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Article

Effect of an Enriched Elevated Platform Rearing System on the Welfare and Bone Quality of Fattening Pigs

by
Yue Yang
1,†,
Sitong Zhou
1,†,
Xin Li
1,
Qin Fu
1,
Xiaohong Zhang
1,
Wenbo Ji
1 and
Honggui Liu
1,2,*
1
College of Animal Science and Technology, Northeast Agricultural University, No. 600 Changjiang Road, Harbin 150030, China
2
Key Laboratory of Swine Facilities Engineering, Ministry of Agriculture and Rural Affairs, Northeast Agricultural University, No. 600 Changjiang Road, Harbin 150030, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agriculture 2024, 14(6), 943; https://doi.org/10.3390/agriculture14060943
Submission received: 2 May 2024 / Revised: 26 May 2024 / Accepted: 29 May 2024 / Published: 17 June 2024
(This article belongs to the Section Farm Animal Production)
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Abstract

:
An intensive breeding environment usually sacrifices the biological needs of pigs and will have a negative impact on the welfare and production efficiency of pigs. In this study, a bedding elevated platform rearing system was established and its effect on the welfare of fattening pigs was evaluated. A total of 456 fattening pigs were divided into the elevated platform rearing system group (EP) and control group (CON). The welfare of pigs during the rearing period (57–97 days of age) and the fattening periods (98–168 days of age) was assessed through behavioral observation, physiological indicators, growth performance, and bone quality. Pigs in the EP group showed less manipulating behavior and more playing behavior than pigs in the CON group during the first 48 h of the test. Moreover, EP pigs expressed more standing, play, and exploratory behaviors and less sitting, lying down, manipulating, and fighting behaviors than the CON pigs during the rearing period. More standing and playing behavior and less sitting, manipulating behavior, and fighting behavior were expressed in the EP group than the CON group during the fattening period. In both of the rearing and fattening periods, serum cortisol concentrations were lower in the EP group than the CON group; C-reactive protein concentrations were significantly higher in the EP group than CON group; TNF-α, IFN-γ, IL-1β, IL-2, IL-6, IgA, IgG, and IgM levels were significantly higher in the EP group than the CON group, but IL-10 levels were significantly lower in the EP group than the CON group. The EP group had less skin lesions and a higher final body weight. Our study confirms that the enriched elevated platform rearing system promotes the expression of positive behaviors and reduced skin and limb lesions, which also improve the growth performance of pigs.

1. Introduction

Modern animal husbandry mostly implements a typical intensive production mode, in which animals are kept in specialized indoor environments and equipped with automated equipment to reduce labor for routine tasks [1]. However, in barren environment rearing systems, animals suffer from more significant welfare issues, such as overcrowding, social restriction, and lameness [2]. In addition, pigs exposed to artificial environments and stressful conditions for extended periods may develop stereotypies and other abnormal behaviors (e.g., sham chewing, bar biting, and increased aggression) [3,4,5], which can manifest boredom and frustration and lead to harmful, manipulating social behaviors, such as frequent ear biting and tail biting [6].
The development of dual-platform rearing systems has been proposed in European countries to address many of the welfare issues associated with barren environment rearing systems to meet the natural behavioral needs of pigs and increase available areas [7,8]. The elevated platforms help to create different functional areas within the pen to improve the welfare of the pigs [7]. Scientific research on elevated platforms for pigs at eight weeks of age [9,10] and fattening pigs [11,12] already started in the 1980s. However, earlier studies only examined and elaborated on the motivation and comfort of pigs using the ramp and demonstrated that the extra space was utilized.
Previous studies have demonstrated that elevated platform rearing systems can positively affect the nursery phase [12] or fattening phase [7] of pigs, for example, the elevated platform provides more space and more options for pigs to have different places to rest [13] or hide from aggressive pigs [11] and to move around without disturbing other companions [7]. However, the previous research on elevated platforms was more aimed at ensuring economic benefits and avoiding the injury of pigs by increasing the usable area of the barn, but only a few studies added other enriched materials to the rearing system to meet the natural behavior needs of pigs, such as playing and exploring [8], to improve animal welfare.
In practical production, the growth performance of pigs is the most intuitive index to measure economic benefits, and it also reflects the welfare level of pigs in the feeding stage. Previous studies have confirmed that setting the trough on the floor area will not have a negative impact on the growth performance of pigs when the feed supply is sufficient [10,11]. Bulens et al. [7] found that the elevated platform had no effect on the weight of pigs in fattening period, and the differences of carcass weight, lean meat percentage, backfat thickness, and meat building index between the groups were also not significant. In addition, the use of elevated platform has a positive effect on the mean daily weight gain of weaned piglets [14]. Compared to a barn without an elevated platform, the skin lesion score of pigs raised in an elevated platform system is also relatively lower [7,14].
In this study, an elevated platform rearing system with bedding and multiple enrichments (chains, toy balls, and chew toys) was constructed, based on previous studies, to analyze the effects of the system on bone quality of and physical damage in pigs and to determine its effects on the behavior, physiology, and growth performance of fattening pigs.

