Efficacy of a phytonutrient supplement at different dietary protein contents on growth performance, gut morphology, digestive enzymes activities and stress indicators of broilers subjected to circular heat stress
Rohollah Ghasemi A , Hossein Ali Ghasemi A B , Iman Hajkhodadadi A and Mahdi Khodaei-Motlagh AA Department of Animal Science, Faculty of Agriculture and Natural Resources, Arak University, Shahid Beheshti Street, 38156-8-8349 Arak, Markazi Province, Iran.
B Corresponding author. Email: h-ghasemi@araku.ac.ir; haghasemi89@gmail.com
Animal Production Science 61(16) 1659-1671 https://doi.org/10.1071/AN20257
Submitted: 26 April 2020 Accepted: 2 June 2021 Published: 8 July 2021
Abstract
Context: Dietary manipulations such as reductions in protein or the addition of bioactive feed additives might alleviate the adverse effects of high ambient temperature in poultry.
Aims: The effects of dietary crude protein (CP) and phytonutrient mixture (PM) on growth performance and physiological responses were evaluated in broilers under circular heat stress (HS).
Methods: In total, 420 1-day-old broiler chickens were randomly distributed to seven treatments in a factorial arrangement (3 × 2), with three levels of CP (normal, medium (95% of the normal CP content) and low (90% of the normal CP content)) and with or without the addition of PM (mixture of 5 mg/kg carvacrol, 3 mg/kg cinnamaldehyde, and 2 mg/kg capsicum oleoresin). The thermoneutral control (TNC) birds were housed in a thermoneutral chamber and fed with a normal-CP diet without PM supplementation. The other six groups were kept in a HS chamber (33°C) for 8 h (1000 hours to 1800 hours).
Key results: After 6 weeks, feeding broiler chickens with low-CP diets had adversely affected growth performance and intestinal protease activities, while mortality rate, heterophile to lymphocyte ratio, and serum cortisol concentration of the low-CP group were lower (P < 0.05) than those of the high-CP group. Dietary PM supplementation also positively influenced (P < 0.05) average daily gain, feed conversion ratio, intestinal lipase and trypsin activities and serum T4 concentration. There were the CP × PM interactions (P < 0.05) for jejunal villus height and villus surface area, indicating that the effect of PM on these responses was more marked at the lower dietary CP contents.
Conclusions: Supplementation with PM can ameliorate the detrimental effects of HS on productive performance and digestive enzyme activities in broilers. The PM supplementation could improve intestinal morphology when applied to the diets of heat-stressed broilers with lower CP contents (95% and 90% of the recommendations).
Implications: Although growth performance was reduced by feeding low-CP diets (90% of the normal CP content), a beneficial effect was observed on the stress indicators of broilers grown in HS conditions. Dietary supplementation of PM might also be an effective strategy to alleviate the adverse effect of HS.
Keywords: essential oils, crude protein, gut health, heat-stressed broilers.
References
Allameh S, Toghyani M (2019) Effect of dietary valine supplementation to low protein diets on performance, intestinal morphology and immune responses in broiler chickens. Livestock Science 229, 137–144.| Effect of dietary valine supplementation to low protein diets on performance, intestinal morphology and immune responses in broiler chickens.Crossref | GoogleScholarGoogle Scholar |
Amiri M, Ghasemi HA, Hajkhodadadi I, Khaltabadi Farahani AH (2019) Efficacy of guanidinoacetic acid at different dietary crude protein levels on growth performance, stress indicators, antioxidant status, and intestinal morphology in broiler chickens subjected to cyclic heat stress. Animal Feed Science and Technology 254, 114208
| Efficacy of guanidinoacetic acid at different dietary crude protein levels on growth performance, stress indicators, antioxidant status, and intestinal morphology in broiler chickens subjected to cyclic heat stress.Crossref | GoogleScholarGoogle Scholar |
AOAC (2000) ‘Official Methods of Analysis of AOAC international.’ 9th rev. edn. (Association of Official Analytical Chemists: Gaithersburg, MD, USA)
Aviagen (2014) ‘Ross 308 Broiler: Nutrition Specification.’ (Aviagen Ltd: Newbridge Midlothian, Scotland, UK)
Awad EA, Zulkifli I, Soleimani AF, Loh TC (2015) Individual non-essential amino acids fortification of a low-protein diet for broilers under the hot and humid tropical climate. Poultry Science 94, 2772–2777.
