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Abanico veterinario

On-line version ISSN 2448-6132Print version ISSN 2007-428X

Abanico vet vol.9  Tepic  2019  Epub Mar 05, 2021

https://doi.org/10.21929/abavet2019.919 

Original article

Frequency of gastrointestinal parasites in cattle at the southern of Sonora, Mexico

Javier Munguía-Xóchihua1  * 
http://orcid.org/0000-0002-8142-5021

Ivette Leal-Franco1 
http://orcid.org/0000-0001-7704-1503

José Muñoz-Cabrera1 
http://orcid.org/0000-0003-2089-5078

Manuel Medina-Chu1 
http://orcid.org/0000-0003-1155-8600

Javier Reyna-Granados1 
http://orcid.org/0000-0001-8898-7177

Pedro López-Castro1 
http://orcid.org/0000-0002-9530-4810

1Departamento de Ciencias Agronómicas y Veterinarias. Instituto Tecnológico de Sonora, 5 de febrero 818 sur. Colonia Centro CP 85000. Cd. Obregón, Sonora. México.


ABSTRACT

Commonly gastroenteric parasites are a health problem in extensive livestock and could be a risk in the productive efficiency in cattle raised at the south of Sonora, Mexico. In order to determine the frequency of the different gastrointestinal parasitic genera in bovines of the southern region of Sonora, a study was divided in high-mountain (n= 218), low-mountain (n= 173), Valley1 (n= 222) and Valley2 (n= 50) regions. The feces were collected from adult cattle and calves (5 to 6 months of age) from January to March and December 2018; January to February 2019. The samples were analyzed by flotation and MacMaster techniques. The morphology was determined obtaining the L3 stage by coproculture. The Eimerias were identified prior to sporulation. The 83.03%, 56.0% and 17.56% were positive for gastrointestinal parasites in high-mountain, low-mountain and Valley1 respectively. Valley2 was negative for nematodes, but 43% were positive for Eimerias. The cattle in the study area showed a low 17.56% to high 83.03% frequency of gastroenteric parasites with the presence of one to eight genera of nematode and one to seven of Eimeria.

Keywords: Cattle; nematodes; eimeria semiarid; mountain

RESUMEN

Comúnmente los parásitos gastroentéricos son un problema sanitario en la ganadería extensiva y pueden ser un riesgo en la eficiencia productiva del ganado al sur de Sonora, México. Para determinar la frecuencia de los diferentes géneros parasitarios gastrointestinales en bovinos de la región sur de Sonora, se dividió un estudio en región Sierra alta (n= 218), Sierra baja (n=173), Valle1 (n= 222) y Valle2 (n= 50). Las heces fueron colectadas de bovinos adultos y becerros (5 a 6 meses de edad) de enero a marzo y diciembre de 2018; enero a febrero de 2019. Las muestras se analizaron mediante las técnicas flotación y MacMaster. La morfología fue determinada al obtener la etapa L3 mediante coprocultivo. Las Eimerias fueron identificadas previa esporulación. Un 83.03%, 56.0% y 17.56% fueron positivos a parásitos gastrointestinales en Sierra alta, Sierra baja y Valle1 respectivamente. El Valle2 fue negativo a nematodos, pero el 43% resulto positivos a Eimerias. Los bovinos en la zona de estudio mostraron una frecuencia de baja 17.56% a alta 83.03% a parásitos gastroentéricos con presencia de uno a ocho géneros de nematodos y de uno a siete de Eimeria.

Palabras clave: Ganado; nematodos; eimerias; semiárido; sierra

INTRODUCTION

The production of beef cattle in Sonora is developed in more than 15 million hectares of summer pastures, 83% of the state area is used, with 1.5 million head of cattle (Denogean et al., 2013). For the farmer, the weather and ecological conditions are a restrictive element for adequate production, which depends on the potential of the forage to meet nutritional needs (Denogean et al., 2013; Retes et al., 2013). The delicate balance of nutrients and health of cattle is at constant risk by being exposed to infections by gastroenteric parasites (PGE), which significantly reduce food consumption, feed conversion and weight gain, with morbidity and mortality in animals young people (Stromberg et al., 2012).

