Medicinal Plants for Prophylaxis and Therapy of Common Infectious Diseases In Poultry–A Systematic Review of In Vivo Studies

Abstract

Medicinal plants for prophylaxis and therapy of common infectious diseases in poultry have been studied for several years. The goal of this review was to systematically identify plant species and evaluate their potential in prophylaxis and therapy of common diseases in poultry caused by bacteria and gastrointestinal protozoa. The procedure followed the recommendations of the PRISMA statement and the AMSTAR measurement tool. The PICOS scheme was used to design the research questions. Two databases were consulted, and publications were manually selected, according to predefined in- and exclusion criteria. A scoring system was established to evaluate the remaining publications. Initially, 4197 identified publications were found, and 77 publications remained after manual sorting, including 38 publications with 70 experiments on bacterial infections and 39 publications with 78 experiments on gastrointestinal protozoa. In total, 83 plant species from 42 families were identified. Asteraceae and Lamiaceae were the most frequently found families with Artemisia annua being the most frequently found plant, followed by Origanum vulgare. As compared to placebo and positive or negative control groups, antimicrobial effects were found in 46 experiments, prebiotic effects in 19 experiments, and antiprotozoal effects in 47 experiments. In summary, a total of 274 positive effects predominated over 241 zero effects and 37 negative effects. Data indicate that O. vulgare, Coriandrum sativum, A. annua, and Bidens pilosa are promising plant species for prophylaxis and therapy of bacterial and protozoal diseases in poultry.

Key words

broiler - laying hen - bacterial infections - protozoal infections - phytotherapy - phytogenic feed additive - literature review - Origanum vulgare (Lamiaceae) - Coriandrum sativum (Apiacea) - Artemisia annua - Bidens pilosa (Asteraceae)

Publikationsverlauf

Eingereicht: 17. März 2021

Angenommen nach Revision: 29. Juni 2021

Artikel online veröffentlicht:
06. August 2021

• References

• 1 Alexandratos N, Bruinsma J. World Agriculture Towards 2030/2050: The 2012 Revision. Rome: Food and Agriculture Organization of the United Nations; 2012
• 2 Lutful Kabir SM. Avian colibacillosis and salmonellosis: a closer look at epidemiology, pathogenesis, diagnosis, control and public health concerns. Int J Environ Res Public Health 2010; 7: 89-114
• 3 Blake DP, Tomley FM. Securing poultry production from the ever-present Eimeria challenge. Trends Parasitol 2014; 30: 12-19
• 4 Noack S, Chapman HD, Selzer PM. Anticoccidial drugs of the livestock industry. Parasitol Res 2019; 118: 2009-2026
• 5 European Medicines Agency. Sales of veterinary antimicrobial agents in 31 European countries in 2017. 2019. Accessed July 20, 2021 at: http://www.ema.europa.eu/en/documents/report/sales-veterinary-antimicrobial-agents-31-european-countries-2017_en.pdf
• 6 Boovaragamoorthy GM, Anbazhagan M, Piruthiviraj P, Pugazhendhi A, Kumar SS, Al-Dhabi NA, Mohammed Ghilan AK, Arasu MV, Kaliannan T. Clinically important microbial diversity and its antibiotic resistance pattern towards various drugs. J Infect Public Health 2019; 12: 783-788
• 7 Lan LH, Sun BB, Zuo BX, Chen XQ, Du AF. Prevalence and drug resistance of avian Eimeria species in broiler chicken farms of Zhejiang province, China. Poult Sci 2017; 96: 2104-2109
• 8 Schwarz A, Loeffler S, Kadlec K. Bacterial resistance to antimicrobial agents and its impact on veterinary and human medicine. Vet Dermatol 2017; 28: 82-e19
• 9 Roth N, Käsbohrer A, Mayrhofer S, Zitz U, Hofacre C, Domig KJ. The application of antibiotics in broiler production and the resulting antibiotic resistance in Escherichia coli: A global overview. Poult Sci 2019; 98: 1791-1804
• 10 Peek HW, Landman WJ. Coccidiosis in poultry: anticoccidial products, vaccines and other prevention strategies. Vet Q 2011; 31: 143-161
• 11 European Union. Regulation (EC) No 1831/2003 of the European Parliament and of the council of 22 September 2003 on additives for use in animal nutrition. OJEU 2003. Accessed July 20, 2021 at: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32003R1831&from=en
• 12 Institute of Veterinary Pharmacology and Toxicology Zurich. CliniPharm CliniTox. 2019. Accessed November 7, 2019 at: https://www.vetpharm.uzh.ch/cpthome.htm
• 13 Williams RB. Intercurrent coccidiosis and necrotic enteritis of chickens: rational, integrated disease management by maintenance of gut integrity. Avian Pathol 2005; 34: 159-180
• 14 Saif YM. Diseases of Poultry. Vol. 11. Ames, Iowa: Iowa State University Press; 2003
