avAbanico veterinarioAbanico vet2007-428X2448-6132Sergio Martínez González10.21929/abavet2021.200101Artículos originalesCoccidiosis en pollos de engorda comerciales en Brazil entre 2012 y 2019: especies principales y grados de daño0000-0001-5118-3060GazoniFabio10000-0002-5308-5656MatteFabrizio10000-0001-5894-8513Chiarelli-AdornoFelipe10000-0002-9253-9526Mariely-JaguezeskiAntonise20000-0002-2416-2747Tellez-IsaiasGuillermo30000-0001-5459-3823Schafer-da-SilvaAleksandro4Vetanco do Brasil Imp. e Exp. LTDA, Chapecó, SC, BrazilVetanco do BrasilChapecóBrazilFederal University of Santa Maria, RS, Brazil.Universidade Federal de Santa MariaFederal University of Santa MariaBrazilDepartment of Poultry Science, University of Arkansas, Fayetteville, AR 72704, United States of America.University of ArkansasDepartment of Poultry ScienceUniversity of ArkansasFayettevilleUSADepartment of Animal Science, State University of Santa Catarina (UDESC), Chapecó, Brazil.Universidade do Estado de Santa CatarinaDepartment of Animal ScienceState University of Santa Catarina (UDESC)ChapecóBrazil
Autor para correspondencia: Rua Raimundo Zanella, 400D - Distrito Industrial Flávio Baldissera - CEP 89813-824. Chapecó, Brazil. gazoni@vetanco.com.br, fabrizio@vetanco.com.br, chiarelli@vetanco.com.br,antonise.jaguezeski@gmail.com, gtellez@uark.edu,aleksandro_ss@yahoo.com.br
Clave: 2020-86.
30042021Jan-Feb202111e1012205202022122020Este es un artículo publicado en acceso abierto bajo una licencia Creative CommonsRESUMEN:
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.
En la cría de aves de corral comercial e intensiva, Eimeria spp., son un protozoo ubicuo, muy extendido en seis continentes (Chapman et al., 2016; Clark et al., 2016). Se han reconocido siete especies de Eimeria (E. acervulina, E. brunetti, E. maxima, E. mitis, E. necatrix, E. praecox y E. tenella). Se diferencian en patogenicidad (McDougald, 2008). Las aves infectadas por Eimeria pueden reducir el rendimiento del crecimiento a través de la función intestinal deteriorada (Kim et al., 2017; Lu et al., 2019). Más comúnmente, las aves permanecen asintomáticas hasta que hay una infección por un gran número de coccidios o alguna otra patología agravante (Williams, 2005; Chapman et al., 2016; Gazoni et al., 2017). A principios de la década de 2000 se estimó que la enfermedad tenía un impacto económico anual de aproximadamente US $ 3 mil millones, con pérdidas para los productores y la industria avícola mundial (Dalloul y Lillehoj, 2006). En Rumanía, en 2016, los investigadores encontraron que las pérdidas económicas totales por cada 24 manadas de 18.000 pollitos fueron de aproximadamente 37.948,2 €, con una media de 3.162,4 € por manada. Estas pérdidas fueron causadas por la mortalidad (34,8%) y la mala conversión alimenticia (65,2%) debido a la coccidiosis (Györke et al., 2016).
Tradicionalmente, el diagnóstico de las granjas se da a través de la detección y enumeración de ooquistes excretados en las heces, además de medir las dimensiones de las aves. Los investigadores post-mortem evalúan la porción intestinal afectada y las lesiones (Long y Joyner, 1984). El diagnóstico específico de infecciones por Eimeria en pollos de engorde es fundamental para una mejor comprensión de la epidemiología y dinámica de la enfermedad y es necesario para la prevención, vigilancia y control efectivo (Morris and Gasser, 2006; Gazoni et al., 2017).
La coccidiosis subclínica se observa comúnmente en granjas avícolas en Brasil, y un diagnóstico preciso es esencial para rastrear las intervenciones, principalmente debido a problemas con la resistencia a los agentes coccidiostáticos (Gazoni et al., 2020). Por lo tanto, el objetivo de este estudio fue determinar la ocurrencia anual de la infección por Eimeria en pollos de engorde industriales de 2012 a 2019 en Brazil.
