Comparative effects of n-hexane and methanol extracts of elecampane (Inula helenium L.) rhizome on growth performance, carcass traits, feed digestibility, intestinal antioxidant status and ileal microbiota in broiler chickens

References

• Abu Bakar MF, Mohamed M, Rahmat A, Fry J. 2009. Phytochemicals and antioxidant activity of different parts of bambangan (Mangifera pajang) and tarap (Artocarpus odoratissimus). Food Chem. 113:479–483.
   Google Scholar
• Aguiar VF, Donoghue AM, Arsi K, Reyes-Herrera I, Metcalf JH, de los Santos FS, Blore PJ, Donoghue DJ. 2013. Targeting motility properties of bacteria in the development of probiotic cultures against Campylobacter jejuni in broiler chickens. Foodborne Pathog Dis. 10:435–441.
   Google Scholar
• Albayrak S, Cinar AK, Paksoy MY, Aksoy A. 2015. An investigation on antioxidant and antimicrobial activities of four Inula helenium L. taxa. Iran J Sci Technol. 39:473–483.
   Google Scholar
• Alfaro DM, Silva AVF, Borges SA, Maiorka FA, Vargas S, Santin E. 2007. Use of Yucca schidigera extract in broiler diets and its effects on performance results obtained with different coccidiosis control methods. J Appl Poult Res. 16:248–254.
   Google Scholar
• Amerah AM, van Rensburg CJ, Plumstead PW, Kromm C, Dunham S. 2012. Effect of feeding diets containing a probiotic or antibiotic on broiler performance, intestinal mucosa-associated avian pathogenic E. coli and litter water-soluble phosphorus. J Appl Anim Nutr. 1:e7.
   Google Scholar
• AOAC. 2000. Official methods of analysis of AOAC international. 17th ed. Arlington (VA): Association of Official Analytical Chemists.
   Google Scholar
• Aviagen. 2014a. Ross 308 broiler nutrition specifications [Internet]. Newbridge (UK): Aviagen Ltd; [accessed 2016 Apr 27]. http://en.aviagen.com/.
   Google Scholar
• Aviagen. 2014b. Ross broiler management handbook [Internet]. Newbridge (UK): Aviagen Ltd; [accessed 2016 Apr 27]. http://en.aviagen.com/.
   Google Scholar
• Banerjee S, Mukhopadhayay SK, Ganguly S. 2013. Phytogenic growth promoter as replacers for antibiotic growth promoter in poultry birds. J Anim Genet Res. 1:6–7.
   Google Scholar
• Baurhoo B, Ferket PR, Zhao X. 2009. Effects of diets containing different concentrations of mannanoligosaccharide or antibiotics on growth performance, intestinal development, cecal and litter microbial populations, and carcass parameters of broilers. Poult Sci. 88:2262–2272.
   Google Scholar
• Boudouda HB, Kabouche A, Aburjai T, Kabouche Z. 2013. GC-MS analysis of Inula graveolens (L.) Desf. from Algeria. J Essent Oil Bear Plant. 16:651–654.
   Google Scholar
• Bourrel C, Vilarem G, Perineau F. 1993. Chemical analysis, bacteriostatic and fungistatic properties of the essential oil of elecampane (Inula helenium L.). J Essent Oil Res. 5:411–417.
   Google Scholar
• Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72:248–254.
   Google Scholar
• Buege JA, Aust SD. 1978. Microsomal lipid peroxidation. Methods Enzymol. 52:302–310.
   Google Scholar
• Cao W, Liu G, Fang T, Wu X, Jia G, Zhao H, Chen X, Wu C, Wang J, Cai J. 2015. Effects of spermine on the morphology, digestive enzyme activities, and antioxidant status of jejunum in suckling rats. RSC Adv. 5:76607–76614.
   Google Scholar
• Cobaxin-Cárdenas ME. 2018. Natural compounds as an alternative to control farm diseases: avian coccidiosis. In: Quiroz-Castañeda RE, editor. Farm animals diseases, recent omic trends and new strategies of treatment. [place unknown]: IntechOpen; p. 135–149.
