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The diversity of Eimeria spp. in cattle in the Brazilian Semiarid region

A diversidade de Eimeria spp. em bovinos no Semiárido do Brasil

Abstract

The aim of the present study was to find out the diversity of Eimeria species in cattle herds in the semiarid region of Brazil. Forty cattle fecal samples were collected from 20 farms in the Paraíba State, Northeast Brazil, and examined by centrifugation-floatation technique in sucrose solution. From each positive animal, 20 oocysts were photographed and measured. Infection by Eimeria spp. was detected in 17.12% (137/800) of the samples analyzed. All the farms had at least one animal that was positive for Eimeria spp. (100%; 20/20). In total, 2740 coccidia were photographed and measured. The species detected were: Eimeria bovis (35.1%); Eimeria canadensis (17.48%); Eimeria auburnensis (14.7%); Eimeria ellipsoidalis (9.7%); Eimeria zuernii (7.22%); Eimeria brasiliensis (4.56%); Eimeria bukidnonensis (3.97%); Eimeria illinoisensis (2.91%); Eimeria wyomingensis (1.42%); Eimeria alabamensis (1.27%); Eimeria cylindrica (0.76%); Eimeria pellita (0.54%); Eimeria ildefonsoi (0.21%); and Eimeria subspherica (0.07%). It was concluded that cattle in the semiarid region of Brazil were parasitized by 14 species of Eimeria. It is thinked that the sanitary management employed, as well as the system used for raising these animals, is the crucial point that leads to high rates of infection in this region.

Keywords:
Coccidia; gastrointestinal protozoa; mixed production; ruminants

Resumo

Objetivou-se descrever a diversidade de Eimeria em rebanhos bovinos do Semiárido do Brasil. Amostras fecais de 40 bovinos foram coletadas, provenientes de 20 fazendas no Estado da Paraíba, Nordeste do Brasil, e examinadas pela técnica de centrífugo-flutuação em solução de sacarose. De cada animal positivo, foram fotografados e mensurados 20 oocistos. A presença de Eimeria spp. foi detectada em 17,12% (137/800) das amostras analisadas. Todas as propriedades tiveram ao menos um animal positivo para Eimeria spp. (100%; 20/20). No total, foram fotografados e mensurados 2.740 coccídios, cujas ocorrências foram: Eimeria bovis (35,1%), seguida de Eimeria canadensis (17,5%), Eimeria auburnensis (14,7%), Eimeria ellipsoidallis (9,7%), Eimeria zuernii (7,22%), Eimeria brasiliensis (4,56%), Eimeria bukidnonensis (3,97%), Eimeria illinoisensis (2,91%), Eimeria wyomingensis (1,42%), Eimeria alabamensis (1,27%), Eimeria cylindrica (0,76%), Eimeria pellita (0,54%), Eimeria ildefonsoi (0,21%) e Eimeria subspherica (0,07%). Concluiu-se que os bovinos do Semiárido do Brasil foram parasitados por 14 espécies de Eimeria, e acredita-se que o manejo sanitário empregado, bem como o sistema de criação desses animais, seja o ponto crucial para os altos índices de infecção nesta região.

Palavras-chave:
Coccídios; protozoários gastrintestinais; produção mista; ruminantes

Introduction

Cattle farming occupies a prominent place in the worldwide agricultural scenario, and Brazil is one of the largest milk producers and meat exporters (Brasil, 2021Brasil. Ministério da Agricultura Pecuária e Abastecimento – MAPA. Pecuária. [online] 2021 [cited 2021 Nov 19]. Available from: https://www.gov.br/agricultura/pt-br/assuntos/politica-agricola/todas-publicacoes-de-politica-agricola/agropecuaria-brasileira-em-numeros/abn-10-2021-1.pdf/view.
https://www.gov.br/agricultura/pt-br/ass...
). In the northeastern region of Brazil, beef cattle products and byproducts are used in food and commerce, thus generating stability and development (Carneiro, 2019Carneiro WMA. Comportamento da Pecuária do Nordeste no Limiar do Século XXI [online] 2019 [cited 2021 Nov 18]. Available from: https://www.bnb.gov.br/documents/45799/1057811/Comportamento+da+Pecu%C3%A1ria+do+Nordeste+no+Limiar+do+S%C3%A9culo+XXI.pdf/2b300bc7-253d-9745-23d3-1c499dac3267?t=1648743903348&download=true
https://www.bnb.gov.br/documents/45799/1...
). In the state of Paraíba, which is within this region of Brazil, cattle raising is also a viable activity that provides one of the main sources of animal protein for human consumption (IBGE, 2020Instituto Brasileiro de Geografia e Estatística ­– IBGE. Anuário estatístico do Brasil [online]. Rio de Janeiro: IBGE; 2020 [cited 2022 Feb 02]. Available from: https://biblioteca.ibge.gov.br/biblioteca-catalogo?id=720&view=detalhes.
https://biblioteca.ibge.gov.br/bibliotec...
). However, there are some obstacles to herd productivity. Among these, parasitism by enteric protozoa is responsible for diarrhea, weight loss and decreased meat and milk production, and may even lead to animal mortality in severe cases (Daugschies & Najdrowski, 2005Daugschies A, Najdrowski M. Eimeriosis in cattle: current understanding. J Vet Med B Infect Dis Vet Public Health 2005; 52(10): 417-427. http://dx.doi.org/10.1111/j.1439-0450.2005.00894.x. PMid:16364016.
http://dx.doi.org/10.1111/j.1439-0450.20...
; Dubey, 2019Dubey JP. Coccidiosis in livestock, poultry, companion animals, and humans. 1st ed. Boca Raton: CRC Press; 2019. http://dx.doi.org/10.1201/9780429294105.
http://dx.doi.org/10.1201/9780429294105...
; Lopez-Osorio et al., 2020Lopez-Osorio S, Villar D, Failing K, Taubert A, Hermosilla C, Chaparro-Gutierrez JJ. Epidemiological survey and risk factor analysis on Eimeria infections in calves and young cattle up to 1 year old in Colombia. Parasitol Res 2020; 119(1): 255-266. http://dx.doi.org/10.1007/s00436-019-06481-w. PMid:31760498.
http://dx.doi.org/10.1007/s00436-019-064...
).

