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Prevalence and seasonal variation of Fasciola hepatica in slaughtered cattle: the role of climate and environmental factors in Mexico

Published online by Cambridge University Press:  20 August 2021

K. Hernández-Guzmán ,
P. Molina-Mendoza ,
J. Olivares-Pérez ,
Y. Alcalá-Canto ,
A. Olmedo-Juárez ,
A. Córdova-Izquierdo  and
A. Villa-Mancera Open the ORCID record for A. Villa-Mancera [Opens in a new window]
K. Hernández-Guzmán
Affiliation:
Ingeniería en Agronomía y Zootecnia, División de Ciencias Naturales, Universidad Intercultural del Estado de Puebla, Puebla, Mexico
P. Molina-Mendoza
Affiliation:
Ingeniería en Agronomía y Zootecnia, División de Ciencias Naturales, Universidad Intercultural del Estado de Puebla, Puebla, Mexico
J. Olivares-Pérez
Affiliation:
Unidad Académica de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Guerrero, Ciudad Altamirano, Guerrero, Mexico
Y. Alcalá-Canto
Affiliation:
Departamento de Parasitología, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de Mexico, CP 04510, CDMX, Mexico
A. Olmedo-Juárez
Affiliation:
Centro Nacional de Investigación Disciplinaria en Salud Animal e Inocuidad (CENID SAI-INIFAP), Jiutepec, Morelos, Mexico
A. Córdova-Izquierdo
Affiliation:
Departamento de Producción Agrícola y Animal, Universidad Autónoma Metropolitana, CP 04960, Unidad Xochimilco, CDMX, Mexico
A. Villa-Mancera*
Affiliation:
Facultad de Medicina Veterinaria y Zootecnia, Benemérita Universidad Autónoma de Puebla, Tecamachalco, CP 75482, Tecamachalco Puebla, Mexico
*
Author for correspondence: A. Villa-Mancera, E-mail: abel.villa@gmail.com
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Abstract

The objective of this study is to determine the prevalence of Fasciola hepatica infection in cattle slaughterhouses, as well as its association with climatic/environmental factors (derived from satellite data), seasonality and climate regions in two states in Mexico. Condemned livers from slaughtered animals were obtained from three abattoirs in the states of Puebla and Veracruz. The overall prevalence of the parasite in cattle between January and December of 2017 was 20.6% (1407 out of 6834); the highest rate of condemnation was observed in Veracruz (26.3%; tropical climate), and the lowest rate was found in Puebla (15.5%; temperate climate). The seasonal prevalence of fluke infection was 18.6%, 14.8% and 28.4% during the wet season, and 17.1%, 12.4% and 22.8% during the dry season in the three abattoir sites, located in the districts of Zacatlán, Teziutlán and Ciudad Alemán, respectively. Liver condemnations due to bovine fasciolosis were prevalent in the Zacatlán, Teziutlán and Ciudad Alemán districts during summer, autumn and summer, respectively. Using generalized estimating equations analysis, we determined six variables – rainfall (wet/dry), land surface temperature day, land surface temperature night, normalized difference vegetation index, seasonality and climate regions (temperate/tropical) – to be significantly associated with the prevalence of condemned livers. Climate region was the variable most strongly associated with F. hepatica infection (odds ratio (OR) 266.59; 95% confidence interval (CI): 241.90–353.34), followed by wet and dry seasons (OR 25.56; 95% CI: 20.56–55.67).

