Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-02T21:34:41.611Z Has data issue: false hasContentIssue false
  • English
  • Français

Fasciola hepatica infection in cattle and the use of simulation models for endemic areas

Published online by Cambridge University Press:  10 September 2020

M.B. Molento Open the ORCID record for M.B. Molento [Opens in a new window] ,
L.H. Dutra Open the ORCID record for L.H. Dutra [Opens in a new window] ,
I.C. Pritsch Open the ORCID record for I.C. Pritsch [Opens in a new window] ,
V.P. Garbin Open the ORCID record for V.P. Garbin [Opens in a new window] ,
A.M. Pereira ,
A. Gavião ,
A.L. Gabriel ,
R.S. de Sousa Open the ORCID record for R.S. de Sousa [Opens in a new window]  and
J.G.A. Viana Open the ORCID record for J.G.A. Viana [Opens in a new window]
M.B. Molento*
Affiliation:
Laboratory of Veterinary Clinical Parasitology, Federal University of Paraná, UFPR, Rua dos Funcionarios, 1540, Curitiba, PR, Brazil
L.H. Dutra
Affiliation:
Ministry of Health, EPISUS, Esplanada dos Ministérios, Bloco G. Brasilia, DF, Brazil
I.C. Pritsch
Affiliation:
Laboratory of Veterinary Clinical Parasitology, Federal University of Paraná, UFPR, Rua dos Funcionarios, 1540, Curitiba, PR, Brazil
V.P. Garbin
Affiliation:
Laboratory of Veterinary Clinical Parasitology, Federal University of Paraná, UFPR, Rua dos Funcionarios, 1540, Curitiba, PR, Brazil
A.M. Pereira
Affiliation:
Department of Preventive Veterinary Medicine, Federal University of Santa Maria, Avenida Roraima, 1000, Santa Maria, Brazil
A. Gavião
Affiliation:
Agricultural Office of the State of Rio Grande do Sul, Rua Bento Gonçalves, 335, Itaqui, RS, Brazil
A.L. Gabriel
Affiliation:
Department of Preventive Veterinary Medicine, Federal University of Santa Maria, Avenida Roraima, 1000, Santa Maria, Brazil
R.S. de Sousa
Affiliation:
Laboratory of Animal Pathology, Federal University of Parana, UFPR, Rua dos Funcionarios, 1540, Curitiba, PR, Brazil
J.G.A. Viana
Affiliation:
Campus Santana do Livramento, Federal University of the Pampa, Santana do Livramento, RS, Brazil
*
Author for correspondence: M.B. Molento, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Fasciolosis is a food-borne disease that causes great distress to a range of hosts, including humans. The objectives of this study were to (1) evaluate the liver damage and carcass weight of cattle naturally infected with Fasciola hepatica from the state of Rio Grande do Sul (RS), Brazil, and to (2) determine the distribution of adult flukes in 12,236 cattle liver from RS. The data from these experiments were used to calculate the overall economic loss due to F. hepatica infection. Eighteen adult Polled Hereford cows were divided into a triclabendazole (TbG) and a F. hepatica-positive group (FhG). For Experiment 1, a generalized linear mixed model revealed a statistical difference in carcass weight (49.8 kg) between TbG and FhG. The Monte Carlo analysis also revealed that the animals’ weight differences were due to the disease. For Experiment 2, the prevalence of infected livers was above 16% (1904/12,236), mostly (20.1%) from the south-west region of RS. The Susceptible-infected-recovered (SIR) epidemic model revealed the evolution of the infection using a high infectivity and low recovery rate. Other distinctive scenarios that occur in RS were also established with different rates of infectivity. The economic assessment showed a potential loss of US$45 million to the beef cattle industry of RS, with an overall State cost of US$90.3 million. These novel findings reveal the importance of fasciolosis infection, which can cause a significant health condition and poor animal welfare.