• 15 Ojimelukwe AE, Emedhem DE, Agu GO, Nduka FO, Abah AE. Populations of Eimeria tenella express resistance to commonly used anticoccidial drugs in southern Nigeria. Int J Vet Sci Med 2018; 6: 192-200
• 16 Disler M, Ivemeyer S, Hamburger M, Vogl CR, Tesic A, Klarer F, Meier B, Walkenhorst M. Ethnoveterinary herbal remedies used by farmers in four north-eastern Swiss cantons (St. Gallen, Thurgau, Appenzell Innerrhoden and Appenzell Ausserrhoden). J Ethnobiol Ethnomed 2014; 10: 32
• 17 Mayer M, Zbinden M, Vogl CR, Ivemeyer S, Meier B, Amorena M, Maeschli A, Hamburger M, Walkenhorst M. Swiss ethnoveterinary knowledge on medicinal plants–a within–country comparison of Italian speaking regions with north-western German speaking regions. J Ethnobiol Ethnomed 2017; 13: 1
• 18 Schmid K, Ivemeyer S, Vogl C, Klarer F, Meier B, Hamburger M, Walkenhorst M. Traditional use of herbal remedies in livestock by farmers in 3 Swiss cantons (Aargau, Zurich, Schaffhausen). Forsch Komplementmed 2012; 19: 125-136
• 19 Mertenat D, Cero MD, Vogl CR, Ivemeyer S, Meier B, Maeschli A, Hamburger M, Walkenhorst M. Ethnoveterinary knowledge of farmers in bilingual regions of Switzerland–Is there potential to extend veterinary options to reduce antimicrobial use?. J Ethnopharmacol 2020; 246: 112184
• 20 Bischoff T, Vogl CR, Ivemeyer S, Klarer F, Meier B, Hamburger H, Walkenhorst M. Plant and natural product based homemade remedies manufactured and used by farmers of six central Swiss cantons to treat livestock. Livest Sci 2016; 189: 110-125
• 21 Mayer M, Vogl CR, Amorena M, Hamburger M, Walkenhorst M. Treatment of organic livestock with medicinal plants: a systematic review of European ethnoveterinary research. Forsch Komplementarmed 2014; 21: 12
• 22 Brendieck-Worm C, Melzig MF. Phytotherapie in der Tiermedizin. Leipzig, New York: Thieme; 2018
• 23 Reichling J, Frater-Schröder M, Saller R, Fitzi-Rathgen J, Gachnian-Mirtscheva R. Heilpflanzenkunde für die Veterinärpraxis. 3 ed. Berlin: Springer; 2016
• 24 Ayrle H, Mevissen M, Kaske M, Nathues H, Gruetzner N, Melzig M, Walkenhorst M. Medicinal plants–prophylactic and therapeutic options for gastrointestinal and respiratory diseases in calves and piglets? A systematic review. BMC Vet Res 2016; 12: 89
• 25 Hashemi SR, Davoodi H. Phytogenics as new class of feed additive in poultry industry. J Anim Vet Adv 2010; 9: 2295-2304
• 26 Gadde U, Kim WH, Oh ST, Lillehoj HS. Alternatives to antibiotics for maximizing growth performance and feed efficiency in poultry: a review. Anim Health Res Rev 2017; 18: 26-45
• 27 Wallace RJ, Oleszek W, Franz C, Hahn I, Baser KH, Mathe A, Teichmann K. Dietary plant bioactives for poultry health and productivity. Br Poult Sci 2010; 51: 461-487
• 28 Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. Plos Medicine 2009; 6
• 29 Moher D, Liberati A, Tetzlaff J, Altman DG. PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 2009; 62: 1006-1012
• 30 Shea BJ, Grimshaw JM, Wells GA, Boers M, Andersson N, Hamel C, Porter AC, Tugwell P, Moher D, Bouter LM. Development of AMSTAR: a measurement tool to assess the methodological quality of systematic reviews. Bmc Med Res Methodol 2007; 7: 10
• 31 Accessed February 1, 2018 at: http://www.webofscience.com/wos/woscc/basic-search
• 32 Accessed February 1, 2019 at: https://pubmed.ncbi.nlm.nih.gov/
• 33 Accessed November 15, 2020 at: http://theplantlist.org/
• 34 Figueiredo AC, Barroso JG, Pedro LG, Scheffer JJC. Factors affecting secondary metabolite production in plants: volatile components and essential oils. Flavour Fragr J 2008; 23: 213-226
• 35 Ghasemi Pirbalouti A, Izadi A, Malek Poor F, Hamedi B. Chemical composition, antioxidant and antibacterial activities of essential oils from Ferulago angulata . Pharm Biol 2016; 54: 2515-2520
• 36 Bilia AR, Santomauro F, Sacco C, Bergonzi MC, Donato R. Essential oil of Artemisia annua L.: an extraordinary component with numerous antimicrobial properties. Evid Based Complement Alternat Med 2014; 2014: 159819
• 37 Ben Farhat M, Jordán MJ, Chaouech-Hamada R, Landoulsi A, Sotomayor JA. Variations in essential oil, phenolic compounds, and antioxidant activity of Tunisian cultivated Salvia officinalis L. J Agric Food Chem 2009; 57: 10349-10356
• 38 Chudnicka A, Matysik G. Research of enzymatic activities of fresh juice and water infusions from dry herbs. J Ethnopharmacol 2005; 99: 281-286
• 39 Qu H, Zhang Y, Wang Y, Li B, Sun W. Antioxidant and antibacterial activity of two compounds (forsythiaside and forsythin) isolated from Forsythia suspensa . J Pharm Pharmacol 2008; 60: 261-266
