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Bovine fasciolosis: Control strategies based on the location of Galba truncatula habitats on farms Gabriela Knubben-Schweizer a,∗ , Paul R. Torgerson b a Clinic for Ruminants with Ambulatory and Herd Health Services at the Centre for Clinical Veterinary Medicine, Ludwig-Maximilians-University Munich, Sonnenstrasse 16, 85764 Oberschleissheim, Germany b Section of Epidemiology, Vetsuisse Faculty, University of Zurich, Winterthurerstrasse 270, 8057 Zurich, Switzerland
a r t i c l e
i n f o
Keywords: Fasciola hepatica Cattle Galba truncatula Snail habitats Control Pasture management
a b s t r a c t Infection of livestock with Fasciola hepatica is a worldwide, economically important and increasing problem. Even though, bovine fasciolosis can be a disease associated with particular regions, there are usually epidemiological issues on individual farms. For this reason, it is recommended to find the source of infection by examination of definite hosts and pastures on a farm. The following factors which promote the transmission of bovine fasciolosis are usually found: (A) Snail habitats are present on pastures used for young stock (prior to first calving) or dry cows only. Pastures for dairy cows are not affected. (B) Snail habitats are present on all pastures for dairy cows. (C) Snail habitats are present on single pastures used for dairy cows. (D) Snail habitats are present on hayfields. For each of these epidemiological situations an individual control strategy is advised. When a control strategy is tailored according to the specific epidemiology found on the individual farm, egg shedding and F. hepatica-seroprevalence can be reduced significantly. This approach can support the responsible use of the available flukicides. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Infection of livestock with Fasciola hepatica is a worldwide, economic problem with increasing importance (Fairweather, 2009). In the north of Germany for instance, the prevalence was previously reported to be 0.6% (Epe et al., 2004), while more recent studies have found mean
∗ Corresponding author at: Klinik für Wiederkäuer mit Ambulanz und Bestandsbetreuung, LMU München, Sonnenstrasse 16, 85764 Oberschleissheim, Germany. Tel.: +49 89 2180 78850; fax: +49 89 2180 78851. E-mail address: [email protected] (G. Knubben-Schweizer).
herd prevalences of between 32.2% and 69.1% (Koch, 2005; Rabeler, 2011; Kuerpick et al., 2012). Despite strategic treatments with different flukicides and sophisticated forecast models, high and even increasing prevalences have been reported elsewhere (Bennema et al., 2009; Rapsch et al., 2006). In addition to likely increases in disease prevalence, future fluke control will also have to deal with the threat of drug (i.e. triclabendazole) resistance (Fairweather, 2011). Economic losses due to bovine fasciolosis can be considerable. In Switzerland for example, such losses have been estimated at several thousand Euros per affected farm (Schweizer et al., 2005). Consequently, control of this parasite is important for economic reasons in addition to reasons of animal welfare.
http://dx.doi.org/10.1016/j.vetpar.2014.12.019 0304-4017/© 2014 Elsevier B.V. All rights reserved.
Please cite this article in press as: Knubben-Schweizer, G., Torgerson, P.R., Bovine fasciolosis: Control strategies based on the location of Galba truncatula habitats on farms. Vet. Parasitol. (2015), http://dx.doi.org/10.1016/j.vetpar.2014.12.019
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Of the several strategies for the control of bovine fasciolosis described, in practice usually strategic anthelmintic control is used with flukicide treatment time and interval depending on the climatic zone (Armour, 1975; Boray, 1971, 1972; Harris and Charleston, 1971; Schneider et al., 1975; Torgerson and Claxton, 1999; Whitehead, 1976). A variety of fasciolicides is available for the treatment of bovine fasiolosis: triclabendazole, albendazole, oxyclozanide, clorsulon, nitroxynil, rafoxanide or oxfendazole (Fairweather, 2011; Gomez-Puerta et al., 2012; MartínezValladares et al., 2010). Of all these agents, triclabendazole is the most effective against immature stages of the parasite, which makes it the drug of choice for the treatment of acute fasciolosis, which is more commonly seen in sheep than in cattle. Due to increasing resistance against triclabendazole (Fairweather, 2011), there are efforts to develop new drugs which are efficacious against immature parasites, but results to date have been disappointing (Fairweather, 2011). Combining compounds can help to increase efficacy against immature stages. For example the combination of clorsulon (2.0 mg/kg) and nitroxynil (10.2 mg/kg) reached an efficiency of 95% against 2-weekold flukes and 99% against 4-week-old flukes (Hutchinson et al., 2009). One of the limits for the use of flukicides in cattle – especially dairy cows – is the legislation regulating drug licencing differing from country to country. In Switzerland for instance, only one clorsulon formulation is authorized (Ivomec® Plus, Biokema SA), but its use is restricted to non-lactating animals. Furthermore, no nitroxynil drug is registered. Instead, triclabendazole is authorized for dairy cows, with a withdrawal time of 12 days for milk (Endex® 19.5%, Novartis AG), whereas it is not authorized in Germany for use in lactating animals. Therefore, practitioners have a responsibility in reducing and optimizing the administration of flukicides. This can be supported by taking the individual epidemiological situation on the farm into account. This review is linked to the EVPC scientific symposium “The two faces of Veterinary Parasitology: from biology to clinical aspects” (2012 annual EVPC meeting León, Spain). The topic addressed is a revised view on control of bovine fasciolosis in the field from the point of view of a practitioner. Therefore, the approach is practical and can help reduce flukicide treatment. 2. Control of bovine fasciolosis based on the location of the snail habitats The transmission of F. hepatica is linked to the intermediate host – a number of species of amphibious snails. In Europe Galba truncatula is a common intermediate host. This snail is found in moist, especially smooth and firm clay soils. Preferred habitats are shallow water, ditches, banks of slowly-moving streams, spring swamps and reeds (Frömming, 1956; Mehl, 1932; Schweizer et al., 2007). In addition, wells (Fig. 1) and cattle watering tanks can provide suitable habitats (Petzold, 1989; Schweizer et al., 2007). The occurrence of G. truncatula and the transmission of F. hepatica depend not only on moisture and soil condition but also on temperature and solar radiation (Armour,
