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Prevalence and risk factors of coccidiosis in calves from Veracruz, México

Prevalência e fatores de risco da coccidiose em bezerros em Veracruz, México

Abstract

The objectives of the present study were: (1) to determine the prevalence of Eimeria spp. sporulated oocysts in calves from 26 Municipalities in the Central Zone of the State of Veracruz, Mexico, (2) to identify the Eimeria spp. infecting calves, and (3) to identify the risk factors associated with the presence of Eimeria spp. in tropical cattle. A total of 930 individual fecal samples were analyzed by using the McMaster technique; then, oocysts were maintained in 2.5% potassium dichromate to allow sporulation. The general prevalence of calves with Eimeria spp. oocysts was 39.7% (370/930). Of a total of 10 identified species, Eimeria canadensis was the most observed, followed by Eimeria bovis and Eimeria zuernii. The statistical analysis showed an association between the age of the calves (5 to 9 months), the presence of other animals, the physiographic regions and the restricted type of husbandry with the presence of Eimeria spp. in calves (P<0.05). Protective risk factors, such as: routine coprological analysis was also associated with a decrease in infection. These data demonstrate the presence of coccidia in cattle from the State of Veracruz, additionally to the necessary measures that must be taken to control this parasitosis.

Keywords:
Cattle; Eimeria spp.; prevalence; risk factors; Veracruz

Resumo

Os objetivos do presente estudo foram: (1) determinar a prevalência de oocistos esporulados de Eimeria spp. em bezerros de 26 municípios na zona central do estado de Veracruz, México; (2) identificar as espécies de Eimeria que infectam bezerros; e (3) identificar os factores de risco associados à presença de Eimeria spp. em bovinos de região tropical. Um total de 930 amostras individuais de fezes foi analisado usando-se a técnica McMaster. Depois oocistos foram mantidos em 2,5% de dicromato de potássio para esporulação. A prevalência geral de animais com oocistos de Eimeria spp. foi de 39,7% (370/930). De um total de 10 espécies identificadas, Eimeria canadensis foi a mais observada, seguida de Eimeria bovis e Eimeria zuernii. A análise estatística indicou uma associação entre a idade dos bezerros (5 a 9 meses), a presença de outros animais, as regiões fisiográficas e o tipo restrito de criação com a presença de Eimeria spp. em bezerros (P<0,05). Os fatores de risco protetores, tais como a análise coprológica de rotina, foram também associados a uma diminuição da infecção. Esses dados indicaram a presença de coccídios em bovinos do estado de Veracruz, além das medidas necessárias que devem ser tomadas para controlar essa parasitose.

Palavras-chave:
Bovinos; Eimeria spp.; prevalência; fatores de risco; Veracruz

Introduction

Bovine coccidiosis is a gastrointestinal disease associated with apicomplexans of the genus Eimeria, where at least 21 species have been reported in cattle around the world (Lee et al., 2018Lee SH, Kim HY, Lee H, Kim JW, Lee YR, Chae MJ, et al. Eimeria species in cattle with diarrhoea in the Republic of Korea regarding age, season, and nature of diarrhoea. Vet Rec 2018; 183(16): 504. http://dx.doi.org/10.1136/vr.104600. PMid:30242082.
http://dx.doi.org/10.1136/vr.104600...
). Coccidiosis is one of the most economically important among diseases in the livestock industry that causes both clinical and subclinical losses, especially in young cattle (Lopez-Osorio et al., 2018). Clinical infection may result in diarrhea, anorexia, weakness, dehydration, and occasional deaths (Tomczuk et al., 2015Tomczuk K, Grzybek M, Szczepaniak K, Studzińska M, Demkowska-Kutrzepa M, Roczeń-Karczmarz M, et al. Analysis of intrinsic and extrinsic factors influencing the dynamics of bovine Eimeria spp. from central-eastern Poland. Vet Parasitol 2015; 214(1-2): 22-28. http://dx.doi.org/10.1016/j.vetpar.2015.09.027. PMid:26455571.
http://dx.doi.org/10.1016/j.vetpar.2015....
); whereas subclinical diseases are defined by weight loss, reduced weight gain, and loss of appetite, resulting in potentially long-lasting effects (Fitzgerald, 1980Fitzgerald PR. The economic impact of coccidiosis in domestic animals. Adv Vet Sci Comp Med 1980; 24: 121-143. PMid:7006338.). Subclinical cases are more common and are proposed to quietly disrupt intestinal physiology, thereby resulting in high feed conversion (Ekawasti et al., 2022Ekawasti F, Nashrulloh MF, Nurcahyo RW, Priyowidodo D, Prastowo J, Firdausy LW. Development of nested duplex PCR assays for detection of pathogen Eimeria species in cattle in Papua, Indonesia. IOP Conf Ser Environ Earth Sci 2022; 976: 0120008. http://dx.doi.org/10.1088/1755-1315/976/1/012008
http://dx.doi.org/10.1088/1755-1315/976/...
). The control of coccidiosis in the herd consists of reducing the parasitic load by improving the hygienic measures of the cattle habitat, as well as stress management and colostrum feeding, among other activities (Bangoura & Bardsley, 2020Bangoura B, Bardsley KD. Ruminant Coccidiosis. Vet Clin North Am Food Anim Pract 2020; 36(1): 187-203. http://dx.doi.org/10.1016/j.cvfa.2019.12.006. PMid:32029184.
http://dx.doi.org/10.1016/j.cvfa.2019.12...
); and/or the use of chemical drugs to inhibit the life cycle as well as eliminate the etiological agents responsible for the disease (Philippe et al., 2014Philippe P, Alzieu JP, Taylor MA, Dorchies P. Comparative efficacy of diclazuril (Vecoxan®) and toltrazuril (Baycox bovis®) against natural infections of Eimeria bovis and Eimeria zuernii in French calves. Vet Parasitol 2014; 206(3-4): 129-137. http://dx.doi.org/10.1016/j.vetpar.2014.10.003. PMid:25458561.
http://dx.doi.org/10.1016/j.vetpar.2014....
).