In the abomasum, the secretory cells that affect the quantity and quality of the hydrochloric acid are damaged, which modifies the pH value up to 6.5 and the efficiency of the digestion and absorption of nutrients is reduced; affects the mineral and protein metabolism, in subclinical and chronic presentation the animals reduce their food consumption by 15 to 20%, which decreases weight gain or there is weight loss; Therefore, nutritional deficiencies are increased and livestock productivity is reduced (Torres, 2006; Biswajit et al., 2017; Oliviera et al., 2017). In some cases, acute anorexia, anemia, toxemia, tissue damage and death can be observed; usually in young animals in growth and sometimes in adults (Johanssos, 2017).

The potential economic impact of parasites in Mexico was estimated and obtained for gastroenteric nematodes US $ 445.10 and for coccidia (Eimeria spp.) US $ 23.78 million, based on the national population in 2013 of 32.4 million cattle (Rodríguez et al., 2017). Due to the detrimental effects on production and health, it is important to have information on the presence of PGE in the region.

The objective of this research was to determine the frequency and genera of gastroenteric parasites in cattle from four sectors of southern Sonora, Mexico.

MATERIAL AND METHODS

Geographic location. The study was conducted in a sector of the High-mountain and the Low-mountain, as well as two sectors of the southern Sonora Valley. In the High-mountain sector, work was carried out in the Yécora municipality, which is located 215 kilometers north of Obregón city, at an altitude of 1540 meters; The prevailing climate is mild subhumid with rains for most of the year. In February and March, the temperature reaches 24.0 °C and the annual average is 24.4 °C, with annual average precipitation of 944 mm (SMN, 2018).

In the Low-mountain sector, work was carried out in the Rosario municipality, in Tesopaco town, located at an altitude of 450 meters; it has a semi-dry or semi-warm climate, with a maximum average temperature of 29.2 °C and minimum of 14.2 °C. Rains predominate during July and August, with an annual average rainfall of 610.1 mm (SMN, 2018).

Sampling. In stockpiles of the High-mountain sector, 218 calves (140 males and 78 females) were sampled and from Low-mountain to 173 calves (130 males and 43 females); they were all cattle breeding grounds, mostly creole weaned or at the beginning of weaning, between 5 and 10 months of age, raised extensively and free grazing. The samples from the Valley 1 region were 222 samples from 8 herds of adult dairy cattle; from the Valley 2 region, there were 50 adult cattle in summer pastures. Sampling was carried out from January to March and December 2018, and from January to February 2019, to conduct an observational and cross-sectional study (Thursfield, 2018). Sampling was carried out for convenience in the collection pens and in the herds, where sampling was allowed (Scheaffer et al., 2012).

To the stool samples, the qualitative flotation and quantitative technique of MacMaster was performed to obtain eggs per gram of feces (HGH), oocysts per gram of feces (OGH); co-culture and Baerman (Yacob et al., 2009); In the latter, the larvae (L3) present were identified based on their morphological characteristics (Pinilla et al., 2018). Sporulation technique was performed to identify Eimerias (Mitchell et al., 2012). Through the Microsoft Excel 2016 program, the results shown in descriptive statistics were obtained (Wayne, 2014).

RESULTS AND DISCUSSION

In the High-mountain were: 83.03% (181/218) positive calves and 16.97% (37/218) negative to gastroenteric parasites. The gender type for nematodes was 88.95% (161/181) positive, cestodes 19.33% (35/181) and protozoa 80.11% (145/181). The MacMaster range for each genus was: 50-900 HGH nematodes, 50-6850 HGH cestodes, 50-5050 OGH protozoa.

The most frequent genera were: Haemonchus spp. 79.5%, Oesophagostomum spp. 40.37% and Trichostrongylus spp. 34.78% (table 1).