1975; Christensen et al., 1976; Kendall and McCullough, 1951; Ollerenshaw, 1959; Petzold, 1989; Ross, 1970; Thomas, 1883). Although suitable meteorological and geographical conditions may promote transmission on a regional scale, there are usually epidemiological factors that increase the risk of bovine fasciolosis on individual farms (Schweizer et al., 2007). In a survey on 70 farms with a known herd health problem of bovine fasciolosis in Switzerland, 40 farms only had one suitable snail habitat on their grasslands (Schweizer et al., 2007). Thus, in almost 60% of the farms visited, an extensive spatial distribution of infectious grasslands could be ruled out. Additionally, in countries such as Switzerland, Austria or Germany, where young stock are often kept on separate pastures from dairy cows (e.g. alpine pastures) it is possible, that these animals become infected when grazing on these separate pastures. If there are no snail habitats on the home farms, these animals do not get re-infected after being turned off the young stock pastures. Thus a strategic anthelmintic treatment of all animals every year is not always cost-effective. For this reason, the following course of action as detailed in Fig. 2, is recommended, in order to control fasciolosis in cattle (Knubben-Schweizer et al., 2011): 1. In order to make a detailed diagnosis of the herd health problem for the first time on a farm1 , it is necessary to detect the affected group of cattle. The control differs if young stock only is infected or if dairy cows repeatedly acquire fasciolosis throughout their productive life. For this reason laboratory tests should be performed in at least five young animals prior to first calving and five dairy cows taking into account the following drawbacks of fecal examination and serology:
- Fecal examination: the parasite can live for up to 26 months in the liver of cattle (Ross, 1968). If young stock are infected on separate pastures (e.g. alpine pastures) and are not treated, the parasite potentially sheds eggs throughout the first lactation of the animal. Thus, the finding of F. hepatica eggs in first lactation cows does not imply that there must be infectious pastures on the home-farm. The infection might have arisen from young stock pastures. Therefore to find the source of infection (young stock pastures vs. dairy cow pastures) the fecal examination of first lactation cows is not useful. - Serology: With serology the infection can be diagnosed early in the prepatent period of the infection. The disadvantage though is that antibodies persist 6–9 (even to 18) months after elimination of the parasites (Hutchinson and Macarthur, 2003). Infection acquired in the first or second year of life of a definite host can therefore still be detected during the second lactation of a dairy cow.
1 In order to monitor the prevalence (e.g. in a control program) fecal samples of 5 animals can be used. The prevalence resulting from 5 fecal samples is associated with the sero-prevalence resulting from the examination of a blood sample from all animals (Knubben-Schweizer et al., 2010). Nevertheless we recommend to repeatedly examine serologically all animals of a group (e.g. dairy cows) for prevalence monitoring due to better comparability.
Please cite this article in press as: Knubben-Schweizer, G., Torgerson, P.R., Bovine fasciolosis: Control strategies based on the location of Galba truncatula habitats on farms. Vet. Parasitol. (2015), http://dx.doi.org/10.1016/j.vetpar.2014.12.019
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Fig. 1. A drinking trough (well) harboring Galba truncatula in a pasture for young stock.
In conclusion in young stock, either fecal examination or serology can be used. Dairy cows should not be sampled at all during the first lactation, fecal examination can be conducted in their second and subsequent lactation while serology is recommended for cows from their third lactation onwards. As a rule of thumb it makes sense to sample the oldest animals that are the longest in the herd. Furthermore, it is recommended to examine all brought in animals immediately after purchase either by fecal examination2 or by serology in order to treat them appropriately before contamination of a pasture that may have suitable snail habitats.
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In order to enhance the sensitivity of the coproscopy we recommend examining 2 × 10 g of feces from the same sample (Rapsch et al., 2006).
2. In a second step the pastures and possibly hay fields (all forage acreage3 should be taken into account depending on the results of the laboratory examinations) must be examined for potential snail habitats and the location of these must be assessed. As the farmer knows the wettest areas on his premises, his assistance is necessary. Furthermore, the use of plant indicators for positive sites of G. truncatula can be very helpful (Rondelaud et al., 2011). Four scenarios of snail habitat sites are possible (KnubbenSchweizer et al., 2010): (A) Snail habitats are present on pastures used for young stock (prior to first calving) or dry cows only. Pastures for dairy cows are not affected.
3 Especially if fresh grass is fed from them. It has to be kept in mind though, that also hay and to the authors’ experience very seldom even grass silage can transmit F. hepatica.
Please cite this article in press as: Knubben-Schweizer, G., Torgerson, P.R., Bovine fasciolosis: Control strategies based on the location of Galba truncatula habitats on farms. Vet. Parasitol. (2015), http://dx.doi.org/10.1016/j.vetpar.2014.12.019
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Fig. 2. Follow-up of the herd health problem “bovine fasciolosis”. From Knubben-Schweizer et al. (2011); authors’ translation.
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(B) Snail habitats are present on all dairy cow pastures. (C) Snail habitats are present on single pastures used for dairy cows. (D) Snail habitats are present on hay fields.
Bovine fasciolosis as a herd health problem is confirmed if at least one of the examined animals (excluding bought in animals) sheds eggs or is serologically positive and at least one snail habitat on a pasture or in a hay field can be found. The following control strategies are recommended for these scenarios:
(A) Treatment of the young stock or the dry cows with a flukicide after bringing the animals off the infectious pasture. (B) Treatment of all dairy cows with a flukicide over the winter period. Additionally, treatment of dry cows during summer period is also advised. This appears to result in a significant increase in the milk production in the following lactation by 1 kg milk per day (Charlier et al., 2012). (C) The pasture rotation system described by Boray (1971, 1972) (for farms with housing in winter and grazing in summer) can be utilized: dairy cows are treated with a flukicide before grazing on the pasture with snail habitat. If the animals get infected on this pasture only (and no other feed harbors metacercariae) the treatments can begin about 8–10 weeks after turning the cows off the pastures with snail habitat, when no juvenile flukes should be present in the liver (except in Switzerland, where triclabendazole is also a treatment option in dairy cows). In spring animals are turned out on pastures without snail habitats. In June and July cows are all allowed
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to graze on pastures with snail habitat but have to be moved to pastures without snails before shedding eggs. (D) Grass should be treated prior to feeding, either by barn drying or making silage (Enigk and Hildebrandt, 1964; Enigk et al., 1964). This ensures that most of the metacercariae present are non-viable.