2. Materials and Methods

2.1. Animals and Management

A total of 456 female fattening pigs [Yorkshire ♂ × (Landrace ♂ × Yorkshire ♀) ♀] were selected in this study for a 110-day trial (rearing period: 57–97 days old; fattening period: 98–168 days old). The experimental pigs had their teeth clipped within three days after birth but without tail docking. After weaning at 35 days of age, they were nursed in the original pens until they were transferred to the trial site at 8 weeks of age (20.86 ± 0.46 kg). The experiment was conducted in two independent fattening barns (the specifications and microclimate parameters of the two barns are identical), each divided into three pens (11.5 m × 8 m), and 76 pigs with similar weight were equally distributed in each pen. Each pen in one of the barns was equipped with elevated platforms and thick bedding, denoted as the EP group (the elevated platform rearing system, EP group), and three pens in the other barn only had a concrete floor (without elevated platform and thick bedding) denoted as the control group (barren environment rearing system, CON group).
The exact specifications of the elevated platform rearing system in the pig house are shown in Figure 1a and Supplementary Figure S1. The thickness of bedding in the thick bedding area was 0.8 m, composed of chaff and rice husk. The platform (2.7 m × 11.5 m) was placed 1 m high above the thick bedding area (2.7 m × 11.5 m) and consisted of a stainless steel leaky seam mesh bed with a 0.6 m high fence to prevent the pigs from falling off the platform. The same number of enrichment items, such as chains, toy balls, and chew toys, were provided on the platform for each treatment group. The platform was connected to the ground by a ramp (0.7 m × 3.8 m) with a slope of 15 degrees. Iron anti-slip bars were installed every 20 cm on the surface of the climbing ramp to facilitate the pigs’ walking. On the opposite side of the platform, multiple troughs and waterers were provided for pigs. The barren environment rearing system (Figure 1b) had only a concrete floor (8 m × 11.5 m) and was not equipped with an elevated platform and thick bedding.
The average usable space of each pig in the CON group was 1.210 m2. The number of pigs raised in the EP group was the same as that in the CON group, and the elevated platform generated an additional space of 0.409 m2 per pig, with the average usable space per pig in the EP group being 1.619 m2. The barns adopted natural lighting and forced ventilated (longitudinal negative pressure ventilation). Each pigsty was equipped with two stainless steel automatic pig feeders and five automatic nipple drinkers. The feed (compound feed for fattening pigs 557, Wellhope Animal Husbandry Co., Ltd., Shenyang, China) was refilled daily at 8 am, and all pigs could eat and drink ad libitum. Before and during the experiment, regular cleaning and disinfection work was carried out to keep the pens clean and hygienic. Manure in the thick bedding area was not cleaned and was manually turned and thrown once every fortnight and new bedding added.

2.2. Skin and Limb Lesion Scoring

In this study, 30 pigs from each pen were selected as focal animals for skin and limb lesion scoring. Skin lesions of the head, shoulders, flanks, buttocks, and back (right and left side, respectively) of each focal pig were assessed, and each part was scored by a scoring system in the range of 0–3, with the highest cumulative total score of 30 (Table 1). Skin lesions of the tail and two ears were scored by a scoring system in the range of 0–2, with the highest cumulative total score of 6 (Table 1). The sum of the scores of each part was recorded as the final cumulative skin lesion score, with results in the range of 0–36 [15]. Lesions at carpus, tarsus, and coronets/claws were also assessed for each pig’s extremities. For each pig, the scores of all limb parts were summed to calculate a cumulative limb score, with results in the range of 0–36 [14]. In this study, the skin and limb lesions of both treatment groups were assessed by an observer at different time points—on the next day after the pigs entered the experimental site (Day 1, 57 days of age), and thereafter, scorings were repeated at an interval of ten days until Day 110 (168 days of age).

2.3. Behavioral Observation

This study used the ‘pen’ as the experimental unit. The behavioral observation was carried out during the first 48 h after the pigs entered the experimental site, and at 07:00–11:00 and 13:00–17:00 every Monday and Friday during the rearing and fattening periods, respectively. Behavioral monitoring equipment, including the HP-P27V-G4-FHD (HP trading Co., Ltd., Shanghai, China) monitor, the network video recorder DS-IT5 (Hikvision Co., Ltd., Hangzhou, China), and cameras DS-2CD2T25-I5 (Hikvision Co., Ltd., Hangzhou, China), was used to record the standing, sitting, lying, manipulating, exploring, playing, and fighting behaviors of focal pigs in each pen. Each group was equipped with two cameras, which were fixed at the height of 2 m above the ground at the northwest corner and southeast corner of the pen. During the 8 h observation period of each behavior observation day, the behaviors of the focal pigs in each pen were observed and recorded for a continuous 30 s every 5 min using a scanning sampling method [16]. State behaviors (such as lying, standing, and sitting) of the focal pigs in each pen were recorded separately and expressed as a percentage of the duration of the daily observation time (average). The occurrence of event behaviors (such as manipulating, exploration, fighting, and playing) were expressed by the number of times the behaviors occurred during the observation period per day. In addition to the above behaviors, other behaviors were not involved in the analysis process. The behavioral categories and definitions are shown in Table 2.

2.4. Growth Performance

The initial weight of the pigs before feeding was recorded before entry to the experimental site (56 days of age). The final weight of the pigs on an empty stomach was recorded at the end of the rearing period (97 days of age) and the end of the fattening period (168 days of age) in the morning. The feed consumption of each treatment group during the trial was counted separately by recording the difference between the weight of the feed provided daily and the weight of the remaining feed in the trough before adding feed on the next day, and the average daily gain (ADG) and feed conversion ratio (FCR) of the pigs were calculated.
ADG   ( kg / day ) = The   initial   weight − The   final   weight   ( kg ) Duration   of   experiment   ( day )
FCR   = Total   feed   consumption   ( kg ) The   initial   weight − The   final   weight   ( kg )