The presence of coccidiosis on farms and in individual animals can be influenced by a wide group of intrinsic and extrinsic factors (Tomczuk et al., 2015Tomczuk K, Grzybek M, Szczepaniak K, Studzińska M, Demkowska-Kutrzepa M, Roczeń-Karczmarz M, et al. Analysis of intrinsic and extrinsic factors influencing the dynamics of bovine Eimeria spp. from central-eastern Poland. Vet Parasitol 2015; 214(1-2): 22-28. http://dx.doi.org/10.1016/j.vetpar.2015.09.027. PMid:26455571.
http://dx.doi.org/10.1016/j.vetpar.2015....
). Perhaps the risk factor most associated with coccidiosis in cattle has been the age of the host. Young animals (less than 1 year old) are more susceptible to coccidiosis, as well as the presence of animals of different ages that are housed in the same place (Hermosilla et al., 2012Hermosilla 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...
). Alcala-Canto et al. (2020)Alcala-Canto Y, Figueroa-Castillo JA, Ibarra-Velarde F, Vera-Montenegro Y, Cervantes-Valencia ME, Alberti-Navarro A. First database of the spatial distribution of Eimeria species of cattle, sheep and goats in Mexico. Parasitol Res 2020; 119(3): 1057-1074. http://dx.doi.org/10.1007/s00436-019-06548-8. PMid:31901110.
http://dx.doi.org/10.1007/s00436-019-065...
mentioned that macroenvironmental variables such as temperature and rainfall influence the presence of Eimeria spp. in cattle and, for some species, different factors such as: rearing system, type of installation, farm size, seasonality and altitude affect the occurrence of coccidiosis. The presence of Eimeria spp. is attributed to subtropical zones with humid - sub-humid climates, the size of the UPB, as well as the feeding type of the animals. Although in Mexico, the State of Veracruz has climatic and management factors that favor the occurrence of Eimeria spp. in cattle, studies at farm level are scarce (INEGI, 2018Instituto Nacional de Estadística y Geografía – INEGI. Aspectos geográficos [online]. 2018 [cited 2019 Apr 10]. Available from: https://www.inegi.org.mx/contenidos/app/areasgeograficas/resumen/resumen_30.pdf
https://www.inegi.org.mx/contenidos/app/...
). The presence of coccidiosis in livestock production units in Mexico represents economic losses of up to $23.7 million dollars per year (Rodríguez-Vivas et al., 2017Rodríguez-Vivas RI, Grisi L, Pérez de León AA, Villela HS, Torres-Acosta JFJ, Fragoso-Sánchez H, et al. Potential economic impact assessment for cattle parasites in Mexico: review. Rev Mex Cienc Pecu 2017; 8(1): 61-74. http://dx.doi.org/10.22319/rmcp.v8i1.4305.
http://dx.doi.org/10.22319/rmcp.v8i1.430...
).

Epidemiological information on the presence of Eimeria spp. in tropical livestock farms is a basic step in building an efficient coccidiosis control program and improving health and well-being. Likewise, updated information is necessary on the species of Eimeria that are circulating in Veracruz. Therefore, the objectives of the present study were: (1) to determine the prevalence of Eimeria spp. oocysts in calves from 26 Municipalities in the central zone of the State of Veracruz, Mexico, (2) to identify Eimeria spp. infecting calves, and (3) to identify the risk factors associated with their presence.

Material and Methods

Ethical considerations

The work was approved by the Bioethics Committee of Faculty of Veterinary Medicine and Zootechnics, University of Veracruz, under the protocol n. 007/21.

Study area and sample size

A cross-sectional study was carried out on 62 production units through 26 Municipalities of the physiographic region of Sotavento, Las Montañas, Papaloapan, Capital and Nautla (from August 2020 to April 2021). These areas belong to the central region of the State of Veracruz, where there is a humid tropical climate with an average annual temperature of 23.4 ± 0.5, an annual rainfall of 1,991 ± 392 mm, and a mean relative humidity (RH) of 85% (INEGI, 2018Instituto Nacional de Estadística y Geografía – INEGI. Aspectos geográficos [online]. 2018 [cited 2019 Apr 10]. Available from: https://www.inegi.org.mx/contenidos/app/areasgeograficas/resumen/resumen_30.pdf
https://www.inegi.org.mx/contenidos/app/...
).

