Determination of exposure to Fasciola hepatica in horses from Uruguay using a recombinant based ELISA

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(1)Veterinarni Medicina, 60, 2015 (9): 483–488. Original Paper. doi: 10.17221/8439-VETMED. Determination of exposure to Fasciola hepatica in horses from Uruguay using a recombinant-based ELISA J. Sanchis1, J. Suarez2, G.V. Hillyer3, J.A. Hernandez2, M.A. Solari4, C. Cazapal-Monteiro2, A.M. Duque de Araujo2, L.M. Madeira de Carvalho5, A. Paz-Silva2, R. Sanchez-Andrade2, M.S. Arias2 1. Parasitology Department, University of República (Regional Norte), Salto, Uruguay Veterinary Faculty, Santiago de Compostela University, Lugo, Spain 3 School of Medicine, University of Puerto Rico, San Juan, USA 4 Parasitology Department, Veterinary Laboratories Division (DILAVE), Uruguay 5 Faculty of Veterinary Medicine, Technical University of Lisbon, Lisbon, Portugal 2. ABSTRACT: The risk of exposure to Fasciola hepatica in horses from Uruguay was evaluated using ELISA and a recombinant surface protein (FhrAPS). Blood samples were collected from 368 horses from different districts. Detection of antibodies and the seasonal IgG pattern against the trematode was also established. The overall seroprevalence was 54% (ranging 23% November to 93% December). Significantly higher values were observed in the Anglo-Arab horses (86%) and in those older than xix year (63%). No sex- or origin-differences were observed. Two primary risk periods for infection in Uruguay have been identified, the end of spring and autumn. Exposure to the fluke should be taken into account among those horses feeding on pastures grazed by ruminants. Using FhrAPS-ELISA, helpful information concerning the risk of horses to the infection by trematode can be obtained. This test allows the opportunity to compare the results achieved in different laboratories by minimising specific regional effects. Keywords: Fasciola hepatica; equine; Uruguay; sensitisation; FhrAPS. Fasciolosis (Fasciola hepatica) is a widespread trematodosis among grazing animals, which become infected by consuming forage or drinking water contaminated by metacercariae, the infective stages that are released by amphibious snails (Lymnaea spp.) acting as their intermediate hosts (Marcos et al. 2008; Sanchis et al. 2011). The effective control of infection in ruminants is based on accurate diagnosis and successful deworming. Currently, the detection of Fasciola-infected animals is based on clinical observations, copromicroscopical tests and/or immunoenzymatic probes (Arias et al. 2012b; Rojo-Vazquez et al. 2012). The majority of studies performed on horses experi-. mentally infected with F. hepatica metacercariae showed that patency (adult flukes) is only reached by a small proportion of the infective stages (Grelck et al. 1977), whereas faecal egg-output has been observed after a period longer than 14–15 weeks post-infection (Soule et al. 1989). This limits the usefulness of faecal examination in the diagnosis of equine fasciolosis, which is therefore habitually discarded. Infection by Fasciola compromises liver function, but clinical signs, such as low-level jaundice, anaemia, and intermittent diarrhoea are not often observed and well-interpreted in equine disease; therefore, liver fluke infection remain undiagnosed. Partially supported by the Xunta de Galicia, Spain (Research Project No. 10MDS261023PR) and Ministerio de Economia y Competitividad, Spain; FEDER (Research Project No. AGL2012-34355), and complies with the current laws for Animal Health Research in Spain.. 483.

