Impact of Thermal Manipulation of Broiler Eggs on Growth Performance, Splenic Inflammatory Cytokine Levels, and Heat Shock Protein Responses to Post-Hatch Lipopolysaccharide (LPS) Challenge
Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Experimental Design and Animal Management
2.2. Post-Hatch Rearing and Growth Performance Monitoring
2.3. LPS Challenge (Phase 2)
2.4. RNA Isolation and cDNA Synthesis
2.5. Relative-Quantitative Real-Time PCR (RT-qPCR)
2.6. Organ Weights
2.7. Statistical Analysis
2.8. Use and Potential Use of AI
3. Results
3.1. The Impact of TM on Hatchability Rate, Body Weight (BW), Body Temperature (Tb), Growth Performance Metrics, and Internal Organ Weight
3.2. Impact of TM and LPS Injection on Body Temperature (Tb) in Broiler Chickens
3.3. The Impact of TM and LPS Challenges on the mRNA Levels of Proinflammatory Cytokines (TNF-α, IL-1β, IL-2, IL-6, IL-12, and IFN-γ)
3.4. Impact of TM and LPS Challenge on mRNA Levels of Anti-Inflammatory Cytokines (IL-10 and TGF-β)
3.5. Impact of TM and LPS Challenge on the mRNA Levels of NF-κB and NF-κBp50 Transcription Factor
3.6. Impact of TM and LPS Challenge on Toll-like Receptors (TLRs) mRNA Levels (TLR 1, TLR 2, TLR 3, and TLR 4)
3.7. Impact of TM and LPS Challenge on mRNA Levels of Heat Shock Proteins and Heat Shock Factors (HSP70, HSP90, HSF-1, and HSF-3)
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
ADG | Average Daily Gain |
BW | Body Weight |
cDNA | Complementary DNA |
DFI | Daily Feed Intake |
DNA | Deoxyribonucleic Acid |
ED | Embryonic Day |
FCR | Feed Conversion Ratio |
GAPDH | Glyceraldehyde-3-Phosphate Dehydrogenase |
H&E | Hematoxylin and Eosin |
HSP | Heat Shock Protein |
HSP70 | 70-kDa Heat Shock Protein |
HSP90 | 90-kDa Heat Shock Protein |
HSF | Heat Shock Factor |
HSF-1 | Heat Shock Factor 1 |
HSF-3 | Heat Shock Factor 3 |
IFN-γ | Interferon Gamma |
IL | Interleukin |
IL-1β | Interleukin 1 Beta |
IL-2 | Interleukin 2 |
IL-6 | Interleukin 6 |
IL-10 | Interleukin 10 |
IL-12 | Interleukin 12 |
IP | Intraperitoneal |
LPS | Lipopolysaccharide |
mRNA | Messenger Ribonucleic Acid |
NF-κB | Nuclear Factor Kappa B |
NF-κBp50 | Nuclear Factor Kappa B p50 Subunit |
RH | Relative Humidity |
RNA | Ribonucleic Acid |
RT-qPCR | Real-Time Quantitative Polymerase Chain Reaction |
SD | Standard Deviation |
Tb | Body Temperature |
TGF-β | Transforming Growth Factor Beta |
TM | Thermal Manipulation |
TLR | Toll-Like Receptor |
TNF-α | Tumor Necrosis Factor Alpha |
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Ingredients (%) | Starter (d1–24) | Grower (d25–35) |
---|---|---|
Corn | 60.20 | 62.0 |
Soybean Meal (CP 40%) | 34.30 | 31.50 |
Concentrate | 3.20 | 2.70 |
Vegetable Oil | 1.00 | 2.50 |
Limestone | 1.10 | 1.10 |
Vitamin and mineral premix * | 0.20 | 0.20 |
Total | 100.00 | 100.00 |
Nutrient Composition (Calculated) ** | ||
Metabolizable energy, kcal/kg | 3110 | 3155 |
Crude Protein (%) | 22.52 | 21.53 |
Lysine (%) | 1.51 | 1.32 |
Methionine (%) | 0.55 | 0.51 |
Calcium | 1.08 | 1.0 |
Available Phosphorus | 0.49 | 0.44 |
The Gene | Sequence (5′–3′) | TM (°C) |
