Coccidiosis in commercial broilers in Brazil between 2012 and 2019: main species and degrees of injury

Gazoni, Fabio; Matte, Fabrizio; Chiarelli-Adorno, Felipe; Mariely-Jaguezeski, Antonise; Tellez-Isaias, Guillermo; Schafer-da-Silva, Aleksandro; Gazoni, Fabio; Matte, Fabrizio; Chiarelli-Adorno, Felipe; Mariely-Jaguezeski, Antonise; Tellez-Isaias, Guillermo; Schafer-da-Silva, Aleksandro

doi:10.21929/abavet2021.2

Services on Demand

Journal

Article

Indicators

Cited by SciELO
Access statistics

Abanico veterinario

On-line version ISSN 2448-6132Print version ISSN 2007-428X

Abanico vet vol.11 Tepic Jan./Dec. 2021 Epub May 21, 2021

https://doi.org/10.21929/abavet2021.2

Original article

Coccidiosis in commercial broilers in Brazil between 2012 and 2019: main species and degrees of injury

Fabio Gazoni¹
http://orcid.org/0000-0001-5118-3060

Fabrizio Matte¹
http://orcid.org/0000-0002-5308-5656

Felipe Chiarelli-Adorno¹
http://orcid.org/0000-0001-5894-8513

Antonise Mariely-Jaguezeski²
http://orcid.org/0000-0002-9253-9526

Guillermo Tellez-Isaias³
http://orcid.org/0000-0002-2416-2747

Aleksandro Schafer-da-Silva⁴
http://orcid.org/0000-0001-5459-3823

^¹Vetanco do Brasil Imp. e Exp. LTDA, Chapecó, SC, Brazil

^²Federal University of Santa Maria, RS, Brazil.

^³Department of Poultry Science, University of Arkansas, Fayetteville, AR 72704, United States of America.

^⁴Department of Animal Science, State University of Santa Catarina (UDESC), Chapecó, Brazil.

ABSTRACT:

The purpose of the present study was to determine the occurrence of coccidiosis in broilers, detect the most commonly occurring species of Eimeria spp, and parasitic burdens in industrial poultry in Brazil from 2012 to 2019. We studied 13,648 birds between 9-49 days of age at 82 companies in 13 Brazilian states. Birds were randomly selected (3-6 birds/aviary) and euthanized. Macroscopic lesions were analyzed, and the intestinal mucosa was scraped to count E. maxima oocysts. The classification of species was based on the size of the oocysts. We also quantified the infectious burden using a scoring system. Subclinical coccidiosis (E. maxima micro) was detected in an average of 34.8%, E. acervulina (16.1%), E. maxima (7.9%), and E. tenella (4.1%) were also identified with annual fluctuations. The count of oocysts was within score 1 (1-10 oocysts/bird) in 47.5-84.4% of the cases; followed by score 2 (11-20), 3 (21-40) and 4 (over 41 oocysts/bird). Subclinical coccidiosis is a cause for concern, with 3.5 out of every ten birds being infected. This is a factor responsible for the lower productive performance of broilers.

Keywords: Coccidiosis; Eimeria acervulina; Eimeria maxima; Eimeria tenella; prevalence

RESUMEN:

El propósito del presente estudio fue determinar la frecuencia de la coccidiosis en pollos de engorde, detectar las especies más comunes de Eimeria spp y cargas parasitarias en aves comerciales en Brasil de 2012 a 2019. Estudiamos 13,648 aves entre 9 y 49 días de edad en 82 empresas en 13 estados brasileños. Las aves se seleccionaron al azar (3 a 6 aves / aviario) y se sacrificaron por eutanasia. Se analizaron las lesiones macroscópicas y se raspó la mucosa intestinal para el conteo de ooquistes de E. maxima. La clasificación de especies se basó en el tamaño de los ooquistes. También cuantificamos la carga infecciosa mediante un sistema de puntuación. Se detectó coccidiosis subclínica (E. maxima micro) en un promedio de 34.8%. E. acervulina (16.1%), E. maxima (7.9%) y E. tenella (4.1%) también se identificaron con fluctuaciones anuales. El conteo de ooquistes estuvo dentro de la puntuación 1 (1 a 10 ooquistes / ave) en el 47.5 al 84.4% de los casos; seguido de una puntuación 2 (11 a 20), 3 (21 a 40) y 4 (más de 41 ooquistes / ave). La coccidiosis subclínica es motivo de preocupación, ya que 3.5 de cada diez aves estaban infectadas. Este es un factor responsable del menor rendimiento productivo de los pollos de engorde.