2.5. Physiological Indexes

At 97 and 168 days of age, 6 pigs with similar weight in each group were randomly selected from the EP and CON groups (24 pigs in total). Each time, 2 groups of pigs (12 in total) were transported to the slaughterhouse by transport vehicles littered with straw bedding, which took about 30 min to transport, avoiding any handling that might cause stress to the pigs during transport. The pigs were slaughtered immediately after being transported to the slaughterhouse. The time from the first pig to the last pig being slaughtered did not exceed 2 h, and the pigs in two groups were slaughtered alternately. Blood samples were collected during slaughter, and 120 mL of blood was taken from each pig. The blood was left to stand for 2 h, and then the supernatant was taken and centrifuged at 3500 r/min for 10 min. Each serum sample was divided into six microcentrifuge tubes (1 mL each) and stored in a freezer at −80 °C. The enzyme-linked immunosorbent assay (ELISA kit, Shanghai HengYuan Biological Technology Co., Ltd., Shanghai, China) was used to detect cortisol (COR), C-reactive protein (CRP), tumor necrosis factor (TNF-α), interferon-gamma (IFN-γ), interleukin 1β (IL-1β), interleukin 2 (IL-2), interleukin 6 (IL-6), interleukin 10 (IL-10), immunoglobulin A (IgA), immunoglobulin G (IgG), and immunoglobulin M (IgM) in serum. The experiment procedure was strict to the kit instructions.

2.6. Bone Sample Collection and Analysis

After slaughter, the forelimb radius and hindlimb tibia were taken from 24 pigs in the EP and CON groups. All obtained bone samples were placed in sealed plastic bags and stored in a freezer at −80 °C. The bone on the left side was used for the quantitative computed tomography (QCT) analysis of bone microstructural parameters. The bone on the right side was used to determine bone breaking strength (BBS). All bones were allowed only one freezing and thawing cycle.
The total of 96 bone samples taken from the freezer were fixed in a solution of paraformaldehyde at a concentration of 4% for 24 h, washed once with 75% alcohol, and then dried. As the bone sample was too large to be sealed in a suitable centrifuge tube, it was stored in a self-sealing bag and finally sent for QCT analysis (Nanchang Shuangjing Biotechnology Co., Ltd., Nanchang, China). The machine scanning parameters were as follows: scanning accuracy/layer thickness: 15 μm, voltage: 80 kV, current: 114 μA, rotation angle: 0 degrees, exposure time: 500 ms, filter selected: 0.5 mm aluminum plate, and pixel combination: 1056 × 1056. After the inspection scan was completed, two-dimensional images were obtained. A three-dimensional reconstruction process was carried out using the Mimics software 26.0 (Materialise NV, Leuven, Belgium) to obtain a three-dimensional image. After the reconstruction was completed, the following parameters were analyzed and detected using the dedicated bone analysis software Abaqus 2022 (Dassault Systèmes, Vélizy-Villacoublay, France): bone mineral density (BMD), bone volume fraction (bone volume/tissue volume, BV/TV), trabecular thickness (Tb.Th), and trabecular separation (Tb.Sp).
After removing the muscle and connective tissue attached to the pig forelimb radius and hindlimb tibia tissue specimens, the bone samples were stored at −80 °C and sent for BBS (Three-point bending test, Shanghai Xiyun Biotechnology Co., Ltd., Shanghai, China). The test was carried out using the UTM 5105 Universal Material Mechanics Testing Machine (Liantai Testing Machine Co., Ltd., Jinan, China). The bone tissue samples were placed on two supporting cross bars with the load bar in the center. All samples were loaded uniformly at a rate of 3 mm/min until the samples were fractured. The maximum bending force and deflection of the tested bone tissue samples before fracture were recorded.

2.7. Statistical Analysis

The statistical software IBM SPSS version 26.0 (IBM, Armonk, NY, USA) was used for the statistical analysis of all data. The normal distribution of the data was tested by the Shapiro–Wilk test, and the homogeneity of variance was analyzed by Levene’s test. The results are expressed as mean ± SE, and the significance level was set at p < 0.05.
Skin and limb lesion scores: After the descriptive analysis of the data, an independent sample t test was conducted with treatment (e.g., elevated platform/none) as the fixed effect and the cumulative scores of skin and limb lesions of the focal pigs as the test variables. The statistical analysis was performed for skin and limb lesion scores of the first day after the experiment began, with the mean values of Days 11–40 and Days 51–110.
Behavior: An independent sample t test was applied to analyze the event and state behaviors of pigs, with the treatment (e.g., elevated platform/none) as the fixed effect. This test was used separately for the three different periods (the first 48 h, the rearing period (mean value), and the fattening periods (mean value)).
Growth performance: An independent sample t test was applied to analyze the weight (at 56, 96, and 168 days of age), ADG, and FCR of pigs, with the treatment (e.g., elevated platform/none) as the fixed effect.
Physiological indexes and bone samples: An independent sample t test was applied to analyze the serum physiological indexes, bone microstructural parameters, and bone breaking strength (BBS) of pigs (at 96 and 168 days of age), with the treatment (e.g., elevated platform/none) as the fixed effect.

3. Results

3.1. Skin and Limb Lesion Scoring

The cumulative skin and limb lesion scores of pigs in the elevated platform rearing system (EP group) and the barren environment rearing system (CON group) during three observation periods (Day 1, Days 11–40, and Days 51–110) are shown in Figure 2. On Day 1 (57 days of age), there was no significant difference in the lesion scores of the skin and limbs between the EP and CON groups (p > 0.05). During the period of Days 11–44 and Days 51–110, the results of the t test showed that the pigs reared in the elevated platform system had significantly lower skin lesion scores than the CON pigs (p < 0.05). During all observation periods, the mean values of the limb lesion scores in the EP group were lower than those in the CON group. However, after the statistical analysis, there was no significant difference between the two groups (p > 0.05), which may be caused by the great difference of limb lesions among individuals within each group (Figure 2).

