High Granulocyte-Macrophage Colony Stimulating Factor to Interleukin 10 Ratio and Marked Antioxidant Enzyme Activities Predominate in Symptomatic Cattle Naturally Infected with Candidatus Mycoplasma haemobos, Theileria orientalis, Theileria sinensis and Trypanosoma evansi
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Ethics Statement
2.2. Animals and Blood Sample Collection
2.3. DNA Extraction
2.4. Detection of Blood Parasites by Conventional PCR
2.5. Quantification of Serum Inflammatory Cytokines in Cattle
2.6. Oxidant and Antioxidant Assays
2.7. Statistical Analysis
3. Results
3.1. Molecular Detection Rate of Blood Parasites in the Symptomatic and Asymptomatic Cattle
3.2. Serum Proinflammatory, Antiinflammatory Cytokine and Oxidant/Antioxidant Levels in Symptomatic and Asymptomatic Cattle
3.2.1. Serum Cytokine and Oxidant/Antioxidant Levels in Symptomatic and Asymptomatic Cattle Naturally Infected with Candidatus Mycoplasma haemobos
3.2.2. Serum Cytokine Levels and Oxidant/Antioxidant Levels in Symptomatic and Asymptomatic Cattle Naturally Infected by Theileria orientalis
3.2.3. Serum Cytokine and Oxidant/Antioxidant Levels in Symptomatic and Asymptomatic Cattle Naturally Infected with Anaplasma marginale
3.2.4. Serum Cytokine Levels in Symptomatic and Asymptomatic Cattle Naturally Infected with Theileria sinensis
3.2.5. Serum Cytokine and Oxidant/Antioxidant Levels in Symptomatic Cattle Naturally Infected with Trypanosoma evansi
3.2.6. Serum Cytokine Levels and Oxidant/Antioxidant Levels in Symptomatic Cattle Naturally Infected with Anaplasma platys
3.3. Pro-Inflammatory and Anti-Inflammatory Cytokine Ratios in Symptomatic and Asymptomatic Cattle Naturally Infected with Blood Parasites
3.3.1. Candidatus Mycoplasma haemobos-Infected Cattle
3.3.2. Theileria orientalis-Infected Cattle
3.3.3. Anaplasma marginale-Infected Cattle
3.3.4. Theileria sinensis-Infected Cattle
3.3.5. Trypanosoma evansi-Infected Cattle
3.3.6. Anaplasma platys-Infected Cattle
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Blood Parasites | Gene of Interest | Primer Sequences (5′–3′) Forward (F) and Reverse (R) | Thermocycling Conditions | Base Pair (bp) | References |
---|---|---|---|---|---|
T. sinensis | MPSP | F-CACTGCTATGTTGTCCAAGAGATATT R- AATGCGCCTAAAGATAGTAGAAAAC | ID: 94 °C/3 min D: 94 °C/1 min A: 56 °C/1 min E: 72 °C/1 min No. of cycles:40 FE: 72 °C/7 min | 887 | [28] |