The main protozoa of veterinary medical interest belong to the phylum Apicomplexa. These are characterized by obligate intracellular parasitism that causes disease and destroys the host cells (Dubey, 2019Dubey JP. Coccidiosis in livestock, poultry, companion animals, and humans. 1st ed. Boca Raton: CRC Press; 2019. http://dx.doi.org/10.1201/9780429294105.
http://dx.doi.org/10.1201/9780429294105...
). The genus Eimeria belongs to the class Sporozoasida, family Eimeriidae, and is transmitted by fecal-oral contamination. It develops in the epithelial cells of the digestive tract, where it causes an enteritis called eimeriosis or coccidiosis (Florião et al., 2016Florião MM, Lopes BB, Berto BP, Lopes CWG. New approaches for morphological diagnosis of bovine Eimeria species: a study on a subtropical organic dairy farm in Brazil. Trop Anim Health Prod 2016; 48(3): 577-584. http://dx.doi.org/10.1007/s11250-016-0998-5. PMid:26873157.
http://dx.doi.org/10.1007/s11250-016-099...
; Martins et al., 2020Martins NS, Motta SP, Santos CC, Moreira AS, Farias NAR, Ruas JL. Eimeriose em bovinos e ovinos: uma inimiga invisível. Braz J Develop 2020; 6(4): 19421-19434. http://dx.doi.org/10.34117/bjdv6n4-201.
http://dx.doi.org/10.34117/bjdv6n4-201...
).

This disease becomes important because of the losses resulting from mortality among young animals and because of the reduced performance of those that recover from the infection, due to their lower food consumption and consequently diminished weight development (Abebe et al., 2008Abebe R, Wossene A, Kumsa B. Epidemiology of Eimeria infections in calves in Addis Ababa and Debre Zeit dairy farms, Ethiopia. Int J Appl Res Vet Med 2008; 6(1): 24-30.). Adult animals are mostly asymptomatic hosts, but serve as sources of infection for young animals, which are more susceptible to infections and may present gastrointestinal disorders and growth retardation (Daugschies & Najdrowski, 2005Daugschies A, Najdrowski M. Eimeriosis in cattle: current understanding. J Vet Med B Infect Dis Vet Public Health 2005; 52(10): 417-427. http://dx.doi.org/10.1111/j.1439-0450.2005.00894.x. PMid:16364016.
http://dx.doi.org/10.1111/j.1439-0450.20...
; Hillesheim & Freitas, 2016Hillesheim LO, Freitas FLC. Ocorrência de eimeriose em bezerros criados em propriedades de agricultura familiar-nota científica. Cienc Anim Bras 2016; 17(3): 472-481. http://dx.doi.org/10.1590/1089-6891v17i333327.
http://dx.doi.org/10.1590/1089-6891v17i3...
).

Several species of Eimeria are known to parasitize cattle. Some of them, such as Eimeria zuernii and Eimeria bovis, are classified as more pathogenic (Bangoura & Daugschies, 2007Bangoura B, Daugschies A. Parasitological and clinical parameters of experimental Eimeria zuernii infection in calves and influence on weight gain and haemogram. Parasitol Res 2007; 100(6): 1331-1340. http://dx.doi.org/10.1007/s00436-006-0415-5. PMid:17265092.
http://dx.doi.org/10.1007/s00436-006-041...
). Animals parasitized by these species have clinical signs associated with bloody diarrhea, dehydration, anorexia and weight loss; depending on the severity of infection, these animals may die (Cardoso et al., 2017Cardoso IS, Marques LSJ, Alves MCD, Sakamoto CAM. Biologia e epidemiologia da eimeriose em ruminantes. Rev Cienc Vet Saúde Pública 2017; 4(Suppl 2): 131-136.).