Table 1 Number and percentage of gastroenteric nematodes in cattle in four regions of southern Sonora 

Nematodos

High-mountain

Frequency

Porcentage (%)

Low-mountain

Frequency

Porcentage (%)

Valley 1

Frecuency

Porcentage (%)

Valley 2

Frecuency

Porcentage (%)
Haemonchusspp. 128 79.5 15 17.85 6 50 0 0
Oesophagostomum spp. 65 40.37 7 8.33 1 8.33 0 0
Trichostrongylus spp. 56 34.78 7 8.33 3 25 0 0
Skrjabinema spp. 40 24.84 0 0 1 8.33 0 0
Cooperia spp. 23 14.28 49 58.33 1 8.33 0 0
Strongyloides spp. 18 11.18 4 4.76 0 0 0 0
Ostertagia spp. 14 8.69 15 17.85 0 0 0 0
Toxacara spp. 1 0.62 0 0 0 0 0 0

Gastroenteric nematode infections occurred in one to eight genera, the most frequent being: single 43.47% (70/161), double 25.46% (41/161) and triple 20.49% (33/161) (table 2).

Table 2 Type of infection by gastroenteric nematodes in cattle four regions of southern Sonora 

High-mountain Porcentage Low-mountain Porcentage Valley 1 Porcentage Valley 2 Porcentage
Type of infection Frecuency (%) Frecuency (%) Frecuency (%) Frecuency (%)
Simple 70 43.47 68 80.9 2 28.5 0 0
Double 41 25.46 16 19.04 5 71.43 0 0
Triple 33 20.49 0 0 0 0 0 0
Quadruple 16 9.93 0 0 0 0 0 0
Quíntuple 1 0.62 0 0 0 0 0 0

In the Low-mountain it was found: 56% (97/173) positive calves and 43.93% (76/173) negative to the parasites under study. The distribution by gender was found for nematodes 86.6% (84/97), positive and protozoan 23.71% (23/97). The MacMaster range was: 50- 300 HGH nematodes and 50-200 OGH protozoan.

The most frequent nematodes were: Cooperia spp. 58.33%, Haemonchus spp. 17.85% and Ostertagia spp. 17.85% (table 1).

With respect to gastroenteric nematode infections, there were one to six genera, the two most frequent were: single 80.9% and double 19.04% (table 2).

In the study the areas of High-mountain and Low-mountain were positive for nematodes in calves, which is consistent with reports where the prevalence of PGE in calves is present and increases in the months close to the year of age; the highest prevalence occurs in calves from 4 to 12 months of age, and the highest frequency between 6 and 9 months (Colina et al., 2013). Another important factor to consider is the coexistence of the calves with the adult bovines, when they are carriers of PGE they contaminate the forage and the infection of the calves is favored (Encalada et al., 2009).

The management of livestock in Sonora state mountains is known as "runs", these are done once or twice a year, is the best season between the months of October to April of the following year. Adults receive reproductive and sanitary management such as deworming and vaccination; Calves are separated and most go to pre-export stockpiles. The adult cattle that remain on the farm when dewormed once, it is not enough to control the populations of PGE; these contaminate grazing areas and calves when infected are evidenced by the results of an infection intensity for PGE from low (0-500 HGH) to medium (550-1000 HGH); It causes a delay in growth, reduced productivity and reinfection of calves due to forage contamination (Encalada et al., 2009).

Regarding the genera of PGE found, it varied in each region of the mountain, which is consistent with a study conducted, which indicates that the nematodes Haemonchus spp., Mecistocirrus spp., Trichostrongylus spp., Cooperia spp., and Oesophagostomum spp, are considered important from a pathological and epidemiological point of view in various geo-ecological, temperate and warm areas (Vázquez et al., 2004). In other regions of Mexico the distribution, diversity of the frequency and genus of PGE in cattle in different states is shown, and they give the guideline of the adaptation that they have to the different ecosystems such as the subtropical and tropical (Quiroz, 2011; Fernández et al., 2015; Figueroa et al., 2018; Pinilla et al., 2018). The results of the two regions of the mountains show an important advance in the knowledge of the frequency and identification of PGE, in calves in southern Sonora.

In the Valley 1 region, 17.56% (39/222) positive and 82.43% (183/222) negative for gastroenteric parasites were found. Regarding the type of gender for nematodes 17.94% (7/39) and protozoa 82.05% (32/39) positive, respectively. The MacMaster range for each parasitic genus was: 50-1100 HGH nematodes and 50-3250 OGH protozoa.

In infections due to gastroenteric nematodes, there were one to five genera, with a double 71.43% and simple 28.5%.

In the Valley 2 region, the presence of PGE was not found and for protozoa, 46% (23/50) positive were obtained, the MacMaster range was 50-100 OGH.

