Focused review: The role of drug combinations for the control of coccidiosis in commercially reared chickens

Anon, 2019 Anon, 2019 Bafundo, 1990, Selection for resistance to monensin, nicarbazin, and the monensin plus nicarbazin combination, Poultry Sci., 69, 1485, 10.3382/ps.0691485 Bafundo, 1989, Research Note: effect of narasin and roxarsone combinations on Eimeria tenella infections in floor-pen raised broilers, Poultry Sci., 68, 1011, 10.3382/ps.0681011 Bafundo, 2021, The effects of a quillaja and yucca combination on performance and carcass traits of coccidia-vaccinated broilers exposed to an enteric disease challenge, Poultry Sci., 100 Bafundo, 1990, Shuttle programs in broilers: effective use of maxiban, nicarbazin, monensin, and narasin, Poultry Sci., 69, 111 Bafundo, 2008, Sensitivity of Eimeria field isolates in the United States: responses of nicarbazin-containing anticoccidials, Poultry Sci., 87, 1760, 10.3382/ps.2008-00129 Bafundo, 2020, The effects of a combination of Quillaja saponaria and Yucca schidigera on Eimeria spp. in broiler chickens, Avian Dis., 64, 300, 10.1637/aviandiseases-D-20-00016 Bafundo, 2021, Concurrent use of saponins and live coccidiosis vaccines: the influence of a quillaja/yucca combination on anticoccidial effects and performance results of vaccinated broilers, Poultry Sci., 100, 100905, 10.1016/j.psj.2020.12.010 Ball, 1964, Synergistic action of sulphaquinoxaline and 2-amino-4-dimethylamino-5-(4-chlorophenyl)-6-ethylpyrimidine in caecal coccidiosis in chickens, J. Comp. Pathol., 74, 487, 10.1016/S0368-1742(64)80055-2 Ball, 1987, Ultrastructural studies of the effects of amprolium and dinitolmide on Eimeria acervulina macrogametes, Parasitol. Res., 73, 293, 10.1007/BF00531080 Bampidis, 2018, Safety and efficacy of Monimax® (monensin sodium and nicarbazin) for chickens for fattening and chickens reared for laying, EFSA J., 16 Beers, 1989, Physiological responses of heat-stressed broilers fed nicarbazin, Poultry Sci., 68, 428, 10.3382/ps.0680428 Bryson, 1955, Microbial drug resistance, Adv. Genet., 7, 1, 10.1016/S0065-2660(08)60092-9 Callender, 1980 Cervantes, 2015, Antibiotic-free poultry production: is it sustainable?, J. Appl. Poultry Res., 24, 91, 10.3382/japr/pfv006 Challey, 1973, Synergism between 4-hydroxyquinoline and pyridone coccidiostats, J. Parasitol., 59, 502, 10.2307/3278783 Chapman, 1976, Eimeria tenella in chickens: studies on resistance to the anticoccidial drugs monensin and lasalocid, Vet. Parasitol., 2, 187, 10.1016/0304-4017(76)90074-1 Chapman, 1978, Drug resistance in coccidia, 387 Chapman, 1980, Studies on the sensitivity of field isolates of Eimeria maxima to combinations of anticoccidial drugs, Avian Pathol., 9, 67, 10.1080/03079458008418387 Chapman, 1982, Anticoccidial drug resistance, 429 Chapman, 1984, Development by genetic recombination of a line of Eimeria tenella resistant to robenidine, decoquinate, and amprolium, Z. Parasitenkd., 70, 437, 10.1007/BF00926683 Chapman, 1989, Field isolates of Eimeria tenella: sensitivity to diclazuril, maduramicin, narasin, salinomycin and a mixture of nicarbazin/narasin, 323 Chapman, 1994, A review of the biological activity of the anticoccidial drug nicarbazin and its application for the control of coccidiosis in poultry, Poultry Sci. Rev., 5, 231 Chapman, 1994, Sensitivity of field isolates of Eimeria to monensin following the use of a coccidiosis vaccine in broiler chickens, Poultry Sci., 73, 476, 10.3382/ps.0730476 Chapman, 1997, Biochemical, genetic, and applied