The sample size (n = 367) was calculated using an expected prevalence of Eimeria spp. of 60% (Alcala-Canto et al., 2020Alcala-Canto Y, Figueroa-Castillo JA, Ibarra-Velarde F, Vera-Montenegro Y, Cervantes-Valencia ME, Alberti-Navarro A. First database of the spatial distribution of Eimeria species of cattle, sheep and goats in Mexico. Parasitol Res 2020; 119(3): 1057-1074. http://dx.doi.org/10.1007/s00436-019-06548-8. PMid:31901110.
http://dx.doi.org/10.1007/s00436-019-065...
), an animal census of 91,589 calves (México, 2018México. Gobierno. Padrón Ganadero Nacional, registro integral del sector pecuario [online]. 2018 [cited 2019 Apr 10]. Available from: https://www.gob.mx/agricultura/es/articulos/padron-nacional-ganadero-registro-integral-del-sector-pecuario-149328
https://www.gob.mx/agricultura/es/articu...
), a confidence level of 95% and statistical error of five (Thrusfield, 1995Thrusfield M. Veterinary epidemiology. 2nd ed. Oxford: Blackwell Publishing; 1995.). The selection of cattle farms and animals were for convenience (Thrusfield, 1995Thrusfield M. Veterinary epidemiology. 2nd ed. Oxford: Blackwell Publishing; 1995.). Due to a greater participation of cattle producers in the study, as well as a greater number of animals within each cattle production unit, the sample size (n) increased to 930 calves.

Animals and sample collection

For each livestock farm, young animals and calves were selected and assigned to three age groups: ≥1 – 4, 5 – 9 and 10 – 13 months (with or without the presence of clinical signs of coccidiosis). Calves dewormed 15 days before the sample collection were excluded from the study.

At least five grams of feces were collected directly from the rectum of each calve in order to perform the parasitological tests mentioned below. The feces were identified by number or name, age, and sex and transported in a plastic cooler (4–5C) to the Parasitology Laboratory of the University of Veracruz, where they were kept in refrigeration at 4º C for 24 hours before analysis.

Laboratory analysis

The fecal oocyst count per gram of feces (OoPG) was determined using McMaster technique according to Taylor et al. (2016)Taylor MA, Coop RL, Wall RL. Veterinary parasitology. 3rd ed. Oxford: Blackwell Publishing; 2016.. Positive samples ≥ 500 OoPG were subjected to a sporulation process, using 2.5% potassium dichromate in Petri plates and incubated at room temperature, followed by oxygenation of the samples every 24 hours for ten days (Cruvinel et al., 2018Cruvinel LB, Nicaretta JE, Bastos TSA, Couto LFM, Santos JBD, Zapa DMB, et al. Eimeria species in dairy and beef cattle of different ages in Goiás state, Brazil. Rev Bras Parasitol Vet 2018; 27(2): 169-176. http://dx.doi.org/10.1590/s1984-296120180038. PMid:29924143.
http://dx.doi.org/10.1590/s1984-29612018...
). The oocysts were isolated by flotation in sugar solution (specific gravity 1.27) (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...
), and approximately 10 oocyst per pool from each farm were identified under an optical microscope using a Velab VE-87 (Puebla, Mexico) x 1000 magnification. This identification was done according to the phenotypic characteristics of the sporulated oocysts according to Taylor et al. (2016)Taylor MA, Coop RL, Wall RL. Veterinary parasitology. 3rd ed. Oxford: Blackwell Publishing; 2016. (Table 1).

Table 1
Description of the sporulated oocyst Eimeria species in cattle from the central zone of Veracruz.

Questionnaire of the Bovine Production Unit

A survey was applied to the managers of the Bovine Production Unit, which contained dichotomous and multiple-choice answers, to obtain information by animal and management practice in the unit. Table 2 shows the variables studied for the analysis of risk factors.

Table 2
Variables considered as possible risk factors for the presence of coccidiosis in calves from the central zone of Veracruz.

Statistical analysis

Prevalence of cattle parasitized with Eimeria spp. was calculated using the following Formula 1:

P r e v a l e n c e = N o . o f a n i m a l s w i t h c o c c i d i o s i s / t o t a l n u m b e r o f s a m p l e d a n i m a l s (1)

Associations between independent and dependent variables were, first, analyzed using univariate analysis with Chi-square (χ2) test with Fisher correction. Posteriorly, all the variables with a significance value of (p) ≤ 0.20 with χ2 test, were entered in a logistic regression model (Stata program Version 14.0, Texas, USA), which provides exact regression estimates, 95% confidence intervals (CI 95%), odd ratios (OR: a measure of association which quantifies the relationship between exposure variables and outcomes), p-values (P), standard error (SE) and a beta value (regression coefficient).

Results

Prevalence of Eimeria spp.

The overall prevalence of calves with coccidiosis in the central zone of the state of Veracruz was 39.7% (370 / 930; CI95% 36.6 - 42.9). This study revealed a higher prevalence of coccidiosis in the physiographic region of Nautla and Capital with 48.8% and 41.3% (42/87, CI95% 38.0-58.6;104/251 CI95%35.5-47.6), respectively; followed by female gender with 39.9% (237/578; CI95% 36.0-44.0) and the presence of diarrhea with 43.0% (96/223; CI95% 36.7 -49.6).

Eimeria species infecting calves

A total of 10 species of Eimeria were identified: Eimeria canadensis, Eimeria bovis, Eimeria cylindrica, Eimeria auburnensis, Eimeria zuernii, Eimeria ellipsoidalis, Eimeria wyomingensis, Eimeria alabamensis, Eimeria bukidnonensis and Eimeria subspherical. Eimeria canadensis was the most observed (25.9%) followed by E. bovis (24.2%) and E. zuernii (15.7%) (Table 3). Images on sporulated Eimeria spp. oocysts are presented in Figure 1. The image of E. bukidnonensis was not displayed due to technical problems; but it was identified through the size and characteristics according to Taylor et al. (2016)Taylor MA, Coop RL, Wall RL. Veterinary parasitology. 3rd ed. Oxford: Blackwell Publishing; 2016..