• 40 Salehi B, Albayrak S, Antolak H, Kręgiel D, Pawlikowska E, Sharifi-Rad M, Uprety Y, Tsouh Fokou PV, Yousef Z, Amiruddin Zakaria Z, Varoni EM, Sharopov F, Martins N, Iriti M, Sharifi-Rad J. Aloe genus plants: from farm to food applications and phytopharmacotherapy. Int J Mol Sci 2018; 19: 2843
• 41 Allen PC, Lydon J, Danforth HD. Effects of components of Artemisia annua on coccidia infections in chickens. Poult Sci 1997; 76: 1156-1163
• 42 Almeida GFD, Horsted H, Thamsborg SM, Hermansen JE. Strategies to Reduce Severity of Coccidia Infections in Organic Poultry Systems by the use of Plant Extracts. In: Rahmann G, Godinho D, eds. Tackling the Future Challenges of Organic Animal Husbandry. Proceedings of the 2nd OAHC. Hamburg/Trenthorst, Germany; 2012: 462-465
• 43 Casella S, Leonardi M, Melai B, Fratini F, Pistelli L. The role of diallyl sulfides and dipropyl sulfides in the in vitro antimicrobial activity of the essential oil of garlic, Allium sativum L., and Leek, Allium porrum L. Phytother Res 2013; 27: 380-383
• 44 Ankri S, Mirelman D. Antimicrobial properties of allicin from garlic. Microbes Infect 1999; 1: 125-129
• 45 Mariita RM, Orodho JA, Okemo PO, Kirimuhuzya C, Otieno JN, Magadula JJ. Methanolic extracts of Aloe secundiflora Engl. inhibits in vitro growth of tuberculosis and diarrhea-causing bacteria. Pharmacognosy Res 2011; 3: 95-99
• 46 Habeeb F, Shakir E, Bradbury F, Cameron P, Taravati MR, Drummond AJ, Gray AI, Ferro VA. Screening methods used to determine the anti-microbial properties of Aloe vera inner gel. Methods 2007; 42: 315-320
• 47 Mohamed TA, Hegazy MF, Abd El Aty AA, Ghabbour HA, Alsaid MS, Shahat AA, Paré PW. Antimicrobial sesquiterpene lactones from Artemisia sieberi . J Asian Nat Prod Res 2017; 19: 1093-1101
• 48 Gupta D, Kumar M. Evaluation of in vitro antimicrobial potential and GC-MS analysis of Camellia sinensis and Terminalia arjuna. Biotechnol Rep (Amst) 2017; 13: 19-25
• 49 Brochot A, Guilbot A, Haddioui L, Roques C. Antibacterial, antifungal, and antiviral effects of three essential oil blends. Microbiologyopen 2017; 6
• 50 Prabuseenivasan S, Jayakumar M, Ignacimuthu S. In vitro antibacterial activity of some plant essential oils. BMC Complement Altern Med 2006; 6: 39
• 51 Sharifi-Rad M, Mnayer D, Morais-Braga MFB, Carneiro JNP, Bezerra CF, Coutinho HDM, Salehi B, Martorell M, Del Mar Contreras M, Soltani-Nejad A, Uribe YAH, Yousaf Z, Iriti M, Sharifi-Rad J. Echinacea plants as antioxidant and antibacterial agents: from traditional medicine to biotechnological applications. Phytother Res 2018; 32: 1653-1663
• 52 Tardugno R, Pellati F, Serio A, Paparella A, Benvenuti S. Phytochemical composition and in vitro antimicrobial activity of selected essential oils on foodborne pathogens. Abstracts of Papers of the American Chemical Society 2015; 249
• 53 Gericke S, Lübken T, Wolf D, Kaiser M, Hannig C, Speer K. Identification of new compounds from sage flowers (Salvia officinalis L.) as markers for quality control and the influence of the manufacturing technology on the chemical composition and antibacterial activity of sage flower extracts. J Agric Food Chem 2018; 66: 1843-1853
• 54 Arshad N, Zitterl-Eglseer K, Hasnain S, Hess M. Effect of Peganum harmala or its beta-carboline alkaloids on certain antibiotic resistant strains of bacteria and protozoa from poultry. Phytother Res 2008; 22: 1533-1538
• 55 Tabari MA, Youssefi MR, Moghadamnia AA. Antitrichomonal activity of Peganum harmala alkaloid extract against trichomoniasis in pigeon (Columba livia domestica). Br Poult Sci 2017; 58: 236-241
• 56 Vasconcelos NG, Croda J, Simionatto S. Antibacterial mechanisms of cinnamon and its constituents: a review. Microb Pathog 2018; 120: 198-203
• 57 Deryabin D, Galadzhieva A, Kosyan D, Duskaev G. Plant-derived inhibitors of AHL-mediated quorum sensing in bacteria: modes of action. Int J Mol Sci 2019; 20: 5588
• 58 Nazzaro F, Fratianni F, Coppola R. Quorum sensing and phytochemicals. Int J Mol Sci 2013; 14: 12607-12619
• 59 Naegeli H, Mevissen M, Walkenhorst M, Ayrle H, Kupper J. Recent challenges in veterinary pharmacotherapy–could medicinal plants be an option?. In: 65th International Congress and Annual Meeting of the Society for Medicinal Plant and Natural Product Research. PMIO; 2017. 4(Suppl 1). S1-S202 DOI: 10.1055/s-0037-1608012
• 60 Manning TS, Gibson GR. Microbial-gut interactions in health and disease. Prebiotics. Best Pract Res Clin Gastroenterol 2004; 18: 287-298
• 61 Pan D, Yu Z. Intestinal microbiome of poultry and its interaction with host and diet. Gut Microbes 2014; 5: 108-119
• 62 Choct M. Managing gut health through nutrition. Br Poult Sci 2009; 50: 9-15