(2) Original Paper. Veterinarni Medicina, 60, 2015 (9): 483–488 doi: 10.17221/8439-VETMED. unless serological methods of detection are used (Haridy et al. 2007; Awad et al. 2009). Because horses fail to develop experimental infections, they are frequently considered resistant to infection with Fasciola (Nansen et al. 1975; Alves et al. 1988; Soykan and Oge 2012). The identification of horses exposed to F. hepatica using immunoenzymatic probes has previously been proposed (Acici et al. 2013). In a recent study, an ELISA with the FhrAPS recombinant surface antigen was used to demonstrate the high seroprevalence of fasciolosis among horses feeding on grasslands formerly pastured by ruminants (Arias et al. 2012a). Because horses and cattle regularly share the same pastures in Uruguay, exposure to the liver trematode in equines from this country has been evaluated in this study.. MATERIAL AND METHODS Area of study. This study was performed from March 2011 to March 2012 in Uruguay (30°05'00'' to 34°58'00'' S, 53°12'00'' to 58°43'40'' W), where cattle breeding is the most important agrarian economic activity. This country has a moderate climate, characterised by significant rainfall in all seasons and small annual variations in temperature, with more than four months averaging above 10 °C (Figure 1). Under these conditions, forage growth occurs throughout the year, and ruminants, including cattle and sheep, are extensively reared (Sanchis et al. 2014). Because of the absence of geographical barriers, no differences in the climate conditions are expected throughout the country (Eleftheratos et al. 2011). Rainfall – – – RH. 120. MaxT. MinT. 100 mm 3, %, °C. 80 60 40. Mar. Feb. Jan 12. Dec. Nov. Oct. Sep. Ago. Jul. Jun. May. Apr. 0. Mar 11. 20. Figure 1. Monthly changes in climate parameters in Uruguay. MaxT = maximal temperature (°C); MinT = minimal temperature (°C); RH = relative humidity (%). 484. Analysis of the seroprevalence of horse fasciolosis. A total of 368 horses representing the AngloArab Breed, Uruguay Creole, Arabian Pure Breed and English Pure Breed from 10 out of 19 districts were bled by veterinary clinicians during equestrian festivals (Table 1). Several horses were bled prior to purchase. The horses were grouped based on their age as follows: G1 (six year) (Table 2). According to their housing, two categories were established: indoors, which included the AngloArabs and English Pure Breed, and outdoors, which included the Uruguay Creoles and Arabians. FhrAPS-ELISA. The presence of IgG antibodies against the liver trematode F. hepatica was evaluated using an ELISA with the FhrAPS recombinant surface protein. The ELISA was 83% sensitive and 86% specific (Arias et al. 2012a). In brief, 1 µg/ml FhrAPS was added to the wells of microtitre plates containing sera (tested in duplicate) diluted 1/100 in 10% PTL (PBS, 0.3% Tween 20 and 10% skimmed milk) and horseradish peroxidase conjugated to rabbit anti-horse IgG (Nordic Immunology Laboratories, The Netherlands) at a 1/1000 dilution. Substrates consisting of 10 mg of ortho-phenylenediamine in 12 ml of citrate buffer and 10 µl of 30% H2O2 were then added to each well. The plates were incubated in the dark for 10 min at room temperature. Finally, the absorbances at 492 nm were measured using a spectrophotometer (Titertek Multiskan). Positive and negative controls were added to each ELISA plate. Serum samples from horses passing F. hepatica by faeces were utilised as positive controls, while the samples collected from three-month-old foals (n = 44) without access to grass or fresh forage served as negative controls. The cut-off value was taken as the mean of the absorbances belonging to the negative controls plus three standard deviations, which was calculated to be 0.347. Statistical analysis. All tests were performed using SPSS for Windows (20.0, SPSS Inc., Chicago, IL, USA). The true prevalence was calculated by taking the sensitivity, specificity and apparent prevalence values into account. The percentages of the true seroprevalence were expressed as the value and the 95% confidence interval and were analysed using the χ2 test. Differences were considered significant at P < 0.05. Correlations among the different parameters were assessed using Pearson’s correlation test. The possible relationship between breed, age, and seroprevalence was estimated by calculating the odds ratio (OR) values (Thrusfield 2005)..