MATERIAL Y MÉTODOSAnimales y recopilación de datos
El seguimiento de la coccidiosis se llevó a cabo en 82 empresas de los estados de Rio Grande do Sul, Santa Catarina, Paraná, Mato Grosso do Sul, São Paulo, Minas Gerais, Rio de Janeiro, Goiás, Distrito Federal, Alagoas, Para, Paraiba y Pernambuco de 2012 y 2019, utilizando 13,648 pollos de engorde. Brasil es un país continental con una variación climática muy particular para cada estado, por lo que no se planteó en consideración de información climática. Los datos fueron divulgados por el Programa de Salud Intestinal (PSI) de Vetanco do Brasil, con el fin de obtener el porcentaje de aves afectadas y su grado de clasificación por puntajes de lesión en colaboración con investigadores de la Universidad Estatal de Santa Catarina (UDESC). Las aves eran de las líneas Cobb 500 y Aviagen y tenían entre 9 y 49 días de edad. Se les suministró piensos preparados por sus respectivas empresas, sin ninguna interferencia del evaluador en términos de formulación o uso de potenciadores del rendimiento y agentes anticoccidiales. El programa anticoccidial más utilizado es el sistema dual, en el que se utiliza un ingrediente activo en la primera fase (del 1º al 21º día de edad) y otro en la segunda fase (del 22º día a 3 días antes del sacrificio), los pollos de engorde No recibir programas de vacunas contra la coccidiosis, con el fin de reducir la posibilidad de aparición de resistencias antimicrobianas.
Colección de muestra
Monitoreamos la salud intestinal de los pollos de engorde usando de 3 a 6 aves por lote (aviario). Las aves se seleccionaron al azar de tres puntos diferentes en el aviario (entrada, medio y fondo). Estas aves fueron sacrificadas por dislocación cervical, seguida de disección para recolección de muestras y evaluación visual.
Evaluación macroscópica de tejidos
En el tracto gastrointestinal se observó la presencia de lesiones causadas por E. acervulina, E. maxima y E. tenella, por ejemplo, figura 1. Cuando estaban presentes, las lesiones se clasificaron según su grado de intensidad, según la metodología de Johnson y Reid (1970), donde la puntuación 0 indica la ausencia de lesión y la puntuación 4 indica daño severo.
Presencia de las lesiones causadas por <italic>E. acervulina</italic>, <italic>E. maxima</italic>, y <italic>E. tenella.</italic>
Técnica de raspado de mucosas y recuento de ooquistes
Para evaluar E. maxima micro, se utilizó la técnica de raspado de la mucosa intestinal para el recuento de ooquistes, realizada en la porción intestinal que rodea el divertículo de Meckel. El contenido fecal se depositó en un portaobjetos, se cubrió con un cubreobjetos y se visualizó en cinco campos (extremidades y centro) para contar ooquistes bajo microscopía óptica (100x). Se utilizaron cuatro puntajes para la clasificación, según Vetanco do Brasil (2011), donde el puntaje 0 representó ausencia de ooquistes; la puntuación 1 representó de 1 a 10 ooquistes; la puntuación 2 representó 11-20 ooquistes; la puntuación 3 representó 21-40 ooquistes, y la puntuación 4 significó más de 41 ooquistes, por ejemplo la figura 2 .
Se utilizaron cuatro puntajes para la clasificación de E. maxima micro
RESULTADOS
La ocurrencia anual mostró diferencias significativas entre especies; mientras que uno era alto, los otros eran más pequeños en el año en cuestión. La coccidiosis subclínica tuvo la mayor incidencia (promedio de 34,8%) durante el período evaluado (2012- 2019), revelando una mayor frecuencia y diseminación en la industria avícola brasileña. Para las lesiones macroscópicas atribuidas a E. acervulina, E. maxima y E. tenella, la ocurrencia promedio fue de 16,1%, 7,9% y 4,1%, respectivamente. También observamos que ninguna de las especies de Eimeria mostró comportamiento lineal; en cambio, demostraron fluctuaciones a lo largo de los años: a veces, hubo un aumento. A veces, hubo una disminución en la ocurrencia (Tabla 1).
