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Dietary enzymatically treated Artemisia annua L. supplementation alleviates liver oxidative injury of broilers reared under high ambient temperature

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Abstract

Heat stress induced by high ambient temperature is a major concern in commercial broiler production. To evaluate the effects of dietary enzymatically treated Artemisia annua L. (EA) supplementation on growth performance and liver oxidative injury of broilers reared under heat stress, a total of 320 22-day-old male broilers were randomly allotted into five groups with eight replicates of eight birds each. Broilers in the control group were housed at 22 ± 1 °C and fed the basal diet. Broilers in the HS, HS-EA1, HS-EA2, and HS-EA3 groups were fed basal diet supplemented with 0, 0.75, 1.00, and 1.25 g/kg EA, respectively, and reared under cyclic high temperature (34 ± 1 °C for 8 h/day and 22 ± 1 °C for 16 h/day). Broilers fed EA diets had higher final body weight, average daily body weight gain, and average daily feed intake, as well as liver concentration of reduced glutathione, activities of antioxidant enzymes, abilities to inhibit hydroxyl radical and superoxide radical (HS-EA2 and HS-EA3), and lower liver concentrations of reactive oxygen metabolites, malondialdehyde, and protein carbonyl (HS-EA1, HS-EA2, and HS-EA3) than HS group (P < 0.05). EA treatment downregulated the mRNA levels of heat shock proteins 70 and 90, upregulated the mRNA levels of nuclear factor erythroid 2-related factor 2 (HS-EA1, HS-EA2, and HS-EA3) and heme oxygenase 1 (HS-EA2 and HS-EA3) in liver of heat-treated broilers (P < 0.05). In conclusion, EA alleviated heat stress-induced growth depression and liver oxidative injury in broilers, possibly through improving the antioxidant capacity and regulating the pertinent mRNA expression. The appropriate inclusion level of EA in broiler diet is 1.00–1.25 g/kg.

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References

  • Ahmad H, Tian J, Wang J, Khan MA, Wang Y, Zhang L, Wang T (2012) Effects of dietary sodium selenite and selenium yeast on antioxidant enzyme activities and oxidative stability of chicken breast meat. J Agri Food Chem 60:7111–7120

    Article  CAS  Google Scholar 

  • Akbarian A, Michiels J, Degroote J, Majdeddin M, Golian A, Smet S (2016) Association between heat stress and oxidative stress in poultry; mitochondrial dysfunction and dietary interventions with phytochemicals. J Anim Sci Biotechnol 7:37–50

    Article  Google Scholar 

  • Akhavan-Salamat H, Ghasemi HA (2016) Alleviation of chronic heat stress in broilers by dietary supplementation of betaine and turmeric rhizome powder: dynamics of performance, leukocyte profile, humoral immunity, and antioxidant status. Trop Anim Health Prod 48:181–188

    Article  Google Scholar 

  • Alam J, Stewart D, Touchard C, Boinapally S, Choi AMK, Cook JL (1999) Nrf2, a Cap’n’Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem 274:26071–26078

    Article  CAS  Google Scholar 

  • Alba M, Esmaeilipour O, Mirmahmoudi R (2015) Effects of Withania coagulans fruit powder and vitamin C on growth performance and some blood components in heat stressed broiler chickens. Livest Sci 173:64–68

    Article  Google Scholar 

  • Bainor A, Chang L, McQuade TJ, Webb B, Gestwicki JE (2011) Bicinchoninic acid (BCA) assay in low volume. Anal Biochem 410:310–312

    Article  CAS  Google Scholar 

  • Belhadj Slimen I, Najar T, Ghram A, Dabbebi H, Ben Mrad M, Abdrabbah M (2014) Reactive oxygen species, heat stress and oxidative-induced mitochondrial damage. A review. Int J Hyperth 30:513–523

  • Belhadj Slimen I, Najar T, Ghram A, Abdrrabba M (2016) Heat stress effects on livestock: molecular, cellular and metabolic aspects, a review. J Anim Physiol Anim Nutr (Berl) 100:401–412

    Article  CAS  Google Scholar 

  • Brisibe EA, Umoren UE, Owai PU, Brisibe F (2008) Dietary inclusion of dried Artemisia annua leaves for management of coccidiosis and growth enhancement in chickens. Afr J Biotechnol 7:4083–4092

    CAS  Google Scholar 

  • Brisibe EA, Umoren UE, Brisibe F, Magalhäes PM, Ferreira JFS, Luthria D, Wu XL, Prior RL (2009) Nutritional characterisation and antioxidant capacity of different tissues of Artemisia annua L. Food Chem 115:1240–1246