• 63 Engberg RM, Grevsen K, Ivarsen E, Fretté X, Christensen LP, Højberg O, Jensen BB, Canibe N. The effect of Artemisia annua on broiler performance, on intestinal microbiota and on the course of a Clostridium perfringens infection applying a necrotic enteritis disease model. Avian Pathol 2012; 41: 369-376
• 64 de Almeida GF, Horsted K, Thamsborg SM, Kyvsgaard NC, Ferreira JF, Hermansen JE. Use of Artemisia annua as a natural coccidiostat in free-range broilers and its effects on infection dynamics and performance. Vet Parasitol 2012; 186: 178-187
• 65 Thøfner IC, Liebhart D, Hess M, Schou TW, Hess C, Ivarsen E, Fretté XC, Christensen LP, Grevsen K, Engberg RM, Christensen JP. Antihistomonal effects of artemisinin and Artemisia annua extracts in vitro could not be confirmed by in vivo experiments in turkeys and chickens. Avian Pathol 2012; 41: 487-496
• 66 Drăgan L, Györke A, Ferreira JF, Pop IA, Dunca I, Drăgan M, Mircean V, Dan I, Cozma V. Effects of Artemisia annua and Foeniculum vulgare on chickens highly infected with Eimeria tenella (Phylum Apicomplexa). Acta Vet Scand 2014; 56: 22
• 67 Loo CS, Lam NS, Yu D, Su XZ, Lu F. Artemisinin and its derivatives in treating protozoan infections beyond malaria. Pharmacol Res 2017; 117: 192-217
• 68 Wang SH, Hu YL, Liu TX. Plant distribution and pharmacological activity of flavonoids. Tradit Chin Med 2019; 4: 269-287
• 69 Talman AM, Clain J, Duval R, Ménard R, Ariey F. Artemisinin bioactivity and resistance in Malaria parasites. Trend Parasitol 2019; 35: 953-963
• 70 Arab HA, Rahbari S, Rassouli A, Moslemi MH, Khosravirad F. Determination of artemisinin in Artemisia sieberi and anticoccidial effects of the plant extract in broiler chickens. Trop Anim Health Prod 2006; 38: 497-503
• 71 Yao WB, Wang F, Wang H. Immunomodulation of artemisinin and its derivatives. Science Bulletin 2016; 61: 1399-1406
• 72 Tariq H, Zia M, Ihsan-Ul-Haq. Muhammad SA, Khan SA, Fatima N, Mannan A, Abbasi AM, Zhang M. Antioxidant, antimicrobial, cytotoxic, and protein kinase inhibition potential in Aloe vera L. Biomed Res Int 2019; 2019: 6478187
• 73 Kumar R, Singh AK, Gupta A, Bishayee A, Pandey AK. Therapeutic potential of Aloe vera–a miracle gift of nature. Phytomedicine 2019; 60: 152996
• 74 Radha MH, Laxmipriya NP. Evaluation of biological properties and clinical effectiveness of Aloe vera: a systematic review. J Tradit Complement Med 2015; 5: 21-26
• 75 Harlev E, Nevo E, Lansky EP, Ofir R, Bishayee A. Anticancer potential of aloes: antioxidant, antiproliferative, and immunostimulatory attributes. Planta Med 2012; 78: 843-852
• 76 Djeraba A, Quere P. In vivo macrophage activation in chickens with Acemannan, a complex carbohydrate extracted from Aloe vera . Int J Immunopharmacol 2000; 22: 365-372
• 77 Kaingu F, Liu D, Wang L, Tao J, Waihenya R, Kutima H. Anticoccidial effects of Aloe secundiflora leaf extract against Eimeria tenella in broiler chicken. Trop Anim Health Prod 2017; 49: 823-828
• 78 Horiuchi M, Seyama Y. Antiinflammatory and antiallergic activity of Bidens pilosa L. var. radiata SCHERFF. J Health Sci 2006; 52: 711-717
• 79 Farah D, Xuan TD, Yasuda M, Tawata S. Chemical composition and antioxidant, antibacterial and antifungal activities of the essential oils from Bidens pilosa Linn. var. Radiata. Food Control 2008; 19: 346-352
• 80 Rabe T, van Staden J. Antibacterial activity of South African plants used for medicinal purposes. J Ethnopharmacol 1997; 56: 81-87
• 81 Bartolome AP, Villasenor I, Yang WC. Bidens pilosa L. (Asteraceae): botanical properties, traditional uses, phytochemistry, and pharmacology. Evid Based Complement Alternat Med 2013; 2013: 340215
• 82 Yang WC, Yang CY, Liang YC, Yang CW, Li WQ, Chung CY, Yang MT, Kuo TF, Lin CF, Liang CL, Chang CL. Anti-coccidial properties and mechanisms of an edible herb, Bidens pilosa, and its active compounds for coccidiosis. Sci Rep 2019; 9: 2896
• 83 Laribi B, Kouki K, MʼHamdi M, Bettaieb T. Coriander (Coriandrum sativum L.) and its bioactive constituents. Fitoterapia 2015; 103: 9-26
• 84 Thompson A, Meah D, Ahmed N, Conniff-Jenkins R, Chileshe E, Phillips CO, Claypole TC, Forman DW, Row PE. Comparison of the antibacterial activity of essential oils and extracts of medicinal and culinary herbs to investigate potential new treatments for irritable bowel syndrome. BMC Complement Altern Med 2013; 13: 338
• 85 Silva F, Ferreira S, Queiroz JA, Domingues FC. Coriander (Coriandrum sativum L.) essential oil: its antibacterial activity and mode of action evaluated by flow cytometry. J Med Microbiol 2011; 60: 1479-1486
• 86 Naderi Farsani M, Hoseinifar SH, Rashidian G, Ghafari Farsani H, Ashouri G, Van Doan H. Dietary effects of Coriandrum sativum extract on growth performance, physiological and innate immune responses and resistance of rainbow trout (Oncorhynchus mykiss) against Yersinia ruckeri. Fish Shellfish Immunol 2019; 91: 233-240