Palabras clave: Coccidiosis; Eimeria acervulina; Eimeria maxima; Eimeria tenella; prevalencia

INTRODUCTION

In commercial and intensive poultry breeding, Eimeria spp. are a ubiquitous protozoan, widespread on six continents (^{Chapman et al., 2016}; ^{Clark et al., 2016}). Seven species of Eimeria have been recognized (E. acervulina, E. brunetti, E. maxima, E. mitis, E. necatrix, E. praecox, and E. tenella). They differ in pathogenicity (^{McDougald, 2008}). Eimeria infection birds can reduce growth performance via the impaired intestinal function (^{Kim et
al., 2017}; ^{Lu et
al., 2019}). More commonly, the birds remain asymptomatic until there is an infection by a large number of coccidia or some other aggravating pathology (^{Williams, 2005}; ^{Chapman et al., 2016}; ^{Gazoni et al., 2017}). It was estimated in the early 2000s that the disease had an annual economic impact of approximately U.S. $3 billion, with losses to producers and the worldwide poultry industry (^{Dalloul and Lillehoj,
2006}). In Romania in 2016, researchers found that total economic losses per 24 flocks of 18,000 chicks were about €37,948.2, with an average of €3,162.4 per flock. These losses were caused by mortality (34.8%) and poor feed conversion (65.2%) due to coccidiosis (^{Györke
et al., 2016}).

Traditionally, the diagnosis of farms occurs through the detection and enumeration of oocysts excreted in the feces, in addition to measuring bird dimensions. Post-mortem investigators evaluate the affected intestinal portion and the lesions (^{Long and Joyner, 1984}). The specific diagnosis of Eimeria infections in broilers is fundamental to a better understanding of the disease's epidemiology and dynamics and is necessary for the prevention, surveillance, and effective control (^{Morris and Gasser, 2006}; ^{Gazoni, et al. 2017}).

Subclinical coccidiosis is commonly seen in poultry farms in Brazil, and accurate diagnosis is essential for tracing interventions, mainly because of problems with resistance to coccidiostats agents (^{Gazoni
et al., 2020}). Therefore, this study's objective was to determine the annual occurrence of Eimeria infection in industrial broilers from 2012 to 2019 in Brazil.

MATERIALS AND METHODS

Animals and data collection

Monitoring of coccidiosis was carried out in 82 companies in the states of Rio Grande do Sul, Santa Catarina, Paraná, Mato Grosso do Sul, São Paulo, Minas Gerais, Rio de Janeiro, Goiás, Distrito Federal, Alagoas, Para, Paraiba and Pernambuco from 2012 and 2019, using 13,648 broilers. Brazil is a continental country with a very particular climatic variation for each state, because of this, it was not raised in consideration of climatic information. The data were released by the Intestinal Health Program (PSI) of Vetanco do Brasil, in order to obtain the percentage of affected birds and their degree of classification by injury scores in collaboration with researchers from the State University of Santa Catarina (UDESC). The birds were from the Cobb 500 and Aviagen lines and were 9-49 days old. They were provided feed prepared by their respective companies, without any interference from the evaluator in terms of formulation or use of performance enhancers and anticoccidial agents. The most commonly used anticoccidial program is the dual system, where an active ingredient is used in the first phase (1^st to 21^st day of age), and another is used in the second phase (22^nd day to 3 days before slaughter), the broilers do not receive vaccines programs coccidiosis, in order to reduce the possibility of the appearance of antimicrobial resistance.

Sample collection

We monitored the intestinal health of broilers using 3-6 birds per flock (aviary). Birds were randomly selected from three different points in the aviary (entrance, middle, and bottom). These birds were euthanized by cervical dislocation, followed by dissection for sample collection and visual evaluation.

Macroscopic tissue evaluation

In the gastrointestinal tract, the presence of lesions caused by E. acervulina, E. maxima, and E. tenella was observed, for example figure 1. When present, lesions were classified according to their degree of intensity, according to the methodology of ^{Johnson and Reid (1970)}, where the score 0 indicates the absence of injury, and score 4 indicates severe damage.