aspects of drug resistance in Eimeria parasites of the fowl, Avian Pathol., 26, 221, 10.1080/03079459708419208 Chapman, 1999, Anticoccidial drugs and their effects upon the development of immunity to Eimeria infections in poultry, Avian Pathol., 28, 521, 10.1080/03079459994317 Chapman, 2001, Use of anticoccidial drugs in broiler chickens in the USA: analysis for the years 1995-1999, Poultry Sci., 80, 572, 10.1093/ps/80.5.572 Chapman, 2009, A landmark contribution to poultry science – prophylactic control of coccidiosis in poultry, Poultry Sci., 88, 813, 10.3382/ps.2008-00316 Chapman, 2017, Coccidiosis in egg laying poultry, 571 Chapman, 2018, Applied strategies for the control of coccidiosis in poultry, CAB Rev., 13, 1, 10.1079/PAVSNNR201813026 Chapman, 2014, Vaccination of chickens against coccidiosis ameliorates drug resistance in commercial poultry production, Int. J. Parasitol. Drugs Drug Resist., 4, 214, 10.1016/j.ijpddr.2014.10.002 Chapman, 2015, Restoration of sensitivity to salinomycin in Eimeria following 5 flocks of broiler chickens reared in floor-pens using drug programs and vaccination to control coccidiosis, Poultry Sci., 94, 943, 10.3382/ps/pev077 Chapman, 2010, Forty years of monensin for the control of coccidiosis in poultry, Poultry Sci., 89, 1788, 10.3382/ps.2010-00931 Chapman, 2013, A selective review of advances in coccidiosis research, vol. 83, 93 Clarke, 1962, A mixture of diaveridine and sulphaquinoxaline as a coccidiostat for poultry- I. Preliminary studies on efficiency against Eimeria tenella and E. necatrix infections, and on toxicity in poultry, Vet. Rec., 74, 845 Clarke, 1964, A mixture of diaveridine and sulphaquinoxaline as a coccidiostat for poultry II. Efficiency against Eimeria acervulina, E. brunetti, and E. maxima infections together with a field survey of coccidiosis in S.E. England, Vet. Rec., 76, 818 Cuckler, 1956, The effect of nicarbazin on the development of immunity to avian coccidia, J. Parasitol., 42, 593, 10.2307/3274879 Cuckler, 1955, Antiparasitic activity of substituted carbanilide complexes, Science, 122, 244, 10.1126/science.122.3162.244.b Cuckler, 1969, Development of resistance in coccidia, Acta Vet., 38, 87 Davies, 1963, Design of therapy for the control of species of Eimeria in the domestic fowl, J. Comp. Pathol., 73, 379, 10.1016/S0368-1742(63)80040-5 Davies, 1954, The practical application of sulphamezathine therapy for caecal coccidiosis, Vet. Rec., 66, 19 del Cacho, 2007, Expression of flotillin-1 on Eimeria tenella sporozoites and its role in host cell invasion, J. Parasitol., 93, 328, 10.1645/GE-992R.1 Dougherty, 1974, Inhibition of mitochondrial energy transduction by carbanilides, Fed. Proc., 33, 1657 Dowling, 1992, Ionophore toxicity in chickens: a review of pathology and diagnosis, Avian Pathol., 21, 355, 10.1080/03079459208418854 2013, Final rule; withdrawal of approval of new animal drug applications, Carbarsone; Roxarsone Fry, 1984, Effects of decoquinate and clopidol on electron transport in mitochondria of Eimeria tenella (Apicomplexa: coccidia), Biochem. Pharmacol., 33, 229, 10.1016/0006-2952(84)90480-5 Goetting, 2011, Pharmacokinetics of veterinary drugs in laying hens and residues in eggs: a review of the literature, J. Vet. Pharmacol. Therapeut., 34, 521, 10.1111/j.1365-2885.2011.01287.x Harris, 1988, Effect of nicarbazin and MaxibanTM on broiler performance when fed to different age broiler males subjected to environmental stress, Poultry Sci., 67, 16 Hodgson, 1969, The incidence of drug