Effect of Feeding Sugarcane Bagasse-Extracted Polyphenolic Mixture on the Growth Performance, Meat Quality, and Oxidative and Inflammatory Status of Chronic Heat-Stressed Broiler Chickens
Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Preparation of the SBPM
2.2. Animals and Experimental Design
2.3. Determination of Blood Oxidative Stress, Inflammatory Parameters, and Intestinal Permeability
2.4. Evaluation of Meat Quality
2.5. Statistical Analysis
3. Results
3.1. Effects on Growth Performance and Body Temperature
3.2. Blood Biochemical Parameters
3.3. Meat Quality
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Alexandratos, N.; Bruinsma, J. World Agriculture Towards 2030/2050: The 2012 Revision; ESA Working Paper; FAO: Rome, Italy, 2012; Available online: https://www.fao.org/4/ap106e/ap106e.pdf (accessed on 30 June 2012).
- Renaudeau, D.; Collin, A.; Yahav, S.; de Basilio, V.; Gourdine, J.L.; Collier, R.J. Adaptation to hot climate and strategies to alleviate heat stress in livestock production. Animal 2012, 6, 707–728. [Google Scholar] [CrossRef] [PubMed]
- Kikusato, M.; Toyomizu, M. Mechanisms underlying the effects of heat stress on intestinal integrity, inflammation, and microbiota in chickens. J. Poult. Sci. 2023, 60, 2023021. [Google Scholar] [CrossRef] [PubMed]
- Brugaletta, G.; Teyssier, J.R.; Rochell, S.J.; Dridi, S.; Sirri, F. A review of heat stress in chickens. Part I: Insights into physiology and gut health. Front. Physiol. 2022, 13, 934381. [Google Scholar] [CrossRef] [PubMed]
- Shakeri, M.; Oskoueian, E.; Le, H.H. Strategies to combat heat stress in broiler chickens: Unveiling the roles of selenium, vitamin E and vitamin C. Vet. Sci. 2020, 7, 71. [Google Scholar] [CrossRef]
- Oni, A.I.; Adeleye, O.O.; Adebowale, T.O.; Oke, O.E. The role of phytogenic feed additives in stress mitigation in broiler chickens. J. Anim. Physiol. Anim. Nutr. 2024, 108, 81–98. [Google Scholar] [CrossRef]
- Hidayat, D.F.; Mahendra, M.Y.N.; Kamaludeen, J.; Pertiwi, H. Lycopene in feed as antioxidant and immuno-modulator improves broiler chicken’s performance under heat-stress conditions. Vet. Med. Int. 2023, 2023, 5418081. [Google Scholar] [CrossRef]
- Liu, W.C.; Ou, B.H.; Liang, Z.L.; Zhang, R.; Zhao, Z.H. Algae-derived polysaccharides supplementation ameliorates heat stress-induced impairment of bursa of Fabricius via modulating NF-κB signaling pathway in broilers. Poult. Sci. 2021, 100, 101139. [Google Scholar] [CrossRef]
- Alagawany, M.; Elnesr, S.S.; Farag, M.R.; El-Naggar, K.; Taha, A.E.; Khafaga, A.F.; Madkour, M.; Salem, H.M.; El-Tahan, A.M.; El-Saadony, M.T.; et al. Betaine and related compounds: Chemistry, metabolism and role in mitigating heat stress in poultry. J. Therm. Biol. 2022, 104, 103168. [Google Scholar] [CrossRef]
- Machineni, L. Lignocellulosic biofuel production: Review of alternatives. Biomass Conver. Biorefin. 2020, 10, 779–791. [Google Scholar] [CrossRef]