• 87 Awad E, Austin B, Lyndon A. Effect of dietary supplements on digestive enzymes and growth performance of rainbow trout (Oncorhynchus mykiss, Walbaum). J Am Sci 2012; 8: 858-864
• 88 Kot B, Wierzchowska K, Piechota M, Czerniewicz P, Chrzanowski G. Antimicrobial activity of five essential oils from Lamiaceae against multidrug-resistant Staphylococcus aureus . Nat Prod Res 2019; 33: 3587-3591
• 89 Horváth P, Koščová J. In vitro antibacterial activity of mentha essential oils against Staphylococcus aureus . Folia Vet 2017; 61: 71-77
• 90 Miguel MG. Antioxidant and anti-inflammatory activities of essential oils: a short review. Molecules 2010; 15: 9252-9287
• 91 Anwar F, Abbas A, Mehmood T, Gilani AH, Rehman NU. Mentha: A genus rich in vital nutra-pharmaceuticals–a review. Phytother Res 2019; 33: 2548-2570
• 92 Lang M, Ferron PJ, Bursztyka J, Montjarret A, Duteil E, Bazire A, Bedoux G. Evaluation of immunomodulatory activities of essential oils by high content analysis. J Biotechnol 2019; 303: 65-71
• 93 Didry N, Dubreuil L, Pinkas M. Antimicrobial activity of thymol, carvacrol and cinnamaldehyde alone or in combination. Pharmazie 1993; 48: 301-304
• 94 Si W, Gong J, Tsao R, Zhou T, Yu H, Poppe C, Johnson R, Du Z. Antimicrobial activity of essential oils and structurally related synthetic food additives towards selected pathogenic and beneficial gut bacteria. J Appl Microbiol 2006; 100: 296-305
• 95 Nowotarska SW, Nowotarski K, Grant IR, Elliott CT, Friedman M, Situ C. Mechanisms of antimicrobial action of cinnamon and oregano oils, cinnamaldehyde, carvacrol, 2,5-dihydroxybenzaldehyde, and 2-hydroxy-5-methoxybenzaldehyde against Mycobacterium avium subsp. paratuberculosis (Map). Foods, 2017; 6: 72
• 96 Major P, Revajová V, Levkut M, Ševčíková Z, Spišáková V, Faixová Z, Levkutová M, Kožárová I, Goldová M, Levkut M. Intestinal mucin dynamic and leukocytic responses of chickens infected with Eimeria acervulina and fed oregano supplemented diet. Acta Veterinaria Brno 2011; 80: 147-156
• 97 Rostami F, Ghasemi HA, Taherpour K. Effect of Scrophularia striata and Ferulago angulata, as alternatives to virginiamycin, on growth performance, intestinal microbial population, immune response, and blood constituents of broiler chickens. Poult Sci 2015; 94: 2202-2209
• 98 Mahboubi M, Kazempour N, Boland Nazar AR. Total phenolic, total flavonoids, antioxidant and antimicrobial activities of Scrophularia striata boiss extracts. Jundishapur J Nat Pharm Prod 2013; 8: 15-19
• 99 Monsef-Esfahani HR, Hajiaghaee R, Shahverdi AR, Khorramizadeh MR, Amini M. Flavonoids, cinnamic acid and phenyl propanoid from aerial parts of Scrophularia striata . Pharm Biol 2010; 48: 333-336
• 100 Govahi R, Ghalamkari G, Toghyani M, Eghbalsaied S, Mohammadrezaei M, Shahryari M, Abari AD. Effect of Ferulago angulata sub. carduchorum on total serum antioxidant activity and some of the humoral immune responses in broiler chicks. J Herbal Drug 2013; 4: 119-126
• 101 Kovač J, Šimunović K, Wu Z, Klančnik A, Bucar F, Zhang Q, Možina SS. Antibiotic resistance modulation and modes of action of (−)-alpha-pinene in Campylobacter jejuni. PLoS One 2015; 10: e0122871
• 102 Zhang HY, Piao XS, Zhang Q, Li P, Yi JQ, Liu JD, Li QY, Wang GQ. The effects of Forsythia suspensa extract and berberine on growth performance, immunity, antioxidant activities, and intestinal microbiota in broilers under high stocking density. Poult Sci 2013; 92: 1981-1988
• 103 Wang Z, Xia Q, Liu X, Liu W, Huang W, Mei X, Luo J, Shan M, Lin R, Zou D, Ma Z. Phytochemistry, pharmacology, quality control and future research of Forsythia suspensa (Thunb.) Vahl: a review. J Ethnopharmacol 2018; 210: 318-339
• 104 Sharifi SD, Khorsandi SH, Khadem AA, Salehi A, Moslehi H. The effect of four medicinal plants on the performance, blood biochemical traits and ileal microflora of broiler chicks. Vet Arh 2013; 83: 69-80
• 105 Cross DE, McDevitt RM, Hillman K, Acamovic T. The effect of herbs and their associated essential oils on performance, dietary digestibility and gut microflora in chickens from 7 to 28 days of age. Br Poult Sci 2007; 48: 496-506
• 106 Jimoh AA, Ibitoye EB, Dabai YU, Garba S. In vivo antimicrobial potentials of garlic against Clostridium perfringens and its promotant effects on performance of broiler chickens. Pak J Biol Sci 2013; 16: 1978-1984
• 107 Ramiah SK, Zulkifli I, Rahim NA, Ebrahimi M, Meng GY. Effects of two herbal extracts and virginiamycin supplementation on growth performance, intestinal microflora population and fatty acid composition in broiler chickens. Asian-Australas J Anim Sci 2014; 27: 375-382
