Adult fox tapeworm, on the left the greatly enlarged proglottis
|( Leuckart , 1863) Vogel, 1955|
The fox tapeworm ( Echinococcus multilocularis ) is a type of tapeworm (Cestoda) and parasitizes mainly in the red fox and other species of the genus Vulpes . Small mammals , especially voles and other rodents, serve as intermediate hosts . The fox tapeworm triggers alveolar (vesicle-like) echinococcosis , a life-threatening worm disease in humans.
Like all species of the genus Echinococcus , the fox tapeworm is a very small representative of the tapeworms , of which individual species can be several meters long. It reaches a length of only around 1.4 to 3.4 millimeters (according to other sources 1.2 to 4.5 millimeters) and is thus slightly shorter than the three-limbed dog tapeworm ( E. granulosus ), which is 2.5 in length to 6 millimeters (according to other sources 2.0 to 11.0 millimeters). The head ( Scolex ) has four suction cups and, like many tapeworms, hooks to attach to the intestinal wall of the host . These are arranged in two rings around the Scolex, the rostellum, each with 13 to 18 hooks of 20 to 34 micrometers in length, the outer hooks being slightly longer than the inner ones.
Its body is divided into two to six, usually four or five, segment-like body sections ( proglottids ) , the last proglottis being greatly enlarged and making up almost half of the entire length of the worm. In the proglottids there is a set of sex organs in which sperm and later eggs are produced. In the front to middle area of the proglottids is the genital opening (genital pore).
The spread of the fox tapeworm is linked to the availability of suitable main and intermediate hosts. The fox tapeworm has a distribution area over the temperate to cold-temperate climatic zones of the northern hemisphere. From the 1980s, however, there was an increasing spread in Germany as far as Lower Saxony and Brandenburg, but reliable figures are hardly available due to the differences in the monitoring system and reporting behavior of the individual federal states. In Europe, the main area of distribution is in Central Europe, especially in Switzerland (focus on the canton of Thurgau ) and in Germany in the Swabian Alb area , the occurrences are increasing. In Asia, the expansion extends from Russia and large parts of Central Asia via China to Japan, parts of Turkey, Iran and India seem to mark the southern edge of the range here. In North America, the occurrences of Alaska and Canada extend south to the states of Nebraska, Iowa, Illinois, Indiana and Ohio. In Europe, only the United Kingdom, Ireland, Finland and Malta are free from this parasite.
In Central Europe there is almost no overlap with the area of distribution for the dog tapeworm ( Echinococcus granulosus ). A reason for this distribution is not yet known. In other regions, namely Turkey, Iran, Central Asia, Siberia and China, both species occur side by side.
Within the range, the incidence and frequency of the fox tapeworm depend on a number of factors, including the individual susceptibility of the hosts available, their respective population density and their food spectrum. This leads to an island-like distribution of the populations within the range. The occurrence of the fox tapeworm and the prevalence of echinococcosis can vary greatly between large regions and between areas of only a few hectares in close proximity.
An example of such fluctuating frequencies comes from human medicine. The highest rate of alveolar echinococcosis ever recorded was determined between 2000 and 2002 in a series of 3200 participants in a district in the Chinese province of Sichuan . The prevalence was 6.2 percent; from village to village it fluctuated between 0 and 14.3 percent. Favoring factors were illiteracy, livestock and dog keeping and the local frequency of small mammals (potential intermediate hosts of the fox tapeworm). In Central Europe, fewer than 5 in 10,000 people develop alveolar echinococcosis.
In some regions up to 72% of foxes are infested (Southwest Germany), in others only up to 5%. A study of the urban fox population in Stuttgart found an infestation rate of 20 percent, in Zurich it was 48 percent. For Upper Bavaria 27% is given. A Germany-wide study found a fox tapeworm infestation rate of 0.3 and 0.35 percent in domestic dogs and cats.