Figure 1 Presence of lesions caused by E. acervulina, E. maxima, and E. tenella.

Mucosa scraping technique and oocyst count

To evaluate E. maxima micro, the intestinal mucosa scraping technique was used to count oocysts, performed in the intestinal portion surrounding Meckel's diverticulum. The fecal content was deposited on a slide, covered by a coverslip, and visualized in five fields (extremities and center) for counting oocysts under optical microscopy (100x). Four scores were used for the classification, according to ^{Vetanco do Brasil (2011)}, where score 0 represented absence of oocysts; score 1 represented 1-10 oocysts; score 2 represented 11-20 oocysts; score 3 represented 21-40 oocysts, and score 4 meant more than 41 oocysts, for example figure 2 .

Figure 2 Four scores were used for the classification for E. maxima micro.

RESULTS

The annual occurrence showed significant differences between species; while one was high, the others were smaller in the year in question. Subclinical coccidiosis had the most increased occurrence (average of 34.8%) during the evaluated period (2012- 2019), revealing greater frequency and dissemination in the Brazilian poultry industry. For macroscopic lesions attributed to E. acervulina, E. maxima, and E. tenella, the average occurrence was 16.1%, 7.9%, and 4.1%, respectively. We also observed that none of the Eimeria species showed linear behavior; instead, they demonstrated fluctuations across years: sometimes, there was an increase. Sometimes, there was a decrease in occurrence (Table 1).

Considering each species across periods, we observed that, in 2012, the occurrences of E. maxima (22.2%) and E. tenella (10.0%) were higher, and they were lower in the other years. E. acervulina had a significant increase in 2016, reaching 30.5% of occurrence, with a gradual decrease after that date (9.7% in 2019). E. maxima micro showed almost incremental growth until 2017 (from 28.8 to 45.5%), remaining with a high annual percentage in the subsequent years (38.0-42.6%). These results are shown in Table 1.

Table 1 Eimeria species and percentage of eimeriosis in broilers between 2012 to 2019.

Species	Annual ocurrence (%)
Species	2012	2013	2014	2015	2016	2017	2018	2019	Average
E. acervulina	9.3	18.7	13.6	13.5	30.5	16.6	17.1	9.7	16.1
E. maxima	22.2	7.8	4.8	5.9	8.1	4.4	4.9	5.4	7.9
E. tenella	10.0	5.0	4.1	2.0	4.5	2.3	1.7	3.1	4.1
E. maxima, micro	28.8	29.1	25.8	33.5	34.7	45.5	38.0	42.6	34.8

In terms of lesion scores, in practically every year and for all species, the oocyst count was within score 1, followed by scores 2, 3, and 4 (this was rarely higher than 3, and when it occurred, it was observed for E. maxima micro). Score 4 was infrequent, often resulting in a null value. The percentage between species and between years did not follow a pattern. Instead it varied for both species and year (Table 2).

Table 2 Percentage of coccidiosis scores (Eimeria) obtained between 2012 and 2019 in broilers from 9 to 49 days in Brazilian agribusiness.

Year	Species	Score(%)
		1	2	3	4
2012	E. acervulina	48.7	39.5	11.8	0.0
	E. maxima	56.1	35.6	7.2	1.1
	E. tenella	79.1	17.2	1.8	1.8
	E. maxima, micro	73.0	9.8	9.4	7.9
2013	E. acervulina	57.0	32.9	9.0	1.1
	E. maxima	69.1	24.1	5.8	1.0
	E. tenella	84.4	12.3	3.3	0.0
	E. maxima, micro	58.8	14.4	7.8	19.0
2014	E. acervulina	65.9	26.5	7.6	0.0
	E. maxima	64.7	25.2	5.9	4.2
4.2	E. tenella	76.5	19.6	3.9	0.0
	E. maxima, micro	65.3	14.6	4.2	15.9
2015	E. acervulina	62.2	27.4	8.9	1.5
	E. maxima	65.8	30.7	3.5	0.0
	E. tenella	69.2	17.9	12.8	0.0
	E. maxima, micro	76.2	12.8	2.5	8.6
2016	E. acervulina	51.0	28.4	18.6	2.0
	E. maxima	59.3	33.3	3.7	3.7
	E. tenella	66.7	13.3	13.3	6.7
	E. maxima, micro	70.7	14.7	7.8	6.9
2017	E. acervulina	81.1	13.8	5.1	0.0
	E. maxima	79.5	15.1	5.5	0.0
	E. tenella	57.9	31.6	10.5	0.0
	E. maxima, micro	71.5	10.3	1.9	16.3
2018	E. acervulina	53.6	41.2	5.2	0.0
	E. maxima	66.7	28.3	5.0	0.0
	E. tenella	76.2	23.8	0.0	0.0
	E. maxima, micro	84.2	6.4	2.3	7.0
2019	E. acervulina	75.8	18.7	5.5	0.0
	E. maxima	66.7	29.4	3.9	0.0
	E. tenella	65.5	34.5	0.0	0.0
	E. maxima, micro	47.5	22.5	2.5	27.5