(3) Veterinarni Medicina, 60, 2015 (9): 483–488. Original Paper. doi: 10.17221/8439-VETMED Table 1. Seroprevalence of fasciolosis in horses from the different departments of Uruguay using the FhrAPS-ELISA. The results are expressed as the prevalence (P) and the 95% confidence interval Department. Positive to the FhrAPS-ELISA. Localisation. n. P (%). 95% CI. Rocha. Southeast. 25. 72. 54–90. Colonia. Southwest. 7. 71. 38–100. Lavalleja. Southeast. 27. 63. 45–81. North. 28. 61. 43–79. Paysandú. Northwest. 80. 61. 51–72. Artigas. Northwest. 59. 51. 38–64. Cerro Largo. Northeast. 56. 46. 33–59. Montevideo. South. 53. 45. 32–59. Rivera. North. 11. 45. 16–75. Canelones. South. 22. 41. 20–61. 368. 54. 49–59. Tacuarembó. Total. RESULTS Seasonal dynamics of IgG antibodies against F. hepatica After slight variations, the IgG values increased significantly from June and peaked in August (Figure  2). Antibodies increased again from October to December (end of spring-beginning of summer), when the highest counts were recorded, and then decreased in March.. Seroprevalence The percentage of horses positive by FhrAPSELISA was 54% (95% CI 49–59), with the lowest val100. Prevalence. 90. 0.7. IgG. 0.6. 80. (%). 60. 0.4. 50. 0.3. 40 30. 0.2. 20. 0.1. Mar. Feb. Jan 12. Dec. Nov. Sep. Oct. Jul. Ago. Jun. May. Apr. Mar 11. 10 0. OD (490 nm). 0.5. 70. ues in the northern districts and the highest values in the southern districts (Table 1); however, these differences were not significant (χ 2 = 12.178, P = 0.203). The percentage of seropositivity varied from 47% in the foals to 63% in horses older than six year (P < 0.05) (Table 2). The oldest equines reached an OR value of 1.7. Based on the Pearson’s test, the seroprevalence and age were significantly correlated (r = 0.243, P = 0.007). For breed, the AngloArabs reached significantly higher seroprevalence values (Table 2), whereas the lowest seropositivity percentage values were recorded for the Creoles (P < 0.05). The OR values were 5.4 for the AngloArabs and 1.4 for the Arabians. Although the mares showed higher percentages of seroprevalence than the stallions, significant differences were not observed (P > 0.05). No significant differences based on housing were observed (P > 0.05). The seroprevalence rapidly increased between November and December, when the highest values were achieved. A slow increase during winter (June-August) was observed, and the percentages of seropositivity peaked again. These monthly variations were significant (χ2 = 51.033, P = 0.001).. 0. Figure 2. Monthly variations in the seroprevalence of fasciolosis and IgG antibodies against the FhrAPS recombinant surface protein in horses from Uruguay (n= 368).. DISCUSSION A serological survey in horses from 10 out of the 19 departments of Uruguay was here performed in order to gain information regarding equine fasciolosis in this country. By analyzing the presence of serum IgG antibodies against the FhrAPS re485.