Table 3
Frequency and morphological measurements of Eimeria spp. identified in the central zone of Veracruz, Mexico.
Figure 1
Images from optical microscope of sporulated Eimeria species oocyst observed (x 1000 magnification) (A) E. bovis, (B) E. zuernii, (C) E. canadensis, (D) E. cylindrica, (E) E. alabamensis, (F) E. wyomingensis, (G) E. auburnensis, (H) E. ellipsoidalis and (I) E. subspherica.

Risk factors

Table 4 shows the univariate analysis of the presence of Eimeria spp. with the type of variable responses. Risk factors that showed greater association with the occurrence of Eimeria spp. in calves were the physiographic region, the age, the presence of other animal species and the type of calf rearing (P<0.05; Table 5). Calves from the region of Nautla had 1.55 greater probability of being infected with Eimeria (OR1.55; CI95% 1.07-2.26) compared with the Papaloapan region. The 5 - 9-month-old group had a higher number of oocysts compared to 10–13-month-old calves (OR 1.49 (CI95% 1.08-2.04; P=0.013). Furthermore, the presence of other animal species [OR of 1.86 (CI95% 1.31-2.55)] and calves with restricted suckling [OR of 2.31 (CI95% 1.37-2.39)] had higher probabilities of being infected with Eimeria spp. These data are summarized in Table 5.

Table 4
Univariate analysis results (x2) for the identification of possible risk factors associated with calves parasitized with Eimeria spp. in the central zone of Veracruz, México.
Table 5
Logistic regression analysis to identify risk factors associated with calves parasitized with Eimeria spp. in the central zone of Veracruz, Mexico.

Protective factors

In this study, we determine that the physiographic region of Papaloapan and the performance of coprological studies in the animal unit should be considered as protective factors, since they obtained OR values of 0.50 (CI95% 0.26-0.99) and 0.29(CI95% 0.19-0.45), respectively.

Discussion

The first objective of the present study was to determine the prevalence of Eimeria spp. oocysts in calves from 26 Municipalities in the center area of the State of Veracruz, México. The overall prevalence of calves with coccidiosis was 39.7%. These results were consistent with the previous ones acquired by Quiroz & Casillas (1971)Quiroz H, Casillas LA. Coccidias de ganado bovino identificadas en México. Tec Pecu Mex [online] 1971 [cited 2019 Apr 10]; 17: 19-22. Available from: https://cienciaspecuarias.inifap.gob.mx/index.php/Pecuarias/article/download/1931/3579
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concerning the prevalence of 38% of the parasite in the south of Veracruz. The State of Veracruz has the ideal conditions that facilitated the presence of Eimeria spp. such as: the climate, physiography, and tropical areas, which are considered the best means for the parasite to survive and reproduce (Lucas et al., 2014Lucas AS, Swecker WS Jr, Lindsay DS, Scaglia G, Neel JPS, Elvinger FC, et al. A study of the level and dynamics of Eimeria populations in naturally infected, grazing beef cattle at various stages of production in the Mid-Atlantic USA. Vet Parasitol 2014; 202(3-4): 201-206. http://dx.doi.org/10.1016/j.vetpar.2014.02.053. PMid:24680603.
http://dx.doi.org/10.1016/j.vetpar.2014....
). This State has tropical and subtropical climates, which facilitate the survival of Eimeria spp. in the yards of young animals (INEGI, 2018Instituto Nacional de Estadística y Geografía – INEGI. Aspectos geográficos [online]. 2018 [cited 2019 Apr 10]. Available from: https://www.inegi.org.mx/contenidos/app/areasgeograficas/resumen/resumen_30.pdf
https://www.inegi.org.mx/contenidos/app/...
). However, the prevalence shown in this analysis is below compared with other studies made in México with cattle (60.2%) (Alcala-Canto et al., 2020Alcala-Canto Y, Figueroa-Castillo JA, Ibarra-Velarde F, Vera-Montenegro Y, Cervantes-Valencia ME, Alberti-Navarro A. First database of the spatial distribution of Eimeria species of cattle, sheep and goats in Mexico. Parasitol Res 2020; 119(3): 1057-1074. http://dx.doi.org/10.1007/s00436-019-06548-8. PMid:31901110.
http://dx.doi.org/10.1007/s00436-019-065...
) and other countries such as Brazil (66%) (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...
), Indonesia (65.4%), (Ekawasti et al., 2022Ekawasti F, Nashrulloh MF, Nurcahyo RW, Priyowidodo D, Prastowo J, Firdausy LW. Development of nested duplex PCR assays for detection of pathogen Eimeria species in cattle in Papua, Indonesia. IOP Conf Ser Environ Earth Sci 2022; 976: 0120008. http://dx.doi.org/10.1088/1755-1315/976/1/012008
http://dx.doi.org/10.1088/1755-1315/976/...
), Iran (63%) (Adinehbeigi et al., 2018Adinehbeigi K, Khedri J, Rahmani K, Moghaddam AA, Hashemi H. Determination and diversity of bovine coccidia in Zabol, east of Iran. Arch Razi Inst 2018; 73(1): 45-53. PMid:30256038.) and Colombia (75.6%) (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.
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). This variation is most likely attributed to the differences in study design, biotic and abiotic factors and husbandry practices of the study animals in different countries (Tamrat et al., 2020Tamrat H, Mekonnen N, Ferede Y, Cassini R, Belayneh N. Epidemiological study on calf diarrhea and coccidiosis in dairy farms in Bahir Dar, North West Ethiopia. Ir Vet J 2020; 73(1): 14. http://dx.doi.org/10.1186/s13620-020-00168-w. PMid:32704347.
http://dx.doi.org/10.1186/s13620-020-001...
), a high animal density, accumulation of organic material and mix of animals of different ages (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...
). On the other hand, in this study, a high prevalence was observed in the physiographic region of “Nautla” with 48.8%. Nautla represents 3.2% of the cattle volume in the state of Veracruz. It has 12 regions with hydrological basins where a warm humid climate prevails with rains all year round. In addition, it has an annual rainfall of 1,383.00 and a maximum temperature of 40o C. The Eimeria spp. shows a significant association with humid and sub-humid areas and high temperatures, in addition to high rainfall that allows the development and abundance of the parasite (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...
).