DISCUSSION

We reported the occurrence of coccidiosis in the Brazilian poultry industry for over seven years. Studies reporting epidemiological characteristics for coccidiosis in Brazil are rare. It is important to pay attention to the species found in the territory; our findings agree with those of other authors who frequently reported E. acervulina, E. maxima and E. tenella (^{Moraes
et al., 2015}; ^{Chapman et al., 2016}; ^{Kim et al., 2017}); these species, in addition to being reported most commonly, are the ones that commonly develop resistance to synthetic drugs (^{Shivaramaiah
et al., 2014}).

All species of Eimeria are widespread on the six continents. However, there may be a regional division in the genetic diversity and population structure of species (^{Prakashbabu
et al., 2017}); or even, as described by ^{Clark et al. (2016)}, there may be genetic variants between the southern and northern hemispheres, representing a risk to food security and animal welfare if it spreads to previously absent areas. This variation is believed to be attributable to the use of anticoccidial drugs and vaccines (^{Prakashbabu et al., 2017}).

A study regarding the prevalence of coccidiosis in Santa Catarina (B.R.) using PCR showed that 96% of the farms were positive for Eimeria, with seven species identified: E. maxima (63.7%) and E. acervulina (63.3%), E. tenella (54.6%), E. mitis (38.6%), E. praecox (25.1%), E. necatrix (24.3%) and E. brunetti (13.1%), with an average of 2.96 species per farm (^{Moraes
et al., 2015}). Another study in a small region of the state of Tocantins reported the occurrence of coccidiosis in all farms, with the presence of E. maxima, E. acervulina, E. mitis, and E. tenella (^{Toledo et al., 2011}). The high preponderance of an Eimeria species may indicate its resistance to the drugs usually exposed, as is the case of E. tenella studied in Nigeria (^{Ojimelukwe et al., 2018}) E. maxima micro and E. acervulina in the present study and the others reported in Brazil. The diagnosis is important and necessary to outline strategies, as according to ^{Teeter
et al. (2008)}, it was observed that for each point of increase in the microscopic evaluation of coccidiosis lesions, daily weight gain decreased 1.5% of the body weight (g) during the six-day challenge period. Therefore, it is essential to know the degree of intestinal damage to quantify the birds' performance.

The rapid intestinal replication cycle (4 to 6 days) and the oral/fecal route make coccidiosis a severe problem of intensive breeding, caused by recurrent infections and resistance to coccidiostats agents (^{Shivaramaiah et al., 2014}). Without effective control, the number of parasites can increase to the point of clinical coccidiosis. To avoid resistance, drug rotation, and vaccination programs are carried out (^{Lan et al.,
2017}). The rotation of coccidiostats agents can help clarify the significant oscillations of occurrence between Eimeria species, as verified in this study.

Vaccination is the most interesting prophylactic measure; however, it is used only in broiler breeders (^{Abdul Rasheed and
Matsler, 2020}) and laying hens (^{Chapman et al., 2014}). Commercial in ovo vaccination for coccidiosis in broilers has become widely accepted in the U.S. poultry industry; however, its effects on performance have yet to be studied (^{Sokale et
al., 2020}). It is essential to emphasize the importance of studies of species prevalence for the development of regional vaccines, as in this study. The use of antimicrobials has been analyzed with a view to replacing them in order to avoid the resistance problem, and several alternatives have been proposed (^{Kim et al.,
2017}; ^{Bortoluzzi et al., 2019}; ^{Lu et al., 2019}; ^{Park et al., 2020}). The low amount of oocysts present in the samples in this study (score 1) and the few observations of the zero score (no oocysts/sample) may indicate the effectiveness of chemical anticoccidials' strategic use via feed.