resistant strains of Eimeria in chickens in Great Britain, 1966, Br. Vet. J., 125, 31, 10.1016/S0007-1935(17)49161-5 Horton-Smith, 1960, Potentiation of sulfadimidine by 2,4-diamino-6,7-di-isopropylpteridine and other 6,7-disubstituted 2,4-diaminopteridines against Eimeria infections of chicks, Br. J. Pharmacol., 15, 298 James, 1980, Thiamine uptake in isolated schizonts of Eimeria tenella and the inhibitory effects of amprolium, Parasitology, 80, 313, 10.1017/S0031182000000779 Jeffers, 1974, Genetic transfer of anticoccidial drug resistance in Eimeria tenella, J. Parasitol., 60, 900, 10.2307/3278505 Jeffers, 1974, Eimeria tenella: incidence, distribution, and anticoccidial drug resistance of isolants in major broiler-producing areas, Avian Dis., 18, 74, 10.2307/1589244 Jeffers, 1974, Eimeria acervulina and E. maxima: incidence, distribution, and anticoccidial drug resistance of isolants in major broiler-producing areas, Avian Dis., 18, 331, 10.2307/1589101 Jeffers, 1989, Anticoccidial drug resistance: a review with emphasis on the polyether ionophores, 295 Jeffers, 1973, Collateral sensitivity to 4-hydroxyquinolines in Eimeria acervulina strains resistant to meticlorpindol, J. Parasitol., 59, 624, 10.2307/3278851 Jones, 2007, A broad view of arsenic, Poultry Sci., 86, 2, 10.1093/ps/86.1.2 Joyner, 1970, Coccidiosis: problems arising from the development of anticoccidial drug resistance, Exp. Parasitol., 28, 122, 10.1016/0014-4894(70)90077-9 Joyner, 1955, Synergism in the chemotherapy of Eimeria tenella, Nature, 176, 975, 10.1038/176975a0 Joyner, 1975, Transferred drug resistance in Eimeria maxima, Parasitology, 71, 385, 10.1017/S0031182000047168 Joyner, 1977, Further observations on the genetic transfer of drug resistance in Eimeria maxima, Parasitology, 74, 205, 10.1017/S0031182000047703 Joyner, 1978, The activity of methyl benzoquate and clopidol against Eimeria maxima: synergy and drug resistance, Parasitology, 76, 369, 10.1017/S003118200004823X Karavolias, 2018, Raised without antibiotics: impact on animal welfare and implications for food policy, Transl. Anim. Sci., 2, 337, 10.1093/tas/txy016 Karlsson, 1978, Development of immunity to coccidiosis in chickens administered anticoccidials in the feed, Avian Dis., 22, 487, 10.2307/1589304 Kawazoe, 1991, Sensitivity of field isolates of E. acervulina to salinomycin, maduramicin, and a mixture of clopidol and methyl benzoquate in the chicken, Avian Pathol., 20, 439, 10.1080/03079459108418782 Kendall, 1956, Synergy between pyrimethamine and sulphonamides used in the control of Eimeria tenella, Proc. Roy. Soc. Med., 49, 874 Kendall, 1956, The synergism between pyrimethamine and sulphadimethylpyrimidine in the control of Eimeria tenella, J. Comp. Pathol., 66, 145, 10.1016/S0368-1742(56)80015-5 Keshavarz, 1982, Anticoccidial drugs: growth and performance depressing effects in young chickens, Poultry Sci., 61, 699, 10.3382/ps.0610699 Kraieski, 2021, Sensitivity of field isolates of Eimeria acervulina and E. maxima from three regions in Brazil to eight anticoccidial drugs, Poultry Sci., 100, 10.1016/j.psj.2021.101233 Lanckriet, 2010, The effect of commonly used anticoccidials and antibiotics in a subclinical necrotic enteritis model, Avian Pathol., 39, 63, 10.1080/03079450903505771 Lima, 2017, Determination of the residue levels of nicarbazin and combination nicarbazin-narasin in broiler chickens after oral administration, PLoS One, 12, 10.1371/journal.pone.0181755 Long, 1963, The effect of a combination of sulphaquinoxaline