.; Olff, M.; Ballieux, R. E. and Heijnen, C. J. 1998. Experimental stress and immunological reactivity: a closer look at perceived uncontrollability. Psychosomatic Medicine 60:359-361. ; Peters et al., 1999Peters, M. L.; Godaert, G. L. R.; Ballieux, R. E.; Brosschot, J. F.; Sweep, F. C. G. J.; Swinkels, L. M. J. W.; van Vliet, M. and Heijnen, C. J. 1999. Immune responses to experimental stress: effects of mental effort and uncontrollability. Psychosomatic Medicine 61:513-524. https://doi.org/10.1097/00006842-199907000-00016
https://doi.org/10.1097/00006842-1999070...
).

In the present study, serum concentration of TNF-α in Damin gilts was higher than that in Large White gilts during the fifth week of lactation. Since it is conventionally accepted that glucocorticoids specifically suppress the release of pro-inflammatory cytokines ( Besedovsky and del Rey, 2000Besedovsky, H. O. and del Rey, A. 2000. The cytokine-HPA axis feed-back circuit. Zeitschrift für Rheumatologie 59(Supplement 2):II26–II30. https://doi.org/10.1007/s003930070014
https://doi.org/10.1007/s003930070014...
; Sapolsky et al., 2000Sapolsky, R. M.; Romero, L. M. and Munck, A. U. 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21:55-89. https://doi.org/10.1210/edrv.21.1.0389
https://doi.org/10.1210/edrv.21.1.0389...
), the reasons for the differences observed in this study might be due to the relatively lower degree of stress that was experienced by Damin gilts under the influence of glucocorticoids compared with Large White gilts under similar states of stress. Extending the lactation period placed both gilt breeds under increased stress, and consequently, the serum concentration of TNF-α gradually decreased, which is similar to previously reported results ( DeRijk et al., 1997DeRijk, R.; Michelson, D.; Karp, B.; Petrides, J.; Galliven, E.; Deuster, P.; Paciotti, G.; Gold, P. W. and Sternberg, E. M. 1997. Exercise and circadian rhythm-induced variations in plasma cortisol differentially regulate interleukin-1β (IL-1β), IL-6, and tumor necrosis factor-α (TNFα) production in humans: high sensitivity of TNFα and resistance of IL-6. Journal of Clinical Endocrinology & Metabolism 82:2182-2191. https://doi.org/10.1210/jcem.82.7.4041
https://doi.org/10.1210/jcem.82.7.4041...
; Besedovsky and Rey, 2000; Sapolsky et al., 2000Sapolsky, R. M.; Romero, L. M. and Munck, A. U. 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21:55-89. https://doi.org/10.1210/edrv.21.1.0389
https://doi.org/10.1210/edrv.21.1.0389...
). A possible explanation for this psychological stress might be beyond the scope of modulated and cell-derived TNF-α. These present findings emphasize the particular importance of TNF-α for assessing animal welfare, health, and psychosocial stress in gilts.

Tumor necrosis factor-α and IL-6 are also important immune-regulatory factors; TNF-α induces Th1-type effector cell differentiation and is a major mediator of cellular immunity ( Salem, 2004Salem, M. L. 2004. Estrogen, a double-edged sword: modulation of TH1-and TH2-mediated inflammations by differential regulation of TH1/TH2 cytokine production. Current Drug Targets-Inflammation & Allergy 3:97-104. https://doi.org/10.2174/1568010043483944
https://doi.org/10.2174/1568010043483944...
). Similarly, the cytokine IL-6 is predominantly secreted by Th2-differentiated T-cells and plays a major role in humoral-mediated immunity ( Jarvis et al., 1997Jarvis, S.; Lawrence, A. B.; McLean, K. A.; Deans, L. A.; Chirnside, J. and Calvert, S. 1997. The effect of environment on behavioural activity, ACTH, (β-endorphin and cortisol in pre-farrowing gilts. Animal Science 65:465-472. https://doi.org/10.1017/S1357729800008663
https://doi.org/10.1017/S135772980000866...
). In general, Th1-type effector T-cells and Th2 effector T-cells both secrete factors that restrict each other’s functions with regard to inflammation and host immunity. In doing so, immunological homeostasis is maintained at the levels of normal cellular and humoral immune competence and functional dynamic balance ( Tsai et al., 1997Tsai, S.; Liaw, Y.; Chen, M.; Huang, C. and Kuo, G. C. 1997. Detection of type 2-like T-helper cells in hepatitis C virus infection: Implications for hepatitis C virus chronicity. Hepatology 25:449-458. https://doi.org/10.1002/hep.510250233
https://doi.org/10.1002/hep.510250233...
). In the present study, extending the lactation period caused significant increases in concentrations of TNF-α and IL-6 in Damin gilts following parturient readjustment and the balance of Th1/Th2 cells in the blood. However, the immune response of Damin gilts was not only restrained, but also showed an increasing tendency. This result might be related to a compensatory mechanism of increasing selected cytokines and establishing a new set-point for immunological homeostasis in an attempt to adapt to the stress the lactation environment induces. The Th1/Th2 cells in the blood of Large White gilts were in a state of disequilibrium at the fifth week postpartum. This also supports the fact that Large White gilts showed potential for immunological injury during extended lactation.

5. Conclusions

Hybrid Damin gilts show improved maternal behavior and physiological immune performance compared with purebred Large White gilts during late lactation. This indicates that hybrid sows inherited good maternal characteristics and immune capacity. However, both production performance and welfare of sows cannot be improved based on this experiment.

Acknowledgments

The authors would like to thank Jian Han for technical assistance, Zhipeng Wang for help in statistical analyses, and all the staff at the Swine Complex for care of the animals. We thank Kelly Zammit, BVSc, from Liwen Bianji, Edanz Group China, for editing the English text of a draft of this manuscript. This study was supported by a grant from the Earmarked Fund for China Agriculture Research System (no. CARS-35), projects C2016016 and 2017RAQXJ062 of the Province Science Foundation of Hei Longjiang in China.

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Publication Dates

  • Publication in this collection
    06 June 2022
  • Date of issue
    2022

History

  • Received
    25 May 2019
  • Accepted
    25 Nov 2020
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