Eimeria alabamensis and Eimeria auburnensis have been reported in outbreaks of moderately pathogenic clinical coccidiosis (Hillesheim & Freitas, 2016Hillesheim LO, Freitas FLC. Ocorrência de eimeriose em bezerros criados em propriedades de agricultura familiar-nota científica. Cienc Anim Bras 2016; 17(3): 472-481. http://dx.doi.org/10.1590/1089-6891v17i333327.
http://dx.doi.org/10.1590/1089-6891v17i3...
). Eimeria ellipsoidalis has been described as an occasional cause of diarrhea (Mielke et al., 1993Mielke D, Rudnick J, Hiepe T. Untersuchungen zur Immunprophylaxe bei der Kokzidiose des Rindes. Vet Med 1993; 48(1): 425-429.). Eimeria brasiliensis, Eimeria bukidnonensis, Eimeria canadensis, Eimeria cylindrica and Eimeria ildefonsoi have been characterized as presenting low pathogenicity, such that they are manifested subclinically (Lima, 2004Lima JD. Coccidiose dos ruminantes domésticos. Rev Bras Parasitol Vet 2004; 13(Suppl 1): 9-13.; Daugschies & Najdrowski, 2005Daugschies A, Najdrowski M. Eimeriosis in cattle: current understanding. J Vet Med B Infect Dis Vet Public Health 2005; 52(10): 417-427. http://dx.doi.org/10.1111/j.1439-0450.2005.00894.x. PMid:16364016.
http://dx.doi.org/10.1111/j.1439-0450.20...
; Das et al., 2015Das M, Deka DK, Sarmah PC, Islam S, Sarma S. Diversity of Eimeria spp. in dairy cattle of Guwahati, Assam, India. Vet World 2015; 8(8): 941-945. http://dx.doi.org/10.14202/vetworld.2015.941-945. PMid:27047181.
http://dx.doi.org/10.14202/vetworld.2015...
; Florião et al., 2016Florião MM, Lopes BB, Berto BP, Lopes CWG. New approaches for morphological diagnosis of bovine Eimeria species: a study on a subtropical organic dairy farm in Brazil. Trop Anim Health Prod 2016; 48(3): 577-584. http://dx.doi.org/10.1007/s11250-016-0998-5. PMid:26873157.
http://dx.doi.org/10.1007/s11250-016-099...
; Hillesheim & Freitas, 2016Hillesheim LO, Freitas FLC. Ocorrência de eimeriose em bezerros criados em propriedades de agricultura familiar-nota científica. Cienc Anim Bras 2016; 17(3): 472-481. http://dx.doi.org/10.1590/1089-6891v17i333327.
http://dx.doi.org/10.1590/1089-6891v17i3...
).

Therefore, identification of the various species of Eimeria spp. becomes very important. This enables focused disease control and prevention measures and favors adequate administration of medicines and disinfection of animal facilities in conventional production systems (Daugschies & Najdrowski, 2005Daugschies A, Najdrowski M. Eimeriosis in cattle: current understanding. J Vet Med B Infect Dis Vet Public Health 2005; 52(10): 417-427. http://dx.doi.org/10.1111/j.1439-0450.2005.00894.x. PMid:16364016.
http://dx.doi.org/10.1111/j.1439-0450.20...
), especially under conditions of higher stocking rates (Lima, 2004Lima JD. Coccidiose dos ruminantes domésticos. Rev Bras Parasitol Vet 2004; 13(Suppl 1): 9-13.).

Considering the scarcity of information and the economic losses caused by coccidiosis, the objective of this study was to describe the diversity of species of Eimeria infecting cattle herds in Northeastern Brazil.

Material and Methods

Experimental design

Between January and December 2020, fecal sample collections were carried out on 20 farms that had cattle herds of more than 40 animals that were raised within a semi-intensive system. These farms were located at municipalities in the State of Paraíba that lie within the intermediate regions of Campina Grande, Patos and Sousa-Cajazeiras, which all have a semi-arid climate (Figure 1). The average annual precipitation in the State of Paraíba is between 250-800 mm. The rainfall is irregular and usually concentrated in the months of March to May. The maximum temperature is 32°C and the minimum is 20°C; the evaporation rates are high and the relative air humidity is close to 70%. The vegetation is predominantly that of the Caatinga biome (INMET, 2010Instituto Nacional de Meteorologia – INMET. Normais climatológicas do Brasil 1981-2010 [online]. Brasília, DF: INMET; 2010 [cited 2021 July 12]. Available from: http://www.inmet.gov.br/portal/index.php?r=clima/normaisClimatologicas.
http://www.inmet.gov.br/portal/index.php...
).

Figure 1
Geographical distribution of Municipalities in the Semiarid region of Paraíba, Northeastern Brazil, in which farms were visited to collect bovine feces.

Forty animals were randomly sampled from each of the 20 farms (which were all dairy farms), without distinction regarding their breed, sex or age, thus totaling 800 sampled animals.

Sample collection and processing for analysis

Feces were collected directly from the rectum of the animals with the aid of clean plastic bags. The animals were identified according to their number, sex, age and farm. The samples were stored in isothermal boxes and were sent to the Veterinary Parasitology Laboratory (VPL) of the Veterinary Hospital of the Federal Institute of Paraíba (IFPB), Sousa, PB, Brazil, for further laboratory analysis.

To investigate the enteric protozoa, the centrifugation-floatation technique in sucrose solution was used, as originally described by Sheather (1923)Sheather AL. The detection of intestinal protozoa and mange parasites by a flotation technique. J Comp Pathol Ther 1923; 36: 266-275. http://dx.doi.org/10.1016/S0368-1742(23)80052-2.
http://dx.doi.org/10.1016/S0368-1742(23)...
and as modified by Duszynski & Wilber (1997)Duszynski DW, Wilber PG. A guideline for the preparation of species descriptions in the Eimeriidae. J Parasitol 1997; 83(2): 333-336. http://dx.doi.org/10.2307/3284470. PMid:9105325.
http://dx.doi.org/10.2307/3284470...
. Through this, any presence of oocysts of Eimeria spp. was determined. Then, the feces of the positive animals were diluted in an aqueous solution of 2.5% potassium dichromate (K2Cr2O7), at a ratio of one-sixth feces to five-sixths solution. This mixture was placed in Petri dishes and left in a B.O.D. chamber at 28 ºC and relative humidity > 80% for 15 days, to await oocyst sporulation.