| Individual non-essential amino acids fortification of a low-protein diet for broilers under the hot and humid tropical climate.Crossref | GoogleScholarGoogle Scholar | 26371331PubMed |
Awad EA, Zulkifli I, Soleimani AF, Aljuobori A (2017) Effects of feeding male and female broiler chickens on low-protein diets fortified with different dietary glycine levels under the hot and humid tropical climate. Italian Journal of Animal Science 16, 453–461.
| Effects of feeding male and female broiler chickens on low-protein diets fortified with different dietary glycine levels under the hot and humid tropical climate.Crossref | GoogleScholarGoogle Scholar |
Bravo D, Utterback P, Parsons CM (2011) Evaluation of a mixture of carvacrol, cinnamaldehyde, and capsicum oleoresin for improving growth performance and metabolizable energy in broiler chicks fed corn and soybean meal. Journal of Applied Poultry Research 20, 115–120.
| Evaluation of a mixture of carvacrol, cinnamaldehyde, and capsicum oleoresin for improving growth performance and metabolizable energy in broiler chicks fed corn and soybean meal.Crossref | GoogleScholarGoogle Scholar |
Bravo D, Pirgozliev V, Rose SP (2014) A mixture of carvacrol, cinnamaldehyde, and capsicum oleoresin improves energy utilization and growth performance of broiler chickens fed maize-based diet. Journal of Animal Science 92, 1531–1536.
| A mixture of carvacrol, cinnamaldehyde, and capsicum oleoresin improves energy utilization and growth performance of broiler chickens fed maize-based diet.Crossref | GoogleScholarGoogle Scholar | 24496847PubMed |
Brenes A, Roura E (2010) Essential oils in poultry nutrition: main effects and modes of action. Animal Feed Science and Technology 158, 1–14.
| Essential oils in poultry nutrition: main effects and modes of action.Crossref | GoogleScholarGoogle Scholar |
Burkholder KM, Thompson KL, Einstein ME, Applegate TJ, Patterson JA (2008) Influence of stressors on normal intestinal microbiota, intestinal morphology, and susceptibility to Salmonella Enteritidis colonization in broilers. Poultry Science 87, 1734–1741.
| Influence of stressors on normal intestinal microbiota, intestinal morphology, and susceptibility to Salmonella Enteritidis colonization in broilers.Crossref | GoogleScholarGoogle Scholar | 18753440PubMed |
Cheng YF, Chen YP, Chen R, Su Y, Zhang RQ, He QF, Wang K, Wen C, Zhou YM (2019) Dietary mannan oligosaccharide ameliorates cyclic heat stress-induced damages on intestinal oxidative status and barrier integrity of broilers. Poultry Science 98, 4767–4776.
| Dietary mannan oligosaccharide ameliorates cyclic heat stress-induced damages on intestinal oxidative status and barrier integrity of broilers.Crossref | GoogleScholarGoogle Scholar | 31005999PubMed |
Chowdhury VS (2019) Heat stress biomarker amino acids and neuropeptide afford thermotolerance in chicks. Journal of Poultry Science 56, 1–11.
| Heat stress biomarker amino acids and neuropeptide afford thermotolerance in chicks.Crossref | GoogleScholarGoogle Scholar |
Czauderna M, Białek M, Białek A, Śliwiński B, Brzóska F (2020) Chemical form of dietary selenium affects the fatty acids profile and oxidative stability of muscles of broilers supplemented with lycopene and oils. European Journal of Lipid Science and Technology 122, 1900132
| Chemical form of dietary selenium affects the fatty acids profile and oxidative stability of muscles of broilers supplemented with lycopene and oils.Crossref | GoogleScholarGoogle Scholar |
Danforth E, Burger A (1984) The role of thyroid hormones in the control of energy expenditure. Clinics in Endocrinology and Metabolism 13, 581–595.
