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Author's personal copy Veterinary Parasitology 190 (2012) 196–203
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Freedom from Echinococcus multilocularis: An Irish perspective T.M. Murphy a,∗ , H. Wahlström b , C. Dold c , J.D. Keegan c , A. McCann d , J. Melville e , D. Murphy d , W. McAteer e a b c d e
Central Veterinary Research Laboratory, Backweston Campus, Young’s Cross, Celbridge, Co. Kildare, Ireland National Veterinary Institute, 75189 Uppsala, Sweden Department of Zoology, Trinity College, Dublin University, Dublin 2, Ireland Dublin Institute of Technology, Kevin Street, Dublin 2, Ireland Department of Agriculture, Agriculture House, Kildare Street, Dublin 2, Ireland
a r t i c l e
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Article history: Received 4 January 2012 Received in revised form 9 May 2012 Accepted 13 May 2012 Keywords: Echinococcus multilocularis Fox Survey Ireland Probability of freedom
a b s t r a c t Echinococcus multilocularis, an emerging zoonotic disease is extending its geographical distribution within the European Union (EU). At present, five member states including Ireland are considered free. Previous EU regulations on importing domestic pets allowed these countries to maintain national rules that required all dogs be treated with an anti-cestode compound before entry. The controls on the movement of pet animals within the EU were recently reviewed by the European Commission and it was decided that the five countries had to demonstrate freedom from E. multilocularis before they could continue with the mandatory tapeworm treatment. The intestines of 220, 307 and 216 foxes were examined, using the sedimentation and counting technique, for the presence of E. multilocularis in 2003, 2009 and 2010 respectively. There was no evidence of the parasite in the foxes. These data together with the negative results from 130 foxes examined by other workers during 1999 and 2000 (Wolfe et al., 2001) were used to estimate the probability of freedom using scenario trees. The result of the model suggested that the probability that Ireland was free from E. multilocularis in 2010 was high, 0.98 (95% confidence interval, 0.94–1.00), thus justifying the retention of the mandatory tapeworm treatment for dogs entering the country from other EU member states. © 2012 Elsevier B.V. All rights reserved.
1. Introduction Alveolar echinococcosis (AE) caused by the larval metacestode stage of the taenid tapeworm Echinococcus multilocularis (EM), is considered one of the more serious emerging zoonotic diseases in temperate and artic regions of the Northern Hemisphere (Craig, 2003). The parasite has both a sylvatic and synanthropic life cycle involving
∗ Corresponding author. Present address: 16 Castleknock Rise, Laurel Lodge, Castleknock, Dublin 15, Ireland. Tel.: +353 18216856. E-mail address:
[email protected] (T.M. Murphy). 0304-4017/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.vetpar.2012.05.009
foxes (Vulpes vulpes) and other canids as definitive hosts and arvicolids and other rodents as intermediate hosts. Some larger mammals, including pigs and horses are also susceptible and can act as aberrant intermediate hosts (Taylor et al., 2007). Humans become infected by accidentally ingesting E. multilocularis eggs in food or water or on hands/fingers contaminated with eggs from fox or dog faeces. The larval cysts, containing variable numbers of protoscoleces, proliferate and expand as multi-vesicular (alveolar) tissue in the primary affected organ, the liver. They are slow growing and consequently there is a long incubation period (5–15 years) until disease is detected, usually at an advanced stage. The disease is of considerable
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public health importance because it is fatal in humans if left untreated. Diagnosis is also difficult and treatment is prolonged and expensive (Torgerson et al., 2008). Until recently, AE was confined to a core area of endemic regions in Austria, France, Germany and Switzerland but now appears to be spreading with cases identified in Belgium, northern France and Poland (Kern et al., 2003). Coincidently, since the early 2000s the prevalence of E. multilocularis amongst foxes in the endemic areas has increased and spread to surrounding countries in central, eastern, northern and western Europe and more recently to Sweden (Manfredi et al., 2002; Strer et al., 2003; Deplazes et al., 2004; Romig et al., 2006; Osterman Lind et al., 2011). It is thought that the spread of the parasite into previously uninfected areas is due to infected foxes migrating from endemic zones (Vertvaeke et al., 2006; Takumi et al., 2008). However, its spread into Sweden was most probably due to an infected dog (Osterman Lind et al., 