The results for NGE of the Valle 1 and Valle 2 regions are less frequent and this may be influenced by the age of the animals in the sampling that were adults (Encalada et al., 2009), the sanitary management of deworming of the herd before sampling; as well as the semi-arid climate conditions of the region (Martínez and Merino, 2011; Baumgard and Rhoads, 2013), which does not favor the formation and viability of the infecting larvae in the environment (table 2).

With respect to the protozoa in the High-mountain, the three most frequent species were:

E. bovis 69.65%, E. alabamensis 34.48% and E. ellipsoidalis 24.13%. In the Low- mountain, E. bovis 65.21% and E. alabamensis predominated 43.47%. In the Valle 1 region the most abundant was E. bovis with 46.5%. In Valley 2 E. ellipsoidalis and E. bukidonensis were found with 25% respectively (table 3).

Table 3 Number and percentage of Eimerias identified from cattle from four regions of southern Sonora 

Protozoario Sierra alta Porcentaje Sierra baja Porcentaje Valle 1 Porcentaje Valle 2 Porcentaje
Frecuencia (%) Frecuencia (%) Frecuencia (%) Frecuencia (%)
E. bovius 101 69.65 13 62.21 15 46.5 1 12.5
E. alabamensis 50 34.48 10 43.47 2 6.25 1 12.5
E. ellipsoidalis 35 24.13 3 13.04 6 21.85 2 25
E.auburnensis 34 23.44 2 8.69 3 9.37 0 0
E.bukidnonensis 28 19.31 0 0 4 12.5 2 25
E.subspherica 26 17.93 1 4.34 7 21.85 1 12.5
E. zurnii 20 13.79 1 4.34 9 28.15 1 12.5

Coccidia infections in High-mountain occurred from one to six genera of Eimeria, the three most frequent were: single 33.10%, double 30.34% and triple 16.55%. In Low-mountain: 43.48% single and 56.52% double. Valley 1 region was simple 71.88% and double 15.63% and Valley 2 region simple 66.66% and double with 33.33% (table 4).

Table 4 Type of Eimeria infection in cattle from four regions of the southern state of Sonora 

Type de infection

High-mountain

Quantily

Porcentage

(%)

Low-mountain

Quantily

Porcentage

(%)

Valley 1

Quantily

Porcentage

(%)

Valley 2

Frecuency

Porcentage

(%)

Simple 48 33.1 10 43.48 23 71.88 4 66.66
Doble 44 30.34 13 56.52 5 15.63 2 33.33
Triple 24 16.55 0 0 3 9.6 0 0
Quadruple 20 13.79 0 0 0 0 0 0
Quíntuple 6 4.13 0 0 1 3.13 0 0
Sextuple 3 2.06 0 0 0 0 0 0

In this study the zones of Valley 1 and Valley 2, several species of Eimeria were positive; This is consistent with works that report that there are at least 13 species of Eimeria that infect cattle, but only some are very pathogenic such as E. bovis and E. zuernii (Das et al., 2015; Pascoti et al., 2011 ) and E. alabamensis (Das et al., 2015). In roofed pens, E. ellipsoidalis, E. alabamensis and E. auburnensis are reported (Mitchell et al., 2012; Forslid et al., 2015).

Eimeria infections can cause severe diarrhea, feces containing blood, fibrin and intestinal tissue; the signs are fever, pain, tenesmus, anemia, dehydration, weakness, anemia and weight loss (Pascoti et al., 2011). This complex of effects has considerable clinical and economic consequences. In endemic areas, first-year calves are at high risk of developing clinical coccidiosis, and infections by several species are common; E. bovis, E. zuernii and E. alabamensis being more common, during the first two weeks of life (Samson et al., 2006; Pascoti et al., 2011), and up to 12 months of age (Mitchell et al. , 2012; Forslid et al., 2015). It is estimated that losses due to reduction in feed efficiency are 25 to 60% percalf, and a 6 to 8% annual loss due to eimeriosis was predicted with a simulator model (Lassen and Osstergaard, 2012).