   Google Scholar
• Cook RH, Bird FH. 1973. Duodenal villus area and epithelial cellular migration in conventional and germ-free chicks. Poult Sci. 52:2276–2280.
   Google Scholar
• Dhama K, Latheef SK, Mani S, Samad HA, Karthik K, Tiwari R, Khan RU, Alagawany M, Farag MR, Alam GM, et al. 2015. Multiple beneficial applications and modes of action of herbs in poultry health and production-a review. Int J Pharmacol. 11:152–176.
   Google Scholar
• Dieumou FE, Teguia A, Kuiate JR, Tamokou JD, Doma UD, Abdullahi US, Chiroma AE. 2011. Effect of supplemented diets with garlic organic extract and streptomycin sulphate on intestinal microflora and nutrients digestibility in broilers. Online J Anim Feed Res. 1:107–113.
   Google Scholar
• Divani A, Bagherzadeh‐Kasmani F, Mehri M. 2018. Plantago ovata in broiler chicken nutrition: performance, carcass criteria, intestinal morphology, immunity, and intestinal bacterial population. J Anim Physiol Anim Nutr. 102:e353–e363.
   Google Scholar
• Eriksson UJ, Borg LAH. 1991. Protection by free oxygen radical scavenging enzymes against glucose-induced embryonic malformations in vitro. Diabetologia. 34:325–331.
   Google Scholar
• Fallahzadeh AR, Mohammadi S. 2016. An investigation of the antinociceptive and anti-inflammatory effects of hydroalcoholic extract of Inula helenium on male rats. J Babol Univ Med Sci. 18:57–63.
   Google Scholar
• Fenton TW, Fenton M. 1979. An improved procedure for the determination of chromic oxide in feed and feces. Can J Anim Sci. 59:631–634.
   Google Scholar
• Flohé L, Günzler WA. 1984. Assays of glutathione peroxidase. Methods Enzymol. 105:114–120.
   Google Scholar
• García V, Catalá-Gregori P, Hernández F, Megías MD, Madrid J. 2007. Effect of formic acid and plant extracts on growth, nutrient digestibility, intestine mucosa morphology, and meat yield of broilers. J Appl Poult Res. 16:555–562.
   Google Scholar
• Giannenas I, Tsalie E, Chronis EF, Mavridis S, Tontis D, Kyriazakis I. 2011. Consumption of Agaricus bisporus mushroom affects the performance, intestinal microbiota composition and morphology, and antioxidant status of turkey poults. Anim Feed Sci Technol. 165:218–229.
   Google Scholar
• Gökbulut A, Özhan O, Satılmış B, Batçıoğlu K, Günal S, Şarer E. 2013. Antioxidant and antimicrobial activities and phenolic compounds of selected Inula species from Turkey. Nat Prod Commun. 8:475–478.
   Google Scholar
• Gong Y, Toivonen PM, Lau OL, Wiersma PA. 2001. Antioxidant system level in ‘Braeburn’ apple is related to its browning disorder. Bot Bull Acad Sin. 42:259–264.
   Google Scholar
• Gu XH, Hao Y, Wang XL. 2012. Overexpression of heat shock protein 70 and its relationship to intestine under acute heat stress in broilers: 2. Intestinal oxidative stress. Poult Sci. 91:790–799.
   Google Scholar
• Habibian M, Sadeghi G, Karimi A. 2019. Comparative effects of powder, aqueous and methanolic extracts of purslane (Portulaca oleracea L.) on growth performance, antioxidant status, abdominal fat deposition and plasma lipids in broiler chickens. Anim Prod Sci. 59:89–100.
   Google Scholar
• Hamady GA, Abdel-Moneim MA, El-Sherbiny MA, El-Shinnawy AM, Motawe HF, El-Chaghaby GA. 2017. Chamomile flower extract as natural dietary growth promoter and antioxidant for broiler chickens. J Anim Plant Sci. 27:1479–1487.