2011). Currently, Great Britain and Ireland are believed to be free of this parasite, as cases of indigenous human and animal infection have never been reported from either island (Wolfe et al., 2001; Gover et al., 2011). Environmental and climatic conditions and the presence of susceptible intermediate and definitive hosts suggest that the British Isles are suitable for the establishment and propagation of E. multilocularis. Increasing international movement of animals, including domestic pets, increases the risk of expanding the geographical range of pathogens and their vectors. Without the derogation to the EU Regulation (EC) No. 998/2003, the likelihood of accidentally introducing an animal infected with E. multilocularis into the United Kingdom (U.K.), from an endemic area in continental Europe, is considered high (Taylor et al., 2006; Torgerson and Craig, 2010). The derogation resulted in the Pet Travel System (PETS), which allows the U.K. and Ireland, along with Finland, Malta and Sweden, to maintain national rules for the entry of companion animals. This ensures that dogs and cats receive an anti-tapeworm treatment within 48 h of travel to any of the aforementioned countries. The European Commission has recently reviewed the controls on the movement of pet animals, in order to harmonise the regulations and to allow the possibility of adopting preventative measures to control diseases, such as E. multilocularis. One of the criteria was that any additional measures had to be scientifically justified and proportionate to the risk of spreading disease following a risk assessment. Thus if a country wants to maintain more severe importation regulations for dogs and cats than those existing in the EU generally, it should conclusively demonstrate freedom from E. multilocularis.
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This paper describes the use of results from four surveys of foxes to determine the presence or absence of E. multilocularis in wildlife in Ireland. The probability that the country was free from this parasite and the sensitivity of the surveillance methods were estimated using a scenario tree model developed by Martin et al. (2007) and Wahlström et al. (2011) and combined the results of four previous surveys of foxes. The study was carried out to provide information for the European Commission on the status of the country vis-à-vis freedom from E. multilocularis at the end of 2010 just prior to the review of EU Regulation (EC) No. 998/2003.
2. Materials and methods 2.1. Surveillance of foxes A total of 743 foxes were examined for E. multilocularis in three surveys during the years 2003, 2009 and 2010 (Table 1.). The number of foxes killed in each county was 16 in the 2003 survey and varied from 3 to 21 in the surveys carried out in 2009 and 2010. The foxes were sent to the nearest Regional Veterinary Laboratory (RVL) for examination. Only the intestines of foxes, which had been delivered to a RVL within 48 h of being killed, were examined for E. multilocularis. The foxes in the three studies had been shot as part of an annual vermin kill and included in a national survey of trichinosis amongst wildlife. On arrival at the RVLs the carcases were opened and ligatures placed at the anterior end of the duodenum close to the pylorus and at the rectum. The intestines were then removed and placed in separate plastic bags and stored at −20 ◦ C before being delivered frozen to the Central Veterinary Research Laboratory (CVRL). Prior to examination for the presence of E. multilocularis the frozen intestines were transferred to −80 ◦ C for at least a further five days. The intestines were thawed overnight at 4 ◦ C and examined using the sedimentation and counting technique (SCT) described by Eckert et al. (2001a), with the following modification. The mucosa was stripped from segments of the small intestine using glass slides and added to a 2 l Scott bottle containing the loose intestinal contents suspended in phosphate buffered saline (PBS). This suspension was thoroughly mixed by vigorous shaking. The mucosal and intestinal contents suspension was then subjected to four cycles of washing and sedimentation with fresh PBS. Each washing and sedimentation cycle took 15 min. The cleared sediment was then examined in aliquots of 5–10 ml in plastic petri dishes, with a counting grid drawn on the bottom, using a stereomicroscope at a magnification of 120×.
Table 1 The number of foxes examined for the presence of Echinococcus multilocularis during 2000, 2003, 2009 and 2010. Year 1999–2000 2003 2009 2010 a
Month
Number of foxes collected
Number of foxes examined for Echinococcus multilocularis
January–February September–December January–February September–November
– 454 373 22 194
130a 220 307 22 194
Data taken from a survey carried out by Wolfe et al. (2001).