The choice of the flukicide generally depends on the clinical form of the disease (acute vs. chronic fasciolosis), the type of animals (young stock, beef cattle, dairy cows), the stage of lactation in dairy cows (lactating, dry), the license of a drug, and the legislations of the country. Available formulations in Germany and Switzerland are listed in Table 1. In order to minimize economic losses for the farmers, when applying a product with milk withdrawal, the recommendation is to treat dry cows. If this is for epidemiological reasons not possible, losses can be minimized by treating single cows only, ideally at the same time as some other necessary treatment such as intramammary antibiotic treatment due to mastitis has to be conducted, in order to minimize milk discard. If several cows have to be treated during winter (as is the case in scenario B), then farmers often agree to treat small groups of cows and hence discard the smallest possible amounts of milk at a time. The control of the efficacy of these control measures was undertaken on 32 dairy farms: 15 farms followed the recommendations, 17 were not compliant (KnubbenSchweizer et al., 2010). The survey was done in the same time period on all farms. The prevalence of F. hepatica infection in the herds where the recommendations were followed decreased significantly from 30.7 to 9.3%, whereas no decrease was found in the herds without control (34.1% on the first visit, 34.1% 3–4 years later; Knubben-Schweizer et al., 2010). Furthermore, the sero-prevalence at the end of the trial differed significantly in between the study groups:
Table 1 Available flukicides in Switzerland and Germany and their possible use in lactating cows. Agent
Switzerland
Germany
Product
Withdrawal time milk
Product
Withdrawal time milk
Triclabendazole
Cydectin® Triclamox pour-on Endex® 19.5%
Not licensed for milk producing animals 12 days
Cydectin® Triclamox pour-on Endofluke® Fasinex® 10%
Not licensed for milk producing animals 47 days Not licensed for milk producing animals Not licensed for milk producing animals 5 days 5 days Not licensed for milk producing animals Not licensed for milk producing animals Not licensed for milk producing animals
Triclaben® 10% Albendazole Clorsulon
Albex 10% Valbazen® 10% Ivomec® Plus
5 days 5 days Not licensed for milk producing animals
Albendazol® 10% Valbazen® 10% Bimectin® Fluke Levatum® Fluke
Closantel
Closamectin® pour-on, Closamectin® for injection
Not licensed for milk producing animals
Closamectin® pour-on
Flukiver® Oxyclozanide
No product licensed
No product licensed but may be imported with special permission: Douvistome® , Zanil®
Not licensed for milk producing animals Zanil® : 3 days Douvistome® : 4.5 days
Please cite this article in press as: Knubben-Schweizer, G., Torgerson, P.R., Bovine fasciolosis: Control strategies based on the location of Galba truncatula habitats on farms. Vet. Parasitol. (2015), http://dx.doi.org/10.1016/j.vetpar.2014.12.019
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21.4% in the herds with control measures vs. 62.1% in the herds without control (P < 0.001, Knubben-Schweizer et al., 2010).
3. Discussion Despite the fact that the risk factors for the transmission of F. hepatica are known for a long time and effective drugs against the infection are available, there is rising concern from increasing prevalence combined with increasing reports of resistance of liver fluke especially against triclabendazole, the most effective agent against immature stages of the parasite (Fairweather, 2011). Many different control strategies have been described in the past, such as chemical and biological control of the snail populations, and control of the infection in the definite host either by chemotherapy or biologically (Torgerson and Claxton, 1999). The method most widely used in practice is strategic anthelmintic control in the definite host. At the moment, there is slow progress in the improvement of treatment or prophylaxis of fasciolosis in the definite host. Therefore, in order to optimize the efficacy of the drugs available, practitioners should concentrate on improving pasture management strategies. None of the possibilities included is perfect and each of them has significant drawbacks: - Environmental protection restricts drainage of wet pastures, the closure of open ditches, and the use of molluscicides (Fairweather, 2011; Torgerson and Claxton, 1999). Molluscicides are rarely if ever used now for the control of fasciolosis because of adverse environmental effects. - Fencing off habitats is regularly used in practice, where usually 1–2 m distance from fence to habitat is applied. To the authors’ experience it is of limited use though, as habitats can alter in size depending on rainfall and the fence will not prohibit the snails from moving to nearby secondary habitats. Migration distances of 30 m have been observed from one spring swamp in the middle of a pasture for dairy cows to puddles at the edges of the pasture. - Pasture rotation systems as described by Boray (1971, 1972) require a detailed knowledge of the location of the habitats on the grasslands of a farm and the intention of the farmer to alter the familiar pasturing sequence and it can only be used in situations, where infectious and non-infectious pastures are present. Furthermore there is some risk of promoting resistance to the flukicide, as only treated cows will shed eggs of surviving flukes. In practice, bovine fasciolosis is usually either diagnosed by the abattoir because of condemned livers or by coproscopy or bulk milk serology in the live animal. Any positive test usually leads to treatment of the whole herd, regardless of the infection status of individual animals. Treatment of the whole herd once a year – usually in winter – is a strategy often used in Germany where an oxyclozanide product with a minimal withdrawal time of 3
days4 for milk may be imported from other EU countries. In Germany a surveillance based on bulk milk serology is widely used. It has to be kept in mind though, that bulk milk will test positive, if 20% of the animals have antibodies (Duscher et al., 2011). In most herds, animals in first and second lactation will contribute considerably to the bulk milk. For this reason, bulk milk can test positive for F. hepatica antibodies even if only young stock are infected. In Switzerland a positive test result usually leads to treatment of dry cows, regardless of the time of year. This has proved to be of benefit for the individual cow but does not appear to reduce the herd prevalence and hence has little effect on parasite transmission (Charlier et al., 2012; Knubben-Schweizer et al., 2010; Mezo et al., 2008). Even though the transmission of the parasite depends on humidity, it could be shown, that in Germany the prevalence of fasciolosis is associated significantly with the proportion of grassed area and water bodies but not with rainfall (Kuerpick et al., 2013). Rainfall might in extreme years alter the in-herd prevalence, but even very dry years do probably not result in an economically important decrease of in-herd prevalence, as the primary habitats that mainly depend on ground water level and water permeability of the soil are usually present independent of rainfall in Germany and Switzerland. Rainfall may alter the size of the primary habitats (especially spring water or swamps) and migration distance of the snails. The presented follow-up does not take these factors into account as it is thought to be a user-friendly, practical tool for veterinarians and farmers to help control bovine fasciolosis in situations where the infection is shown to be present in the herd and potential snail habitats are found. As the epidemiological picture varies according to individual farms, a detailed diagnosis of the affected pasture and group of animals is strongly recommended. After analysis of the operational conditions, the appropriate measures can be taken. In situations where only young stock is infected, there is little value in treating all animals every year. The problem will be solved when the animals are treated following removal from the infectious pasture. In situations, where habitats lie on single dairy cow pastures, the pasture rotation system described by Boray (1971, 1972) will probably reduce the application of flukicides overtime. The progress and success of an individual control program in order to reduce the transmission of F. hepatica can be surveyed by repeated serology of the dairy cows. To the authors’ experience it is sufficient, to repeat the laboratory examination after 2–4 years. 4. Conclusions It could be shown, that following a control strategy designed according to the specific epidemiology found on the individual farm, egg shedding and seroprevalence in cattle infected with F. hepatica can be reduced significantly (Knubben-Schweizer et al., 2010). Furthermore, individual
