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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 150 dogs) 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 climate change. Epidemiology, ecology and adaptation measures.
measures that help to avoid sandfly bites are of great In: Menne B, Ebi KL (eds) Climate change and adaption strategies for human health. Steinkopff Verlag, Darmstadt, pp 1–449 Naucke TJ (2002) Leishmaniose, eine Tropenkrankheit und deren Vektoren (Diptera, Psychodidae, Phlebotominae) in Mitteleuropa.
Denisia 184:163–178 Naucke TJ (2007) Leishmaniasis—entering Germany. Tierärztliche Bogdan C, Schoenian G, Banuls AL, Hide M, Pratlong F, Lorenz E, Naucke TJ, Lorentz S, Gruenewald HW (2006) Laboratory testing of the Roellinghoff M, Mertens R (2001) Visceral leishmaniasis in a insect repellents IR3535® and DEET against Phlebotomus mascittii German child who had never entered a known endemic area: case and P. duboscqi (Diptera: Psychodidae). Int J Med Microbiol 296 report and review of the literature. Clin Infect Dis 32:302–306 Callot J (1950) Présence de Phlebotomus larroussei en Alsace.
Naucke TJ, Pesson B (2000) Presence of Phlebotomus (Trans- Annales de Parasitologie Humaine et Comparée 25:112 phlebotomus) mascittii Grassi, 1908 (Diptera, Psychodidae) in Depaquit J, Naucke TJ, Schmitt C, Ferté H, Léger N (2005) A molecular analysis of the subgenus Transphlebotomus Artemiev, Naucke TJ, Schmitt C (2004) Is leishmaniasis becoming endemic in 1984 (Phlebotomus, Diptera, Psychodidae) inferred from ND4 Germany? Int J Microbiol 293(Suppl. 37):179–181 mtDNA with new northern records of Phlebotomus mascittii Péhu B (1931) Sur un cas de kala-azar survenu chez un enfant de 5 ans n’ayant jamais quitté les Vosges. Lyon Med 147:731–734 Galli-Valerio B (1912) Beobachtungen über Culiciden und Mitteilung Otranto D, Paradies P, Lia RP, Latrofa MS, Testini G, Cantacessi C, über das Vorkommen von Phlebotomus papatasi (Scop.) im Mencke N, Galli G, Capelli G, Stanneck D (2007) Efficacy of a Kanton Waadt. Zentralblatt für Bakteriologie 43:222–226 combination of 10% imidacloprid/ 50% permethrin for the Gothe R (1991) Leishmaniosen des Hundes in Deutschland: Erreger- prevention of leishmaniasis in kennelled dogs in an endemic fauna und -biologie, Epidemiologie, Klinik, Pathogenese, Diag- nose, Therapie und Prophylaxe. Kleintierpraxis 36:69–84 Schmitt C (2002) Untersuchungen zur Biologie und Verbreitung von Koehler K, Stechele M, Hetzel U, Domingo M, Schönian G, Zahner H, Phlebotomus (Transphlebotomus) mascittii Grassi 1908 (Diptera: Burkhardt E (2002) Cutaneous leishmaniosis in a horse in southern Psychodidae) in Deutschland. Thesis, Institut für Medizinische Germany caused by Leishmania infantum. Vet Parasitol 109:9–17 Kuhn GK (1999) Global warming and leishmaniasis in Italy. Bull Vogel R (1931) Beobachtungen über blutsaugende Zweiflügler im

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