---|---|---|
β-Actin | F: ACCGCAAATGCTTCTAAACC R: ATAAAGCCATGCCAATCTCG | 60 |
GAPDH | F: TTGTCTCCTGTGACTTCAATGGTG R: ACGGTTGCTGTATCCAAACTCAT | 60 |
TNF-α | F: GACAGCCTATGCCAACAAGTA R: TTACAGGAAGGGCAACTCATC | 60 |
IL-1 β | F: CCCGCCTTCCGCTACA R: CACGAAGCACTTCTGGTTGATG | 60 |
IL-2 | F: GAGAGCATCCGGATAGTGAAT R: TGTGGAGGCTTTGCATAAGAG | 60 |
IL-6 | F: AAATCCCTCCTCGCCAATCT R: CCCTCACGGTCTTCTCCATAAA | 60 |
IL-12 | F: CTGTGGCTCGCACTGATAAA R: CAATGACCTCCAGGAACATCTC | 60 |
IFN-γ | F: ACCTTCCTGATGGCGTGAAG R: GCGCTGGATTCTCAAGTCGT | 60 |
IL-10 | F: CAGCAATCCAGAGACGATGAA R: AGTGGACTTGCACTGGAATAG | 60 |
TGF-β | F: GGGTGTCCCATACCATTTAGAG R: CCCTTTAACGCAGAGGGATT | 60 |
NF-κB | F: GATGTGGAGACAGACAGCTAAC R: CATAAGACGCACCACACTGA | 60 |
NF-κB p50 | F: CACAGCTGGAGGGAAGTAAAT R: TTGAGTAAGGAAGTGAGGTTGAG | 60 |
TLR 1 | F: AGTCCATCTTTGTGTTGTCGCC R: ATTGGCTCCAGCAAGATCAGG | 60 |
TLR 2 | F: GATTGTGGACAACATCATTGACTC R: AGAGCTGCTTTCAAGTTTTCCC | 60 |
TLR 3 | F: TCAGTACATTTGTAACACCCCGCC R: GGCGTCATAATCAAACACTCC | 60 |
TLR 4 | F: AGTCTGAAATTGCTGAGCTCAAAT R: GCGACGTTAAGCCATGGAAG | 60 |
HSP 70 | F: CGGGCAAGTTTGACCTAA R: TTGGCTCCCACCCTATCTCT | 60 |
HSP 90 | F: TCCTGTCCTGGCTTTAGTTT R: AGGTGGCATCTCCTCGGT | 60 |
HSF 1 | F: CAGGGAAGCAGTTGGTTCACTACACG R: CCTTGGGTTTGGGTTGCTCAGTC | 60 |
HSF 3 | F: GAGTTCCAGCACCCTTTCTT R: TCTTTCCACAGGGCCTTATTT | 60 |
Parameter | CON | TM | p-Value |
---|---|---|---|
True hatchability % 1 | 93.03 ± 0.541 a | 93.71 ± 1.092 a | 0.633 |
Unfertilized eggs % 2 | 4.36 ± 0.316 a | 1.72 ± 0.015 b | 0.014 |
Hatch time (h) | 496.9 ± 5.3 a | 488.3 ± 4.2 b | 0.040 |
Embryonic death % 3 | 2.61 ± 0.857 a | 3.72 ± 0.828 a | 0.451 |
Hatchability of fertile % 4 | 97.27 ±0.888 a | 95.35 ± 1.126 a | 0.311 |
Chick Abnormalities % 5 (at hatching) | 0.94 ± 0.313 a | 3.36 ± 1.519 a | 0.259 |
Item | Group | Day 7 | Day 14 | Day 21 | Day 28 | Day 35 | Overall (Day 1–35) |
---|---|---|---|---|---|---|---|
BW | CON | 182 ± 2.13 a | 511.04 ± 4.07 a | 1126.25 ± 10.91 a | 1911.01 ± 18.64 a | 2729.29 ± 38.11 a | 2729.29 ± 38.11 a |
TM | 183.33 ± 1.4 a | 481.33 ± 5.60 b | 1048.75 ± 11.65 b | 1764.68 ± 15.71 b | 2519.51 ± 32.81 b | 2519.51 ± 32.81 b | |
ADFI | CON | 25.22 ± 0.18 a | 59.29 ± 1.14 a | 116.39 ± 1.37 a | 170.58 ± 1.56 a | 207.55 ± 2.70 a | 115.81 ± 0.88 a |
TM | 23.13 ± 0.26 b | 54.67 ± 1.23 b | 105.84 ± 1.46 b | 152.66 ± 1.92 b | 168.53 ± 3.89 b | 100.96 ± 0.90 b | |
ADG | CON | 20.34 ± 0.32 a | 47 ± 0.49 a | 87.89 ± 1.57 a | 112.11 ± 2.44 a | 116.83 ± 5.29 a | 76.85 ± 1.09 a |
TM | 20.52 ± 0.30 a | 42.57 ± 0.85 b | 81.06 ± 1.20 b | 102.28 ± 1.99 b | 107.49 ± 5.07 a | 70.85 ± 0.96 b | |
FCR | CON | 0.97 ± 0.01 a | 1.26 ± 0.03 a | 1.33 ± 0.02 a | 1.53 ± 0.03 a | 1.85 ± 0.12 a | 1.51 ± 0.02 a |
TM | 0.88 ± 0.01 b | 1.29 ± 0.03 a | 1.31 ± 0.02 a | 1.50 ± 0.03 a | 1.59 ± 0.08 a | 1.40 ± 0.02 b |
Organ/Tissue | CON | TM | p-Value |
---|---|---|---|
Liver | 0.345 | ||
Absolute weight (g) | 59.77 ± 2.87 a | 51.90 ± 2.52 a | |
Relative weight | 2.19 ± 0.105 a | 2.06 ± 0.10 a | |
Spleen | 0.561 | ||
Absolute weight | 3.55 ± 0.38 a | 3.02 ± 0.23 a | |
Relative weight | 0.13 ± 0.014 a | 0.12 ± 0.009 a | |
