Abstract
Coccidiosis is a deadly disease that hampers chicken’s productivity and welfare. Thus, the disease is a major menace to the global poultry industry. Coccidiosis which is caused by the apicomplexan parasite of the genus Eimeria has seven known species which affect the different parts of the intestinal tract of chickens. The disease which occurs by ingestion of sporulated oocyst has been associated with poor poultry management system. Mixed infection among the species of this parasite contributes to both pathogenicity and misdiagnosis of the disease. A progress in identification and diagnosis approach which cuts across pathological, morphological and molecular has been reported for this parasite. Control measures which include anticoccidial drugs, vaccines and natural products have dominated literature for this disease. However, the emergence of genetic and antigenic diversity with implication on resistance to anticoccidials among different strains of Eimeria parasite has generated concerns on the effectiveness of the current anticoccidial vaccines. A new look on the control strategy therefore becomes imperative. This study reviews the current trends on the identification and control of chicken coccidiosis with focus on (1) Avian coccidiosis (2) Epidemiology of chicken coccidiosis (3) Eimeria parasite and distribution in poultry (4) Diagnosis of Eimeria parasite (5) Control measures of coccidiosis (6) Threats posed by genetic and antigenic diversity of Eimeria parasite on coccidiosis control. Genomic study on diversity of Eimeria parasite becomes imperative for effective vaccine design against coccidiosis.
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Introduction
Over the decades, the world has been experiencing a continuous growth in human population. According to UN DESA (2017), the current human population of 7.6 billion has been projected to a population of 9.8 and 11.2 billion respectively by 2050 and 2100. To meet this ever-growing population, food, shelter and clothing become imperative. Food production carries a larger percentage of these basic human needs as its availability determines the existence of human population (Erb et al. 2012). In view of this, much demand has been on the agricultural sector of each nation to increase food production that is safe for human consumption that will meet the ever-growing population.
Poultry industry is one of the fastest growing sub-sector of agriculture that contributes to global nutrition (Mottet and Tempio 2017) and thus a major driving force of the economy. Chicken, a major poultry bird contributes greatly to agricultural production through the supply of meat and eggs (Hald 2010). However, chickens are also host to many deadly diseases which hamper on productivity and compromise welfare resulting in high mortality in some cases. Among many diseases that affect chickens globally, coccidiosis is a house-hold name associated with high level of mortality in poultry industry (Blake and Tomley 2014).
Chicken coccidiosis is an enteric disease that impairs growth and suppresses the immune system resulting in high mortality which has been estimated to cost more than US$3billion annually in poultry industry (Blake and Tomley 2014). The disease is caused by a protozoan apicomplexan parasites of genus Eimeria which consist of over 1000 species (Blake 2015).
In chicken, seven species of Eimeria have been identified among which E. tenella, E. maxima and E. acervulina have been regarded as the most economically significant species (Thenmozhi et al. 2014). Co-infection of Eimeria species (Haug et al. 2008; Jenkins et al. 2008) is common in coccidiosis which contributes not only to pathogenicity but also leads to misleading diagnosis.
Identification of Eimeria species is important as it provides the bedrock for effective control measure. Morphological approach based on examination of oocyst by microscope and some parasitological parameters were the first-generation approach used in the identification of Eimeria species (Long and Joyner 1984). However, several limitations such as complexity, expertise and confusing characteristics among species have reduced the efficacy of this method (Kawahara et al. 2010). This has given room for molecular approach.
The control measure against this parasite has been through the use anticoccidial drugs, vaccines and strict management practice (Godwin and Morgan 2015). However, the emergence of resistant strains has threatened the effectiveness of these anticoccidials necessitating a modification in the present control method.
This review summarized the recent trends in the diagnosis and control of Eimeria parasite in chickens viz-a viz; avian coccidiosis, epidemiology of chicken coccidiosis, Eimeria parasite and distribution in poultry, identification and diagnosis of Eimeria parasite, control measures of coccidiosis and threats posed by genetic and antigenic diversity of Eimeria parasite on coccidiosis control.