(4) Original Paper. Veterinarni Medicina, 60, 2015 (9): 483–488 doi: 10.17221/8439-VETMED. Table 2. Seroprevalence of fasciolosis in horses from the different departments of Uruguay using the FhrAPS-ELISA according to intrinsic factors. The results are expressed as the prevalence (P), 95% confidence interval (CI), and odds ratio (OR) n Age (year). Seroprevalence P (%). 95% CI. value. 95% CI. <3. 88. 47. 42–52. 0.7. 0.4–1.1. 3– 6. 163. 52. 47–57. 0.9. 0.6–1.3. >6. 117. 63. 58–68. 1.7. 1.1–2.7. 2. Statistics Anglo-Arab Breed. Arabian Pure Breed. χ = 6.188, P = 0.045. 21. 86. 82–89. 5.4. 1.6–18.8. 45. 62. 57–67. 1.4. 0.8–2.7. Uruguay Creole. 111. 50. 45–55. 0.8. 0.5–1.2. English Pure Breed. 191. 52. 0.8. 0.5–1.2. 47–57. χ2 = 10.969, P = 0.012. Statistics Sex. mares. 196. 55. stallions. 172. 53. 50–60 48–58 Statistics. combinant surface protein, exposure to F. hepatica was demonstrated in more than half of the sampled horses. Although the seroprevalence of fasciolosis increased from north to south, significant differences were not observed, which may partially be due to the absence of geographical barriers that allow for the development of the liver trematode (Nari et al. 1986). The presence of antibodies against F. hepatica was age-related, with the lowest values in the youngest horses and the highest values in the oldest animals. These data are consistent with previous results suggesting a cumulative effect of infection throughout the life of the horse (Arias et al. 2012a; Getachew et al. 2010). Previous investigations in Uruguay indicate that calves exhibit the highest seroprevalence against F. hepatica crude antigens (Sanchis et al. 2011). One unexpected result was the elevated percentages of positivity in the FhrAPS-ELISA among the Anglo-Arabs, because the owners stated that these horses remained stabled throughout the majority of the day and therefore have no or limited access to grass. Likewise, the highest seroprevalences were obtained among the English Pure Breed, Arab and Anglo-Arab equines from Spain (85%, 75% and 60%, respectively). However, significant differences were not observed in the seropositivity regarding the equine breed (Arias et al. 2012a). It is possible that the horses are allowed access to paddocks for exercise, which may increase the 486. OR. χ2 = 0.096, P = 0.757. risk of exposure to the metacercariae. By contrast, the lowest seropositivity values were found in the Uruguay Creoles, which are horses that receive less care and attention, in theory at least. In a recent survey, the lowest seroprevalence in Crossbreds from Uruguay has been associated with cattle that pasture on nutrient-poor grasslands, which become dry during summer, thereby reducing the risk of infection (Sanchis et al. 2014). Because it is difficult for Fasciola to reach the adult stage in horses, the excretion of F. hepatica eggs in the faeces occurs only occasionally; therefore, the role of horses as potential trematode reservoirs has been underestimated (Arias et al. 2012a). However, the delay in mature trematode development allows the immune system to stay in contact with the trematodes and antigens, thereby eliciting a strong humoral immune response (Phiri et al. 2006). Accordingly, the analysis of horse serum samples provides useful information of the risk of F. hepatica infection. The analysis of the seasonal pattern of IgG antibodies against the FhrAPS recombinant surface protein showed increased incrementally in the autumn and then significantly in the winter. Exposure to F. hepatica requires the ingestion of forage and/ or water containing metacercariae, and the presence of these infective stages depends on their release by the snails acting as intermediate hosts, as well as on their capability to survive under adverse climate conditions. Because of the decrease.