A. marginale | MSP4 | F- CATCTCCCATGAGTCACGAAGTGGC R- GCTGAACAGGAATCTTGCTCCAAG | ID: 95 °C/5 min D: 95 °C/1 min A: 65 °C/2 min E: 72 °C/1 min No. of cycles:40 FE: 72 °C/10 min | 761 | [29] |
T. orientalis | MPSP | F- CTTTGCCTAGGATACTTCCT R -ACGGCAAGTGGTGAGAACT | ID: 94 °C/4 min D: 94 °C/1 min A: 63 °C/1 min E: 72 °C/1 min No. of cycles:40 FE: 72 °C/7 min | 776 | [30] |
T. evansi | RoTaT 1.2 VSG | F- 5′-GCGGGGTGTTTAAAGCAATA-3′ R- 5′-ATTAGTGCTGCGTGTGTTCG-3′ | ID: 94 °C/4 min D: 94 °C/1 min A: 59 °C/1 min E: 72 °C/1 min No. of cycles:40 FE: 72 °C/5 min | 208 | [31] |
Candidatus Mycoplasma haemobos | 16 SrRNA | F- GAGTTAGTTATTAAAGCTTTAT R- ATTCATGAGGTACTATCAGTTG | ID: 94 °C/5 min D: 94 °C/30 s A: 55 °C/30 s E: 72 °C/30 s No. of cycles:40 FE: 72 °C/7 min | 279 | [32] |
A. platys | 16SrRNA | PLATYS F- AAGTCGAACGGATTTTTGTC PLATYS R -CTTTAACTTACCGAACC | ID: 95 °C/5 min D: 95 °C/30 s A: 55 °C/30 s E: 72 °C/90 s No. of cycles:40 FE: 72 °C/5 min | 504 | [33] |
Blood Parasites | No. of Cattle | Occurrence (%) (95% Confidence Interval) |
---|---|---|
Candidatus Mycoplasma haemobos | 70 | 53.9 (45.3–62.2) |
Theileria orientalis | 65 | 50 (41.5–58.5) |
Anaplasma marginale | 49 | 37.8 (29.8–46.3) |
Theileria sinensis | 32 | 24.6 (18.0–32.3) |
Trypanosoma evansi | 4 | 3.08 (1.20–7.64) |
Anaplasma platys | 7 | 5.38 (2.63–10.7) |
Proinflammatory/ Anti-Inflammatory Cytokines | C. Mycoplasma haemobos Infected Cattle (Symptomatic) (n = 3) | C. Mycoplasma haemobos Infected Cattle (Asymptomatic) (n = 12) | Clinically Healthy Cattle (n = 8) |
---|---|---|---|
Interleukin 12 (ng/L) | 4.11 ± 0.05 b | 5.71 ± 1.19 c | 2.36 ± 0.08 a |
Interleukin 10 (ng/L) | 40.78 ± 3.87 b | 50.45 ± 3.27 b | 19.53 ± 0.43 a |
GM-CSF (pg/mL) | 745.73 ± 3.02 b | 717.75 ± 2.81 b | 81.68 ± 1.26 a |
Interleukin 4 (ng/L) | 864.70 ± 13.36 c | 795.64 ± 12.74 b | 349.85 ± 3.05 a |
Interferon-γ (pg/mL) | 163.18 ± 1.05 a | 184.50 ± 5.26 b | 167.42 ± 4.38 a |
Oxidant/antioxidant Markers | |||
Malondialdehyde (nM/mL) | 3.70 ± 1.60 c | 2.51 ± 0.16 b | 1.37 ± 0.02 a |
Superoxide dismutase (U/mL) | 945.36 ± 4.87 b | 977.16 ± 9.72 b | 546.6 ± 4.64 a |
Glutathione peroxidase (U/mL) | 138.24 ± 2.10 b | 138.63 ± 1.59 b | 54.40 ± 0.45 a |
Proinflammatory/ Anti-Inflammatory Cytokines | T. orientalis Infected Cattle (Symptomatic) (n = 4) | T. orientalis Infected Cattle (Asymptomatic) (n = 9) | Clinically Healthy Cattle (n = 8) |
---|---|---|---|
Interleukin 12 (ng/L) | 5.83 ± 0.53 b | 5.20 ± 0.24 b | 2.36 ± 0.08 a |
Interleukin 10 (ng/L) | 45.87 ± 5.16 b | 38.60 ± 2.41 b | 19.53 ± 0.43 a |
