Abstract
Eimeria spp. infections lead to acute or chronic intestinal disorders in small ruminants, being responsible for important economic losses worldwide. The aim of this study was to assess the risk factors associated with Eimeria spp. infection in small ruminants of the microregion of Garanhuns, state of Pernambuco, Northeastern Brazil. Fecal samples (n = 822) were obtained from goats (n = 414) and sheep (n = 408) and evaluated by the modified Gordon and Whitlock technique. Risk factors were assessed through univariate analysis and logistical regression. Oocysts of Eimeria species were detected in 62.9% (517/822) of the animals, with 77.8% (322/414) in goats and 47.8% (195/408) in sheep. For goats, the herd size (OR = 5.52), rearing system (OR = 1.57), feeding place (OR = 2.60), absence of mineral salt in the diet (OR = 2.54), flooring type (OR = 2.83) and periodicity of cleaning (OR = 5.39) were considered risk factors. Conversely, for sheep only the herd size (OR = 3.16) and rearing system (OR = 2.45) were important factors associated with infection by Eimeria spp. Data herein obtained brings meaningful information on the epidemiology of coccidiosis in small ruminants in Northeastern Brazil. The knowledge of these risk factors is useful to contribute to the development of preventive measures, thereby, reducing the economic impact caused by these protozoa in small ruminant production.
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Introduction
Protozoa belonging to the genus Eimeria (Apicomplexa) are obligate intracellular parasites of the intestinal epithelium, responsible for an economically important parasitic disease commonly known as coccidiosis. The main species that infect goats are Eimeria arloingi and Eimeria ninakohlyakimovae, whereas sheep are mainly affected by Eimeria ovinoidalis and Eimeria crandallis (Chartier and Paraud 2012; Souza et al. 2015; Sharma et al. 2017). It is known that the main route of transmission is through ingestion of sporulated oocysts (Bakunzi et al. 2010; Hashemnia et al. 2015). After that, the hatched sporozoites invade the intestinal cells and undergo multiple generations of asexual reproduction followed by sexual reproduction, resulting in damage to the intestinal lining and consequently inadequate nutrient absorption causing a reduction in weight gain (Ozmen et al. 2012).
For a long time, attention has been paid to coccidiosis due to its economic impact on ruminant production. In fact, in the United States is estimated that the economic losses may reach 341 million dollars annually (Grilo and Carvalho 2014). In addition, a previous study conducted in Europe demonstrated that the prophylactic treatment of coccidiosis represents a cost of 4.88 USD per calf (Lassen and Østergaard 2012). The cost for small ruminant production has not been assessed, but it is believed that the losses are worldwide present, especially in young animals.
Several factors related to the host, environment and parasite are associated with the occurrence of Eimeria infection (Rehman et al. 2011). The age of the host is considered an important risk factor, since it is known that small ruminants become infected within the first few days after birth, eliminating oocysts in the faeces by the second week of life (Saratsis et al. 2011). Conversely, older animals are sources of infection due to the frequent elimination of low numbers of oocysts in the faeces for long time (Foreyt 1990). Similarly, post-partum females are also responsible for maintaining a high burden of oocysts in the environment, facilitating the infection of young animals (Silva et al. 2007).
Subclinical infection is the most common manifestation of the disease, which has a significant impact on herd health and production (Lopez-Osorio et al. 2019). One of the first signs is a delay in development, especially in young animals (Andrade Júnior et al. 2012). However, when clinical infection occurs, signs such as diarrhea, anorexia, weight loss and dehydration can be observed. Knowledge of the inherent aspects of the course of infection is important in defining the appropriate preventative measures, as the administration of drugs, most of the time, does not successfully control coccidiosis (Young et al. 2011).
The assessment of risk factors is pivotal, as it helps to adopt prophylactic measures, consequently reducing the occurrence of Eimeria infection in small ruminants (Souza et al. 2015). However, these factors are poorly investigated in many regions where the rearing of goats and sheep is an important economic activity (Carrau et al. 2018). Thus, the aim of this study was to assess the risk factors associated with infection by Eimeria spp. in small ruminants from Northeastern Brazil.
Materials and methods
Study area
This study was performed in sheep and goats from private farms in the Garanhuns microregion (8°53′25″ South and 36°29′34″ West), state of Pernambuco, Northeastern Brazil (Fig. 1). The climate in this area is characterized as semi-arid with an annual average of temperature of 22 °C (from 17 to 30 °C), 900 m above sea level, average rainfall of 147 mm (from 25 to 295 mm), and relative humidity of 90%.
Animals, sampling and laboratorial procedures
Goat (n = 35,770) and sheep (n = 99,606) population number on the study area (IBGE 2016) was considered to define minimum sample size (n = 384) for each species. Moreover, it was considered a prevalence estimated in 50%, a confidence level of 95% and statistical error of 5% (Thrusfield 2004). The farms were randomly selected by convenience (Reis 2003). There were no exclusion criteria regarding breed, gender, age and rearing systems of the animals.