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Table 2 Input values used in the model to quantify the probability of freedom from Echinococcus multilocularis in Ireland in 2010. Input values used in the model
References
Initial prior probability of freedom Design prevalence fox Sensitivity of the test (sedimentation and counting technique) Probability of imported dog coming from EM-infected country
0.50 0.01 Pert (0.90, 0.98, 0.99)
Boue et al. (2010) (Hofer et al., 2000; Eckert, 2003; expert opinion).
Probability of dog coming from EM-infected country being infected with EM Noncompliance with import requirements Probability of an infected dog excreting eggs Probability of initiation of an endemic cycle
Pert (0.0, 0.003, 0.07)
0.61
Extrapolated from data on DAFF files, i.e. records of applications for permission to import dogs via the international airports at Cork, Dublin and Shannon during 2009 and 2010 John Melville (pers. comm.) Dyachenko et al. (2008), Deplazes et al. (1999), Gottstein et al. (2001), Vågsholm (2008) Tomina Saha (2011, pers. comm.) Wahlström et al. (2011) Wahlström et al. (2011)
0.05 Pert (0.42, 0.60, 1) Pert (0.3, 0.5, 0.7)
A further 130 foxes examined over a 15 month period during 1999/2000 were also included in this study (Wolfe et al., 2001). All the foxes were assumed to have been examined in 2000 for the purposes of the analysis, as it was considered that this assumption would not affect the output of the model. 2.2. Study design An estimation of the probability of freedom from E. multilocularis was carried out using scenario trees according to the procedures described by Martin et al. (2007) and Wahlström et al. (2011). Using this method, results from several independent components of a complex surveillance system can be combined into a single measure; i.e. the sensitivity of the combined surveillance activities. The model is based on two key assumptions: all the results of the surveillance system are negative, i.e. disease is not detected, and that the specificity of the surveillance system is 100%. Given a defined design prevalence (P*) (which in this study was 1%) the probability of freedom is then calculated. 2.3. The model 2.3.1. Design prevalence and test sensitivity The design prevalence P* is the expected prevalence of infected animals given that the infection is present in the country. A design prevalence of 1% was used for the present study in accordance with the recommendation of the European Food Safety Authority (Table 2, Boue et al., 2010). The sensitivity of the sedimentation and counting technique (SCT) has been estimated to be 98–100% (Hofer et al., 2000; Eckert, 2003). However, since E. multilocularis had never been found in Ireland, it was considered that Irish personnel would be less experienced in recognising the parasite than technicians in central Europe. It was also thought that this would result in lower sensitivity for the test. Hence the sensitivity of the SCT in the present study was described with a Pert distribution with the following parameters 0.90, 0.98 and 0.99 (Table 2). 2.3.2. Probability of introduction It was assumed that the only way E. multilocularis would be introduced into Ireland was by the introduction of
infected dogs from countries where the tapeworm was present. Based on data from 2009 to 2010 (Table 3), it was postulated that on average 742 dogs were introduced annually to Ireland from countries other than the United Kingdom. Extrapolating from official data, on the number and country of origin of applications to the Department of Agriculture, Food and Fisheries (DAFF) for permission to import dogs via the main international airports at Cork, Dublin and Shannon, it was estimated that 61% of all dogs imported originated from countries where the parasite was endemic (J. Melville, pers. comm.). The prevalence of infected dogs in these countries was described by a pert distribution with parameters 0.0, 0.003 and 0.07 (Table 2, Dyachenko et al., 2008; Deplazes et al., 1999; Gottstein et al., 2001). The