Epidemiology of Eimeria infections in sheep raised extensively in a semiarid region of Brazil

Epidemiologia da infecção por Eimeria em ovinos criados extensivamente em região semiárida no Brasil

Luiz Eduardo Barreto de Souza Jurandir Ferreira da Cruz Milton Rezende Teixeira Neto George Rêgo Albuquerque Antonio Diego Brandão Melo Daniel Mario Tapia Tapia About the authors

Abstract

The aim of this study was to identify and determine the prevalence of Eimeria species affecting sheep raised extensively in a semiarid region of Brazil. Fecal samples of native sheep were collected during the rainy and dry seasons. The degree of infection was determined by counting oocysts per gram (OPG) of feces, and the morphometric method was used for species identification. Oocysts were found in all the properties assessed, in which 68.3% of the animals were infected. The prevalence of oocysts was influenced by the season and animal category (P<0.05). It was higher during the rainy season than the dry season (80.2% vs. 55.8%) and highest in young animals than the adults animals (68.2% vs. 39.6%). The OPG was lower during the dry season (1,269 ± 312 vs. 4,400 ± 1,122). Ten species were found; of these, E. ovinoidalis, E. granulosa, E. faurei, and E. crandallis were the most frequent. E. ovinoidalis and E. crandallis were found in all properties, with their prevalences being 19.4% and 13.6% respectively. The high prevalence of pathogenic species shows that eimeriosis is a risk for animals raised extensively in the semiarid region.

Keywords:
Coccidiosis; morphometry; oocyts; OPG; parasitosis

Resumo

Objetivou-se neste estudo identificar e determinar a prevalência de espécies de Eimeria que parasitam ovinos criados extensivamente em região semi-árida. Amostras de fezes de ovinos nativos foram coletados durante as estações chuvosa e seca. O grau de infecção foi determinado pela contagem de oocistos por grama de fezes (OoPG)e o método morfométrico foi utilizado para a identificação das espécies. Foram encontrados oocistos em todas os rebanhos avaliados e observou-se que 68,3% dos animais estavam infectados. A prevalência de oocistos foi influenciada pela estação climática e pela categoria dos animais (P<0,05), sendo mais alta durante a estação chuvosa em relação a estação seca (80,2% vs. 55,8%) e em animais jovens em relação aos animais adultos (68,2% vs. 39,6%). O OoPG foi menor durante a estação seca (1.269 ± 312 vs. 4.400 ± 1.122). Dez espécies foram encontradas sendo a E. ovinoidalis, E. granulosa, E. faurei, e E. crandallis as mais frequentes. E. ovinoidalis e E. crandallis foram encontrados em todas as propriedades, com prevalências de 19,4% e 13,6%, respectivamente. A alta prevalência de espécies patogênicas mostra que eimeriose é um risco para os animais criados extensivamente na região semiárida.

Palavras-chave:
Coccidiose; morfometria; oocistos; OoPG; parasitose

Introduction

Eimeriosis is an endoparasitosis, which, in ruminants, is characterized by diarrhea that can lead to death. The subclinical form causes intestinal function impairment, which delays the animal’s growth (DENIZ, 2009Deniz A. Coccidiose ovina: revisão bibliográfica. Albéitar 2009; 3: 4-11.) and decreases its performance (TAYLOR et al., 2011Taylor MA, Marshall RN, Marshall JA, Catchpole J, Bartram D. Dose-response effects of diclazuril against pathogenic species of ovine coccidia and the development of protective immunity. Vet Parasitol 2011; 178(1-2): 48-57. http://dx.doi.org/10.1016/j.vetpar.2010.12.024. PMid:21232870.
http://dx.doi.org/10.1016/j.vetpar.2010....
).

In sheep, eimeriosis has great economic importance due to its high prevalence in many parts of the world (BAKUNZI et al., 2010Bakunzi FR, Thwane SN, Motsei LE, Dzoma BM. Diversity and seasonal occurrence of species in a mixed flock of communally reared sheep and goats in Mafikeng in the North West Province, South Africa. EimeriaJ S Afr Vet Assoc 2010; 81(3): 148-150. http://dx.doi.org/10.4102/jsava.v81i3.137. PMid:21247039.
http://dx.doi.org/10.4102/jsava.v81i3.13...
). Even though eimeriosis is considered an emergent disease with a growing sanitary risk (TAYLOR, 2012Taylor MA. Emerging parasitic diseases of sheep. Vet Parasitol 2012; 189(1): 2-7. http://dx.doi.org/10.1016/j.vetpar.2012.03.027. PMid:22525586.
http://dx.doi.org/10.1016/j.vetpar.2012....
), there are few studies about the epidemiology of eimeriosis in sheep raised extensively in semiarid regions, where the sheep industry plays a significant economic role (COSTA et al., 2011Costa KMFM, Ahid SMM, Vieira LS, Vale AM, Soto-Blanco B. Efeitos do tratamento com closantel e ivermectina na carga parasitária, no perfil hematológico e bioquímico sérico e no grau Famacha de ovinos infectados com nematódeos. Pesqui Vet Bras 2011; 31(12): 1075-1082. http://dx.doi.org/10.1590/S0100-736X2011001200007.
http://dx.doi.org/10.1590/S0100-736X2011...
).

