Echinococcus infections in the Baltic region

Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2015 Echinococcus infections in the Baltic region Marcinkute, Audrone ; Šarkunas, Mindaugas ; Moks, Epp ; Saarma, Urmas ; Jokelainen, Pikka ; Bagrade, Guna ; Laivacuma, Sniedze ; Strupas, Kęstutis ; Sokolovas, Vitalijus ; Deplazes, Peter Abstract: In the Baltic countries, the two zoonotic diseases, alveolar echinococcosis (AE) caused by Echinococcus multilocularis, and cystic echinococcosis (CE) caused by Echinococcus granulosus, are of increasing public health concern. Observations from Estonia, Latvia and Lithuania indicate that the distribution of both parasites is wider in the Baltics than previously expected. In this paper, we review and discuss the available data, regarding both parasitoses in animals and humans, from the Baltic countries and selected adjacent regions. The data are not easily comparable but reveal a worrisome situation as the number of human AE and CE cases is increasing. Despite improvements in diagnostics and treatment, AE has a high morbidity and mortality in the Baltic region. For the control of both zoonoses, monitoring transmission patterns and timely diagnosis in humans as well as the development of local control programs present major challenges. DOI: https://doi.org/10.1016/j.vetpar.2015.07.032 Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-114969 Journal Article Published Version The following work is licensed under a Creative Commons: Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) License. Originally published at: Marcinkute, Audrone; Šarkunas, Mindaugas; Moks, Epp; Saarma, Urmas; Jokelainen, Pikka; Bagrade, Guna; Laivacuma, Sniedze; Strupas, Kęstutis; Sokolovas, Vitalijus; Deplazes, Peter (2015). Echinococcus infections in the Baltic region. Veterinary Parasitology, 213(3-4):121-131. DOI: https://doi.org/10.1016/j.vetpar.2015.07.032 Veterinary Parasitology 213 (2015) 121–131 Contents lists available at ScienceDirect Veterinary Parasitology journal homepage: www.elsevier.com/locate/vetpar Echinococcus infections in the Baltic region Audronė Marcinkutė a,1 , Mindaugas Šarkūnas b,∗,1 , Epp Moks c , Urmas Saarma c , ˛ Strupas h , Pikka Jokelainen d,e , Guna Bagrade f , Sniedze Laivacuma g , Kestutis h i Vitalijus Sokolovas , Peter Deplazes a Clinic of Infectious, Chest Diseases, Dermatovenereology and Allergology, Vilnius University and University Hospital Santariškiu˛ Clinics, Lithuania Department of Infectious Diseases, Veterinary Academy, Lithuanian University of Health Sciences, Tilžės Street 18, 47181 Kaunas, Lithuania c Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Estonia d Institute of Veterinary Medicine and Animal Sciences, Estonian University of Life Sciences, Tartu, Estonia e Faculty of Veterinary Medicine, University of Helsinki, Finland f Latvian State Forest Research Institute “Silava”, Salaspils, Latvia g Riga Stradins University, Riga, Latvia h Santariškiu˛ Clinics, Vilnius University, Lithuania i Institute of Parasitology, University of Zürich, Switzerland b a r t i c l e i n f o Keywords: Echinococcus multilocularis Echinococcus granulosus Echinococcosis Emerging infectious diseases Estonia Latvia Lithuania Epidemiology Zoonoses a b s t r a c t In the Baltic countries, the two zoonotic diseases, alveolar echinococcosis (AE) caused by Echinococcus multilocularis, and cystic echinococcosis (CE) caused by Echinococcus granulosus, are of increasing public health concern. Observations from Estonia, Latvia and Lithuania indicate that the distribution of both parasites is wider in the Baltics than previously expected. In this paper, we review and discuss the available data, regarding both parasitoses in animals and humans, from the Baltic countries and selected adjacent regions. The data are not easily comparable but reveal a worrisome situation as the number of human AE and CE cases is increasing. Despite improvements in diagnostics and treatment, AE has a high morbidity and mortality in the Baltic region. For the control of both zoonoses, monitoring transmission patterns and timely diagnosis in humans as well as the development of local control programs present major challenges. © 2015 Published by Elsevier B.V. 1. Introduction Species of the genus Echinococcus Rudolphi, 1801 are small intestinal cestodes of carnivore definitive hosts. Parasite eggs, which can survive in the environment, are infective to a variety of herbivorous and omnivorous intermediate or accidental hosts. The larval stages (metacestodes) in the intermediate hosts have a high potential for asexual reproduction and production of numerous protoscoleces (Thompson, 1995). Metacestodes of Echinococcus granulosus, a complex of species, strains and genotypes with a taxonomy under revision (reviewed Romig et al., 2015), are causing cystic echinococcosis (CE; hydatic disease) in intermediate and in human accidental hosts, with a high global burden of disease (Budke et al., 2006). Metacestodes (cysts from a few cm to up to 10–30 cm) can be seen during meat inspection, autopsy or necropsy. Therefore, in contrast to many ∗ Corresponding author. E-mail address: [email protected] (M. Šarkūnas). 1 These authors contributed equally to this study. http://dx.doi.org/10.1016/j.vetpar.2015.07.032 0304-4017/© 2015 Published by Elsevier B.V. other infectious diseases, historic observations are of value for the understanding of the epidemiology of these zoonotic parasites. The “northern biotype of E. granulosus” (Raush, 1995), currently named E. canadensis, which includes the cervid strain or genotypes G8 and G10 (Romig et al., 2015; Oksanen and Lavikainen, 2015), is transmitted almost exclusively in a wild animal cycle with the wolf as definitive hosts and ungulates of the family Cervidae as intermediate hosts. In addition, domesticated reindeer and dogs (as definitive hosts) can be involved in certain epidemiological situations. Only few zoonotic infections with the cervid strain have been observed in humans, associated with relatively moderate pathology, mainly in the lungs (Romig et al., 2015; Oksanen and Lavikainen, 2015). In contrast, in endemic regions of southern and central Europe, E. granulosus (sheep strain, genotypes G1, G2, G3), and E. granulosus pig strain (genotype G7; also grouped under E. canadensis, and proposed as E. intermedius) occur mostly in synanthropic cycles with the domestic dog as definitive and sheep (G1) or pigs (G7) as major intermediate hosts, respectively. Echinococcus multilocularis is transmitted in Europe mainly by wild animals, with the red fox (Vulpes vulpes), the wolf (Canis lupus) and the raccoon dog (Nyctereutes procyonoides) as definitive hosts 122 A.. Marcinkutė et al. / Veterinary Parasitology 213 (2015) 121–131 Table 1 Echinococcus species recorded until 2014 in the Baltic countries Estonia, Latvia and Lithuania. Country Species, strain (genotype) Definitive hosts Intermediate and aberranta hosts, (human) References Estonia E. granulosus Dog Pig, cattle, sheep, moose E. granulosus (G1) E. canadensis, cervid strains (G8, G10) E. multilocularis Dog Wolf Moose, roe deer Saar (1931); Lešins (1955); University of Tartu (zoological collection) Laurimaa et al. (2015b) Moks et al. (2006, 2008); I. Jõgisalu (pers. comm.) Moks et al. (2005), Laurimaa et al. (2015c) Latvia Lithuania a E. granulosus E. canadensis, cervid strain (G10) E. multilocularis E. granulosus E. granulosus; pig strain (G7) E. multilocularis Fox, raccoon dog Pig, sheep Wolf Fox, wolf, raccoon dog Vaivarina (1950) Bagrade and Saarma (unpublished) Bagrade et al. (2008, 2009);Bagrade, (2008);Poļakova, (2009) Dog, wolf Dog Pig, cattle, sheep (human) Pig, cattle,a human Fox, raccoon dog, dog Ondatra zibethicus, (Microtus sp.; pig,a human) Historic citations see Sections 5.1.1 and 5.2.1 Bružinskaitė et al. (2009); Marcinkutė et al. (2006) Mažeika et al. (2003) ; Bružinskaitė et al. (2007, 2009); Bružinskaitė-Schmidhalter et al. (2012); (Loibiene R. and Šarkūnas M., personal communication) Non-fertile metacestodes, therefore no significance for transmission. and rodents mainly of the genera Arvicola, Microtus and Myodes as intermediate hosts (Eckert et al., 2011). Domestic dogs and, to a lesser extent, cats can be involved in the transmission cycle (Deplazes et al., 2011). The parasite is endemic in the northern hemisphere: the highest prevalence of infection is reported in Central Europe, North America (mostly in Alaska and the northern part of Canada) and in the arctic, subarctic and temperate climate zones of Asia (Eckert et al., 2011). Humans may get infected by uptake of eggs, and the tumour-like growth of the metacestode stage of E. multilocularis, mainly in the liver, may lead to a serious disease—alveolar echinococcosis (AE). The numbers of recently reported human AE cases have increased in some endemic areas in Central Europe as well as in the Baltics (Bružinskaitė et al., 2007) and Poland (Nahorski et al., 2013). Although generally a rare disease, AE is of considerable public health importance because of the severe pathology of the tumour-like infection, the high lethality rate of untreated cases and high cost of treatment (WHO, 2001; Vuitton et al., 2015). Since the 1990s, extensive epidemiological studies have revealed that the known central–European endemic area of E. multilocularis is much larger than previously known, including regions in the north and east (WHO, 2001; Romig et al., 2006; Sikó et al., 2011; Vuitton et al., 2015). The parasite has been reported in the Baltics in Lithuania (Mažeika et al., 2003), Estonia (Moks et al., 2005) and Latvia (Bagrade et al., 2008), and in neighbouring Poland (Malczewski et al., 1995) and Belarus (Shimalov and Shimalov, 2001). In this paper, we review historic and recent epidemiological data from the Baltic region, including locally published reports that are not easily available to a broader readership. 