probability that an imported dog was infected with E. multilocularis (EM) was calculated as: P(InfDog) = P(EM C) ∗ ×P(Inf ) ∗ ×P(NonCompl) where P(EM C) is the probability that an imported dog originates from an infected country, P(Inf) is the probability that a dog from an infected country is infected and P(NonCompl) is the probability that an introduced dog does not comply with the import requirements. The probability that the infection was introduced to Ireland during any year was calculated according to the binomial distribution as 1 − A, where A is the probability that the infection was not introduced to Ireland. A = [1 − P(InfDog)]
n
where P(InfDog) is the probability that an imported dog was infected with E. multilocularis and n is the number of annually imported dogs. Given introduction, the probability that E. multilocularis would become established and endemic was considered to Table 3 The number of dogs imported into Ireland through the Pet Passport Scheme and the number of dogs whose documentation was non compliant with the scheme’s regulations. Year
Imported dogs (n)
Dogs non-compliant (n)
Non-compliance %
2009 2010
725 760
14 11
1.9 1.4
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be dependent on the probability of infected dogs excreting eggs and the probability of the excreted eggs initiating an endemic cycle. The infection cycle in dogs is circa 120 days and constitutes a prepatent period approximately 28 days and an effective patent period of approximately 43 days (95% confidence interval (CI), 21.9–93.1) (Anonymous, 2001; Kapel et al., 2006). Therefore, it was thought that dogs imported after 71 (28 + 43) days post infection would excrete very few eggs and were unlikely to initiate an endemic cycle. Based on this, it was considered that approximately 60% (71/120) (95% CI: 42% (49.9/120) to 100% (121/120)) of imported infected dogs would excrete sufficient eggs to be able to initiate an endemic cycle (Wahlström et al., 2011). Furthermore, the risk of initiating an endemic cycle was considered to be dependent on the presence of suitable hosts. As no data is available, the same estimate as used by Wahlström et al. (2011) was used, i.e. that 50% (minimum 30%, maximum 70%) of infected dogs would excrete eggs in areas suitable for the initiation of an endemic cycle. Hence given introduction, the risk of an endemic cycle being initiated was described as a probability parameterised as: Pert (0.42, 0.6, 1) × Pert (0.3, 0.5, 0.7) where Pert (0.42, 0.6, 1) is the probability that an infected imported dog would excrete eggs and Pert (0.3, 0.5, 0.7) is the probability that an endemic cycle would be initiated given introduction of an infected dog excreting eggs (Table 2). 2.3.3. Surveillance system component sensitivity The annual sensitivity of the surveillance system for foxes (SSC) was calculated for all 11 years. For year y the sensitivity of the SSC (SSCSey ), i.e. the probability of a positive test result in at least one of the animals tested that year given, that foxes were infected at the designated design prevalence (P*) was calculated as: SSCSey = 1 − [(1 − Se × P∗)Ny ] where Se is the sensitivity of the test, Ny is the number of foxes tested in year y and P* is the design prevalence. 2.3.4. Calculation of the probability of freedom from E. multilocularis The probability that Ireland was free from E. multilocularis was calculated using Bayes theorem (Martin et al., 2007). A prior probability of infection is required for this calculation and because the parasite had previously never been recorded in Ireland, a non-informative prior probability of infection (0.5) in January 2000 was used, assuming no prior information about the disease status. The posterior probability of freedom (PostPFree) from infection was calculated for each of the 11 years as: PostPFreey =
1 − PriorPInfy 1 − PriorPInfy × SSCSey
where PriorPInfy is the pre-surveillance probability that Ireland was infected at the start of year y and SSCSey is the sensitivity of the SSC for that year.