Bovine coccidiosis is a gastrointestinal disease associated with apicomplexans of the genus Eimeria, where at least 21 species have been reported in cattle around the world (Lee et al., 2018Lee SH, Kim HY, Lee H, Kim JW, Lee YR, Chae MJ, et al. Eimeria species in cattle with diarrhoea in the Republic of Korea regarding age, season, and nature of diarrhoea. Vet Rec 2018; 183(16): 504. http://dx.doi.org/10.1136/vr.104600. PMid:30242082.
http://dx.doi.org/10.1136/vr.104600...
). The second objective of this study was to be observed Eimeria spp. natural infecting calves. From a total of 10 species of Eimeria were identified, E. canadensis was the most observed followed by E. bovis and E. zuernii. Of the 12 Eimeria spp. previously reported for Mexico by Alcala-Canto et al. (2020)Alcala-Canto Y, Figueroa-Castillo JA, Ibarra-Velarde F, Vera-Montenegro Y, Cervantes-Valencia ME, Alberti-Navarro A. First database of the spatial distribution of Eimeria species of cattle, sheep and goats in Mexico. Parasitol Res 2020; 119(3): 1057-1074. http://dx.doi.org/10.1007/s00436-019-06548-8. PMid:31901110.
http://dx.doi.org/10.1007/s00436-019-065...
, E. cylindrica and E. ellipsoidalis were the most observed in cattle. However, in the same spatial distribution of Eimeria species of cattle in Mexico, E. canadensis was the most encountered species with a frequency of 77.58% in temperate humid climates, but also had a high prevalence in warm semi humid and humid climates with 68.13% and 67.08%, respectively. The presence of E. canadensis does not cause significant damage to the intestine of the infected animals, since this species is not considered pathogenic within the pathogenicity classification (Bangoura & Bardsley, 2020Bangoura B, Bardsley KD. Ruminant Coccidiosis. Vet Clin North Am Food Anim Pract 2020; 36(1): 187-203. http://dx.doi.org/10.1016/j.cvfa.2019.12.006. PMid:32029184.
http://dx.doi.org/10.1016/j.cvfa.2019.12...
), however, their high frequency in this study deserves future epidemiological and clinical studies throughout the year. It is mentioned that economical losses due to subclinical disease even are higher than clinical coccidiosis (Fitzgerald, 1980Fitzgerald PR. The economic impact of coccidiosis in domestic animals. Adv Vet Sci Comp Med 1980; 24: 121-143. PMid:7006338.) because it is more common and can affect the productive and reproductive parameters in cattle (Larsson et al., 2006Larsson A, Dimander SO, Uggla A, Waller P, Höglund J. Effects of single or concurrent infections with Eimeria alabamensis and gastrointestinal nematodes on the performance of calves on pasture. Parasitol Res 2006; 99(1): 84-89. http://dx.doi.org/10.1007/s00436-005-0109-4. PMid:16496174.
http://dx.doi.org/10.1007/s00436-005-010...
).