| The role of thyroid hormones in the control of energy expenditure.Crossref | GoogleScholarGoogle Scholar | 6391756PubMed |
De Souza LFA, Espinha LP, de Almeida EA, Lunedo R, Furlan RL, Macari M (2016) How heat stress (continuous or cyclical) interferes with nutrient digestibility, energy and nitrogen balances and performance in broilers. Livestock Science 192, 39–43.
| How heat stress (continuous or cyclical) interferes with nutrient digestibility, energy and nitrogen balances and performance in broilers.Crossref | GoogleScholarGoogle Scholar |
Ghasemi HA, Nari N (2020) Effect of supplementary betaine on growth performance, blood biochemical profile, and immune response in heat-stressed broilers fed different dietary protein levels. Journal of Applied Poultry Research 29, 301–313.
| Effect of supplementary betaine on growth performance, blood biochemical profile, and immune response in heat-stressed broilers fed different dietary protein levels.Crossref | GoogleScholarGoogle Scholar |
Ghasemi HA, Ghasemi R, Torki M (2014) Periodic usage of low-protein methionine-fortified diets in broiler chickens under high ambient temperature conditions: effects on performance, slaughter traits, leukocyte profiles and antibody response. International Journal of Biometeorology 58, 1405–1414.
| Periodic usage of low-protein methionine-fortified diets in broiler chickens under high ambient temperature conditions: effects on performance, slaughter traits, leukocyte profiles and antibody response.Crossref | GoogleScholarGoogle Scholar | 24122339PubMed |
Hafeez A, Männer K, Schieder C, Zentek J (2016) Effect of supplementation of phytogenic feed additives (powdered vs. encapsulated) on performance and nutrient digestibility in broiler chickens. Poultry Science 95, 622–629.
| Effect of supplementation of phytogenic feed additives (powdered vs. encapsulated) on performance and nutrient digestibility in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 26706360PubMed |
Hashemipour H, Kermanshahi H, Golian A, Veldkamp T (2013) Metabolism and nutrition: effect of thymol and carvacrol feed supplementation on performance, antioxidant enzyme activities, fatty acid composition, digestive enzyme activities, and immune response in broiler chickens. Poultry Science 92, 2059–2069.
| Metabolism and nutrition: effect of thymol and carvacrol feed supplementation on performance, antioxidant enzyme activities, fatty acid composition, digestive enzyme activities, and immune response in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 23873553PubMed |
He X, Lu Z, Ma B, Zhang L, Li J, Jiang Y, Zhou G, Gao F (2019) Effects of dietary taurine supplementation on growth performance, jejunal morphology, appetite-related hormones, and genes expression in broilers subjected to chronic heat stress. Poultry Science 98, 2719–2728.
| Effects of dietary taurine supplementation on growth performance, jejunal morphology, appetite-related hormones, and genes expression in broilers subjected to chronic heat stress.Crossref | GoogleScholarGoogle Scholar | 30778570PubMed |
He S, Chen L, He Y, Chen F, Ma Y, Xiao D, He J (2020) Resveratrol alleviates heat stress-induced impairment of intestinal morphology, barrier integrity and inflammation in yellow-feather broilers. Animal Production Science
| Resveratrol alleviates heat stress-induced impairment of intestinal morphology, barrier integrity and inflammation in yellow-feather broilers.Crossref | GoogleScholarGoogle Scholar |
Hu F, Gao X, She R, Chen J, Mao J, Xiao P, Shi R (2017) Effects of antimicrobial peptides on growth performance and small intestinal function in broilers under chronic heat stress. Poultry Science 96, 798–806.