Fresh faecal samples (n = 822) were collected in goats (n = 414) and sheep (n = 408), from March 2017 to May 2018. Of the animals enrolled, 144 and 270 goats, and 172 and 236 sheep were classified as young (≤ 12 months old) and adults (> 12 months old), respectively. Collection was performed using plastic gloves, and after that, samples were stored at 4 °C in isothermal boxes until parasitological procedures. Each sample was individually processed by the modified Gordon and Whitlock technique (Gordon and Whitlock 1939). For the analysis of the risk factors, an investigative questionnaire based on information about the herd and sanitary conditions was applied to farmers following all the ethical guidelines for research, respecting the confidentiality of the interviewed people, which read and signed an informed consent previously approved by the ethical committee (License number 06/2017).
Data analysis
Descriptive statistical analysis was performed to obtain relative and absolute frequency. In addition, the Lilliefors test was used to verify the normality of the data. The Chi-square test with Yates correction (χ2) was used to compare the occurrence of Eimeria species infecting goats and sheep, as well as the occurrence of the protozoan in different ages of the small ruminants. Subsequently, for the analysis of the risk factors associated with Eimeria infection an univariate analysis of the variables of interest and logistic regression analysis considering as dependent variable the results of test (Gordon and Whitlock technique) was performed. Odds ratio (OR) values were obtained for each parameter assessed. The significance level was set at 5%. All analyses were carried out using the EPIINFOTM7.2.2.6 software.
Results
Of all samples analyzed, 62.9% (517/822) were positive for Eimeria spp. oocysts, being 77.8% (322/414) of goats (mean 560,155 ± 1,485,174) and 47.8% (195/408) of sheep (mean 166,769 ± 1,478,003) (χ2 = 77,881, p = 0.0000). No statistical difference was observed between the positivity and age of both species (χ2 = 1.027; p = 0.3109).
The univariate analysis associated only the herd size and rearing system as risk factors for the infection by Eimeria spp. in sheep. Conversely, in goats, the herd size, rearing system, feeding place (Fig. 2), absence of mineral salt in the diet, flooring type (Fig. 3) and periodicity of cleaning were considered risk factors (Tables 1 and 2).
Discussion
This study describes risk factors associated with infection by Eimeria spp. in small ruminants reared in Northeastern region of Brazil. The overall prevalence herein obtained (i.e., 77.8% for goats and 47.8% for sheep) revealed high parasitism by Eimeria spp. in both animal species. Currently, coccidiosis is one of the most important threats for small ruminant production (Souza et al. 2015; Carrau et al. 2018).
Several risk factors have been associated with infection by Eimeria species in ruminants, especially in bovines (Makau et al. 2017; Lopez-Osorio et al. 2019). Less data regarding small ruminants (i.e., goats and sheep) have been produced worldwide. However, this study identifies some risk factors associated with infection by these protozoans. It is known that the age is considered an important risk factor for infection by Eimeria species, however, in this study animals of different ages were equally exposed to Eimeria spp., differing from other studies in which young animals were more affected (Carrau et al. 2018; Squire et al. 2019).
Interestingly the herd size and rearing system were risk factors for the infection of both species. It has already been indicated that intensive and semi-intensive breeding systems, where high population density occurs, contribute to the propagation of coccidia species (Sharma et al. 2017). A common practice adopted in the farms herein studied was the partial confinement (usually at night) of animals. This data demonstrates that in the present study the semi-intensive rearing system and the high density of animals might have directly influenced infection by Eimeria spp. in goats and sheep.
Other risk factors such as feeding place, type of floor, absence of mineral salt in the diet and periodicity of cleaning were observed only for goats. It is important to note, that all factors mentioned above (except the use of mineral salt) are related to hygiene. Faecal contamination of water and food is important for the transmission of many protozoa, especially in places where animals are fed directly over the soil, favoring the ingestion of sporulated oocysts (Sharma et al. 2017). Precarious hygiene conditions (e.g., uncemented floor) associated with overcrowding in intensive rearing systems result in high levels of infection (Squire et al. 2019). Therefore, it is important to highlight that the place and conditions of food supply are fundamental, since proximity with the soil favors faecal contamination and consequent animal infection. A routine practice adopted in some farms enrolled in the present study was the usage of mineral salt. The absence of mineral salt in the diet of goats has also been considered a risk factor in the studied area. Currently, it is known that many formulations of mineral salt contain coccidiostatic compounds (e.g., decoquinate and monensin) that are used for the prophylaxis of coccidiosis (Andrade Júnior et al. 2012).
It is noteworthy that this study was the first to identify risk factors for infection by Eimeria spp. in goats and sheep in the study area. The data herein presented are important for understanding the factors that influence the occurrence of the infection by this protozoan. Accordingly, knowledge of these parameters is of great importance for the development of prophylactic strategies suitable for the different conditions and to minimize the economic losses for small ruminant production.