Keywords

Fasciola hepaticafasciolosisprevalenceepidemiologyseasonalitygeographic information systemcattleslaughterhouseMexico
Type
Research Paper
Information
Journal of Helminthology , Volume 95 , 2021 , e46
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Andrews, S, Graczyk, T, Fried, B, Fairweather, I, Threadgold, L and Torgerson, P (1999) Fasciolosis. pp. 1–29 in Dalton, JP (Ed) The life cycle of Fasciola hepatica. Wallingford, Oxon, UK, CAB International Oxon.Google Scholar
Arias-Pacheco, C, Lucas, JR, Rodriguez, A, Cordoba, D and Lux-Hoppe, EG (2020) Economic impact of the liver condemnation of cattle infected with Fasciola hepatica in the Peruvian Andes. Tropical Animal Health and Production 52, 1927–1932.CrossRefGoogle ScholarPubMed
Arias, M, Lomba, C, Dacal, V, et al. (2011) Prevalence of mixed trematode infections in an abattoir receiving cattle from northern Portugal and north-west Spain. Veterinary Record 168, 408.CrossRefGoogle Scholar
Barbosa, R, Pinto, C, Garcia, P and Rodrigues, A (2019) Prevalence of fasciolosis in slaughtered dairy cattle from Sao Miguel Island, Azores, Portugal. Veterinary Parasitology: Regional Studies and Reports 17, 100319.Google ScholarPubMed
Bennema, SC, Ducheyne, E, Vercruysse, J, Claerebout, E, Hendrickx, G and Charlier, J (2011) Relative importance of management, meteorological and environmental factors in the spatial distribution of Fasciola hepatica in dairy cattle in a temperate climate zone. International Journal for Parasitology 41, 225–233.CrossRefGoogle Scholar
Bernardo, CdC, Carneiro, MB, Avelar, BRd, Donatele, DM, Martins, IVF and Pereira, MJS (2011) Prevalence of liver condemnation due to bovine fasciolosis in Southern Espírito Santo: temporal distribution and economic losses. Revista Brasileira de Parasitologia Veterinária 20, 49–53.CrossRefGoogle Scholar
Caravedo, MA, White, AC Jr, Morales, ML, et al. (2021) Comparison of liver condemnation and bile microscopy as tools to estimate Fasciola hepatica prevalence and burden in the Anta Province of Cusco in Peru. Vector-Borne and Zoonotic Diseases. https://doi.org/10.1089/vbz.2020.2753.CrossRefGoogle ScholarPubMed
Charlier, J, Vercruysse, J, Morgan, E, van Dijk, J and Williams, DJ (2014) Recent advances in the diagnosis, impact on production and prediction of Fasciola hepatica in cattle. Parasitology 141, 326–335.CrossRefGoogle ScholarPubMed
Charlier, J, Ghebretinsae, AH, Levecke, B, Ducheyne, E, Claerebout, E and Vercruysse, J (2016) Climate-driven longitudinal trends in pasture-borne helminth infections of dairy cattle. International Journal for Parasitology 46, 881–888.CrossRefGoogle ScholarPubMed
Cruz-Mendoza, I, Quiroz-Romero, H, Correa, D and Gomez-Espinoza, G (2011) Transmission dynamics of Fasciola hepatica in the plateau region of Mexico. Effect of weather and treatment of mammals under current farm management. Veterinary Parasitology 175, 73–79.CrossRefGoogle ScholarPubMed
da Costa, RA, Corbellini, LG, Castro-Janer, E and Riet-Correa, F (2019) Evaluation of losses in carcasses of cattle naturally infected with Fasciola hepatica: effects on weight by age range and on carcass quality parameters. International Journal for Parasitology 49, 867–872.CrossRefGoogle ScholarPubMed
Durr, P, Tait, N and Lawson, A (2005) Bayesian hierarchical modelling to enhance the epidemiological value of abattoir surveys for bovine fasciolosis. Preventive Veterinary Medicine 71, 157–172.CrossRefGoogle ScholarPubMed
Dutra, LH, Molento, MB, Naumann, CR, Biondo, AW, Fortes, FS, Savio, D and Malone, JB (2010) Mapping risk of bovine fasciolosis in the south of Brazil using geographic information systems. Veterinary Parasitology 169, 76–81.CrossRefGoogle ScholarPubMed
García, E (1988) Modificaciones al sistema climático de Köppen. Mexico DF, Mexico, Instituto de Geografía. Universidad Nacional Autónoma de México.Google Scholar
Malone, J, Gommes, R, Hansen, J, Yilma, J, Slingenberg, J, Snijders, F, Nachtergaele, F and Ataman, E (1998) A geographic information system on the potential distribution and abundance of Fasciola hepatica and F. Gigantica in east Africa based on food and agriculture organization databases. Veterinary Parasitology 78, 87–101.CrossRefGoogle Scholar
Martins, IVF, de Avelar, BR, Pereira, MJS and da Fonseca, AH (2012) Application of a geographical information system approach for risk analysis of fascioliasis in southern Espírito Santo State, Brazil. Geospat Health 6, S87–S93.CrossRefGoogle Scholar
McCann, CM, Baylis, M and Williams, DJ (2010) The development of linear regression models using environmental variables to explain the spatial distribution of Fasciola hepatica infection in dairy herds in England and Wales. International Journal for Parasitology 40, 1021–1028.CrossRefGoogle ScholarPubMed