Knowledge of the prevalence of parasitic species and the predisposing factors for infections by these species is essential for evaluating the infection potential and minimizing the economic impact of eimeriosis (YAKHCHALI & GOLAMI, 2008Yakhchali M, Golami E. infection (Coccidia: Eimeriidae) in sheep of different age groups in Sanandaj city, Iran. EimeriaVet Arhiv 2008; 78(1): 57-64.). Conversely, the degree of infection depends on environmental conditions, the immunological response of the animal (CAVALCANTE et al., 2012Cavalcante ACR, Teixeira M, Monteiro JP, Lopes CWG. species in dairy goats in Brazil. EimeriaVet Parasitol 2012; 183(3-4): 356-358. http://dx.doi.org/10.1016/j.vetpar.2011.07.043. PMid:21852038.
http://dx.doi.org/10.1016/j.vetpar.2011....
), and parasitic species (REEG et al., 2005Reeg KJ, Gauly M, Bauer C, Mertens C, Erhardt G, Zahner H. Coccidial infections in housed lambs: oocyst excretion, antibody levels and genetic influences on the infection. Vet Parasitol 2005; 127(3-4): 209-219. http://dx.doi.org/10.1016/j.vetpar.2004.10.018. PMid:15710521.
http://dx.doi.org/10.1016/j.vetpar.2004....
). Species vary with respect to pathogenicity, pre-patent period, and the rate of oocyst elimination (GAULY et al., 2001Gauly M, Krauthahn C, Bauer C, Erhardt G. Pattern of oocyst output and repeatability in naturally infected suckling Rhön Lambs. EimeriaJ Vet Med B Infect Dis Vet Public Health 2001; 48(9): 665-673. http://dx.doi.org/10.1046/j.1439-0450.2001.00493.x. PMid:11765802.
http://dx.doi.org/10.1046/j.1439-0450.20...
). Thus, eimeriosis diagnoses based on the quantification of oocysts in fecal samples does merit a relative strategic value (LIMA, 2004Lima JD. Coccidiose dos ruminantes domésticos. Rev Bras Vet Parasitol 2004; 13(S1): 9-13.).

Identification of Eimeria species may be based on biological and morphological characteristics (MARTYNOVA-VANKLEY et al., 2008Martynova-Vankley A, Syvyk A, Teplova I, Hume M, Nalian A. Rapid detection of avian species using denaturing gradient gel electrophoresis. EimeriaPoult Sci 2008; 87(9): 1707-1713. http://dx.doi.org/10.3382/ps.2008-00098. PMid:18753436.
http://dx.doi.org/10.3382/ps.2008-00098...
). Biological identification, which uses molecular methods for protein and amino acid identification, requires specific and costly equipment (BARKWAY et al., 2011Barkway CP, Pocock RL, Vrba V, Blake DP. Loop-mediated isothermal amplification (LAMP) assays for the species-specific detection of that infect chickens. EimeriaBMC Vet Res 2011; 7(67): 1-8. PMid:22053893.). Thus, due to its practicality, morphological characterization utilizing morphometry of sporulated oocysts has been the most common identification method used to differentiate species in many epidemiological studies (AHID et al., 2009Ahid SMM, Medeiros VMC, Bezerra ACDS, Maia MB, Xavier VM, Vieira LS. Espécies de gênero Schneider, 1875 (EimeriaApicomplexa: Eimeriidae) em pequenos ruminantes na mesorregião oeste do estado do Rio Grande do Norte, Brasil. Ciênc Anim Bras 2009; 10(3): 984-989.).

The infection by coccidia from genus Eimeria generally has a multi-specific character (CAVALCANTE et al., 2012Cavalcante ACR, Teixeira M, Monteiro JP, Lopes CWG. species in dairy goats in Brazil. EimeriaVet Parasitol 2012; 183(3-4): 356-358. http://dx.doi.org/10.1016/j.vetpar.2011.07.043. PMid:21852038.
http://dx.doi.org/10.1016/j.vetpar.2011....
), yet 15 species that parasitize sheep have been described (SARATSIS et al., 2011Saratsis A, Joachim A, Alexandros S, Sotiraki S. Lamb coccidiosis dynamics in different dairy production systems. Vet Parasitol 2011; 181(2-4): 131-138. http://dx.doi.org/10.1016/j.vetpar.2011.04.027. PMid:21571436.
http://dx.doi.org/10.1016/j.vetpar.2011....
). Among the different species capable of infecting sheep, only E. ovinoidalis and E. crandallis cause the clinical symptomatology of eimeriosis; there is little evidence that other species are pathogenic (GREGORY & CATCHIPOLE, 1990Gregory MW, Catchipole J. Ovine coccidiosis: the patology of infection. Eimeria crandallisInt J Parasitol 1990; 20(7): 849-860. http://dx.doi.org/10.1016/0020-7519(90)90022-F. PMid:2276861.
http://dx.doi.org/10.1016/0020-7519(90)9...
). Consequently, the objective of this study was to identify and quantify the Eimeria species that parasitize sheep raised extensively in a semiarid region of Brazil, and the roles of animal category and the climatic season in the severity of infection.