4 Until recently the oxyclozanide product had a zero-withdrawal time for milk.
Please cite this article in press as: Knubben-Schweizer, G., Torgerson, P.R., Bovine fasciolosis: Control strategies based on the location of Galba truncatula habitats on farms. Vet. Parasitol. (2015), http://dx.doi.org/10.1016/j.vetpar.2014.12.019
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control strategies might help contribute to a reduced use of flukicides. The presented follow-up is suitable for pasture and herd management situations in temperate zones with regular rainfall as found in Switzerland, Austria and in the South of Germany. In regions and countries with differing animal husbandry practices or differing climatic conditions the control methods would have to be adapted. A pasture rotation system for whole year grazing for example is also described by Boray (1971). Conflict of interest statement None of the authors of this paper has a financial of personal relationship with other people or organisations that could inappropriately influence or bias the content of the paper. References Armour, J., 1975. The epidemiology and control of bovine fascioliasis. Vet. Rec. 96, 198–201. Bennema, S., Vercruysse, J., Claerebout, E., Schnieder, T., Strube, C., Ducheyne, E., Hendrickx, G., Charlier, J., 2009. The use of bulk-tank milk ELISAs to assess the spatial distribution of Fasciola hepatica. Ostertagia ostertagi and Dictyocaulus viviparus in dairy cattle in Flanders (Belgium). Vet. Parasitol. 165, 51–57. Boray, J.C., 1971. Fortschritte in der Bekämpfung der Fasciolose. Schweiz. Arch. Tierheilkd. 113, 361–386. Boray, J.C., 1972. Bekämpfung der Fasciolose und der Dicrocoeliose des Rindes. Schweiz. Arch. Tierheilkd. 114, 639–651. Charlier, J., Hostens, M., Jacobs, J., Van Ranst, B., Duchateau, L., Vercruysse, J., 2012. Integrating fasciolosis control in the dry cow management: the effect of closantel treatment on milk production. PLoS ONE 7 (8), e43216, http://dx.doi.org/10.1371/journal.pone.0043216. Christensen, N.O., Nansen, P., Flemming, F., 1976. The influence of temperature on the infectivity of Fasciola hepatica miracidia to Lymnaea truncatula. J. Parasitol. 62, 698–701. Duscher, R., Duscher, G., Hofer, J., Tichy, A., Prosl, H., Joachim, A., 2011. Fasciola hepatica – monitoring the milky way? The use of tank milk for liver fluke monitoring in dairy herds as a base for treatment strategies. Vet. Parasitol. 178, 273–278. Enigk, K., Hildebrandt, J., 1964. Zur Lebensdauer der Metacercarien von Fasciola hepatica im Heu. Tierarztl. Umsch. 19, 592–595. Enigk, K., Hildebrandt, J., Zimmer, E., 1964. Zur Lebensdauer der infektiösen Larven von Haustierhelminthen in Silage. Dtsch. Tierarztl. Wochenschr. 71, 533–537. Epe, C., Coati, N., Schnieder, T., 2004. Ergebnisse parasitologischer Kotuntersuchungen von Pferden, Wiederkäuern, Schweinen, Hunden, Katzen, Igeln und Kaninchen. Dtsch. Tierarztl. Wochenschr. 111, 243–247. Fairweather, I., 2009. Triclabendazole progress report, 2005–2009: an advancement of learning? J. Helminthol. 83, 139–150. Fairweather, I., 2011. Reducing the future threat from (liver) fluke: realistic prospect or quixotic fantasy? Vet. Parasitol. 180, 133–143. Frömming, E., 1956. L. (Galba) truncatula Müller. In: Biologie der mitteleuropäischen Süsswasserschnecken. Duncker & Humblot, Berlin, pp. 120–129. Gomez-Puerta, L.A., Gavidia, C., Lopez-Urbina, M.T., Garcia, H.H., Gonzalez, A.E., 2012. Efficacy of a single oral dose of oxfendazole against Fasciola hepatica in naturally infected sheep. Am. J. Trop. Med. Hyg. 86, 486–488. Harris, R.E., Charleston, W.A.G., 1971. Control of fascioliasis – some theoretical and practical considerations. N. Z. Vet. J. 19, 65–72. Hutchinson, G.W., Dawson, K., Fitzgibbon, C.C., Martin, P.J., 2009. Efficacy of an injectable combination anthelmintic