   Google Scholar
• Hashemi SR, Davoodi H. 2012. Herbal plants as new immuno-stimulator in poultry industry: a review. Asian J Anim Vet Adv. 7:105–116.
   Google Scholar
• Hernández F, Madrid J, García V, Orengo J, Megías MD. 2004. Influence of two plant extracts on broilers performance, digestibility, and digestive organ size. Poult Sci. 83:169–174.
   Google Scholar
• Huo Y, Shi H, Li W, Wang M, Li X. 2010. HPLC determination and NMR structural elucidation of sesquiterpene lactones in Inula helenium. J Pharm Biomed Anal. 51:942–946.
   Google Scholar
• Jamroz D, Orda J, Kamel C, Wiliczkiewicz A, Wertelecki T, Skorupinska J. 2003. The influence of phytogenic extracts on performance, nutrient digestibility, carcass characteristics, and gut microbial status in broiler chickens. J Anim Feed Sci. 12:583–596.
   Google Scholar
• Jung KA, Choi BH, Kwak MK. 2015. The c-MET/PI3K signaling is associated with cancer resistance to doxorubicin and photodynamic therapy by elevating BCRP/ABCG2 expression. Pharmacol. 87:465-476.
   Google Scholar
• Karásková K, Suchy P, Strakova E. 2015. Current use of phytogenic feed additives in animal nutrition: a review. Czech J Anim Sci. 60:521–530.
   Google Scholar
• Kataoka M, Hirata K, Kunikata T, Ushio S, Iwaki K, Ohashi K, Ikeda M, Kurimoto M. 2001. Antibacterial action of tryptanthrin and kaempferol, isolated from the indigo plant (Polygonum tinctorium Lour.), against helicobacter pylori-infected Mongolian gerbils. J Gastroenterol. 36:5–9.
   Google Scholar
• Katerere DR, Naidoo V. 2010. Herbal medicines for pet and companion animals. In: Katerere DR, Luseba D, editors. Ethnoveterinary botanical medicine: herbal medicines for animal health. Boca Raton (FL): CRC Press; p. 389–408.
   Google Scholar
• Khalaji S, Zaghari M, Hatami KH, Hedari-Dastjerdi S, Lotfi L, Nazarian H. 2011. Black cumin seeds, Artemisia leaves (Artemisia sieberi), and Camellia L. plant extract as phytogenic products in broiler diets and their effects on performance, blood constituents, immunity, and cecal microbial population. Poult Sci. 90:2500–2510.
   Google Scholar
• Kiczorowska B, Al-Yasiry ARM, Samolińska W, Marek A, Pyzik E. 2016. The effect of dietary supplementation of the broiler chicken diet with Boswellia serrata resin on growth performance, digestibility, and gastrointestinal characteristics, morphology, and microbiota. Livest Sci. 191:117–124.
   Google Scholar
• Kyslychenko AA, Fedosov AI, Dorovskyy OV, Sahaidak-Nikitiuk RV. 2015. The economic substantiation for production of gastric teas as promising medicines for treating gastro-intestinal tract diseases. Vìsn Farm. 4:31–36.
   Google Scholar
• Lee JY, Kim SB, Chun J, Song KH, Kim YS, Chung SJ, Cho HJ, Yoon IS, Kim DD. 2016. High body clearance and low oral bioavailability of alantolactone, isolated from Inula helenium, in rats: extensive hepatic metabolism and low stability in gastrointestinal fluids. Biopharm Drug Dispos. 37:156–167.
   Google Scholar
• Levkut M, Marcin A, Revajová V, Lenhardt L, Danielovič I, Hecl J, Blanár J, Levkutová M, Pistl J. 2011. Influence of oregano extract on the intestine, some plasma parameters and growth performance in chickens. Act Vet. 61:215–225.
   Google Scholar
• Marković R, Šefer D, Krstić M, Petrujkić B. 2009. Effect of different growth promoters on broiler performance and gut morphology. Arch Med Vet. 41:163–169.