Materials and Methods

The study was carried out in 20 rural properties located in the southwest of Bahia, Brazil (14° 36’ S, 41° 08’ O), at an altitude of 353 m. The climate in that region is classified as tropical-Aw according to the Köepen-Geiger classification (PEEL et al., 2007Peel MC, Finlayson BL, McMahon TC. Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci 2007; 11(5): 1633-1644. http://dx.doi.org/10.5194/hess-11-1633-2007.
http://dx.doi.org/10.5194/hess-11-1633-2...
), with very well-defined dry seasons (from April to October) and wet seasons (from November to March) (Figure 1). The pluviometric annual mean index is 656 mm (INMET, 2012Instituto Nacional de Meteorologia – INMET. Banco de dados meteorológicos para ensino e pesquisa [online]. Brasília: INMET; 2012 [cited 2012 Mar 15]. Available from: http://www.inmet.gov.br/portal/index.php?r=bdmep/bdmep
http://www.inmet.gov.br/portal/index.php...
) and the region predominantly contains open arboreal caatinga vegetation (SEI, 2012Superintendência de Estudos Econômicos e Sociais da Bahia – SEI. [online]. 2012 [cited 2012 Feb 15]. Available from: http://www.sei.ba.gov.br/metaside/consulta/frame_metadados.wsp?tmp.tabela=t8.
http://www.sei.ba.gov.br/metaside/consul...
).

Figure 1
Minimum (-■-) and maximum (-▲-) temperatures and pluvial precipitation (▄) from January to December 2011 (INMET, 2012Instituto Nacional de Meteorologia – INMET. Banco de dados meteorológicos para ensino e pesquisa [online]. Brasília: INMET; 2012 [cited 2012 Mar 15]. Available from: http://www.inmet.gov.br/portal/index.php?r=bdmep/bdmep
http://www.inmet.gov.br/portal/index.php...
).

The sampled herds were composed of adaptated local breed sheep raised extensively in Caatinga pastures, supplemented with cactus forage (Opuntia ficus) during the most critical period of the dry season. The animals without a history of anti-coccidial treatment were grouped into four categories: ram, ewe, and male and female lambs (age, ≤6 months). The number of sampled animals corresponded to 20% of the total category, except the ram category, which was 100%. A total of 464 individual fecal samples were collected from 20 herds; among these, 238 were obtained during the rainy season (from December to January) and 226 during the dry season (from June to July).

Fecal samples collected directly from the rectum were placed in plastic bags and kept under refrigeration prior to laboratory analysis. The oocyst count expressed in oocysts per gram of feces (OPG) was performed using the McMaster technique of flotation in saturated saline solution developed by Gordon & Whitlock (1939)Gordon HM, Whitlock HVA. A new technique for counting nematodes eggs in sheep faeces. J Counc Sci Ind Res 1939; 12: 50-52. and modified by Ueno & Gonçalves (1998)Ueno H, Gonçalves PC. Manual para o diagnóstico das helmintoses de ruminantes. Tokyo: Japan International Cooperation Agency; 1998.. After gaze filtration, the samples containing Eimeria were grouped by collection site, placed in Petri dishes containing potassium dichromate (2.5%), and kept for seven days at room temperature. Eimeria species were identified by the form aspects, the presence or absence of micropyle and micropylar caps, major and minor diameter measurements of the oocysts and sporocysts, and the morphometric index (MI). The MI was obtained by the equation MI = larger diameter/smaller diameter (LEVINE et al., 1980Levine ND, Corliss JO, Cox FEG, Deroux G, Grain G, Honigberg BM, et al. A newly revised classification of the protozoa. J Protozool 1980; 27(1): 37-58. http://dx.doi.org/10.1111/j.1550-7408.1980.tb04228.x. PMid:6989987.
http://dx.doi.org/10.1111/j.1550-7408.19...
; HASSUM et al., 2002Hassum IC, Paiva RV, Menezes RCAA. Freqüencia, dinâmica e morfologia dos oocistos de Eimeria bakuensis (Apicomplexa: Eimeriidae) em ovinos de diferentes categorias de produção de uma criação no município de Petrópolis/RJ. Rev Bras Parasitol Vet 2002; 11(1): 19-25.; AHID et al., 2009Ahid SMM, Medeiros VMC, Bezerra ACDS, Maia MB, Xavier VM, Vieira LS. Espécies de gênero Schneider, 1875 (EimeriaApicomplexa: Eimeriidae) em pequenos ruminantes na mesorregião oeste do estado do Rio Grande do Norte, Brasil. Ciênc Anim Bras 2009; 10(3): 984-989.). A hundred randomly sampled oocysts from each farm were photographed using an Olympus Camera DP71 attached to an Olympus BX51 light microscope (Olympus, Center Valley, PA, USA) at 40× magnification. The oocysts were analyzed using Image Pro-Express 6.0 software (Media Cybernetics, Silver Springs, MD, USA). Fecal oocyst counts were transformed into the logarithm of OPG plus one [log (OPG + 1)] to obtain normal distribution. The average OPG, according to the category of animals and the season, as well as the diameters of oocysts and sporocysts and the morphometric index were compared by Scott-Knott test (SAEG, 9.1). The prevalence of Eimeria species was compared by the Chi-square test (EXCEL, 2007), while the frequencies on the oocystograms were compared by the Kruskal-Wallis test. All differences were considered significant at P<0.05.