Mehmood, K, Zhang, H, Sabir, AJ, et al. (2017) A review on epidemiology, global prevalence and economical losses of fasciolosis in ruminants. Microbial Pathogenesis 109, 253–262.CrossRefGoogle ScholarPubMed
Munguía-Xóchihua, J, Ibarra-Velarde, F, Ducoing-Watty, A, Montenegro-Cristino, N and Quiroz-Romero, H (2007) Prevalence of Fasciola hepatica (ELISA and fecal analysis) in ruminants from a semi-desert area in the northwest of Mexico. Parasitology Research 101, 127–130.CrossRefGoogle Scholar
Ojeda-Robertos, NF, González-Garduño, R, Cornelio-Cruz, S, et al. (2020) Factores asociados al decomiso de hígados positivos a Fasciola sp en una zona endémica del sureste de México. Revista Mexicana de Ciencias Pecuarias 11, 565–575.CrossRefGoogle Scholar
Ouchene-Khelifi, N, Ouchene, N, Dahmani, H, Dahmani, A, Sadi, M and Douifi, M (2018) Fasciolosis due to Fasciola hepatica in ruminants in abattoirs and its economic impact in two regions in Algeria. Tropical Biomedicine 35, 181–187.Google ScholarPubMed
Palacio Collado, D, Bertot Valdés, JA, Beltrao Molento, M, Vázquez Gil, Á, Izquierdo Pérez, N, Arenal Cruz, A and Arteaga Campbell, A (2017) Comportamiento estacional de Fasciola hepatica en bovinos sacrificados en el matadero Chacuba, Camagüey, Cuba. Revista de Producción Animal 29, 30–35.Google Scholar
Qin, H, Gao, X, Wang, H and Xiao, J (2016) Relative importance of meteorological and geographical factors in the distribution of Fasciola hepatica infestation in farmed sheep in Qinghai Province, China. Parasite 23, 59.CrossRefGoogle ScholarPubMed
Quevedo, LS, Bruhn, FRP, Teixeira, JLR, Alberti, TS, Scheid, HV, Raffi, MB, Sallis, ESV and Schild, AL (2018) Epidemiological and clinical-pathological aspects of fasciolosis in livers of cattle slaughtered in southern Brazil. Pesquisa Veterinária Brasileira 38, 1761–1766.CrossRefGoogle Scholar
Rapsch, C, Schweizer, G, Grimm, F, Kohler, L, Bauer, C, Deplazes, P, Braun, U and Torgerson, PR (2006) Estimating the true prevalence of Fasciola hepatica in cattle slaughtered in Switzerland in the absence of an absolute diagnostic test. International Journal for Parasitology 36, 1153–1158.CrossRefGoogle ScholarPubMed
Rojas, D and Cartín, JA (2016) Prevalencia de Fasciola hepatica y pérdidas económicas asociadas al decomiso de hígados en tres mataderos de clase a de Costa Rica. Agronomía Costarricense 40, 53–62.CrossRefGoogle Scholar
Sabourin, E, Alda, P, Vázquez, A, Hurtrez-Boussès, S and Vittecoq, M (2018) Impact of human activities on fasciolosis transmission. Trends in Parasitology 34, 891–903.CrossRefGoogle ScholarPubMed
Sanchez-Vazquez, MJ and Lewis, FI (2013) Investigating the impact of fasciolosis on cattle carcase performance. Veterinary Parasitology 193, 307–311.CrossRefGoogle ScholarPubMed
Sandholt, I, Rasmussen, K and Andersen, J (2002) A simple interpretation of the surface temperature/vegetation index space for assessment of surface moisture status. Remote Sensing of Environment 79, 213–224.CrossRefGoogle Scholar
Selemetas, N and de Waal, T (2015) Detection of major climatic and environmental predictors of liver fluke exposure risk in Ireland using spatial cluster analysis. Veterinary Parasitology 209, 242–253.CrossRefGoogle ScholarPubMed
Sokal, RR and Rohlf, FJ (1995) Biometry: the principles and practise of statistic in biological research. 3rd edn. New York, WH Freeman and Company.Google Scholar
Theodoropoulos, G, Theodoropoulou, E, Petrakos, G, Kantzoura, V and Kostopoulos, J (2002) Abattoir condemnation due to parasitic infections and its economic implications in the region of Trikala, Greece. Journal of Veterinary Medicine, Series B 49, 281–284.CrossRefGoogle ScholarPubMed
Torgerson, P and Claxton, J (1999) Fasciolosis. Epidemiology and control. Wallingford, Oxon, UK, CAB International Oxon. pp. 113–149.Google Scholar
Villa-Mancera, A and Reynoso-Palomar, A (2019a) Bulk tank milk ELISA to detect IgG1 prevalence and clustering to determine spatial distribution and risk factors of Fasciola hepatica-infected herds in Mexico. Journal of Helminthology 93, 704–710.CrossRefGoogle Scholar
Villa-Mancera, A and Reynoso-Palomar, A (2019b) High prevalence, potential economic impact, and risk factors of Fasciola hepatica in dairy herds in tropical, dry and temperate climate regions in Mexico. Acta Tropica 193, 169–175.CrossRefGoogle Scholar
Villa-Mancera, A, Reynoso-Palomar, A, Olivares-Perez, J, Ortega-Vargas, S, Cruz-Mendoza, I and Quiroz-Romero, H (2015) Motility of Fasciola hepatica miracidia assessed with a computer-assisted sperm analyser. Journal of Helminthology 89, 453–457.CrossRefGoogle ScholarPubMed
Yilma, J and Malone, J (1998) A geographic information system forecast model for strategic control of fasciolosis in Ethiopia. Veterinary Parasitology 78, 103–127.CrossRefGoogle ScholarPubMed
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