Munita et al. Parasites Vectors (2019) 12:525 https://doi.org/10.1186/s13071-019-3779-y Parasites & Vectors RESEARCH Open Access Liver fuke in Irish sheep: prevalence and associations with management practices and co-infection with rumen fuke Maria Pia Munita1,2* , Rosemary Rea2, Ana Maria Martinez‑Ibeas1, Noel Byrne1, Guy McGrath3, Luis Enrique Munita‑Corbalan4, Mary Sekiya5, Grace Mulcahy5 and Ríona G. Sayers1 Abstract Background: The present study aimed to identify the national prevalence of Fasciola hepatica in Irish sheep and to conduct a risk analysis assessment based on management and treatment practices in participating focks. Also, co‑infection with rumen fuke was quantifed and its association with liver fuke and management practices was assessed. Methods: A total of 305 sheep focks were selected ensuring even national representation of the sheep population. Participating farms were asked to complete a survey questionnaire on farm management practices and submit faecal samples during the winter of 2014–2015. Pooled faecal samples were analysed for the presence of F. hepatica and co‑ infection with rumen fuke. Apparent and true prevalence were calculated, additionally, the rate of co‑infection with rumen fuke was also obtained. Correlation and regression analyses were used for assessing associations between management practices, liver fuke infection and co‑infection with rumen fuke. Results: The national true prevalence of F. hepatica was 50.4% (n 305). Regional prevalence varied from 41% in the east to 52% in the south. Co‑infection with rumen fuke was observed= in 40% of the studied population and corre‑ lated with increased F. hepatica egg counts (OR 2.9; P 0.001). Predominant breeds were Sufolk, Texel and Horned Mountain breeds. Beef cattle were the most frequent= type≤ of other livestock present on farms and mixed species grazing was frequently reported (73%). More than half of the focks reported a mid‑to‑late lambing period (March‑ April). Use of mountain land for grazing was of 32%. Flukicides were most commonly used twice over the autumn‑ winter period. Regression analyses highlighted signifcant association of F. hepatica status, with the presence of other livestock on farm, frequency of fukicides used during the winter and clinical presentation of liver fuke. A signifcant increase in eggs per gram of faeces was observed in Charollais sheep in comparison with all other breeds. Co‑infec‑ tion with F. hepatica and Calicophoron daubneyi was also signifcantly associated with the presence of other livestock on the farm, type of fukicide used and clinical fasciolosis. Conclusions: The present study provides up‑to‑date information on the prevalence of F. hepatica in Irish sheep and adds insight to the epidemiology of the disease. These fndings will be useful for designing new holistic control meas‑ ures for F. hepatica infection. Keywords: Fasciola hepatica, Sheep, Prevalence, Co‑infection, Calicophoron daubneyi, Breed, Treatment, Flukicide, Liver fuke *Correspondence: [email protected] 1 Animal and Grassland Research and Innovation Centre (AGRIC), Teagasc, Moorepark, Fermoy, County Cork, Ireland Full list of author information is available at the end of the article © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Munita et al. Parasites Vectors (2019) 12:525 Page 2 of 14 Background diference between the two parasites is their pathology. Fasciola hepatica, commonly known as the liver fuke, Following ingestion and excystment, F. hepatica will is a helminth parasite of mammals and a member of migrate from the intestinal lumen, from the intestinal the Class Trematoda [1, 2]. It infects cattle, sheep, goat, wall and peritoneum to reach the bile ducts for matura- horse, deer and humans as defnitive hosts [3]. Te par- tion [3], whereas immature paramphistome will attach asite has a worldwide distribution and is considered an to the small intestine mucosa for feeding before reaching important disease of domestic livestock, especially in the fore stomachs for maturation [15]. In contrast to F. temperate climatic zones [4]. Fasciolosis has been esti- hepatica, clinical paramphistomosis is rare, and is chiefy mated to account for annual losses of €90 million to the caused by large burdens of juveniles in the small intestine Irish livestock industry and €2.5 billion worldwide [5]. as adults in the forestomachs appear to be well tolerated In sheep, liver fuke infection afects productivity and [12, 15]. While F. hepatica can be treated with a range of welfare [3]. It is a predisposing risk factor for mastitis [6] fukicides, adult rumen fukes are only susceptible to oxy- and drop in coagulation parameters [7]. Te ingestion of clozanide, with closantel being reported as having some large numbers of infective stages of the parasite can cause efcacy against adult stages [16, 17]. Tis factor