Veterinary Parasitology 190 (2012) 196–203
Contents lists available at SciVerse ScienceDirect
Veterinary Parasitology
journal homepage: www.elsevier.com/locate/vetpar
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
i n f o
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
T.M. Murphy et al. / Veterinary Parasitology 190 (2012) 196–203
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.
197
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).
198
T.M. Murphy et al. / Veterinary Parasitology 190 (2012) 196–203
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
T.M. Murphy et al. / Veterinary Parasitology 190 (2012) 196–203
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.
199
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
200
T.M. Murphy et al. / Veterinary Parasitology 190 (2012) 196–203
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
T.M. Murphy et al. / Veterinary Parasitology 190 (2012) 196–203
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
201
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
202
T.M. Murphy et al. / Veterinary Parasitology 190 (2012) 196–203
acknowledged. The study was funded by the Department
of Agriculture and Food.
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