The Combined Effect of Weaning Stress and Immune Activation during Pig Gestation on Serum Cytokine and Analyte Concentrations
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Chemistry Analysis
2.2. Cytokine and Cortisol Analysis
2.3. Statistical Modeling and Testing
3. Results
3.1. Effect of Maternal Immune Activation, Weaning and Sex on Serum Chemistry and Cortisol Levels
3.2. Effect of Maternal Immune Activation, Weaning and Sex on Serum Immune Parameter Levels
3.3. Discriminant Analysis of the Effects of Maternal Immune Activation, Weaning and Sex on Serum Chemistry and Immune Parameters
4. Discussion
4.1. Maternal Immune Activation, Weaning and Sex Effects on Serum Chemistry and Cortisol Levels
4.2. Maternal Immune Activation, Weaning and Sex Effects on Serum Immune Parameter Levels
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Analyte 1 | Maternal Immune Activation | Sex | Weaning | Activation-Sex | Activation-Weaning | Weaning-Sex | Activation-Weaning-Sex |
---|---|---|---|---|---|---|---|
AG Ratio | 0.053 | 0.609 | 0.666 | 0.355 | 0.040 | 0.801 | 0.175 |
Albumin a | 0.553 | 0.810 | 0.169 | 0.335 | 0.223 | 0.757 | 0.059 |
AlkPhos b | 0.110 | 0.397 | 0.804 | 0.808 | 0.214 | 0.657 | 0.599 |
AnionGap c | 0.075 | 0.573 | 0.011 | 0.151 | 0.962 | 0.393 | 0.027 |
AST b | 0.094 | 0.542 | 0.282 | 0.492 | 0.112 | 0.707 | 0.651 |
Bicarbonate c | 0.136 | 0.885 | 0.083 | 0.634 | 0.433 | 0.711 | 0.045 |
Bilirubin d | 0.548 | 0.514 | 0.011 | 0.361 | 0.246 | 0.433 | 0.018 |
BUN d | 0.216 | 0.566 | 0.072 | 0.377 | 0.022 | 0.431 | 0.082 |
Calcium d | 0.033 | 0.195 | 0.016 | 0.425 | 0.514 | 0.562 | 0.060 |
Chloride c | 0.020 | 0.820 | 0.084 | 0.899 | 0.936 | 0.533 | 0.028 |
Cholesterol d | 0.040 | 0.159 | 0.602 | 0.307 | 0.102 | 0.937 | 0.020 |
CPK b | 0.034 | 0.988 | 0.230 | 0.037 | 0.151 | 0.795 | 0.082 |
Creatinine d | 0.019 | 0.827 | 0.102 | 0.215 | 0.726 | 0.791 | 0.018 |
GGT b | 0.897 | 0.830 | 0.015 | 0.415 | 0.665 | 0.490 | 0.257 |
GLDH b | 0.547 | 0.444 | 0.697 | 0.707 | 0.521 | 0.363 | 0.254 |
Globulin e | 0.025 | 0.211 | 0.227 | 0.329 | 0.334 | 0.486 | 0.080 |
Glucose d | 0.869 | 0.388 | 0.002 | 0.412 | 0.289 | 0.830 | 0.277 |
NaK Ratio | 0.131 | 0.437 | 0.151 | 0.268 | 0.835 | 0.112 | 0.522 |
Phosphorus d | 0.811 | 0.308 | 0.159 | 0.821 | 0.737 | 0.473 | 0.065 |
Potassium c | 0.332 | 0.052 | 0.215 | 0.280 | 0.922 | 0.148 | 0.036 |
Protein a | 0.045 | 0.556 | 0.170 | 0.289 | 0.804 | 0.948 | 0.028 |
Sodium c | 0.028 | 0.626 | 0.416 | 0.723 | 0.948 | 0.483 | 0.061 |