   Google Scholar
• Martín A, Colín B, Aranda E, Benito MJ, Córdoba MG. 2007. Characterization of Micrococcaceae isolated from Iberian dry-cured sausages. Meat Sci. 75:696–708.
   Google Scholar
• Martin KW, Ernst E. 2003. Herbal medicines for treatment of bacterial infections: a review of controlled clinical trials. J Antimicrob Chemother. 51:241–246.
   Google Scholar
• Mirakzehi MT, Hosseini SJ, Saleh H. 2017. The effects of hydroalcoholic extracts of Withania somnifera root, Withania coagulans fruit and 1, 25-dihydroxycholecalciferol on immune response and small intestinal morphology of broiler chickens. J Appl Anim Res. 45:591–597.
   Google Scholar
• Mueller K, Blum NM, Kluge H, Mueller AS. 2012. Influence of broccoli extract and various essential oils on performance and expression of xenobiotic-and antioxidant enzymes in broiler chickens. Br J Nutr. 108:588–602.
   Google Scholar
• Nagarani G, Abirami A, Nikitha P, Siddhuraju P. 2014. Effect of hydrothermal processing on total polyphenolics and antioxidant potential of underutilized leafy vegetables, Boerhaavia diffusa and Portulaca oleracea. Asian Pac J Trop Biomed. 4:S468–S477.
   Google Scholar
• Orhan N, Gökbulut A, Orhan DD. 2017. Antioxidant potential and carbohydrate digestive enzyme inhibitory effects of five Inula species and their major compounds. South Afr J Botany. 111:86–92.
   Google Scholar
• Park EJ, Kim YM, Park SW, Kim HJ, Lee JH, Lee DU, Chang KC. 2013. Induction of HO-1 through p38 MAPK/Nrf2 signaling pathway by ethanol extract of Inula helenium L. reduces inflammation in LPS-activated RAW 264.7 cells and CLP-induced septic mice. Food Chem Toxicol. 55:386–395.
   Google Scholar
• Paymard J, Nobakht A, Mazlum F, Moghaddam M. 2013. The effects of different levels of dried aerial parts powder and extract of pennyroyal (Mentha pulegium) medicinal plant on performance, egg quality, blood biochemical and immunity parameters of laying hens. Iran J Appl Anim Sci. 3:589–594.
   Google Scholar
• Petkova N, Vrancheva R, Mihaylova D, Ivanov I, Pavlov A, Denev P. 2015. Antioxidant activity and fructan content in root extracts from elecampane (Inula helenium L.). J BioSci Biotechnol. 4:101–107.
   Google Scholar
• Petzke KJ, Schuppe S, Rohn S, Rawel HM, Kroll J. 2005. Chlorogenic acid moderately decreases the quality of whey proteins in rats. J Agric Food Chem. 53:3714–3720.
   Google Scholar
• Ramos FA, Takaishi Y, Shirotori M, Kawaguchi Y, Tsuchiya K, Shibata H, Higuti T, Tadokoro T, Takeuchi M. 2006. Antibacterial and antioxidant activities of quercetin oxidation products from yellow onion (Allium cepa) skin. J Agric Food Chem. 54:3551–3557.
   Google Scholar
• Richters. 2015. Herb and vegetable catalogue [Internet]. Goodwood (Canada): Otto Richter and Sons Ltd; [accessed 2018 Jun 4]. https://www.richters.com/.
   Google Scholar
• Rohn S, Petzke KJ, Rawel HM, Kroll J. 2006. Reactions of chlorogenic acid and quercetin with a soy protein isolate–influence on the in vivo food protein quality in rats. Mol Nutr Food Res. 50:696–704.
   Google Scholar
• Samuel KG, Wang J, Yue HY, Wu SG, Zhang HJ, Duan ZY, Qi GH. 2017. Effects of dietary gallic acid supplementation on performance, antioxidant status, and jejunum intestinal morphology in broiler chicks. Poult Sci. 96:2768–2775.