• 108 Gracia MI, Millán C, Sánchez J, Guyard-Nicodème M, Mayot J, Carre Y, Csorbai A, Chemaly M, Medel P. Efficacy of feed additives against Campylobacter in live broilers during the entire rearing period: Part B. Poult Sci 2016; 95: 886-892
• 109 Arczewska-Wlosek A, Swiatkiewicz S. Improved performance due to dietary supplementation with selected herbal extracts of broiler chickens infected with Eimeria spp. J Anim Feed Sci 2013; 22: 257-263
• 110 Waihenya RK, Mtambo MM, Nkwengulila G, Minga UM. Efficacy of crude extract of Aloe secundiflora against Salmonella gallinarum in experimentally infected free-range chickens in Tanzania. J Ethnopharmacol 2002; 79: 317-323
• 111 Shokraneh M, Ghalamkari G, Toghyani M, Landy N. Influence of drinking water containing Aloe vera (Aloe barbadensis Miller) gel on growth performance, intestinal microflora, and humoral immune responses of broilers. Veterinary World 2016; 9: 1197-1203
• 112 Akhtar M, Hai A, Awais MM, Iqbal Z, Muhammad F, ul Haq A, Anwar MI. Immunostimulatory and protective effects of Aloe vera against coccidiosis in industrial broiler chickens. Vet Parasitol 2012; 186: 170-177
• 113 Youn HJ, Noh JW. Screening of the anticoccidial effects of herb extracts against Eimeria tenella . Vet Parasitol 2001; 96: 257-263
• 114 Khalaji S, Zaghari M, Hatami K, Hedari-Dastjerdi S, Lotfi L, Nazarian H. 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 2011; 90: 2500-2510
• 115 Kaboutari J, Arab HA, Ebrahimi K, Rahbari S. Prophylactic and therapeutic effects of a novel granulated formulation of Artemisia extract on broiler coccidiosis. Trop Anim Health Prod 2014; 46: 43-48
• 116 Pirali Kheirabadi K, Kaboutari Katadj J, Bahadoran S, Teixeira da Silva JA, Dehghani Samani A, Cheraghchi Bashi M. Comparison of the anticoccidial effect of granulated extract of Artemisia sieberi with monensin in experimental coccidiosis in broiler chickens. Exp Parasitol 2014; 141: 129-133
• 117 Chang CL, Chung CY, Kuo CH, Kuo TF, Yang CW, Yang WC. Beneficial effect of Bidens pilosa on body weight gain, food conversion ratio, gut bacteria and coccidiosis in chickens. PLoS One 2016; 11: e0146141
• 118 Yang WC, Tien YJ, Chung CY, Chen YC, Chiou WH, Hsu SY, Liu HY, Liang CL, Chang CL. Effect of Bidens pilosa on infection and drug resistance of Eimeria in chickens. Res Vet Sci 2015; 98: 74-81
• 119 Chang CL, Yang CY, Muthamilselvan T, Yang WC. Field trial of medicinal plant, Bidens pilosa, against eimeriosis in broilers. Sci Rep 2016; 6: 24692
• 120 Lan L, Zuo B, Ding H, Huang Y, Chen X, Du A. Anticoccidial evaluation of a traditional Chinese medicine-Brucea javanica-in broilers. Poult Sci 2016; 95: 811-818
• 121 Ahmad A, Abid H, Waheed S, Tarar OM, Zahra Y, Tehmina S, Ali TM. Effects of replacing antibiotic growth promoters (AGPS) with botanical extracts and oils in feed of laying hens on production, performance and some microbial counts in feces. J Anim Plant Sci 2016; 26: 893-900
• 122 Chowdhury S, Mandal GP, Patra AK, Kumar P, Samanta I, Pradhan S, Samanta AK. Different essential oils in diets of broiler chickens: 2. Gut microbes and morphology, immune response, and some blood profile and antioxidant enzymes. Anim Feed Sci Technol 2018; 236: 39-47
• 123 Tabatabaei SM, Badalzadeh R, Mohammadnezhad GR, Balaei R. Effects of cinnamon extract on biochemical enzymes, TNF-alpha and NF-kappa B gene expression levels in liver of broiler chickens inoculated with Escherichia coli . Pesqui Vet Bras 2015; 35: 781-787
• 124 Hosseinzadeh H, Alaw Qotbi AA, Seidavi A, Norris D, Brown D. Effects of different levels of coriander (Coriandrum sativum) seed powder and extract on serum biochemical parameters, microbiota, and immunity in broiler chicks. ScientificWorldJournal 2014; 2014: 628979
• 125 Ghazanfari S, Mohammadi Z, Moradi MA. Effects of coriander essential oil on the performance, blood characteristics, intestinal microbiota and histological of broilers. Braz J Poultry Sci 2015; 17: 419-426
• 126 Ebrahimi H, Rahimi S, Khaki P, Grimes JL, Kathariou S. The effects of probiotics, organic acid, and a medicinal plant on the immune system and gastrointestinal microflora in broilers challenged with Campylobacter jejuni . Turkish J Vet Anim Sci 2016; 40: 329-336
• 127 Orengo J, Buendía AJ, Ruiz-Ibáñez MR, Madrid J, Del Río L, Catalá-Gregori P, García V, Hernández F. Evaluating the efficacy of cinnamaldehyde and Echinacea purpurea plant extract in broilers against Eimeria acervulina . Vet Parasitol 2012; 185: 158-163
• 128 Peek HW, Halkes SB, Mes JJ, Landman WJ. In vivo screening of four phytochemicals/extracts and a fungal immunomodulatory protein against an Eimeria acervulina infection in broilers. Vet Q 2013; 33: 132-138
