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      Eimeria species occurrence varies between geographic regions and poultry production systems and may influence parasite genetic diversity

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          Highlights

          • Multivariate analysis revealed comparable poultry clusters in north and south India.

          • Eimeria species occurrence varied between system clusters.

          • E. tenella occurrence across systems may underpin region-specific genetic diversity.

          • E. necatrix was found to be more common in north than south India.

          Abstract

          Coccidiosis is one of the biggest challenges faced by the global poultry industry. Recent studies have highlighted the ubiquitous distribution of all Eimeria species which can cause this disease in chickens, but intriguingly revealed a regional divide in genetic diversity and population structure for at least one species, Eimeria tenella. The drivers associated with such distinct geographic variation are unclear, but may impact on the occurrence and extent of resistance to anticoccidial drugs and future subunit vaccines. India is one of the largest poultry producers in the world and includes a transition between E. tenella populations defined by high and low genetic diversity. The aim of this study was to identify risk factors associated with the prevalence of Eimeria species defined by high and low pathogenicity in northern and southern states of India, and seek to understand factors which vary between the regions as possible drivers for differential genetic variation. Faecal samples and data relating to farm characteristics and management were collected from 107 farms from northern India and 133 farms from southern India. Faecal samples were analysed using microscopy and PCR to identify Eimeria occurrence. Multiple correspondence analysis was applied to transform correlated putative risk factors into a smaller number of synthetic uncorrelated factors. Hierarchical cluster analysis was used to identify poultry farm typologies, revealing three distinct clusters in the studied regions. The association between clusters and presence of Eimeria species was assessed by logistic regression. The study found that large-scale broiler farms in the north were at greatest risk of harbouring any Eimeria species and a larger proportion of such farms were positive for E. necatrix, the most pathogenic species. Comparison revealed a more even distribution for E. tenella across production systems in south India, but with a lower overall occurrence. Such a polarised region- and system-specific distribution may contribute to the different levels of genetic diversity observed previously in India and may influence parasite population structure across much of Asia and Africa. The findings of the study can be used to prioritise target farms to launch and optimise appropriate anticoccidial strategies for long-term control.

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          Most cited references32

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          Securing poultry production from the ever-present Eimeria challenge.

          The intestinal disease coccidiosis, caused by protozoan parasites of the genus Eimeria, is one of the most important livestock diseases in the world. It has a high impact in the poultry industry where parasite transmission is favoured by high-density housing of large numbers of susceptible birds. Coccidiosis control in poultry is achieved by careful husbandry combined with in-feed anticoccidial drugs or vaccination with live parasites. However, outbreaks of coccidiosis still occur and subclinical infections, which significantly impact on productivity and food security, are common due to widespread drug resistance, high parasite prevalence, and environmental persistence. Herein, we review some recent approaches for the production of cheaper third generation vaccines, based on robust methods for identification of immunoprotective antigens and the use of transgenic Eimeria. Copyright © 2013 Elsevier Ltd. All rights reserved.
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            Forty years of monensin for the control of coccidiosis in poultry.

            In July 1971, the polyether ionophorous antibiotic monensin was introduced in the United States for the control of coccidiosis in poultry. At that time, prospects for new anticoccidial agents were not good. Amprolium had enjoyed several years of use, but many other compounds had been abandoned as resistance to them developed. After the introduction of monensin, most commercial broilers were medicated with the drug and it is still widely used for this purpose today. Apart from in poultry, monensin is also used to control coccidiosis in game birds, sheep, and cattle. Indeed, more animals have been medicated with ionophores, such as monensin, for control of disease than any other medicinal agents in the history of veterinary medicine. In this review, we discuss the discovery, mode of action, and efficacy of monensin, together with matters of importance to the poultry industry such as commercial use, drug resistance, toxicity, pharmacology and residues, host immunity to coccidiosis, and effects in other avian species.
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              Population, genetic, and antigenic diversity of the apicomplexan Eimeria tenella and their relevance to vaccine development.

              The phylum Apicomplexa includes serious pathogens of humans and animals. Understanding the distribution and population structure of these protozoan parasites is of fundamental importance to explain disease epidemiology and develop sustainable controls. Predicting the likely efficacy and longevity of subunit vaccines in field populations relies on knowledge of relevant preexisting antigenic diversity, population structure, the likelihood of coinfection by genetically distinct strains, and the efficiency of cross-fertilization. All four of these factors have been investigated for Plasmodium species parasites, revealing both clonal and panmictic population structures with exceptional polymorphism associated with immunoprotective antigens such as apical membrane antigen 1 (AMA1). For the coccidian Toxoplasma gondii only genomic diversity and population structure have been defined in depth so far; for the closely related Eimeria species, all four variables are currently unknown. Using Eimeria tenella, a major cause of the enteric disease coccidiosis, which exerts a profound effect on chicken productivity and welfare, we determined population structure, genotype distribution, and likelihood of cross-fertilization during coinfection and also investigated the extent of naturally occurring antigenic diversity for the E. tenella AMA1 homolog. Using genome-wide Sequenom SNP-based haplotyping, targeted sequencing, and single-cell genotyping, we show that in this coccidian the functionality of EtAMA1 appears to outweigh immune evasion. This result is in direct contrast to the situation in Plasmodium and most likely is underpinned by the biology of the direct and acute coccidian life cycle in the definitive host.
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                Author and article information

                Contributors
                Journal
                Vet Parasitol
                Vet. Parasitol
                Veterinary Parasitology
                Elsevier
                0304-4017
                1873-2550
                15 January 2017
                15 January 2017
                : 233
                : 62-72
                Affiliations
                [a ]Department of Production and Population Health, Royal Veterinary College, North Mymms, Hertfordshire, UK
                [b ]Department of Veterinary Parasitology, Madras Veterinary College, Tamil Nadu Veterinary and Animal Sciences University, Chennai, India
                [c ]Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh, India
                [d ]Department of Pathology and Pathogen Biology, Royal Veterinary College, North Mymms, Hertfordshire, UK
                [e ]Augusta University, Augusta, GA, USA
                [f ]Department of Animal Biotechnology, Madras Veterinary College, Tamil Nadu Veterinary and Animal Sciences University, Chennai, India
                Author notes
                [* ]Corresponding author at: Department of Pathology and Pathogen Biology, Royal Veterinary College, North Mymms, Hertfordshire, UK.Department of Pathology and Pathogen BiologyRoyal Veterinary CollegeNorth MymmsHertfordshireUK dblake@ 123456rvc.ac.uk
                [1]

                These authors have contributed equally to the work.

                Article
                S0304-4017(16)30504-0
                10.1016/j.vetpar.2016.12.003
                5239766
                28043390
                44dd338a-6847-4e68-b175-36114399afd8
                © 2016 The Author(s)

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 26 August 2016
                : 24 October 2016
                : 3 December 2016
                Categories
                Research Paper

                Parasitology
                eimeria,chickens,epidemiology,genetic diversity
                Parasitology
                eimeria, chickens, epidemiology, genetic diversity

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