Results

Eimeria species oocysts were found in 68.3% of the fecal samples, and parasites were verified in at least one of the animal categories on all of the properties. Furthermore, in 90% of the properties, all animal categories (young, adults, male, female) showed infection by Eimeria.

The animal category significantly influenced oocyst prevalence (P<0.05). During the dry season, young animals (males and females) showed values higher than adults (68.2% vs. 39.6%, respectively). During the rainy season, young females showed higher prevalence than adults (P<0.05). In the rainy season, sex also contributed to oocyst prevalence, with males showing higher values than females (P<0.05). Similarly, the season influenced the prevalence of oocysts, since it was higher during the rainy season than the dry season (P<0.05), with average values of 80.2% and 55.8%, respectively (Table 1).

Table 1
Prevalence and number of Eimeria sp. oocysts in fecal samples of sheep raised in extensively extensively in the semiarid region.

In young animals in both seasons, the intensity of Eimeria infection (4,620.4 ± 1,029.6 OPG) was relatively high. The maximum OPG values for lambs (male and female) and adults (rams and ewes) were observed during the rainy season (17 × 104; 11 × 104; 9 × 103; and 4.4 × 103 OPG, respectively). The average infection observed in dry and rainy seasons (1,269 ± 312 vs. 4,400 ± 1,123 OPG, respectively) showed that the season had influence on the infection intensity (P<0.05).

The rate of animals that showed high infection intensity varied according to the season. During the dry season, 23.7% of the young and 1.0% of the adult animals had OPG≥1.103, and during the rainy season, the corresponding numbers rose to 48.2% and 12.4%, respectively. The animal category influenced the infection intensity. All the samples that showed OPG>1.104 (5.1%) were from young animals. Individuality also influenced the infection intensity since an expressive variation in the OPG was noted among individuals of the same category, especially among young animals, regardless of the weather season (Table 2).

Table 2
Frequency of oocistograms with low (<1.103), medium (1.103-1.104) and high (>104) infection intensity in sheep raised extensively in the semiarid region.

Ten Eimeria species were identified in the samples of feces analyzed: E. ovinoidalis, E. granulosa, E. faurei, E. crandallis, E. ahsata, E. parva, E. bakuensis, E. intricata, E. pallida, and E. punctata.

The most prevalent five species (E. ovinoidalis, E. granulosa, E. faurei, E. crandallis, and E. ahsata) corresponded to 80.1% of the oocysts identified. E. crandallis and E. ovinoidalis, with higher pathogenic potential, represented 33.0% of the total oocysts identified, from which E. ovinoidalis was the most prevalent (19.5%) in both seasons (P<0.05) and was present in 100.0% of the studied properties. The prevalence of E. ovinoidalis, E. intricata, and E. bakuensis was influenced by the season: the first two species were more prevalent during the dry season and E. bakuensis during the rainy season (P<0.05). Nevertheless, the prevalence of most of the species was not influenced by the season. E. intricata, E. pallida, and E. punctata were the least prevalent species, together totaling 3.4% of the oocysts identified during the two seasons (Table 3).

Table 3
Oocysts and sporocysts diameters of Eimeria found in fecal samples of sheep raised extensively in the semiarid region.