    Article  CAS  Google Scholar 

  • Cherian G, Orr A, Burke IC, Pan W (2013) Feeding Artemisia annua alters digesta pH and muscle lipid oxidation products in broiler chickens. Poult Sci 92:1085–1090

    Article  CAS  Google Scholar 

  • Costantini D, Dell’Omo G (2006) Effects of T-cell-mediated immune response on avian oxidative stress. Comp Biochem Physiol Part A Mol Integr Physiol 145:137–142

    Article  Google Scholar 

  • Engberg RM, Grevsen K, Ivarsen E, Fretté X, Christensen LP, Højberg O, Jensen BB, Canibe N (2012) The effect of Artemisia annua L. on broiler performance, on intestinal microbiota and on the course of a Clostridium perfringens infection applying a necrotic enteritis disease model. Avian Pathol 41:369–376

    Article  Google Scholar 

  • Ferreira J, Janick J (2009) Annual Wormwood (Artemisia annua L.): New Crop FactSHEET. www.hort.purdue.edu/newcrop/cropfactsheets/artemisia.pdf

  • Ferreira JF, Luthria DL, Sasaki T, Heyerick A (2010) Flavonoids from Artemisia annua L. as antioxidants and their potential synergism with artemisinin against malaria and cancer. Molecules 15:3135–3170

    Article  CAS  Google Scholar 

  • Ghazi S, Amjadian T, Norouzi S (2015) Single and combined effects of vitamin C and oregano essential oil in diet, on growth performance, and blood parameters of broiler chicks reared under heat stress condition. Int J Biometeorol 59:1019–1024

    Article  Google Scholar 

  • Gholamrezaie Sani L, Mohammadi M, Jalali Sendi J, Abolghasemi SA, Roostaie Ali Mehr M (2013) Extract and leaf powder effect of Artemisia annua L. on performance, cellular and humoral immunity in broilers. Iran J Vet Res 14:15–20

    Google Scholar 

  • Gouveia SC, Castilho PC (2013) Artemisia annua L.: essential oil and acetone extract composition and antioxidant capacity. Ind Crop Prod 45:170–181

    Article  CAS  Google Scholar 

  • Hosseini-Vashan SJ, Golian A, Yaghobfar A (2016) Growth, immune, antioxidant, and bone responses of heat stress-exposed broilers fed diets supplemented with tomato pomace. Int J Biometeorol 60:1183–1192

    Article  CAS  Google Scholar 

  • Jones DP (2002) Redox potential of GSH/GSSG couple: assay and biological significance. Methods in Enzymol 348:93–112

    Article  CAS  Google Scholar 

  • Kim KS, Lee S, Lee YS, Jung SH, Park Y, Shin KH, Kim BK (2003) Anti-oxidant activities of the extracts from the herbs of Artemisia apiacea. J Ethnopharmacol 85:69–72

    Article  Google Scholar 

  • Lin H, Decuypere E, Buyse J (2006) Acute heat stress induces oxidative stress in broiler chickens. Comp Biochem Physiol Part A Mol Integr Physiol 144:11–17

    Article  Google Scholar 

  • Mack LA, Felver-Gant JN, Dennis RL, Cheng HW (2013) Genetic variation alter production and behavioral responses following heat stress in 2 strains of laying hens. Poult Sci 92:285–294

    Article  CAS  Google Scholar 

  • Niture SK, Kaspar JW, Shen J, Jaiswal AK (2010) Nrf2 signaling and cell survival. Toxicol Appl Pharmacol 244:37–42

    Article  CAS  Google Scholar 

  • Nollen EAA, Morimoto RI (2002) Chaperoning signaling pathways: molecular chaperones as stress-sensing “heat shock” proteins. J Cell Sci 115:2809–2816

    CAS  Google Scholar 

  • NRC (1994) Nutrient requirements of poultry, 9th edn. National Academy Press, Washington, DC

    Google Scholar 

  • Pietta PG (2000) Flavonoids as antioxidants. J Nat Prod 63:1035–1042

    Article  CAS  Google Scholar 

  • Puri M, Sharma D, Barrow CJ (2012) Enzyme-assisted extraction of bioactives from plants. Trends Biotechnol 30:37–44

    Article  CAS  Google Scholar 

  • Ryu BK, Ahn BO, Oh TY, Kim SH, Kim WB, Lee EB (1998) Studies on protective effect of DA-9601, Artemisia asiatica extract, on acetaminophen- and CCl4-induced liver damage in rats. Arch Pharm Res 21:508–513