2. Echinococcus spp. in the Baltic countries Since the 1990s, due to the changes in the epidemiological situation or improved diagnostic techniques and medical care, the number of registered human CE and later on AE cases started to increase in Lithuania and Latvia, while remaining at relatively low levels in Estonia. Most information on Echinococcus infections is available for animals. Recent and historic data are reviewed for the different Baltic countries in the following chapters. As shown in Table 1, four confirmed genotypes of the E. granulosus complex, namely the sheep strain (G1), pig strain (G7), and cervid strains (G8 and G10), have been identified in different hosts. The first report on an E. multilocularis infection in the region was published in 2003 in Lithuania (Mažeika et al., 2003), followed shortly by reports from the two other Baltic countries. To date, most data are available from definitive hosts, whereas the intermediate rodent hosts have not been systematically investigated for the presence of E. multilocularis in the Baltic region. 3. Occurrence and transmission of Echinococcus spp. in Estonia 3.1. Animal infections in Estonia 3.1.1. Echinococcus granulosus complex Historically, the first Estonian record of E. granulosus dates back to 1904 when the parasite was included in the zoological collection of the University of Tartu. The material was collected near the town Tartu. Unfortunately, the host was not documented and the sample is not preserved. However, E. granulosus cysts were reported in the 1930s from pigs (Saar, 1931), and later in pigs, sheep and wild cervids (Lešins, 1955). Notably, 147 (15.7%) out of 938 pigs were infected (Lešins, 1955). Prevalences ranged between 5 and 31.4% in different areas and were highest in counties near the Latvian border and Lake Peipus. The parasite was also detected in other intermediate host species: in 10 out of 244 sheep (4.1%) and in 7 out of 1117 (0.6%) large cervids (unspecified, presumably moose, Alces alces). After that, there were no more reports of Echinococcus infections for almost half a century, neither from the meat inspections nor from parasitological investigations of wild cervids in the 1970s (Järvis, 1993). In more recent studies, E. granulosus has been found in Estonian wildlife. Wild intermediate host species include moose and roe deer (Capreolus capreolus), whereas the grey wolf has been identified as the definitive host. In domesticated intermediate hosts, the parasite has been detected in pigs, sheep and cattle (Tables 1 and 2; Estonian Veterinary and Food Laboratory, 2014). In 2003, adult stages of the E. granulosus complex were detected in 1 out of 26 investigated grey wolves (3.8%; Moks et al., 2006). The parasite was identified as E. canadensis (G10). Infection in wolves and wild cervids (Moks et al., 2006, 2008; I. Jõgisalu, Estonian Environmental Agency, personal communication) suggest a wild animal cycle for this tapeworm in Estonia. In 2004–2005, E. canadensis cysts were detected in 16 (0.8%) out of 123 A.. Marcinkutė et al. / Veterinary Parasitology 213 (2015) 121–131 2038 hunted moose (Moks et al., 2008). Most of the cysts were in the lungs, and the number of cysts ranged from one to six per animal. The phylogenetic position of the Estonian genotypes has been examined in detail (Moks et al., 2008; Saarma et al., 2009). Of the parasite samples from moose, 11 belonged to genotype G8 and 5 to genotype G10, and this was the first record of G8 in Eurasia (Moks et al., 2008). The Estonian Veterinary and Food Laboratory has reported a few cases of Echinococcus sp. infections in farm animals and in wildlife in 2004–2006, likely to belong to the E. granulosus complex (Estonian Veterinary and Food Laboratory, 2014). In 2004, 4 out of 444 084 pigs (0.0009%) and 8 out of 6202 moose (0.1%) were found to be infected. Cysts were also detected in 2 out of 1787 imported reindeers (0.1%) in 2005, and in 1 out of 53 903 cattle (0.002%) in 2007. Although there are no reported cases of E. granulosus infection in companion animals, a recent investigation revealed this species in dogs (Laurimaa et al., 2015b). 3.1.2 Echinococcus multilocularis E. multilocularis has been found in Estonia in both rural and urban areas, but so far only in the definitive host species (Table 1). The parasite was identified in Estonia for the first time in 2003 (Moks et al., 2005) in 5 out of 17 (29.4%) red foxes. In these foxes, the number of adult E. multilocularis ranged from 3 to 927, and the parasite species was confirmed with molecular methods including sequencing. A more recent study, involving a considerably larger number of red foxes from across the country, showed that the prevalence of E. multilocularis in red foxes has remained virtually unchanged (Laurimaa L., unpublished data). E. multilocularis was recently identified also in raccoon dogs (Laurimaa et al., 2015c). The red fox and raccoon dog were the main hosts of rabies in Estonia for decades (Süld et al., 2014). In 2013, Estonia officially declared its rabies-free status. Shortly after the start of the antirabies vaccination campaign in autumn 2005, the number of foxes and raccoon dogs increased considerably. Moreover, foxes started to colonize Estonian urban areas, where they have been reported in 33 out of the 47 cities nationwide (Plumer et al., 2014). In the city of Tartu, 2 (7.1%) out of 28 fox faeces but none of the analysed 91 dog faeces were positive for E. multilocularis (Laurimaa et al., 2015a). In this study a non-invasive genetic method was applied that allows the identification of both E. multilocularis and the host species from carnivore faecal samples. 3.2. Human infections in Estonia To date, 13 cases of echinococcosis in humans have officially been registered in Estonia (Estonian Health Board, 2014). However, AE and CE have yet to be confirmed in this country as the causative species of Echinococcus was not identified. These human echinococcosis cases have been reported as follows: single cases in 1986, 2000, 2003, 2008, and 2014 (until September 2014); two cases in 2007; and three cases in both 2012 and 2013. The patient in the year 1986 was a foreigner, and three other cases are classified as imported. Only two cases of human echinococcosis have been described in more detail. In one of them, a single large cyst (15 × 12 × 10 cm) was successfully surgically removed from the right lung of a 62-yearold male patient (Lapidus et al., 2004). The diagnosis was confirmed by histopathology based on wall structure and presence of protoscoleces. In another case a suspected liver cyst was removed laparoscopically from a younger female patient complaining of severe abdominal pain in 2005. During surgery, the cyst ruptured, and in the following years new cysts were found in several organs, and further surgical interventions and albendazole treatment were attempted with limited success (Kivi, 2011). 