(5) Veterinarni Medicina, 60, 2015 (9): 483–488. Original Paper. doi: 10.17221/8439-VETMED. in temperature during the autumn (March-June), development of the Fasciola stages inside the snails surviving the summer is delayed; therefore, the cercariae are slowly released by the intermediate hosts, which may take up to four months (Nari et al. 1986; Acosta 1993). Temperature values of less than 10 °C together with a reduction of rainfall and relative humidity decrease the activity of the snails; therefore, the lowest IgG counts were observed in September. The temperature rises in the spring (SeptemberDecember), which increases the activity of Lymnaea intermediate hosts (Castro et al. 2001), and thus the risk to horses that ingest the metacercariae with herbage. This may explain why the highest IgG values were observed in the horses at the end of the spring (December). Fasciolosis is endemic in cattle from Uruguay, as shown by 46% (26–67%) liver seizure for Fasciola in 2007 (INIA-INAC 2009). An overall seroprevalence of 67% has been reported (Sanchis et al. 2014), whereas the percentage of cattle passing eggs in the faeces reached 15% in some areas. In this study, the presence of antibodies against F. hepatica in 54% of horses from Uruguay was detected. These results are consistent with those obtained in NW Spain, an endemic area where the seroprevalence of fasciolosis is 71% in cattle, 68% in sheep and 60% in horses, as demonstrated by FhrAPS-ELISA (Arias et al. 2007; Paz-Silva et al. 2007; Arias et al. 2012a). In conclusion, analysis of horse sera for the presence of antibodies against F. hepatica is useful for determining the distribution of infection. Two primary risk periods for F. hepatica liver fluke infection in Uruguay were identified. The first period is the end of the spring, and the second period is in the autumn. Exposure to the liver fluke should be taken into account among those horses feeding on pastures also grazed by ruminants. The FhrAPSELISA gives useful information about the risk of liver fluke infection for horses. This assay minimises the impact of specific regional effects, and in this way, the results obtained in different laboratories can be compared.. Acknowledgement Partially supported by the Xunta de Galicia, Spain (Research Project No. 10MDS261023PR) and Ministerio de Economia y Competitividad, Spain;. FEDER (Research Project No. AGL2012-34355), and complies with the current laws for Animal Health Research in Spain. Dr. Arias has received a fellowship from the “Parga Pondal” Research Program (XUGA, Spain). Jaime Sanchis received a research grant (Edmundus 17; Banco de Santander– USC, Spain) for his PhD thesis at the University of Santiago de Compostela (Spain). We thank Mrs. B. Valcarcel for preparing and editing the manuscript.. REFERENCES Acici M, Bolukbas CS, Gurler AT, Umur S, Buyuktanir O (2013): Seroprevalence of fasciolosis in equines of the Black Sea Region, Turkey. Journal of Equine Veterinary Science 33, 62–66. Acosta D (1993): Epidemiology and control of F. hepatica in Uruguay (in Spanish). In: Nari A, Fiel C (eds.): Parasitic Diseases of Economic Importance in Cattle: Epidemiological Basis for Prevention and Control. Hemisferio Sur, Uruguay. 233–256. Alves RM, van Rensburg LJ, van Wyk JA (1988): Fasciola in horses in the Republic of South Africa: a single natural case of Fasciola hepatica and the failure to infest ten horses either with F. hepatica or Fasciola gigantica. Onderstepoort Journal of Veterinary Research 55, 157–163. Arias M, Morrondo P, Hillyer GV, Sanchez-Andrade R, Suarez JL, Lomba C, Pedreira J, Diaz P, Diez-Banos P, Paz-Silva A (2007): Immunodiagnosis of current fasciolosis in sheep naturally exposed to Fasciola hepatica by using a 2.9 kDa recombinant protein. Veterinary Parasitology 146, 46–49. Arias MS, Pineiro P, Hillyer GV, Francisco I, Cazapal-Monteiro CF, Suarez JL, Morrondo P, Sanchez-Andrade R, Paz-Silva A (2012a): Enzyme-linked immunosorbent assays for the detection of equine antibodies specific to a recombinant Fasciola hepatica surface antigen in an endemic area. Parasitology Research 110, 1001–1007. Arias MS, Martinez-Carrasco C, León-Vizcaino L, Paz-Silva A, Diez-Banos P, Morrondo P, Alonso F (2012b): Detection of antibodies in wild ruminants to evaluate exposure to liver trematodes. Journal of Parasitology 98, 754–759. Awad WS, Ibrahim AK, Salib FA (2009): Using indirect ELISA to assess different antigens for the serodiagnosis of Fasciola gigantica infection in cattle, sheep and donkeys, Research in Veterinary Science 86, 466–471. Castro O, Heinzen T, Carballo M (2001): Dynamics of Lymnaea viator infection with F. hepatica in natural conditions in Uruguay (in Spanish). Veterinaria Uruguay 36, 13–20. Eleftheratos K, Tselioudis G, Zerefos C, Nastos P, Douvis C, Kapsomenakis I (2011): Observed and predicted cli-. 487.