The infestation rate of intermediate hosts increases with age and appears to fluctuate with the weather, with the cold causing an increase, but the amount of precipitation playing a lesser role. In Zurich and neighboring Rifferswil, water voles ( Arvicola terrestris ) were examined for infestation with fox tapeworms in 2007 and 2008 . The prevalence of an infestation with fox tapeworm larvae was around 15 percent over the entire study, but in one study area it fluctuated between around 40 and almost 80 percent.
The fox tapeworm has been spreading beyond its original range in Europe since the end of the 20th century. At the end of the 1980s, only Germany, Austria, Switzerland and France were known to enzootic areas in Central Europe . Since then, both the infection rate of foxes and the number of occurrences in these countries have increased sharply. There are first finds and evidence of newly created enzootic areas from the Netherlands, Belgium, Luxembourg, Poland, the Czech Republic, Slovakia (1999), Italy, Spitzbergen (1999), Denmark (2000) and Hungary (2002). There were comparable developments in North America, where the fox tapeworm spread from northern Canada to some central US states, and from Japan, where a small population expanded to the entire island of Hokkaidō .
One of the reasons for the spread of the fox tapeworm and its often increasing population density is considered to be that the red fox populations have increased sharply in Central Europe since the 1980s due to the success of the vaccination programs against rabies and the lower level of hunting, in Central Europe between 1980 and 1995 Quadruple. In addition to the introduction of rabies vaccination programs, the restructuring of agricultural production and the drop in prices for fox pelts are cited as possible reasons for the spread in Eastern Europe .
One consequence of the increased population pressure on the foxes is that they increasingly colonize urban areas and bring the fox tapeworm closer to humans. The number of foxes found dead or shot in the city of Zurich has increased twenty-fold since 1985. A comparison of the Swiss case numbers of alveolar echinococcosis determined since the 1950s with the national hunting statistics showed that fluctuations in the number of foxes shot with a delay of 10 to 15 years, corresponding to the assumed incubation period , followed an increase or decrease in diseases. In the United States, where the coyote ( Canis latrans ) is an important major host of the fox tapeworm, its immigration to the suburbs is viewed with concern.
The introduction of the fox tapeworm to Svalbard represents a special case . The arctic fox is the only main host on the island , and originally there was no small mammal as an intermediate host. The first observations of mice were made in the 1970s near the settlements of Russian miners; it is believed that they arrived on the island with imported animal feed. The rodents were initially mistakenly regarded as field mice ; it was not until 1990 that they were identified as Eastern European field mice by means of DNA analyzes . Their original range extends from the Balkans via Finland to Siberia. In the summer of 1999, an examination of individual animals for parasite infestation was carried out as part of a biological study of the mouse population. During this and a more extensive study in the following year, it was found that the fox tapeworm not only occurs frequently in mice, but that its population density is one of the highest ever recorded. The only possible explanation for the occurrence of the fox tapeworm is considered to be the migration of infected arctic foxes across the polar ice. The tapeworm eggs excreted by the infected foxes were ingested by the mice introduced by humans, which enabled the fox tapeworm to establish itself on Svalbard.
Attempts to reduce the exposure to parasites in the foxes through drug treatment were initially successful, and the number of worm eggs released into the environment could be reduced. However, the exposure of the intermediate hosts to worm larvae remained high, and the fox tapeworm life cycle is maintained in a region even if only 1 percent of the intermediate hosts are infected. Therefore, the control of the fox tapeworm requires continued treatment of the ultimate hosts. Where control measures are carried out, they are most effective before the start of the cold season, as worm eggs excreted in cool weather remain infectious for a particularly long time and the infection rate of intermediate hosts increases more sharply.
Several states that are currently free of fox tapeworm or suspected to be free of fox tapeworm have restrictions on the importation of animals that are potential carriers of an infection. For this reason, Great Britain, Ireland, Malta, Sweden and Finland require a certificate of recent deworming when crossing the border with pets such as dogs or domestic cats . For a transitional period, these regulations are in line with European Union law . In addition, as far as the mainland is concerned, Norway officially considers itself free of fox tapeworm and has made comparable entry regulations. These Norwegian restrictions apply to entry from all countries other than Great Britain, Ireland, Malta, Sweden and Finland and are also in line with European law. Sweden and Finland are striving to prove that they are free from fox tapeworms and thus to be able to make an indefinite regulation.