Triglycerides d | 0.197 | 0.705 | 0.004 | 0.707 | 0.777 | 0.283 | 0.085 |
Cortisol e | 0.627 | 0.201 | 0.010 | 0.146 | 0.261 | 0.048 | 0.048 |
BodyWeight f | 0.857 | 0.439 | 0.057 | 0.097 | 0.341 | 0.942 | 0.224 |
Analyte 1 | Control Female | PRRSV Female | Control Male | PRRSV Male | Control | PRRSV | Female | Male |
---|---|---|---|---|---|---|---|---|
AG Ratio | 0.594 | 0.620 | 0.099 | 0.126 | 0.126 | 0.148 | 0.716 | 0.982 |
Albumin | 0.013 | 0.720 | 0.065 | 0.847 | 0.008 | 0.530 | 0.071 | 0.178 |
AlkPhos | 0.632 | 0.387 | 0.631 | 0.490 | 0.457 | 0.330 | 0.799 | 0.911 |
Anion Gap | 0.026 | 0.107 | 0.214 | 0.080 | 0.058 | 0.034 | 0.023 | 0.090 |
AST | 0.384 | 0.892 | 0.786 | 0.542 | 0.339 | 0.197 | 0.824 | 0.204 |
Bicarbonate | 0.055 | 0.104 | 0.048 | 0.161 | 0.007 | 0.042 | 0.013 | 0.020 |
Bilirubin | 0.053 | 0.284 | 0.027 | 0.870 | 0.897 | 0.039 | 0.077 | 0.673 |
BUN | 0.008 | 0.473 | 0.176 | 0.570 | 0.009 | 0.407 | 0.202 | 0.871 |
Calcium | 0.168 | 0.150 | 0.035 | 0.020 | 0.271 | 0.003 | 0.041 | 0.145 |
Chloride | 0.372 | 0.092 | 0.031 | 0.107 | 0.011 | 0.008 | 0.015 | 0.005 |
Cholesterol | 0.437 | 0.487 | 0.346 | 0.651 | 0.139 | 0.455 | 0.274 | 0.221 |
CPK | 0.065 | 0.682 | 0.385 | 0.888 | 0.059 | 0.763 | 0.375 | 0.564 |
Creatinine | 0.045 | 0.110 | 0.143 | 0.044 | 0.139 | 0.093 | 0.113 | 0.117 |
GGT | 0.276 | 0.554 | 0.093 | 0.063 | 0.052 | 0.064 | 0.158 | 0.021 |
GLDH | 0.610 | 0.141 | 0.709 | 0.759 | 0.662 | 0.222 | 0.169 | 0.839 |
Globulin | 0.276 | 0.328 | 0.550 | 0.090 | 0.881 | 0.140 | 0.166 | 0.594 |
Glucose | 0.753 | 0.109 | 0.835 | 0.235 | 0.950 | 0.337 | 0.361 | 0.299 |
NaK Ratio | 0.453 | 0.745 | 0.258 | 0.348 | 0.798 | 0.974 | 0.408 | 0.069 |
Phosphorus | 0.013 | 0.137 | 0.013 | 0.035 | 0.002 | 0.309 | 0.124 | 0.086 |
Potassium | 0.515 | 0.969 | 0.064 | 0.191 | 0.502 | 0.292 | 0.822 | 0.027 |
Protein | 0.075 | 0.034 | 0.459 | 0.084 | 0.264 | 0.433 | 0.316 | 0.369 |
Sodium | 0.123 | 0.065 | 0.021 | 0.056 | 0.270 | 0.227 | 0.241 | 0.558 |
Triglycerides | 0.012 | 0.144 | 0.300 | 0.359 | 0.011 | 0.086 | 0.006 | 0.168 |
Cortisol | 0.006 | 0.097 | 0.174 | 0.958 | 0.002 | 0.149 | 0.003 | 0.321 |
Body Weight | 0.273 | 0.093 | 0.237 | 0.137 | 0.619 | 0.069 | 0.201 | 0.251 |
Analyte 1 | Female Nursed | Female Weaned | Male Nursed | Male Weaned | Nursed | Weaned | Male | Female |
---|---|---|---|---|---|---|---|---|
AG Ratio | 0.105 | 0.031 | 0.640 | 0.022 | 0.246 | 0.017 | 0.119 | 0.039 |
Albumin | 0.941 | 0.224 | 0.451 | 0.447 | 0.898 | 0.266 | 0.999 | 0.324 |