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(nitroxynil + clorsulon + ivermectin) against early immature Fasciola hepatica compared to triclabendazole combination flukicides given orally or topically to cattle. Vet. Parasitol. 162, 278–284. Hutchinson, G.W., Macarthur, E., 2003. Validation of French Antibody ELISA for Liver Fluke. Meat & Livestock, Australia, www. redmeatinnovation.com.au/working-with-mla/report-templates/ sample-final-report Kendall, S.B., McCullough, F.S., 1951. The emergence of the Cercariae of Fasciola hepatica from the Snail Limnea truncatula. J. Helminthol. 25, 77–92. Knubben-Schweizer, G., Rüegg, S., Torgerson, P.R., Rapsch, C., Grimm, F., Hässig, M., Deplazes, P., Braun, U., 2010. Control of bovine fasciolosis in dairy cattle in Switzerland with emphasis on pasture management. Vet. J. 186, 188–191. Knubben-Schweizer, G., Scheuerle, M., Pfister, K., 2011. Die Bekämpfung des grossen Leberegels beim Rind. Tierarztl. Prax. 39 (G), 289–298. Koch, S., (Doctoral thesis) 2005. Untersuchungen zur Verbreitung von Fasciola hepatica im bayerischen Milchviehbestand, Munich. Kuerpick, B., Schnieder, T., Strube, C., 2012. Seasonal pattern of Fasciola hepatica antibodies in dairy herds in Northern Germany. Parasitol. Res. 111, 1085–1092. Kuerpick, B., Contraths, F.J., Staubach, C., Fröhlich, A., Schnieder, T., Strube, C., 2013. Seroprevalence and GIS-supported risk factor analysis of Fasciola hepatica infections in dairy herds in Germany. Parasitology 140, 1051–1060. Martínez-Valladares, M., del Rosario Famularo, M., Fernández-Pato, N., Castanón-Ordónez, L., Cordero-Pérez, C., Rojo-Vázquez, F.A., 2010. Efficacy of nitroxynil against Fasciola hepatica resistant to triclabendazole inanaturally infected sheep flock. Parasitol. Res. 107, 1205–1211. Mehl, S., 1932. Die Lebensbedingungen der Leberegelschnecke (Galba truncatula Müller). Untersuchungen über Schale, Verbreitung, Lebensgeschichte, natürliche Feinde und Bekämpfungsmöglichkeiten. Dr. F. P. Datterer & Cie, München. Mezo, M., González-Warleta, M., Castro-Hermida, J.A., Ubeira, F.M., 2008. Evaluation of the flukicide treatment policy for dairy cattle in Galicia (NW Spain). Vet. Parasitol. 157, 235–243. Ollerenshaw, C.B., 1959. The ecology of the liver fluke (Fasciola hepatica). Vet. Rec. 71, 957–965. Petzold, F., (Doctoral thesis) 1989. Zur Populationsdynamik von Galba truncatuala (Müll.) und deren Infektion mit Fasciola hepatica (L.) in einem endemischen Voralpengebiet der Schweiz. University of Basel. Rabeler, M., (Doctoral thesis) 2011. Untersuchungen zum Vorkommen und zur wirtschaftlichen Bedeutung der Fasciolose in Milchkuhherden Norddeutschlands, Giessen. Rapsch, C., Schweizer, G., Grimm, F., Kohler, L., Bauer, C., Deplazes, P., Braun, U., Torgerson, P.R., 2006. Estimating the true prevalence of Fasciola hepatica in cattle slaughtered in Switzerland in the absence of an absolute diagnostic test. Int. J. Parasitol. 36, 1153–1158. Rondelaud, D., Hourdin, P., Vignoles, P., Dreyfuss, G., Cabaret, J., 2011. The detection of snail host habitats in liver fluke infected farms by use of plant indicators. Vet. Parasitol. 181, 166–173. Ross, J.G., 1968. The life span of Fasciola hepatica in cattle. Vet. Rec. 82, 587–589. Ross, J.G., 1970. The epidemiology of fascioliasis in Northern Ireland. Vet. Rec. 87, 370–372. Schneider, F., Eckert, J., Keller, H., 1975. Ein Modellversuch zur planmässigen medikamentellen Fasciolose-Bekämpfung. Schweiz. Arch. Tierheilkd. 117, 185–191. Schweizer, G., Braun, U., Deplazes, P., Torgerson, P.R., 2005. Estimating the financial losses due to bovine fasciolosis in Switzerland. Vet. Rec. 157, 188–193. Schweizer, G., Meli, M.L., Torgerson, P.R., Lutz, H., Deplazes, P., Braun, U., 2007. Prevalence of Fasciola hepatica in the intermediate host Lymnaea truncatula detected by real time TaqMan PCR in populations from 70 Swiss farms with cattle husbandry. Vet. Parasitol. 150, 164–169. Thomas, A.P., 1883. The life history of the liver-fluke (Fasciola hepatica). Q. J. Microsc. Sci. 23, 99–133. Torgerson, P., Claxton, J., 1999. Epidemiology and control. In: Dalton, J.P. (Ed.), Fasciolosis. Cabi Publishing, Oxon/New York, pp. 113–149. Whitehead, J.D., 1976. Observations on the repeated treatment for fascioliasis of stock on a farm in south-west England. Vet. Rec. 98, 5–9.
