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Dietary vegetable oils inclusion on the performance, hormonal levels and hsp 70 gene expression in broilers under heat stress

ABSTRACT.

The aim of the present study was to compare the effects of unsaturated and saturated oils on the performance, hormonal levels and hsp gene expression in broiler chickens exposed to heat stress. 300 one-day male broiler chicks were assigned to 4 treatments (Diets containing palm, corn, linseed or olive oils) with 5 replicates. At day 28 of age, 2 chickens were removed from each replicate, then blood samples and liver tissue samples were collected for analyses. Feeding linseed and olive oil reduced feed conversion ratio compared to corn and palm oils. The lowest level of insulin was for chickens fed linseed oil and corn oil. The highest level of corticosterone was found in chickens fed palm oil and the lowest level was for those received linseed oil. Chickens received linseed and corn oils had the highest levels of T3 and T4 and those fed palm and olive oils had the lowest levels. The highest HSP 70 gene expression was for chickens fed diet containing olive and linseed oils and the lowest one was for those fed corn and palm oils. It was concluded that olive oil and linseed oil could improve performance and heat tolerance of chickens under heat stress.

Keywords:
corticosterone; insulin; heat shock protein; heat tolerance

Introduction

Vegetable oils are used in the industrial broiler diets as supplementary energy source and an important source of essential fatty acids (Leeson, Diaz, Gonzalo, & Summers, 1995Leeson, S., Diaz, G., Gonzalo, J., & Summers, J. D. (1995). Poultry metabolic disorders and mycotoxins. Guelph, ON: University Books.). In addition, lipids have lower heat increment than carbohydrates (Musharaf & Latshaw, 1999Musharaf, N. A., & Latshaw, J. D. (1999). Heat increment as affected by protein and amino acid nutrition. World's Poultry Science Journal, 55(3), 233-240. doi: 10.1079/WPS19990017
https://doi.org/10.1079/WPS19990017...
), therefore a part of energy of carbohydrate in broiler rations substituted with energy of lipids during heat stress period (Syafwan, Kwakkel, & Verstegen, 2011Syafwan, S., Kwakkel, R. P., & Verstegen, M. W. A. (2011). Heat stress and feeding strategies in meat-type chickens. World's Poultry Science Journal, 67(4), 653-674. doi: 10.1017/S0043933911000742.
https://doi.org/10.1017/S004393391100074...
).

Some studies speculated that inclusion of vegetable oils in broiler diets could enhance the performance (Ailhaud et al., 2006Ailhaud, G., Massiera, F., Weill, P., Legrand, P., Alessandri, J.-M., & Guesnet, P. (2006). Temporal changes in dietary fats: role of n− 6 polyunsaturated fatty acids in excessive adipose tissue development and relationship to obesity. Progress in Lipid Research, 45(3), 203-236. doi: 10.1016/j.plipres.2006.01.003
https://doi.org/10.1016/j.plipres.2006.0...
; He, Yang, & Guo, 2007He, X., Yang, X., & Guo, Y. (2007). Effects of different dietary oil sources on immune function in cyclophosphamide immunosuppressed chickens. Animal Feed Science and Technology, 139(3-4), 186-200. doi: 10.1016/j.anifeedsci.2007.01.0.09
https://doi.org/10.1016/j.anifeedsci.200...
), increase the function of immune system and antibody titer production (Sadeghi, Mirmohseni, Shawrang, & Aminafshar, 2013Sadeghi, A. A., Mirmohseni, M., Shawrang, P., & Aminafshar, M. (2013). The effect of soy oil addition to the diet of broiler chicks on the immune response. Turkish Journal of Veterinary and Animal Sciences, 37(3), 264-270. ) and improve the health status (Moslehi, Sadeghi, Shawrang, & Aminafshar, 2016Moslehi, A., Sadeghi, A. A., Shawrang, P., & Aminafshar, M. (2016). Blood lipid components and SREBP-1 gene expression in broiler chickens fed different dietary lipid sources. Acta Scientiae Veterinariae, 44, 1-9. ) in normal and heat stress conditions. In contrast, some reports (Sijben, De Groot, Nieuwland, Schrama, & Parmentier, 2000Sijben, J. W. C., De Groot, H., Nieuwland, M. G. B., Schrama, J. W., & Parmentier, H. K. (2000). Dietary linoleic acid divergently affects immune responsiveness of growing layer hens. Poultry Science, 79(8), 1106-1115. doi: 10.1093/ps/79.8.1106.
https://doi.org/10.1093/ps/79.8.1106....
) rejected mentioned benefits.