4. Occurrence and transmission of Echinococcus spp. in Latvia 4.1. Animal infections in Latvia 4.1.1. Echinococcus granulosus complex Historical data on Echinococcus infections in Latvia is limited. Based on slaughterhouse records, 0.8% of sheep and 2.8% of pigs were infected with E. granulosus (Vaivarina, 1950; reviewed by Danilevičus, 1964). The pig–dog life cycle was considered most typical for the region. Collected data from the archive of the Parasitological Laboratory (Latvia University of Agriculture, Faculty of Veterinary Medicine) on dynamics of helminthoses in Latvia in 1976–1996 shows that the incidence of echinococcosis in cattle was 0.001–0.11%, 0.005–0.2% in sheep and 0.002–0.2% in pigs (Anna Krūklı̄te, Faculty of Veterinary Medicine, Latvia, personal communication). Furthermore, the Latvian Food and Veterinary Service has reported cases of echinococcosis in farm animals in 2004–2007 and 2010 of <0.2% (LFVS, 2004–2010). These reported cases were not specified, but most likely belong to the E. granulosus complex. There are no confirmed reported cases on E. granulosus infection in dogs in Latvia for at least two decades. Genetically confirmed data on E. granulosus infection in Latvian wildlife is available for wolves (Bagrade and Saarma, unpublished data), (Tables 1 and 3). Echinococcus parasites identified by morphological features have been detected in 1 (2.9%) of 34 investigated wolves (Bagrade et al., 2009), however this finding was later confirmed to be E. canadensis (G10) (Bagrade and Saarma, unpublished data). There is no recent information about Echinococcus infection in wild intermediate host species, and historical research done on the helminth fauna of cervids has not revealed CE infections (Prieditis and Daija, 1972; Michelson, 1976). The populations of Table 2 Prevalence studies on E. granulosus and E. multilocularis in wild and domestic animals in Estonia. Host species Echinococcus sp. No positive/investigated Prevalence % (95% CI) Location (if specified) References Pig Sheep Moose Pig Moose Reindeer Cattle Fox Wolf Moose Fox Dog Raccoon dog E. granulosus E. granulosus E. granulosus Echinococcus sp. Echinococcus sp. Echinococcus sp. Echinococcus sp. E. multilocularis E. granulosus (G10) E. granulosus(G8, G10) E. multilocularis E. granulosus (G1) E. multilocularis 147/938 10/244 7/1117 4/444 084 8/6202 2/1787 1/53903 5/17 1/26 16/2038 2/28 4/181 4/249 15.7 (13.5–18.1) 4.1 (2.1–7.2) 0.6 (0.3–1.2) 0.0009 (0.0004–0.002) 0.1 (0.06–0.2) 0.1 (0.02–0.4) 0.002 (0.0005–0.009) 29.4 (11.7–53.7) 4 (0–14) 0.8 (0.5–1.2) 7.1(1.2–21.7) 2.2 (0.6–5.6) 1.6 (2.4–5.6) Eastern and Southeastern Estonia Slaughterhouses in Tartu, Otepää Slaughterhouses in Mustvee, Võru Most parts of Estonia Most parts of Estonia Imported Most parts of Estonia Tartumaa, Põlvama, Hiiumaa Järvamaa Harjumaa, Raplamaa, Läänemaa, Pärnumaa Tartu, urban foxes Tartu (urban area) Järvamaa, Saaremaa Lešins (1955) a EVFL—Estonian Veterinary and Food Laboratory, 2014. EVFLa EVFLa EVFLa Moks et al. (2005) Moks et al. (2006) Moks et al. (2008) Laurimaa et al. (2015a) Laurimaa et al. (2015b) Laurimaa et al. (2015c) 124 A.. Marcinkutė et al. / Veterinary Parasitology 213 (2015) 121–131 Table 3 Prevalence studies on E. granulosus and E. multilocularis in wild and domestic animals in Latvia. Host species Echinococcus sp. Sheep Pig Fox E. granulosus E. granulosus E. multilocularis No positive/investigated Prevalence% (95% CI) Location (if specified) References Not specified Vaivarina (1950) 16/45 8/42 0.8 2.8 35.6 (23.2–50.2) 19.1 (10.0–33.3) Bagrade et al. (2008) Poļakova (2009) Raccoon dog E. multilocularis E. granulosus E. multilocularis 2/34 1/34 1/19 6/42 5.9 (0.65–20.07) 2.9 (0.00–16.22) 5.3 (0.1–26.0) 14.3 (5.4–28.5) Pig Cattle Sheep and goats Echinococcus sp. Echinococcus sp. Echinococcus sp. 2/504680 1/90760 1/8978 Most parts of Latvia Rı̄ga, Valka and Jelgava districts Dobele, Ugāle Saulkrasti Ugāle Rı̄ga, Valmiera and Jelgava districts Most parts of Latvia Most parts of Latvia Most parts of Latvia Wolf a 0.0004 0.001 0.01 Bagrade et al. (2009) Bagrade (2008) Poļakova (2009) LFVSa LFVSa LFVSa LFVS - Latvian Food and Veterinary Service, 2004—2010. wildlife animals involved in the known E. canadensis (G10) life cycle are stable with a tendency to increase in Latvia (data of the State Forest Service). Echinococcus identified based on morphological features on genus level, has been reported in foxes hunted in Latvia (Keidāns et al., 2005) and Echinococcus metacestodes have been diagnosed in beavers (Castor fiber) (Kaspržaka et al., 2004). However, in both these findings, the Echinococcus sp. was not confirmed by molecular tools. 4.1.2 Echinococcus multilocularis So far, E. multilocularis parasites in Latvian wildlife have been found in canids (Tables 1 and 3). Investigations of red foxes (n = 45) during 2003–2008 from various regions of the country revealed a prevalence of 35.6% with an intensity of infection ranging from 1 to 1438 worms (Bagrade et al., 2008). In the same study, 19 raccoon dogs were examined, and a lower prevalence of 5.3% was determined (Bagrade, 2008). Other investigations conducted by the former National Diagnostic Centre of Latvia (now Institute of Food Safety, Animal Health and Environment “BIOR”) in 2007–2008 (material collected from 3 head forestries) revealed prevalences of 14.3% in raccoon dogs (n = 42) and 19.1% in foxes (n = 42) (Poļakova, 2009). A recently performed survey (2010–2014) conducted by “BIOR” in collaboration with LSFRI “Silava” on the helminth fauna of foxes (n = 430) and raccoon dogs (n = 305) in Latvia revealed almost a halved prevalence of E. multilocularis in foxes whereas the prevalence in raccoon dogs was similar to the data of the survey conducted in 2003–2008 (Bagrade and Deksne, unpublished data). The population of raccoon dogs in Latvia is stable but there has been a decreasing tendency of fox numbers in recent years (data of the State Forest Service). From 34 wolves examined, 2 (5.9%) were infected with E. multilocularis with worm burdens of 62 and 380 (Bagrade et al., 2009). 4.2. Human infections in Latvia 4.2.1 Cystic echinococcosis Only fragmented information is available concerning the epidemiological situation of human CE and AE in Latvia. In the period 1999–2005, 29 CE cases were registered at the Infectology Centre of Latvia (Keiss et al., 2007). During the last decade, awareness of echinococcosis has increased and since 2001, an increase in human CE cases has been recorded. In the Infectology Centre of Latvia, 11 new cases were registered (0.43/100.000 inhabitants per year) in 2005. Later on, the number of diagnosed human CE cases has risen to 17 in 2008 (0.77 cases/100.000 inhabitants per year) but decreased and remained stable in the years 2009–2012 (0.27–0.34 cases /100.000 inhabitants per year). Since echinococcosis is not a notifiable infectious disease in Latvia, the number of presently reported cases is probably underestimated. Data of 93 Latvian patients with CE, diagnosed in the period between 2002 and 2012, was recently reported by Laivacuma and Viksna (2014a). Diagnosis was based on ultrasonography and computer tomography (CT), serology and in some cases morphological investigations of biopsy or surgically obtained material from space occupying lesions. The majority (72.7%) of CE patients were females aged between 56 and 65 years. The majority of patients lived in a rural household (71.9%) and owned dogs (56.1%) or livestock (35.1%). The most frequent complaints at the moment of admission were abdominal discomfort or tightness (38.5%), abdominal pain (24.0%), malaise (15.4%), jaundice (11.5%) and skin itching (10.6%). Ultrasound analyses showed that echinococcosis manifested more often as a solitary lesion (64.9%) in the right hepatic lobe (62.2%) in an otherwise unchanged liver (65.8%). The size of lesion was <5 cm in 40.5% of cases. Analysis of the cysts at the moment of diagnosis most often revealed 3rd (CE3) and 4th (CE4) stage (according to the WHO classification criteria). Chemotherapy was applied in 82 out of 93 patients (88.5%), but most patients received only one course of albendazole per year. Radical metacestode resection was performed in 18 (19.3%) patients, while PAIR was performed on 19 (20.4%) patients (Laivacuma and Viksna, 2014a). 4.2.2 Alveolar echinococcosis As with CE, no systematic data collection on the occurrence of AE in Latvia has been done. In the report by Tulin et al. (2012), 29 AE cases registered at the Pauls Stradins University Hospital during the period 1996–2010 are summarised. Radical operations were performed in 12 (41.3%) of these AE patients, 11 of them had asymptomatic or none complicated disease. Recurrence appeared in 1 patient (8.3%). Non-radical or palliative operations due to AE complications were performed in 15 patients (51.7%). Postoperative complications occurred in 17% of AE patients, and 1 patient died. In the period 1999–2010, 14 human AE cases were registered at the Infectology Centre of Latvia. As diagnosis was mainly based on serological findings, seronegative cases of AE must be considered. Eleven of these AE patients were women. At the time of diagnosis, the youngest patient was 13 and the oldest 63 years old (majority of patients were of 51–56 years old). Ultrasonographic evaluation of Echinococcus lesions showed that all patients had abnormalities in the liver, but in 2 patients other organs (kidney and lung) were affected. In 6 patients, structures adjacent to the liver (bile ducts and blood vessels) were affected by the metacestode, which is characteristic for E. multilocularis infections (Laivacuma and Viksna, 2014b). A.. Marcinkutė et al. / Veterinary Parasitology 213 (2015) 121–131 5. Occurrence and transmission of Echinococcus spp. in Lithuania 5.1. Animal infections in Lithuania 5.1.1. Echinococcus granulosus complex First historical cases of E. granulosus cysts in cattle (Gelažius, 1924) and pigs (Sniečkienė, 1937) in Lithuania were mentioned by veterinary practitioners. In