Wild animals kept in laboratories are potential carriers of viruses, bacteria and parasites. These might be a risk to people who have contact with those animals. We demonstrate this by the example of the American laboratory woodchuck (Marmota monax) which has been kept in our laboratory for 6 years (n=155). Beside Capillaria hepatica, the filaria Ackertia marmotae and the cestode Taenia crassiceps have been found. These three species were recognised outside the routine monitoring for parasites. As C. hepatica and T. crassiceps are human pathogens, the potential for transmission to humans and other woodchucks is estimated. Precautionary measures such as treatment to eradicate and hygiene instructions are discussed

Büttner, Dietmar

Hilken, Gero

Militzer, Klaus

English

Journals from University of Tartu

Scand. J. Lab. Anim. Sci. No. 3. 2003. Vol. 30.Three important endoparasites of laboratory woodchucks(Marmota monax) caught in the wild:Capillaria hepatica, Ackertia marmotae, and Taenia crassicepsby Gero Hilken, Dietmar Büttner & Klaus MilitzerCentral Animal Laboratory, University Clinic of Essen, Hufelandstraße 55, D-45122 Essen, GermanySummaryWild animals kept in laboratories are potential carriers of viruses, bacteria and parasites. These might be arisk to people who have contact with those animals. We demonstrate this by the example of the Americanlaboratory woodchuck (Marmota monax) which has been kept in our laboratory for 6 years (n=155). Beside Capillaria hepatica, the filaria Ackertia marmotae and the cestode Taenia crassiceps have beenfound. These three species were recognised outside the routine monitoring for parasites. As C. hepatica andT. crassiceps are human pathogens, the potential for transmission to humans and other woodchucks is estimated. Precautionary measures such as treatment to eradicate and hygiene instructions are discussed.IntroductionThe daily routine in an animal laboratory is orien-tated towards protecting animals from infections,which are free from pathogenic germs. A differentstrategy is required when animals caught in the wildare kept in a laboratory. In principle, they may all becarriers of parasites, which might be dangerous toother animals or humans. But information is nor-mally not available concerning the potential spec-trum of parasites of the population, from which theanimals have been taken. Therefore, it is difficult toassess the risk to people, when they working withsuch animals.Woodchucks (Rodentia, Sciuridae) are often carri-ers of a particular hepadnavirus (WoodchuckHepatitis Virus). Because of the similarity to humanviral hepatitis, this species is regularly used as ananimal model to examine different aspects of hepa-titis (Young & Sims 1979, Snyder 1985, Marion1988, Korba et al. 1989, Lu et al. 1999). The bre-eding of woodchucks in captivity is very difficult. Purpose-bred animals are unobtainable yet. There-fore nearly all experiments were carried out with animals caught in the wild. The present studyreports three cases of different infections that regu-larly occurred in our laboratory. Together with ashort review of the corresponding literature advicesfor laboratory animal facilities are given. Animal keepingIn our laboratory 155 woodchucks (Marmotamonax Linné, 1758), caught in the wild in the USA(Northeastern Wildlife, South Plymouth) were keptsince 1991 (Figure 1). Animals were housed underCorrespondence to: Dr. Gero HilkenTel.: (0201) 723 4663Fax: (0201) 723 5941Email: gero.hilken@uni-essen.deFig. 1 The laboratory Woodchuck (Marmota monax).151Scand.  J. Lab. Anim. Sci.  No. 3.  2003. Vol.  30152.standardised laboratory conditions: constant12L:12D photoperiod, room temperature 20°C 2°C, humidity 50%  5%. Guinea pig diet wereprovided ad libitum, together with salad and fruits.Cages (100cm x 65cm x 89cm) were subdividedinto two parts (length 50cm each): one filled withstraw for shelter, in the other one water and foodwas available. Case reports The infections of woodchucks with Taenia crassi-ceps (Cestoda, Taeniidae), Capillaria hepatica(Nematoda, Capillariidae) and Ackertia marmotae(Nematoda, Onchocercidae) which will be reportedhere, were discovered during health control.Taenia crassiceps (Zeder, 1800). Two animalsshowed conspicuous swellings: one at the left hindleg, the other at the jaw-bone. Because it was pre-sumed at the beginning that there were tight absces-ses, the animals were anaesthetised and investi-gated. The left hind extremity of the first affectedanimal showed a clear swelling and was nearlyunmoveable. After the skin was cut, an opaque masswas revealed in the subcutis, in which single vesic-les could be distinguished on closer inspection(Figure 2). It was suspected that the vesicles couldbe cestodal stages but the large number was confu-sing. More than thousand of these