References
Andrade Júnior ALF, Silva PC, Aguiar EM, Santos FGDA (2012) Use of coccidiostat in mineral salt and study on ovine eimeriosis. Braz J Vet Parasitol 21:16–21
Bakunzi FR, Thwane SN, Motsei LE, Dzoma BM (2010) Diversity and seasonal occurrence of Eimeria species in a mixed flock of communally reared sheep and goats in Mafikeng in the North West Province, South Africa. J S Afr Vet Assoc 81:148–150
Carrau T, Silva LMR, Pérez D, Failing K, Mantínez-Carrasco C, Macías J, Taubert A, Hermosilla C, Ruiz Y (2018) Associated risk factors influencing ovine Eimeria infections in southern Spain. Vet Parasitol 263:54–58
Chartier C, Paraud C (2012) Coccidiosis due to Eimeria in sheep and goats, a review. Small Rumin Res 103:84–92
Foreyt WJ (1990) Coccidiosis and cryptosporidiosis in sheep and goats. Vet Clin North Am Food Anim Pract 6:655–669
Gordon HM, Whitlock HV (1939) A new technique for counting nematode eggs in sheep faeces. J Sci Ind Res 12:50–52
Grilo ML, Carvalho LM (2014) Coccidiose em ruminantes pequenos agentes e grandes problemas nas diarreias parasitárias. Prev Vet Med 1:34–48
Hashemnia M, Rezaei F, Chalechale A (2015) Prevalence, intensity, and pathological lesions of Eimeria infection in goats in western Iran. Comp Clin Path 24:805–810
IBGE-Instituto Brasileiro de Geografia e Estatística (2016) Cidades—Produção da Pecuária Municipal
Lassen B, Østergaard S (2012) Estimation of the economical effects of Eimeria infections in Estonian dairy herds using a stochastic model. Prev Vet Med 106:258–265
Lopez-Osorio S, Villar D, Failing K, Taubert A, Hermosilla C, Chaparro-Gutierrez JJ (2019) Epidemiological survey and risk factor analysis on Eimeria infections in calves and young cattle up to 1 year old in Colombia. Parasitol Res 1:1–12
Makau DN, Gitau GK, Muchemi GK, Thomas LF, Cook EAJ, Wardrop NA, Fèvre EM, Glanville WA (2017) Environmental predictors of bovine Eimeria infection in western Kenya. Trop Anim Health Prod 49:409–416
Ozmen O, Adanir R, Haligur M (2012) Immunohistochemical detection of the cytokine and chemokine expression in the gut of lambs and kids with coccidiosis. Small Rumin Res 105:345–350
Rehman T, Khan MN, Sajid MS, Abbas RZ, Arshad M, Iqbal A (2011) Epidemiology of Eimeria and associated risk factors in goats of district Toba Tek Singh, Pakistan. Indian J Anim Sci 82:282–285
Reis JC (2003) Estatística aplicada à pesquisa em ciência veterinária, Copyright, Recife, Brasil
Saratsis A, Joachim A, Alexandros S, Sotiraki S (2011) Lamb coccidiosis dynamics in different dairy production systems. Vet Parasitol 181:131–138
Sharma DK, Paul S, Rout PK, Mandal A, Bhusan S, Sharma N, Kushwah YK (2017) Caprine coccidiosis in semi-arid India: dynamics and factors affecting fecal oocysts count. J Adv Vet Anim Res 4:52–57
Silva TP, Facury Filho EJ, Nunes ABV, Albuquerque FHMAR, Ferreira PM, Carvalho AU (2007) Dinâmica da infecção natural por Eimeria spp. em cordeiros da raça Santa Inês criados em sistema semi-intensivo no Norte de Minas Gerais. Braz J Vet Res Anim Sci 59:1468–1472
Souza LEB, Cruz JF, Teixeira Neto MR, Albuquerque GR, Melo ADB, Tapia DMT (2015) Epidemiology of Eimeria infections in sheep raised extensively in a semiarid region of Brazil. Braz J Vet Parasitol 24:410–415
Squire SA, Robertson ID, Yang R, Avi I, Ryana U (2019) Prevalence and risk factors associated with gastrointestinal parasites in ruminant livestock in the Coastal Savannah zone of Ghana. Acta Trop 199:105126
Thrusfield MV (2004) Epidemiologia Veterinária, 2nd edn. Roca, São Paulo
Young G, Alley ML, Foster DM, Smith GW (2011) Efficacy of amprolium for the treatment of pathogenic Eimeria species in Boer goat kids. Vet Parasitol 178:346–349
Acknowledgements
Authors would like thank Bronwyn Campbell for her suggestions on the manuscript. Authors also thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the financial support. This study resulted from a Master of Science dissertation of the first author (Postgraduate Program in Ruminants Health and Reproduction), developed at the Federal Rural University of Pernambuco.
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This study was approved by the Ethics Committee for Animal Experimentation (ECAE) of the Universidade Federal Rural de Pernambuco under the license number: 06/2017. All applicable international, national, and/or institutional guidelines for the care and use of animals enrolled in the present study were followed.
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de Macedo, L.O., Bezerra-Santos, M.A., de Mendonça, C.L. et al. Prevalence and risk factors associated with infection by Eimeria spp. in goats and sheep in Northeastern Brazil. J Parasit Dis 44, 607–612 (2020). https://doi.org/10.1007/s12639-020-01235-3
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DOI: https://doi.org/10.1007/s12639-020-01235-3