Avian coccidiosis
Among parasitic diseases that affect the poultry industry, coccidiosis is renowned as a dreadful disease that causes economic loss. It is caused by Eimeria species of the phylum apicomplexa. Over 1000 species of Eimeria have been reported to infect different host animals such as chicken, duck, turkey, cattle, rabbit, sheep and domestic dog and cat (Blake 2015). In chicken, seven species have been described which are E. tenella, E. maxima, E. mitis, E. acervulina, E. brunetti, E. praecox, and E. necatrix. The level of lesion caused by these species in different area of the gut is associated with their level of pathogenicity (Morris et al. 2007).
Eimeria oocyst is the main cause of coccidiosis which get into chickens via ingestion of food, water and litter contaminated with oocyst (Shivaramaiah et al. 2014). The oocyst which grows on the fecal shed by infected birds can also be transported to the chicken house through personnel that move from house to house (Belli et al. 2006). The conditions under which most broilers and other birds that are commercially reared for meat grow also contribute to the easy spread of the disease.
Coccidia oocyst is a thick wall which is resistant to both mechanical and chemical damage coupled with proteolytic degradation (Mai et al. 2009). The infective ability of oocyst is due to its ability to sporulate. Sporulated oocysts are infectious while unsporulated oocysts are not (Lal et al. 2009). The sporulated oocyst can survive outside its host for 602 days while unsporulated oocysts can survive for about 7 months in the ceacum of their host (Quiroz-Castañeda and Dantán-González 2015). The thick wall of the oocyst has been associated with its bilayer structure which is composed of lipid and protein. The protein layer has been reported to provide the oocyst with great stability against extreme cold and heat while the lipid layer provides cushion against chemical damage (Belli et al. 2006).
Epidemiology of chicken coccidiosis
Coccidiosis disease is promoted by poor housing and management system of poultry (Musa et al. 2010). The disease is more rampant in the intensive deep litter system. This kind of system does not only support the breeding of oocyst but also increases the incidence of infection among chickens. Coccidia oocyst sporulate under warmth condition of about 25–30 °C with adequate aeration and water while dry condition at 10 °C delays sporulation (Mohammed and Sunday 2015). Coccidiosis affects chicken of all ages, but the infection begins at younger age when the immune system is immature. The disease affects both the intestine and caecum with incubation period of 5–6 days respectively (Musa et al. 2010). Coccidia infection outbreak occurs when chicks ingest large quantities of sporulated oocyst. Reduced food intake, bloody diarrhea and loss of weight are some of the symptoms associated with infected birds (Blake 2015). The severity of the disease is dependent on the number of Eimeria species that co-infect the birds. Among the seven species of Eimeria that infect chickens, E. tenella, E. brunetti, E. maxima and E. necatrix have been reported as highly pathogenic while E. praecox is the least pathogenic (Jadhav et al. 2011; Nematollahi et al. 2008). Coccidia oocysts are shed by infected chickens through their fecal droppings and these contaminate water, food and soil (Gharekhani et al. 2014).
Eimeria parasite and distribution in poultry
Among different diseases that infect poultry, parasitic diseases also play a key role especially among village chickens. Examples of common poultry parasites include; mites, lice, ticks, helminths, fleas and coccidia. Most poultry birds are infected by more than one intestinal parasite type and this also contributes to their wide distribution (Poulsen et al. 2000; Sandhu et al. 2009).
The prevalence of Eimeria parasite has been reported among different farms in various geographical region by several studies (Sultana et al. 2017; Györke et al. 2013; Gharekhani et al. 2014; Mohammed and Sunday 2015). Recent studies by Malatji et al. (2016) reported the prevalence rate of 29.46% of Eimeria parasite among local chickens of Limpopo and KwaZulu-Natal of South Africa. Mortality rate of 54.3, 31.7, 70.9 and 52.9% associated with Eimeria parasite have been reported in Turkey, India, Ethiopia and Nigeria respectively (Karaer et al. 2012; Sharma et al. 2009; Oljira et al. 2012 and Muazu et al. 2008).