Various studies have been conducted in different countries such as Peru, Brazil, the United States, India and England; where the most frequent Eimerias identified were: E. bovis, E. zuernii, E. auburnensis, E. ellipsoidalis; less frequently E. subspherica, E. bukidnonesis, E. cylindrica, E. Canadians and E. alabamensis (Pascoti et al., 2011; Mitchell et al., 2012; Colina et al., 2013; Lucas et al., 2014; Das et al., 2015).

In Mexico, studies conducted on bovines in Yucatán and Guerrero, the most frequent Eimerias were: E. bovis, E. ellipsoidalis and E. zuerni; to a lesser extent, we found: E. auburnensis and E. canadensis and E. parva (Rodríguez et al., 1996; Figueroa et al., 2018).

In the present investigation, the four sectors had presence of E. bovis, E. alabamensis, E. ellipsoidalis and E. auburnensis, their frequency varies by different age groups and environmental conditions; this indicates the viability of sporulated oocysts, which is more than one year (Lucas et al., 2014). Most studies of natural Eimeria infections in cattle confirm that calves under one year of age have a high prevalence of infection and eliminate the greatest number of oocysts by feces into the environment (Colina et al., 2013; Lucas et al., 2014). Transmission is influenced by adult cattle that are asymptomatic carriers, which favor frequent infection in young animals (Mitchell et al., 2012; Colina et al., 2013); which can occur in the rest areas or "dumps" and grazing within the summer pastures, as well as in the housing pens.

CONCLUSION

It is shown that cattle raised in the study area showed a frequency of low 17.56% to high 83.03% of gastroenteric parasites, with the presence of one to eight nematode genera; and from one to seven genera of protozoa.

ACKNOWLEDGMENT

The authors thank the support for the donation granted by the Program for the Promotion and Support of Research (PROFAPI) of the Technological Institute of Sonora, for the donation granted for the realization of this work (PROFAPI_2018_0047 and PROFAPI_ 2019_0052).

LITERATURA CITADA

BAUMGARD LH, Rhoads RP Jr. 2013. Effects of heat stress on post absorptive metabolism and energetics. Annual Review of Animal Biosciences. 1:311-337.ISSN: 21658102, 21658110. DOI: 10.1146/annurev-animal-031412-103644. [ Links ]

BISWAJIT D, Konch P, Rahman T, Upadhyaya TN, Pathak DC, Tamuli SM, Phangchoo CV, Begum SA. 2017. Ocurrence and pathology of Haemonchus contortus infections in goats. Journal of Entomology and Zoology Studies. 5(3):1284-1287. E-ISSN:2320-7078, P-ISSN:2349-6800, DOI: http://dx.doi.org/10.22271/j.ento. http://www.entomoljournal.com, http://www.entomoljournal.com/archives/2017/vol5issue3/PartR/5-3-122-461.pdfLinks ]

COLINA JC, Mendoza GA, Jara CA. 2013. Prevalencia del parasitismo por Eimeria en bovinos, Bos taurus, del Distrito Pacanga (La Libertad, Perú). Y su relación con factores sociodemográficos y ambientales. Rebiolest. 1(2): e72-e78. http://revistas.unitru.edu.pe/index.php/ECCBB/issue/view/299/showTocLinks ]

DAS M, Deka DK, Sarmah PG, Islam S, Sarma S. 2015. Diversity of Eimeria spp. in dairy cattle of Guwahati, Assam India. Veterinary World. EISSN: 2231-0916. DOI:10.14202. http://www.veterinaryworld.org/Vol.8/August-2015/2.pdfLinks ]

DENOGEAN BFG, Moreno MS, Ayala AF, Ibarra FA, Martin RMH, Retes LR. 2013. La ganadería bovina para carne en Sonora, México en la actualidad. XXVI Congreso Internacional en Administración de Empresas Agropecuarias. Hermosillo, Sonora. 30 y 31 de mayo y 1 de junio 2013. 56-65 p. [ Links ]

ENCALADA MLA, Corbala BJA, Vargas MJJ, García RMJ, Uicab BL, Río RJ. 2009. Prevalencia de nematodos gastroentéricos de becerros en sistema doble propósito del municipio de Escárcega, Campeche, México. Agrociencia. 43(6): 569-576. ISSN: 1405-3195. http://www.redalyc-org/articulo.oa?id=30215549002Links ]