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The risk of introduction was taken into account when calculating the prior probability of freedom for the coming year. The annual probability of introduction (PIntro) represents the probability that disease was introduced into Ireland and established at the design prevalence (P*) (Martin et al., 2007). The prior probability that the country was infected at the beginning of y + 1 is given by the function: PriorPInfy+1 = PostInfy + PIntro − (PostPInfy × PIntro) where PriorPInfy+1 is the prior probability of infection in year y + 1, PostInfy is the posterior probability of infection in year y and PIntro is the probability of introduction (Martin et al., 2007). 2.4. Scenario analysis Three “what-if” scenarios were run to evaluate the effect of changes in the design prevalence (P*) on the probability of freedom. The design prevalence for foxes was decreased from 1% to 0.5%, 0.1% and 0.05% covering the lowest prevalence of E. multilocularis reported for wildlife in endemic areas (Eckert, 1996, 1997). 2.5. Stochastic simulation The model was developed using Excel 2007 (Microsoft Corporation, Redmond, WA, USA) and @RISK, (Palisade, Newfield, NY, USA) and run with 10,000 iterations for each scenario. 3. Results and discussion In the Scandinavian countries that are free from E. multilocularis, data from surveys of foxes are considered the most important indicator of the presence or absence of this parasite in wildlife (Wahlström et al., 2011). A design prevalence of 1% was used for these surveys in agreement with the guidelines for harmonised monitoring for E. multilocularis within the EU (Boue et al., 2010). The SCT was selected as the test of choice for this study as it is has a high sensitivity and specificity and it is considered the “gold standard” for comparison with other diagnostic procedures such as coproantigen ELISA and copro-DNA-PCR (Deplazes and Eckert, 2001; Eckert, 2003). However, as the laboratory personnel were unfamiliar with adult E. multilocularis because the parasite had never been recorded in Ireland, a lower test sensitivity was attributed to the SCT. There was no evidence of E. multilocularis infection in any of the animals examined. The cumulative probability of the country being free of this parasite at the end of 2010 was high, 0.98 (95% CI: 0.94–1.00). This suggested that there was a very high probability that the prevalence of E. multilocularis in foxes was lower than 1%. The sensitivity of the surveillance system varied from 0.0% for those years when there was no survey to 95% in 2009 when 307 foxes were examined. When the design prevalence was decreased to 0.5%, 0.1% and 0.05% the probability of freedom decreased to 0.87, 0.35 and 0.27. In this scenario, the surveillance sensitivity was not sufficient to document freedom at 0.1% or
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at lower design prevalence. The results of the model, highlights the need to examine a sufficient number of animals each year, approximately 300, to conform to the design prevalence designated by the European Commission (Boue et al., 2010). If practicable, a larger number of foxes should be examined by the SCT in order to maintain a high probability of freedom. However, it should be pointed out that the probability of freedom calculated by the model uses a design prevalence of 1%, i.e. it models the probability of having less than 1% infected foxes in the country. If stricter criteria are used, such as a lower design prevalence of 0.1% the probability of freedom as well as the sensitivity of the SSCs would decrease as shown by Wahlström et al. (2011). Negative results from a surveillance system with a high sensitivity may not guarantee freedom from disease but they do suggest that the level of infection is below the specified or designated design prevalence. E. multilocularis was found recently in foxes in Sweden despite the sensitivity of the wildlife surveillance carried out over the previous ten years being high (Wahlström et al., 2011; Osterman Lind et al., 2011). It has been suggested that the translocation of infected dogs introduced E. multilocularis to Sweden and western Canada (where an European strain of the tapeworm was found) (Peregrine et al., 2010, cited by Jenkins et al., 2011; Osterman Lind et al., 2011). A survey of domestic dogs on the Japanese islands of Honshu and Kyushu demonstrated the possibility of introducing E. multilocularis to a clean area by the transport of infected pets from Hokkaido where the parasite is endemic (Nonaka et al., 2009). The importation of dogs infected with E. multilocularis into the U.K., if the requirement for anti-cestode treatment is relaxed, is considered inevitable given the level of dog migration. For example, 70,000 dogs participated in the pet passport scheme (PETS) in 2010 (DEFRA, 2010; Torgerson and Craig, 2010). The pet passport scheme is a system that allows pet owners bring their dogs into the U.K. without quarantine once they have been vaccinated against rabies and treated for tapeworms. In Sweden the number of imported pets is not known but based on data from 2003, it was estimated that approximately 1100 dogs were imported annually from countries where the disease is endemic (Vågsholm, 2008). The risk of introducing E. multilocularis may be lower in Ireland as only circa 750 dogs per year are recorded as imported (Table 3). However, for the purposes of this study a large proportion (61%) of these animals were assumed to originate from an area with endemic disease. This figure may be too high; it was extrapolated from official data on the number and country of origin of the limited number of applications to DAFF for permission to import dogs via the main international airports. The majority of dogs imported into the country travel by surface transportation and to date information on the country of origin of the animals has not been recorded at the control points at the ferry ports. The assumption on the level of non-compliance to EU Regulation (EC) No. 998/2003 used in this study is also associated with a degree of uncertainty. A total of 1–2% of pet owners, at point of entry, was found to have not complied with the mandatory tapeworm treatment regulation