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Bovine fasciolosis: Control strategies based on the location of Galba truncatula habitats on farms Gabriela Knubben-Schweizer a,∗ , Paul R. Torgerson b a Clinic for Ruminants with Ambulatory and Herd Health Services at the Centre for Clinical Veterinary Medicine, Ludwig-Maximilians-University Munich, Sonnenstrasse 16, 85764 Oberschleissheim, Germany b Section of Epidemiology, Vetsuisse Faculty, University of Zurich, Winterthurerstrasse 270, 8057 Zurich, Switzerland
a r t i c l e
i n f o
Keywords: Fasciola hepatica Cattle Galba truncatula Snail habitats Control Pasture management
a b s t r a c t Infection of livestock with Fasciola hepatica is a worldwide, economically important and increasing problem. Even though, bovine fasciolosis can be a disease associated with particular regions, there are usually epidemiological issues on individual farms. For this reason, it is recommended to find the source of infection by examination of definite hosts and pastures on a farm. The following factors which promote the transmission of bovine fasciolosis are usually found: (A) Snail habitats are present on pastures used for young stock (prior to first calving) or dry cows only. Pastures for dairy cows are not affected. (B) Snail habitats are present on all pastures for dairy cows. (C) Snail habitats are present on single pastures used for dairy cows. (D) Snail habitats are present on hayfields. For each of these epidemiological situations an individual control strategy is advised. When a control strategy is tailored according to the specific epidemiology found on the individual farm, egg shedding and F. hepatica-seroprevalence can be reduced significantly. This approach can support the responsible use of the available flukicides. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Infection of livestock with Fasciola hepatica is a worldwide, economic problem with increasing importance (Fairweather, 2009). In the north of Germany for instance, the prevalence was previously reported to be 0.6% (Epe et al., 2004), while more recent studies have found mean
∗ Corresponding author at: Klinik für Wiederkäuer mit Ambulanz und Bestandsbetreuung, LMU München, Sonnenstrasse 16, 85764 Oberschleissheim, Germany. Tel.: +49 89 2180 78850; fax: +49 89 2180 78851. E-mail address: [email protected] (G. Knubben-Schweizer).
herd prevalences of between 32.2% and 69.1% (Koch, 2005; Rabeler, 2011; Kuerpick et al., 2012). Despite strategic treatments with different flukicides and sophisticated forecast models, high and even increasing prevalences have been reported elsewhere (Bennema et al., 2009; Rapsch et al., 2006). In addition to likely increases in disease prevalence, future fluke control will also have to deal with the threat of drug (i.e. triclabendazole) resistance (Fairweather, 2011). Economic losses due to bovine fasciolosis can be considerable. In Switzerland for example, such losses have been estimated at several thousand Euros per affected farm (Schweizer et al., 2005). Consequently, control of this parasite is important for economic reasons in addition to reasons of animal welfare.
http://dx.doi.org/10.1016/j.vetpar.2014.12.019 0304-4017/© 2014 Elsevier B.V. All rights reserved.
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Of the several strategies for the control of bovine fasciolosis described, in practice usually strategic anthelmintic control is used with flukicide treatment time and interval depending on the climatic zone (Armour, 1975; Boray, 1971, 1972; Harris and Charleston, 1971; Schneider et al., 1975; Torgerson and Claxton, 1999; Whitehead, 1976). A variety of fasciolicides is available for the treatment of bovine fasiolosis: triclabendazole, albendazole, oxyclozanide, clorsulon, nitroxynil, rafoxanide or oxfendazole (Fairweather, 2011; Gomez-Puerta et al., 2012; MartínezValladares et al., 2010). Of all these agents, triclabendazole is the most effective against immature stages of the parasite, which makes it the drug of choice for the treatment of acute fasciolosis, which is more commonly seen in sheep than in cattle. Due to increasing resistance against triclabendazole (Fairweather, 2011), there are efforts to develop new drugs which are efficacious against immature parasites, but results to date have been disappointing (Fairweather, 2011). Combining compounds can help to increase efficacy against immature stages. For example the combination of clorsulon (2.0 mg/kg) and nitroxynil (10.2 mg/kg) reached an efficiency of 95% against 2-weekold flukes and 99% against 4-week-old flukes (Hutchinson et al., 2009). One of the limits for the use of flukicides in cattle – especially dairy cows – is the legislation regulating drug licencing differing from country to country. In Switzerland for instance, only one clorsulon formulation is authorized (Ivomec® Plus, Biokema SA), but its use is restricted to non-lactating animals. Furthermore, no nitroxynil drug is registered. Instead, triclabendazole is authorized for dairy cows, with a withdrawal time of 12 days for milk (Endex® 19.5%, Novartis AG), whereas it is not authorized in Germany for use in lactating animals. Therefore, practitioners have a responsibility in reducing and optimizing the administration of flukicides. This can be supported by taking the individual epidemiological situation on the farm into account. This review is linked to the EVPC scientific symposium “The two faces of Veterinary Parasitology: from biology to clinical aspects” (2012 annual EVPC meeting León, Spain). The topic addressed is a revised view on control of bovine fasciolosis in the field from the point of view of a practitioner. Therefore, the approach is practical and can help reduce flukicide treatment. 2. Control of bovine fasciolosis based on the location of the snail habitats The transmission of F. hepatica is linked to the intermediate host – a number of species of amphibious snails. In Europe Galba truncatula is a common intermediate host. This snail is found in moist, especially smooth and firm clay soils. Preferred habitats are shallow water, ditches, banks of slowly-moving streams, spring swamps and reeds (Frömming, 1956; Mehl, 1932; Schweizer et al., 2007). In addition, wells (Fig. 1) and cattle watering tanks can provide suitable habitats (Petzold, 1989; Schweizer et al., 2007). The occurrence of G. truncatula and the transmission of F. hepatica depend not only on moisture and soil condition but also on temperature and solar radiation (Armour,
1975; Christensen et al., 1976; Kendall and McCullough, 1951; Ollerenshaw, 1959; Petzold, 1989; Ross, 1970; Thomas, 1883). Although suitable meteorological and geographical conditions may promote transmission on a regional scale, there are usually epidemiological factors that increase the risk of bovine fasciolosis on individual farms (Schweizer et al., 2007). In a survey on 70 farms with a known herd health problem of bovine fasciolosis in Switzerland, 40 farms only had one suitable snail habitat on their grasslands (Schweizer et al., 2007). Thus, in almost 60% of the farms visited, an extensive spatial distribution of infectious grasslands could be ruled out. Additionally, in countries such as Switzerland, Austria or Germany, where young stock are often kept on separate pastures from dairy cows (e.g. alpine pastures) it is possible, that these animals become infected when grazing on these separate pastures. If there are no snail habitats on the home farms, these animals do not get re-infected after being turned off the young stock pastures. Thus a strategic anthelmintic treatment of all animals every year is not always cost-effective. For this reason, the following course of action as detailed in Fig. 2, is recommended, in order to control fasciolosis in cattle (Knubben-Schweizer et al., 2011): 1. In order to make a detailed diagnosis of the herd health problem for the first time on a farm1 , it is necessary to detect the affected group of cattle. The control differs if young stock only is infected or if dairy cows repeatedly acquire fasciolosis throughout their productive life. For this reason laboratory tests should be performed in at least five young animals prior to first calving and five dairy cows taking into account the following drawbacks of fecal examination and serology:
- Fecal examination: the parasite can live for up to 26 months in the liver of cattle (Ross, 1968). If young stock are infected on separate pastures (e.g. alpine pastures) and are not treated, the parasite potentially sheds eggs throughout the first lactation of the animal. Thus, the finding of F. hepatica eggs in first lactation cows does not imply that there must be infectious pastures on the home-farm. The infection might have arisen from young stock pastures. Therefore to find the source of infection (young stock pastures vs. dairy cow pastures) the fecal examination of first lactation cows is not useful. - Serology: With serology the infection can be diagnosed early in the prepatent period of the infection. The disadvantage though is that antibodies persist 6–9 (even to 18) months after elimination of the parasites (Hutchinson and Macarthur, 2003). Infection acquired in the first or second year of life of a definite host can therefore still be detected during the second lactation of a dairy cow.