GM-CSF (pg/mL) | 454.55 ± 8.74 b | 473.88 ± 8.97 b | 81.68 ± 1.26 a |
Interleukin 4 (ng/L) | 689.50 ± 10.34 b | 705.15 ± 11.64 b | 349.85 ± 3.05 a |
Interferon-γ (pg/mL) | 276.97 ± 16.35 b | 261.15 ± 10.87 b | 167.42 ± 4.38 a |
Oxidant/antioxidant markers | |||
Malondialdehyde (nM/mL) | 3.97 ± 0.93 b | 3.01 ± 0.45 b | 1.37 ± 0.02 a |
Superoxide dismutase (U/mL) | 854.31 ± 20.83 b | 921.80 ± 21.77 b | 546.6 ± 4.64 a |
Glutathione peroxidase (U/mL) | 188.83 ± 6.64 b | 186.00 ± 3.97 b | 54.40 ± 0.45 a |
Proinflammatory/ Anti-Inflammatory Cytokines | Anaplasma marginale Infected Cattle (Symptomatic) (n = 3) | Anaplasma marginale Infected Cattle (Asymptomatic) (n = 3) | Clinically Healthy Cattle (n = 8) |
---|---|---|---|
Interleukin 12 (ng/L) | 20.03 ± 1.80 b | 37.35 ± 1.12 c | 2.36 ± 0.08 a |
Interleukin 10 (ng/L) | 39.50 ± 3.18 a | 342.53 ± 12.41 b | 19.53 ± 0.43 a |
GM-CSF (pg/mL) | 515.62 ± 12.41 b | 517.80 ± 19.76 b | 81.68 ± 1.26 a |
Interleukin 4 (ng/L) | 749.66 ± 9.66 b | 964.86 ± 4.35 b | 349.85 ± 3.05 a |
Interferon-γ (pg/mL) | 291.96 ± 29.48 b | 373.91 ± 28.045 c | 167.42 ± 4.38 a |
Oxidant/Antioxidant Markers | |||
Malondialdehyde (nM/mL) | 3.88 ± 1.81 b | 2.18 ± 0.05 a | 1.37 ± 0.02 a |
Superoxide dismutase (U/mL) | 1236.33 ± 10.88 b | 932.99 ± 17.24 b | 546.6 ± 4.64 a |
Glutathione peroxidase (U/mL) | 145.20 ± 1.12 b | 277.74 ± 9.49 c | 54.40 ± 0.45 a |
Proinflammatory/ Anti-Inflammatory Cytokines | Theileria sinensis Infected Cattle (Symptomatic) (n = 3) | Theileria sinensis Infected Cattle (Asymptomatic) (n = 3) | Clinically Healthy Cattle (n = 8) |
---|---|---|---|
Interleukin 12 (ng/L) | 17.88 ± 3.35 b | 3.50 ± 0.66 a | 2.36 ± 0.08 a |
Interleukin 10 (ng/L) | 52.36 ± 1.60 c | 40.92 ± 1.71 b | 19.53 ± 0.43 a |
GM-CSF (pg/mL) | 340.63 ± 15.24 b | 318.09 ± 12.77 b | 81.68 ± 1.26 a |
Interleukin 4 (ng/L) | 965.24 ± 17.29 c | 686.64 ± 6.41 b | 349.85 ± 3.05 a |
Interferon-γ (pg/mL) | 352.90 ± 14.50 b | 256.05 ± 12.94 ab | 167.42 ± 4.38 a |
Oxidant/antioxidant markers | |||
Malondialdehyde (nM/mL) | 5.10 ± 0.05 b | 4.00 ± 1.51 b | 1.37 ± 0.02 a |
Superoxide dismutase (U/mL) | 969.90 ± 5.69 c | 937.66 ± 13.03 b | 546.6 ± 4.64 a |
Glutathione peroxidase (U/mL) | 242.53 ± 12.82 b | 235.91 ± 6.34 b | 54.40 ± 0.45 a |
Proinflammatory/ Anti-Inflammatory Cytokines | T. evansi Infected Cattle (Symptomatic) (n = 4) | Clinically Healthy Cattle (n = 8) |
---|---|---|
Interleukin 12 (ng/L) * | 8.96 ± 0.53 | 2.36 ± 0.08 |
Interleukin 10 (ng/L) * | 71.00 ± 1.83 | 19.53 ± 0.43 |