In our study, E. bovis and E. zuernii were detected with an important frequency of 24.2% and 15.7%, respectively. This finding agrees with Quiroz & Casillas (1971)Quiroz H, Casillas LA. Coccidias de ganado bovino identificadas en México. Tec Pecu Mex [online] 1971 [cited 2019 Apr 10]; 17: 19-22. Available from: https://cienciaspecuarias.inifap.gob.mx/index.php/Pecuarias/article/download/1931/3579
https://cienciaspecuarias.inifap.gob.mx/...
who described E. bovis as the most frequent in cattle. These results are also consistent with several authors reporting the species E. bovis and E. zuernii identified more frequently in the fecal samples analyzed (Bruhn et al., 2012Bruhn FR, Silva FA Jr, Carvalho AH, Orlando DR, Rocha CMBM, Guimarães AM. Occurrences of Eimeria spp. and gastrointestinal nematodes in dairy calves in southern Minas Gerais, Brazil. Rev Bras Parasitol 2012; 21(2): 171-175. http://dx.doi.org/10.1590/S1984-29612012000200019. PMid:22832761.
http://dx.doi.org/10.1590/S1984-29612012...
; Lee et al., 2018Lee SH, Kim HY, Lee H, Kim JW, Lee YR, Chae MJ, et al. Eimeria species in cattle with diarrhoea in the Republic of Korea regarding age, season, and nature of diarrhoea. Vet Rec 2018; 183(16): 504. http://dx.doi.org/10.1136/vr.104600. PMid:30242082.
http://dx.doi.org/10.1136/vr.104600...
; Hamid et al., 2019Hamid PH, Kristianingrum YP, Prastowo S. Bovine coccidiosis cases of beef and dairy cattle in Indonesia. Vet Parasitol Reg Stud Rep 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...
; Ola-Fadunsin et al., 2020Ola-Fadunsin SD, Rabiu M, Hussain K, Sanda IM, Ganiyu IA. Epidemiological studies of Eimeria species of cattle in Ilorin, North-Central Nigeria. Ann Parasitol 2020; 66(3): 373-384. PMid:33128863.; Cruvinel et al., 2021Cruvinel LB, Ferreira LL, Nicaretta JE, Couto LFM, Zapa DMB, Cavalcante ASA, et al. Eimeria spp. in naturally infected beef cattle: dynamics of oocysts excretion, prevalence, and comparison between parasitological diagnostics. Prev Vet Med 2021; 194: 105447. http://dx.doi.org/10.1016/j.prevetmed.2021.105447. PMid:34333412.
http://dx.doi.org/10.1016/j.prevetmed.20...
). Although mixed infections are commonly observed under natural conditions, only two highly pathogenic species E. zuernii and E. bovis are generally involved in the highest number of clinical cases in calves and can cause moderate to severe enteritis (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...
). These animals have abdominal pain, fever, anemia, dehydration, weakness, anorexia (Li et al., 2021Li DL, Gong QL, Ge GY, Wang Q, Sheng CY, Ma BY, et al. Prevalence and infection risk factors of bovine Eimeria in China: a systematic review and meta-analysis. Parasite 2021; 28: 61. http://dx.doi.org/10.1051/parasite/2021055. PMid:34374643.
http://dx.doi.org/10.1051/parasite/20210...
) and tenesmus (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...
). Authors also reports that mortality might reach 7-20% (Pilarczyk et al., 1999Pilarczyk B, Bablicka R, Prost M. The dynamics of Eimeria spp. infection in calves treated and untreated with Baycox®. Med Weter [online] 1999 [cited 2019 Apr 10]; 55(8): 523-526. Available from: https://eurekamag.com/research/003/300/003300389.php
https://eurekamag.com/research/003/300/0...
). Eimeria bovis is one of the main species that produce clinical signals in animals, among which are weight loss, damage to the intestinal endothelium and intermittent hemorrhagic diarrhea (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...
). In the case of E. bovis and E. zuernii predominate in animals from 4 and 3 months of age (Cruvinel et al., 2018Cruvinel LB, Nicaretta JE, Bastos TSA, Couto LFM, Santos JBD, Zapa DMB, et al. Eimeria species in dairy and beef cattle of different ages in Goiás state, Brazil. Rev Bras Parasitol Vet 2018; 27(2): 169-176. http://dx.doi.org/10.1590/s1984-296120180038. PMid:29924143.
http://dx.doi.org/10.1590/s1984-29612018...
). However, the presence of mixed infections of E. zuernii and E. bovis has been observed in different ages of animals (Bangoura et al., 2012Bangoura 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 2012; 110(2): 875-881. http://dx.doi.org/10.1007/s00436-011-2569-z. PMid:21808979.
http://dx.doi.org/10.1007/s00436-011-256...
). This implies that it is not only to observe the presence of Coccidia in the feces, but also to make an identification by species to establish control measures to reduce economic losses in the UPB.

The identification of species and genus through morphological characteristics is controversial because can be subjective and ambiguous between intraspecies variations (Kawahara et al., 2010Kawahara F, Zhang G, Mingala CN, Tamura Y, Koiwa M, Onuma M, et al. Genetic analysis and development of species-specific PCR assays based on ITS-1 region of rRNA in bovine Eimeria parasites. Vet Parasitol 2010; 174(1-2): 49-57. http://dx.doi.org/10.1016/j.vetpar.2010.08.001. PMid:20817404.
http://dx.doi.org/10.1016/j.vetpar.2010....
; 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...
). It is mentioned that the size, color and surface of the wall can vary in the ocysts of a given species (Dubey, 2019Dubey JP. Coccidiosis in livestock, poultry, companion animals, and humans. Boca Raton: CRC Press; 2019. http://dx.doi.org/10.1201/9780429294105.
http://dx.doi.org/10.1201/9780429294105...
); therefore, the morphological study is not conclusive and further confirmation by molecular techniques such as PCR is recommended. The presence of specific primers allows molecular identification to be a rapid technique for the diagnosis of pathogenic Eimeria spp. (Kawahara et al., 2010Kawahara F, Zhang G, Mingala CN, Tamura Y, Koiwa M, Onuma M, et al. Genetic analysis and development of species-specific PCR assays based on ITS-1 region of rRNA in bovine Eimeria parasites. Vet Parasitol 2010; 174(1-2): 49-57. http://dx.doi.org/10.1016/j.vetpar.2010.08.001. PMid:20817404.
http://dx.doi.org/10.1016/j.vetpar.2010....
). The classification through six specific primers for the pathogenic Eimeria species by PCR has been reported (Kawahara et al., 2010Kawahara F, Zhang G, Mingala CN, Tamura Y, Koiwa M, Onuma M, et al. Genetic analysis and development of species-specific PCR assays based on ITS-1 region of rRNA in bovine Eimeria parasites. Vet Parasitol 2010; 174(1-2): 49-57. http://dx.doi.org/10.1016/j.vetpar.2010.08.001. PMid:20817404.
http://dx.doi.org/10.1016/j.vetpar.2010....
; Al-Jubory & Al-Rubaie, 2016Al-Jubory QJA, Al-Rubaie HMA. Molecular identification and characterization and phylogenetic study of six Eimeria species in cattle in Al-Najaf province. Euphrates J Agricult Sci 2016; 8(3): 83-96.; Lee et al., 2018Lee SH, Kim HY, Lee H, Kim JW, Lee YR, Chae MJ, et al. Eimeria species in cattle with diarrhoea in the Republic of Korea regarding age, season, and nature of diarrhoea. Vet Rec 2018; 183(16): 504. http://dx.doi.org/10.1136/vr.104600. PMid:30242082.
http://dx.doi.org/10.1136/vr.104600...
; Ekawasti et al., 2022Ekawasti F, Nashrulloh MF, Nurcahyo RW, Priyowidodo D, Prastowo J, Firdausy LW. Development of nested duplex PCR assays for detection of pathogen Eimeria species in cattle in Papua, Indonesia. IOP Conf Ser Environ Earth Sci 2022; 976: 0120008. http://dx.doi.org/10.1088/1755-1315/976/1/012008
http://dx.doi.org/10.1088/1755-1315/976/...
). Therefore, this aspect requires further research to confirm by PCR Eimeria spp. circulating at the UPB in the State of Veracruz, Mexico.