- Shabbirahmed, A.M.; Haldar, D.; Dey, P.; Patel, A.K.; Singhania, R.R.; Dong, C.D.; Purkait, M.K. Sugarcane bagasse into value-added products: A review. Environ. Sci. Pollut. Res. Int. 2022, 29, 62785–62806. [Google Scholar] [CrossRef]
- Hewawansa, U.H.A.J.; Houghton, M.J.; Barber, E.; Costa, R.J.S.; Kitchen, B.; Williamson, G. Flavonoids and phenolic acids from sugarcane: Distribution in the plant, changes during processing, and potential benefits to industry and health. Compr. Rev. Food Sci. Food Saf. 2024, 23, e13307. [Google Scholar] [CrossRef] [PubMed]
- Awais, M.M.; Akhtar, M.; Muhammad, F.; ul Haq, A.; Anwar, M.I. Immunotherapeutic effects of some sugar cane (Saccharum officinarum L.) extracts against coccidiosis in industrial broiler chickens. Exp. Parasitol. 2011, 128, 104–110. [Google Scholar] [CrossRef] [PubMed]
- El-Abasy, M.; Motobu, M.; Nakamura, K.; Koge, K.; Onodera, T.; Vainio, O.; Toivanen, P.; Hirota, Y. Preventive and therapeutic effects of sugar cane extract on cyclophosphamide-induced immunosuppression in chickens. Int. Immunopharmacol. 2004, 4, 983–990. [Google Scholar] [CrossRef] [PubMed]
- Motobu, M.; Amer, S.; Koyama, Y.; Hikosaka, K.; Sameshima, T.; Yamada, M.; Nakamura, K.; Koge, K.; Kang, C.B.; Hayasidani, H.; et al. Protective effects of sugar cane extract on endotoxic shock in mice. Phytother. Res. 2006, 20, 359–363. [Google Scholar] [CrossRef] [PubMed]
- Kikusato, M.; Toyomizu, M. Differential effects of heat stress on oxidative status of skeletal muscle with different muscle fibre compositions in broiler chicken. J. Anim. Feed Sci. 2019, 28, 78–82. [Google Scholar] [CrossRef]
- Kikusato, M.; Xue, G.; Pastor, A.; Niewold, T.A.; Toyomizu, M. Effects of plant-derived isoquinoline alkaloids on growth performance and intestinal function of broiler chickens under heat stress. Poult. Sci. 2021, 100, 957–963. [Google Scholar] [CrossRef]
- Shakeri, M.; Cottrell, J.J.; Wilkinson, S.; Le, H.H.; Suleria, H.A.R.; Warner, R.D.; Dunshea, F.R. A dietary sugarcane-derived polyphenol mix reduces the negative effects of cyclic heat exposure on growth performance, blood gas status, and meat quality in broiler chickens. Animals 2020, 10, 1158. [Google Scholar] [CrossRef]
- Furukawa, K.; Kikusato, M.; Kamizono, T.; Toyomizu, M. Time-course changes in muscle protein degradation in heat-stressed chickens: Possible involvement of corticosterone and mitochondrial reactive oxygen species generation in induction of the ubiquitin-proteasome system. Gen. Comp. Endocrinol. 2016, 228, 105–110. [Google Scholar] [CrossRef]
- Wang, J.; Xue, X.; Liu, Q.; Zhang, S.; Peng, M.; Zhou, J.; Chen, L.; Fang, F. Effects of duration of thermal stress on growth performance, serum oxidative stress indices, the expression and localization of ABCG2 and mitochondria ROS production of skeletal muscle, small intestine and immune organs in broilers. J. Therm. Biol. 2019, 85, 102420. [Google Scholar] [CrossRef]