After this sporulation period, centrifugation-floatation was performed in a new sucrose solution. From this, a drop of the surface material was removed, placed on a slide under a coverslip, and the oocysts were viewed using a MAX-300 microscope with 40X and 100X objectives. This was coupled to a microcomputer through the MvImage® software, in the same way as described by Araújo et al. (2020)Araújo HG, Silva JT, Sarmento WF, Silva SS, Bezerra RA, Azevedo SS, et al. Diversity of enteric coccidia in pigs from the Paraíba Semiarid Region of Northeastern Brazil. Rev Bras Parasitol Vet 2020; 29(4): e009120. http://dx.doi.org/10.1590/s1984-29612020079. PMid:33053055.
http://dx.doi.org/10.1590/s1984-29612020...
.

From each positive sample, 20 intact sporulated oocysts of the genus Eimeria were photographed and measured in terms of the maximum, average and minimum diameters, and the Shape Index (SI) of these oocysts and sporocysts was calculated. In addition, the thickness of the oocyst wall was measured and the presence or absence of internal morphological structures was noted. To make morphological identifications of Eimeria species, the reference keys for sporulated oocysts described by Levine & Ivens (1967)Levine ND, Ivens V. The sporulated oocysts of Eimeria illinoisensis n. sp. and of other species of Eimeria of the ox. J Protozool 1967; 14(2): 351-360. http://dx.doi.org/10.1111/j.1550-7408.1967.tb02008.x. PMid:6068382.
http://dx.doi.org/10.1111/j.1550-7408.19...
, Levine (1985)Levine ND. Protozoan parasites of domestic animals and of man. 2nd ed. Urbana: Burgess Publishing; 1985., Duszynski & Wilber (1997)Duszynski DW, Wilber PG. A guideline for the preparation of species descriptions in the Eimeriidae. J Parasitol 1997; 83(2): 333-336. http://dx.doi.org/10.2307/3284470. PMid:9105325.
http://dx.doi.org/10.2307/3284470...
, Berto et al. (2014)Berto BP, McIntosh D, Lopes CWG. Studies on coccidian oocysts (Apicomplexa: eucoccidiorida). Rev Bras Parasitol Vet 2014; 23(1): 1-15. http://dx.doi.org/10.1590/S1984-29612014001. PMid:24728354.
http://dx.doi.org/10.1590/S1984-29612014...
and Florião et al. (2016)Florião MM, Lopes BB, Berto BP, Lopes CWG. New approaches for morphological diagnosis of bovine Eimeria species: a study on a subtropical organic dairy farm in Brazil. Trop Anim Health Prod 2016; 48(3): 577-584. http://dx.doi.org/10.1007/s11250-016-0998-5. PMid:26873157.
http://dx.doi.org/10.1007/s11250-016-099...
were used.

Statistical analysis

The mean diameter, lower limit, upper limit, standard deviation and coefficient of variation (CV) of the oocysts of Eimeria spp. and their sporocysts were evaluated using the Microsoft Office Excel 2010® software.

Results

Oocysts of Eimeria spp. were found on 100% (20/20) of the farms visited. The presence of oocysts was detected in 17.12% (137/800) of the samples. It was found that 10.21% (14/137) of the cattle were parasitized by only one Eimeria species; 27% (37/137) were parasitized by two different species; 23.35% (32/137) had three species; 16.78% (23/137) were parasitized by four species; 14.59% (20/137) were parasitized by five species; 4.37% (6/137) were parasitized by six species; and 3.64% (5/137) were parasitized by seven different species of Eimeria.

Based on the morphological characteristics of 2,740 intact sporulated oocysts, 14 species of the genus Eimeria were identified, which are listed here in descending order of frequency of occurrence: E. bovis Züblin, 1998 (Figure 2A); E. canadensis Bruce, 1921 (Figure 2B); E. auburnensis Cristenses and Poeter, 1939 (Figure 2C); E. ellipsoidalis Becker & Frye, 1929 (Figure 2D); E. zuernii Rivolta, 1878 (Figure 2E); E. brasiliensis Torres & Ramos, 1939 (Figure 2F); E. bukidnonensis Tubangui, 1939 (Figure 2G); E. illinoisensis Levine & Ivens, 1967 (Figure 2H); E. wyomingensis Huizinga & Winger, 1942 (Figure 2I); E. alabamensis Christenses, 1941 (Figure 2J); E. cylindrica Wilson, 1931 (Figure 2K); E. pellita Supperer, 1952 (Figure 2L); E. ildefonsoi Torres & Ramos, 1939 (Figure 2M); and E. subspherica Christenses, 1941 (Figure 2N).

Figure 2
Photomicrographs of oocysts of Eimeria spp. in cattle in the Semiarid region of Paraíba, Northeastern Brazil. A: Eimeria bovis; B: Eimeria canadensis; C: Eimeria auburnensis; D: Eimeria ellipsoidalis; E: Eimeria zuernii; F: Eimeria brasiliensis; G: Eimeria bukidnonensis; H: Eimeria illinoisensis; I: Eimeria wyomingensis; J: Eimeria alabamensis; K: Eimeria cylindrica; L: Eimeria pellita; M: Eimeria ildefonsoi; N: Eimeria subspherica.