(6) Original Paper. Veterinarni Medicina, 60, 2015 (9): 483–488 doi: 10.17221/8439-VETMED. mate changes in Uruguay and adjacent areas. Journal of Geosciences 45, 83–90. Getachew M, Innocent GT, Trawford AF, Reid SWJ, Love S (2010): Epidemiological features of fasciolosis in working donkeys in Ethiopia. Veterinary Parasitology 169, 335–339. Grelck H, Horchner F, Wohrl H (1977): Experimental infection of horses with Fasciola hepatica. Berliner und Munchener Tierarztliche Wochenschrift 90, 371–373. Haridy FM, Morsy GH, Abdou NE, Morsy TA (2007): Zoonotic fascioliasis in donkeys: ELISA (Fges) and postmortum examination in the Zoo, Giza, Egypt. Journal of the Egyptian Society of Parasitology 37, 1101–1110. INIA-INAC, Instituto Nacional de. Investigacion Agropecuaria-Instituto Nacional de Carnes (2009): Second Audit of the Quality of the meat chain of beef from Uruguay (in Spanish). INAC, Uruguay. 46 pp. Marcos LA, Terashima A, Gotuzzo E (2008): Update on hepatobiliary flukes: fascioliasis, opisthorchiasis and clonorchiasis. Current Opinion in Infectious Diseases 21, 523–530. Nansen P, Andersen S, Hesselholt M (1975): Experimental infection of the horse with Fasciola hepatica. Experimental Parasitology 37, 15–19. Nari A, Cardozo H, Solari MA, Petraccia C, Acosta D (1986): Preliminary study on the development of Limnaea viatrix D’Orbigny (1835) under controlled conditions of temperature and humidity. Veterinaria 22, 13–17. Paz-Silva A, Hillyer GV, Arias MS, Sanchez-Andrade R, Pedreira J, Suarez JL, Lomba C, Diaz P, Francisco I, DiezBanos P, Morrondo P (2007): A cross-sectional study of fascioliasis in autochthonous cattle from NW Spain by. using a 2.9-kDa recombinant protein. Journal of Applied Research in Veterinary Medicine 5, 52–56. Phiri IK, Phiri AM, Harrison LJ (2006): Serum antibody isotype responses of Fasciola-infected sheep and cattle to excretory and secretory products of Fasciola species. Veterinary Parasitology 141, 234–242. Rojo-Vazquez FA, Meana A, Valcarcel F, Martinez-Valladares M (2012): Update on trematode infections in sheep. Veterinary Parasitology 189, 15–38. Sanchis J, Miguelez S, Solari MA, Pineiro P, Macchi MI, Maldini G, Venzal J, Morrondo P, Diez-Banos P, SanchezAndrade R, Paz-Silva A, Arias MS (2011): Seroprevalence of bovine fasciolosis in department Salto (Uruguay). Revista Ibero-Latinoamericana de Parasitologia 70, 163–171. Sanchis J, Hillyer G, Madeira de Carvalho LM, Macchi MI, Gomes C, Maldini G, Siltwell G, Venzal JM, Paz-Silva A, Sanchez-Andrade R, Arias MS (2014): Update on fasciolosis in extensively managed cattle from Uruguay and Portugal by using a recombinant protein-based ELISA. Archivos de Medicina Veterinaria 47, 201–208. Soule C, Boulard C, Levieux D, Barnouin J, Plateau E (1989): Experimental equine fascioliasis: evolution of serologic, enzymatic and parasitic parameters. Annals of Veterinary Research 20, 295–307. Soykan E, Oge H (2012): The prevalence of liver trematodes in equines in different cities of Turkey. Turkiye Parazitoloji Dergisi 36, 152–155. Thrusfield M (ed.) (2005): Veterinary Epidemiology. Blackwell Science Ltd, Oxford. 584 pp. Received: 2014–05–28 Accepted after corrections: 2015–08–11. Corresponding Author: Maria Sol Arias, Santiago de Compostela University, Veterinary Faculty, Animal Pathology Department, Parasitology and Parasitic Diseases, Epidemiology and Zoonoses, Equine Diseases Study Group, COPAR (GI-2120), 27002 Lugo, Spain E-mail: mariasol.arias@usc.es. 488.

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