- Mujahid, A.; Akiba, Y.; Warden, C.H.; Toyomizu, M. Sequential changes in superoxide production, anion carriers and substrate oxidation in skeletal muscle mitochondria of heat-stressed chickens. FEBS Lett. 2007, 581, 3461–3467. [Google Scholar] [CrossRef]
- Lin, H.; Decuypere, E.; Buyse, J. Acute heat stress induces oxidative stress in broiler chickens. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2006, 144, 11–17. [Google Scholar] [CrossRef] [PubMed]
- Mir, N.A.; Rafiq, A.; Kumar, F.; Singh, V.; Shukla, V. Determinants of broiler chicken meat quality and factors affecting them: A review. J. Food Sci. Technol. 2017, 54, 2997–3009. [Google Scholar] [CrossRef] [PubMed]
- Baéza, E.; Guillier, L.; Petracci, M. Review: Production factors affecting poultry carcass and meat quality attributes. Animal 2022, 16 (Suppl. 1), 100331. [Google Scholar] [CrossRef] [PubMed]
- Garcia, A.F.; Murakami, A.E.; Duarte, C.R.; Rojas, I.C.; Picoli, K.P.; Puzotti, M.M. Use of vitamin d3 and its metabolites in broiler chicken feed on performance, bone parameters and meat quality. Asian-Australas. J Anim. Sci. 2013, 26, 408–415. [Google Scholar] [CrossRef] [PubMed]
- Zaboli, G.; Huang, X.; Feng, X.; Ahn, D.U. How can heat stress affect chicken meat quality?—A review. Poult. Sci. 2019, 98, 1551–1556. [Google Scholar] [CrossRef]
- Wang, R.R.; Pan, X.J.; Peng, Z.Q. Effects of heat exposure on muscle oxidation and protein functionalities of pectoralis majors in broilers. Poult. Sci. 2009, 88, 1078–1084. [Google Scholar] [CrossRef]
- Del Vesco, A.P.; Gasparino, E.; Grieser, D.e.O.; Zancanela, V.; Soares, M.A.; Neto, A.R. Effects of methionine supplementation on the expression of oxidative stress-related genes in acute heat stress-exposed broilers. Br. J. Nutr. 2015, 113, 549–559. [Google Scholar] [CrossRef]
- Scanes, C.G. Biology of stress in poultry with emphasis on glucocorticoids and the heterophil to lymphocyte ratio. Poult. Sci. 2016, 95, 2208–2215. [Google Scholar] [CrossRef]
- Lan, R.; Li, Y.; Chang, Q.; Zhao, Z. Dietary chitosan oligosaccharides alleviate heat stress-induced intestinal oxidative stress and inflammatory response in yellow-feather broilers. Poult. Sci. 2020, 99, 6745–6752. [Google Scholar] [CrossRef]
- Vicuña, E.A.; Kuttappan, V.A.; Galarza-Seeber, R.; Latorre, J.D.; Faulkner, O.B.; Hargis, B.M.; Tellez, G.; Bielke, L.R. Effect of dexamethasone in feed on intestinal permeability, differential white blood cell counts, and immune organs in broiler chicks. Poult. Sci. 2015, 94, 2075–2080. [Google Scholar] [CrossRef]
- Yvon, S.; Beaumont, M.; Dayonnet, A.; Eutamène, H.; Lambert, W.; Tondereau, V.; Chalvon-Demersay, T.; Belloir, P.; Paës, C. Effect of diet supplemented with functional amino acids and polyphenols on gut health in broilers subjected to a corticosterone-induced stress. Sci. Rep. 2024, 14, 1032. [Google Scholar] [CrossRef] [PubMed]