The morphological characteristics and respective occurrence rates of the Eimeria species obtained in this study are described in Table 1. The percentages of occurrence and the mean values for the length, width, standard deviation, morphometric index, coefficient of variation and number of oocysts and sporocysts found in these Eimeria species are described in Table 2.

Table 1
Occurrence and morphology of oocysts and sporocysts of Eimeria spp. in cattle in the semiarid region of northeastern Brazil.
Table 2
Micrometric measurements of oocysts and sporocysts of Eimeria spp. infecting cattle in the semiarid region of Northeast Brazil.

Discussion

The present study was the first to identify and describe distinct species of Eimeria parasitizing cattle in the semiarid region of Northeastern Brazil. Because of the high occurrence rates found, along with the presence of highly pathogenic species, we think that the number of cases of bovine coccidiosis was high. According to Hamid et al. (2019)Hamid PH, Kristianingrum YP, Prastowo S. Bovine coccidiosis cases of beef and dairy cattle in Indonesia. Vet Parasitol Reg Stud Reports 2019; 17: 100298. http://dx.doi.org/10.1016/j.vprsr.2019.100298. PMid:31303235.
http://dx.doi.org/10.1016/j.vprsr.2019.1...
and Dubey (2019)Dubey JP. Coccidiosis in livestock, poultry, companion animals, and humans. 1st ed. Boca Raton: CRC Press; 2019. http://dx.doi.org/10.1201/9780429294105.
http://dx.doi.org/10.1201/9780429294105...
, coccidiosis is distributed worldwide, reaching up to 100% of calves in the first weeks of age. Thus, it has a high impact on livestock development and economic results. The high incidence of infections by Eimeria spp. is associated with higher prevalence of the subclinical form, which therefore makes it difficult to assess the real economic impact caused by eimeriosis in cattle herds. The most frequent clinical sign is severe and/or hemorrhagic diarrhea; presence of the subclinical form is associated with less pathogenic species, low environmental pressure from more pathogenic species or an acquired immune response that already exists (Daugschies et al., 2007Daugschies A, Agneessens J, Goossens L, Mengel H, Veys P. The effect of a metaphylactic treatment with diclazuril (Vecoxan) on the oocyst excretion and growth performance of calves exposed to a natural Eimeria infection. Vet Parasitol 2007; 149(3-4): 199-206. http://dx.doi.org/10.1016/j.vetpar.2007.08.003. PMid:17850970.
http://dx.doi.org/10.1016/j.vetpar.2007....
; Gillhuber et al., 2014Gillhuber J, Rugamer D, Pfister K, Scheuerle MC. Giardiosis and other enteropathogenic infections: a study on diarrhoeic calves in Southern Germany. BMC Res Notes 2014; 7(1): 112. http://dx.doi.org/10.1186/1756-0500-7-112. PMid:24568139.
http://dx.doi.org/10.1186/1756-0500-7-11...
).

This investigation also revealed that 14 species of Eimeria were present, which can be considered to be a high level of diversity. Lopez-Osorio et al. (2020)Lopez-Osorio S, Villar D, Failing K, Taubert A, Hermosilla C, Chaparro-Gutierrez JJ. Epidemiological survey and risk factor analysis on Eimeria infections in calves and young cattle up to 1 year old in Colombia. Parasitol Res 2020; 119(1): 255-266. http://dx.doi.org/10.1007/s00436-019-06481-w. PMid:31760498.
http://dx.doi.org/10.1007/s00436-019-064...
found similar diversity among cattle in different production systems in Colombia, in which identified 13 species of Eimeria. Seven species of Eimeria were also found by Das et al. (2015)Das M, Deka DK, Sarmah PC, Islam S, Sarma S. Diversity of Eimeria spp. in dairy cattle of Guwahati, Assam, India. Vet World 2015; 8(8): 941-945. http://dx.doi.org/10.14202/vetworld.2015.941-945. PMid:27047181.
http://dx.doi.org/10.14202/vetworld.2015...
, in dairy cattle in India; and by Florião et al. (2016)Florião MM, Lopes BB, Berto BP, Lopes CWG. New approaches for morphological diagnosis of bovine Eimeria species: a study on a subtropical organic dairy farm in Brazil. Trop Anim Health Prod 2016; 48(3): 577-584. http://dx.doi.org/10.1007/s11250-016-0998-5. PMid:26873157.
http://dx.doi.org/10.1007/s11250-016-099...
, on an organic dairy cattle farm in Rio de Janeiro, Brazil.