    Article  CAS  Google Scholar 

  • Sahin K, Orhan C, Akdemir F, Tuzcu M, Ali S, Sahin N (2011) Tomato powder supplementation activates Nrf-2 via ERK/AKt signaling pathway and attenuates heat stress-related responses in quails. Anim Feed Sci Technol 165:230–237

    Article  CAS  Google Scholar 

  • Sahin K, Orhan C, Tuzcu Z, Tuzcu M, Sahin N (2012) Curcumin ameloriates heat stress via inhibition of oxidative stress and modulation of Nrf2/HO-1 pathway in quail. Food Chem Toxicol 50:4035–4041

    Article  CAS  Google Scholar 

  • Sangokoya C, Telen MJ, Chi JT (2010) microRNA miR-144 modulates oxidative stress tolerance and associates with anemia severity in sickle cell disease. Blood 116:4338–4348

    Article  CAS  Google Scholar 

  • SAS Institute Inc (2008) SAS/STAT® 9.2 user’s guide. SAS Institute Inc, Cary, NC

    Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108

    Article  CAS  Google Scholar 

  • Shahidi F, Janitha PK, Wanasundara PD (1992) Phenolic antioxidants. Crit Rev Food Sci Nutr 32:67–103

    Article  CAS  Google Scholar 

  • Tu Y (2011) The discovery of artemisinin (qinghaosu) and gifts from Chinese medicine. Nat Med 17:1217–1220

    Article  CAS  Google Scholar 

  • Tuorkey MJ (2015) Cancer therapy with phytochemicals: present and future perspectives. Biomed Environ Sci 28:808–819

    Article  Google Scholar 

  • Wan XL, Niu Y, Zheng XC, Huang Q, Su WP, Zhang JF, Zhang LL, Wang T (2016a) Antioxidant capacities of Artemisia annua L. leaves and enzymatically treated Artemisia annua L. in vitro and in broilers. Anim Feed Sci Technol 221:27–34

    Article  CAS  Google Scholar 

  • Wan XL, Song ZH, Niu Y, Cheng K, Zhang JF, Ahmad H, Zhang LL, Wang T (2016b) Evaluation of enzymatically treated Artemisia annua L. on growth performance, meat quality, and oxidative stability of breast and thigh muscles in broilers. Poult Sci. doi:10.3382/ps/pew307

    Google Scholar 

  • Wang J, Zhu Q, Ahmad H, Zhang X, Wang T (2013) Combination of linseed and palm oils is a better alternative than single oil for broilers exposed to high environmental temperature. J Poult Sci 50:332–339

    Article  CAS  Google Scholar 

  • Windisch W, Schedle K, Plitzner C, Kroismayr A (2008) Use of phytogenic products as feed additives for swine and poultry. J Anim Sci 86:140–148

    Article  Google Scholar 

  • Yang H, Chowdhury VS, Bahry MA, Tran PV, Do PH, Han G, Zhang R, Tagashira H, Tsubata M, Furuse M (2016) Chronic oral administration of pine bark extract (flavangenol) attenuates brain and liver mRNA expressions of HSPs in heat-exposed chicks. J Therm Biol 60:140–148

    Article  CAS  Google Scholar 

  • Zhang JF, Hu ZP, Lu CH, Yang MX, Zhang LL, Wang T (2015a) Dietary curcumin supplementation protects against heat-stress-impaired growth performance of broilers possibly through a mitochondrial pathway. J Anim Sci 93:1656–1665

    Article  CAS  Google Scholar 

  • Zhang J, Hu Z, Lu C, Bai K, Zhang L, Wang T (2015b) Effect of various levels of dietary curcumin on meat quality and antioxidant profile of breast muscle in broilers. J Agric Food Chem 63:3880–3886

    Article  CAS  Google Scholar 

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Correspondence to Tian Wang.

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The animal research procedures in the present study were approved by Institutional Animal Care and Use Committee of Nanjing Agricultural University (Nanjing, P. R. China).

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Wan, X., Zhang, J., He, J. et al. Dietary enzymatically treated Artemisia annua L. supplementation alleviates liver oxidative injury of broilers reared under high ambient temperature. Int J Biometeorol 61, 1629–1636 (2017). https://doi.org/10.1007/s00484-017-1341-1

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  • DOI: https://doi.org/10.1007/s00484-017-1341-1

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