Way of life
The life cycle begins with the adult fox tapeworm that has established itself in the small intestine of a final host. The self-fertilized eggs, which contain the first larval stage of the fox tapeworm, mature in its last proglottis . By shedding the last proglottis, up to 200 mature eggs are released into the intestines of the final host every day and are released into the environment with the faeces. The eggs are very cold-resistant and can remain infectious for months.
Voles in particular serve as intermediate hosts, but all other mammals, including humans, can also function as false intermediate hosts. Even dogs can be intermediate and final hosts at the same time when they consume fox droppings. After the eggs have been taken up by an intermediate host, the egg capsule dissolves and the so-called oncosphere or hexacanthene larva (6-hook larva) is released. It is believed that the low pH of the environment and the bile trigger the process and that the composition of the bile also plays a role in the host specificity of the fox tapeworm.
The larva penetrates the epithelial tissue of the intestinal wall and reaches the intermediate host's liver via the mesenteric veins and the portal vein , but in exceptional cases it can also affect the lungs, heart or spleen. The oncosphere settles in the tissue and forms the second larval stage, the metacestode , or fin, a bladder filled with gelatinous mass, which is separated from the surrounding organ by a wall of connective tissue. How this process is triggered and controlled is not known.
As the infection progresses, more and more fins arise from the wall of the metacestode through budding; a larval structure is created, which consists of an accumulation of bubble-like fins and infiltrates the host tissue. It is therefore differentiated as hydatide of the alveolar (bladder-like) type from the hydatide of the cystic type of dog tapeworm, in which a large hydatid bladder is formed by budding inwards. During budding, cell clusters or individual cells of the metacestode can become detached, reach other organs via the host's bloodstream, attach themselves there and form further foci.
After two to four months in a suitable intermediate host, the third larval stage in the Finns is the protoscolices with their inverted heads, and the budding and growth of the metacestodes come to a standstill.
In humans, as false hosts, the budding of the metacestodes is greatly slowed down and at most only a few protoscolices are formed. The metacestode grows outwards, and degradation processes occur in its center. This creates a slowly increasing mass of necrotic tissue that is covered by a relatively thin layer of living parasite tissue.
The disease makes the intermediate host weaker and weaker and thus easy prey for the ultimate host (dog, fox, cat). Even after the natural death of the intermediate host, the metacestodes remain infectious for a long time, so that animals that feed on carrion can also become final hosts. If the ultimate host ingests metacestodes with the food, they are digested and the released protoscolices turn out their holding organs, with which they fix themselves in the small intestine of the host. They grow into the new generation of tapeworms by forming new proglottids on the "head" that has now been transformed into the scolex of the new tapeworm.
Their nutrition in the main host is commensal , the food is absorbed through their outer skin, the syncytial neodermis . It consists of the “food pulp” that is present in the small intestine and from which the worm absorbs the nutrients. The metabolism proceeds anaerobically via glycolysis . Thousands of worms can exist in the ultimate host without seriously affecting it. If the infestation is severe, the parasites are evenly distributed over the entire small intestine; if there are few parasites, the first third of the host's small intestine usually remains free.
The fox tapeworm infected as main hosts, especially members of the genus Vulpes , in Central Europe, Asia and North America, the red fox and the circumpolar regions of the arctic fox . In addition, coyote , wolf and domestic dog and, more rarely, wildcat and house cat can be attacked. Fox tapeworms are hardly harmful to the end host , even if they are heavily infested . Cats do not seem to play a role in the epidemiology of the fox tapeworm, the number of excreted eggs is low and their infectivity has not been proven.
Small mammals, especially voles , which are the most common intermediate hosts in Germany, serve as intermediate hosts. Infection with the fox tapeworm larvae leads to severe weakening or death within a few months.