and amprolium against different species of Eimeria in chickens, Vet. Rec., 75, 645 Long, 1976, A guide to the laboratory techniques used in the study and diagnosis of avian coccidiosis, Folia Vet. Lat., 6, 201 Long, 1988, Anticoccidial activity of combinations of narasin and nicarbazin, Poultry Sci., 67, 248, 10.3382/ps.0670248 Lux, 1954, The chemotherapy of Eimeria tenella I. Dihydropyrimidines and dihydrotriazenes, Antibiot. Chemother. (Wash. D C), 4, 971 Malik, 2016, Synergistic approach for treatment of chicken coccidiosis using berberine – a plant natural product, Microb. Pathog., 93, 56, 10.1016/j.micpath.2016.01.012 Mathis, 2006, Increased level of Eimeria sensitivity to diclazuril after using a live coccidiosis vaccine, Avian Dis., 50, 321, 10.1637/7455-101305R1.1 Mathis, 1984, Effectiveness of therapeutic anticoccidial drugs against recently isolated coccidia, Poultry Sci., 63, 1149, 10.3382/ps.0631149 McDougald, 1977 McDougald, 1978 McDougald, 2008, Protozoal infections, 1067 McDougald, 1980, Mortality from heat stress in broiler chickens influenced by anticoccidial drugs, Poultry Sci., 59, 2421 McDougald, 1981, Anticoccidial activity of salinomycin (AHR-3096C) and compatibility with roxarsone in floor-pen experiments with broilers, Poultry Sci., 60, 2416, 10.3382/ps.0602416 McDougald, 1986, Drug-sensitivity of 99 isolates of coccidia from broiler farms, Avian Dis., 30, 690, 10.2307/1590570 McLoughlin, 1973, Efficacy of Novastat against twelve strains of Eimeria tenella and the development of a Novastat-resistant strain, Avian Dis., 17, 582, 10.2307/1589157 McLoughlin, 1975, Sequential use of coccidiostats: effect on development by Eimeria tenella of resistance to amprolium, nicarbazin, Unistat and zoalene, Avian Dis., 19, 424, 10.2307/1589067 McLoughlin, 1967, Drug resistance in Eimeria tenella: V. the experimental development of a nicarbazin-resistant strain, J. Parasitol., 53, 930, 10.2307/3276810 McManus, 1967, Response of six strains of Eimeria brunetti to two antagonists of para-aminobenzoic acid, J. Protozool., 14, 379, 10.1111/j.1550-7408.1967.tb02013.x Mesa, 2021, Survey of coccidia on commercial broiler farms in Colombia: frequency of Eimeria species, anticoccidial sensitivity, and histopathology, Poultry Sci., 100, 10.1016/j.psj.2021.101239 Muthamilselvan, 2016, Herbal remedies for coccidiosis control: a review of plants, compounds, and anticoccidial actions, Evid. Based Complement. Alternat. Med., 2016, 10.1155/2016/2657981 Noack, 2019, Anticoccidial drugs of the livestock industry, Parasitol. Res., 118, 2009, 10.1007/s00436-019-06343-5 Norton, 1975, The development of drug-resistant strains of Eimeria maxima in the laboratory, Parasitology, 71, 153, 10.1017/S0031182000053233 Norton, 1978, The appearance of bisporocystic oocysts of Eimeria maxima in drug treated chicks, Parasitology, 77, 243, 10.1017/S0031182000050216 Parker, 2021, Impact assessment of the reduction or removal of ionophores used for controlling coccidiosis in the UK broiler industry, Vet. Rec., 189, e513, 10.1002/vetr.513 Peek, 2003, Resistance to anticoccidial drugs of Dutch avian Eimeria spp. field isolates originating from 1996, 1999 and 2001, Avian Pathol., 32, 391, 10.1080/0307945031000121149 Peek, 2006, Higher incidence of Eimeria spp. field isolates sensitive for diclazuril and monensin associated with the use of live coccidiosis vaccination with ParacoxTM-5 in broiler farms, Avian Dis., 50, 434, 10.1637/7486-121205R.1 Peeters, 1994, Sensitivity of avian Eimeria spp. to