Although the occurrence rate of Eimeria spp. observed among the cattle studied here (17.12%; 137/832) can be considered high, it differed from the results found by Hillesheim & Freitas (2016)Hillesheim LO, Freitas FLC. Ocorrência de eimeriose em bezerros criados em propriedades de agricultura familiar-nota científica. Cienc Anim Bras 2016; 17(3): 472-481. http://dx.doi.org/10.1590/1089-6891v17i333327.
http://dx.doi.org/10.1590/1089-6891v17i3...
, in the State of Paraná, Brazil, who reported that the prevalence of coccidia was 48.2% (53/110) among the animals evaluated, on family-run farms. The rate in the present study was also lower than the prevalences recorded by Lopez-Osorio et al. (2020)Lopez-Osorio S, Villar D, Failing K, Taubert A, Hermosilla C, Chaparro-Gutierrez JJ. Epidemiological survey and risk factor analysis on Eimeria infections in calves and young cattle up to 1 year old in Colombia. Parasitol Res 2020; 119(1): 255-266. http://dx.doi.org/10.1007/s00436-019-06481-w. PMid:31760498.
http://dx.doi.org/10.1007/s00436-019-064...
in Colombia and by Hastutiek et al. (2019)Hastutiek P, Yuniarti WM, Djaeri M, Lastuti NDR, Suprihati E, Suwanti LT. Prevalence and diversity of gastrointestinal protozoa in Madura cattle at Bangkalan Regency, East Java, Indonesia. Vet World 2019; 12(2): 198-204. http://dx.doi.org/10.14202/vetworld.2019.198-204. PMid:31040558.
http://dx.doi.org/10.14202/vetworld.2019...
in Indonesia, with 75.5% (1006/1333) and 53.42% (190/357), respectively, in the cattle herds evaluated. We think that the semi-intensive rearing system used on the farms studied here may have had a relationship with the lower rates of infections found in the present study. Higher levels of coccidia are mainly related to fecal-oral contamination in feedlots (Kimeli et al., 2020Kimeli P, VanLeeuwen J, Gitau G, Heider L, McKenna S, Greenwood S. Management factors associated with time-to-onset and fecal egg/oocyst counts of gastrointestinal parasites in heifer calves on Kenyan smallholder farms. Vet Parasitol 2020; 283: 109174. http://dx.doi.org/10.1016/j.vetpar.2020.109174. PMid:32629206.
http://dx.doi.org/10.1016/j.vetpar.2020....
). In addition, the high average annual temperatures and low rainfall to which oocysts are subjected in the environment of the semiarid climate may have led to reduction of their survival and consequent reduction of reinfection of the animals.

Notable numbers of species of Eimeria were identified parasitizing the same individuals. It can be highlighted that some animals (5/137) had up to seven different species. This demonstrates that there was high potential for coinfection among the cattle in the herds examined. Mixed infections were also observed by Abebe et al. (2008)Abebe R, Wossene A, Kumsa B. Epidemiology of Eimeria infections in calves in Addis Ababa and Debre Zeit dairy farms, Ethiopia. Int J Appl Res Vet Med 2008; 6(1): 24-30. in Ethiopia, ranging from two to eight species per animal. Amid the diversity of Eimeria species infecting the same animal, it is difficult to control these parasites through vaccines (Sultana et al., 2014Sultana R, Maqbool A, Ahmad M, Anjum AA, Ilyas Ch S, Ahmad MS. Control of Coccidiosis in calves by vaccination. J Bacteriol Parasitol 2014; 5(4): 4. http://dx.doi.org/10.4172/2155-9597.1000197.
http://dx.doi.org/10.4172/2155-9597.1000...
; Dubey, 2019Dubey JP. Coccidiosis in livestock, poultry, companion animals, and humans. 1st ed. Boca Raton: CRC Press; 2019. http://dx.doi.org/10.1201/9780429294105.
http://dx.doi.org/10.1201/9780429294105...
), since the variability of Eimeria spp. is very high. Studies have indicated that the real impact of coinfections by Eimeria spp. is still uncertain, considering that clinical signs of diarrhea in calves have been found only in association with single infections by E. zuernii or E. bovis (Bangoura et al., 2011Bangoura B, Mundt HC, Schmäschke R, Westphal B, Daugschies A. Prevalence of Eimeria bovis and Eimeria zuernii in German cattle herds and factors influencing oocyst excretion. Parasitol Res 2011;109(1 Suppl 1): 129-138. http://dx.doi.org/10.1007/s00436-011-2409-1. PMid:21739382.
http://dx.doi.org/10.1007/s00436-011-240...
; Enemark et al., 2013Enemark HL, Dahl J, Enemark JMD. Eimeriosis in Danish dairy calves – correlation between species, oocyst excretion and diarrhoea. Parasitol Res 2013;112(S1 Suppl 1): 169-176. http://dx.doi.org/10.1007/s00436-013-3441-0. PMid:23765344.
http://dx.doi.org/10.1007/s00436-013-344...
; Lopez-Osorio et al., 2020Lopez-Osorio S, Villar D, Failing K, Taubert A, Hermosilla C, Chaparro-Gutierrez JJ. Epidemiological survey and risk factor analysis on Eimeria infections in calves and young cattle up to 1 year old in Colombia. Parasitol Res 2020; 119(1): 255-266. http://dx.doi.org/10.1007/s00436-019-06481-w. PMid:31760498.
http://dx.doi.org/10.1007/s00436-019-064...
).