Ingesting fox tapeworm eggs can also infect deer , elk , reindeer, bison , domestic and wild boar , horses, nutrias and primates including humans. If the fox tapeworm larvae growing in them do not pass to new main hosts through the consumption of meat or carrion from the intermediate host, then it is a question of false intermediate hosts, since the life cycle of the parasite expires with the death of its host. In humans, infection with the fox tapeworm eggs triggers alveolar echinococcosis , a life-threatening worm disease . In contrast to the infestation of regular intermediate hosts, the course of the disease in humans is insidious, the incubation period can be up to 15 years.
|Relationships within the genus Echinococcus|
|Two different phylogenetic trees based on mitochondrial DNA (mtDNA) and nuclear DNA ( nuclear DNA ). The brackets stand for different genotypes .
Nakao et al. 2007, Saarma et al. 2009
The first scientific description of Echinococcus multilocularis was made by Rudolf Leuckart in 1863. The systematics of the genus Echinococcus and thus also the systematic position of the fox tapeworm has not yet been conclusively clarified. The main problem here are the numerous forms of Echinococcus granulosus described as genotypes (designated as G1, G2, etc. in the cladograms) , which cannot be recognized as monophyletic clades in previous molecular biological investigations . In the current literature and therefore also in the adjacent cladograms, some of these are already regarded as separate species E. equinus , E. ortleppi , E. canadensis and E. intermedius .
The previous molecular biological investigations on the systematics of the Echinococcus species are based on mitochondrial and nuclear DNA ( core DNA ). The results of these two studies differ significantly: when using the core DNA, the fox tapeworm and the E. shiquicus endemic to Tibet represent the two basal species of the genus, and the different genotypes of E. granulosus form a taxon with E. felidis . When using mitochondrial DNA, however, these two species are placed in the middle of the E. granulosis genotypes.
Saarma et al. 2009 advocate the use of the core DNA to determine the phylogenetic relationships , since the mitochondrial DNA in this case of the parasitic way of life does not trace the actual development of the species due to its random mutation rate without recombination . According to this analysis, Echinococcus multilocularis is the most basic species of the genus, followed by E. shiquicus .
In the context of public health care there is great interest in reliably identifying the fox tapeworm as a pathogen of a life-threatening zoonosis and in providing information about its distribution and frequency.
In the adult stage and as a larva, the fox tapeworm can be reliably distinguished from the other representatives of the genus Echinococcus with the help of external features . However, the eggs can be confused with those of other species of the genera Echinococcus and Taenia , and a reliable identification requires genetic analysis .
Macroscopic or microscopic examination or DNA analysis are used to identify the larvae in intermediate hosts. In humans, various serological tests are used to diagnose an infection before symptoms appear.
In the case of the main hosts, the diagnosis is possible through an examination of the small intestine as part of a necropsy , which searches for adult fox tapeworms. Today the feces of both living and dead final hosts can be examined for coproantigens with a specific ELISA and by DNA detection using PCR . These methods are also suitable for examining faecal samples found in nature and are used for the systematic examination of the populations of foxes, dogs and cats as well as in veterinary diagnosis . Their main advantage lies in the lower risk to the personnel involved in the investigation. The reliability of the ELISA lags behind that of a necropsy under unfavorable conditions such as an additional infection with the dog tapeworm . The high technical effort and costs speak against DNA analyzes.
In Germany, the direct or indirect detection of Echinococcus sp. (also of the fox tapeworm) not subject to notification by name according to (3) of the Infection Protection Act (IfSG). The reporting obligation primarily concerns laboratories (see IfSG).
In Austria, suspected cases, illnesses and deaths from the fox tapeworm (Echinococcus multilocularis) are notifiable (in accordance with (1) (1) of the 1950 Epidemic Act). Doctors and laboratories, among others, are obliged to report this ( Epidemics Act).
- Where the fox tapeworm really lurks (background article in Wissenschaft.de from May 30, 2007)
- Patient information from the German Association of Internists
- Spiegel Online: Scary parasite
- Situation in Austria (PDF; 340 kB)
- Fox tapeworm podcast at www.forstcast.net
- University of Würzburg: Fox tapeworm 
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