- Hadid, R.; Spinedi, E.; Chautard, T.; Giacomini, M.; Gaillard, R.C. Role of several mediators of inflammation on the mouse hypothalamo-pituitary-adrenal axis response during acute endotoxemia. Neuroimmunomodulation 1999, 6, 336–343. [Google Scholar] [CrossRef] [PubMed]
- Beishuizen, A.; Thijs, L.G. Endotoxin and the hypothalamo-pituitary-adrenal (HPA) axis. J. Endotoxin. Res. 2003, 9, 3–24. [Google Scholar] [PubMed]
- Lauridsen, C. From oxidative stress to inflammation: Redox balance and immune system. Poult. Sci. 2019, 98, 4240–4246. [Google Scholar] [CrossRef]
- Teng, Z.; Yuan, C.; Zhang, F.; Huan, M.; Cao, W.; Li, K.; Yang, J.; Cao, D.; Zhou, S.; Mei, Q. Intestinal absorption and first-pass metabolism of polyphenol compounds in rat and their transport dynamics in Caco-2 cells. PLoS ONE 2012, 7, e29647. [Google Scholar] [CrossRef]
- Kikusato, M. Phytobiotics to improve health and production of broiler chickens: Functions beyond the antioxidant activity. Anim. Biosci. 2021, 34, 345–353. [Google Scholar] [CrossRef]
- Yamauchi, K.; Buwjoom, T.; Koge, K.; Ebashi, T. Histological alterations of the intestinal villi and epithelial cells in chickens fed dietary sugar cane extract. Br. Poult. Sci. 2006, 47, 544–553. [Google Scholar] [CrossRef]
- El-Abasy, M.; Motobu, M.; Shimura, K.; Na, K.J.; Kang, C.B.; Koge, K.; Onodera, T.; Hirota, Y. Immunostimulating and growth-promoting effects of sugar cane extract (SCE) in chickens. J Vet. Med. Sci. 2002, 64, 1061–1063. [Google Scholar] [CrossRef]
- Fangueiro, J.F.; de Carvalho, N.M.; Antunes, F.; Mota, I.F.; Pintado, M.E.; Madureira, A.R.; Costa, P.S. Lignin from sugarcane bagasse as a prebiotic additive for poultry feed. Int. J. Biol. Macromol. 2023, 239, 124262. [Google Scholar] [CrossRef]
- Loo, Y.T.; Howell, K.; Suleria, H.; Zhang, P.; Liu, S.; Ng, K. Fibre fermentation and pig faecal microbiota composition are affected by the interaction between sugarcane fibre and (poly)phenols. Int. J. Food Sci. Nutr. 2023, 74, 219–233. [Google Scholar] [CrossRef]
Ingredient (Bird Age/Stage) | 0–10 d (Starter) | 11–25 d (Grower) | 26–35 d (Finisher-1) | 36–42 d (Finisher-2) |
---|---|---|---|---|
Corn | 49.410 | 51.410 | 55.990 | 58.490 |
Sorghum | 10.000 | 10.000 | 10.000 | 10.000 |
Soybean meal | 26.500 | 27.500 | 23.500 | 21.000 |
Corn gluten meal (CP60) | 5.000 | 3.000 | 3.000 | 3.000 |
Fish meal (CP65) | 4.000 | 3.000 | 3.000 | 3.000 |
Vegetable oil | 1.000 | 1.900 | 1.900 | 2.000 |
Salt | 0.330 | 0.350 | 0.340 | 0.350 |
CaHPO4 | 1.500 | 1.050 | 0.800 | 0.700 |
Calcium bicarbonate | 0.980 | 0.750 | 0.650 | 0.600 |
L-Lysine hydrochloride | 0.300 | 0.220 | 0.180 | 0.180 |
DL-Methionine | 0.330 | 0.320 | 0.210 | 0.250 |
L-Threonine | 0.140 | 0.100 | 0.070 | 0.070 |
Choline chloride | 0.080 | 0.060 | 0.060 | 0.060 |
Selenium | 0.030 | 0.030 | 0.030 | 0.030 |
Vitamin/mineral mix * | 0.400 | 0.310 | 0.270 | 0.270 |