during 2009 and 2010 (Table 3). However, once detected, this cohort of dogs did not represent a disease threat as they were placed in quarantine for a few days and given a tapeworm treatment before being allowed entry into the country. It is believed, that despite the limited number of designated ferry and airports through which it is allowed to import dogs, and the vigilance of veterinary officers at the border controls that a number of undocumented dogs are imported each year. Not withstanding the paucity of reliable data on the degree of non-compliance in Ireland, it was proposed for this study to adopt the level suggested for the U.K. where it is thought to be about 5% (Tomina Saha, pers. comm.). The same line of reasoning on the level of non-compliance was used in the study for Sweden, Norway and Finland (Wahlström et al., 2011). In these countries, the possibility of controlling the importation of dogs is less due to land borders and implementation of the Schengen agreement. It can therefore be concluded that the level of non-compliance used in the present study may have been a conservative estimate. In addition, the possibility of the introduction of an infected animal into Great Britain may signify a danger as theoretically, it could be transported unhindered to Ireland on account of the Common Travel Area agreement between the U.K. and the Republic of Ireland. However, for the purposes of this study this risk was considered negligible and therefore not included in the model. If accidentally introduced, the probability of E. multilocularis becoming established in Ireland is considered to be high. The oceanic temperate climate is ideal for the prolonged survival of eggs outside of the host (Eckert and Deplazes, 2004). Suitable intermediate hosts such as wood mouse (Apodemus sylvaticus) and the bank vole (Myodes glareolus) are present in the country and form a stable part of the diet of foxes (Morgan, 2008; Sleeman et al., 2008). Socio-economic conditions are also conducive to the transmission of the parasite at the human/domestic pet/wildlife interface (Kern et al., 2004). There is a high level of agricultural activity with clusters of intensive horticulture in the peri-urban areas of the major cities (Anonymous, 2004). It is estimated that there are circa 690,000 dogs in the country and 35.5% households have one or more dogs (Downes et al., 2009). Recreational pursuits, such as hunting with dogs, hill walking, orienteering and gardening. that bring humans and their pets in close contact with wildlife are popular and may contribute to the transmission of E. multilocularis (Kern et al., 2004). Once established in an environment E. multilocularis has a propensity to spread rapidly. The Japanese island of Hokkaido covers 78,000 km2 (the comparable figure for Ireland is 84,000 km2 ) and the parasite expanded from 8% in 1981 to over 90% of the island by 1991 (Suzuki et al., 1996 cited by Eckert et al., 2001b). If the parasite is introduced to Ireland the long-term consequences could be a high prevalence amongst rural and urban foxes as is the situation in many parts of Europe (Deplazes et al., 2004; Torgerson and Craig, 2010). However, the spread of the tapeworm to domestic pets may be more problematic. In Germany and Switzerland the overall prevalence of E. multilocularis in dogs is 0.24% and 0.30% respectively (Deplazes et al., 1999; Dyachenko et al., 2008). However, in areas of
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high endemicity, the prevalence in dogs can be higher, up to 7% in Switzerland and in Slovakia, a country where the disease is considered to be emerging; it is 2.8% (Antolova et al., 2009; Gottstein et al., 2001). The fox and dog definitive hosts are refractory to the presence of the adult tapeworm in the small intestine. However, on rare occasions there may be health implications for domestic pets as dogs can also be intermediate hosts and concurrent infection of metacestodes in the liver and adult stages in the intestine have been observed (Deplazes and Eckert, 2001). The source of AE in the liver can be either eggs in the environment or eggs from a recent or current patent intestinal infection that contaminated the skin and fur and were ingested by the dog whilst grooming. The pathogenesis of the parasite in dogs as an intermediate host is similar to AE in humans (Deplazes and Eckert, 2001). Although it is difficult to quantify, the resultant chronic illness may have an impact on the welfare of the animals with additional veterinary costs for the pet owner. Animal welfare problems may also arise if primates kept either as pets or maintained in zoos become infected (Deplazes and Eckert, 2001). It is difficult to predict the likely consequences of accidental introduction