the 1960s, single cases were registered in livestock animals (Nainys and Kazlauskas, 1954; Šivickis, 1955). More detailed observations were reported by Čygas (1956, 1957) in four districts of central Lithuania: 22.3% of pigs (215/965; CI 19.7–25.0), 6.7% of sheep (39/580; CI 4.8–9.1) and 1.1% of cattle (8/729; CI 0.5–2.2) were infected with E. granulosus metacestodes. Epidemiological investigations for Echinococcus spp. in animals are summarised in Table 4. In a study on seasonal dynamics of E. granulosus in pigs (Danilevičius, 1962), the prevalences were comparable during all seasons in pigs over 9 months of age. However, in 7–9 and 3–7 month old pigs, prevalences increased from 5.2% and 1.8% in April to 12.3% and 5.4% in November, respectively. Danilevičius (1964) reported prevalences of E. granulosus in pigs ranging between 5.0 and 12.9% in most parts of Lithuania (1961–1962; n = 30 641). The prevalence was higher in pigs from small farms (10.5%) when compared to those in large industrial farms (8.3%). Home slaughtering of pigs and sheep is traditional in Lithuania, and E. granulosus was documented in a dog-pig life cycle in the sixties (Danilevičius, 1964). The helminth fauna of carnivores from Lithuania has been investigated in few earlier studies. During necropsy of various carnivores, E. granulosus was found in 4 out of 19 dogs (21.0%) and 1 out of 41 wolves (2.4%) (Kazlauskas and Prūsaitė, 1976). According to Musteikaitė et al. (1961), amongst other Taeniid cestodes, E. granulosus was prevalent in 5 out of 83 (6.02%) necropsied dogs from south-eastern Lithuania while no E. granulosus infection was found in cats. The mean prevalence of E. granulosus in dogs was 7.8% (1958–1962; n = 102) in the south and north of Lithuania, with more frequent infections in rural dogs (6 out of 44 dogs; 13.6%) as compared to urban dogs (2 out of 58 dogs from Vilnius Šiauliai; 3.4%;) (Danilevičius, 1964). From the sixties until the end of the century, only data from the Lithuanian State Veterinary Service (LSVS) on prevalences of Echinococcus infections in slaughtered animals was available. According to this data, the annual incidences of E. granulosus were 0.02–0.1% in cattle and 0.04–1.09% in pigs (LSVS, 1996). In a study performed in the southwestern part of Lithuania during 2005–2006, CE was detected in 13.2% (81/612) of pigs reared in small family farms and in 4.1% of those reared in industrial farms. Molecular analysis of isolated taeniid eggs revealed Taenia spp. in 10.8%, E. granulosus (G 6/7) in 3.8% and E. multilocularis in 0.8% of the dogs investigated. In addition, 3 samples from livers of humans, 1 sample from a cow, 7 samples from pigs, and eggs from 8 dog faeces samples confirmed the presence of the ‘pig strain’ (G 6/7) (Bružinskaitė et al., 2009). The high prevalence of CE (13.2%), T. hydatigena larval stages (2.5%) and E. multilocularis lesions (0.5%) in pigs indicates that there is a high exposure of pigs to cestode eggs primarily in small farms where dogs are often kept to guard the premises. Usually, the majority of these dogs are chained, which may limit their access to offal of home-slaughtered pigs. However, 3.5% of chained dogs were infected with E. granulosus, possibly due to the fact that many dogs were fed with offal, without regular anthelmintic treatment. Presently, a significant proportion of pigs (36%) are reared in small family farms in Lithuania (Department of Statistics, Lithuania) and considerable numbers of these pigs, which are intended for home consumption, are slaughtered under home conditions. A 125 questionnaire study suggested that there may be some propensities for seasonal transmission of E. granulosus in Lithuania as 60.4% of farmers slaughter pigs during the cold period of the year. This tradition causing a seasonal transmission of E. granulosus infections has already been discussed by Danilevičius (1964). If confirmed, seasonal control programs could be effective against E. granulosus sensu lato (s.l.) in Lithuania. In a pilot study over 4 consecutive years in Lithuania (Radziulis et al., 2011), the effect of regular praziquantel dosing of dogs four times per year during the period of the most intensive pig slaughtering (October–April) in endemic villages was examined. It was shown that regular deworming of dogs was sufficient to reduce the prevalence of E. granulosus in dogs from 5.9% (CI95% 3.6–9.1%) to 0% (CI95% 0.0–0.9%), in contrast to the control villages without intervention in which no significant reduction was observed. The prevalence of CE in the villages with treated dogs was 38.2% and 44.2% in fattener pigs and sows, respectively, at the beginning of the study, and they decreased to 0% (CI95% 0.0–0.9%) in the third year of the study. 5.1.2. Echinococcus multilocularis The presence of the most important definitive and intermediate hosts for E. multilocularis suggested that conditions to maintain its life cycle are favourable in Lithuania. Important intermediate rodent hosts (e.g. Arvicola terrestris, Microtus arvalis) were recorded in Lithuania by Prūsaitė et al. (1988). In later studies performed in different landscapes of Lithuania, the presence of other possible intermediate hosts was recorded by Balčiauskas and Juškaitis (1997), Juškaitis and Baranauskas (2001), and Mažeikytė (2002). In these studies, it was shown that populations of rodents were mainly composed of Myodes glareolus, M. arvalis, Apodemus flavicolis, Microtus agrestis, and Apodemus agrarius. While the rodent intermediate hosts have not been investigated systematically in the past, E. multilocularis was identified morphologically for the first time in one of 5 muskrats (Ondatra zibethicus) captured in the Šilutė district (Mažeika et al., 2003). Only recently, in the framework of an EMIRO project, a first E. multilocularis infection in a Microtus sp. (out of 300) was observed (Loibienė R. and Šarkūnas M., personal communication). Furthermore, infertile and calcified metacestodes of E. multilocularis were identified by PCR in 0.5% (3/685) of pig livers, and 2 out of 240 dogs (0.8%) from the same area excreted E. multilocularis eggs (Bružinskaitė et al., 2009) as confirmed by multiplex PCR (Trachsel et al., 2007). Older studies in potential definitive hosts of E. multilocularis do not document the occurrence of this parasite in Lithuania. Out of 164 hunted red foxes (collected from 24 districts in the whole of Lithuania) and 10 raccoon dogs (from the northern part of Lithuania) examined morphologically, none were infected with Echinococcus spp. (Danilevičius, 1964). Furthermore, during necropsy of various carnivores, E. granulosus was identified in dogs and wolves but no record was made of Echinococcus spp. in 122 red foxes and 58 raccoon dogs examined (Kazlauskas and Prūsaitė, 1976). E. multilocularis intestinal stages were detected for the first time in a study performed during 2001–2006. E. multilocularis was isolated in 158 (58.7%) of 269 red foxes examined and positive foxes were found in most of the investigated areas in Lithuania (Bružinskaitė-Schmidhalter et al., 2012). Furthermore, in this study a high prevalence of E. multilocularis (53%; CI 37.9–68.3%) was registered in the suburban area of Kaunas city. Worm burdens varied between 1 and 20 924 (mean 1309), and 17% of the infected adult red foxes were harbouring heavy infections (>1000 worms per animal) while none of the juvenile foxes were heavily infected. This result differs from other studies that have suggested urban juvenile foxes play a major role in the transmission of E. multilocularis (Deplazes et al., 2004). 126 A.. Marcinkutė et al. / Veterinary Parasitology 213 (2015) 121–131 Table 4 Prevalence studies for E. granulosus and E. multilocularis in wild and domestic animals in Lithuania. Host species Echinococcus sp. No positive/investigated Prevalence % (95% CI) Location, if specified Reference Pig Dog Fox Raccoon dog E. granulosus E. granulosus Echinococcus sp. Echinococcus sp. 2 640/30 641 8/102 0/164 0/10 8.6 (8.3–8.9) 7.8 (3.8–14.9) 0.0 (0.00–2.75) 0.0 (0.00–32.09) Most parts of Lithuania Danilevičius (1964) Wolf Dog Fox Raccoon dog E. granulosus E. granulosus E. multilocularis E. multilocularis 1/41 4/19 0/122 0/58 2.4 (0.01–3.74) 21.0 (7.95–3.89) 0.0 (0.00–3.67) 0.0 (0.00–7.43) Not specified Kazlauskas and Prūsaitė (1976) Dog E. granulosus 5/83 6.0 (2.27–13.67) South eastern Lithuania Musteikaitė et al. (1961) Dog E. granulosus E. multilocularis 9/240 2/240 3.8 (1.7–7.0) 0.8 (0.1–0.3) Southwestern Lithuania Bružinskaitė et al. (2009) Dog E. granulosus E. multilocularis 19/360 4/360 5.28 (3.2–8.1) 1.11 (0.0–2.8) Southwestern Lithuania Radziulis et al. (2011) Fox Raccoon dog E. multilocularis E. multilocularis 158/269 7/85 58.7 (52.6–64.7) 8.2 (3.4–16.2) 22 Districts of Lithuania Bružinskaitė-Schmidhalter et al. (2012) The high prevalences and abundance of E. multilocularis in the different districts in rural and peri-urban red foxes (36–83%, up to 20,924 worms per animal) and raccoon dogs (0–17%, up to 2379 worms per animal) (Bružinskaitė, 2007) allow the conclusion that the whole of Lithuania has to be regarded as a highly endemic area with high environmental contamination with parasite eggs. 5.2. Human infections in Lithuania 5.2.1. Cystic echinococcosis In the 19th century, only single human CE cases were diagnosed in Lithuania, and during 1920–1940, three case reports with surgery or autopsy findings of CE were published (Dakinevičius, 1931; Buinevičius, 1935; Zubinas, 1936). In another report summarising surgical liver interventions in 400 patients between the 1940s and 1970s, liver CE was diagnosed in three patients (Šiurkus, 1969). Based on analysis of data collected from 54 hospitals in 1958–1961, seven cases of human CE were registered in Lithuania (Danilevičius, 1964). The age-range of the patients was 35–69 years. Two of the patients died. The morbidity during this period increased from 0.03/100.000 in 1958 to 0.1/100.000 in 1960. In the last decade, the diagnostic techniques have improved and the incidence of human CE cases has increased up to 13 new registered cases per year in 2005 (0.39/100.000 inhabitants per year) (Marcinkutė et al., 2006). Later on, the number of diagnosed human CE cases rose to 35 in 2009 (1.11 cases/100 000 inhabitants per year) remaining at a comparable level until 2013 (1.15 cases/100 000 inhabitants per year) (Table 5). The reported CE cases were recorded only at the University Hospital of Infectious Diseases and Tuberculosis and at the Santariškiu˛ Clinics, Vilnius University. As no obligatory notification of CE exists in Lithuania, it can be assumed that the number of reported cases is underestimated in some districts. Most CE cases were registered from southeastern and northwestern areas of Lithuania with a particularly high number of CE cases registered from the Vilnius district (Fig. 1). Based on these findings, the Vilnius district has to be considered a hyper-endemic zone. Based on the geographical distribution of findings in animal hosts and the origin of the reported human cases, it can be concluded that the transmission of E. granulosus may occur throughout the whole country. 5.2.2 Alveolar echinococcosis From 1997, when the first confirmed AE cases were diagnosed in Lithuania, until 2006, 80 AE cases have been diagnosed at the State Hospital for Tuberculosis and Infectious Diseases in cooperation with the Santariškiu˛ Clinic (Vilnius University) (Bružinskaitė et al., 2007). Diagnoses were based on serologic testing using ELISA (Bordier Affinity, Crissier, Switzerland), Western blot (LDBIO, Lyon, France) and imaging methods (ultrasound scan, computed tomography), and were confirmed by histopathologic examination or typical liver lesion morphologic features. Of these AE patients, 81% were farmers or people involved in agricultural activities. Since 2007, 10–23 new cases were recorded annually (Table 5). The AE cases were recorded from many parts of the country (Fig. 2) suggesting that the whole territory of Lithuania should be considered as an endemic area for AE. According to the data presented in Table 5, a total of 179 AE cases have been registered over a 16-year period (1997–2013). The mean age at first diagnosis was 60 years (range 21–83) and 65.9% were women. The incidence of AE varied from 0.03 in 2004 to 0.57 in 2009 and 0.74 in 2012 per 100,000 of inhabitants (Table 5). AE primarily affected the liver, mostly the right lobe and both lobes in about one third of the cases. A quarter of the cases had extra-hepatic disseminations. Despite diagnostic and treatment innovations, AE still causes a high mortality in Lithuania. In the period of 1997–2013, 130 of the 179 registered patients with human AE received anthelmintic treatment and 53 of them died within the 16-year observation period. The longest survival from diagnosis was 16 years (23.8% of them received radical surgery). Mortality was 3.3% in 2003, 15.1% in 2007, 3.6% on average during 2008–2010 and 9.9% in 2011–2013. In 35.4% of cases, survival was less than one year from diagnosis due to late diagnosis at stage IV of the disease. 6. Selected neighbouring areas 6.1. General considerations Historic data and new information concerning the occurrence of E. granulosus and E. multilocularis are available from the surrounding areas of Estonia, Latvia and Lithuania. It is obvious that CE has been present for decades in the area. Also E. multilocularis has been observed for several decades, at least focally, although it is not possible to estimate the abundance of this species retrospectively. 6.2. Poland Geographically, Poland is located south of the Baltic States and has been known as an endemic area of E. multilocularis since 1995. In this paper, however, we will only focus on the epidemiological 127 A.. Marcinkutė et al. / Veterinary Parasitology 213 (2015) 121–131 Table 5 Number of human cases and minimala incidences of cystic (CE) and alveolar echinococcosis (AE) originating from all regions of Lithuania and diagnosed at the University Hospital of Infectious Diseases and Tuberculosis and at the Santariškiu˛ Clinics, Vilnius University during 1995–2013 (A. Marcinkutė, Lithuanian (Vilnius) Echinoregistry, November 2014). 1997 1998 1999 2000 2001 2002 2003 CE Cases/year Incidence; cases/100.000 1 0.03 5 0.14 4 0.11 1 0.01 7 0.20 9 0.26 8 11 13 0.23 0.33 0.39 AE Cases/year Incidence; cases/100.000 No of died AE patients 1 0.03 – 0 0 – 0 0 – 1 0.03 – 4 16 0.12 0.46 1 1 a 2004 2005 2006 2007 9 8 0.028 0.25 9 16 17 17 0.26 0.47 0.51 0.52 3 1 7 7 2008 2009 2010 2011 2012 8 35 32 23 24 0.25 1.11 1.03 0.76 0.8 2013 2014 34 24 1.15 0.82 5 13 18 13 10 22 16 10 0.15 0.41 0.57 0.42 0.33 0.74 0.54 0.34 3 5 3 4 6 3 5 – As data from other hospitals is missing, the incidence may be underestimated. situation on the border area to Lithuania. CE has been documented in Poland in the past for example in pigs (4.5%), beef cattle (0.007%), sheep and goats (18.7%) (Derylo and Szilman, 1998); the occurrence of CE in pigs was confirmed recently (Gawor et al., 2014). As in Lithuania, the pig strain (G7) seems to be of major zoonotic significance in Poland (Dybicz et al., 2013). In red foxes, E. multilocularis was described for the first time in the Gdansk region, around 300 km away from Lithuanian border (Malczewski et al., 1995). The high prevalence of this tapeworm in red foxes in the northeast (34.5%) and southeast (39.3%) of Poland with foci of infection in some counties (up to 70% foxes infected) represents a high potential risk for human infection in these areas (Gawor et al., 2004; Karamon et al., 2014). A recent review about human AE (1990–2011) in Poland is documenting a continuous increase of AE cases during the last two decades (Nahorski et al., 2013). It should be noted that this increase began shortly after the first detection of the parasite in foxes. Considering the long incubation period of human AE of up to 15 years, it can be assumed that human AE already existed in the past. This view is supported by the fact that two AE patients were diagnosed in Poland in the seventies of the last century (Nahorski et al., 2013). 6.3. Belarus Data published in the late 1950s revealed that E. granulosus metacestodes were found in 1.3% of cattle, 2.8% of sheep and 14.4% of pigs in Belarus (Chashuk and Chunosov, 1958). The original paper is not available for detailed analysis but high prevalence of E. granulosus in pigs indicates that the dog–pig life cycle was probably present in that time. E. multilocularis was reported to occur in Belarus in animals, as adult and larval stages, and in humans decades ago. In a recent paper, a retrospective overview of data on the occurrence of E. multilocularis in its intermediate and definitive hosts was provided by Shimalov (2011). According to old records the E. multilocularis metacestodes were found in the striped field mouse (A. agrarius) in the Luninetsk district and in two bank voles (M. glareolus) from the Luninetsk and Vitebsk regions (Merkusheva, 1963). Later, metacestodes of E. multilocularis were probably found in beavers and bank voles in the Berezina Biosphere Reserve (Kolbin and Karasev, 1965; Arzamasov et al., 1982, 1983) however, these findings were most probably misdiagnosed as metacestodes of E. granulosus (Merkusheva and Bobkova, 1981). Fig. 1. Distribution of human cases of cystic echinococcosis in 1997–2013 in Lithuania. The numbers indicate cases reported in the districts. (A. Marcinkutė, Lithuanian Vilnius-Echinoregistry, 2013). 