heart | 0.001 | ||
Absolute weight | 13.73 ± 0.55 | 9.47 ± 0.66 | |
Relative weight | 0.503 ± 0.020 a | 0.376 ± 0.026 b | |
Small Intestine | <0.0001 | ||
Absolute weight | 76.96 ± 5.05 a | 39.30 ± 2.60 b | |
Relative weight | 2.82 ± 0.185 a | 1.56 ± 0.103 b | |
Large Intestine | 0.053 | ||
Absolute weight | 21.83 ± 2.46 a | 14.87 ± 1.01 a | |
Relative weight | 0.80 ± 0.09 a | 0.59 ± 0.04 a | |
digestive System | <0.0001 | ||
Absolute weight | 265.82 ± 9.83 a | 173.34 ± 11.34 a | |
Relative weight | 9.74 ± 0.36 a | 6.88 ± 0.45 b | |
Gizzard weight | 0.0042 | ||
Absolute weight | 45.58 ± 1.45 a | 32.25 ± 2.67 b | |
Relative weight | 1.67 ± 0.053 a | 1.28 ± 0.106 b | |
proventriculus | <0.001 | ||
Absolute weight | 9.28 ± 0.49 a | 5.80 ± 0.43 b | |
Relative weight | 0.34 ± 0.018 a | 0.23 ± 0.017 b | |
gallbladder | 0.644 | ||
Absolute weight | 0.79 ± 0.08 a | 0.78 ± 0.08 a | |
Relative weight | 0.029 ± 0.003 a | 0.031 ± 0003 a | |
Small Intestine length (mm) | 202.0 ± 7.66 a | 161.0 ± 5.39 b | <0.001 |
Large intestine length (mm) | 27.50 ± 1.73 a | 2.052 ± 6.21 a | 0.287 |
Before LPS Injection | (°C) | CON-Saline | Control-LPS | TM-Saline | TM-LPS |
40.36 ± 0.32 | 40.55 ± 0.11 a | 40.79 ± 0.18 | 40.80 ± 0.22 | ||
1 h After LPS injection | (°C) | CON-Saline | Control-LPS | TM-Saline | TM-LPS |
40.19 ± 0.25 | 40.19 ± 0.14 b | 40.60 ± 0.15 | 40.34 ± 0.36 | ||
3 h After LPS injection | (°C) | CON-Saline | Control-LPS | TM-Saline | TM-LPS |
40.43 ± 0.18 | 40.33 ± 0.17 | 40.68 ± 0.20 | 40.86 ± 0.17 | ||
6 h After LPS injection | (°C) | CON-Saline | Control-LPS | TM-Saline | TM-LPS |
40.40 ± 0.27 | 40.59 ± 0.17 | 40.85 ± 0.29 | 40.61 ± 0.20 |
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Al-Zghoul, M.B.; Hundam, S.; Mayyas, M.; Gerrard, D.E.; Dalloul, R.A. Impact of Thermal Manipulation of Broiler Eggs on Growth Performance, Splenic Inflammatory Cytokine Levels, and Heat Shock Protein Responses to Post-Hatch Lipopolysaccharide (LPS) Challenge. Animals 2025, 15, 1736. https://doi.org/10.3390/ani15121736
Al-Zghoul MB, Hundam S, Mayyas M, Gerrard DE, Dalloul RA. Impact of Thermal Manipulation of Broiler Eggs on Growth Performance, Splenic Inflammatory Cytokine Levels, and Heat Shock Protein Responses to Post-Hatch Lipopolysaccharide (LPS) Challenge. Animals. 2025; 15(12):1736. https://doi.org/10.3390/ani15121736
Chicago/Turabian StyleAl-Zghoul, Mohammad Borhan, Seif Hundam, Mohammad Mayyas, David E. Gerrard, and Rami A. Dalloul. 2025. "Impact of Thermal Manipulation of Broiler Eggs on Growth Performance, Splenic Inflammatory Cytokine Levels, and Heat Shock Protein Responses to Post-Hatch Lipopolysaccharide (LPS) Challenge" Animals 15, no. 12: 1736. https://doi.org/10.3390/ani15121736
APA StyleAl-Zghoul, M. B., Hundam, S., Mayyas, M., Gerrard, D. E., & Dalloul, R. A. (2025). Impact of Thermal Manipulation of Broiler Eggs on Growth Performance, Splenic Inflammatory Cytokine Levels, and Heat Shock Protein Responses to Post-Hatch Lipopolysaccharide (LPS) Challenge. Animals, 15(12), 1736. https://doi.org/10.3390/ani15121736