Keywords

Fasciolosishistopathologylivertrematodecattle welfarerisk analysis
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e185
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aleixo, MA, Freitas, DF, Dutra, LH, Malone, J, Martins, IVF and Molento, MB (2015) Fasciola hepatica: epidemiology, perspectives in the diagnostic and the use of geoprocessing systems for prevalence studies. Semina 36(3), 1451–1466.Google Scholar
Aleri, JW, Hine, BC, Pyman, MF, Mansell, PD, Wales, WJ, Mallard, B and Fisher, AD (2016) An assessment of immune and stress responsiveness in Holstein-Friesan cows selected for high and low feed conversion efficiency. Animal Production Science 57(2), 244–251.CrossRefGoogle Scholar
Arias-Pacheco, C, Lucas, JR, Rodríguez, A, Córdoba, 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. https://doi.org/10.1007/s11250-020-02211-y.CrossRefGoogle ScholarPubMed
Bennema, SC, Scholte, RG, Molento, MB, Medeiros, C and Carvalho, OS (2014) Fasciola hepatica in bovines in Brazil: data availability and spatial distribution. Journal of the Tropical Medical Institute of Sao Paulo 56, 35–41.CrossRefGoogle ScholarPubMed
Bennema, SC, Molento, MB, Scholte, RG, Carvalho, OS and Pritsch, I (2017) Modelling the spatial distribution of Fasciola hepatica in bovines using decision tree, logistic regression and GIS query approaches for Brazil. Parasitology 144, 1677–1685.CrossRefGoogle ScholarPubMed
Bostelmann, SCW, Luz, E, Thomaz-Soccol, V and Cirio, SM (2000) Comparative liver histopathology from cattle, water buffalos and sheep infected with Fasciola hepatica. Archives of Veterinary Science 5, 95–100.Google Scholar
Breslow, NE and Clayton, DG (1993) Approximate inference in generalized linear mixed models. Journal of the American Statistical Association 88(421), 9.Google Scholar
Byrne, AW, McBride, S, Lahuerta-Marin, A, Guelbenzu, M, McNair, J, Skuce, RA and McDowell, SW-J (2016) Liver fluke (Fasciola hepatica) infection in cattle in Northern Ireland: a large-scale epidemiological investigation utilizing surveillance data. Parasites & Vectors 9(1), 209.CrossRefGoogle Scholar
Centro de Estudos Avançados em Economia Aplicada (CEPEA) (2016) GDP Gross domestic product – data from 1995 to 2015. Piracicaba, Brazil, University of Sao Paulo.Google Scholar
Charlier, J, Levecke, B, Devleesschauwer, B, Vercruysse, J and Hogeveen, H (2013) The economic effects of whole-herd versus selective anthelmintic treatment strategies in dairy cows. Journal of Dairy Science 95(6), 2977–2987.CrossRefGoogle Scholar
Cucco, DC, Abdalla, BB, Chiocca, M, Sá, J, Zieher, G, Agostini, VP and Theodorovicz, ET (2015) Perfil dos bovinos abatidos pelos principais abatedouros/frigoríficos do estado de Santa Catarina. NESPRO Bulletin 5, 1–3.Google Scholar
Cwiklinski, K, Jewhurst, H, McVeigh, P, et al. (2018) Infection by the helminth parasite Fasciola hepatica requires rapid regulation of metabolic, virulence, and invasive factors to adjust to its mammalian host. Molecular & Cellular Proteomics 17, 792–809.CrossRefGoogle ScholarPubMed
Dutra, LH, Molento, MB, Naumann, CRC, Biondo, AW, Fortes, FS, Savio, D and Malone, JB (2010) Epidemiology of bovine fasciolosis in Brazil using geographic information system. Veterinary Parasitology 169, 76–81.CrossRefGoogle Scholar
Gavinho, B, Kulek, ACG and Molento, MB (2008) Quantitative determination and geographic distribution of Fasciola hepatica in slaughter beef cattle in Sao Jose dos Pinhais, PR. p. 128 in Annals 16o EVINCI/UFPR, Curitiba, PR (Congress).Google Scholar