AlkPhos | 0.180 | 0.407 | 0.221 | 0.144 | 0.136 | 0.336 | 0.073 | 0.127 |
Anion Gap | 0.887 | 0.224 | 0.021 | 0.091 | 0.146 | 0.154 | 0.038 | 0.424 |
AST | 0.457 | 0.717 | 0.486 | 0.163 | 0.362 | 0.095 | 0.502 | 0.693 |
Bicarbonate | 0.442 | 0.097 | 0.125 | 0.075 | 0.186 | 0.063 | 0.073 | 0.160 |
Bilirubin | 0.615 | 0.206 | 0.381 | 0.148 | 0.289 | 0.634 | 0.195 | 0.704 |
BUN | 0.071 | 0.903 | 0.232 | 0.845 | 0.079 | 0.842 | 0.480 | 0.209 |
Calcium | 0.484 | 0.435 | 0.162 | 0.250 | 0.109 | 0.187 | 0.233 | 0.123 |
Chloride | 0.035 | 0.241 | 0.213 | 0.082 | 0.052 | 0.049 | 0.006 | 0.137 |
Cholesterol | 0.300 | 0.675 | 0.086 | 0.716 | 0.044 | 0.323 | 0.624 | 0.196 |
CPK | 0.088 | 0.005 | 0.930 | 0.539 | 0.312 | 0.012 | 0.578 | 0.005 |
Creatinine | 0.521 | 0.706 | 0.028 | 0.221 | 0.062 | 0.180 | 0.012 | 0.450 |
GGT | 0.781 | 0.466 | 0.754 | 0.708 | 0.407 | 0.706 | 0.308 | 0.861 |
GLDH | 0.847 | 0.348 | 0.979 | 0.510 | 0.898 | 0.267 | 0.723 | 0.447 |
Globulin | 0.028 | 0.022 | 0.262 | 0.017 | 0.076 | 0.016 | 0.057 | 0.017 |
Glucose | 0.222 | 0.073 | 0.391 | 0.751 | 0.403 | 0.191 | 0.672 | 0.476 |
NaK Ratio | 0.796 | 0.999 | 0.208 | 0.259 | 0.504 | 0.565 | 0.095 | 0.942 |
Phosphorus | 0.505 | 0.555 | 0.285 | 0.840 | 0.648 | 0.322 | 0.525 | 0.586 |
Potassium | 0.673 | 0.695 | 0.201 | 0.126 | 0.567 | 0.417 | 0.132 | 0.973 |
Protein | 0.071 | 0.028 | 0.064 | 0.019 | 0.167 | 0.296 | 0.054 | 0.640 |
Sodium | 0.153 | 0.229 | 0.281 | 0.090 | 0.145 | 0.098 | 0.029 | 0.063 |
Triglycerides | 0.152 | 0.377 | 0.387 | 0.394 | 0.130 | 0.247 | 0.256 | 0.126 |
Cortisol | 0.787 | 0.360 | 0.138 | 0.983 | 0.436 | 0.461 | 0.329 | 0.422 |
Body Weight | 0.781 | 0.755 | 0.990 | 0.261 | 0.321 | 0.968 | 0.908 | 0.114 |
Analyte 1 | Con Fem Nur | Con Fem Wea | Con Mal Nur | Con Mal Wea | PRR Fem Nur | PRR Fem Wea | PRR Mal Nur | PRR Mal Wea | SE 3 |
---|---|---|---|---|---|---|---|---|---|
AG Ratio 2 | 0.55 ab | 0.60 ab | 0.49 bc | 0.65 a | 0.26 d | 0.19 d | 0.41 c | 0.22 d | 0.07 |
Albumin 4 | 1.05 | 1.16 | 1.04 | 1.13 | 1.06 | 1.08 | 1.09 | 1.08 | 0.04 |
AlkPhos 5 | 6.73 | 6.78 | 6.84 | 6.79 | 6.51 | 6.64 | 6.65 | 6.56 | 0.07 |
Anion Gap 6 | 2.81 abc | 2.96 ef | 2.89 def | 2.94 ef | 2.80 ab | 2.88 cde | 2.76 a | 2.84 bcd | 0.04 |
AST 5 | 3.61 | 3.94 | 3.43 | 3.50 | 3.84 | 3.81 | 3.73 | 4.02 | 0.27 |
Bicarbonate 6 | 3.17 bc | 3.08 a | 3.15 b | 3.09 a | 3.22 c | 3.17 bc | 3.22 c | 3.18 bc | 0.03 |
Bilirubin 7 | −0.96 ab | 0.23 d | −1.02 ab | 0.07 d | −1.14 a | −0.51 c | −0.70 c | −0.80 abc | 0.22 |