Eimeria infection in chickens are due to co-infection of different Eimeria species and this causes mild to severe lesion (Jenkins et al. 2008). Different sites of the gastrointestinal tract are habited by specific chicken Eimeria species i.e.: E. acervulina develops in the duodenum, E. maxima and E. mitis grows in the middle of small intestine while E. tenella, E. brunetti and E. necatrix grows in the caeca, rectum and small intestine. The prevalence of Eimeria infection in chickens has also been reported to be influenced by favourable weather condition and the poultry management system (Etuk et al. 2004).
Identification and diagnosis of Eimeria parasite
Prior to the advent of molecular methods, traditional methods such as cross-immunity, characteristics lesions, site of development and pathogenicity were used in the identification of Eimeria species (Singla and Gupta 2012). However, the methods are time consuming, labour intensive and require high level of expertise (Shirley et al. 2005). Pathological and morphological analysis such as lesion site, oocysts shape and size could be used to confirm the presence of coccidiosis but the identification of precise Eimeria species is needful for the control of the disease as it reveals the level of resistance either to drug or vaccine (Lee et al. 2010). Although this method is still currently in use, they are complemented with molecular methods in most research.
Alternative method to the traditional method is the introduction of computational method called COCCIMORPH which uses oocyst morphology in the identification of Eimeria species (Castañón et al. 2007). Among the parameters which the software uses in the identification of Eimeria species include; curvature, geometry and texture. Kumar et al. (2014) reported corresponding agreement of COCCIMORPH with nested PCR-ITS-1 as they were both effective with E. acervulina and E. mitis though the computational approach was less sensitive to E. brunetti, E. tenella and E. praecox.
Molecular method uses PCR assay by amplification of specific gene in the DNA sequences of Eimeria parasite. ITS-1 and ITS-2 are sequences which are excised from rDNA precursor through post transcription. They have been widely used in the identification of all the seven species of Eimeria in chickens using specific primers (Haug et al. 2007, 2008; Hamidinejat et al. 2010; Jenkins et al. 2006). Although Lew et al. (2003) reported significant variation among E. maxima isolates of different samples indicating the use of two distinct primers for this species, ITS-1 is highly sensitive due to high number of rDNA repeats and provides diagnostic tool for accurate identification of Eimeria species in turkey and rabbit (Vrba et al. 2010; Cook et al. 2010; Oliveira et al. 2011). Targeting primers at conserved ribosomal DNA sequences (5.8S and 28S) have also been used in Eimeria species identification with high level of genetic variants (Morris et al. 2007; Cantacessi et al. 2008).
In addition to the use of ITS-1 and ITS-2, Random Amplified Polymorphic DNA (RAPD) have been used to develop Sequence Characterized Amplified Region (SCAR) primers for the identification of each Eimeria species (Fernandez et al. 2003). These primers have been tested for the amplification of Eimeria species. Fernandez et al. (2003) combined the SCAR primers for the seven species of Eimeria for the development of multiplex PCR assay which are used for simultaneously discrimination of all species of Eimeria infecting chickens in a single tube reaction. SCAR markers have since then been used by various studies in the detection of Eimeria species (Carvalho et al. 2011, Ogedengbe et al. 2011, Blake et al. 2008). The limitation of SCAR method is that it may be less sensitive as compared to ITS-1 and ITS-2 which are present in the multiple copies of Eimeria genome (Vrba et al. 2010).
To corroborate this, Kumar et al. (2014) compared different three PCR protocols for the identification of Eimeria species vis-à-vis nested PCR-ITS-1, Multiplex SCAR PCR in one tube and two tube reaction. The study confirmed the sensitivity of nested PCR- ITS-1 for Eimeria species identification while better result was also reported in multiplex SCAR PCR in two tube reaction as compared to one tube. The use of nested PCR-ITS-1 for the identification of Eimeria species has been employed in different studies (Lew et al. 2003; Kumar et al. 2015) though the protocol is not without its own limitation such as the time, cost and complexity associated with the use of two PCR steps (Kumar et al. 2014).