3.2. Behavior

The statistical results of the event and state behaviors are shown in Table 3. Within 48 h after the start of the experiment, the pigs raised in the elevated platform system showed less manipulating behavior (p = 0.043) and more playing behavior (p < 0.001) than the pigs in the CON group. Compared to the barren environment, the pigs spent more time standing (p = 0.007) and less time sitting and lying in elevated platform systems than in the barren environment system during the rearing period (Psitting = 0.005, Plying = 0.011). In addition, due to the existence of the elevated platform, the pigs in the EP group showed more exploring and playing behaviors (p < 0.001), while the manipulating and fighting behaviors against their peers were significantly reduced (p < 0.001). Similar to the rearing phase, the pigs in the EP group showed more standing (p = 0.010) and less sitting (p = 0.002) than the pigs in the CON group during the fattening period. The EP pigs also showed more playing behaviors (p < 0.001) and less manipulating and fighting behaviors than the CON pigs (p < 0.001).

3.3. Physiology Indexes

According to the analysis results of the serum physiological indexes of pigs (at 97 and 168 days of age), it can be seen that the elevated platform rearing system had a significant effect on the stress and immune levels of the pigs (Table 4). Compared to the CON group, the pigs in the EP group had a significantly lower serum cortisol concentration (p < 0.01) and a significantly higher serum C-reactive protein concentration (p < 0.001) in both the rearing and fattening periods. During the periods of rearing and fattening, the levels of TNF-α, IFN-γ, IL-1β, IL-2, and IL-6 in the EP pigs were significantly higher than those in the CON pigs (p < 0.001). However, the IL-10 level of the CON pigs was higher during the rearing period (p < 0.001), while that in the EP pigs was higher during the fattening period (p < 0.001). The IgA, IgG, and IgM levels of the EP pigs were significantly higher than those of the CON pigs in both the rearing and fattening periods (p < 0.01).

3.4. Growth Performance

Growth performance was based on the fact that there was no significant difference in the initial weight between two groups (Table 5). The final body weight of the EP group was significantly higher than that of the CON group at the end of the rearing (p = 0.020) and fattening periods (p = 0.010). However, there was no significant difference in the average daily gain and feed conversion ratio between the two groups during the rearing and fattening periods (p > 0.05).

3.5. Bone Sample Analysis

Table 6 shows the bone microstructural parameters of the bone trabecula region selected from the bone samples scanned by QCT. The results show that there are no significant differences in the bone volume fraction (BV/TV), bone mineral density (mg HA/cm3), trabecular separation (Tb.Sp), and trabecular thickness (Tb.Th) of the radius and tibia between the EP and CON groups at the end of rearing and fattening (p > 0.05). The results of the maximum bending force and deflection of the bone samples measured by the three-point bending test show that there are also no significant differences between the EP group and the CON group at the end of rearing and fattening (p > 0.05).

4. Discussion

4.1. Behavior

Behavior is an integral part of animal welfare and is the result of an animal successfully coping with its environment and exhibiting specific behaviors [22,23]. In this study, it was observed that the fattening pigs in the elevated platform rearing system showed less lying behavior and more standing behavior during the rearing and fattening periods, that is, the pigs in the EP group were more active than the pigs in the CON group, which is consistent with the results of previous studies [7,14]. Compared to the pigs in the EP group, the pigs in the CON group showed more lying behavior, which may indicate a lack of interest in a relatively barren environment. This study also found reduced sitting behavior in the pigs in the EP group, which the environmental enrichment within the EP group may influence. In studies on enriched environments, it was found that pigs exhibited less sitting behavior when enrichments were added to the enclosures [24]. However, Hill et al. found that enrichment had no significant effect on the overall duration of “lying” and “sitting” behaviors [25]. In their study, the pigs were only provided with toys as enrichment materials, while in our study, a more complex activity area was set up for pigs to explore; so, providing more activity areas for pigs may be a better choice for environmental enrichment.
Bulens et al. [7] found that the presence of platforms led to a reduced manipulating behavior of pigs towards their companions in the enclosures, and the present study results are consistent with their findings, as evidenced by a significant reduction in manipulating behavior towards their companions in the EP group throughout the fattening period. However, the platform may not be the only factor contributing to this. The study suggests that this could also be related to the addition of enrichment, such as bedding and toys in the EP group. Several studies have confirmed this conjecture, and Bolhuis et al. [26] found that pigs kept in barren environments showed more manipulating behavior than those in enriched environments.
Some studies have shown that enriched environments increase exploratory behavior in pigs; for example, Bolhuis et al. [26] found that pigs in enriched environments showed more nosing of the floor, scraping the floor, and chewing than pigs in poor environments; and Scott et al. [27] assessed exploratory behavior in pigs housed in straw bedding and found that pigs using straw bedding spent up to 20% of their time exploring the straw. In this study, like other toys (chains, toy balls, and chew toys), bedding was added to the pen as a kind of enriched material. Therefore, the exploring behavior included exploration directed at bedding. Similarly, we observed that the pigs in the elevated platform rearing system exhibited more frequent exploratory behavior than the pigs in the barren environment. There are also some researches that revealed that pigs reared in enriched environments (e.g., straw and more space) showed more playing behavior and expressed it earlier than pigs reared in poor environments [28,29]. The results of this study are consistent with previous work in that the elevated platform rearing system increased playing behavior in fattening pigs, where may be related to the addition of enrichments, such as thick bedding and toys, to the elevated platform rearing system.
Fighting behavior in pigs is a common and normal behavior driven primarily by forming social or dominance hierarchies. The highly combative nature may pose damaging challenges to the welfare of pigs. The present study found that fighting behavior was lower in the EP group than in the CON group at different stages, which is consistent with previous findings [7,14], that is, the presence of the platform reduced the frequency of fighting. Our study found that the provision of platforms increased the space for pigs to move around and may have reduced the number of conflicts among pigs. Differences in fighting behavior may also be related to environmental enrichment. Some studies have shown that an enriched environment effectively reduces aggressive behavior in pigs, such as hanging enrichment items or adding straw [30]. In addition, the environment enriched by adding straw and an enlarged space may stimulate the playing behavior and greatly reduce the tendency of pigs to express the aggressive behavior during food competition later in life [31]. Combined with the results of exploratory and playing behavior of the CON pigs in this study, we further hypothesized that the elevated platform system could reduce the incidence of fighting behavior in fattening pigs at different growth stages.