In addition to the loss of performance, coccidiosis is a predisposing factor for an even more harmful pathology in birds, such as necrotic enteritis (^{Williams, 2005}; ^{Adhikari et a}). E. maxima's presence was considered by ^{Paiva and McElroy (2014)}) to be an essential risk factor for promoting Clostridium perfringens, and this must be considered in the search for effective control methods for farms in Brazil.

For herd monitoring, the mucosa visualization and oocyst counting, and classification technique remains the most viable for the Brazilian agribusiness, to the detriment of the qPCR test, also available for diagnosis and quantification (^{Velkers et al.,
2010}). This would considerably increase the monitoring and require differential care of the samples.

CONCLUSIONS

In conclusion, subclinical coccidiosis has a worrying prevalence, with every ten birds 3.5 having coccidiosis. This is one of the factors that likely causes reductions in the broiler batches' productive performance as well as being a predisposing factor for clostridiosis. Because attempts to eradicate the parasite by quarantine, disinfection, and sanitation have not been successful (^{McDougald, 2008}), it is of fundamental importance that professionals in the poultry sector to carry out subclinical coccidiosis assessments routinely, thereby being able to intervene if necessary, to maintain the productive performance of broilers.

LITERATURA CITADA

Abdul Rasheed MS, Matsler PL. 2020. Assessment of protection against Eimeria tenella in broiler breeders conferred by a live anticoccidial vaccine and effects of vaccination on early pullet growth. Journal Applied of Poultry Research. 29(2):447-454. ISSN: 1056-6171. https://doi.org/10.1016/j.japr.2020.02.002 [ Links ]

Adhikari P, Kiess A, Adhikari R, Jha R. 2020. An approach to alternative strategies to control avian coccidiosis and necrotic enteritis. Journal Applied of Poultry Research. 29(2):515-534. ISSN: 1056-6171. https://doi.org/10.1016/j.japr.2019.11.005 [ Links ]

Bortoluzzi C, Fernandes JIM, Doranalli K, Applegate TJ. 2019. Effects of dietary amino acids in ameliorating intestinal function during enteric challenges in broiler chickens. Animal Feed Science and Technology. 262:114383. ISSN: 0377-8401. https://doi.org/10.1016/j.anifeedsci.2019.114383 [ Links ]

Chapman HD, Jeffers TK. 2014. Vaccination of chickens against coccidiosis ameliorates drug resistance in commercial poultry production. International Journal for Parasitology: Drugs and Drug Resistance. 4(3):214-217. ISSN: 0020-7519. https://doi.org/10.1016/j.ijpddr.2014.10.002 [ Links ]

Chapman HD, Barta JR, Hafeez MA, Matsler P, Rathinam T, Raccoursier M. 2016. The epizootiology of Eimeria infections in commercial broiler chickens where anticoccidial drug programs were employed in six successive flocks to control coccidiosis. Poultry Science. 95(8):1774-1778. ISSN: 0032-5791. https://doi.org/10.3382/ps/pew091 [ Links ]

Clark EL, Macdonald SE, Thenmozhi V, Kundu K, Garg G, Kumar S, Nolan MJ, Sudhakar NR, Adebambo AO, Lawal IA, Álvarez Zapata R, Awuni JA, Chapman HD, Karimuribo E, Mugasa CM, Namangala B, Rushton J, Sao X, Kumarasamy Thangaraj, Srinivasa Rao AS, Tewari AK, Banerjee PS, Raj GD, Raman M, Tomley FM, Blake DP. 2016. Cryptic Eimeria genotypes are common across the southern but not northern hemisphere. International Journal for Parasitology. 46(9):537-544. ISSN: 0020-7519. https://doi.org/10.1016/j.ijpara.2016.05.006 [ Links ]