Especies de <italic>Eimeria</italic> y porcentaje de eimeriosis en pollos de engorde entre 2012 a 2019
Especies
Ocurrencia anual (%)
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
Considerando cada especie a través de períodos, observamos que, en 2012, las ocurrencias de E. maxima (22.2%) y E. tenella (10.0%) fueron mayores y menores en los otros años. E. acervulina tuvo un aumento significativo en 2016, alcanzando el 30,5% de ocurrencia, con una disminución gradual a partir de esa fecha (9,7% en 2019). E. maxima micro mostró un crecimiento casi incremental hasta 2017 (del 28,8 al 45,5%), manteniéndose con un alto porcentaje anual en los años posteriores (38,0- 42,6%). Estos resultados se muestran en la Tabla 1.
En cuanto a las puntuaciones de las lesiones, en todos los años prácticamente y para todas las especies, el recuento de ooquistes estuvo dentro de la puntuación 1, seguido de las puntuaciones 2, 3 y 4 (rara vez fue superior a 3, y cuando ocurrió, se observó para E .máxima micro). La puntuación 4 fue poco frecuente, lo que a menudo resulta en un valor nulo. El porcentaje entre especies y entre años no siguió un patrón. En cambio, varió para ambas especies y año (Tabla 2).
Porcentaje de puntajes de coccidiosis (Eimeria) obtenidos entre 2012 y 2019 en pollos de engorde de 9 a 49 días en la agroindustria brasileña
Año
Especies
Puntuacion(%)
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
DISCUSIÓN
Reportamos la ocurrencia de coccidiosis en la industria avícola brasileña por más de siete años. Los estudios que informan las características epidemiológicas de la coccidiosis en Brasil son raros. Es importante prestar atención a las especies que se encuentran en el territorio; nuestros hallazgos concuerdan con los de otros autores que reportaron frecuentemente E. acervulina, E. maxima y E. tenella (Moraes et al., 2015; Chapman et al., 2016; Kim et al., 2017); estas especies, además de ser reportadas con mayor frecuencia, son las que comúnmente desarrollan resistencia a las drogas sintéticas (Shivaramaiah et al., 2014).
Todas las especies de Eimeria están muy extendidas en los seis continentes. Sin embargo, puede haber una división regional en la diversidad genética y la estructura poblacional de las especies (Prakashbabu et al., 2017); o incluso, como describen Clark et al. (2016), puede haber variantes genéticas entre los hemisferios sur y norte, lo que representa un riesgo para la seguridad alimentaria y el bienestar animal si se propaga a áreas previamente ausentes. Se cree que esta variación es atribuible al uso de medicamentos y vacunas anticoccidiales (Prakashbabu et al., 2017).
Un estudio sobre la prevalencia de coccidiosis en Santa Catarina (BR) mediante PCR mostró que el 96% de las fincas fueron positivas para Eimeria, con siete especies identificadas: E. maxima (63,7%) y E. acervulina (63,3%), E. tenella (54,6%), E. mitis (38,6%), E. praecox (25,1%), E. necatrix (24,3%) y E. brunetti (13,1%), con un promedio de 2,96 especies por explotación (Moraes et al., 2015). Otro estudio en una pequeña región del estado de Tocantins reportó la ocurrencia de coccidiosis en todas las granjas, con la presencia de E. maxima, E. acervulina, E. mitis y E. tenella (Toledo et al., 2011). La alta preponderancia de una especie de Eimeria puede indicar su resistencia a los fármacos habitualmente expuestos, como es el caso de E. tenella estudiado en Nigeria (Ojimelukwe et al., 2018) E. maxima micro y E. acervulina en el presente estudio y el otros informaron en Brasil. El diagnóstico es importante y necesario para delinear estrategias, según Teeter et al. (2008), se observó que por cada punto de aumento en la evaluación microscópica de las lesiones de coccidiosis, el aumento de peso diario disminuyó un 1,5% del peso corporal (g) durante el período de desafío de seis días. Por tanto, es fundamental conocer el grado de daño intestinal para cuantificar el rendimiento de las aves.