cysts were foundinside the subcutis and also deeper in the muscularsystem of the thigh. The cysts varied in shape, fromround to egg shape (Figure 3) and moved quitequickly when they were alive. Under the microsco-pe, most of the scolices were just recognizable asunclear whitish areas. Some cysts were ready toturn their scolices (S) out and in others buddingprocesses (C) could be observed (Figure 3). The second animal showed the same symptoms.The location of the infection were the muscles ofthe left lower jaw-bone and the swelling reached theneck region. Therefore the animal was not able toclose the mouth completely. Due to the poor condi-tion of the two animals and the initially unclear dia-gnosis - it could not be ruled out that the animalkeepers might be put in danger at this point - theanimals were killed under anaesthesia by an overd-ose of Ketamin and Xylazin. Material was taken fora later determination, that proved that the cysts werecysticerci of the cestode Taenia crassiceps.Fig. 2-3 Subcutaneous infection with cysticerci ofTaenia crassiceps. – 2) Opened hind extremity: some hundred cysticercibecome evident (overview); 3) Cysticerci, detail (S: scolex, C: budding cysts).Scand.  J. Lab. Anim. Sci.  No. 3.  2003. Vol.  30153.Ackertia marmotae (Webster, 1967). - When skincells of 3 woodchucks were cultivated, many she-athed microfilaria of Ackertia marmotae werediscovered in cell cultures. Due to their pointed tailends, they were easy to identify (Figure 4). Togetherwith larval stages, the adults were also observed.The adult nematodes were very mobile and stayedin the culture for several days. Blood smears (Giem-sa staining) from the 3 affected animals, revealed A.marmotae in only one animal.Fig. 4 Sheathed microfilaria of Ackertia marmotae, the pointed tail end is clearly recognisable.Capillaria hepatica (Bancroft, 1893). - During thehistological examination of a liver biopsy, an infe-ction of the liver parenchyma with Capillariahepatica was diagnosed in three animals (Figure 5).The liver showed a whitish-yellow focus, compris-ing clusters of eggs. The infection was identified bythe characteristic eggs (length 48-62  µm, width 29-37 µm), which have two pole plugs (Figure 6, P).The affected areas of the liver had become granulo-ma-like, with leuco-lymphocytic infiltration (Figu-re 5).DiscussionParasite biology and human pathogenity Taenia crassiceps. - The infection with T. crassicepsis caused by the ingestion of the intermediate host(rodents), which carries cysticerci. The prepatentperiod lasts 31-42 days and the patent period is 2 to5 years (Mehlhorn et al. 1993). Cysticerci canreproduce asexually by shooting at the distant scol-ex pole (Figure 3), even single cells can turn intocomplete cysts (Toledo et al. 1997). Reproductionin the abdominal cavity has been reported (Chernin& McLaren 1983, Toledo et al. 1997). Carnivoreslike dogs, foxes, cats, and pigs can be infected withT. crassiceps as definitive hosts (Blair & Campbell1976, Rietschel 1981, Kunstÿr 1992, Chermette etal. 1993, Schuster et al. 1993, Alvarez et al. 1995).The cysticercosis has been associated with immunesuppression (Villa & Kuhn 1996). Human infectionhas been known and Aids patients appear to be part-icularly at risk (Klinker et al. 1992). Two cases havebeen reported of cysticerci embedding themselvesin the front eye chamber of children (Shea et al.1973, Arocker-Mettinger et al. 1992). One of theseinfections was transmitted by a pet dog (Arocker-Mettinger et al. 1992).Fig. 5-6 Capillaria hepatica. – 5) Affected liver parenchyma, overview; 6) Length section of eggs (P: pole plug)Scand.  J. Lab. Anim. Sci.  No. 3.  2003. Vol.  30154.Capillaria hepatica. - The life cycle of C. hepaticahas been well investigated (Müller et al. 1990). Theadult stages live in the liver parenchyma directlyunder the surface of the organ and the eggs remainthere too for the entire life of the host (Mehlhorn etal. 1993). As a rule, rodents, especially rats andmice are the most important hosts of C. hepatica(Farhang-Azad 1977a, Kunstÿr 1992, Ruempler1995). In the case of rats, cannibalism has been de-scribed as the most important method of transmis-sion (Farhang-Azad 1977b). However, a far largerspectrum of hosts exists as monotremata (2 spe-cies), marsupials (67 species), rabbits, cats, dogs,foxes and primates are also affected (Kunstÿr 1992,Singleton et al. 1991, Mehlhorn et al., 1993). Infec-tions with deadly courses have also been reported inprimates and humans (Kunstÿr 1992, Gonzales Bar-ranco et al. 1996, El Nassery et al. 1996). Ackertia marmotae. - The incubation period of A.marmotae lasts for several months, the prepatentperiod 18 months and the patent period lasts someyears. According to Cohn et al. (1986), 92% ofwoodchucks captured in the wild are infected by A.marmotae. When kept