Calculated values | ||||
Crude protein (%) | 23.0 | 21.5 | 20.0 | 19.0 |
Metabolizable energy (kcal/kg) | 3000 | 3050 | 3100 | 3200 |
Calcium (%) | 0.99 | 0.76 | 0.66 | 0.61 |
Nonphytate phosphorus (%) | 0.52 | 0.43 | 0.37 | 0.35 |
Lysine (%) | 1.33 | 1.21 | 1.10 | 1.04 |
Methionine/cysteine (%) | 1.01 | 0.94 | 0.82 | 0.83 |
Threonine (%) | 0.88 | 0.80 | 0.72 | 0.70 |
Age (Period) | Thermoneutral, SBPM (ppm) | Heat-Stressed, SBPM (ppm) | SEM | ANOVA | ||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
0 | 75 | 150 | 300 | 0 | 75 | 150 | 300 | Temp. | Diet | Temp. × Diet | ||
Body weight, g | ||||||||||||
10 d | 336 | 336 | 328 | 337 | - | - | - | - | 4 | - | 0.107 | - |
25 d | 1415 a | 1425 a | 1424 a | 1409 a | 1179 c | 1157 c | 1224 b | 1383 a | 24 | p < 0.001 | p < 0.001 | p < 0.001 |
35 d | 2313 b | 2437 a | 2475 a | 2409 ab | 1998 d | 1988 d | 2110 c | 2294 b | 37 | p < 0.001 | p < 0.001 | p < 0.001 |
42 d | 3168 a | 3255 a | 3300 a | 3233 a | 2686 d | 2710 cd | 2849 c | 3016 b | 54 | p < 0.001 | p < 0.001 | p < 0.001 |
Body weight gain, g | ||||||||||||
0–10 d | 292 | 293 | 285 | 294 | - | - | - | - | 4 | - | 0.103 | - |
11–25 d | 1080 a | 1085 a | 1097 a | 1076 a | 843 c | 825 c | 894 b | 1043 a | 25 | p < 0.001 | p < 0.001 | p < 0.001 |
26–35 d | 898 | 1011 | 1051 | 1000 | 819 | 832 | 886 | 911 | 45 | p < 0.001 | p < 0.001 | 0.283 |
36–42 d | 855 | 818 | 825 | 824 | 688 | 722 | 739 | 722 | 61 | p < 0.001 | 0.993 | 0.7792 |
0–42 d | 3125 a | 3212 a | 3257 a | 3190 a | 2643 d | 2667 c | 2806 c | 2973 b | 54 | p < 0.001 | p < 0.001 | p < 0.001 |
Feed intake, g | ||||||||||||
0–10 d | 297 | 297 | 293 | 301 | - | - | - | - | 7 | - | 0.620 | - |
11–25 d | 1402 a | 1394 a | 1380 a | 1384 a | 1222 b | 1219 b | 1235 b | 1372 a | 40 | p < 0.001 | 0.038 | 0.015 |
26–35 d | 1461 b | 1535 a | 1534 a | 1531 a | 1384 c | 1336 bc | 1411 b | 1439 b | 33 | p < 0.001 | 0.032 | 0.048 |
36–42 d | 1539 | 1445 | 1460 | 1500 | 1366 | 1322 | 1325 | 1311 | 42 | p < 0.001 | 0.096 | 0.647 |
0–42 d | 4701 | 4674 | 4665 | 4717 | 4267 | 4170 | 4264 | 4422 | 65 | p < 0.001 | 0.022 | 0.173 |
Feed conversion ratio | ||||||||||||
0–10 d | 1.02 | 1.01 | 1.03 | 1.03 | - | - | - | - | 0.02 | - | 0.937 | - |
11–25 d | 1.30 | 1.29 | 1.26 | 1.29 | 1.45 | 1.48 | 1.38 | 1.32 | 0.05 | p < 0.001 | 0.067 | 0.126 |
26–35 d | 1.63 | 1.52 | 1.47 | 1.54 | 1.71 | 1.61 | 1.60 | 1.58 | 0.06 | 0.012 | 0.022 | 0.797 |
36–42 d | 1.86 | 1.81 | 1.78 | 1.83 | 2.02 | 1.85 | 1.83 | 1.83 | 0.16 | 0.463 | 0.659 | 0.918 |
0–42 d | 1.51 b | 1.46 bc | 1.43 c | 1.48 b | 1.62 a | 1.57 ab | 1.52 b | 1.49 b | 0.03 | p < 0.001 | 0.003 | 0.047 |
Parameters | Thermoneutral (SBPM, ppm) | Heat-Stressed (SBPM, ppm) | SEM | Two-Way ANOVA | ||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
0 | 75 | 150 | 300 | 0 | 75 | 150 | 300 | Temp. | Diet | Temp. × Diet | ||