Despite the contribution of PCR-based method in the identification of Eimeria species, the limitation of this assay is the difficulty associated with extraction of DNA from the Eimeria oocyst. Eimeria oocyst processed from fecal samples are resistant to chemical agents and thus their disruption becomes imperative for quality DNA. Different chemical agents for oocyst disruption have been reported (Zhao et al. 2001; Haug et al. 2007; Carvalho et al. 2011).
Beyond the use of PCR-based method, quantitative assay such as real-time PCR (qPCR) amplification of ITS-1, ITS-2 and SCAR markers have been used in different studies to identify Eimeria species (Blake et al. 2008; Kawahara et al. 2008). Lalonde and Gajadhar (2011) reported that a qPCR assay with melting curve analysis and primers conserved in various protozoa could detect E. acervulina in a mixture of oocyst. Similarly, the study of Kirkpatrick et al. (2009) confirmed the identification of all the seven species of Eimeria from pure oocysts cultures using a high-resolution melting curve analysis with a qPCR directed at ITS-1 sequences. The cost associated with this assay has limited its routine application.
To minimize cost associated with molecular methods in Eimeria species identification, Loop-mediated Isothermal amplification (LAMP) has been developed as alternative approach (Barkway et al. 2011). The presence of isothermal enzymes and intercalating dyes in this technology means that reaction can be run without the use of thermocycler and electrophoresis. This has given the technology an edge over other molecular methods. Different studies on the use of LAMP assay for apicomplexan parasites detection has been reported (Karanis et al. 2007; He et al. 2009; Thekisoe et al. 2010; Sun et al. 2017). However, this technology still need much improvement for it to be a standard assay.
Despite the wide use of ITS-1 and ITS-2 in Eimeria identification, the only drawback is the intraspecific and intragenomic variations that exist in these genes which contribute to their poor species delineation. In view of this, Ogedengbe et al. (2011) described cytochrome c oxidase subunit 1 (COI) as highly effective in species delineation of different organism including Eimeria. Different studies on the use of COI in the identification of Eimeria species have been reported (Schwarz et al. 2009; Hafeez et al. 2016; Rathinam et al. 2015; Ogedengbe et al. 2018). The only limitation of this gene in species identification is that it has few reference sequences in the public data. Therefore, combination of multiple locus such as ITS and COI is a new approach currently being explored for the identification of Eimeria species.
Control measure of coccidiosis
Due to drastic effect of coccidiosis on the poultry, different control methods have been deployed. Thorough biosecurity coupled with the use of prophylactics were the first strategies deployed in the control of this disease. Synthetic drugs (Table 1) such as amprolium, nicarbazin, diclazuril, and toltrazuril were used effectively to control coccidiosis disease in poultry for many years (Shivaramaiah et al. 2014). The drugs target the sporozoite/merozoite developmental stage of the parasite. However, the constraint of this strategy in the control of coccidiosis disease is the emergence of drug resistant isolates of Eimeria parasite (Peek and Landman 2011). High percentage of field isolate of E. acervulina and E. maxima couple with E. tenella obtained from 28 farms in 12 states of the United State showed partial or complete resistance to renowned synthetics drugs-nicarbazin and narasin (Bafundo et al. 2008). Public pressure to reduce drugs in the food chain has led to search for alternative strategy to the control of coccidiosis (Peek and Landman 2011).
Among the alternative measures explored is the use of natural products (Table 2) which include probiotics, plant extracts and fungal extracts. Probiotics is the use of bacteria as feed to improve the immune system of the chicken against infection. Dalloul et al. (2005) reported the effectiveness of Lactobacillus-based probiotics, Primalac which reduced the oocyst shedding and increase T and B cell-specific cytokine against E. avervulina infection. In a similar manner, the study of Lee et al. (2007) confirmed the effectives of Pediococcus-based probiotics in improving performance against E. acervulina and E. tenella infection. Since then, a consistent report on the use of probiotics either alone or together with other supplements has been confirmed to reduce microscopic lesion in birds infected with coccidiosis (Chen et al. 2016; Ritzi et al. 2014).