| Effects of antimicrobial peptides on growth performance and small intestinal function in broilers under chronic heat stress.Crossref | GoogleScholarGoogle Scholar | 28173474PubMed |
İpçak HH, Alçiçek A (2018) Addition of capsicum oleoresin, carvacrol, cinnamaldehyde and their mixtures to the broiler diet II: effects on meat quality. Journal of Animal Science and Technology 60, 9
| Addition of capsicum oleoresin, carvacrol, cinnamaldehyde and their mixtures to the broiler diet II: effects on meat quality.Crossref | GoogleScholarGoogle Scholar | 29736255PubMed |
Iranian Council of Animal Care (1995) ‘Guide to the care and use of experimental animals. Vol. 1.’ (Isfahan University of Technology: Isfahan, Iran)
Jang IS, Ko YH, Kang SY, Lee CY (2007) Effect of a commercial essential oil on growth performance, digestive enzyme activity and intestinal microflora population in broiler chickens. Animal Feed Science and Technology 134, 304–315.
| Effect of a commercial essential oil on growth performance, digestive enzyme activity and intestinal microflora population in broiler chickens.Crossref | GoogleScholarGoogle Scholar |
Khajali F, Raei A, Aghaei A, Qujeq D (2010) Evaluation of a dietary organic selenium supplement at different dietary protein concentrations on growth performance, body composition and antioxidative status of broilers reared under heat stress. Asian–Australasian Journal of Animal Sciences 23, 501–507.
| Evaluation of a dietary organic selenium supplement at different dietary protein concentrations on growth performance, body composition and antioxidative status of broilers reared under heat stress.Crossref | GoogleScholarGoogle Scholar |
Lee SH, Lillehoj HS, Jang SI, Lee KW, Bravo D, Lillehoj EP (2011) Effects of dietary supplementation with phytonutrients on vaccine-stimulated immunity against infection with Eimeria tenella. Veterinary Parasitology 181, 97–105.
| Effects of dietary supplementation with phytonutrients on vaccine-stimulated immunity against infection with Eimeria tenella.Crossref | GoogleScholarGoogle Scholar | 21676547PubMed |
Lillehoj HS, Kim DK, Bravo DM, Lee SH (2011) Effects of dietary plant-derived phytonutrients on the genome-wide profiles and coccidiosis resistance in the broiler chickens. BMC Proceedings 5, S34
| Effects of dietary plant-derived phytonutrients on the genome-wide profiles and coccidiosis resistance in the broiler chickens.Crossref | GoogleScholarGoogle Scholar | 21645315PubMed |
Løtvedt P, Fallahshahroudi A, Bektic L, Altimiras J, Jensen P (2017) Chicken domestication changes expression of stress-related genes in brain, pituitary and adrenals. Neurobiology of Stress 7, 113–121.
| Chicken domestication changes expression of stress-related genes in brain, pituitary and adrenals.Crossref | GoogleScholarGoogle Scholar | 28879214PubMed |
Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. The Journal of Biological Chemistry 193, 265–275.
| Protein measurement with the Folin phenol reagent.Crossref | GoogleScholarGoogle Scholar | 14907713PubMed |
Lynn KR, Clevette-Radford NA (1984) Purification and characterization of hevain, a serine protease from Hevea brasiliensis. Phytochemistry 23, 963–964.
| Purification and characterization of hevain, a serine protease from Hevea brasiliensis.Crossref | GoogleScholarGoogle Scholar |
Masouri L, Salari S, Sari M, Tabatabaei S, Masouri B (2017) Effect of feed supplementation with Satureja khuzistanica essential oil on performance and physiological parameters of broilers fed on wheat- or maize-based diets. British Poultry Science 58, 425–434.
| Effect of feed supplementation with Satureja khuzistanica essential oil on performance and physiological parameters of broilers fed on wheat- or maize-based diets.Crossref | GoogleScholarGoogle Scholar | 28494165PubMed |
Moran ET (2014) Intestinal events and nutritional dynamics predispose Clostridium perfringens virulence in broilers. Poultry Science 93, 3028–3036.
| Intestinal events and nutritional dynamics predispose Clostridium perfringens virulence in broilers.Crossref | GoogleScholarGoogle Scholar | 25260526PubMed |
Oke OE, Emeshili UK, Iyasere OS, Abioja MO, Daramola JO, Ladokun AO, Abiona JA, Williams TJ, Rahman SA, Rotimi SO (2017) Physiological responses and performance of broiler chickens offered olive leaf extract under a hot humid tropical climate. Journal of Applied Poultry Research 26, 376–382.