During heat stress period, activation of some genes like heat shock protein 70 is important for heat resistance (Raghebian, Sadeghi, & Aminafshar, 2017Raghebian, M., Sadeghi, A. A., & Aminafshar, M. (2017). Impact of dietary energy density on the liver health of broilers exposed to heat stress and their performance during finisher period. Journal of Livestock Science, 8, 122-130. ; Taleb, Sadeghi, Shawrang, Chamani, & Aminafshar, 2017Taleb, Z., Sadeghi, A. A., Shawrang, P., Chamani, M., & Aminafshar, M. (2017). Effect of energy levels and sources on the blood attributes and immune response in broiler chickens exposed to heat stress. Journal of Livestock Science, 8, 52-58. ). An interesting study showed that heat stress could up regulate the hepatic expression of heat shock protein in broilers. Also reported that heat stress induced the hepatic lipogenesis in chickens and they mentioned that this effect probably mediated by heat shock protein (Flees et al., 2017Flees, J., Rajaei-Sharifabadi, H., Greene, E., Beer, L., Hargis, B. M., Ellestad, L., ... Dridi, S. (2017). Effect of Morinda citrifolia (noni)-enriched diet on hepatic heat shock protein and lipid metabolism-related genes in heat stressed broiler chickens. Frontiers in Physiology, 8, 919. doi: 10.3389/fphys.2017.0.0919
https://doi.org/10.3389/fphys.2017.0.091...
). In the literature there was no information concerning the effects of dietary oils inclusion on heat shock proteins and blood lipid attributes. A study speculated that dietary lipid supplementation could improve the heat tolerance in broiler chickens and also performance in heat-stressed broiler chickens (Zulkifli, Liew, Israf, Omar, & Hair-Bejo, 2003Zulkifli, I., Liew, P. K., Israf, D. A., Omar, A. R., & Hair-Bejo, M. (2003). Effects of early age feed restriction and heat conditioning on heterophil/lymphocyte ratios, heat shock protein 70 expression and body temperature of heat-stressed broiler chickens. Journal of Thermal Biology, 28(3), 217-222. doi: 10.1016/S0306-4565(02)00058-X
https://doi.org/10.1016/S0306-4565(02)00...
).

Therefore, the main objective of present study was to evaluate and compare the effect of vegetable oils inclusion in diet on the performance, blood attributes and hsp 70 genes expression in broiler chickens under heat stress.

Material and methods

This experiment was carried out under the ethical guidelines of the Islamic Azad University of Tehran Science and Research Branch (93/987-2014).

Animals and dietary treatments

The present study was done in a research farm located near Karaj city (Alborz, Iran). Three hundred 1-day old Cobb 500 broiler chicks was provided from hatchery and placed in a environment controlled house. In a completely randomized design, chicks were assigned to 4 treatment groups (4 types of vegetable oils) with 5 replicates and 15 chicks per each replicate. Diets were formulated based on the Cobb 500 requirement recommendations. Dietary treatments were iso-nutritive with the same feeds and, but included one of vegetable oils at the same level. Treatments were 1: saturated oil (palm oil), 2: source of n-6 fatty acid (corn oil), 3: a source of n-3 fatty acid (flaxseed oil) and a source of n-9 fatty acid (olive oil). The experimental vegetable oils were included in the starter, grower and finisher rations as 1.5, 3.0 and 4.0%, respectively. During trial, chicks had free access fresh water and experimental diet. For inducing heat stress in chickens, house temperature was raised to 34 ± 1°C for 6 hours per day from day 11 to 41 of age. The increase in temperature in each day was done from 10:00 to 16:00 and then house temperature decreased to 22 ± 1°C. The relative humidity of house was maintained in 60-70%. At days 28 and 42 of age, chick’s weight and feed consumption was measured and feed conversion ratio was calculated for grower and finisher periods.