128 A.. Marcinkutė et al. / Veterinary Parasitology 213 (2015) 121–131 Fig. 2. Distribution of human cases of alveolar echinococcosis in 1997–2013 in Lithuania. The numbers indicate cases reported in the districts. (A. Marcinkutė, Lithuanian Vilnius-Echinoregistry). In the Bialowieza Forest, E. multilocularis metacestodes were found in the 1970s by Shimalov in the bank vole (M. glareolus) and field vole (M. agrestis) during field practice by biology students of the Brest State Pedagogical Institute (now Brest State University) (Shimalov, 2010). In the Belarusian Polesie, metacestodes of E. multilocularis were isolated from two common shrews (Sorex araneus), Eurasian water shrew (Neomys fodiens), tundra vole (Microtus oeconomus), common vole (Microstus arvalis), wood mouse (Apodemus sylvaticus), two common hamsters (Cricetus cricetus), muskrats (Ondatra zibethica), European water voles (A. terrestris), five bank voles (M. glareolus) and three field mice (A. agrarius) during 1980–1999 (Shimalov, 1991, 2002; Shimalov and Shimalov, 2001). In 2002, Anisimova (2002) reported E. multilocularis metacestodes in 2.6% of examined bank voles and 0.9% of striped field mice, trapped in the forest of Polesie State Radiation and Ecological Reserve while Dubina et al. (2002) in 1 out of 17 investigated nutria (Myocastor coypus) in the Vitebsk region. The definitive host for E. multilocularis is the red fox in the central (Anisimova, 2003) and the southern part of Belarus (Shimalov and Shimalov, 2001, 2003). However, information on cases of human AE is limited; two cases were briefly reviewed by Shimalov (2011). In one case, metacestodes were found in the liver of a woman from the Brest area (Korzan et al., 1997), the other patient was a woman from the Mogilev Region (Call for help, 2008). 6.4. North European part of Russia: Kaliningrad, Pskov and Saint Petersburg provinces Historically, the North European part of Russia was considered to be the area in the former Soviet Union with active transmission of E. multilocularis but no AE in humans (Peklo, 2014). While the possibility for E. multilocularis transmission in the domestic life cycle was questioned, E. granulosus was considered the only species in domestic animals in this part of Russia (Petrov, 1957). The same areas were considered endemic for E. granulosus by Darchenkova et al., (1998), mainly attributed to parasite transmission in traditional husbandry systems involving a dog–reindeer life cycle. 6.4.1. Kaliningrad province In this province, located between the southern Lithuanian and the northern Polish border, E. granulosus was reportedly prevalent in the 1960s. Data presented by Danilin (1961) showed that 0.55–6.8% of cattle and 11.3% of slaughtered pigs were infected with E. granulosus. Recently, 20 human Echinococcus sp. cases (0.1–0.3/100 000) were registered in adults during the years 2003–2012, and 1 case in a child during 1996–2012. The highest number of human cases was recorded in 2011: 4 cases, (0.42/100 000), (Peklo, 2014). 6.4.2. Pskov and Saint Petersburg provinces Until 1983, human Echinococcus infections were not recorded in this area due to the absence of a reporting system. In Pskov province, bordering Latvia and Estonia, 5 infections with Echinococcus sp. were registered in adults and 1 in a child during 1996–2012. This corresponds to 0.1/100 000 cases in adults (2003, 2006–2009) and 0.9/100 000 cases in children (2009) (Peklo, 2014). In the Saint-Petersburg province bordering Estonia, 18 infections with Echinococcus sp. were registered between 1996 and 2012 representing 0.06–0.2 cases per 100 000 of inhabitants. Interestingly, a high number of human Echinococcus cases were registered in large cities. For example, in 1996–2012 up to 14 cases/year were registered in adults in Saint-Petersburg (0.1–0.3/100,000) (Peklo, 2014). A.. Marcinkutė et al. / Veterinary Parasitology 213 (2015) 121–131 7. Discussion and conclusions E. granulosus (genotypes G1, G7, G8 and G10) and E. multilocularis are present in various wild and domestic animals in one or more of the Baltic States: Estonia, Latvia and Lithuania. However, the full host range and the transmission patterns need to be further investigated. A common problem is that available data on animal infections are scarce and thus the contribution of different hosts to the local epidemiology of these parasites is largely unknown. For Estonia and Latvia, the data originate primarily from few research projects, while official monitoring programs require substantial improvements. The domestic cycle of E. granulosus (pig strain) is best known in Lithuania. The small-scale, on-farm transmission pattern (farm dogs and pigs) and the seasonal home slaughtering tradition appear to be the major risks for parasite transmission in the rural environments. So far, this strain is considered responsible for the majority of human CE cases in Lithuania. A promising pilot control experiment confirmed that the treatment of dogs with praziquantel over 4 years during the season of home slaughtering of pigs significantly reduced parasite transmission. The wild animal cycle of E. canadensis (G8 and G10) has been in the focus in Latvia and Estonia. The main wild intermediate host species is moose. Dogs and wolves are the main definitive host species reported so far. The zoonotic significance of this strain has not been documented in the Baltic countries as yet. Observations from Estonia, Latvia and Lithuania indicate that the distribution of E. multilocularis is wider than previously anticipated in Europe. Historic data provide some hints that the parasite may have existed in the area in the past. However, new data with very high prevalences of E. multilocularis in foxes and raccoon dogs and a recently increasing incidence of AE in humans in Lithuania support the hypothesis that the epidemiological situation may have changed in the last two decades in some areas, associated with a higher infection risk for humans. E. multilocularis is detected in definitive host species such as the red fox, raccoon dog, wolf and domestic dog. The intermediate host species have been investigated only in Lithuania. The red fox can be considered as the most important species for the transmission of E. multilocularis to humans. The increase in the red fox and raccoon dog populations accompanied by the invasion of foxes into urban areas, as earlier described for central Europe (Deplazes et al., 2004), may substantially increase the risk for transmission of E. multilocularis to humans also in urban Baltic environments. The respective epidemiological importance of rural dogs and raccoon dogs is still largely unknown and deserves further study. However, the identification of E. multilocularis in dogs in Lithuania suggests that transmission of the parasite can occur in close vicinity to the human population. In Estonia and Latvia, the published information on Echinococcus infections of domestic animals is scarce. Finland, which is located across the Baltic Sea north of Estonia, is considered free of E. multilocularis. The risk of exporting the parasite from the Baltics to Finland is targeted by treatment requirements for dogs (Wahlström et al., 2015). In humans, cases of AE and CE have been increasing since the 1990s in Latvia and Lithuania, while remaining at relatively low levels in Estonia. In Latvia and Lithuania, the differentiation between AE and CE is routinely done, whereas in Estonia the cases are registered simply as echinococcosis. In the future, the causative species of all human infections should be characterised, and the data and samples stored for further morphologic and molecular analyses. Collection of comparable data is crucial for efficient monitoring and decision-making regarding preventive and treatment measures. Severe human cases are frequent, indicating that AE and CE often are diagnosed at a rather late stage. Improved awareness 129 and diagnostics could result in implementing improved preventive measures and better treatment success. Careful follow-up of the patients, as well as proper staging, are also essential for treatment decisions. Acknowledgments The study was financially supported by the Food and Agriculture Organisation of the United Nations (FAO, project TCP/LIT/3001, T), the SwissBaltNet (supporter: GEBERT RÜF STIFTUNG), the EMIDAERA NET framework (with the EMIRO project ‘The significance of rodent communities for the distribution of Echinococcus multilocularis: ecological and experimental investigations’, grant number 1.12.18 EMIDA EMIRO), institutional research funding (IUT-2032) from the Estonian Ministry of Education and Research, grant ESF8525 as well as the health promotion research programme TerVe 3.2.1002.11-0002 EKZE SS from the Estonian Research Council, the European Union through the European Regional Development Fund (Centre of Excellence FIBIR), the Estonian Doctoral School of Ecology and Environmental Sciences, and the institutional research funding from the Latvian Council of Science (06.1958, 09.1432, 09.1559) and the Latvian Ministry of Agriculture acting in accordance with Hunting Law, and in collaboration with Institute of Food Safety, Animal Health and Environment “BIOR”. References Anisimova, E.I., 2002. Izvestija of Belorusian NAS. Ser. Biol. Sci. 4, 90–92 (in Belorussian). Anisimova, E.I., 2003. Izvestija of Belorusian NAS. Ser. Biol. Sci. 4, 100–107 (in Belorussian). Arzamasov, I.T., Merkusheva, I.V., Chykilewskaya, I.V. 1983. The Structure of Parasitocenosis in Rodents in Geobotanic Subzones in Belarus. Minsk (in Russian). Arzamasov, I.T., Merkusheva, I.V., Chykilewskaya, I.V., 1982. Izvestiya AS BSSR. Ser. Biol. Sci. 5, 89–94 (in Russian). Bagrade, G., 2008. Helminth fauna of wild felids and canids in Latvia. In: PhD Thesis. University of Latvia, Riga. Bagrade, G., Šnábel, V., Romig, T., Ozoliņ, J., Hüttner, M., Miterpáková, M., Švecová, D., Dubinský, P., 2008. Echinococcus multilocularis is a frequent parasite of red foxes (Vulpes vulpes) in Latvia. Helminthologia 45, 157–161. Bagrade, G., Kirjušina, M., Vismanis, K., Ozoliņš, J., 2009. Helminths parasites of the wolf Canis lupus from Latvia. J. Helminthol. 