Discussion

The prevalence of Eimeria speciesoocysts is influenced by the husbandry system, showing a direct relationship between the technification level and infection intensity (CAI & BAI, 2009Cai KZ, Bai JL. Infection intensity of gastrointestinal nematodosis and coccidiosis of sheep raised under three types of feeding and management regims in Ningxia Hui Autonomous Region, China. Small Rumin Res 2009; 85(2-3): 111-115. http://dx.doi.org/10.1016/j.smallrumres.2009.07.013.
http://dx.doi.org/10.1016/j.smallrumres....
). Previous studies reported 92.7% prevalence of Eimeria sp. oocysts in an intensive system (SARATSIS et al., 2011Saratsis A, Joachim A, Alexandros S, Sotiraki S. Lamb coccidiosis dynamics in different dairy production systems. Vet Parasitol 2011; 181(2-4): 131-138. http://dx.doi.org/10.1016/j.vetpar.2011.04.027. PMid:21571436.
http://dx.doi.org/10.1016/j.vetpar.2011....
), 78.3% in a semi-intensive system (HASSUM & MENEZES, 2005Hassum IC, Menezes RCAA. Infecção natural por espécies do gênero em pequenos ruminantes criados em dois municípios do estado do Rio de Janeiro. EimeriaRev Bras Parasitol Vet 2005; 14(3): 95-100. PMid:16229752.), and 25.3% and 58.9% in extensive system (AHID et al., 2009Ahid SMM, Medeiros VMC, Bezerra ACDS, Maia MB, Xavier VM, Vieira LS. Espécies de gênero Schneider, 1875 (EimeriaApicomplexa: Eimeriidae) em pequenos ruminantes na mesorregião oeste do estado do Rio Grande do Norte, Brasil. Ciênc Anim Bras 2009; 10(3): 984-989.; BRITO et al., 2009Brito DRB, Santos ACG, Teixeira WC, Guerra RMSNC. Parasitos gastrintestinais em caprinos e ovinos da microrregião do Alto Mearim e Grajaú, no Estado do Maranhão, Brasil. Ciênc Anim Bras 2009; 10(3): 967-974.). Limiting factors related to the environment (climate and management) or to the animal (genetic and immunologic status) may promote dissemination and increase the prevalence of coccidia even in extensive systems (CHARTIER & PARAUD, 2012Chartier C, Paraud C. Coccidiosis due to in sheep and goats, a review. EimeriaSmall Rumin Res 2012; 103(1): 84-92. http://dx.doi.org/10.1016/j.smallrumres.2011.10.022.
http://dx.doi.org/10.1016/j.smallrumres....
).

The animal category was a significant factor influencing oocysts excretion, because young animals were more affected than adults, regardless of the season. The high susceptibility of young animals is related to immunological aspects once the species-specific immunity against Eimeria sp. occurs after the initial infection (SILVA et al., 2011Silva RM, Facury-Filho EJ, Souza MF, Ribeiro MFB. Natural infection by spp. in cohort of lambs raised extensively in Northeast Brazil. EimeriaRev Bras Parasitol Vet 2011; 20(2): 134-139. http://dx.doi.org/10.1590/S1984-29612011000200008. PMid:21722488.
http://dx.doi.org/10.1590/S1984-29612011...
).

Sex was also an factor influencing eimeriosis prevalence, especially in the rainy season. The ram’s susceptibility to infection by Eimeria sp. can be attributed to immunosuppression caused by elevated plasma levels of androgens, mainly testosterone, throughout the breeding season (BHAT et al., 2012Bhat S, Mir M, Qadir S, Allaie I, Khan H, Husain I, et al. Prevalence of gastro-intestinal parasitic infections in sheep of Kashmir valley of India. Vet World 2012; 5(11): 667-671. http://dx.doi.org/10.5455/vetworld.2012.667-671.
http://dx.doi.org/10.5455/vetworld.2012....
). During the rainy season, physical exhaustion from the intense reproductive activity, certainly contributed to the increased susceptibility of the male to eimeriosis.

Climate-related aspects, especially the moisture caused by rain in places where drainage is difficult, may influence the prevalence of Eimeria sp. A warm and moist environment provides ideal conditions for oocyst sporulation and thereby increases the potential for infection (TAYLOR, 2012Taylor MA. Emerging parasitic diseases of sheep. Vet Parasitol 2012; 189(1): 2-7. http://dx.doi.org/10.1016/j.vetpar.2012.03.027. PMid:22525586.
http://dx.doi.org/10.1016/j.vetpar.2012....
). The effect of weather on oocyst sporulation can be potentiated by extreme variations in pluviometry and temperature that occur throughout the year (KHAN et al., 2011Khan MN, Rehman T, Iqbal Z, Sajid MS, Ahmad M, Riaz M. Prevalence and associated risk factors of sheep of Punjab, Pakistan. EimeriaWorld Acad Sci Eng Technol 2011; 5(7): 334-338.). This fact was observed in the area where the present study was carried out, where maximum and minimum monthly values of temperature and pluviometry during the dry and rainy season were 15-30 °C and 15-140 mm, respectively. Recognizing that an environment with high moisture and mild temperature leads to oocyst sporulation, promoting its higher elimination (TAYLOR, 2012Taylor MA. Emerging parasitic diseases of sheep. Vet Parasitol 2012; 189(1): 2-7. http://dx.doi.org/10.1016/j.vetpar.2012.03.027. PMid:22525586.
http://dx.doi.org/10.1016/j.vetpar.2012....
), the rainy season in the semiarid region presents favorable environmental conditions for oocyst sporulation of Eimeria, suggesting the necessity of management targeted toward its control during this critical period of the infection.