Eimeria bovis was the most frequently found species (35.1%), and it stood out as the most pathogenic species among the more than 20 species of Eimeria already described in cattle (Daugschies & Najdrowski, 2005Daugschies A, Najdrowski M. Eimeriosis in cattle: current understanding. J Vet Med B Infect Dis Vet Public Health 2005; 52(10): 417-427. http://dx.doi.org/10.1111/j.1439-0450.2005.00894.x. PMid:16364016.
http://dx.doi.org/10.1111/j.1439-0450.20...
; Bangoura & Daugschies, 2007Bangoura B, Daugschies A. Parasitological and clinical parameters of experimental Eimeria zuernii infection in calves and influence on weight gain and haemogram. Parasitol Res 2007; 100(6): 1331-1340. http://dx.doi.org/10.1007/s00436-006-0415-5. PMid:17265092.
http://dx.doi.org/10.1007/s00436-006-041...
; Deplazes et al., 2016Deplazes P, Eckert J, Mathis A, von Samson-Himmelstjerna G, Zahner H. Parasitology in Veterinary Medicine. The Netherlands: Wageningen Academic Publishers; 2016. http://dx.doi.org/10.3920/978-90-8686-274-0.
http://dx.doi.org/10.3920/978-90-8686-27...
). According to Hermosilla et al. (2012)Hermosilla C, Ruiz A, Taubert A. Eimeria bovis: an update on parasite-host cell interactions. Int J Med Microbiol 2012; 302(4-5): 210-215. http://dx.doi.org/10.1016/j.ijmm.2012.07.002. PMid:22925990.
http://dx.doi.org/10.1016/j.ijmm.2012.07...
and Lopez-Osorio et al. (2020)Lopez-Osorio S, Villar D, Failing K, Taubert A, Hermosilla C, Chaparro-Gutierrez JJ. Epidemiological survey and risk factor analysis on Eimeria infections in calves and young cattle up to 1 year old in Colombia. Parasitol Res 2020; 119(1): 255-266. http://dx.doi.org/10.1007/s00436-019-06481-w. PMid:31760498.
http://dx.doi.org/10.1007/s00436-019-064...
, the clinical conditions caused by these species give rise to enteric infections that result in severe hemorrhagic typhlocolitis, clinically characterized by hemorrhagic and catarrhal diarrhea.

The other two most frequent species were E. canadensis (17.48%) and E. auburnensis (14.70%). This finding differed from the sequence observed by Vidal et al. (2013)Vidal LGP, Fagundes TF, Pantoja CS, Menezes RCAA. Morfometria de oocistos de Eimeria em bezerras segundo a faixa etária e a intensidade de infecção, Munícipio de Piraí, RJ. Rev Bras Saúde Prod Anim 2013; 14(4): 765-777. http://dx.doi.org/10.1590/S1519-99402013000400004.
http://dx.doi.org/10.1590/S1519-99402013...
, who found that the species E. ellipsoidalis (39.7%), E. alabamensis (18.4%) and E. bovis (12.1%) predominated in calves in the state of Rio de Janeiro, in southeastern Brazil; and also differed from the findings of Hillesheim & Freitas (2016)Hillesheim LO, Freitas FLC. Ocorrência de eimeriose em bezerros criados em propriedades de agricultura familiar-nota científica. Cienc Anim Bras 2016; 17(3): 472-481. http://dx.doi.org/10.1590/1089-6891v17i333327.
http://dx.doi.org/10.1590/1089-6891v17i3...
, in calves in Paraná, southern Brazil, where E. bovis, E. auburnensis and E. alabamensis were the most frequently encountered species, with rates of 23.6%, 11.8% and 9.1%, respectively. These species caused outbreaks of clinical coccidiosis of considerable pathogenicity.

Eimeria canadensis, E. ellipsoidalis, E. brasiliensis, E. bukidnonensis, E. illinoisensis, E. wyomingensis, E. alabamensis, E. cylindrica, E. pellita, E. ildefonsoi and E. subspherica, which were also described in the present study, are considered to be highly prevalent worldwide (Eckert et al., 1995Eckert J, Braun R, Shirley MW, Coudert P. Biotechnology: guidelines on techniques in coccidiosis research. 1st ed. Brussels: Publication Officce; 1995.; Florião et al., 2016Florião MM, Lopes BB, Berto BP, Lopes CWG. New approaches for morphological diagnosis of bovine Eimeria species: a study on a subtropical organic dairy farm in Brazil. Trop Anim Health Prod 2016; 48(3): 577-584. http://dx.doi.org/10.1007/s11250-016-0998-5. PMid:26873157.
http://dx.doi.org/10.1007/s11250-016-099...
). Even in the absence of clinical disease, cattle can be severely affected due to damage inflicted on intestinal tissue, thereby compromising the digestive process and general homeostasis, with adverse effects on wellbeing and animal performance (Daugschies & Najdrowski, 2005Daugschies A, Najdrowski M. Eimeriosis in cattle: current understanding. J Vet Med B Infect Dis Vet Public Health 2005; 52(10): 417-427. http://dx.doi.org/10.1111/j.1439-0450.2005.00894.x. PMid:16364016.
http://dx.doi.org/10.1111/j.1439-0450.20...
).

One important morphological tool that helps to differentiate the species of the genus Eimeria is the SI. This consists of dividing the largest diameter by the smallest. Oocysts may vary in size but their MIs show a rectilinear trend that reflects the volumetric shape of the sporulated oocysts. This SI is more precise for comparison between species than the average of dimensions, and also for comparing intraspecific variation (Long & Joyner, 1984Long PL, Joyner LP. Problems in the identification of species of Eimeria. J Protozool 1984; 31(4): 535-541. http://dx.doi.org/10.1111/j.1550-7408.1984.tb05498.x. PMid:6392531.
http://dx.doi.org/10.1111/j.1550-7408.19...
; Vidal et al., 2013Vidal LGP, Fagundes TF, Pantoja CS, Menezes RCAA. Morfometria de oocistos de Eimeria em bezerras segundo a faixa etária e a intensidade de infecção, Munícipio de Piraí, RJ. Rev Bras Saúde Prod Anim 2013; 14(4): 765-777. http://dx.doi.org/10.1590/S1519-99402013000400004.
http://dx.doi.org/10.1590/S1519-99402013...
; Araújo et al., 2020Araújo HG, Silva JT, Sarmento WF, Silva SS, Bezerra RA, Azevedo SS, et al. Diversity of enteric coccidia in pigs from the Paraíba Semiarid Region of Northeastern Brazil. Rev Bras Parasitol Vet 2020; 29(4): e009120. http://dx.doi.org/10.1590/s1984-29612020079. PMid:33053055.
http://dx.doi.org/10.1590/s1984-29612020...
).