limits a highly pathogenic sub-acute presentation in lambs, its control and increases the possibility of resistance as characterised by hepatic haemorrhage and lesions, treatment rotations are not applicable [18]. Te possibil- resulting in sudden death [1, 8]. Infammatory mediators ity that rumen fuke has adapted to the Irish climate more from liver damage might also afect early pregnancy [8]. efectively than liver fuke, in addition to the fact that Chronic fasciolosis, the most common clinical presen- treatment against F. hepatica opens up the niche for par- tation, might lead to emaciation, especially in more sus- amphistomes, may result in the gradual replacement of F. ceptible animals and in ewes in the advanced stages of hepatica by paramphistomes [19]. gestation [8]. In contrast to the dairy and beef sector, the A previous F. hepatica pilot prevalence study in a small cost of liver fuke in sheep enterprises is largely unquanti- population of Irish sheep confrmed infection in 62% of fed at a national and regional level [9]. animals [20], one of the highest recorded in Europe [9]. Fasciola hepatica has an indirect life-cycle, with lar- Tere are no up-to-date cross-sectional prevalence stud- val stages depending on a molluscan intermediate host ies of F. hepatica in Irish sheep. Also, information on the for their development. Te intermediate host species is relationship between F. hepatica, management factors largely determined by geographical location. In Europe, and paramphistomes on a national scale is scarce. Te the most important snail in the fuke life-cycle is Galba present study aimed to generate national prevalence data truncatula [10]. In Ireland, Radix spp. and other genera for F. hepatica in Irish sheep focks and to conduct a risk have also been described as intermediate hosts, in addi- analysis based on management and treatment practices tion to G. truncatula [11]. Temperature and moisture are in participating focks. Additionally, the study aimed to the most important environmental factors for the pres- quantify the association and level of co-infection with ence of G. truncatula and F. hepatica development as wet rumen fuke. soils with temperatures higher than 10 °C are required for their development [2]. Te Irish climate provides ideal Methods environmental conditions for F. hepatica in winter and Sample population early summer. Te peak of infection in Irish sheep usually Te present study was conducted between November occurs in late winter and spring, following the summer 2014 and January 2015, coinciding with the high-risk infection of snails [8]. Conventionally control meas- period for fuke infection in the Irish temperate climate; ures against F. hepatica chiefy rely on the use of anthel- 2014 was considered to be one of the warmest years in mintics. However, ideally, management practices and Ireland [21], probably benefting the parasite. Flocks treatment should be used strategically, based on diagno- were recruited using Teagasc (Irish Food and Agricul- sis- and evidence-based control measures for efectively ture Development Authority) networks of Irish sheep reducing parasite burdens. farmers via 50 national Teagasc sheep advisors. Addi- Paramphistomes, or rumen fukes, are represented tionally, application forms were distributed through by Calicophoron daubneyi and Paramphistomum ley- Teagasc Newsletters and the Irish Farmer’s Journal for deni in Ireland; however, the predominant species is C. circulation within farming and related communities. daubneyi [12, 13]. Rumen fukes infect the same inter- Te application form consisted of a short question- mediate snail hosts as F. hepatica [14]. Infections of both naire requesting the Teagasc advisor’s name, herd num- rumen fukes and F. hepatica are acquired by ingestion ber, farmer’s name, postal address, GPS coordinates of encysted metacercariae on grass. Probably the biggest of the farmyard, mobile number, fock size (number Munita et al. Parasites Vectors (2019) 12:525 Page 3 of 14 of breeding animals), lambing season and preferred Flock classifcation and management practices months of sampling. More than 350 applications were Te classifcation of F. hepatica status (positive or nega- received. A total of 322 focks were targeted, selected tive) was assigned based on the presence or absence of by stratifed geographical location and fock size, to liver fuke eggs in pooled faecal samples. Classifcation of represent the national geographic spread according co-infection (observed or not observed) was assigned to to the Census of Agriculture (2010) [22]. Once focks focks based on the presence or absence of both F. hepat- were selected, farmers were informed by post and were ica and rumen fuke eggs in the pooled samples. requested to post back a consent form and dosing pro- Region (west, east and south) and fock size were tocols.