Parasitol ResDOI 10.1007/s00436-008-1052-y
T. J. Naucke & B. Menn & D. Massberg & S. Lorentz
Received: 10 April 2008 / Accepted: 26 May 2008
Abstract This study has provided evidence for the natural
been 11 cases of leishmaniasis in Germany in which an
occurrence of sandflies in Germany. Two species belonging to
autochthonous origin was confirmed or which were highly
the genus Phlebotomus were detected. Phlebotomus (Lar-
likely to have been of indigenous origin. Data from the
roussius) perniciosus, a proven vector of leishmaniasis, was
German meteorological service indicate that Germany
found in association with an autochthonous case of canine
currently has a Mediterranean climate, with an annual
leishmaniasis near Kaiserslautern. Two hundred thirty-seven
average temperature of 10°C being reached or exceeded in
specimens of Phlebotomus (Transphlebotomus) mascittii
several regions. This type of climate is also appropriate for
were caught in 17 different locations in Baden-Wuerttemberg
the living conditions of sandflies. Therefore, it is assumed
and Rhineland-Palatinate. The northernmost finding in
that sandflies have a greater geographical distribution in
Germany (and Europe) was near Cochem (Moselle). P.
Germany than the first studies suggested, being mainly
mascittii has not yet been confirmed as a vector of
restricted to the southern region of Baden-Wuerttemberg.
leishmaniasis, but its competence is strongly suspected. In
The risk of an autochthonous canine infection occurring in
addition to the detection of the vector, since 1991, there have
Germany is very low. The rapidly increasing number ofimported cases of leishmaniasis in dogs means that special
attention must be focused on veterinary advice to dog
owners about prophylaxis. The results indicate that the use
of repellents and preventive behavioural measures is vital.
University Hospital Bonn,Sigmund Freud Straße 25,53105 Bonn, Germanye-mail: [email protected]
In western Europe, phlebotomine sandflies (Diptera: Psy-
Department of Zoology, Division of Parasitology,University of Hohenheim,
chodidae) are abundant in the Mediterranean area where
species of the Phlebotomus genus are of special importancebecause of their role as proven or suspected vectors of
Institute for Zoomorphology, Cytology and Parasitology,Heinrich Heine University,
Leishmania spp. are obligate intracellular parasites prop-
agating in reticuloendothelial cells of their host. In Europe,
Leishmania infantum is the main causal agent. So far, 11zymodenes of
Institute of Biology, Division of Zoology, Kassel University,
have been typed using biochemical and molecular biological
methods. In dogs, clinical signs may vary from cutaneous tovisceral manifestations, e.g. dogs infected in southern Greece
predominantly show skin involvement and lymphadenopathy,
Parasitus Ex e.V., Vollbergstraße 37,53859 Niederkassel, Germany
whereas the main clinical symptoms in infected dogs in
Table 1 Variation of clinical signs in dogs infected with L. infantum
leishmaniasis or vector competence is strongly suspected.
in different regions (sample size ≥
Phlebotomus (Larroussius) perniciosus is a proven vector
for human and canine leishmaniasis. The main hosts are
dogs, humans, horses and rodents (in order of relevance).
The main hosts of Phlebotomus (Transphlebotomus)
mascittii are humans and dogs. This species has not yet
been confirmed as a vector of leishmaniasis, but its
anthropophilic and zoophilic behaviour and belongs to the
subgenera Adlerius and Larroussius, which include all the
potential vectors of Mediterranean kala-azar. Furthermore,
P. mascittii was the only species found in geographical
areas where autochthonous cases of leishmaniasis were
described (e.g. in the Vosges; Péhu ).
In Germany, leishmaniasis is the most frequently imported
arthropod-borne disease in dogs as well as the most severe
infection of this type. Although in central Europe leishman-iasis is generally regarded as an ‘exotic disease’, there isevidence for the natural occurrence of sandflies in Germany,and cases of autochthonous origin have been confirmed.
southern Spain are splenomegaly and hepatomegaly (Table ).
Without medical treatment, up to 90% of dogs die within1 year.
Sandflies are the vectors of Leishmania spp. Adult
and autochthonous leishmaniasis in Germany
sandflies feed on sap, honeydew and/or excretions ofaphids. For the development of their eggs, female sandflies
It is a widely held belief that the Alps form a natural barrier to
additionally need to suck blood (Fig. ), for which,
the geographical distribution of sandflies due to climatic
different species of sandflies prefer different animal species
conditions. In fact, however, there are regions in Germany
or humans. With their blood meal, they incorporate
with a Mediterranean climate which is appropriate for the
amastigote Leishmania in monocytes from the host (human
living conditions of sandflies. Data from the German
or animal reservoir—dog, fox, cat, rodents and possibly
meteorological service for the 5-year period from 2001 to
others). These amastigotes develop into infectious promas-
2005 indicate several regions where an annual average
tigotes in the gut of sandflies and may be transmitted to
temperature of 10°C is reached or even exceeded, especially
along the Rhine rift up to Frankfurt and around Cologne/Bonn
In Europe, 23 species of sandflies from two genera are
known. Several of these species are proven vectors of
P. mascittii has already been found in neighbouring
countries: in western and southern Switzerland in 1912 and1931, respectively (Galli-Valerio , Vogel inFrance in 1950 close to the German border in Strasbourg(Callot and recently in 2001 in Sainte-Cécile(Florenville) in Belgium (Depaquit et al. ).