| Physiological responses and performance of broiler chickens offered olive leaf extract under a hot humid tropical climate.Crossref | GoogleScholarGoogle Scholar |
Omidi M, Taherpour K, Cheraghi J, Ghasemi HA (2015) Influence of cardamom essential oils and seeds on growth performance, blood characteristics and immunity of broilers. Animal Production Science 55, 573–579.
| Influence of cardamom essential oils and seeds on growth performance, blood characteristics and immunity of broilers.Crossref | GoogleScholarGoogle Scholar |
Oso AO, Suganthi RU, Reddy GBM, Malik PK, Thirumalaisamy G, Awachat VB, Selvaraju S, Arangasamy A, Bhatta R (2019) Effect of dietary supplementation with phytogenic blend on growth performance, apparent ileal digestibility of nutrients, intestinal morphology, and cecal microflora of broiler chickens. Poultry Science 98, 4755–4766.
| Effect of dietary supplementation with phytogenic blend on growth performance, apparent ileal digestibility of nutrients, intestinal morphology, and cecal microflora of broiler chickens.Crossref | GoogleScholarGoogle Scholar | 30951593PubMed |
Placha I, Takacova J, Ryzner M, Cobanova K, Laukova A, Strompfova V, Venglovska K, Faix S (2014) Effect of thyme essential oil and selenium on intestine integrity and antioxidant status of broilers. British Poultry Science 55, 105–114.
| Effect of thyme essential oil and selenium on intestine integrity and antioxidant status of broilers.Crossref | GoogleScholarGoogle Scholar | 24397472PubMed |
Salah AS, Mahmoud MA, Ahmed-Farid OA, El-Tarabany MS (2019) Effects of dietary curcumin and acetylsalicylic acid supplements on performance, muscle amino acid and fatty acid profiles, antioxidant biomarkers and blood chemistry of heat-stressed broiler chickens. Journal of Thermal Biology 84, 259–265.
| Effects of dietary curcumin and acetylsalicylic acid supplements on performance, muscle amino acid and fatty acid profiles, antioxidant biomarkers and blood chemistry of heat-stressed broiler chickens.Crossref | GoogleScholarGoogle Scholar | 31466762PubMed |
Scanes CG (2016) Biology of stress in poultry with emphasis on glucocorticoids and the heterophil to lymphocyte ratio. Poultry Science 95, 2208–2215.
| Biology of stress in poultry with emphasis on glucocorticoids and the heterophil to lymphocyte ratio.Crossref | GoogleScholarGoogle Scholar | 27252367PubMed |
Shirzadi H, Shariatmadari F, Karimi Torshizi MA, Rahimi S, Masoudi AA, Zaboli G, Hedayat-Evrigh N (2020) Plant extract supplementation as a strategy for substituting dietary antibiotics in broiler chickens exposed to low ambient temperature. Archives of Animal Nutrition
| Plant extract supplementation as a strategy for substituting dietary antibiotics in broiler chickens exposed to low ambient temperature.Crossref | GoogleScholarGoogle Scholar | 31852306PubMed |
Somogyi M (1960) Modification of two methods for the assay of amylase. Clinical Chemistry 6, 23–35.
| Modification of two methods for the assay of amylase.Crossref | GoogleScholarGoogle Scholar | 13832788PubMed |
Song ZH, Cheng K, Zheng XC, Ahmad H, Zhang LL, Wang T (2018) Effects of dietary supplementation with enzymatically treated Artemisia annua on growth performance, intestinal morphology, digestive enzyme activities, immunity, and antioxidant capacity of heat-stressed broilers. Poultry Science 97, 430–437.
| Effects of dietary supplementation with enzymatically treated Artemisia annua on growth performance, intestinal morphology, digestive enzyme activities, immunity, and antioxidant capacity of heat-stressed broilers.Crossref | GoogleScholarGoogle Scholar | 29077887PubMed |
Syafwan S, Kwakkel R, Verstegen M (2011) Heat stress and feeding strategies in meat-type chickens. World’s Poultry Science Journal 67, 653–674.