83, 63–68. Balčiauskas, L., Juškaitis, R., 1997. Diversity of small mammal communities in Lithuania (1. A review). Acta Zool. Lituan. Biodivers. 7, 29–45. Bružinskaitė, R., 2007. Epidemiology of Echinococcus species with reference to helminths of red foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) in Lithuania. In: PhD Thesis. Lithuanian Veterinary Academy, Department of Infectious Diseases. Bružinskaitė, R., Marcinkutė, A., Strupas, K., Sokolovas, V., Deplazes, P., Mathis, A., Eddi, C., Šarkūnas, M., 2007. Alveolar echinococcosis, Lithuania. Emerg. Infect. Dis. 13, 1618–1619. Bružinskaitė, R., Šarkūnas, M., Torgerson, P.R., Mathis, A., Deplazes, P., 2009. Echinococcosis in pigs and intestinal infection with Echinococcus spp. in dogs in Southwestern Lithuania. Vet. Parasitol. 160, 237–241. Bružinskaitė-Schmidhalter, R., Šarkūnas, M., Malakauskas, A., Mathis, A., Torgerson, P., Deplazes, P., 2012. Helminths of red foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) in Lithuania. Parasitology 139, 120–127. Budke, C.M., Deplazes, P., Torgerson, P.R., 2006. Global cystic echinococcosis. Emerg. Infect. Dis. 12, 296–303. Buinevičius, K., 1935. Clinical observations of Echinococcus et Abscessus hepatitis. University of Vytautas Magnus In: Proceedings of Medicine Faculty, 2, pp. 451–454 (in Lithuanian). Call for help. 2008. People’s Doctor. December, 23, P. 26 (in Russian). Chashuk, V.P., Chunosov, M.N., 1958. Issues of helminthiasis in man and farm animals in Belarusian SSR. Proceedings of the first zoological conference of Belarusian SSR., 130–132, 272–274 (in Russian). Čygas, J.J. 1956. Helminth and helminthiasis in pigs, cattle and sheep in Lithuanian SSR. Thesis of a Doctoral Degree (in Russian). Čygas, J.J. 1957. Fauna of helminths in pigs, cattle and sheep, distribution of main helminthiases and their seasonal dynamics in Lithuanian SSR. Abstracts of the First Scientific Coordination Conference on Parasitological Problems in Lithuanian SSR, Latvian SSR, Estonian SSR and Belorusian SSR., 130–132 (in Russian). Dakinevičius, S., 1931. Three cases of human cystic echinococcosis. Medicina (Mex) 11, 716–727 (in Lithuanian). Danilevičius, E., 1962. Swine echinococcosis according to various seasons in the Lithuanian SSR. Acta Parasitol. Lith. 4, 111–114. 130 A.. Marcinkutė et al. / Veterinary Parasitology 213 (2015) 121–131 Danilevičius, E., 1964. Echinococcosis in Lithuanian SSR and immunodiagnosis in pigs. In: PhD Thesis. Lithuanian Veterinary Institute (in Lithuanian). Danilin, B.F., 1961. About epizootology of echinococcosis in farm animals. Proceedings of Kaliningrad Veterinary Research Station, 2, 108–110 (in Russian). Darchenkova, N.N., Pliuscheva, G.L., Zavoykin, V.D., 1998. Analysis of cartographic models for distribution of biohelminthoses in Russia, in relation to the tasks of the federal program “Children of the North”. Med. Parazitol. Par. Inf. 3, 33–38 (in Russian). Deplazes, P., Hegglin, D., Gloor, S., Romig, T., 2004. Wilderness in the city: the urbanization of Echinococcus multilocularis. Trends Parasitol. 20, 77–84. Deplazes, P., van Knapen, F., Schweiger, A., Overgaauw, P.A., 2011. Role of pet dogs and cats in the transmission of helminthic zoonoses in Europe, with a focus on echinococcosis and toxocarosis. Vet. Parasitol. 182, 41–53. Derylo, A., Szilman, P., 1998. Prevalence of echinococcosis in swine, beef-cattle, sheep and goats in Poland during 1995–1997. Wiadom. Parazytik. 44, 413. Dubina, I.N., Karasev, N.F., Penkevich, V.A., 2002. Epidemiology, diagnosis, treatment and prevention of parasitic diseases in humans. Tr. III Intern. scientific and practical. Conf. Vitebsk, 195–199 (in Russian). ˛ Dybicz, M., Gierczak, A., Dabrowska, J., Rdzanek, Ł., Michałowicz, B., 2013. Molecular diagnosis of cystic echinococcosis in humans from central Poland. Parasitol. Int. 62, 364–367. Eckert, J., Deplazes, P., Kern, P., 2011. Alveolar echinococcosis (Echinococcus multilocularis) and neotropical forms of echinococcosis (Echinococcus vogeli and Echinococcus oligarthrus). In: Palmer, S.R., Soulsby, L., Torgerson, P.R., Brown, D.W.G. (Eds.), Oxford Textbook of Zoonoses Biology, Clinical Practice, and Public Health Control. Oxford University Press, pp. 669–699. Estonian Health Board. 2014. Nakkushaigustesse haigestumine (in Estonian). http://www.terviseamet.ee/nakkushaigused/nakkushaigustessehaigestumine.html. Communicable disease bulletin. http://www.terviseamet. ee/en/cdc/communicable-disease-bulletin.html (Accessed 07.12.14.). Estonian Veterinary and Food Laboratory (EVFL). 2014. Loomahaiguste diagnostika. Aruanded. (in Estonian) http://www.vetlab.ee/ ?a=page&page=42f088c48f3e323aa1bbc (Accessed 09.12.14.). Gawor, J., Malczewski, A., Stefaniak, J., Nahorski, W., Paul, M., Kacprzak, E., Myjak, P., 2004. Risk of alveococcosis for humans in Poland. Przegl. Epidemiol. 58, 459–465 (in Polish). Gawor, J., Fraczyk, M., Salamatin, R. 2014. Echinococcus granulosus in pigs in central Poland—the pilot study. ESCCAP Abstract Booklet, 2014 Echinococcus, p 43. Gelažius, P., 1924. Rupture of the heart and artery pulmonalis in bull. Vet. Zootech. 40, 4–5 (in Lithuanian). Järvis, T. 1993. Helminths of wild artiodactyls in Estonia and their helminthosis control; PhD thesis. Estonian Agric. Univ., Tartu 103 (in Estonian). Juškaitis, R., Baranauskas, K., 2001. Diversity of small mammals in Northwestern Lithuania (Mažeikiai district). Acta Zool. Lith. 11, 343–348. Karamon, J., Kochanowski, M., Sroka, J., Cencek, T., Różycki, M., Chmurzyńska, E., ˛ E., 2014. The prevalence of Echinococcus multilocularis in red foxes Bilska-Zajac, in Poland-current results (2009–2013). Parasitol. Res. 113, 317–322. Kaspržaka, M., Keidāns, P., Krūklı̄te, A., 2004. Researches of beaver helminth fauna in Kandavas region of Zemites district. In: Thesis of Students Scientific Conference, Jelgava, LLU, pp. 66–67. Kazlauskas, J., Prūsaitė, J., 1976. Helminths of carnivores in Lithuania. Acta Parasitol. Lith. 12, 33–40 (in Russian). Keidāns, P., Krūklı̄te, A., Keidāne, D., 2005. Endoparasites of red foxes in Latvia. In: Proceedings of the First Symposium of the Scandinavian–Baltic Society for Parasitology, Vilnius, Lithuania, p. 81. Keiss, J., Sondore, V., Cernusenko, A., Viksna, L., Rozentale, B., 2007. Current trends in echinococcosis in Latvia. The 17th European Congress of Clinical Microbiology and Infectious Diseases (ECCMID) & 25th International Congress of Chemotherapy (ICC). Conference Proceedings. Kivi, K., 2011. A killer-tapeworm in Estonia. Eesti Ekspress, 21, July (in Estonian). Kolbin, L.V., Karasev, N.F., 1965. Materials of the scientific. Conf. VOG. M. 1, 120–123 (in Russian). Korzan, A.I., Galbadrax, D., Chistenko, G.H., 1997. Antropozoonotic diseases, prevention and control measures: proceedings of the Intern. scientific and practical. Conf. Mn., 145–147 (in Russian). Laivacuma, S., Viksna, L., 2014. Cystic echinococcosis in Latvia. ESCCAP Conference Echinococcus. Abstract Booklet, 25. Laivacuma, S., Viksna, L. 2014. Case Analysis of Alveolar Echinococcosis. Riga Stradins University Scientific Conference 2014 Abstracts, p. 184 (in Latvian). Lapidus, N., Loit, H.M., Arro, A., 2004. A huge echinococcal cyst in lungs. Eesti Arst 83, 839–842 (in Estonian). Latvian Food and Veterinary Service (LFVS), 2004–2010. Report on trends and sources of zoonoses, zoonotic agents and food-born outbreaks. Annual report (in Latvian). Laurimaa, L., Davison, J., Plumer, L., Süld, K., Oja, R., Moks, E., Keis, M., Hindrikson, M., Kinkar, L., Laurimäe, T., Abner, J., Remm, J., Anijalg, P., Saarma, U., 2015a. Noninvasive detection of Echinococcus multilocularis tapeworm in urban area, Estonia. Emerg. Infect. Dis. 21, 163–164, http://dx.doi.org/10.3201/eid2101. 140136. Laurimaa, L., Davison, J., Süld, K., Plumer, L., Oja, R., Moks, E., Keis, M., Hindrikson, M., Kinkar, L., Laurimäe, T., Abner, J., Remm, J., Anijalg, P., Saarma, U., 2015b. First report of highly pathogenic Echinococcus granulosus genotype G1 in European Union urban environment. Parasite Vector 8, 182, http://dx.doi.org/ 10.1186/s13071-015-0796-3. Laurimaa, L., Süld, K., Moks, E., Valdmann, H., Umhang, G., Knapp, J., Saarma, U., 2015c. First report of the zoonotic tapeworm Echinococcus multilocularis in raccoon dogs in Estonia, and comparisonswithothercountries in Europe. Vet. Parasitol. 