1 In order to monitor the prevalence (e.g. in a control program) fecal samples of 5 animals can be used. The prevalence resulting from 5 fecal samples is associated with the sero-prevalence resulting from the examination of a blood sample from all animals (Knubben-Schweizer et al., 2010). Nevertheless we recommend to repeatedly examine serologically all animals of a group (e.g. dairy cows) for prevalence monitoring due to better comparability.
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Fig. 1. A drinking trough (well) harboring Galba truncatula in a pasture for young stock.
In conclusion in young stock, either fecal examination or serology can be used. Dairy cows should not be sampled at all during the first lactation, fecal examination can be conducted in their second and subsequent lactation while serology is recommended for cows from their third lactation onwards. As a rule of thumb it makes sense to sample the oldest animals that are the longest in the herd. Furthermore, it is recommended to examine all brought in animals immediately after purchase either by fecal examination2 or by serology in order to treat them appropriately before contamination of a pasture that may have suitable snail habitats.
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In order to enhance the sensitivity of the coproscopy we recommend examining 2 × 10 g of feces from the same sample (Rapsch et al., 2006).
2. In a second step the pastures and possibly hay fields (all forage acreage3 should be taken into account depending on the results of the laboratory examinations) must be examined for potential snail habitats and the location of these must be assessed. As the farmer knows the wettest areas on his premises, his assistance is necessary. Furthermore, the use of plant indicators for positive sites of G. truncatula can be very helpful (Rondelaud et al., 2011). Four scenarios of snail habitat sites are possible (KnubbenSchweizer et al., 2010): (A) Snail habitats are present on pastures used for young stock (prior to first calving) or dry cows only. Pastures for dairy cows are not affected.
3 Especially if fresh grass is fed from them. It has to be kept in mind though, that also hay and to the authors’ experience very seldom even grass silage can transmit F. hepatica.
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Fig. 2. Follow-up of the herd health problem “bovine fasciolosis”. From Knubben-Schweizer et al. (2011); authors’ translation.
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(B) Snail habitats are present on all dairy cow pastures. (C) Snail habitats are present on single pastures used for dairy cows. (D) Snail habitats are present on hay fields.
Bovine fasciolosis as a herd health problem is confirmed if at least one of the examined animals (excluding bought in animals) sheds eggs or is serologically positive and at least one snail habitat on a pasture or in a hay field can be found. The following control strategies are recommended for these scenarios:
(A) Treatment of the young stock or the dry cows with a flukicide after bringing the animals off the infectious pasture. (B) Treatment of all dairy cows with a flukicide over the winter period. Additionally, treatment of dry cows during summer period is also advised. This appears to result in a significant increase in the milk production in the following lactation by 1 kg milk per day (Charlier et al., 2012). (C) The pasture rotation system described by Boray (1971, 1972) (for farms with housing in winter and grazing in summer) can be utilized: dairy cows are treated with a flukicide before grazing on the pasture with snail habitat. If the animals get infected on this pasture only (and no other feed harbors metacercariae) the treatments can begin about 8–10 weeks after turning the cows off the pastures with snail habitat, when no juvenile flukes should be present in the liver (except in Switzerland, where triclabendazole is also a treatment option in dairy cows). In spring animals are turned out on pastures without snail habitats. In June and July cows are all allowed
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to graze on pastures with snail habitat but have to be moved to pastures without snails before shedding eggs. (D) Grass should be treated prior to feeding, either by barn drying or making silage (Enigk and Hildebrandt, 1964; Enigk et al., 1964). This ensures that most of the metacercariae present are non-viable.
The choice of the flukicide generally depends on the clinical form of the disease (acute vs. chronic fasciolosis), the type of animals (young stock, beef cattle, dairy cows), the stage of lactation in dairy cows (lactating, dry), the license of a drug, and the legislations of the country. Available formulations in Germany and Switzerland are listed in Table 1. In order to minimize economic losses for the farmers, when applying a product with milk withdrawal, the recommendation is to treat dry cows. If this is for epidemiological reasons not possible, losses can be minimized by treating single cows only, ideally at the same time as some other necessary treatment such as intramammary antibiotic treatment due to mastitis has to be conducted, in order to minimize milk discard. If several cows have to be treated during winter (as is the case in scenario B), then farmers often agree to treat small groups of cows and hence discard the smallest possible amounts of milk at a time. The control of the efficacy of these control measures was undertaken on 32 dairy farms: 15 farms followed the recommendations, 17 were not compliant (KnubbenSchweizer et al., 2010). The survey was done in the same time period on all farms. The prevalence of F. hepatica infection in the herds where the recommendations were followed decreased significantly from 30.7 to 9.3%, whereas no decrease was found in the herds without control (34.1% on the first visit, 34.1% 3–4 years later; Knubben-Schweizer et al., 2010). Furthermore, the sero-prevalence at the end of the trial differed significantly in between the study groups:
Table 1 Available flukicides in Switzerland and Germany and their possible use in lactating cows. Agent
Switzerland
Germany
Product
Withdrawal time milk
Product
Withdrawal time milk
Triclabendazole
Cydectin® Triclamox pour-on Endex® 19.5%
Not licensed for milk producing animals 12 days
Cydectin® Triclamox pour-on Endofluke® Fasinex® 10%
Not licensed for milk producing animals 47 days Not licensed for milk producing animals Not licensed for milk producing animals 5 days 5 days Not licensed for milk producing animals Not licensed for milk producing animals Not licensed for milk producing animals
Triclaben® 10% Albendazole Clorsulon
Albex 10% Valbazen® 10% Ivomec® Plus
5 days 5 days Not licensed for milk producing animals
Albendazol® 10% Valbazen® 10% Bimectin® Fluke Levatum® Fluke
Closantel
Closamectin® pour-on, Closamectin® for injection
Not licensed for milk producing animals
Closamectin® pour-on
Flukiver® Oxyclozanide
No product licensed
No product licensed but may be imported with special permission: Douvistome® , Zanil®
Not licensed for milk producing animals Zanil® : 3 days Douvistome® : 4.5 days
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21.4% in the herds with control measures vs. 62.1% in the herds without control (P < 0.001, Knubben-Schweizer et al., 2010).