   Google Scholar
• Segelman AB, inventor; Natures Sunshine Products Inc., assignee. 2001 Feb 13. Composition and method for treating and preventing Helicobactor-pylori-associated stomach gastritis, ulcers and cancer. United States patent US 6,187,313.
   Google Scholar
• Seo JY, Lim SS, Kim JR, Lim JS, Ha YR, Lee IA, Kim EJ, Park JHY, Kim JS. 2008. Nrf2-mediated induction of detoxifying enzymes by alantolactone present in Inula helenium. Phytother Res. 22:1500–1505.
   Google Scholar
• Seo JY, Park J, Kim HJ, Lee IA, Lim JS, Lim SS, Choi SJ, Park JHY, Kang HJ, Kim JS. 2009. Isoalantolactone from Inula helenium caused Nrf2-mediated induction of detoxifying enzymes. J Med Food. 12:1038–1045.
   Google Scholar
• Shanmugam B, Shanmugam KR, Ravi S, Subbaiah GV, Mallikarjuna K, Reddy KS. 2014. Antibacterial activity and phytochemical screening of Phyllanthus niruri in ethanolic, methanolic and aqueous extracts. Int J Pharmaceut Sci Rev Res. 27:85–89.
   Google Scholar
• Son DJ, Lee SE, Park BS. 2003. Inhibitory effects of naturally occurring flavonoids on a human intestinal bacterium, Clostridium perfringens. Food Sci Biotechnol. 12:180–182.
   Google Scholar
• Sowndhararajan K, Cho H, Yu B, Song J, Kim S. 2016. Effect of inhalation of essential oil from Inula helenium L. root on electroencephalographic (EEG) activity of the human brain. Eur J Integr Med. 8:453–457.
   Google Scholar
• Spiridon I, Bodirlau R, Teaca CA. 2011. Total phenolic content and antioxidant activity of plants used in traditional Romanian herbal medicine. Open Life Sci. 6:388–396.
   Google Scholar
• Spiridon I, Nechita C, Niculaua M, Silion M, Armatu A, Teacă CA, Bodîrlău R. 2013. Antioxidant and chemical properties of Inula helenium root extracts. Open Chem. 11:1699–1709.
   Google Scholar
• Squires S, Fisher M, Gladstone O, Rogerson S, Martin P, Martin S, Lester H, Sygall R, Underwood N. 2012. Comparative efficacy of flubendazole and a commercially available herbal wormer against natural infections of Ascaridia galli, Heterakis gallinarum and intestinal Capillaria spp. in chickens. Vet Parasitol. 185:352–354.
   Google Scholar
• Stef L, Dumitrescu G, Drinceanu D, Stef D, Mot D, Julean C, Tatileanu R, Corcionivoschi N. 2009. The effect of medicinal plants and plant extracted oils on broiler duodenum morphology and immunological profile. Roman Biotechnol Lett. 14:4606–4614.
   Google Scholar
• Stojanović-Radić Z, Čomić L, Radulović N, Blagojević P, Denić M, Miltojević A, Rajković J, Mihajilov-Krstev T. 2012. Antistaphylococcal activity of Inula helenium L. root essential oil: eudesmane sesquiterpene lactones induce cell membrane damage. Eur J Clin Microbiol Infect Dis. 31:1015–1025.
   Google Scholar
• Tiwari M, Pandey A, Agrawal A, Dubey GP. 2014. Herbal sources of antibacterial potential: a review. World J Pharm Pharm Sci. 3:388–399.
   Google Scholar
• Todorov SD, Dicks LMT. 2005. Lactobacillus plantarum isolated from molasses produces bacteriocins active against gram-negative bacteria. Enzyme Microb Technol. 36:318–326.
   Google Scholar
• Tvrdá E, Lukáč N, Lukáčová J, Kňažická Z, Massányi P. 2013. Stimulating and protective effects of vitamin E on bovine spermatozoa. J Microbiol Biotechnol Food Sci. 2:1386–1395.