TBARS | 38.6 c | 31.7 d | 31.1 d | 33.8 cd | 58.2 a | 50.7 b | 48.1 bc | 43.2 c | 2.7 | p < 0.001 | p < 0.001 | 0.045 |
CORT | 24.3 c | 26.2 c | 25.1 c | 28.1 c | 53.8 a | 51.4 a | 48.3 ab | 40.6 b | 2.8 | p < 0.001 | 0.019 | 0.047 |
UA | 77.6 c | 80.1 c | 82.2 bc | 76.4 c | 101.5 a | 86.7 b | 88.0 b | 85.8 b | 3.5 | p < 0.001 | 0.012 | 0.002 |
IL-6 | 37.0 d | 35.7 d | 34.0 d | 36.7 d | 87.6 a | 73.4 b | 66.4 bc | 62.4 c | 3.0 | p < 0.001 | p < 0.001 | p < 0.001 |
IL-1β | 9.5 | 8.2 | 8.0 | 8.3 | 29.7 | 25.9 | 22.0 | 20.7 | 2.5 | p < 0.001 | 0.024 | 0.135 |
FITC-d | 0.28 c | 0.32 c | 0.32 c | 0.31 c | 0.64 a | 0.48 b | 0.52 b | 0.50 b | 0.03 | p < 0.001 | 0.023 | p < 0.001 |
Parameters | Thermoneutral (SBPM, ppm) | Heat-Stressed (SBPM, ppm) | SEM | Two-Way ANOVA | ||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
0 | 75 | 150 | 300 | 0 | 75 | 150 | 300 | Temp. | Diet | Temp. × diet | ||
Drip loss, % | ||||||||||||
Breast | 1.92 | 1.63 | 1.44 | 1.48 | 4.07 | 3.75 | 2.66 | 3.26 | 0.3 | p < 0.001 | 0.003 | 0.217 |
Thigh | 1.96 | 1.71 | 1.89 | 2.03 | 3.74 | 3.51 | 2.94 | 3.05 | 0.3 | p < 0.001 | 0.336 | 0.197 |
Glutathione, μmol/g wet tissue | ||||||||||||
Breast | 2.70 a | 2.65 ab | 2.69 a | 2.70 a | 2.12 c | 2.30 c | 2.43 cb | 2.46 b | 0.1 | p < 0.001 | 0.0365 | 0.0347 |
Thigh | 4.01 a | 3.88 a | 4.05 a | 3.85 a | 2.57 bc | 2.61 b | 2.78 ab | 2.97 a | 0.1 | p < 0.001 | 0.2044 | 0.0432 |
TBARS, nmol/g wet tissue | ||||||||||||
Breast | 28.2 c | 23.5 cd | 21.1 d | 24.9 cd | 66.3 a | 55.4 b | 43.6 c | 37.1 c | 2.7 | p < 0.001 | p < 0.001 | p < 0.001 |
Thigh | 78.6 c | 69.3 cd | 60.3 d | 68.0 cd | 110.0 a | 95.4 b | 87.5 c | 83.3 c | 2.7 | p < 0.001 | p < 0.001 | 0.0013 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kikusato, M.; Namai, F.; Yamada, K. Effect of Feeding Sugarcane Bagasse-Extracted Polyphenolic Mixture on the Growth Performance, Meat Quality, and Oxidative and Inflammatory Status of Chronic Heat-Stressed Broiler Chickens. Animals 2024, 14, 3443. https://doi.org/10.3390/ani14233443
Kikusato M, Namai F, Yamada K. Effect of Feeding Sugarcane Bagasse-Extracted Polyphenolic Mixture on the Growth Performance, Meat Quality, and Oxidative and Inflammatory Status of Chronic Heat-Stressed Broiler Chickens. Animals. 2024; 14(23):3443. https://doi.org/10.3390/ani14233443
Chicago/Turabian StyleKikusato, Motoi, Fu Namai, and Katsushige Yamada. 2024. "Effect of Feeding Sugarcane Bagasse-Extracted Polyphenolic Mixture on the Growth Performance, Meat Quality, and Oxidative and Inflammatory Status of Chronic Heat-Stressed Broiler Chickens" Animals 14, no. 23: 3443. https://doi.org/10.3390/ani14233443
APA StyleKikusato, M., Namai, F., & Yamada, K. (2024). Effect of Feeding Sugarcane Bagasse-Extracted Polyphenolic Mixture on the Growth Performance, Meat Quality, and Oxidative and Inflammatory Status of Chronic Heat-Stressed Broiler Chickens. Animals, 14(23), 3443. https://doi.org/10.3390/ani14233443