• 129 Hashemi SR, Zulkifli I, Davoodi H, Zunita Z, Ebrahimie M. Growth performance, intestinal microflora, plasma fatty acid profile in broiler chickens fed herbal plant (Euphorbia hirta) and mix of acidifiers. Anim Feed Sci Technol 2012; 178: 167-174
• 130 Zulkifli I, Hashemi SR, Somchit MN, Zunita Z, Loh TC, Soleimani AF, Tang SC. Effects of Euphorbia hirta and virginiamycin supplementation to the diet on performance, digestibility, and intestinal microflora population in broiler chickens. Arch Geflügelk 2012; 76: 6-12
• 131 Gonzalez-Gil F, Diaz-Sanchez S, Pendleton S, Andino A, Zhang N, Yard C, Crilly N, Harte F, Hanning I. Yerba mate enhances probiotic bacteria growth in vitro but as a feed additive does not reduce Salmonella Enteritidis colonization in vivo . Poult Sci 2014; 93: 434-440
• 132 Vase-Khavari K, Mortezavi SH, Rasouli B, Khusro A, Salem AZM, Seidavi A. The effect of three tropical medicinal plants and superzist probiotic on growth performance, carcass characteristics, blood constitutes, immune response, and gut microflora of broiler. Trop Anim Health Prod 2019; 51: 33-42
• 133 Cetin E, Yibar A, Yesilbag D, Cetin I, Cengiz SS. The effect of volatile oil mixtures on the performance and ilio-caecal microflora of broiler chickens. Br Poult Sci 2016; 57: 780-787
• 134 Franciosini MP, Casagrande-Proietti P, Forte C, Beghelli D, Acuti G, Zanichelli D, dal Bosco A, Castellini C, Trabalza-Marinucci M. Effects of oregano (Origanum vulgare L.) and rosemary (Rosmarinus officinalis L.) aqueous extracts on broiler performance, immune function and intestinal microbial population. J Appl Anim Res 2016; 44: 474-479
• 135 Mohiti-Asli M, Ghanaatparast-Rashti M. Comparing the effects of a combined phytogenic feed additive with an individual essential oil of oregano on intestinal morphology and microflora in broilers. J Appl Anim Res 2017; 46: 184-189
• 136 Scocco P, Forte C, Franciosini MP, Mercati F, Casagrande-Proietti P, DallʼAglio C, Acuti G, Tardella FM, Trabalza-Marinucci M. Gut complex carbohydrates and intestinal microflora in broiler chickens fed with oregano (Origanum vulgare L.) aqueous extract and vitamin E. J Anim Physiol Anim Nutr (Berl) 2017; 101: 676-684
• 137 Scheurer W, Spring P, Maertens L. Effect of 3 dietary phytogenic products on production performance and coccidiosis in challenged broiler chickens. J Appl Poul Res 2013; 22: 591-599
• 138 Arshad N, Neubauer C, Hasnain S, Hess M. Peganum harmala can minimize Escherichia coli infection in poultry, but long-term feeding may induce side effects. Poult Sci 2008; 87: 240-249
• 139 Tanweer AJ, Chand N, Saddique U, Bailey CA, Khan RU. Antiparasitic effect of wild rue (Peganum harmala L.) against experimentally induced coccidiosis in broiler chicks. Parasitol Res 2014; 113: 2951-2960
• 140 El-Abasy M, Motobu M, Na KJ, Shimura K, Nakamura K, Koge K, Onodera T, Hirota Y. Protective effects of sugar cane extracts (SCE) on Eimeria tenella infection in chickens. J Vet Med Sci 2003; 65: 865-871
• 141 Awais MM, Akhtar M, Muhammad F, ul Haq A, Anwar MI. Immunotherapeutic effects of some sugar cane (Saccharum officinarum L.) extracts against coccidiosis in industrial broiler chickens. Exp Parasitol 2011; 128: 104-110
• 142 Piesova E, Makova Z, Levkut M, Faixova Z, Pistl J, Marcin A, Levkut M. The effects of sage extract feed supplementation on biochemical parameters, weight of internal organs and Salmonella counts in chickens. Res Vet Sci 2012; 93: 1307-1308
• 143 Agostini PS, Solà-Oriol D, Nofrarías M, Barroeta AC, Gasa J, Manzanilla EG. Role of in-feed clove supplementation on growth performance, intestinal microbiology, and morphology in broiler chicken. Livest Sci 2012; 147: 113-118
• 144 Sadek KM, Ahmed HA, Ayoub M, Elsabagh M. Evaluation of Digestarom and thyme as phytogenic feed additives for broiler chickens. Europ Poult Sci 2014; 78: 12
• 145 Grabensteiner E, Liebhart D, Arshad N, Hess M. Antiprotozoal activities determined in vitro and in vivo of certain plant extracts against Histomonas meleagridis, Tetratrichomonas gallinarum and Blastocystis sp. Parasitol Res 2008; 103: 1257-1264
• 146 Wang ML, Suo X, Gu JH, Zhang WW, Fang Q, Wang X. Influence of grape seed proanthocyanidin extract in broiler chickens: effect on chicken coccidiosis and antioxidant status. Poult Sci 2008; 87: 2273-2280
• 147 Altop A, Erener G, Duru ME, Isik K. Effects of essential oils from Liquidambar orientalis Mill. leaves on growth performance, carcass and some organ traits, some blood metabolites and intestinal microbiota in broilers. Br Poult Sci 2018; 59: 121-127