Similarly, significant reduction in the mortality of birds infected with coccidiosis has been reported among different plant extracts (Drăgan et al. 2014; Gholamrezaie Sani et al. 2013; Habibi et al. 2016; Nghonjuyi et al. 2015). The antimalaria ‘artemisinin’ derived from the herb Artemisia annua has been reported to have damaging effects on the macrogametocyte of E. tenella by limiting the expression of sarcoplasmic-endoplasmic reticulum calcium ATPase enzyme (del Cacho et al. 2010). Increase body-weight and reduced lesion scores are some of the advantages of plants extracts reported in these studies. As against the background of rearing birds in a controlled environment before infecting them with Eimeria parasite, Chang et al. (2016) recently evaluated the field trial anticoccidial efficacy of Bidens pilosa in broiler chickens. The study confirmed increased body-weight, reduced lesion scores, decreased oocyst per gram of feaces in birds with feed supplemented with 0.025% of B. pilosa. The combined use of plant extracts and probiotics as anticoccidial has also been reported (Djezzar et al. 2014). Despite the success reported by plant extracts, little understanding about their mode of action and the concern on their safety and toxicity has limited their commercial usage.
For decades, vaccine has been used for the control of coccidiosis. Live non-attenuated vaccines which have a virulence has been proven effective against this disease (Shirley 1992). The first commercially produced live non-attenuated anticoccidial vaccine CocciVac and its variants CocciVac-B, CocciVac-D and Immucox have been highly successful and are still in use today (Jenkins et al. 2012; Milbradt et al. 2014). However, the risk of disease outbreak of these vaccines led to attenuated vaccines (Quiroz-Castañeda and Dantán-González 2015).
The virulence of attenuated anticoccidial vaccine is usually reduced. This is done by screening for more precocious Eimeria isolate i.e. isolates with shortened pre-patent period due to lack of one or more secondary schizogony compared to the Eimeria strain with normal life-cycle (Mathis et al. 2017). Although attenuated anticoccidial vaccines are still much in use today, their low degree of immune protection has called for their use with adjuvants (Ahmad et al. 2016). This has given room to recombinant and sub-unit vaccines.
Recombinant anticoccidial vaccines make use of Eimeria species antigens that have immunogenic properties to trigger effective immune response. However, the genetic diversity of this vaccine antigens and the inefficiency of the vaccine to tackle co-infection of Eimeria species has led to various modification of recombinant vaccines. Song et al. (2015a) reported the efficacy of multivalent epitope DNA vaccines against coccidiosis in chicken. The vaccine which was made up of four most effective T-cell epitopes of each Eimeria species antigen increased body weight gain, alleviated enteric lesion, reduced oocyst produced by infected birds and triggered anti-coccidial index of more than 170 against E. tenella, E. acervulina, E. maxima and E. necatrix (Song et al. 2015a). In a similar way, multivalent sub-unit vaccine which consists of recombinant antigens from four species of Eimeria (E. tenella, E. acervulina, E. maxima and E. necatrix) has been reported to provide partial protection against coccidiosis caused by these species (Song et al. 2015b). Different studies on the use of vaccines in the control of coccidiosis in chickens have been reported (Huang et al. 2015; Yin et al. 2015).
To further combat the menace of coccidiosis and reduce resistance to the control methods, different strategies such as shuttle and rotation programme have been employed. This entails the combination of different drugs (synthetic or ionophores) of different mode of actions. This has increase the effectiveness of anticoccidial drugs but has no control over the emergence of resistance among the parasite species (Lee et al. 2009). Similarly, (Stringfellow et al. 2011) suggested a combined strategy of proper and uniform vaccine administration couple with boosting the intestinal tract of younger birds with pathogen-free microbiota. Recent study also reported increased body weight and decreased lesion scores among birds treated with both vaccines and water-applied probiotics (Ritzi et al. 2016).