212, 200–205. Lešins, K. L. 1955. Analyses of helminth fauna and seasonal dynamics of helminthosis of farm animals in South-East of ESSR. Can. Dissertation. Tartu–Moscow, 181 (in Russian). Lithuanian State Veterinary Service (LSVS). 1996 The Results of Parasitological Examinations. Annual Report. p. 46 (in Lithuanian). Malczewski, A., Rocki, B., Ramisz, A., Eckert, J., 1995. Echinococcus multilocularis (Cestoda), the causative agent of alveolar echinococcosis in humans first record in Poland. J. Parasitol. 81, 318–321. Marcinkutė, A., Bareišienė, M.V., Bružinskaitė, R., Šarkūnas, M., Tamakauskienė, R., Vėlyvytė, D., 2006. Cystic echinococcosis in Lithuania. Lith. Gen. Pract. 10, 8–11 (in Lithuanian). Mažeika, V., Paulauskas, A., Balčiauskas, L., 2003. New data on the helminth fauna of rodents of Lithuania. Acta Zool. Lith. 13, 41–47. Mažeikytė, R., 2002. Small mammals in the mosaic landscape of eastern Lithuania: species composition, distribution and abundance. Acta Zool. Lith. 12, 381–391. Merkusheva, I. V. 1963. Fauna and Ecology of Parasites of Rodents. Minsk. 53–137 (in Russian). Merkusheva, I. V., Bobkova A.F., 1981. The catalog of helminths in domestic and wild animals in Belarus. Minsk. p. 23 (in Russian). Michelson, V. 1976. Materials of helminth fauna in some of game animals in the Latvian SSR. Parasitological Investigations in Baltic Countries. Riga: Zinatne, 157–158 (in Russian). Moks, E., Saarma, U., Valdmann, H., 2005. Echinococcus multilocularis in Estonia. Emerg. Infect. Dis. 11, 1973–1974. Moks, E., Jõgisalu, I., Saarma, U., Talvik, H., Järvis, T., Valdmann, H., 2006. Helminthologic survey of the wolf (Canis lupus) in Estonia, with an emphasis on Echinococcus granulosus. J. Wildl. Dis. 42, 359–365. Moks, E., Jõgisalu, I., Valdmann, H., Saarma, U., 2008. First report of Echinococcus granulosus G8 in Eurasia and a reappraisal of the phylogenetic relationships of ‘genotypesп’ G5–G10. Parasitology 135, 647–654. Musteikaitė, L., Kazlauskas, J., Danilevičius, E., 1961. On the intestinal helminths of dogs and cats. Acta Parasitol. Lith. 3, 17–20 (in Russian). Nahorski, W.L., Knap, J.P., Pawłowski, Z.S., Krawczyk, M., Polański, J., Stefaniak, J., Patkowski, W., Szostakowska, B., Pietkiewicz, H., Grzeszczuk, A., ˛ E., Wnukowska, N., Paul, M., Kacprzak, E., Felczak-Korzybska, I., Gołab, Sokolewicz-Bobrowska, E., Niścigorska-Olsen, J., Czyrznikowska, A., Chomicz, L., Cielecka, D., Myjak, P., 2013. Human alveolar echinococcosis in Poland: 1990–2011. PLoS. Negl. Trop. Dis. 7 (1), e1986, http://dx.doi.org/10.1371/ journal.pntd.0001986. Nainys, J., Kazlauskas, J., 1954. Review of parasitological expeditions. Proceedings of Institute of Animal Husbandry and Veterinary, I, 52–61 (in Lithuanian). Oksanen, A., Lavikainen, A., 2015. Host ecology and Echinococcus canadensis transmission in the North. Vet. Patrasitol., in press. Peklo, G.N. 2014. [Echinococcosis and Trichinellosis in the Northwestern Federal district (Inventories of biohelminths in Russian Federation)]. Federal service for supervision of protection Consumer rights and welfare. Tyumen Research institute of boundary Infectious pathology, Rospotrebnadzor. Tyumen, 2012–2014 (in Russian). Petrov, A.M. 1957. Modern views on the epizootiology and epidemiology of echinococcosis. Abstracts of Scientific Conference VOG, 2, 12–14 (in Russian). Plumer, L., Davison, J., Saarma, U., 2014. Rapid urbanization of red foxes in Estonia: distribution, behaviour, attacks on domestic animals, and health-risks related to zoonotic diseases. PLoS One 9 (12), e115124, http://dx.doi.org/10.1371/ journal.pone.0115124. Poļakova, A., 2009. Fox (Vulpes vulpes) and raccoon dog (Nyctereutes procyonoides) helminth fauna in Latvia. In: MSc Degree Thesis. LLU, Jelgava (in Latvian). Prieditis, A.A., Daija, G.G. 1972. On helminth fauna in game animals in Latvian SSR. Riga, Zinatne. P123–156 (in Russian). Prūsaitė, J., Mažeikytė, R., Pauža, D., Paužienė, N., Baleišis, R., Juškaitis, R., Mickus A., Grušas A., Skeiveris R., Bluzma, P., Bielova, O., Baranauskas, K., Mačionis A., Balčiauskas, L., Janulaitis, Z. 1988. Fauna of Lithuania. Mokslas, Vilnius (in Lithuanian). Radziulis, K., Šarkūnas, M., Deplazes, P. 2011. The impact of regular praziquantel treatment of dogs on the E. granulosus prevalence in pigs and dogs in endemic villages of south-west Lithuania. 24th World Congress of Hydatidology. Abstracts book,. OXI-1. P. 199. Raush, R.L., 1995. Life cycle patterns and geographic distribution of Echinococcus species. In: Thompson, R.C.A., Lymbery, A.Y. (Eds.), Echinococcus and Hydatid Disease. CAB Int., pp. 89–134. Romig, T., Dinkel, A., Mackenstedt, U., 2006. The present situation of echinococcosis in Europe. Parasitol. Int. 55, S187–S191. Romig, T., Ebi, D., Wassermann, M., 2015. Taxonomy and molecular epidemiology of E. granulosus sensu lato. Vet. Parasitol., pii: S0304-4017(15)00375-1. doi: 10.1016/j.vetpar.2015.07.035. [Epub ahead of print]. Saar, F., 1931. Echinococcus unilocularis reasons to defend. Estonian Vet. Rev. 1–2, 27 (in Estonian). Saarma, U., Jõgisalu, I., Moks, E., Varcasia, A., Lavikainen, A., Oksanen, A., Simsek, S., Andresiuk, V., Denegri, G., Gonzalez, L.M., Ferrer, E., Garate, T., Rinaldi, L., Maravilla, P., 2009. A novel phylogeny for the genus Echinococcus based on nuclear data challenges relationships based on mitochondrial evidence. Parasitology 136, 317–328. A.. Marcinkutė et al. / Veterinary Parasitology 213 (2015) 121–131 Shimalov, V.V., 1991. Helminths, common to man and wildlife on reclaimed lands of Belarusian Polesie. Dis. Cand. Biol. Sci. Minsk (in Russian). Shimalov, V.V., 2002. Helminth fauna in small rodents (Mammalia: Rodentia) of channel banks of meliorated territories. Parasitology 36, 247–252 (in Russian). Shimalov, V.V., 2010. Bialowieza forest: history, nature, tourism. In: Proceedings Intern. Scientific and Practical. Conference on the 600th Anniversary of Wilderness Protection in the Bialowieza Forest, Brest, pp. 368–378. Shimalov, V.V., 2011. The prevalence of Echinococcus multilocularis (cestoda, taeniidae) in the southwestern part of Belarus. The news of the National Academy of Sciences. Ser. Biol. Sci. 4, 108–112. Shimalov, V.V., Shimalov, V.T., 2001. Alveococcosis in Belorussian Polesie. Parasitology 35, 145–148 (In Russian). Shimalov, V.T., Shimalov, V.V., 2003. Helminth fauna of red fox (Vulpes vulpes Linnaeus, 1758) in southern Belarus. Parasitol. Res. 89, 77–78. Sikó, S.B., Deplazes, P., Ceica, C., Tivadar, C.S., Bogolin, I., Popescu, S., Cozma, V., 2011. Echinococcus multilocularis in south-eastern Europe (Romania). Parasitol. Res. 108, 1093–1097. Šiurkus, T., 1969. On the liver Echinococcus. Acta Parasitol. Lith. 9, 111–115 (in Russian). Šivickis, P., 1955. Parasitology expedition. In: Proceedings of Institute of Animal Husbandry and Veterinary, Lithuanian SSR Academy of Sciences (in Lithuanian). Sniečkienė, P., 1937. News in diagnostics and section of communicable diseases. Vet. Zootech. 4, 136–159 (in Lithuanian). Süld, K., Valdmann, H., Laurimaa, L., Soe, E., Davison, J., Saarma, U., 2014. An invasive vector of zoonotic disease sustained by anthropogenic resources: the raccoon dog in Northern Europe. PLoS One 9 (5), e96358, http://dx.doi.org/10. 1371/journal.pone.0096358. 131 Thompson, R.C.A., 1995. Biology and systematics of Echinococcus. In: Thompson, R.C.A., Lymbery, A.Y. (Eds.), Echinococcus and Hydatid Disease. CAB Int., pp. 1–50. Trachsel, D., Deplazes, P., Mathis, A., 2007. Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134, 911–920. Tulin, A.I., Ribenieks, R., Pogodina, E.N., Stutska, R., Shavlovskis, I., Gardovskis, I., 2012. Diagnostics and surgical treatment of liver echinococcosis in Latvia. Vestnik khirurgii imeni I.I. Grekova, 171, 38–44 (in Russian). Vaivarina, G.F., 1950. Fauna of helminths and helminthiasis in agricultural animals of major species in Latvian SSR. Thesis of a Doctoral Degree, Library of WUIHS (in Russian). Wahlström, H., Enemark, H.L., Davidson,R, K., Oksanen, A., 2015. Actions taken and future considerations due to the findings of E. multilocularis in two Scandinavian countries. Vet. Parasitol., http://dx.doi.org/10.1016/j.vetpar.2015.07.0374. Vuitton, D.A., Demonmero, F., Knapp, J., Richou, C., Grenouillet, F., Chauchet, A., Vuitton, L., Bresson-Hadni, S., Million, L., 2015. Clinical epidemiology of human AE in Europe. Vet. Parasitol. 213, 110–120. WHO, 2001. WHO/OIE Manual on Echinococcosis in Humans and Animals: A Public Health Problem of Global Concern. In: Eckert, J., Gemmell, M.A., Meslin, F.X., Pawłowski, Z.S. (Eds.). World Organisation for Animal Health, Paris, ISBN 92-9044-522-X. Zubinas, F.A., 1936. Case study of Echinococcus et abscessus hepatitis. Medicina (Mex) 10, 746–749 (in Lithuanian).