   Google Scholar
• Uni Z. 2006. Early development of small intestinal function. In: Perry GC, editor. Avian gut function in health and disease. Wallingford (UK): CABI Publishing; p. 29–42.
   Google Scholar
• Uni Z, Noy Y, Sklan D. 1995. Posthatch changes in morphology and function of the small intestines in heavy-and light-strain chicks. Poult Sci. 74:1622–1629.
   Google Scholar
• Urban J, Kokoska L, Langrova I, Matejkova J. 2008. In vitro anthelmintic effects of medicinal plants used in Czech Republic. Pharm Biol. 46:808–813.
   Google Scholar
• Váradyová Z, Kišidayová S, Čobanová K, Grešáková Ľ, Babják M, Königová A, Urda Dolinská M, Várady M. 2017. The impact of a mixture of medicinal herbs on ruminal fermentation, parasitological status and hematological parameters of the lambs experimentally infected with Haemonchus contortus. Small Ruminant Res. 151:124–132.
   Google Scholar
• Visek WJ. 1978. The mode of growth promotion by antibiotics. J Anim Sci. 46:1447–1469.
   Google Scholar
• Wang J, Zhao YM, Zhang B, Guo CY. 2015. Protective effect of total phenolic compounds from Inula helenium on hydrogen peroxide-induced oxidative stress in SH-SY5Y cells. Ind J Pharm Sci. 77:163–169.
   Google Scholar
• Wang L, Piao XL, Kim SW, Piao XS, Shen YB, Lee HS. 2008. Effects of Forsythia suspensa extract on growth performance, nutrient digestibility, and antioxidant activities in broiler chickens under high ambient temperature. Poult Sci. 87:1287–1294.
   Google Scholar
• Wang XH, Dai JT. 2012. Research on scavenging effect of Chinese herbal medicine extractive on hydroxyl free radical by photometry. Chin J Spect Lab. 27:1756–1758.
   Google Scholar
• Willis WL, King K, Iskhuemhen OS, Ibrahim SA. 2009. Administration of mushroom extract to broiler chickens for bifidobacteria enhancement and Salmonella reduction. J Appl Poult Res. 18:658–664.
   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.
   Google Scholar
• Wu Y, Zhou Y, Lu C, Ahmad H, Zhang H, He J, Zhang L, Wang T. 2016. Influence of butyrate loaded clinoptilolite dietary supplementation on growth performance, development of intestine and antioxidant capacity in broiler chickens. PLoS One. 11:e0154410.
   Google Scholar
• Yao L, Jiang Y, Datta N, Singanusong R, Liu X, Duan J, Raymont K, Lisle A, Xu Y. 2004. HPLC analyses of flavanols and phenolic acids in the fresh young shoots of tea (Camellia sinensis) grown in Australia. Food Chem. 84:253–263.
   Google Scholar
• Yason CV, Summers BA, Schat KA. 1987. Pathogenesis of rotavirus infection in various age groups of chickens and turkeys: pathology. Am J Vet Res. 48:927–938.
   Google Scholar
• Youn HJ, Noh JW. 2001. Screening of the anticoccidial effects of herb extracts against Eimeria tenella. Vet Parasitol. 96:257–263.
   Google Scholar
• Youssef MS, Saber SM, Hassane AMA, Arafa RF. 2015. Evaluation of antibacterial activities of some egyptian medicinal plant extracts. J Eco Heal Env. 3:49–57.
   Google Scholar
• Zhang XH, Sun ZY, Cao FL, Ahmad H, Yang XH, Zhao LG, Wang T. 2015. Effects of dietary supplementation with fermented ginkgo leaves on antioxidant capacity, intestinal morphology and microbial ecology in broiler chicks. Br Poult Sci. 56:370–380.
   Google Scholar
• Zou Y, Wei HK, Xiang QH, Wang J, Zhou YF, Peng J. 2016. Protective effect of quercetin on pig intestinal integrity after transport stress is associated with regulation oxidative status and inflammation. J Vet Med Sci. 78:1487–1494.
   Google Scholar