Sampling and analyses

On day 28 of age, the blood samples of 2 chicks per replicate were randomly collected directly from heart using vacuum tubes containing EDTA-gel.

The plasma T3 and T4 concentration were determined using relative ELISA kits according to manufacturer directions (Biocheck Inc., Foster City, CA, USA). Plasma corticosterone concentration was measured using autoanalyser (BS-120 model, Minbray Co., USA) and commercial available kit (Pars Azmon Co., Tehran, Iran). Plasma insulin level was measured enzymatically and by chicken antibody against insulin using photometric method and commercial kits (Cusabio Co., TX, USA).

After blood sampling, chicks were sacrificed by cervical dislocation, then liver was removed. Liver sample was collected and frozen in liquid nitrogen and then stored at -70°C until analysis of HSP70 gene expression.

Analysis of HSP70 gene expression

Accuzol reagent (10 mL g-1 of tissue) was used for total RNA extraction from the grounded liver samples according to the manufacturer directions (Bioneer, Cat. No. K-2102). After extraction, cDNA was synthesized from RNA sample (1 ug) by reverse transcription method using commercial cDNA Reverse Transcriptase kit (Bioneer Co., Seoul, South Korea). The resulting cDNA was placed in freezer at -20°C prior to use. Specific primer pairs (Gallus gallus, AY, 372 bp-763790, forward: 5'-AGCGTAACACCACCATTCC-3', reverse: 5'-ACGCTCCTGCAAGATAGTGAT-3') was designed and quantitative PCR analysis was done using Quanti Fast SYBER Green PCR kit (QIAGEN, Cat. No. 204052). Reference gene was GAPDH gene (M-32599, 230 bp, forward: 5'-TGAAAGTCGGAGTCAACGGAT-3', reverse: 5'-ACGCTCCTGGAAGATAGTGAT-3'). Amplification of HSP70 gene was performed as described by Aminoroaya, Sadeghi, Ansari-pirsaraei, and Kashan (2016Aminoroaya, K., Sadeghi, A. A., Ansari-pirsaraei, Z., & Kashan, N. (2016). Effect of cyclical cold stress during embryonic development on aspects of physiological responses and HSP70 gene expression of chicks. Journal of Thermal Biology, 61, 50-54. doi: 10.1016/j.jtherbio.2016.08.008
https://doi.org/10.1016/j.jtherbio.2016....
). The relative HSP70 expression ratio as target gene was normalized to GAPDH gene using 2-ΔΔct procedure as previously described by Aminoroaya et al. (2016Aminoroaya, K., Sadeghi, A. A., Ansari-pirsaraei, Z., & Kashan, N. (2016). Effect of cyclical cold stress during embryonic development on aspects of physiological responses and HSP70 gene expression of chicks. Journal of Thermal Biology, 61, 50-54. doi: 10.1016/j.jtherbio.2016.08.008
https://doi.org/10.1016/j.jtherbio.2016....
).

Statistical Analysis

Before ANOVA analysis, the normal distribution of data was evaluated using Kolmogorov-Smirnov test. SAS (2004Statistical Analysis Software [SAS]. (2004). SAS/STAT User guide, Version 9.1.1. Cary, NC: SAS Institute Inc.) software (version 9.1, SAS Institute, Cary, NC, USA) was used for statistical analysis based on ANOVA appropriate for completely randomized design to determine the effects of treatment groups on performance, hormonal levels and HSP70 gene expression. Mean comparison was done using the Tukey test. Probability values of less than 0.05 were considered significant.

Results and discussion

Table 1 show the dietary oils effects on daily feed intake, daily gain and FCR of broiler chicks at grower and finisher periods. There were significant differences (p < 0.05) among treatments for daily feed intake, daily gain and feed conversion ratio of chickens during grower and finisher periods. Lower feed conversion ratio was for chicken fed linseed oil and olive oil (p < 0.05).

Table 1
Effects of vegetable oils on daily feed intake, daily gain and feed conversion ratio.