The quantity of excreted oocysts can vary depending on the infecting dose of oocysts (GREGORY & CATCHIPOLE, 1987Gregory MW, Catchipole J. Ovine coccidiosis: the pathology of infection. Eimeria ovinoidalisInt J Parasitol 1987; 17(6): 1099-1111. http://dx.doi.org/10.1016/0020-7519(87)90162-7. PMid:3654051.
http://dx.doi.org/10.1016/0020-7519(87)9...
, 1990Gregory MW, Catchipole J. Ovine coccidiosis: the patology of infection. Eimeria crandallisInt J Parasitol 1990; 20(7): 849-860. http://dx.doi.org/10.1016/0020-7519(90)90022-F. PMid:2276861.
http://dx.doi.org/10.1016/0020-7519(90)9...
) and the animal's immune status (REEG et al., 2005Reeg KJ, Gauly M, Bauer C, Mertens C, Erhardt G, Zahner H. Coccidial infections in housed lambs: oocyst excretion, antibody levels and genetic influences on the infection. Vet Parasitol 2005; 127(3-4): 209-219. http://dx.doi.org/10.1016/j.vetpar.2004.10.018. PMid:15710521.
http://dx.doi.org/10.1016/j.vetpar.2004....
). Therefore, individual influences play a role in the degree of infection. Oocystograms with values >104 indicate high infection intensity and are generally linked to typical diarrheal syndromes of this endoparasitosis (COZMA & TITILINCU, 2007Cozma V, Titilincu A. Etio-pathogenetical researches in coccidiosis of the lambs bred in big groups, in an unit from the west of Romania. Bull Univ Agric Sci Vet Med 2007; 64(1-2): 392-398.). However, the diagnosis of eimeriosis cannot be excluded when the OPG is low or non-existent. Adult animals that excrete small amounts of oocysts are important in the epidemiology of eimeriosis; the oocysts released by these animals are usually the cause of infection in young animals (PLATZER et al., 2005Platzer B, Prosl H, Cieslicki M, Joachim A. Epidemiology of infections in an Austrian milking sheep flock and control with diclazuril. EimeriaVet Parasitol 2005; 129(1-2): 1-9. http://dx.doi.org/10.1016/j.vetpar.2004.11.031. PMid:15817196.
http://dx.doi.org/10.1016/j.vetpar.2004....
).

Regarding the prevalence of Eimeria sp., there have been 15 species identified that parasitize sheep (SARATSIS et al., 2011Saratsis A, Joachim A, Alexandros S, Sotiraki S. Lamb coccidiosis dynamics in different dairy production systems. Vet Parasitol 2011; 181(2-4): 131-138. http://dx.doi.org/10.1016/j.vetpar.2011.04.027. PMid:21571436.
http://dx.doi.org/10.1016/j.vetpar.2011....
). Previous studies suggest that species and their respective prevalences vary according to the region, probably due to the influence of climate (KHAN et al., 2011Khan MN, Rehman T, Iqbal Z, Sajid MS, Ahmad M, Riaz M. Prevalence and associated risk factors of sheep of Punjab, Pakistan. EimeriaWorld Acad Sci Eng Technol 2011; 5(7): 334-338.) and husbandry systems (CAI & BAI, 2009Cai KZ, Bai JL. Infection intensity of gastrointestinal nematodosis and coccidiosis of sheep raised under three types of feeding and management regims in Ningxia Hui Autonomous Region, China. Small Rumin Res 2009; 85(2-3): 111-115. http://dx.doi.org/10.1016/j.smallrumres.2009.07.013.
http://dx.doi.org/10.1016/j.smallrumres....
). In three studies carried out in the Rio Grande do Norte State of Brazil, eight species of Eimeria were identified, from which E. bakuensis, E. ovinoidalis, E. parva, and E. faurei were the most prevalent (AHID et al., 2009Ahid SMM, Medeiros VMC, Bezerra ACDS, Maia MB, Xavier VM, Vieira LS. Espécies de gênero Schneider, 1875 (EimeriaApicomplexa: Eimeriidae) em pequenos ruminantes na mesorregião oeste do estado do Rio Grande do Norte, Brasil. Ciênc Anim Bras 2009; 10(3): 984-989.). In the Pernambuco State, E. ahsata, E. crandallis, E. faurei, and E. intricata (TEMBUE et al., 2009Tembue AASM, Ramos RAN, Lima MM, Faustino MAG, Meunier IMJ, Alves LC. Espécies do gênero Schneider, 1875 (Apicomplexa: Eimeriidae) em pequenos ruminantes, provenientes do município de Ibimirim, Estado de Pernambuco. EimeriaVet Not 2009; 15(2): 51-57. PMid:19136685.) and in the Rio Grande do Sul State, E. parva, E. ashata, E. punctata, and E. granulosa (SILVA et al., 2008Silva FRC, Souza JD, Fialho CG, Escopeli KS, Araújo FAP. Identificação das espécies de spp. em ovinos criados no município de Mostardas/RS. EimeriaVet Foco 2008; 6(1): 16-20.) were the most prevalent species. The analysis of all this information shows that the survey of the species present in a determined region, especially the pathogenic ones, has great importance in facilitating our understanding of the epidemiology (LIMA, 2004Lima JD. Coccidiose dos ruminantes domésticos. Rev Bras Vet Parasitol 2004; 13(S1): 9-13.) of eimeriosis and contributes to defining strategies for its control in a herd.