4.2. Body and Limb Lesion Scoring

Except for the first day of the experiment, the EP group had lower skin lesion scores than the CON group during the rearing and fattening periods, suggesting that the availability of the platform reduced the cumulative skin lesion score of pigs in the EP group. Other related studies have produced the same results, finding a significant difference in skin lesion scores between pigs raised in an elevated platform system and a barren environment during the nursing period [14]. In addition, the results may also have been affected by the straw bedding, not just by the elevated platform. However, the elevated platform reduced the skin lesion score during the fattening period, with more significant damage to ears, tails, and shoulders in pigs without elevated platform [7]. This study found significant differences in the skin lesion score between the groups on Days 11–31 and 41–101, possibly due to the enriched environment alleviating the social stress associated with the mixed group. Previous research demonstrates that pigs in rearing systems containing straw have significantly lower lesion scores than those kept in straw-free systems [32,33].
Damage to the limbs usually results in altered natural movement, often in the form of lameness, which is the leading cause of premature culling in pigs of all stages, often involving welfare and health issues [34]. This study found that the EP group had lower limb lesion scores than the CON group throughout the fattening period, which may be related to the addition of thick bedding to the pig house. Previous studies have found that the severity of hoof and limb injuries in fattening pigs is reduced on floors with straw bedding [35,36]. To date, no research has shown that the elevated platforms or ramps in pens increase the risk of injury. The results of Laves et al. showed that pigs raised in pens with an elevated platform had lower skin lesion scores [14].
This study also revealed that, as the pigs grew, the limb lesion score increased in both the EP and CON groups, which may have been caused by the fact that both barn floor compositions contained concrete floors. Previous studies have shown that concrete floors present a higher risk of bursitis and bone scabs on the limbs of fattening pigs compared to metal or plastic floors [37]. Also, this study found that the degree of limb damage was not stable in the fattening CON group, which the dirtier ground may have caused in the CON group. It has been shown that poor sanitation can cause hoof damage and that the presence of excessive urine and feces on the ground can weaken hoof hardness and increase hoof vulnerability [38]. Excess urine and feces may also increase the chance of slips and falls, leading to abrasions, bruises, and fractures to limbs and feet [39]. Although the results were not significantly different, the relatively lower limb lesion score of pigs in the EP group may indicate that the elevated platform rearing system is more conducive to limb health. However, the addition of straw bedding may also be a factor affecting limb lesions.

4.3. Physiology and Immunity

Cortisol (steroid hormone) is an indicator of psychological stress. When the organism is stressed or mentally threatened, the hypothalamic–pituitary–adrenal (HPA) axis is activated, and the adrenal glands release glucocorticoids (GCs), which accelerate the secretion of cortisol by the endocrine system [40]. This study found that serum cortisol concentrations were significantly lower in the EP group than in the CON group, suggesting that transport caused more significant stress to the pigs in the CON group. Because the pigs raised in the elevated platform system were very familiar with the use of the ramp, when the pigs were transported from the fattening pens to the trailer through ramps, the loading process caused less stress to the pigs [41,42]. Other studies have produced results consistent with the those of the present study, with pigs reared in barren conditions experiencing more pre-slaughter stress than those reared in enriched environments [43]. The increase in salivary cortisol after transport was more substantial in pigs reared in barren environments than in enriched environments [31,44].
Because the pigs in the control and EP groups were raised in different barns, we disinfected both barns regularly before and throughout the experiment to reduce the influence of pathogenic microorganisms on the different groups of pigs. Because the pigs in the two groups came from the same source, the feeding process of the experiment was also the same, which further controlled the influence of germ pressure. In this study, increased concentrations of TNF-α, IFN-γ, IL-1β, IL-2, and IL-6 and reduced IL-10 were detected in the serum of the pigs in the EP group after transport, indicating that pigs in the EP group had a greater immune response capacity and better immunomodulatory effects when experiencing acute stress. It was revealed that TNF-α, IL-1β, and IL-6, pro-inflammatory cytokines, are the first line of defense against infection in animals [45]. In contrast, the pigs in the CON group were in a barren environment during their lifetime. Chronic stress may have inhibited the immune system from generating an immune response, resulting in reduced responsiveness to these cytokines.
IgA, IgG, and IgM are common indicators of the magnitude of immunity. In this study, the serum IgA, IgG, and IgM levels in the EP pigs were significantly higher than those in the CON pigs at the end of the rearing and fattening periods. However, the cortisol levels in the CON pigs were significantly higher than those in the EP pigs, but TNF-α, IL-2, and IL-6 levels were significantly lower than those in the EP pigs after transport. This may be due to glucocorticoids negatively affecting the innate immune response, reducing the number of circulating monocytes and thereby reducing the pro-inflammatory cytokines IL-2, IL-6, TNF-α, and IL-12 [46]. Therefore, there may be immunosuppression in the CON pigs in this study, which leads to the lower levels of proinflammatory cytokines and immunoglobulins than those of the EP pigs. The research results of Ekkel et al. [47] revealed a high immunoglobulin response to intradermal injections of phytohemagglutinin in pigs in a ‘stress-free’ rearing system. In such systems, all possible sources of stress, such as mixing or temperature stress, are avoided. According to our results, the pigs in the EP group struggled to increase their humoral immunity levels when experiencing acute stress to cope and adapt to a stressful environment.
C-reactive protein (CRP) is a positive acute phase protein (APP) inflammatory marker in pigs [48,49], and elevated levels of positive APP are a reflection not only of inflammation and infection but also of psychological stress, such as transport and transfer [50,51]. In this study, serum C-reactive protein was higher in the EP group than in the CON group, which may also be caused by immunosuppression in the CON pigs [52]. C-reactive protein has an antibody-like regulatory function, and its increased concentration may help the body to resist infections caused by transport stress and reduce tissue damage. The short-term rise in inflammatory mediators, such as CRP, during the acute phase of stress is an adaptive response necessary to protect the body from pathogens [53]. Therefore, the elevated platform feeding system improved the immune response ability of pigs when exposed to acute stress.