3. Discussion Despite the fact that the risk factors for the transmission of F. hepatica are known for a long time and effective drugs against the infection are available, there is rising concern from increasing prevalence combined with increasing reports of resistance of liver fluke especially against triclabendazole, the most effective agent against immature stages of the parasite (Fairweather, 2011). Many different control strategies have been described in the past, such as chemical and biological control of the snail populations, and control of the infection in the definite host either by chemotherapy or biologically (Torgerson and Claxton, 1999). The method most widely used in practice is strategic anthelmintic control in the definite host. At the moment, there is slow progress in the improvement of treatment or prophylaxis of fasciolosis in the definite host. Therefore, in order to optimize the efficacy of the drugs available, practitioners should concentrate on improving pasture management strategies. None of the possibilities included is perfect and each of them has significant drawbacks: - Environmental protection restricts drainage of wet pastures, the closure of open ditches, and the use of molluscicides (Fairweather, 2011; Torgerson and Claxton, 1999). Molluscicides are rarely if ever used now for the control of fasciolosis because of adverse environmental effects. - Fencing off habitats is regularly used in practice, where usually 1–2 m distance from fence to habitat is applied. To the authors’ experience it is of limited use though, as habitats can alter in size depending on rainfall and the fence will not prohibit the snails from moving to nearby secondary habitats. Migration distances of 30 m have been observed from one spring swamp in the middle of a pasture for dairy cows to puddles at the edges of the pasture. - Pasture rotation systems as described by Boray (1971, 1972) require a detailed knowledge of the location of the habitats on the grasslands of a farm and the intention of the farmer to alter the familiar pasturing sequence and it can only be used in situations, where infectious and non-infectious pastures are present. Furthermore there is some risk of promoting resistance to the flukicide, as only treated cows will shed eggs of surviving flukes. In practice, bovine fasciolosis is usually either diagnosed by the abattoir because of condemned livers or by coproscopy or bulk milk serology in the live animal. Any positive test usually leads to treatment of the whole herd, regardless of the infection status of individual animals. Treatment of the whole herd once a year – usually in winter – is a strategy often used in Germany where an oxyclozanide product with a minimal withdrawal time of 3
days4 for milk may be imported from other EU countries. In Germany a surveillance based on bulk milk serology is widely used. It has to be kept in mind though, that bulk milk will test positive, if 20% of the animals have antibodies (Duscher et al., 2011). In most herds, animals in first and second lactation will contribute considerably to the bulk milk. For this reason, bulk milk can test positive for F. hepatica antibodies even if only young stock are infected. In Switzerland a positive test result usually leads to treatment of dry cows, regardless of the time of year. This has proved to be of benefit for the individual cow but does not appear to reduce the herd prevalence and hence has little effect on parasite transmission (Charlier et al., 2012; Knubben-Schweizer et al., 2010; Mezo et al., 2008). Even though the transmission of the parasite depends on humidity, it could be shown, that in Germany the prevalence of fasciolosis is associated significantly with the proportion of grassed area and water bodies but not with rainfall (Kuerpick et al., 2013). Rainfall might in extreme years alter the in-herd prevalence, but even very dry years do probably not result in an economically important decrease of in-herd prevalence, as the primary habitats that mainly depend on ground water level and water permeability of the soil are usually present independent of rainfall in Germany and Switzerland. Rainfall may alter the size of the primary habitats (especially spring water or swamps) and migration distance of the snails. The presented follow-up does not take these factors into account as it is thought to be a user-friendly, practical tool for veterinarians and farmers to help control bovine fasciolosis in situations where the infection is shown to be present in the herd and potential snail habitats are found. As the epidemiological picture varies according to individual farms, a detailed diagnosis of the affected pasture and group of animals is strongly recommended. After analysis of the operational conditions, the appropriate measures can be taken. In situations where only young stock is infected, there is little value in treating all animals every year. The problem will be solved when the animals are treated following removal from the infectious pasture. In situations, where habitats lie on single dairy cow pastures, the pasture rotation system described by Boray (1971, 1972) will probably reduce the application of flukicides overtime. The progress and success of an individual control program in order to reduce the transmission of F. hepatica can be surveyed by repeated serology of the dairy cows. To the authors’ experience it is sufficient, to repeat the laboratory examination after 2–4 years. 4. Conclusions It could be shown, that following a control strategy designed according to the specific epidemiology found on the individual farm, egg shedding and seroprevalence in cattle infected with F. hepatica can be reduced significantly (Knubben-Schweizer et al., 2010). Furthermore, individual
4 Until recently the oxyclozanide product had a zero-withdrawal time for milk.
Please cite this article in press as: Knubben-Schweizer, G., Torgerson, P.R., Bovine fasciolosis: Control strategies based on the location of Galba truncatula habitats on farms. Vet. Parasitol. (2015), http://dx.doi.org/10.1016/j.vetpar.2014.12.019
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