Among the ten species identified in the present study, six exhibited a micropylar cap (E. intricata, E. ahsata, E. bakuensis, E. granulosa, E. crandallis, and E. punctata). The presence or absence of a micropylar cap, the oocyst and sporocyst diameters, and the shape of the oocysts are reliable criteria to differentiate Eimeria species (HASSUM et al., 2007Hassum IC, Valladares GS, Menezes RCAA. Diferenciação das espécies de Eimeria parasitas de ovinos pelo uso da regressão linear e algoritimos morfológicos. Rev Bras Parasitol Vet 2007; 16(2): 97-104. PMid:17706012.). Regarding E. intricata, the polar (>50 µm) and equatorial (>35 µm) diameter of the oocysts were decisive for the identification. The measurements of the major and minor diameter of the oocysts and sporocysts are sufficient to identify E. intricata, E. ahsata, and E. pallida (LEVINE et al., 1980Levine ND, Corliss JO, Cox FEG, Deroux G, Grain G, Honigberg BM, et al. A newly revised classification of the protozoa. J Protozool 1980; 27(1): 37-58. http://dx.doi.org/10.1111/j.1550-7408.1980.tb04228.x. PMid:6989987.
http://dx.doi.org/10.1111/j.1550-7408.19...
). E. ahsata was differentiated from the other species with a micropylar cap by its ovoid format (HIDALGO-ARGÜELLO & CORDERO-DEL-CAMPILLO, 1988Hidalgo-Argüello MR, Cordero-Del-Campillo M. Epizootiology of coccidiosis in León (Spain). Eimeria ahsataVet Parasitol 1988; 27(3-4): 183-191. http://dx.doi.org/10.1016/0304-4017(88)90032-5. PMid:3369071.
http://dx.doi.org/10.1016/0304-4017(88)9...
).

Differentiation of E. ovinoidalis from the other species without a micropylar cap was determined by the diameter and the form (spherical or ovoid) of the oocysts; identification of E. crandallis, E. bakuensis, and E. granulosa was performed by the form (elliptical or spherical) of the oocysts (DENIZ, 2009Deniz A. Coccidiose ovina: revisão bibliográfica. Albéitar 2009; 3: 4-11.). The spherical form of the E. parva oocysts differs from the elliptical shape of the E. pallida (LEVINE et al., 1980Levine ND, Corliss JO, Cox FEG, Deroux G, Grain G, Honigberg BM, et al. A newly revised classification of the protozoa. J Protozool 1980; 27(1): 37-58. http://dx.doi.org/10.1111/j.1550-7408.1980.tb04228.x. PMid:6989987.
http://dx.doi.org/10.1111/j.1550-7408.19...
). The MI was strategic to differentiate some species (HASSUM et al., 2002Hassum IC, Paiva RV, Menezes RCAA. Freqüencia, dinâmica e morfologia dos oocistos de Eimeria bakuensis (Apicomplexa: Eimeriidae) em ovinos de diferentes categorias de produção de uma criação no município de Petrópolis/RJ. Rev Bras Parasitol Vet 2002; 11(1): 19-25.), in conjunction with the oocyst form; for example, in the differentiation between E. bakuensis and E. granulosa (Table 4), E. granulosa a presents pyriform shape and E. bakuensis shows an urn format, that is, elliptical with straight sides (LEVINE et al., 1980Levine ND, Corliss JO, Cox FEG, Deroux G, Grain G, Honigberg BM, et al. A newly revised classification of the protozoa. J Protozool 1980; 27(1): 37-58. http://dx.doi.org/10.1111/j.1550-7408.1980.tb04228.x. PMid:6989987.
http://dx.doi.org/10.1111/j.1550-7408.19...
). Although the morphometric method has limitations in differentiating the species due to overlap of some parameters (BERRIATUA et al., 1995Berriatua E, Gibson WC, Morgan KL. Development of DNA probes for the ovine Eimeria species E. crandallis and E. ovinoidalis.Parasitol Res 1995; 81(3): 222-229. PMid:7770428.), the combined use of these elements increases the efficiency of this method and provides satisfactory reliability to identify the species of Eimeria that parasitize sheep.