The third objective was to identify the risk factors associated with the presence of Eimeria spp. in calves. In this study, different risk factors related to intrinsic (age) and extrinsic factors (e.g., physiographic region, presence of other animal species, type of calf rearing and coprological studies) were identified in livestock production units. The 5 - 9-month-old group had a higher number of oocysts compared to 10–13-month-old calves. The prevalence of Eimeria natural infection in cattle is highly age dependent (Cornelissen et al., 1995Cornelissen AWCA, Verstegen R, van den Brand H, Perie NM, Eysker M, Lam TJGM, et al. An observational study of Eimeria species in housed cattle on Dutch dairy farms. Vet Parasitol 1995; 56(1-3): 7-16. http://dx.doi.org/10.1016/0304-4017(94)00671-X. PMid:7732653.
http://dx.doi.org/10.1016/0304-4017(94)0...
). Young animals up to 1 year of life are usually the most susceptible; also, some studies indicate that this disease is manifested in animals less than 18 months, on average (Makau et al., 2017Makau DN, Gitau GK, Muchemi GK, Thomas LF, Cook EA, Wardrop NA, et al. Environmental predictors of bovine Eimeria infection in western Kenya. Trop Anim Health Prod 2017; 49(2): 409-416. http://dx.doi.org/10.1007/s11250-016-1209-0. PMid:28054227.
http://dx.doi.org/10.1007/s11250-016-120...
). As a result, when they grow into adults, they usually become asymptomatic hosts after recurrent reinfections, serving as a source of infection for younger animals (Matjila & Penzhorn, 2002Matjila PT, Penzhorn BL. Occurrence and diversity of bovine coccidia at three localities in South Africa. Vet Parasitol 2002; 104(2): 93-102. http://dx.doi.org/10.1016/S0304-4017(01)00605-7. PMid:11809329.
http://dx.doi.org/10.1016/S0304-4017(01)...
). 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 that the most susceptible age to Eimeria spp. was between 3 and 6 months, concurring with our findings, where risk was observed in calves between 5 and 9 months of age. The logistic regression analysis revealed an OR of 1.49 (CI95% 1.08-2.54; P = 0.01), associated with a possible lack of immune response or low immunity (Yun et al., 2000Yun CH, Lillehoj HS, Lillehoj EP. Intestinal immune responses to coccidiosis. Dev Comp Immunol 2000; 24(2-3): 303-324. http://dx.doi.org/10.1016/S0145-305X(99)00080-4. PMid:10717295.
http://dx.doi.org/10.1016/S0145-305X(99)...
). Therefore, there is a concordance with what has been observed by other authors regarding this factor (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...
; Almeida et al., 2011Almeida VA, Magalhães VCS, Neta ESM, Munhoz AD. Frequency of species of the genus Eimeria in naturally infected cattle in Southern Bahia, Northeast Brazil. Rev Bras Parasitol Vet 2011; 20(1): 78-81. http://dx.doi.org/10.1590/S1984-29612011000100017. PMid:21439239.
http://dx.doi.org/10.1590/S1984-29612011...
; Rehman et al., 2011Rehman TU, Khan MN, Sajid MS, Abbas RZ, Arshad M, Iqbal Z, et al. Epidemiology of Eimeria and associated risk factors in cattle of district Toba Tek Singh, Pakistan. Parasitol Res 2011; 108(5): 1171-1177. http://dx.doi.org/10.1007/s00436-010-2159-5. PMid:21110042.
http://dx.doi.org/10.1007/s00436-010-215...
; Tomczuk et al., 2015Tomczuk K, Grzybek M, Szczepaniak K, Studzińska M, Demkowska-Kutrzepa M, Roczeń-Karczmarz M, et al. Analysis of intrinsic and extrinsic factors influencing the dynamics of bovine Eimeria spp. from central-eastern Poland. Vet Parasitol 2015; 214(1-2): 22-28. http://dx.doi.org/10.1016/j.vetpar.2015.09.027. PMid:26455571.
http://dx.doi.org/10.1016/j.vetpar.2015....
). It should be mentioned that although calves obtain immunoglobulins from the colostrum, these are not enough to prevent an infection of the apicomplexans (Faber et al., 2002Faber JE, Kollmann D, Heise A, Bauer C, Failing K, Bürger HJ, et al. Eimeria infections in cows in the periparturient phase and their calves: oocyst excretion and levels of specific serum and colostrum antibodies. Vet Parasitol 2002; 104(1): 1-17. http://dx.doi.org/10.1016/S0304-4017(01)00610-0. PMid:11779651.
http://dx.doi.org/10.1016/S0304-4017(01)...
).