4.4. Growth Performance and Bone Quality

This study showed no difference in the initial body weight between the EP and CON groups. In contrast, the body weight at the end of the rearing and fattening periods increased significantly in the EP group compared to the CON group, indicating that the elevated platform rearing system has a positive effect (facilitation) on the growth performance of pigs. Similar results have been obtained from studies of weaned piglets during the nursery period, with Laves et al. [14] showing that the pigs with an elevated platform gained more weight than the animals in the CON group. The positive effect of the elevated platform rearing system on daily weight gain is therefore evident not only for the nursery period but also for the fattening period. This result contradicts the results of other related studies, but it may be the result of differences in rearing practices and stocking densities. In previous studies, 20–60 kg and 30–125 kg fattening pigs were investigated, respectively, but no effect of the elevated platform on the average daily gain of pigs was found [7,11]. However, the pigs in Fraser’s study were not allowed to feed freely and the stocking density was 0.99 m2/per pig in Bulens et al.’s study [7,11]. Turner et al. [54] observed that daily weight gain tends to increase in pens with lower stocking densities. This study also found that the average daily gain and feed conversion ratio of fattening pigs in the EP group showed a tendency to outperform the high CON group, which may be related to the enriched environment in the EP and the barren environment in the CON group. The same results were also found in other studies: Beattie et al. [30] found that pigs in enriched environments had higher growth rates and higher average daily weight gains and that pigs in enriched environments had a lower feed conversion ratio than pigs in depleted environments because higher levels of stress adversely affected the feed conversion ratio [55].
Using QCT images is a valuable method for assessing the microstructure and quality of bones. The bone mineral density (BMD, g/cm3) represents the mass of minerals per unit volume of bone tissue and depends on the volume of the bone and the degree of mineralization within the bone [56]. Although the BMD was not statistically significant between the two groups in this study, the EP pigs had higher BMD values at the end of rearing and fattening periods than the CON group, which may be related to the exercise intensity, as the pigs in the EP group had free access to the climbing ramp. In a similar study, adult rats were tested by running on a treadmill and an increase in the BMD was observed in all four limbs [57]. Specific essential bone structural parameters, including BV/TV, Tb.Th, and Tb.Sp, are commonly used to analyze the microstructure of bone trabeculae [58]. The bone trabecular volume fraction [BV/TV (%)] represents the proportion of cancellous space and the volumetric aspects of trabecular bone [59]. It is commonly used to predict fracture risks and is closely related to bone strength and quality [60]. Jiang et al. [61] found that, for healthy growing bones, a rise in BV/TV is usually associated with a rise in BMD. The increase in Tb.Th observed during exercise is part of normal bone development [62]. However, we did not observe a difference in Tb.Th between the two groups throughout the fattening phase. Increases in Tb.Th and BV/TV are associated with a higher bone strength [60]. It is generally accepted that the significant decrease in Tb.Sp is associated with a concomitant increase in BV/TV and Tb.Th [63].
Bone strength and stiffness are closely related to the bone mineral content. In mouse-related studies, an 8-week exercise process increased the strength and toughness of the structure, suggesting that changes in bone tissue quality may increase fracture resistance independent of bone mass [64]. This study found that the maximum bending force and maximum winding of the porcine radius and tibia were numerically higher in the EP group than in the CON group, suggesting that the provision of exercise opportunities may lead to changes in tissue levels that increase mechanical strength. The mechanical properties of bone are closely related to its microstructure. Combined with the three-point bending test and QCT, bone strength can be effectively predicted [65]. Therefore, we need to investigate the effects of exercise on the bone structural parameters or bone strength of pigs in future studies.

5. Conclusions

Taken together, environmental enrichment in the elevated platform rearing system can increase weight gain and the expression of positive behaviors, and reduce negative behaviors and its damage to the organism in fattening pigs. Therefore, the elevated platform rearing system is a physical environment enrichment rearing system that provides an essential theoretical basis for improving pig health and animal welfare-type pig housing.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agriculture14060943/s1, Figure S1. The on-site photo of the elevated platform rearing system.

Author Contributions

Conceptualization, Y.Y., S.Z., W.J. and H.L.; methodology, Y.Y., S.Z., W.J. and H.L.; software, X.L.; validation, Y.Y., S.Z. and Q.F.; formal analysis, Y.Y., S.Z., W.J. and H.L.; investigation, Y.Y., S.Z. and X.L.; resources, H.L.; data curation, Y.Y., S.Z. and X.L.; writing—original draft preparation, Y.Y. and S.Z.; writing—review and editing, W.J. and H.L.; visualization, Y.Y. and S.Z.; supervision, X.Z.; project administration, W.J. and H.L.; funding acquisition, H.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Basic Research Support Program for Outstanding Young Teachers of Provincial Undergraduate Universities in Heilongjiang Province and Cooperative Innovation and Extension System for Heilongjiang Modern Agricultural Industry Technology of Pig, grant number YQTH2023182.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki and approved by the Institutional Review Board of Institutional Animal Care and Use Committee of Northeast Agriculture University (protocol code: IACUCNEAU20220601).