Dalloul RA, Lillehoj HS. 2006. Poultry coccidiosis: recent advancements in control measures and vaccine development. Expert Review of Vaccines. 2006(5):143-163. ISSN: 1476-0584. https://doi.org/10.1586/14760584.5.1.143 [ Links ]

Gazoni FL, Adorno FC, Matte F, Malta T, Felin MR, Urbano T, Zampar A, Hernandez- Velasco X, Tellez G. 2017. Study of the correlation between intestinal health and prevalence of coccidiosis in broiler chickens of brazilian agribusinesses between the years 2015 and 2016. International Journal of Poultry Science. 16(10):381-386. ISSN: 1682-8356. https://doi.org/10.3923/ijps.2017.381.386 [ Links ]

Gazoni FL, Adorno FC, Matte F, Alves AJ, Campagnoni IDP, Urbano T, da Silva AS. 2020. Correlation between intestinal health and coccidiosis prevalence in broilers in Brazilian agroindustries. Parasitology International. 76:102027. ISSN: 1383-5769. https://doi.org/10.1016/j.parint.2019.102027 [ Links ]

Györke A, Kalmár Z, Pop, LM, Şuteu OL. 2016. The economic impact of infection with Eimeria spp. in broiler farms from Romania. Revista Brasileira de Zootecnia. 45(5):273-280. ISSN: 1806-9290. https://doi.org/10.1590/S1806-92902016000500010 [ Links ]

Johnson J, Reid WM. 1970. Anticoccidial Drugs: lesion scoring techniques in battery and floor-pen experiments with chickens. Experimental Parasitology. 28:30-36. ISSN: 0014-4894. https://doi.org/10.1016/0014-4894(70)90063-9 [ Links ]

Kim E, Leung H, Akhtar N, Li J, Barta JR, Wang Y, Kiarie E. 2017. Growth performance and gastrointestinal responses of broiler chickens fed corn-soybean meal diet without or with exogenous epidermal growth factor upon challenge with Eimeria. Poultry Science. 96(10):3676-3686. ISSN: 0032-5791. https://doi.org/10.3382/ps/pex192 [ Links ]

Lan LH, Sun B.B., Zuo BXZ, Chen XQ, Du AF. 2017. Prevalence and drug resistance of avian Eimeria species in broiler chicken farms of Zhejiang province, China. Poultry Science. 96(7):2104-2109. ISSN: 0032-5791. https://doi.org/10.3382/ps/pew499 [ Links ]

Long PL, Joyner LP. 1984. Problems in the identification of species of Eimeria. The Journal of Protozoology. 31(4):535-541. ISSN:1550-7408. https://doi.org/10.1111/j.1550-7408.1984.tb05498.x [ Links ]

Lu Z, Thanabalan A, Leung H, Akbari Moghaddam Kakhki R, Patterson R, Kiarie EG. 2019. The effects of feeding yeast bioactives to broiler breeders and/or their offspring on growth performance, gut development, and immune function in broiler chickens challenged with Eimeria. Poultry Science. 98(12):6411-6421. ISSN: 0032-5791. https://doi.org/10.3382/ps/pez479 [ Links ]

McDougald LR. 2008. “Protozoal infections”. In: Saif YM, Fadly AM, Glisson JR, McDougald LR, Nolan LK, Swayne DE. Editors. Diseases of Poultry. 12th ed. Ames, Iowa, Blackwell Publishing. Pp. 1067. ISBN-13:978-0-8138-0718-8 [ Links ]

Moraes JC, França M, Sartor AA, Bellato V, de Moura AB, Magalhães MDLB, Miletti LC. 2015. Prevalence of Eimeria spp. in broilers by multiplex PCR in the southern region of Brazil on two hundred and fifty farms. Avian Diseases. 59(2):277-281. ISSN: 0005-2086. https://doi.org/10.1637/10989-112014-Reg [ Links ]

Morris GM, Gasser RB. 2006. Biotechnological advances in the diagnosis of avian coccidiosis and the analysis of genetic variation in Eimeria. Biotechnology Advances. 24(6):590-603. ISSN: 0734-9750. https://doi.org/10.1016/j.biotechadv.2006.06.001 [ Links ]

