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    Topic review

    Resilience in Growing Pigs

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    Submitted by: Houda Laghouaouta

    Definition

    Resilience can be defined as the ability of the animal to rapidly recover its productivity despite the perturbations that might occur during its productive life.

    1. Introduction 

    Selective breeding for improved resilience would provide resistant animals with robust phenotypes [1]. Thus, it would increase the profitability and the sustainability of the production systems. However, there is no straightforward quantification method for resilience. Resilience indicators have been elaborated based on productivity-related traits [2][3][4][5] and immune phenotypes [6][7] in several livestock species. In this review, a total of 445 commercial Duroc pigs were challenged with an attenuated Aujeszky vaccine at 12 weeks of age (experimental group) and 95 pigs were inoculated with phosphate-buffered saline (control group). The deviation from the expected body weight given the growth curve of control pigs (∆BW) and the increment of the acute-phase protein haptoglobin (∆HP) at 4 days post-vaccination (DPV) were suggested as resilience indicators in growing pigs. Challenged pigs that maintained their productivity and had a minor activation of the acute-phase protein haptoglobin were deemed resilient, whereas pigs that had low ∆BW values and high activation of haptoglobin were deemed susceptible. Pigs were also classified based on ∆BW relative to the expected body weight (BW) at 28 DPV (%BW) and ∆HP relative to the basal level of haptoglobin (%HP).  

    2. Descriptive Statistics for the Novel Resilience Indicators

    Descriptive statistics for the suggested resilience indicators are given in Table 1. Average ∆BW and %BW were −0.68 kg and −1.42%, respectively, indicating that on average, the observed BW of challenged pigs at 28 DPV was lower than the expected BW given the theoretical growth curve. Average ∆HP and %HP were +0.03 mg/mL and +5.40%, respectively, showing an increment of haptoglobin concentration in plasma at 4 DPV. All the resilience indicators had high standard deviation values.
    Table 1. Descriptive statistics for the resilience indicators in pigs from the experimental group.
    Trait Mean SD 1 Min Max
    ∆BW 2 (kg) −0.68 3.64 −13.2 +10.1
    %BW 3 (%) −1.42 7.26 −24.4 +19.3
    ∆HP 4 (mg/mL) +0.03 0.70 −1.41 +2.65
    %HP 5 (%) +5.40 60.4 −89.2 +292

    1 Standard deviation; 2 Body weight deviation from the expected growth curve of control pigs at 28 days post-vaccination (DPV); 3 Ratio between ∆BW and the expected body weight at 28 DPV given the growth curve of control pigs; 4 Haptoglobin increment at 4 DPV; 5 Ratio between ∆HP and the basal level of haptoglobin.

    Phenotypic correlations between the resilience indicators are reported in Table 2. A negative and low correlation was reported between ∆BW and ∆HP (r = −0.09, p < 0.05), suggesting that they capture different aspects of resilience.

    Table 2. Correlations between the resilience indicators.
    Trait ∆BW 1 ∆HP 2 %BW 3 %HP 4
    ∆BW 1 −0.09 * 0.99 *** −0.14 **
    ∆HP   1 −0.09 ns 0.94 ***
    %BW     1 −0.14 **
    %HP       1

    1 Body weight deviation from the expected growth curve of non-vaccinated pigs at 28 days post-vaccination (DPV); 2 Haptoglobin increment at 4 DPV; 3 Ratio between ∆BW and the expected body weight at 28 DPV given the growth curve of control pigs. 4 Ratio between ∆HP and the basal level of haptoglobin; 5 * p < 0.05; ** p < 0.01; *** p < 0.001; ns non-significant.

    3. Classification of Pigs’ Resilience

    Pigs were classified based on the resilience indicated by both the deviation from the expected growth curve and the increment of haptoglobin at 4 DPV. First, individuals were grouped into resilient or susceptible groups based on ∆BW and ∆HP (Figure 1). On average, the resilient pigs (N = 25) showed positive values of ∆BW (+3.54 kg) and %BW (+6.60%) and negative values of ∆HP (−0.71 mg/mL) and %HP (−61.2%). In contrast, the susceptible group (N = 33) had low and negative values of ∆BW (−6.00 kg) and %BW (−11.7%) and positive values of ∆HP (+1.17 mg/mL) and %HP (+108%) (Table 3).Thus, ∆BW and ∆HP allowed us to separate two groups with extreme responses to challenge. 
    Figure 1. Classification of pigs as resilient, average, and susceptible based on the first (Q1) and the third (Q3) quartiles of ∆BW and ∆HP. ∆BW: body weight deviation from the expected growth curve of control pigs at 28 days post-vaccination, ∆HP: haptoglobin increment at 4 days post-vaccination.
    Table 3. Mean and standard deviation (SD) of the resilience indicators of pigs from the resilient (R, N = 25) and susceptible (S, N = 33) groups.
    Trait Group Mean SD
    ∆BW 1 (kg) R +3.54 1.42
    S −6.00 2.44
    %BW 2 (%) R +6.60 2.81
    S −11.7 5.13
    ∆HP 3 (mg/mL) R −0.71 0.18
    S +1.17 0.61
    %HP 4 (%) R −61.2 18.9
    S +108.4 68.2

    1 Body weight deviation from the expected growth curve of control pigs at 28 days post-vaccination (DPV); 2 Ratio between ∆BW and the expected body weight at 28 DPV given the growth curve of control pigs; 3 Haptoglobin increment at 4 DPV; 4 Ratio between ∆HP and the basal level of haptoglobin.