FERNÁNDEZ FA, Arieta RR, Graillet JE, Romero SD, Romero FM, Felipe AI. 2015. Prevalencia de nematodos gastroentéricos en bovinos doble propósito en 10 ranchos de Hidalgotitlán, Veracruz, México. Abanico Veterinario. 5(2):13-18. ISSN 2448-6132. E-ISSN:2007-4240 DOI:10.21929/abavet. [ Links ]

FIGUEROA A, Pineda RSA, Godínez JF, Vargas AD, Rodríguez BE. 2018. Parásitos gastrointestinales de ganado bovino y caprino en Quechultenango, Guerrero, México. Agroproductividad. 11(6): 97-104. ISSN: 2594-0252.http://www.revista-agroproductividad.org/index.php/agroproductividadLinks ]

FORSLID A, Christensson D, Dahl J, Grandi G, Enemark JMD. 2015. Bovine eimeriosis in Swedish calves: Epidemiology and insights into sampling procedures. Veterinary Parasitology. 1(2):16-29. ISSN: 2405-9390. http://dx.doi.org/10.1016/j.vprsr.2016.02.004 [ Links ]

JOHANSSOS L. 2017. The impact of gastrointestinal parasites on weight gain, activity patterns and behaviors in cattle on pasture. Departament of animal environment and healthy no. 688. Skara. Swedish University of Agricultural Sciences. 4-6 p. ISSN: 1652- 200X. [ Links ]

LASSEN B, Ostergaard S. 2012. Estimation of the economic effects of Eimeria in Estonian dairy herds using a stochastic model. Preventive Veterinary Medicine. ISSN:106:258-265. DOI:10.1016/j.prevetmed.2012.04.005. [ Links ]

LUCAS AS, Swecker WS, Linday DS, Scaglia G, Neel JPS, Elvinger FC, Zajac AM. 2014. 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. Veterinary Parasitology. 202:201-206. ISSN: 0304-4017 DOI: http:dx.doi.org/10.1016/j.vetpar.2014.02.052 [ Links ]

MARTÍNEZ J, Merino S. 2011. Host-parasite interaction under extreme climatic conditions. Current Zoology. 57(3):390-405. ISSN: 1674-5507. https://doi.org/10.1093/czoolo/57.3.390 [ Links ]

MITCHELL ESE, Smith RP, Ellis IJ. 2012. Husbandry risk factors associated with subclinical coccidiosis in young cattle. The Veterinary Journal. 193:119-123.ISBN:1090-0233. DOI:10.1016/j.tvjl.2011.09.017 [ Links ]

OLIVIERA MCS, Nicodemo MIF, Pezzopane JRM, Gusma MR, Chagas ACS, Giglioti R, Bilhassi TB, Santana CH, Goncalves TC, Rabelo TA, Neo TA. 2017. Gastrointestinal nematode infection in beef cattle raised in silvopastoral and conventional systems in Sao Paulo state, Brazil. Agroforest Systems. 91(3):495-507. ISSN: 1572-680. https://doi.org/10.1007/s10457-016-9950-y [ Links ]

PASCOTI BFR, López MA, Alves DF, Perazza CA, Ferrazani PM, Guimaraes Am. 2011. Frequency of species of Eimeria in females of the Holstein-friesian breed at the post- weaning stage during autumn and winter. Revista Brasileña Parasitología Veterinaria. Jaboticabal. 20(4):303-307. ISSN: 1984-2961.http://www.scielo.br/pdf/rbpv/v20n4/a08v20n4.pdfLinks ]

PINILLA JC, Flórez P, Sierra MT, Morales E, Sierra R, Vásquez MC, Todon JA, Sánchez A, Ortiz D. 2018. Point prevalence of gastrointestinal parasites in double purpose cattle or Rio de Oro and Aguachica municipalities, Cesar state, Colombia. Veterinary Parasitology. Regional studies and reports. 12:26-30. ISBN: 2405-9390 https://doi.org/10.1016/j.vprsr.2018.01.003 [ Links ]

QUIROZ RH, Figueroa J, Ibarra F, López M. 2011. Epidemiología de enfermedades parasitarias en animales domésticos. In Quiroz H, Figueroa J, Ibarra F, López M. (Eds). Revista FMVZ. UNAM. México. 257 p. ISBN: 978-607-00-4015-3. [ Links ]