GM-CSF (pg/mL) * | 555.42 ± 20.7 | 81.68 ± 1.26 |
Interleukin 4 (ng/L) * | 770.41 ± 14.82 | 349.85 ± 3.05 |
Interferon-γ (pg/mL) * | 277.02 ± 5.41 | 167.42 ± 4.38 |
Oxidant/Antioxidant Markers | ||
Malondialdehyde (nM/mL) * | 13.73 ± 0.15 | 1.37 ± 0.02 |
Superoxide dismutase (U/mL) * | 1162.76 ± 19.01 | 546.6 ± 4.64 |
Glutathione peroxidase (U/mL) * | 128.51 ± 2.10 | 54.40 ± 0.45 |
Proinflammatory/ Anti-Inflammatory Cytokines | Anaplasma platys Infected Cattle (Symptomatic) (n = 3) | Clinically Healthy Cattle (n = 8) |
---|---|---|
Interleukin 12 (ng/L) * | 58.60 ± 0.07 | 2.36 ± 0.08 |
Interleukin 10 (ng/L) * | 665.04 ± 5.05 | 19.53 ± 0.43 |
GM-CSF (pg/mL) * | 422.28 ± 10.93 | 81.68 ± 1.26 |
Interleukin 4 (ng/L) * | 1279.33 ± 20.12 | 349.85 ± 3.05 |
Interferon-γ (pg/mL) * | 350.12 ± 4.26 | 167.42 ± 4.38 |
Oxidant/Antioxidant Markers | ||
Malondialdehyde (nM/mL) * | 5.84 ± 0.15 | 1.37 ± 0.02 |
Superoxide dismutase (U/mL) * | 1561.46 ± 15.74 | 546.6 ± 4.64 |
Glutathione peroxidase (U/mL) * | 343.14 ± 14.09 | 54.40 ± 0.45 |
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Agina, O.A.; Cheah, K.T.; Sayuti, N.S.A.; Shaari, M.R.; Isa, N.M.M.; Ajat, M.; Zamri-Saad, M.; Mazlan, M.; Hamzah, H. High Granulocyte-Macrophage Colony Stimulating Factor to Interleukin 10 Ratio and Marked Antioxidant Enzyme Activities Predominate in Symptomatic Cattle Naturally Infected with Candidatus Mycoplasma haemobos, Theileria orientalis, Theileria sinensis and Trypanosoma evansi. Animals 2021, 11, 2235. https://doi.org/10.3390/ani11082235
Agina OA, Cheah KT, Sayuti NSA, Shaari MR, Isa NMM, Ajat M, Zamri-Saad M, Mazlan M, Hamzah H. High Granulocyte-Macrophage Colony Stimulating Factor to Interleukin 10 Ratio and Marked Antioxidant Enzyme Activities Predominate in Symptomatic Cattle Naturally Infected with Candidatus Mycoplasma haemobos, Theileria orientalis, Theileria sinensis and Trypanosoma evansi. Animals. 2021; 11(8):2235. https://doi.org/10.3390/ani11082235
Chicago/Turabian StyleAgina, Onyinyechukwu Ada, Kim Tho Cheah, Nurul Syahirah Ahmad Sayuti, Mohd Rosly Shaari, Nur Mahiza Md Isa, Mokrish Ajat, Mohd Zamri-Saad, Mazlina Mazlan, and Hazilawati Hamzah. 2021. "High Granulocyte-Macrophage Colony Stimulating Factor to Interleukin 10 Ratio and Marked Antioxidant Enzyme Activities Predominate in Symptomatic Cattle Naturally Infected with Candidatus Mycoplasma haemobos, Theileria orientalis, Theileria sinensis and Trypanosoma evansi" Animals 11, no. 8: 2235. https://doi.org/10.3390/ani11082235