Additionally, the presence of other animal species in the bovine production unit was considered a potential risk factor with an OR of 1.86 (CI95% 1.31-2.65; P= 0.001) since they facilitate the accumulation of organic matter. 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 Rehman et al. (2011)Rehman TU, Khan MN, Sajid MS, Abbas RZ, Arshad M, Iqbal Z, et al. Epidemiology of Eimeria and associated risk factors in cattle of district Toba Tek Singh, Pakistan. Parasitol Res 2011; 108(5): 1171-1177. http://dx.doi.org/10.1007/s00436-010-2159-5. PMid:21110042.
http://dx.doi.org/10.1007/s00436-010-215...
suggest that the lack of cleaning and sanitation, followed by poor sanitation, optimal humidity, concentration of organic matter and temperature are important factors for oocyst sporulation and survival in contaminated soils. Furthermore, the restricted calf suckling was also considered as a risk factor with an OR of 2.31 (CI95% 1.37-3.89 and P=0.002). In this research, the type of rearing is defined by the way the calves consume the milk, either artificially or directly from the mother (restricted or continuous). Tomczuk et al. (2015)Tomczuk K, Grzybek M, Szczepaniak K, Studzińska M, Demkowska-Kutrzepa M, Roczeń-Karczmarz M, et al. Analysis of intrinsic and extrinsic factors influencing the dynamics of bovine Eimeria spp. from central-eastern Poland. Vet Parasitol 2015; 214(1-2): 22-28. http://dx.doi.org/10.1016/j.vetpar.2015.09.027. PMid:26455571.
http://dx.doi.org/10.1016/j.vetpar.2015....
described the highest extent of invasions in those farms where calves were raised with their mothers. Mother ewes have also been found to be the main source of infection for lambs cohabiting with them. Therefore, there is a strong association between possible infected mothers and calves with low immunity who are susceptible to the parasite infection. On the other hand, low Eimeria spp. infections were observed in animals that undergo routine coprological studies for the control and treatment of parasites in livestock management. These results agree with the findings of Philippe et al. (2014)Philippe P, Alzieu JP, Taylor MA, Dorchies P. Comparative efficacy of diclazuril (Vecoxan®) and toltrazuril (Baycox bovis®) against natural infections of Eimeria bovis and Eimeria zuernii in French calves. Vet Parasitol 2014; 206(3-4): 129-137. http://dx.doi.org/10.1016/j.vetpar.2014.10.003. PMid:25458561.
http://dx.doi.org/10.1016/j.vetpar.2014....
who demonstrated that metaphylactic treatment with diclazuril and toltrazuril reduce the impact of coccidiosis by previously identifying the specific parasite to attack. The Papalopan region had an OR of 0.50 (CI95% 0.26-0.99; P=0.05), suggesting a decrease of the parasite with this variable. The three Municipalities that belong to this physiographic region have dry seasons from September to May approximately, which coincides with the months in which the samples were collected. For an oocyst to be infectious, it must sporulate and mature. An adequate amount of oxygen and moisture is required for oocyst sporulation to occur. If there are periods of drought with constant high temperatures and a decrease in relative humidity, the cycle is interrupted, so the oocyst dies and ceases to be an infectious agent for the calf (Rodríguez-Hawkins, 2011Rodríguez-Hawkins AR. Determinación de los factores de riesgo en la presentación de Eimeria ssp. en crias de alpacas en el centro de investigación y producción (cip) la raya-Puno [thesis]. Lima, Perú: Universidad Nacional Mayor de San Marcos; 2011.).

Conclusion

This work revealed the diversity of Eimeria species in calves in central region of Veracruz, Mexico. The risk of infection was observed in intrinsic and extrinsic factors, such as age and type of calf rearing. This study will help to implement adequate antiparasitic therapies and management strategies for Eimeria spp. infection control, but it also highlights the need to monitor Eimeria species considered non-pathogenic in UPBs over time.

Acknowledgements

We are grateful for the participation of the Torreon del Molino parasitology laboratory team, the Universidad Veracruzana, the Centro de Enseñanza, Investigación y Extensión en Ganadería Tropical and the managers of the production units that allowed us to use their facilities during the pandemic.

  • How to cite: Olivares-Muñoz A, Alonso-Díaz MA, Romero-Salas D, Cruz-Romero A, Barrientos-Morales M, Pinos-Rodríguez JM. Prevalence and risk factors of coccidiosis in calves from Veracruz, México. Rev Bras Parasitol Vet 2022; 31(3): e005622. https://doi.org/10.1590/S1984-29612022043

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Publication Dates

  • Publication in this collection
    08 Aug 2022
  • Date of issue
    2022

History

  • Received
    21 Apr 2022
  • Accepted
    14 July 2022
Colégio Brasileiro de Parasitologia Veterinária FCAV/UNESP - Departamento de Patologia Veterinária, Via de acesso Prof. Paulo Donato Castellane s/n, Zona Rural, , 14884-900 Jaboticabal - SP, Brasil, Fone: (16) 3209-7100 RAMAL 7934 - Jaboticabal - SP - Brazil
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