In Germany, the first four sandflies were trapped in 1999
at three different locations near Breisach (Kaiserstuhl;Naucke and Pesson In the following years, studieswere extended to the north, following the Rhine rift(Naucke and Schmitt ). By 2007, a total of 237specimens of P. mascittii had been caught in 16 differentlocations in Baden-Wuerttemberg and one location inRhineland-Palatinate, the latter near Cochem (on the Moselriver) being the northernmost finding of a sandfly species inEurope (coordinates: 50°19′41.2″ N, 07°15′36.9″ E; Fig. In addition, the first breeding area in Germany was found in
Fig. 1 Female of P. Mascittii almost completely engorged with blood
an old barn in the village of Neuenburg (Naucke ).
The natural occurrence of sandflies in Germany has beenproven definitely. P. perniciosus probably migrated fromFrance through the Saarland, P. mascittii followed theRhine rift and the course of the Moselle.
It has to be assumed that sandflies have a wider geo-
graphical distribution in Germany than these initial investiga-tions indicate, as they were mainly restricted to the southernpart of Baden-Wuerttemberg. The majority of the other regionsin Germany in which climatic conditions are suitable forsandflies and/or where autochthonous cases of leishmaniasishave been reported have not been investigated yet.
In addition, it has to be assumed that the number of
sandflies is higher than the numbers of trapped specimenssuggest. P. mascittii is presumed to be averse to light, so itscapture might only be an accidental occurrence which doesnot represent the true density and spread of the population.
In recent years, evidence of the northernmost occurrence
of sandflies in Germany, and indeed in Europe, hasgradually shifted from 47°55′05.3″ N (Bremgarten, Nauckeand Pesson to 48°44′42.2″ N (Baden-Baden, Naucke) and recently to 50°19′41.2″ N (Cochem).
The reported geographical distribution of endemic
leishmaniasis has expanded since the 1990s. This spreadis due to a combination of factors, among them increasedmonitoring, more intensive research, demographic changes,land use/land cover changes that create new habitats and
Fig. 2 Climates (German meteorological service), distribution ofsandflies and of autochthonous cases of leishmaniasis in Germany
changes in microclimate and seasonal climate (Lindgrenand Naucke ). In the longer term, by about the year
Sandflies were trapped with CDC light traps which were
2025, climate change might have resulted in appropriate
placed in different locations overnight. Most frequently,
conditions for sandflies to live and multiply even in
they were caught in old barns and near human dwellings.
Under the climatic conditions in Germany, the sandflies
As not only dogs but also humans are hosts of P.
were active from June to August (Schmitt ).
mascittii, it is extremely important to establish a final
In 2001, P. perniciosus, a proven vector of L. infantum,
answer to the question of whether this species of sandflies
was detected for the first time in Germany (Naucke and
Schmitt Fig. ). In 1998/1999, a suspected case of
The number of dogs in Germany that are infected by L.
autochthonous leishmaniasis in a dog was reported to local
infantum during a vacation trip to Mediterranean countries
veterinarians in the village of Gehrweiler (Rhineland-
or are imported from these regions is rapidly increasing.
Palatinate). Throughout the summer of 2001, a CDC light
Founded in 2002, ‘Parasitus Ex e.V.’, an international club
trap was placed there, and four sandflies of the species P.
for owners of Leishmania-positive dogs, is today already
perniciosus (one male, three females) were caught.
providing therapeutic care for 2,465 dogs in Germany. It is
Since 1991, there have been 11 cases of humane/canine/
estimated that overall, there are about 20,000 infected dogs
feline/equine leishmaniasis in Germany in which an
in Germany. Therapy of leishmaniasis is only symptomatic,
autochthonous origin was confirmed or which were highly
so infected animals represent a reservoir of the causal agent.
likely to have been of indigenous origin. Most of the cases
Though the risk of autochthonous infection in Germany is
occurred in regions where sandflies have been found or
still very low, veterinary advice on prophylaxis for dog
where the climate is appropriate for their living conditions
owners planning a vacation in Mediterranean countries and
(Fig. ). Four of these cases were published: one dog each
people aiming to import an animal from these countries
in Landsberg/Lech (Bavaria) and near Cologne (Gothe
), one infant (Bogdan et al. and one horse near
Repellents are vital for prophylaxis, as shown in
laboratory experiments and in a recent field trial (Naucke
et al. Otranto et al. Additionally, behavioural
Lindgren E, Naucke TJ (2006) Leishmaniasis: Influences of climate and
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