In this study, the broiler chickens were fed iso-nutritive diets and the oils supplemented at the same level in grower and finisher periods. Significant differences for feed intake, gain and feed conversion ratio among chicks fed diet containing different vegetable oils were observed that is in line with the results of Nobakht, Tabatbaei, and Khodaei (2011Nobakht, A., Tabatbaei, S., & Khodaei, S. (2011). Effects of different sources and levels of vegetable oils on performance, carcass traits and accumulation of vitamin E in breast meat of broilers. Current Research Journal of Biological Sciences, 3(6), 601-605. ), who found that when supplemented different oil sources in broiler diets, significant differences were found for growth performance of broilers. Our finding is incontinence with finding of El-Deek et al. (2005) who reported that different source of vegetable oils had no significant effect on performance of broiler chickens under heat stress. Higher performance of chicks fed olive and linseed oils may be related to beneficial effects of these oils on plasma hormonal levels (Table 2) and gene expression of hsp 70 (Figure 1).

Plasma hormonal concentrations of chickens fed dietary oils were presented in Table 2. The lowest level of insulin was for chickens fed linseed oil and corn oil. Glucose and insulin levels were the highest in plasma of chickens fed palm oil (p < 0.05). In fact, insulin resistance occur in chicks fed diet containing palm oil. Some animal and human studies have shown that saturated fatty acid especially palmitic acid could increase the insulin resistance (Saidpour et al., 2011Saidpour, A., Zahediasl, S., Kimiagar, M., Vafa, M., Ghasemi, A., Abadi, A., ... Zarkesh, M. (2011). Fish oil and olive oil can modify insulin resistance and plasma desacyl-ghrelin in rats. Journal of Research in Medical Sciences, 16(7), 862-871. ).

Table 2
Effects of feeding diet containing vegetable oils on hormonal level

A study showed that high levels of palmitic acid in the diet could increase the demand for insulin secretion (Keita, Ramírez-San Juan, Paniagua-Castro, Garduño-Siciliano, & Quevedo, 2013Keita, H., Ramírez-San Juan, E., Paniagua-Castro, N., Garduño-Siciliano, L., & Quevedo, L. (2013). The long-term ingestion of a diet high in extra virgin olive oil produces obesity and insulin resistance but protects endothelial function in rats: a preliminary study. Diabetology & Metabolic Syndrome, 5(1), 53-58. doi: 10.1186/1758-5996-5-53
https://doi.org/10.1186/1758-5996-5-53...
). Another study has shown a relationship between saturated lipid, found in palm oil, and high plasma insulin level (Marshall et al., 1997Marshall, J. A., Bessesen, D. H., & Hamman, R. F. (1997). High saturated fat and low starch and fiber are associated with hyperinsulinaemia in a non-diabetic population: the San Luis Valley DiabetesStudy. Diabetologia, 40, 430-438.). Some studies showed that palmitic acid, found in palm oil, impaired the function of ß-cell and also insulin sensitivity, finally resulted in insulin resistance. In contrast to palmitic acid, oleic acid found in olive oil could control the blood glucose level by optimizing insulin production in pancreas and improving body glucose uptake and use, resulted in lowering of blood glucose levels (Keita et al., 2013Keita, H., Ramírez-San Juan, E., Paniagua-Castro, N., Garduño-Siciliano, L., & Quevedo, L. (2013). The long-term ingestion of a diet high in extra virgin olive oil produces obesity and insulin resistance but protects endothelial function in rats: a preliminary study. Diabetology & Metabolic Syndrome, 5(1), 53-58. doi: 10.1186/1758-5996-5-53
https://doi.org/10.1186/1758-5996-5-53...
). A report indicated that olive oil inclusion in diet significantly reduced the fasting plasma glucose due to the presence of a beneficial compound in olive oil named Oleuropein (Al Jamal & Ibrahim, 2011Al Jamal, A. R., & Ibrahim, A. (2011). Effects of olive oil on lipid profiles and blood glucose in type2 diabetic patients. International Journal of Diabetes and Metabolism, 19, 19-22. ). It is known that unsaturated fatty acids may affect phospholipids membranes and modulate the insulin sensitivity in these membranes (Abbott, Else, Atkins, & Hulbert, 2012Abbott, S. K., Else, P. L., Atkins, T. A., & Hulbert, A. J. (2012). Fatty acid composition of membrane bilayers: importance of diet polyunsaturated fat balance. Biochimica Et Biophysica Acta (BBA)-Biomembranes, 1818(5), 1309-1317. doi: 10.1016/j.bbamem.2012.01.011
https://doi.org/10.1016/j.bbamem.2012.01...
). Animal studies have demonstrated that n-6 PUFA, found in corn oil, in comparison to n-3 PUFA, found in linseed oil, could decrease the insulin sensitivity (Jucker, Cline, Barucci, & Shulman, 1999Jucker, B. M., Cline, G. W., Barucci, N., & Shulman, G. I. (1999). Differential effects of safflower oil versus fish oil feeding on insulin-stimulated glycogen synthesis, glycolysis, and pyruvate dehydrogenase flux in skeletal muscle: a 13C nuclear magnetic resonance study. Diabetes, 48(1), 134-140. doi: 10.2337/diabetes.48.1.134
https://doi.org/10.2337/diabetes.48.1.13...
; Saidpour et al., 2011Saidpour, A., Zahediasl, S., Kimiagar, M., Vafa, M., Ghasemi, A., Abadi, A., ... Zarkesh, M. (2011). Fish oil and olive oil can modify insulin resistance and plasma desacyl-ghrelin in rats. Journal of Research in Medical Sciences, 16(7), 862-871. ). In contrast to our results, a study showed that linseed oil had no effect on fasting blood glucose and insulin levels (Brostow et al., 2011Brostow, D. P., Odegaard, A. O., Koh, W.-P., Duval, S., Gross, M. D., Yuan, J.-M., & Pereira, M. A. (2011). Omega-3 fatty acids and incident type 2 diabetes: the Singapore Chinese Health Study. The American Journal of Clinical Nutrition, 94(2), 520-526. doi: 10.3945/ajcn.110.009357
https://doi.org/10.3945/ajcn.110.009357...
).