BUN 7 | 1.90 a | 2.19 bc | 1.92 ab | 2.07 abc | 2.33 c | 2.22 c | 2.20 c | 2.12 abc | 0.14 |
Calcium 7 | 2.39 de | 2.34 bcd | 2.43 e | 2.33 abc | 2.37 cd | 2.31 ab | 2.37 cd | 2.28 a | 0.03 |
Chloride 6 | 4.62 cd | 4.63 cd | 4.61 bc | 4.64 d | 4.59 a | 4.62 cd | 4.60 ab | 4.62 cd | 0.01 |
Cholesterol 7 | 5.56 d | 5.44 cd | 5.30 bc | 5.14 ab | 5.39 cd | 5.51 cd | 5.01 a | 5.08 ab | 0.12 |
CPK 5 | 6.42 c | 6.89 d | 6.27 bc | 6.50 c | 5.94 ab | 5.80 a | 6.25 bc | 6.29 bc | 0.18 |
Creatinine 7 | −0.51 ab | −0.37 ab | −0.46 ab | −0.36 b | −0.56 ab | −0.40 ab | −0.65 a | −0.46 ab | 0.15 |
GGT 5 | 3.65 | 3.79 | 3.63 | 3.80 | 3.61 | 3.69 | 3.66 | 3.84 | 0.08 |
GLDH 5 | 0.70 | 0.57 | 0.45 | 0.49 | 0.65 | 0.38 | 0.46 | 0.38 | 0.18 |
Globulin 7 | 0.47 a | 0.55 a | 0.51 a | 0.46 a | 0.81 c | 0.92 c | 0.67 b | 0.84 c | 0.06 |
Glucose 6 | 4.75 | 4.82 | 4.87 | 4.83 | 5.13 | 4.67 | 5.12 | 4.80 | 0.12 |
NaK Ratio | 3.49 | 3.54 | 3.56 | 3.51 | 3.51 | 3.54 | 3.50 | 3.47 | 0.04 |
Phosphorus 6 | 2.26 | 2.33 | 2.22 | 2.29 | 2.23 | 2.31 | 2.17 | 2.29 | 0.02 |
Potassium 5 | 1.42 cd | 1.37 ab | 1.35 a | 1.40 bc | 1.39 abc | 1.39 abc | 1.41 bc | 1.45 d | 0.02 |
Protein 4 | 1.53 a | 1.58 ab | 1.52 a | 1.54 a | 1.64 bcd | 1.71 d | 1.63 bc | 1.69 cd | 0.04 |
Sodium 5 | 4.92 | 4.94 | 4.92 | 4.94 | 4.90 | 4.93 | 4.90 | 4.93 | 0.01 |
Triglycerides 6 | 3.92 a | 4.56 cd | 4.13 ab | 4.40 bc | 4.36 bc | 4.84 d | 4.39 bc | 4.66 cd | 0.20 |
Cortisol 8 | 3.20 a | 3.90 d | 3.32 ab | 3.58 bc | 3.15 a | 3.61 bcd | 3.56 bc | 3.57 bc | 0.16 |
Body Weight 9 | 6.35 | 5.89 | 5.86 | 6.13 | 5.69 | 6.31 | 5.45 | 5.92 | 0.25 |
Cytokine | Maternal Immune Activation | Sex | Weaning | Activation-Sex | Activation-Weaning | Sex-Weaning | Activation-Weaning-Sex |
---|---|---|---|---|---|---|---|
GM-CSF 1 | 0.512 | 0.400 | 0.759 | 0.136 | 0.217 | 0.702 | 0.679 |
IFN-γ | 0.407 | 0.025 | 0.164 | 0.551 | 0.055 | 0.533 | 0.434 |
IL-1α | 0.463 | 0.021 | 0.513 | 0.096 | 0.119 | 0.132 | 0.419 |
IL-1β | 0.490 | 0.050 | 0.440 | 0.330 | 0.019 | 0.071 | 0.290 |
IL-1ra | 0.505 | 0.707 | 0.369 | 0.791 | 0.085 | 0.408 | 0.725 |
IL-4 | 0.511 | 0.047 | 0.275 | 0.201 | 0.022 | 0.084 | 0.339 |
IL-2 | 0.642 | 0.052 | 0.398 | 0.195 | 0.019 | 0.067 | 0.337 |
IL-6 | 0.911 | 0.079 | 0.604 | 0.503 | 0.019 | 0.122 | 0.411 |
IL-10 | 0.494 | 0.038 | 0.398 | 0.147 | 0.047 | 0.068 | 0.285 |
IL-12 | 0.481 | 0.890 | 0.497 | 0.273 | 0.144 | 0.138 | 0.161 |
IL-18 | 0.452 | 0.035 | 0.370 | 0.209 | 0.022 | 0.084 | 0.315 |