RETES, López R, Rivera M, Ibarra F, Moreno F, Medina DS, Ballesteros FG. 2013. Análisis de rentabilidad de repasto de becerros en Sonora. Revista Mexicana de Agronegocios. 17(33): 588-598. ISSN:1405-9282 https://www.redalyc.org/articulo.oa?id=14127709018Links ]

RODRÍGUEZ VRI, Domínguez AJL, Torres AFF. 1996. Epidemiological factors associated to bovine coccidiosis in calves (Bos indicus) in a subhumid tropical climate. Revista Biomédica. 7(4):211-218. ISSN: 2007-8447. DOI: https://doi.org/10.32776/revbiomed.v10i1.186 [ Links ]

RODRÍGUEZ VRI, Grisi L, Pérez LAA, Silva VH, Torres AJFJ, Fragoso SH, Romero SD, Rosario CR, Saldierma F, García CD. 2017. Evaluación del impacto económico potencial de los parásitos del ganado bovino en México. Revisión. Revista Mexicana Ciencias Pecuarias. 8(1):61-74. ISSN-e: 2448-6698 http://Dx.doi.org/10.22319/rmcp.v8i1.430 [ Links ]

SAMSON HGV, Epe C, Wirtherle N, Heyden VVD, Welz C, Radeloff I, Beening J, Carr D, Hellmann K, Schnieder T, Krieger K. 2006. Clinical and epidemiological characteristics of Eimeria infections in first year grazing cattle. Veterinary Parasitology. 136:215-221. ISSN: 0340-4017. DOI:10.1016/j.vetpar.2005.11.022 [ Links ]

SCHEAFFER RL, Mendenhall W, Ott RL, Gerow KG. 2012. Elementary survey sampling. Seven edition student ed. Boston MA. Books-Cole. 49-53 p.ISBN: 13-978-0-8400-5361-9 [ Links ]

SMN. (Sistema Meteorológico Nacional). 2018. http://smn.cna.gob.mx/es/informacion-climatologica-ver-estado?estado=son . Fecha de ingreso 28 de mayo 2018. [ Links ]

STROMBERG B, Gasbarre LC, Waite A, Bechtold D, Brown MS, Robinson NA, Olson EJ, Newcomb H. 2012. Cooperia punctate: effect cattle productivity?. Veterinary Parasitology. 183:284-291 PMID: 21821358 DOI:10.1016/j.vetpar.2011.07.030 [ Links ]

THURSFIELD M. 2018. Veterinary Epidemiology. Wiley-Blackwell Publishing. USA. Fourth Edition. 219-251 p. ISBN: 978-1118280287. [ Links ]

TORRES AJFJ. 2006. The effect of supplementary feeding in browsing criollo kids and hair sheep naturally infected with gastrointestinal nematodes. Herbivores: Assessment of intake, digestibility and the roles of secondary compounds. 34: 261-278.DOI: https://doi.org/10.1017/S1463981500042473 [ Links ]

VÁZQUEZ PVM, Flores CJ, Santiago VC, Herrera RD, Palacios FA, Liébano HE, Pelcastre OA. 2004. Frecuencia de nematodos gastroentéricos en bovinos de tres áreasde clima subtropical húmedo de México. Técnica Pecuaria México. 42 (2): 237-245. ISSN- e: 2448-6698. ISSN: 0040-1889. https://www.redalyc.org/articulo.oa?id=61342209Links ]

WAYNE WD. 2014. Bioestadística: Base para el análisis de la ciencia para la salud. Cuarta edición. Ed. Limusa-Wiley. México, D.F. 1-12 p. ISBN:97896818643. [ Links ]

YACOB CH, Mistre AH, Adem AH, Basu AK. 2009. Parasitological and clinical responses of lambs experimentally infected with Haemonchus contortus (L3) with and without ivermectin treatment. Veterinary Parasitology. 166: 119-123. ISSN: 1873-2550. ISSN:0304-4017. DOI:10.1016/j.vetpar.2009.07.038. [ Links ]

Received: February 24, 2019; Accepted: September 28, 2019

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