Data Availability Statement

None of the data were deposited in an official repository. The datasets used for the results presented in this study are available from the corresponding author upon reasonable request.

Acknowledgments

The authors would like to thank members of the Animal Behavior and Welfare Laboratory in the College of Animal Science and Technology.

Conflicts of Interest

None of the authors have any financial or personal relationships that could inappropriately influence or bias the content of the paper.

Abbreviations

ADGAverage daily gain
BBSBone breaking strength
BMDBone mineral density
BV/TVBone volume fraction
CONControl group
CORCortisol
CRPC-reactive protein
EPElevated platform rearing system group
FCRFeed conversion ratio
IFN-γInterferon-gamma
Ig-Immunoglobulin
IL-Interleukin
QCTQuantitative computed tomography
Tb.SpTrabecular separation
Tb.Thtrabecular thickness
TNF-αtumor necrosis factor

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Agriculture 14 00943 g001
Figure 1. The top view of pig houses of (a) the elevated platform rearing system and (b) the barren environment rearing system.
Figure 1. The top view of pig houses of (a) the elevated platform rearing system and (b) the barren environment rearing system.
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Figure 2. Effect of elevated platform pens on (a) skin lesions and (b) limb lesions in fattening pigs. * indicates significant differences between groups at p < 0.05; ** indicates p < 0.01.
Figure 2. Effect of elevated platform pens on (a) skin lesions and (b) limb lesions in fattening pigs. * indicates significant differences between groups at p < 0.05; ** indicates p < 0.01.
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Table 1. The scoring system used to assess skin and limb lesions [14,15].
Table 1. The scoring system used to assess skin and limb lesions [14,15].
ScoreDefinitions
Skin lesion
(head, shoulders, flanks, buttocks, and back)		0No injuries
1Less than 5 shallower injuries
25–10 shallower wounds or less than 5 deeper wounds
3More than 10 shallower wounds or more than 5 deeper wounds
Skin lesion
(ears and tails)		0No injuries
1Superficial injuries
2Obvious injuries or fresh bleeding wounds
Limb lesion0No injuries
1Superficial injury or slight limp
2More profound injuries or severe lameness
3Enlargement in one or more locations
Table 2. Behavioral categories and definitions [17,18,19,20,21].
Table 2. Behavioral categories and definitions [17,18,19,20,21].
Behavior Description
State behavior
LyingBody weight supported by the abdomen or sides
StandingBody weight is supported by four legs (including feeding, excreting, and walking)
SittingBody weight supported by hindquarters and front legs
Event behavior
ManipulatingGnawing, sucking, or chewing on the ears, tail, or other body parts of a companion in an enclosure in a continuous state
ExploringSmelling, sniffing, licking, and arching any part of the enclosure, including walls, floor, bedding, toys, troughs, and water spouts (except when in use)
FightingHead butting or biting another pig
PlayingRunning, jumping, rolling, and spinning with other pigs or alone, sometimes gently pushing their companions; biting toys with their muzzle and bobbing their heads, or dragging them (regardless of the body position)
Table 3. Behavioral differences between the elevated platform rearing system and the barren environment rearing system.
Table 3. Behavioral differences between the elevated platform rearing system and the barren environment rearing system.
BehaviorThe First 48 h The Rearing PeriodThe Fattening Period
EPCONp-ValueEPCONp-ValueEPCONp-Value
Standing, %46.75 ± 4.8233.71 ± 8.410.22746.17 ± 2.9332.39 ± 3.720.00737.38 ± 1.3730.69 ± 0.820.010
Sitting, %0.81 ± 0.140.85 ± 0.120.8271.17 ± 0.101.99 ± 0.240.0050.95 ± 0.062.31 ± 0.130.002
Lying, %52.44 ± 4.8365.44 ± 8.510.23252.67 ± 2.9765.61 ± 3.710.01161.67 ± 1.3966.99 ± 0.820.191
Manipulating9.50 ± 2.7217.25 ± 1.310.04312.56 ± 1.3824.38 ± 2.21<0.0019.56 ± 0.6422.79 ± 1.48<0.001
Exploring103.00 ± 36.8575.75 ± 15.220.52085.44 ± 6.7946.25 ± 5.70<0.00156.24 ± 5.3844.29 ± 3.570.069
Fighting7.00 ± 1.4713.75 ± 2.560.0625.63 ± 0.5611.50 ± 0.88<0.0015.47 ± 0.3310.21 ± 0.59<0.001
Playing36.00 ± 2.688.25 ± 1.31<0.00122.81 ± 2.517.81 ± 0.77<0.00125.97 ± 1.919.71 ± 0.53<0.001