In comparison to previous our study (Sadeghi et al., 2013Sadeghi, A. A., Safaei, A., & Aminafshar, M. (2013). The effects of dietary oil sources on performance, serum corticosterone level, antibody titers and LFN-γ gene expression in broiler chickens. Kafkas Universitesi Veteriner Fakultesi Dergisi, 20(6), 857-862. doi: 10.9775/kvfd.2014.11163.
https://doi.org/10.9775/kvfd.2014.11163....
), the levels of corticosterone in the present study was high, which shows that chickens are exposed to heat stress. The highest level of corticosterone was found in plasma of chickens fed palm oil and the lowest level was for those received linseed oil (p < 0.05). A study showed that dietary fatty acid composition had significant effect on corticosterone level (Stachoń, Fürstenberg, & Gromadzka-Ostrowska, 2006Stachoń, M., Fürstenberg, E., & Gromadzka-Ostrowska, J. (2006). Effects of high-fat diets on body composition, hypothalamus NPY, and plasma leptin and corticosterone levels in rats. Endocrine, 30(1), 69-74. ). It was speculated that inclusion of olive oil in diet could increase adrenal corticosterone secretion (Pál et al., 2015Pál, L., Kulcsár, M., Poór, J., Wágner, L., Nagy, S., Dublecz, K., & Husvéth, F.(2015). Effect of feeding different oils on plasma corticosterone in broiler chickens. Acta Veterinaria Hungarica, 63(2), 179-188. doi: 10.1556/AVet.2015.015
https://doi.org/10.1556/AVet.2015.015...
). Despite the studies demonstrated the impact of fatty acids on the hypothalamic-pituitary-adrenal axis, the exact mechanism is still not clear.