Ojimelukwe AE, Emedhem DE, Agu GO, Nduka FO, Abah AE. 2018. Populations of Eimeria tenella express resistance to commonly used anticoccidial drugs in southern Nigeria. International Journal of Veterinary Science and Medicine. 6(2):192-200. ISSN: 2314-4599. https://doi.org/10.1016/j.ijvsm.2018.06.003 [ Links ]

Paiva D, McElroy A. 2014. Necrotic enteritis: applications for the poultry industry. Journal Applied of Poultry Research. 23:557-566. ISSN: 1056-6171. https://doi.org/10.3382/japr.2013-00925 [ Links ]

Park I, Lee Y, Goo D, Zimmerman NP, Smith AH, Rehberger T, Lillehoj HS. 2020. The effects of dietary Bacillus subtilis supplementation, as an alternative to antibiotics, on growth performance, intestinal immunity, and epithelial barrier integrity in broiler chickens infected with Eimeria maxima. Poultry Science. 99(2):725-733. ISSN: 0032- 5791. https://doi.org/10.1016/j.psj.2019.12.002 [ Links ]

Prakashbabu BC, Thenmozhi V, Limon G, Kundu K, Kumar S, Garg R, Banerjee PS, Clark EL, Srinivasa Rao ASR , Raj DG, Raman M, Banerjee PS , Tomley FM, Guitian J, Blake DP. 2017. Eimeria species occurrence varies between geographic regions and poultry production systems and may influence parasite genetic diversity. Veterinary Parasitology. 233:62-72. ISSN: 1873-2550. https://doi.org/10.1016/j.vetpar.2016.12.003 [ Links ]

Shivaramaiah C, Barta RJ, Hernandez-Velasco X, Tellez G, Hargis BM. 2014. Coccidiosis: recent advancements in the immunobiology of Eimeria species, preventive measures, and the importance of vaccination as a control tool against these Apicomplexan parasites. Veterinary Medicine. 5:23-34. ISSN: 2230-2034. https://doi.org/10.2147/VMRR.S57839 [ Links ]

Sokale AO, Williams CJ, Triplett MD, Hoerr FJ, Peebles ED. 2020. Effects of stage of broiler embryo development on coccidiosis vaccine injection accuracy, and subsequent oocyst localization and hatchling quality. Poultry Science. 99(1):189-195. ISSN: 0032-5791. https://doi.org/10.3382/ps/pez592 [ Links ]

Teeter RG, Beker A, Brown C, Broussard C, Fitz-Coy S, Radu J, Newman L. (2008). Transforming coccidiosis-mediated lesion scores into production and calorific cost. Proc. 23rd World Poult. Congr., Brisbane, Australia. 29.06.2008-04.07.2008. Pp.18-21. https://wenku.baidu.com/view/9df3d94fe45c3b3567ec8ba4.html [ Links ]

Toledo GA, Almeida JDDM, Almeida KDS, Freitas FLDC. 2011. Coccidiosis in broiler chickens raised in the Araguaína region, State of Tocantins, Brazil. Revista Brasileira de Parasitologia Veterinaria. 20(3):249-252. ISSN 0103-846X. http://dx.doi.org/10.1590/S1984-29612011000300014 [ Links ]

Velkers FC, Blake DP , Graat EAM, Vernooij JCM, Bouma A, De Jong MCM Stegeman JA. 2010. Quantification of Eimeria acervulina in faeces of broilers: Comparison of McMaster oocyst counts from 24 h faecal collections and single droppings to real-time PCR from cloacal swabs. Veterinary Parasitology. 169(1-2):1-7. ISSN: 0304-4017. https://doi.org/10.1016/j.vetpar.2010.01.001 [ Links ]

Vetanco do Brasil. 2011. Programa de Saúde Intestinal. Padrão microscópio de escore para E. maxima. Pp. 20 -21. https://www.vetanco.com/br/publicacoes-tecnicas/ [ Links ]

Williams RB. 2005. Intercurrent coccidiosis and necrotic enteritis of chickens: rational, integrated disease management by maintenance of gut integrity. Avian Pathology. 34(3):159-180. ISSN: 0307-9457. https://doi.org/10.1080/03079450500112195 [ Links ]

Received: May 22, 2020; Accepted: December 22, 2020; Published: January 04, 2021

Code:2020-86

Este es un artículo publicado en acceso abierto bajo una licencia Creative Commons