animals Review Chronic Wasting Due to Liver and Rumen Flukes in Sheep Alexandra Kahl 1,*, Georg von Samson-Himmelstjerna 1, Jürgen Krücken 1 and Martin Ganter 2 1 Institute for Parasitology and Tropical Veterinary Medicine, Freie Universität Berlin, Robert-von-Ostertag-Str. 7-13, 14163 Berlin, Germany; [email protected] (G.v.S.-H.); [email protected] (J.K.) 2 Clinic for Swine and Small Ruminants, Forensic Medicine and Ambulatory Service, University of Veterinary Medicine Hannover, Foundation, Bischofsholer Damm 15, 30173 Hannover, Germany; [email protected] * Correspondence: [email protected] Simple Summary: Chronic wasting in sheep is often related to parasitic infections, especially to infections with several species of trematodes. Trematodes, or “flukes”, are endoparasites, which infect different organs of their hosts (often sheep, goats and cattle, but other grazing animals as well as carnivores and birds are also at risk of infection). The body of an adult fluke has two suckers for adhesion to the host’s internal organ surface and for feeding purposes. Flukes cause harm to the animals by subsisting on host body tissues or fluids such as blood, and by initiating mechanical damage that leads to impaired vital organ functions. The development of these parasites is dependent on the occurrence of intermediate hosts during the life cycle of the fluke species. These intermediate hosts are often invertebrate species such as various snails and ants. This manuscript provides an insight into the distribution, morphology, life cycle, pathology and clinical symptoms caused by infections of liver and rumen flukes in sheep. Furthermore, we address the diagnosis, treatment and prevention measures, as well as the current knowledge about genomic resources. Abstract: Grazing sheep and goats are constantly exposed to helminth infections in many parts of Citation: Kahl, A.; von the world, including several trematode species that causes a range of clinical diseases. The clinical Samson-Himmelstjerna, G.; Krücken, picture of flukes is dependent upon the organs in which they develop and the tissues they damage J.; Ganter, M. Chronic Wasting Due to within the respective organs. Accordingly, infections with the common liver fluke Fasciola hepat- Liver and Rumen Flukes in Sheep. ica, which, as juvenile worm migrates through the liver parenchyma for several weeks, may be Animals 2021, 11, 549. https:// doi.org/10.3390/ani11020549 associated with hepatic disorders such as impairment of carbohydrate, protein and fat metabolism, followed by chronic wasting. In contrast, the lancet fluke Dicrocoelium dendriticum, which does not Academic Editor: Delia Lacasta exhibit tissue migration and thus does not lead to major tissue damage and bleeding, also does not lead to significant clinical symptoms. Rumen flukes such as Cotylophoron daubneyi cause catarrhal Received: 28 December 2020 inflammation during their migration through the intestinal and abomasal epithelium during its Accepted: 17 February 2021 juvenile stages. Depending on the infection intensity this may result in a range of clinical symptoms Published: 19 February 2021 including diarrhoea, inappetence or emaciation. In this review, we aim to provide an update on the current knowledge on flukes particularly concerning the clinical relevance of the most important Publisher’s Note: MDPI stays neutral fluke species in sheep. with regard to jurisdictional claims in published maps and institutional affil- Keywords: sheep; trematodes; flukes; infection; wasting; emaciation iations. 1. Introduction Copyright: © 2021 by the authors. Digenea are platyhelminths of the class Trematoda and have at least two hosts where Licensee MDPI, Basel, Switzerland. the definitive host is a vertebrate while the first intermediate host is most often a mollusk This article is an open access article (frequently a gastropod) or rarely a polychaet. Various invertebrate and vertebrate species distributed under the terms and may serve as intermediate and paratenic hosts [1]. Accordingly, fluke prevalence is highly conditions of the Creative Commons Attribution (CC BY) license (https:// dependent on the macro- and microclimatic conditions that enable survival and interactions creativecommons.org/licenses/by/ with specific intermediate hosts [2,3]. Grazing animals, particularly sheep, are highly 4.0/). susceptible to various fluke species. In Europe, these include the common liver fluke Animals 2021, 11, 549. https://doi.org/10.3390/ani11020549 https://www.mdpi.com/journal/animals Animals 2021, 11, x FOR PEER REVIEW 2 of 20 Animals 2021, 11, 549 2 of 20 susceptible to various fluke species. In Europe, these include the common liver fluke Fasci- ola hepatica, the lancet fluke Dicrocoelium dendriticum and various