Threats posed by genetic and antigenic diversity of Eimeria parasite on coccidiosis control
The emergence of anticoccidial-resistant Eimeria species has not only heightened the public concern about this parasite but has also led to consistent modification in the control measure and strategy against coccidiosis. Genetic diversity among Eimeria species as shown in Table 3 is a potential contributor to Eimeria resistance to anticoccidial.
Genetic diversity entails the emergence of new variants among the species of Eimeria. Different approaches such as single or multilocus sequence typing, restriction fragment length polymorphism (PCR-RFLP), amplified fragment length polymorphism (AFLP) and random amplified polymorphic DNA (RAPD) and variable number tandem repeat (VNTR) have unraveled the differences among Eimeria species isolates from various regions (Ogedengbe et al. 2011; Blake et al. 2011; Lim et al. 2012; Pegg et al. 2016).
Recent study by Tan et al. (2017) reported genetic diversity among eight E. tenella isolates from different region of Hubei China and this formed two branched cluster based on their geographical distribution with phylogenetic branch length of 0.49–0.75.
Moreover, the report of Blake et al. (2015) indicated genetic diversity and population structure among E. tenella in different regions- India, Egypt, Libya and Nigeria. The author also indicated low level of haplotypes among E. tenella in northern India (Haryana, Punjab, Utterak-hand and Uttar Pradesh) as compared with southern India (Kerala, Karnataka, Andhra Pradesh and Tamil Nadu) with high and unique haplotypes.
Exploring the risk factors associated with coccidiosis, Prakashbabu et al. (2017) reported diversity in the distribution of Eimeria species according to poultry unit size, management and system within and between northern and southern India.
Further comparative study into Internal Transcribed Spacer (ITS-1 and ITS-2) sequences of Eimeria has shown three Operational Taxonomic Units (OTUx, OTUy and OTUz) which share similarity with some known species of Eimeria (Godwin and Morgan 2015). These OTUs have been reported to be abundant in some geographical regions but their spread to other regions is a concern as they could limit the effectiveness of current live vaccines.
Similarly, apical membrane antigen 1(AMA-1) has been reported as protective antigen in sub-unit vaccine development against myriads of apicomplexan parasites including E. tenella, E. maxima and P. falciparum (Blake et al. 2011; Drew et al. 2012; Jiang et al. 2012). As against the background of allelic polymorphism among AMA-1 which has limited their use in P. falciparum, AMA-1 is a potential candidate for E. tenella vaccine due to its inhibitory capacity on parasite invasion (Jiang et al. 2012). Although low level of allelic polymorphism has been reported among AMA-1 of E. tenella and E. maxima, in vivo studies have also shown some degree of strain-specific immune escape (resistance) among the vaccine candidate for E. tenella, E. acervulina and E. maxima (Awad et al. 2013; Healer et al. 2004; Smith et al. 2002; Wu et al. 2014). Therefore, allelic diversity in this candidate vaccine antigen is a potential constraint to the effectiveness of subunit vaccine use against coccidiosis in poultry.
Conclusion
Despite the key role poultry industry plays in the economy of each nation, the menace of coccidiosis has been a limiting factor. Though the fight against chicken coccidiosis has been on for several decades, the resurgence of this disease coupled with new variants among Eimeria parasite in different geographical areas demands a fresh attention on their control measures. The current methods of anticoccidial drugs, vaccines and strict management practice have proven effective but the emergence of genetic and antigenic diversity is a major threat on the effectiveness of the present anticoccidial vaccines and drugs. To design an effective vaccine, it is imperative to understand the dynamism in the evolution of diversity among genes that encodes potential vaccine antigens at the genome level along with the associated factors that drive this diversity.
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Financial support by the National Research Foundation of South Africa (Grant Numbers: 112886 and 112768) is gratefully acknowledged.
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Fatoba, A.J., Adeleke, M.A. Diagnosis and control of chicken coccidiosis: a recent update. J Parasit Dis 42, 483–493 (2018). https://doi.org/10.1007/s12639-018-1048-1
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DOI: https://doi.org/10.1007/s12639-018-1048-1