Abbreviations: EP = Elevated platform rearing system group; CON = Control group. The results are expressed as “mean ± SEM”. The event behaviors were quantified as the number of occurrences (times/day) and state behaviors were quantified as percentages of the duration of the daily observation time (%).
Table 4. Effect of the elevated platform pens on the physiology and immunity of pigs.
Table 4. Effect of the elevated platform pens on the physiology and immunity of pigs.
ItemThe Rearing PeriodThe Fattening Periods
EPCONp-ValueEPCONp-Value
COR, nmol/L18.72 ± 0.3221.19 ± 0.410.00121.14 ± 0.1322.49 ± 0.380.008
CRP, μg/L2924.01 ± 26.122302.18 ± 25.08<0.001106.99 ± 1.2985.16 ± 0.88<0.001
TNF-α, pg/mL514.32 ± 4.37426.89 ± 2.65<0.0012700.34 ± 32.062305.59 ± 21.67<0.001
IFN-γ, pg/mL2873.76 ± 32.342509.04 ± 21.50<0.001459.57 ± 4.64425.56 ± 5.52<0.001
IL-1β, ng/mL55.79 ± 0.3141.61 ± 0.39<0.0012808.63 ± 24.442371.28 ± 22.46<0.001
IL-2, pg/mL626.32 ± 5.70481.09 ± 7.40<0.00148.79 ± 0.4641.18 ± 0.29<0.001
IL-6, ng/L1249.02 ± 13.371000.71 ± 15.19<0.001615.52 ± 3.21494.96 ± 4.96<0.001
IL-10, ng/L197.53 ± 2.88232.41 ± 2.79<0.0011151.14 ± 5.041044.39 ± 8.84<0.001
IgA, μg/L47.63 ± 0.3539.03 ± 0.94<0.00144.04 ± 0.2439.25 ± 0.53<0.001
IgG, μg/L403.96 ± 3.89370.20 ± 4.00<0.001452.75 ± 4.51398.83 ± 3.48<0.001
IgM, μg/L61.09 ± 0.3845.84 ± 1.62<0.00156.51 ± 1.0045.15 ± 0.59<0.001
Abbreviations: EP = Elevated platform rearing system group; CON = Control group; COR = Cortisol; CRP = C-reactive protein. The results are expressed as “mean ± SEM”.
Table 5. Effect of the elevated platform pens on the growth performance of pigs.
Table 5. Effect of the elevated platform pens on the growth performance of pigs.
ItemThe Rearing PeriodThe Fattening Period
EPCONp-ValueEPCONp-Value
Initial body weight (kg)20.86 ± 0.4620.09 ± 0.510.25941.30 ± 0.8539.66 ± 0.840.172
Final body weight (kg)42.61 ± 0.9039.77 ± 0.820.02099.14 ± 1.7293.35 ± 1.400.010
Average daily gain (kg)0.57 ± 0.020.52 ± 0.020.0520.85 ± 0.030.79 ± 0.020.070
Feed conversion ratio2.47 ± 0.142.72 ± 0.140.2692.66 ± 0.232.84 ± 0.170.575
Abbreviations: EP = Elevated platform rearing system group; CON = Control group. The results are expressed as “mean ± SEM”.
Table 6. Effect of the elevated platform rearing system on the bone microstructural parameters and bone strength of pigs.
Table 6. Effect of the elevated platform rearing system on the bone microstructural parameters and bone strength of pigs.
Experimental PeriodItemRadial BoneTibia Bone
EPCONp-ValueEPCONp-Value
Rearing periodBV/TV, %0.33 ± 0.040.31 ± 0.030.6500.35 ± 0.010.03 ± 0.040.603
BMD,
mg HA/cm3		525.24 ± 50.42446.56 ± 11.630.203484.25 ± 3.80456.14 ± 10.710.069
Tb.Sp, mm0.35 ± 0.030.37 ± 0.010.5590.40 ± 0.020.48 ± 0.050.215
Tb.Th, mm0.18 ± 0.010.17 ± 0.020.7000.23 ± 0.020.23 ± 0.0020.829
maximum bending force, N1640.73 ± 204.821546.66 ± 196.790.7572120.97 ± 131.792120.06 ± 260.960.998
maximum deflection, mm5.38 ± 0.495.27 ± 1.000.9257.41 ± 2.577.37 ± 1.640.991
Fattening periodBV/TV, %0.53 ± 0.040.40 ± 0.050.1230.34 ± 0.020.27 ± 0.080.445
BMD,
mg HA/cm3		533.06 ± 10.03520.24 ± 14.840.514455.59 ± 4.45455.08 ± 10.690.966
Tb.Sp, mm0.36 ± 0.030.43 ± 0.010.0840.44 ± 0.030.53 ± 0.080.372
Tb.Th, mm0.35 ± 0.020.25 ± 0.020.2000.26 ± 0.010.22 ± 0.030.254
maximum bending force, N4004.32 ± 465.703078.94 ± 607.120.2935344.63 ± 213.835092.80 ± 364.640.583
maximum deflection, mm7.84 ± 0.226.87 ± 1.210.5086.26 ± 0.715.84 ± 0.500.651
Abbreviations: EP = Elevated platform rearing system group; CON = Control group; BV/TV = Bone volume fraction; BMD = Bone mineral density; Tb.Sp = Trabecular separation; Tb.Th = Trabecular thickness. The results are expressed as “mean ± SEM”.
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Yang, Y.; Zhou, S.; Li, X.; Fu, Q.; Zhang, X.; Ji, W.; Liu, H. Effect of an Enriched Elevated Platform Rearing System on the Welfare and Bone Quality of Fattening Pigs. Agriculture 2024, 14, 943. https://doi.org/10.3390/agriculture14060943

AMA Style

Yang Y, Zhou S, Li X, Fu Q, Zhang X, Ji W, Liu H. Effect of an Enriched Elevated Platform Rearing System on the Welfare and Bone Quality of Fattening Pigs. Agriculture. 2024; 14(6):943. https://doi.org/10.3390/agriculture14060943

Chicago/Turabian Style

Yang, Yue, Sitong Zhou, Xin Li, Qin Fu, Xiaohong Zhang, Wenbo Ji, and Honggui Liu. 2024. "Effect of an Enriched Elevated Platform Rearing System on the Welfare and Bone Quality of Fattening Pigs" Agriculture 14, no. 6: 943. https://doi.org/10.3390/agriculture14060943

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