Girão, E and Ueno, H (1994) Four-sieve technique. p. 62in Ueno, H and Gonçalves, PC (Eds) Diagnostic manual for ruminant helminth infections. Porto Alegre, JICA Press.Google Scholar
Graham-Brown, J, Hartley, C, Clough, H, Kadioglu, A, Baylis, M and Williams, DJL (2018) Dairy heifers naturally exposed to Fasciola hepatica develop a type 2 immune response and concomitant suppression of leukocyte proliferation. Infection and Immunity 86, e00607–e00617.CrossRefGoogle ScholarPubMed
Hussain, KL and Zghair, ZR (2017) Prevalence of fasciolosis in ruminant in Karbala city. Journal of Entomology and Zoological Studies 5, 364–369.Google Scholar
IBGE, Instituto Brasileiro de Geografia e Estatística (2016) Quarterly information for slaughter animals. IBGE, automatic system for data recovery – SIDRA. Brasília, Brazil, IBGE.Google Scholar
IEPE, Instituto de Estudos e Pesquisas Econômicas (2016) Economic indicators. Porto Alegre, Brazil, Federal University of Rio Grande do Sul.Google Scholar
Kantzoura, V, Kouam, M, Demiris, N, Feidas, H and Theodoropoulos, G (2011) Risk factors and geospatial modelling for the presence of Fasciola hepatica infection in sheep and goat farms in the Greek temperate Mediterranean environment. Parasitology 138(7), 926–938.CrossRefGoogle ScholarPubMed
Khan, MK, Sajid, MS, Khan, MN, Iqbal, Z, Arshad, M and Hussain, A (2011) Point prevalence of bovine fasciolosis and the influence of chemotherapy on the milk yield in a lactating bovine population from the district of Toba Tek Singh. Pakistan Journal of Helminthology 85, 334–338.CrossRefGoogle Scholar
Malone, JB and Craig, TM (1994) Cattle liver flukes: risk assessment and control. The Compenium: Food Animal Parasitology 1, 747–753.Google Scholar
Manly, BFJ (2006) Randomization, bootstrap and Monte Carlo methods in biology. 2nd edn. Wyoming, EUA, 480 pp.Google Scholar
Mas-Coma, S, Valero, MA and Bargues, MD (2009) Chapter 2. Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Advances in Parasitology 69, 41–146.CrossRefGoogle ScholarPubMed
Mazeri, S, Rydevik, G, Handel, I, Bronsvoort, BMD and Sargison, N (2017) Estimation of the impact of Fasciola hepatica infection on time taken for UK beef cattle to reach slaughter weight. Nature Scientific Report 7, 7319.CrossRefGoogle ScholarPubMed
Mehmood, K, Zhang, H, Sabir, AJ, et al. (2017) A review on epidemiology, global prevalence and economical losses of fasciolosis in ruminants. Microbiology and Pathogeny 109, 253–262.CrossRefGoogle ScholarPubMed
Molento, MB, Bennema, S, Bertot, J, Pritsch, IC and Arenal, A (2018) Bovine fascioliasis in Brazil: economic impact and forecasting. Veterinary Parasitology: Regional Studies and Reports 12, 1–3.Google ScholarPubMed
Monteiro Noel, KM, Fontes-Pereira, AMA, Castillo, R, Fernández, O, Fonseca, O and Percedo, MI (2013) Prevalencia de hígados de comisados y pérdidas económicas por Fasciola sp. en Huambo, Angola. Revista de Salud Animal 35(2), 89–93.Google Scholar
Oliveira, DR, Ferreira, DM, Stival, CC, Romero, F, Cavagnolli, F, Kloss, A, Araújo, FB and Molento, MB (2008) Triclabendazole resistance involving Fasciola hepatica in sheep and goats during an outbreak in Almirante Tamandare, Parana, Brazil. Brazilian Journal of Veterinary Parasitology 17, 149–153.Google ScholarPubMed