seven chemical and five ionophore anticoccidials in five Belgian integrated broiler operations, Avian Dis., 38, 483, 10.2307/1592069 Reece, 1988, Review of adverse effects of chemotherapeutic agents in poultry, World’s Poult. Sci. J., 44, 193, 10.1079/WPS19880020 Register, 2014, 79 Reid, 1972, Anticoccidials used in the poultry industry: time of action against the coccidial life cycle, Folia Vet. Lat., 2, 641 Rogers, 1962, Thiamine antagonists, Ann. N. Y. Acad. Sci., 98, 412, 10.1111/j.1749-6632.1962.tb30563.x Ryley, 1975, Lerbek, a synergistic mixture of methyl benzoquate and clopidol for the prevention of chicken coccidiosis, Parasitology, 70, 377, 10.1017/S0031182000052148 Ryley, 1980, Drug resistance in coccidia, Adv. Vet. Sci. Comp. Med., 24, 99 Ryley, 1973, Chemotherapy of chicken coccidiosis, Adv. Pharmacol. Chemother., 11, 221, 10.1016/S1054-3589(08)60459-7 Ryley, 1976, Laboratory studies with some older anticoccidials, Parasitology, 73, 287, 10.1017/S0031182000046989 Smith II, 1983, Influence of monensin on the cation influx and glycolysis of Eimeria tenella sporozoites in vitro, J. Parasitol., 69, 666, 10.2307/3281137 Smith II, 1979, Eimeria tenella: accumulation and retention of anticoccidial ionophores by extracellular sporozoites, Exp. Parasitol., 48, 325, 10.1016/0014-4894(79)90115-2 Smith II, 1981, Effect of ionophores on survival, penetration, and development of Eimeria tenella sporozoites in vitro, J. Parasitol., 67, 511, 10.2307/3280482 Tamas, 1989, Development of resistance against narasin and narasin+nicarbazin, Poultry Sci., 68, 146 Tonkinson, 1987, Anticoccidial efficacy of various ratios of narasin and nicarbazin, Poultry Sci., 66, 187 Vereecken, 2020, Synergistic effect of a combination of nicarbazin and monensin against coccidiosis in the chicken caused by Eimeria spp, Avian Pathol., 49, 389, 10.1080/03079457.2020.1756226 Vereecken, 2021, Restoration of the sensitivity of Eimeria acervulina to anticoccidial drugs in the chicken following use of a live coccidiosis vaccine, Vet. Parasitol., 292, 10.1016/j.vetpar.2021.109416 Wang, 1975, Studies of the mitochondria from Eimeria tenella and inhibition of the electron transport by quinolone coccidiostats, Biochim. Biophys. Acta, 396, 210, 10.1016/0005-2728(75)90035-3 Wang, 1976, Inhibition of the respiration of Eimeria tenella by quinolone coccidiostats, Biochem. Pharmacol., 25, 343, 10.1016/0006-2952(76)90225-2 Wang, 1978, Biochemical and nutritional aspects of coccidia, 135 Wang, 1982, Biochemistry and physiology of coccidia, 167 Wang, 1975, Dihydrofolate reductase from Eimeria tenella: rationalization of chemotherapeutic efficacy of pyrimethamine, J. Protozool., 22, 564, 10.1111/j.1550-7408.1975.tb05234.x Warren, 1966, The incidence of drug-resistant strains of Eimeria species in chickens in Great Britain, 1964/65, Br. Vet. J., 122, 534, 10.1016/S0007-1935(17)40256-9 Weppelman, 1977, Eimeria tenella: the selection and frequency of drug-resistant mutants, Exp. Parasitol., 42, 56, 10.1016/0014-4894(77)90061-3 White, 1983, Evaluation of a mixture of trimethoprim and sulphaquinoxaline for the treatment of bacterial and coccidial diseases of poultry, Vet. Rec., 113, 608 Wiernusz, 1995, Nicarbazin effects on broiler thermobalance during high ambient temperature stress, Poultry Sci., 74, 577, 10.3382/ps.0740577 Williams, 1998, Analysis of the phenotypes in field populations of E. acervulina expressing dual drug-resistance to decoquinate and clopidol, Avian Pathol., 27, 67, 10.1080/03079459808419276