Molecular tools are already being studied and are available for identifying oocysts of coccidia in cattle (Hastutiek et al., 2022Hastutiek P, Lastuti NDR, Suwanti LT, Sunarso A, Suprihati E, Kurniawati DA, et al. Coproparasitological examinations and molecular determination of Eimeria species in Madura cattle reared on Madura Island, Indonesia. Parasitol Int 2022; 86: 102478. http://dx.doi.org/10.1016/j.parint.2021.102478. PMid:34626806.
http://dx.doi.org/10.1016/j.parint.2021....
). However, Lopez-Osorio et al. (2020)Lopez-Osorio S, Villar D, Failing K, Taubert A, Hermosilla C, Chaparro-Gutierrez JJ. Epidemiological survey and risk factor analysis on Eimeria infections in calves and young cattle up to 1 year old in Colombia. Parasitol Res 2020; 119(1): 255-266. http://dx.doi.org/10.1007/s00436-019-06481-w. PMid:31760498.
http://dx.doi.org/10.1007/s00436-019-064...
and Vidal et al. (2013)Vidal LGP, Fagundes TF, Pantoja CS, Menezes RCAA. Morfometria de oocistos de Eimeria em bezerras segundo a faixa etária e a intensidade de infecção, Munícipio de Piraí, RJ. Rev Bras Saúde Prod Anim 2013; 14(4): 765-777. http://dx.doi.org/10.1590/S1519-99402013000400004.
http://dx.doi.org/10.1590/S1519-99402013...
demonstrated that oocyst morphology is still an appropriate and reliable method for differentiating coccidia in epidemiological surveys. This was also shown by Araújo et al. (2020)Araújo HG, Silva JT, Sarmento WF, Silva SS, Bezerra RA, Azevedo SS, et al. Diversity of enteric coccidia in pigs from the Paraíba Semiarid Region of Northeastern Brazil. Rev Bras Parasitol Vet 2020; 29(4): e009120. http://dx.doi.org/10.1590/s1984-29612020079. PMid:33053055.
http://dx.doi.org/10.1590/s1984-29612020...
, through identifying species of coccidia in pigs in the semiarid region of northeastern Brazil.

Nonetheless, oocysts and/or sporocysts with MIs greater than 1.1 should always be described carefully. These may have a variety of shapes, such as ellipsoidal, ovoid or pear-shaped, i.g.: they form a so-called “ellipsoidal complex”. On the other hand, spherical oocysts usually have an MI of 1.0, while subspherical oocysts have MIs between 1.0 and 1.1 (Levine, 1985Levine ND. Protozoan parasites of domestic animals and of man. 2nd ed. Urbana: Burgess Publishing; 1985.; Berto et al., 2014Berto BP, McIntosh D, Lopes CWG. Studies on coccidian oocysts (Apicomplexa: eucoccidiorida). Rev Bras Parasitol Vet 2014; 23(1): 1-15. http://dx.doi.org/10.1590/S1984-29612014001. PMid:24728354.
http://dx.doi.org/10.1590/S1984-29612014...
).

Our measurements of the length and width of the oocysts and sporocysts showed CVs below 25%. According to Siqueira & Tibúrcio (2011)Siqueira AL, Tibúrcio JD. Estatística na área da saúde: conceitos, metodologia, aplicações e prática computacional. 1. ed. Belo Horizonte: Editora Coopmed; 2011., CVs below 10% are considered low, while those above 30% are considered very high. In the current study, the CVs of oocyst length and width were lower than those of sporocysts, i.e. the oocysts were more homogeneous, thus only showing low to medium dispersion.

Conclusion

The diversity of Eimeria species is high among cattle in the semiarid region of northeastern Brazil. E. bovis, which is considered to be the most pathogenic species, showed the highest frequency of occurrence. Multiple infections by up to seven species were found in the animals. The semi-intensive rearing system and the semiarid conditions to which oocysts are exposed may have been limiting factors regarding their survival. These conditions may therefore have acted towards reduction of reinfection among the animals, since, despite the high rate of occurrence of infections that was found, these values were lower than those reported from studies conducted in other locations.

Acknowledgements

This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

  • How to cite: Melo LRB, Sousa LC, Lima BA, Silva ALP, Lima EF, Ferreira LC et al. The diversity of Eimeria spp. in cattle in the Brazilian Semiarid region. Braz J Vet Parasitol 2022; 31(3): e006422. https://doi.org/10.1590/S1984-29612022037

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    » http://dx.doi.org/10.1590/S1519-99402013000400004

Publication Dates

  • Publication in this collection
    11 July 2022
  • Date of issue
    2022

History

  • Received
    25 Apr 2022
  • Accepted
    20 June 2022
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