• 148 López CAA, Lima KRS, Manno MC, Tavares FB, Fernandes Neto DL, Jesus MLC, Viana MAO, Fonseca LAB. Effects of cashew nut shell liquid (CNSL) on the performance of broiler chickens. Arq Bras Med Vet Zootec 2012; 64: 1027-1035
• 149 Wang D, Zhou L, Li W, Zhou H, Hou G. Anticoccidial effects of areca nut (Areca catechu L.) extract on broiler chicks experimentally infected with Eimeria tenella. Exp Parasitol 2018; 184: 16-21
• 150 Nweze NE, Obiwulu IS. Anticoccidial effects of Ageratum conyzoides . J Ethnopharmacol 2009; 122: 6-9
• 151 Ahad S, Tanveer S, Nawchoo IA, Malik TA. Anticoccidial activity of Artemisia vestita (Anthemideae, Asteraceae)–a traditional herb growing in the Western Himalayas, Kashmir, India. Microb Pathog 2017; 104: 289-295
• 152 Michels MG, Bertolini LC, Esteves AF, Moreira P, Franca SC. Anticoccidial effects of coumestans from Eclipta alba for sustainable control of Eimeria tenella parasitosis in poultry production. Vet Parasitol 2011; 177: 55-60
• 153 Bakari GG, Max RA, Mdegela RH, Phiri EC, Mtambo MM. Effect of resinous extract from Commiphora swynnertonii (Burrt) on experimental coccidial infection in chickens. Trop Anim Health Prod 2013; 45: 455-459
• 154 Ogbe AO, Atawodi SE, Abdu PA, Sannusi A, Itodo AE. Changes in weight gain, faecal oocyst count and packed cell volume of Eimeria tenella-infected broilers treated with a wild mushroom (Ganoderma lucidum) aqueous extract. J S Afr Vet Assoc 2009; 80: 97-102
• 155 Zhang DF, Sun BB, Yue YY, Zhou QJ, Du AF. Anticoccidial activity of traditional Chinese herbal Dichroa febrifuga Lour. extract against Eimeria tenella infection in chickens. Parasitol Res 2012; 111: 2229-2233
• 156 Ghazaghi M, Mehri M, Bagherzadeh-Kasmani F. Effects of dietary Mentha spicata on performance, blood metabolites, meat quality and microbial ecosystem of small intestine in growing Japanese quail. Anim Feed Sci Tech 2014; 194: 89-98
• 157 Bozkurt M, Ege G, Aysul N, Akşit H, Tüzün AE, Küçükyılmaz K, Borum AE, Uygun M, Akşit D, Aypak S, Şimşek E, Seyrek K, Koçer B, Bintaş E, Orojpour A. Effect of anticoccidial monensin with oregano essential oil on broilers experimentally challenged with mixed Eimeria spp. Poult Sci 2016; 95: 1858-1868
• 158 Kurekci C, Al Jassim R, Hassan E, Bishop-Hurley SL, Padmanabha J, McSweeney CS. Effects of feeding plant-derived agents on the colonization of Campylobacter jejuni in broiler chickens. Poult Sci 2014; 93: 2337-2346
• 159 Guo FC, Kwakkel RP, Williams BA, Parmentier HK, Li WK, Yang ZQ, Verstegen MW. Effects of mushroom and herb polysaccharides on cellular and humoral immune responses of Eimeria tenella-infected chickens. Poult Sci 2004; 83: 1124-1132
• 160 Rubio LA, Brenes A, Setién I, de la Asunción G, Durán N, Cutuli MT. Lactobacilli counts in crop, ileum and caecum of growing broiler chickens fed on practical diets containing whole or dehulled sweet lupin (Lupinus angustifolius) seed meal. Br Poult Sci 1998; 39: 354-359
• 161 Ahad S, Tanveer S, Malik TA, Nawchoo IA. Anticoccidial activity of fruit peel of Punica granatum L. Microb Pathog 2018; 116: 78-83
• 162 Lengsfeld C, Faller G, Hensel A. Okra polysaccharides inhibit adhesion of Campylobacter jejuni to mucosa isolated from poultry in vitro but not in vivo . Anim Feed Sci Technol 2007; 35: 113-125
• 163 Ola-Fadunsin SD, Ademola IO. Direct effects of Moringa oleifera Lam (Moringaceae) acetone leaf extract on broiler chickens naturally infected with Eimeria species. Trop Anim Health Prod 2013; 46: 1423-1428
• 164 Anosa GN, Okoro OJ. Anticoccidial activity of the methanolic extract of Musa paradisiaca root in chickens. Trop Anim Health Prod 2011; 43: 245-248
• 165 Papazahariadou M, Papadopoulos E, Christaki E, Georgopoulou I, Florou-Paneri P, Tserveni-Goussi A, Yannakopoulos A. Use of Fraxinus ornus as an alternative anti-coccidian in broilers experimentally infected with Eimeria tenella . Rev Med Vet (Toulouse) 2010; 161: 326-331
• 166 Wang D, Zhou L, Li W, Zhou H, Hou G. Anticoccidial effect of Piper sarmentosum extracts in experimental coccidiosis in broiler chickens. Trop Anim Health Prod 2016; 48: 1071-1078
• 167 Retnani Y, Dan TM. Taryati. Morinda citrifolia L. leaf extract as antibacterial Salmonella typhimurium to increase productivity of quail (Coturnix coturnix japonica). Pak J Biol Sci 2014; 17: 560-564
• 168 Erhan MK, Bolukbasi SC. Citrus peel oils supplementation in broiler diet: effects on performance, jejunum microflora and jejunum morphology. Braz J Poultry Sci 2017; 19: 15-21
• 169 Charal JW, Bidner TD, Southern LL, Janes ME, Gutierrez ME, Lavergne TA. Anise oil dosage and its effect on growth performance and jejunal lesions during a Clostridium perfringens challenge in battery trials, and growth performance in a floor pen trial. J Appl Poult Res 2017; 26: 240-252