under laboratory conditions,the number of infected animals was reduced conti-nuously even without treatment. However, after 39months, 53 % of the animals were still affected. Thedevelopment of microfilariae to the third larval stage stops in the laboratory, because their interme-diate host (Ixodes cooki), is not present (Ko 1972,Cohn et al. 1986). For this reason, animals born inthe laboratory show no infection. There have beenreports (Mehlhorn et al., 1993) that filaria causehyalinized hardening areas in affected zones, oede-ma, fistula, general condition disorders, shaggy fur,emaciation, visual impairment (due to microfilariaentering the eyes). Slight infection is often symp-tomless. The effects of A. marmotae on the host areunknown.Significance for Animal LaboratoriesUntil now just a few authors (e. g. Albert et al. 1972,Snyder 1985, Cohn et al. 1986) have investigatedwoodchuck parasites and human pathogenic parasi-tes have only been reported in a few cases. There-fore personnel who are in contact with these ani-mals and their organs are often unaware of thehealth risks. However, our case report shows thatwhen animals captured in the wild are used, greatcare should be taken. The probability of humaninfection may be small, but the consequences areconsiderable if infected. The findings can also beapplied to other animals captured in the wild. Twoof the parasites which have been proven here toinfect woodchucks (C. hepatica, T. crassiceps) canalso be brought into the laboratory by other rodents.The woodchuck which was infected by T. crassi-ceps had already been kept in the Central AnimalLaboratory for 11 months. Ruempler (1995) statedthat treatment against the cysticerci of Taenia is notpossible. Campbell & Blair (1974) report, on theother hand that cyst stages are sensitive to thiaben-dazole. However, for safety reasons it seemsappropriate to kill the affected woodchuck, as reci-dive could appear (Chermette et al. 1993). Becausein the case of T. crassiceps, transmission can alsooccur without an intermediate host, this cestoderepresents a potential risk to other woodchucks(cannibalism) as well as to humans. Since even iso-lated cells can lead to infection (Toledo et al. 1997)great caution should be exercised, particularly whenhandling organ material. Technical or scientificemployees, who work with liver cells of wood-chucks can also be infected by C. hepatica, if theycontravene rules of hygiene. On the other hand, thedanger that woodchucks could infect each other isconsidered remote (cannibalism). However, as theeggs remain in the host life long, if not treated, thedanger of infection is potentially present for years.ConsequencesObviously, not all the infected animals are detectedby routine examination. This is why staff are orde-red to observe strict hygiene rules. Newly deliveredwoodchucks are kept in quarantine in the CentralAnimal Laboratory Essen for three months beforebeing used in experiments. Because many wood-chucks are frequently infected with A. marmotaeScand.  J. Lab. Anim. Sci.  No. 3.  2003. Vol.  30155.(compare Cohn et al., 1986), treatment is imperati-ve. According to several authors, ivermectin is sui-table for the treatment of A. marmotae as well as C.hepatica (Mehlhorn et al. 1993, El Nassery et al.1996, Kirkpatrick & Nelson 1987). Therefore allnewly delivered animals are preventively treatedwith ivermectin (ivomec®, MSD AGVET, 0.2mg/kg body mass). In addition, the introduction ofA. marmotae into the laboratory is stopped by usingan ectoparasiticum (for example Fipronil [Frontli-ne®, Merial]) to fight the intermediate host. Addi-tionally, woodchucks are given praziquantel (Dron-cit®, 1 x 5 mg/kg body mass, s.c.) to preventcestodal infection. However, it must be assumedthat not all parasital stages can be successfully defe-ated by these treatments. This is why the measuresof hygiene include wearing coats, gloves and facemasks. In order to recognise illness as early as pos-sible, our animals are regularly weighed and exami-ned.Acknowledgements We are very grateful to Dr. S. Wade (New York Dia-gnostic Laboratory) and Prof. Dr. B. C. Tennant(Cornell University) for their classification of Tae-nia crassiceps. We would like to thank Dr. M. Luand Prof. Dr. M. Roggendorf (both Institute of Viro-logy, Essen) for their cooperation in the healthmonitoring of the woodchucks. 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Three important endoparasites of laboratory woodchucks (Marmota monax) caught in the wild: Capillaria hepatica, Ackertia marmotae, and Taenia crassiceps

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Three important endoparasites of laboratory woodchucks (Marmota monax) caught in the wild: Capillaria hepatica, Ackertia marmotae, and Taenia crassiceps

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