Chickens received linseed and corn oils had the highest levels of T3 and T4 and those fed palm and olive oils had the lowest levels (p < 0.05). An interesting study showed that lipid source and level may have opposite effects on thyroid hormone levels (Lachowicz, Koszela-Piotrowska, & Rosołowska-Huszcz, 2009Lachowicz, K., Koszela-Piotrowska, I., & Rosołowska-Huszcz, D. (2009). Dietary fat type and level affect thyroid hormone plasma concentrations in rats. Journal of Animal and Feed Sciences, 18(3), 541-550. doi: 10.22358/jafs/66430/2009
https://doi.org/10.22358/jafs/66430/2009...
). The increase in T3 and T4 levels related to the effects of fatty acids on thyrotropin secretion (Clandinin, Claerhout, & Lien, 1998Clandinin, M. T., Claerhout, D. L., & Lien, E. L. (1998). Docosahexaenoic acid increases thyroid-stimulating hormone concentration in male and adrenal corticotrophic hormone concentration in female weanling rats. The Journal of Nutrition, 128(8), 1257-1261. doi: 10.1093/jn/128.8.1257
https://doi.org/10.1093/jn/128.8.1257...
).

Figure 1 shows the relative gene expression of HSP 70 for chickens fed different dietary oils. There were differences (p < 0.05) among treatments for gene expression. The highest HSP 70 gene expression was for chickens fed diet containing olive and linseed oils and the lowest one was for those fed corn and palm oils.

Figure 1
The relative gene expression of hsp 70 in chickens fed diet containing different vegetable oils.

It has been reported that lipids could directly and indirectly impact on the expression of genes. The direct is fast and has cute control on the expression levels and indirectly impact on the cell membrane composition and intracellular signaling (Kaput & Rodriguez, 2004Kaput, J., & Rodriguez, R. L. (2004). Nutritional genomics: the next frontier in the postgenomic era. Physiological Genomics, 16(2), 166-177. doi: 10.1152/physiolgenomics.00107.2003
https://doi.org/10.1152/physiolgenomics....
). In the literature there was no report concerning the impact of lipids on gene expression of hsp 70. The hsp 70 proteins are involved in the heat tolerance development (Zhao et al., 2014Zhao, F. Q., Zhang, Z. W., Qu, J. P., Yao, H. D., Li, M., Li, S., & Xu, S. W. (2014). Cold stress induces antioxidants and Hsps in chicken immune organs. Cell Stress and Chaperones, 19(5), 635-648. ); therefore, our results show that olive oil and linseed oil could influence on the heat tolerance compared to corn and palm oils.

Conclusion

It was concluded that olive oil and linseed oil could improve performance and heat tolerance of chickens under heat stress.

References

  • Abbott, S. K., Else, P. L., Atkins, T. A., & Hulbert, A. J. (2012). Fatty acid composition of membrane bilayers: importance of diet polyunsaturated fat balance. Biochimica Et Biophysica Acta (BBA)-Biomembranes, 1818(5), 1309-1317. doi: 10.1016/j.bbamem.2012.01.011
    » https://doi.org/10.1016/j.bbamem.2012.01.011
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    » https://doi.org/10.1016/j.plipres.2006.01.003
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    » https://doi.org/10.3389/fphys.2017.0.0919
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    » https://doi.org/10.1016/j.anifeedsci.2007.01.0.09
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  • Pál, L., Kulcsár, M., Poór, J., Wágner, L., Nagy, S., Dublecz, K., & Husvéth, F.(2015). Effect of feeding different oils on plasma corticosterone in broiler chickens. Acta Veterinaria Hungarica, 63(2), 179-188. doi: 10.1556/AVet.2015.015
    » https://doi.org/10.1556/AVet.2015.015
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  • Sadeghi, A. A., Mirmohseni, M., Shawrang, P., & Aminafshar, M. (2013). The effect of soy oil addition to the diet of broiler chicks on the immune response. Turkish Journal of Veterinary and Animal Sciences, 37(3), 264-270.
  • Sadeghi, A. A., Safaei, A., & Aminafshar, M. (2013). The effects of dietary oil sources on performance, serum corticosterone level, antibody titers and LFN-γ gene expression in broiler chickens. Kafkas Universitesi Veteriner Fakultesi Dergisi, 20(6), 857-862. doi: 10.9775/kvfd.2014.11163.
    » https://doi.org/10.9775/kvfd.2014.11163.
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Publication Dates

  • Publication in this collection
    24 Oct 2019
  • Date of issue
    2020

History

  • Received
    22 Sept 2018
  • Accepted
    26 Feb 2019
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