rumen fluke species be- longing to the genera Paramphistomum or Calicophoron. Fluke infections in sheep cause a wideFasciola variety hepatica of clinical, the lancet symptoms fluke Dicrocoelium depending dendriticumon the specificand organs various associated rumen fluke with species their developmentbelonging to theand generamanifestationParamphistomum [4]. Whileor chroniCalicophoronc wasting. Fluke is not infections a key clinical in sheep sign cause for all a ofwide the varietyabove-mentioned of clinical symptoms fluke infections, depending it is onconsidered the specific a condition organs associated that always with arises their dependingdevelopment on andthe different manifestation factors [4 within]. While the chronic parasite–host wasting interaction. is not a key This clinical paper sign aims for atall providing of the above-mentioned an overview on fluke the infections,current knowledge it is considered of fluke a conditioninfections thatfor alwaysthe develop- arises mentdepending of this onoften-occu the differentrring factors clinical within picture. the parasite–host interaction. This paper aims at providing an overview on the current knowledge of fluke infections for the development 2.of Fasciolidae this often-occurring with Emphasis clinical on picture. the Common Liver Fluke 2. FasciolidaeMembers of with the Emphasisfamily Fasciolidae on the Common, also known Liver as Flukethe common liver flukes, are trem- atodes that parasitize in the liver of particular herbivore mammals, especially in rumi- Members of the family Fasciolidae, also known as the common liver flukes, are trema- nants. Infections of other species as definitive hosts (e.g., equines, pigs, hares, dogs and todes that parasitize in the liver of particular herbivore mammals, especially in ruminants. rats) [5] are also possible but occur rarely. The highest pathogenic impact is in sheep, Infections of other species as definitive hosts (e.g., equines, pigs, hares, dogs and rats) [5] where fasciolosis may cause high morbidity and mortality leading to economic loss of are also possible but occur rarely. The highest pathogenic impact is in sheep, where fasci- EUR 635 million per year just in Europe due to production losses and treatment costs [6]. olosis may cause high morbidity and mortality leading to economic loss of EUR 635 million Furthermore, not only animals but also humans are at risk of infection by consuming per year just in Europe due to production losses and treatment costs [6]. contaminated freshwater plants carrying the infectious metacercariae of the parasite. Furthermore, not only animals but also humans are at risk of infection by consuming Thus,contaminated making fasciolosis freshwater a plants zoonotic carrying disease. the Human infectious fasciolosis metacercariae particularly of the parasite. occurs in Thus, de- velopingmaking fasciolosiscountries a[7], zoonotic but in animals, disease. Humanthe disease fasciolosis is common particularly in many occurs parts inof developingthe world constitutingcountries [7 ],a butserious in animals, animal thehealth disease problem. is common in many parts of the world constituting a serious animal health problem. 2.1. Distribution of and Anatomical Differences between Fasciola Species 2.1. DistributionThere are two of anddifferent Anatomical species Differences of the parasite between that Fasciola differ Species in their spatial distribution. FasciolaThere hepatica are twois distributed different species globally of in the temperate parasite thatand differsubtropical in their areas spatial in distribu-Europe, America,tion. Fasciola Asia, hepatica Australiais distributed and some globallyparts of inAfrica, temperate whereas and Fasciola subtropical gigantica areas exists in Europe, only inAmerica, tropical Asia,areas Australia of Africa andand someAsia [8]. parts of Africa, whereas Fasciola gigantica exists only in tropicalFasciola areas hepatica of Africa (Figure and Asia1) is a [ 8grey-brownish,]. leaf-shaped fluke with an approximate size ofFasciola about hepatica1.8–5.0 cm(Figure in length1) is a and grey-brownish, 1.0 cm in width leaf-shaped [9] (p.172). fluke This with species an approximate has a conical size anteriorof about end, 1.8–5.0 which cm in is length delimited and 1.0by cmobvious in width shoulders [9] (p.172). [10] This (p.78). species The has major a conical parts anterior of the fluke’send, which bodies is delimitedserve for byreproduction, obvious shoulders which [re10sults] (p.78). in an The extremely major parts high of therate fluke’s of egg bodies pro- duction,serve for so reproduction, that a single which fluke resultsmay produce in an extremely up to 25,000 high rateeggs of per egg day production, [11]. The so oval, that goldena single yellow