| Heat stress and feeding strategies in meat-type chickens.Crossref | GoogleScholarGoogle Scholar |
Tietz N, Fiereck EA (1966) A specific method for serum lipase determination. Clinica Chimica Acta 13, 352–358.
| A specific method for serum lipase determination.Crossref | GoogleScholarGoogle Scholar |
Torki M, Nasiroleslami M, Ghasemi HA (2017) The effects of different protein levels in laying hens under hot summer conditions. Animal Production Science 57, 927–934.
| The effects of different protein levels in laying hens under hot summer conditions.Crossref | GoogleScholarGoogle Scholar |
Ullah Z, Rehman ZU, Yin Y, Stein HH, Hayat Z, Ahmed G, Nisa MU, Akhtar M, Sarwar M (2017) Comparative ileal digestibility of amino acids in 00-rapeseed meal and rapeseed meal fed to growing male broilers. Poultry Science 96, 2736–2742.
| Comparative ileal digestibility of amino acids in 00-rapeseed meal and rapeseed meal fed to growing male broilers.Crossref | GoogleScholarGoogle Scholar | 28453657PubMed |
Wan X, Jiang L, Zhong H, Lu Y, Zhang L, Wang T (2017) Effects of enzymatically treated Artemisia annua L. on growth performance and some blood parameters of broilers exposed to heat stress. Animal Science Journal 88, 1239–1246.
| Effects of enzymatically treated Artemisia annua L. on growth performance and some blood parameters of broilers exposed to heat stress.Crossref | GoogleScholarGoogle Scholar | 28052518PubMed |
Wirnt R (1974a) Chymotrypsin, measurements with n-benzoyll-tyrosin ethyl ester as substrate. In ‘Methods of Enzymatic Analysis’. 2nd edn. (Ed. H Ulrich Bergmeyer) pp. 1009–1012. (Verlag Chemie: Weinheim, Germany)
Wirnt R (1974b) Trypsin, measurement with nα-p-toluenesulfonyl-l-arginine methyl ester as substrate. In ‘Methods of Enzymatic Analysis’. 3rd edn. (Ed. H Ulrich Bergmeyer) pp. 1021–1024. (Verlag Chemie: Weinheim, Germany)
Wu G, Wu Z, Dai Z, Yang Y, Wang W, Liu C, Wang B, Wang J, Yin Y (2013) Dietary requirements of ‘nutritionally non-essential amino acids’ by animals and humans. Amino Acids 44, 1107–1113.
| Dietary requirements of ‘nutritionally non-essential amino acids’ by animals and humans.Crossref | GoogleScholarGoogle Scholar | 23247926PubMed |
Wu G, Bazer FW, Dai Z, Li D, Wang J, Wu Z (2014) Amino acid nutrition in animals: protein synthesis and beyond. Annual Review of Animal Biosciences 2, 387–417.
| Amino acid nutrition in animals: protein synthesis and beyond.Crossref | GoogleScholarGoogle Scholar | 25384149PubMed |
Xu Y, Lai X, Li Z, Zhang X, Luo Q (2018) Effect of chronic heat stress on some physiological and immunological parameters in different breed of broilers. Poultry Science 97, 4073–4082.
| Effect of chronic heat stress on some physiological and immunological parameters in different breed of broilers.Crossref | GoogleScholarGoogle Scholar | 29931080PubMed |
Yi D, Hou Y, Tan L, Liao M, Xie J, Wang L, Ding B, Yang Y, Gong J (2016) N-acetylcysteine improves the growth performance and intestinal function in the heat-stressed broilers. Animal Feed Science and Technology 220, 83–92.
| N-acetylcysteine improves the growth performance and intestinal function in the heat-stressed broilers.Crossref | GoogleScholarGoogle Scholar |
Zaman QU, Mushtaq T, Nawaz H, Mirza MA, Mahmood S, Ahmad T, Babar ME, Mushtaq MMH (2008) Effect of varying dietary energy and protein on broiler performance in hot climate. Animal Feed Science and Technology 146, 302–312.
| Effect of varying dietary energy and protein on broiler performance in hot climate.Crossref | GoogleScholarGoogle Scholar |