Table 4
Prevalence of Eimeria species oocysts in fecal samples of sheep raised extensively in the semiarid region.

Although species such as E. intricata, E. pallida, and E. punctata are not considered pathogenic to sheep (LE SUEUR et al., 2009Le Sueur C, Mage C, Mundt HC. Efficacy of toltrazuril (Baycox® 5% suspension) in natural infections with pathogenic Eimeria spp. in housed lambs. Parasitol Res 2009; 104(5): 1157-1162. http://dx.doi.org/10.1007/s00436-008-1305-9. PMid:19085006.
http://dx.doi.org/10.1007/s00436-008-130...
), the high prevalence of E. ovinoidalis and E. crandallis identified in the present study suggest that eimeriosis is an emerging disease condition of sheep raised under extensive systems in the semiarid region. E. ovinoidalis is the species that presented higher pathogenic potential for sheep, since even in low quantities (1.103) it is able to cause damage to the small intestine, with epithelium loss and atrophy of microvilli membranes (GREGORY & CATCHIPOLE, 1987Gregory MW, Catchipole J. Ovine coccidiosis: the pathology of infection. Eimeria ovinoidalisInt J Parasitol 1987; 17(6): 1099-1111. http://dx.doi.org/10.1016/0020-7519(87)90162-7. PMid:3654051.
http://dx.doi.org/10.1016/0020-7519(87)9...
). Intense infection by this species causes disequilibrium of the intestinal microflora, allowing the proliferation of Gram-positive bacteria and worsening the scope of diarrhea (YAKHCHALI & GOLAMI, 2008Yakhchali M, Golami E. infection (Coccidia: Eimeriidae) in sheep of different age groups in Sanandaj city, Iran. EimeriaVet Arhiv 2008; 78(1): 57-64.).

The high prevalence of E. ovinoidalis in different regions and husbandry systems (GUL & DEGER, 2002Gul A, Deger S. Prevalence and species found in sheep in the Van region. EimeriaTurk J Vet Anim Sci 2002; 26: 859-864.; TOULAH, 2007Toulah FH. Prevalence and comparative morphological study of four sp. of sheep in Jeddah area, Saudi Arabia. EimeriaJ Biol Sci 2007; 7(2): 413-416. http://dx.doi.org/10.3923/jbs.2007.413.416.
http://dx.doi.org/10.3923/jbs.2007.413.4...
; HASAN & ABED, 2012Hasan MH, Abed HM. A study of species in sheep in Mosul City. EimeriaIraq J Vet Sci 2012; 26(1): 45-53.) may be attributed to its high reproduction potential when compared to the other species (REEG et al., 2005Reeg KJ, Gauly M, Bauer C, Mertens C, Erhardt G, Zahner H. Coccidial infections in housed lambs: oocyst excretion, antibody levels and genetic influences on the infection. Vet Parasitol 2005; 127(3-4): 209-219. http://dx.doi.org/10.1016/j.vetpar.2004.10.018. PMid:15710521.
http://dx.doi.org/10.1016/j.vetpar.2004....
). E. crandallis, found in 95.0% of the evaluated properties, also presents considerable pathogenic potential; in high infection (≥1.105), it is capable of causing intestinal microvilli destruction (GREGORY & CATCHIPOLE, 1990Gregory MW, Catchipole J. Ovine coccidiosis: the patology of infection. Eimeria crandallisInt J Parasitol 1990; 20(7): 849-860. http://dx.doi.org/10.1016/0020-7519(90)90022-F. PMid:2276861.
http://dx.doi.org/10.1016/0020-7519(90)9...
) and compromises regeneration of the mucous membrane, which causes irreversible changes to the animal’s development (TAYLOR et al., 2003Taylor MA, Catchpole J, Marshall J, Marshall RN, Hoeben D. Histopathological observations on the activity of diclazuril (Vecoxan®) against the endogenous stages of in sheep. Eimeria crandallisVet Parasitol 2003; 116(4): 305-314. http://dx.doi.org/10.1016/S0304-4017(03)00256-5. PMid:14580801.
http://dx.doi.org/10.1016/S0304-4017(03)...
). Thus, the high infection intensity in young animals during the rainy season, coupled with the high prevalence of pathogenic species, show that eimeriosis is a potential risk for sheep raised under extensive systems in semiarid region.

Acknowledgements

The authors thank the State University of Southwest Bahia for supporting this research and Foundation for Research Support of the Bahia State (FAPESB) by a PhD scholarship.

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Publication Dates

  • Publication in this collection
    04 Dec 2015
  • Date of issue
    Oct-Dec 2015

History

  • Received
    18 June 2015
  • Accepted
    14 Sept 2015
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