TNF-α | 0.799 | 0.157 | 0.423 | 0.500 | 0.120 | 0.777 | 0.950 |
Analyte 1 | Con Fem Nur 2 | Con Fem Wea | Con Mal Nur | Con Mal Wea | PRR Fem Nur | PRR Fem Wea | PRR Mal Nur | PRR Mal Wea | SE 3 |
---|---|---|---|---|---|---|---|---|---|
GM-CSF | 0.19 | 0.15 | 0.16 | 0.12 | 0.15 | 0.18 | 0.22 | 0.32 | 0.08 |
IFN-γ | 57.12 | 38.29 | 47.31 | 30.25 | 60.00 | 70.78 | 52.67 | 47.80 | 10.33 |
IL-1α | 0.25 | 0.20 | 0.25 | 0.19 | 0.29 | 0.44 | 0.24 | 0.23 | 0.06 |
IL-1β | 1.05 a | 0.94 a | 1.02 a | 0.68 a | 0.99 a | 1.86 b | 1.00 a | 1.03 a | 0.25 |
IL-1ra | 1.32 | 1.27 | 1.30 | 1.13 | 0.78 | 1.28 | 0.92 | 1.10 | 0.28 |
IL-2 | 1.44 a | 1.34 a | 1.47 a | 0.97 a | 1.40 a | 2.90 b | 1.30 a | 1.45 a | 0.40 |
IL-4 | 6.31 a | 5.55 a | 6.63 a | 3.66 a | 5.23 a | 12.57 b | 4.80 a | 5.29 a | 1.90 |
IL-6 | 0.52 ab | 0.44 a | 0.5 ab | 0.33 a | 0.33 a | 0.67 b | 0.33 a | 0.36 a | 0.11 |
IL-10 | 2.47 a | 2.32 a | 2.54 a | 1.74 a | 2.59 a | 4.96 b | 2.40 a | 2.34 a | 0.66 |
IL-12 | 0.80 | 0.69 | 0.74 | 0.62 | 0.69 | 0.89 | 0.90 | 0.78 | 0.10 |
IL18 | 4.65 a | 4.22 a | 4.59 a | 3.19 a | 4.70 a | 8.54 b | 4.40 a | 4.65 a | 1.07 |
TNF-α | 0.65 | 0.53 | 0.55 | 0.39 | 0.47 | 0.53 | 0.44 | 0.47 | 0.12 |
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Rymut, H.E.; Rund, L.A.; Bolt, C.R.; Villamil, M.B.; Southey, B.R.; Johnson, R.W.; Rodriguez-Zas, S.L. The Combined Effect of Weaning Stress and Immune Activation during Pig Gestation on Serum Cytokine and Analyte Concentrations. Animals 2021, 11, 2274. https://doi.org/10.3390/ani11082274
Rymut HE, Rund LA, Bolt CR, Villamil MB, Southey BR, Johnson RW, Rodriguez-Zas SL. The Combined Effect of Weaning Stress and Immune Activation during Pig Gestation on Serum Cytokine and Analyte Concentrations. Animals. 2021; 11(8):2274. https://doi.org/10.3390/ani11082274
Chicago/Turabian StyleRymut, Haley E., Laurie A. Rund, Courtni R. Bolt, Maria B. Villamil, Bruce R. Southey, Rodney W. Johnson, and Sandra L. Rodriguez-Zas. 2021. "The Combined Effect of Weaning Stress and Immune Activation during Pig Gestation on Serum Cytokine and Analyte Concentrations" Animals 11, no. 8: 2274. https://doi.org/10.3390/ani11082274
APA StyleRymut, H. E., Rund, L. A., Bolt, C. R., Villamil, M. B., Southey, B. R., Johnson, R. W., & Rodriguez-Zas, S. L. (2021). The Combined Effect of Weaning Stress and Immune Activation during Pig Gestation on Serum Cytokine and Analyte Concentrations. Animals, 11(8), 2274. https://doi.org/10.3390/ani11082274