and establishment of E. multilocularis on Irish society. Alveolar echinococcosis is one of the most aggressive chronic diseases of the liver. Its true morbidity is masked and the disease can go unnoticed for prolonged periods due to a long asymptomatic incubation period assumed to be between 5 and 15 years (Torgerson et al., 2008). In Austria the number of new AE cases per year is circa 2.5 cases and in Switzerland the number of cases can vary from 7.2 to 19.5, corresponding to a minimum incidence of 0.10 and a maximum of 0.26 cases/100,000 (Schweiger et al., 2007). A higher incidence, 0.8/100,000 has been reported from Lithuania (Audrone et al., 2011). In Ireland, an incidence rate similar to Switzerland would result in 4–11 cases/year. The greatest economic impact on a community is the public health costs associated with diagnosis and treatment of AE, including hospitalisation, surgery and prolonged anthelmintic medication of affected individuals. In Switzerland these costs were estimated to be D 108,762/patient increasing to D 182,594 if saved pension costs are included. However, the true value to the country is likely to be more as the authors did not include costs for the 2–3 years of life lost/individual (Torgerson et al., 2008). Consequences for parasitised individuals include a compromised quality of life and reduced productive capacity during the symptomatic phase resulting in a marked increase in years lived with disability (YLDs) and a reduction in life expectancy, i.e. increase in years of life lost (YLLs; Torgerson et al., 2010). The establishment of E. multilocularis may also have significance for the wider society, especially, rural communities. Given that agricultural related activities especially, those that involve soil contact such as horticulture are considered important risk factors for AE, farmers and horticulturalists may have to adopt measures to reduce the risk, such as wearing gloves when handling vegetables and soil and washing hands before taking meals after working on their farms (Kern et al., 2004). Another risk factor for humans is allowing dogs freedom to hunt rodents, in
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particular in areas where the landscape composition provides an optimal habitat to support large populations of rodent intermediate hosts and long-term survival of tapeworm eggs. This has been shown to be predominantly grasslands where the soil has a high humidity (Staubach et al., 2001; Danson et al., 2004; Graham et al., 2005). There may also be costs to public health regulatory authorities associated with increased wildlife surveillance to determine the present and future distribution of the parasite. Although over time, some of the costs associated with these surveys may be reduced by using geographical information systems to target specific environment niches of the intermediate and definitive wildlife hosts (Staubach et al., 2001; Graham et al., 2005). It is generally accepted that the uncontrolled movement of definitive wildlife hosts of E. multilocularis from endemic to non-endemic areas invariably leads to the establishment of the tapeworm in the clean areas (Vertvaeke et al., 2006; Takumi et al., 2008). A similar situation may arise if no restrictions are placed on the movement of domestic pets from infected zones (Nonaka et al., 2009; Peregrine et al., 2010, cited by Jenkins et al., 2011). It has been recommended that all potential definitive hosts before national or international travel from endemic to non-endemic regions should be treated in a quarantine unit on two consecutive days with therapeutic doses of praziquantel (Droncit, Bayer AG, Germany) and have valid veterinary certification of the E. multilocularis status of the region/country of origin and an import licence from the veterinary authorities in the country of destination. The authors justified these measures on account of the high risk posed by the translocation of definitive hosts (Eckert et al., 2001c). Given that in endemic areas there is an 85% probability that every week one dog for every 10,000 dogs will be exposed to infection (Torgerson and Craig, 2010), the mandatory requirement for dogs irrespective of they being native to or just visiting continental Europe, to receive an anti-tapeworm treatment before travelling is appropriate and proportionate to the risk of importing E. multilocularis into those countries covered by PETS. There has been no evidence of human echinococcosis in Ireland prior to it being declared a notifiable disease in 2004 (Anonymous, 2005). There have also been no reports of autochthonous cases since it was made notifiable. The results of the recent wildlife surveys reported here given a design prevalence of 1% for defining freedom as suggested by EFSA (Boue et al., 2010), indicate that there is there is a high probability that Ireland is free from E. multilocularis. These results, which document freedom from disease, together with the fact that once established in an area the parasite is impossible, with present knowledge, to eradicate, strengthen the case for retention of the mandatory regulation requiring all dogs travelling to this country from European Union and ETA member states other than Finland, Malta, U.K. and Norway receive an anthelmintic treatment before embarking on a ferry or airplane. Acknowledgements The assistance of the Research Officers and staff at the Regional Veterinary Laboratories is gratefully
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