Oyarzún-Ruiz, P, Alvelo, C, Vera, F and Moroni, M (2019) Histopathological findings of Fasciola hepatica infection in non-native European hare (Lepus europaeus) in Southern Chile. Brazilian Journal of Veterinary Parasitology 28, 145–150.Google Scholar
Periago, MV, Valero, MA, Panova, M and Mas-Coma, S (2006) Phenotypic comparison of allopatric populations of Fasciola hepatica and Fasciola gigantica from European and African bovines using a computer image analysis system (CIAS). Parasitology Research 99, 368.CrossRefGoogle Scholar
Pritsch, IC and Molento, MB (2018) Recount of reported cases of human fascioliasis in Brazil over the last 60 years. Journal of Tropical Pathology 47, 1–11.Google Scholar
Pritsch, IC, Stanula, ECA, dos Anjos, A, Bertot, JA and Molento, MB (2019) Fascioliasis in buffaloes: a 5-year forecast analysis of the disease based on a 15-year survey in Brazil. Brazilian Journal of Veterinary Parasitology 28, 410–415.Google ScholarPubMed
Rahmeto, A, Fufa, A, Mulugeta, B, Solomon, M, Bekele, M and Alemayehu, R (2010) Fasciolosis: prevalence, financial losses due to liver condemnation and evaluation of a simple sedimentation diagnostic technique in cattle slaughtered at Hawassa Municipal abattoir, southern Ethiopia. Ethiopian Veterinary Journal 14, 39–51.Google Scholar
Raunelli, F and Gonzalez, S (2009) Strategic control and prevalence of Fasciola hepatica in Cajamarca. Peru: A pilot study. Journal of Applied Research and Veterinary Medicine 7, 145–152.Google Scholar
Ross, JG (1968) The life span of Fasciola hepatica in cattle. Veterinary Record 82, 587–589.Google Scholar
Ross, JG (1970) The economics of Fasciola hepatica infections in cattle. British Veterinary Journal 126, 13–15.Google ScholarPubMed
Schweizer, G, Braun, U, Deplazes, P and Torgerson, PR (2005) Estimating the financial losses due to bovine fasciolosis in Switzerland. Veterinary Record 157, 188–193.CrossRefGoogle ScholarPubMed
Silva, AEP, Freitas, CC, Dutra, LV and Molento, MB (2016) Assessing the risk of bovine fasciolosis using linear regression analysis for the state of Rio Grande do Sul, Brazil. Veterinary Parasitology 217, 7–13.CrossRefGoogle Scholar
Silva, AEP, Freitas, CC, Dutra, LV and Molento, MB (2020) Correlation between climate data and land altitude for Fasciola hepatica infection in cattle in Santa Catarina, Brazil. Brazilian Journal of Veterinary Parasitology 29(3), e008520.Google ScholarPubMed
Swai, ES and Ulicky, E (2009) An evaluation of the economic losses resulting from condemnation of cattle livers and loss of carcass weight due to Fasciolosis: a case study from Hai town abattoir, Kilimanjaro region, Tanzania. Livestock Research and Rural Development 21, 186.Google Scholar
Taibi, A, Aissi, M, Harhoura, K, Zenia, S, Zait, H and Hamrioui, B (2019) Evaluation of Fasciola hepatica infections in cattle in Northeastern Algeria and the effects on both enzyme and hepatic damage, confirmed by scanning electron microscopy. Acta Parasitology 64, 112–128.CrossRefGoogle ScholarPubMed
Torgerson, P and Claxton, J (1999) Epidemiology and control. pp. 113–139in Dalton, JP (Ed.) Fasciolosis. 1st edn.Oxford, London, CABI Press.Google Scholar
Trivilin, LO, Sousa, DR, Carvalho Nunes, L, Sousa Rocha, N and Martins, IVF (2014) Histopathology aspects and fibrosis evaluation of bovine naturally infected livers by Fasciola hepatica. Archives of Veterinary Science 19, 61–69.CrossRefGoogle Scholar
Vynnycky, E and White, R (2010) Introduction to infectious disease modelling. 368 pp. Oxford University Publishing.Google Scholar