    Pigs were also grouped into resilient and susceptible groups based on the resilience indicated by %BW and %HP (Figure 2). Individuals were colored according to their group classification using ∆BW and ∆HP in order to visualize the concordance between the first and the second classifications. The concordance was high with a kappa value of 0.8 and an overall agreement of 95%, indicating that ∆BW and ∆HP are not sensitive to the animal's expected BW nor the basal level of haptoglobin and are consequently potential indicators of resilience.
    Pigs were also classified into resilient, average, and susceptible based on the observed BW at 28 DPV (Figure S1) and the combination of the BW deviation from the expected BW at 28 DPV estimated based on each pig’s average daily gain before challenge (∆BWADG) and ∆HP (Figure S2). The concordance was low (kappa = 0.1) between the classification obtained by the observed BW at 28 DPV and the combination of “∆BW and ∆HP” indicating that ∆BW and ∆HP do not only capture the differences in the observed BW. The concordance was moderate (kappa = 0.5) between the classification indicated by “∆BWADG and ∆HP” and “∆BW and ∆HP”. Thus, pigs could be consistently classified as resilient, average or susceptible based on ∆BWADG and ∆HP without using a control group.
    Figure 2. Projection of the resilient, average, and susceptible groups obtained with the first (Q1) and third (Q3) quartiles of ∆BW and ∆HP on the plane defined by %HP and %BW. Individuals were colored according to their group classification using the criterion from Figure 1 to visualize concordance between both methods. ∆BW: body weight deviation from the expected growth curve of control pigs at 28 days post-vaccination (DPV), ∆HP: haptoglobin increment at 4 DPV, %BW: ratio between ∆BW and the expected body weight at 28 DPV, %HP: ratio between ∆HP and the basal level of haptoglobin.
    The growth curves of animals from the resilient and susceptible groups were similar at the beginning of the experiment (Figure 3). After the challenge at 12 weeks of age, resilient animals were able to withstand the perturbations and showed faster growth than susceptible ones. At the end of the fattening period (30 weeks of age), the resilient pigs showed a greater carcass weight than susceptible ones (107.7 and 92.1 kg, respectively).
    Figure 3. Growth curves of pigs from the resilient and susceptible groups. The grey band represents the confidence interval. Individuals were colored according to their group classification using the criterion from Figure 1.

    4. Heritability Estimates

    The features of the marginal posterior distributions of the heritability estimates for the resilience indicators are displayed in Table 4. Both ∆BW and %BW had a moderate heritability of 0.33 and 0.37, with P0.10 (i.e. the probability of the heritability being greater than 0.10) of 0.94 and 0.93, respectively. Heritability estimates of ∆HP and %HP were 0.16 and 0.13, with P0.10 of 0.66 and 0.53, respectively. Heritabilities for ∆BW at 28 DPV have not been reported before but our estimated value is similar to the heritability of BW reported in Duroc pigs at 180 days of age (0.31) [8]. Our heritability estimates for haptoglobin are within the range of those reported in the literature [9][10]. The experimental sample size limits the accuracy of the heritability estimates. However, P0.10 showed that the resilience indicators are genetically controlled and consequently, may be improved through selective breeding
    Table 4. Heritability estimates for the resilience indicators.
    Trait Mean 1 P0.10 2 HPD95% 3
    ∆BW 4 0.33 0.94 0.02–0.65
    %BW 5 0.37 0.93 0.02–0.74
    ∆HP 6 0.16 0.66 0.00–0.38
    %HP 7 0.13 0.53 0.00–0.32

    1 Mean of the marginal posterior distribution of the heritability; 2 Probability of the heritability estimate being greater than 0.10; 3 Highest posterior density interval at 95% of probability; 4 Body weight deviation from the expected growth curve of non-vaccinated pigs at 28 days post-vaccination (DPV); 5 Ratio between ∆BW and the expected body weight at 28 DPV given the growth curve of control pigs; 6 Haptoglobin increment at 4 DPV; 7 Ratio between ∆HP and the basal level of haptoglobin.

    5. Conclusions

    Altogether, we propose ∆BW and ∆HP as novel resilience indicators in growing pigs. The suggested indicators are easy to measure, genetically controlled and show substantial variability between animals. Thus, they may be improved through selective breeding. This approach may be applied to quantify resilience in other species using different infectious and non-infectious challenges. Moreover, genomic studies on resilient and susceptible animals can help in elucidating the molecular basis of the resilient response. 

    This entry is adapted from 10.3390/ani11102970

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