El ciclo de replicación intestinal rápido (4 a 6 días) y la vía oral/fecal hacen de la coccidiosis un problema severo de reproducción intensiva, causado por infecciones recurrentes y resistencia a agentes coccidiostáticos (Shivaramaiah et al., 2014). Sin un control efectivo, el número de parásitos puede aumentar hasta el punto de producir coccidiosis clínica. Para evitar resistencias, se llevan a cabo programas de rotación de fármacos y vacunación (Lan et al., 2017). La rotación de agentes coccidiostáticos puede ayudar a esclarecer las oscilaciones significativas de ocurrencia entre especies de Eimeria, como se verifica en este estudio.
La vacunación es la medida profiláctica más interesante; sin embargo, solo se utiliza en reproductoras de pollos de engorde (Abdul Rasheed y Matsler, 2020) y gallinas ponedoras (Chapman et al., 2014). La vacunación comercial in ovo contra la coccidiosis en pollos de engorde se ha vuelto ampliamente aceptada en la industria avícola de EE. UU sin embargo, sus efectos sobre el rendimiento aún no se han estudiado (Sokale et al., 2020). Es fundamental enfatizar la importancia de los estudios de prevalencia de especies para el desarrollo de vacunas regionales, como en este estudio. Se ha analizado el uso de antimicrobianos con miras a reemplazarlos para evitar el problema de resistencias y se han propuesto varias alternativas (Kim et al., 2017; Bortoluzzi et al., 2019; Lu et al., 2019; Park et al., 2020). La baja cantidad de ooquistes presentes en las muestras de este estudio (puntuación 1) y las pocas observaciones de la puntuación cero (sin ooquistes/muestra) pueden indicar la eficacia del uso estratégico de anticoccidiales químicos a través de piensos.
Además de la pérdida de rendimiento, la coccidiosis es un factor predisponente para una patología aún más dañina en las aves, como la enteritis necrótica (Williams, 2005; Adhikari et al., 2020). La presencia de E. maxima fue considerada por Paiva y McElroy (2014) como un factor de riesgo esencial para la promoción de Clostridium perfringens, y esto debe ser considerado en la búsqueda de métodos de control efectivos para las granjas en Brasil.
Para el monitoreo del rebaño, la técnica de visualización de mucosas y recuento de ooquistes y clasificación sigue siendo la más viable para la agroindustria brasileña, en detrimento de la prueba qPCR, también disponible para diagnóstico y cuantificación (Velkers et al., 2010). Esto aumentaría considerablemente el seguimiento y requeriría un cuidado diferencial de las muestras.
CONCLUSIONES
En conclusión, la coccidiosis subclínica tiene una prevalencia preocupante, ya que 3,5 de cada diez aves tienen coccidiosis. Este es uno de los factores que probablemente causa reducciones en el desempeño productivo de los lotes de pollos de engorde, además de ser un factor predisponente para la clostridiosis. Debido a que los intentos de erradicar el parásito mediante cuarentena, desinfección y saneamiento no han tenido éxito (McDougald, 2008), es de fundamental importancia que los profesionales del sector avícola realicen evaluaciones subclínicas de coccidiosis de manera rutinaria, pudiendo así intervenir si es necesario, para mantener el desempeño productivo de los pollos de engorde.
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Code:2020-86
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.
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 METHODSAnimals 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 (1st to 21st day of age), and another is used in the second phase (22nd 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.
Presence of lesions caused by <italic>E. acervulina</italic>, <italic>E. maxima</italic>, and <italic>E. tenella.</italic>
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 .
Four scores were used for the classification for <italic>E. maxima</italic> 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.
<italic>Eimeria</italic> species and percentage of eimeriosis in broilers between 2012 to 2019.
Species
Annual ocurrence (%)
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).
Percentage of coccidiosis scores (<italic>Eimeria</italic>) 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.