Figure
Figure. Cysticercosis-like eye infection caused by the tapeworm Taenia martis in a woman. A) Fundus at the patient's initial visit, before medical therapy. The cyst lies subretinally at the temporal upper branch vessels; adjacent intraretinal and subretinal bleeding and central subhyaloid bleeding can be seen. B) After 8 days of medical therapy, the cyst size had decreased markedly. The physis of the larva (A and B) is reminiscent of the armatetrathyridium (or fimbriocercus), a larval form typical for the tapeworm subspecies T. martis martis. C) Cyst at patient's initial visit. D) Cyst at the time of surgery. E) Surgically removed monocephalic cysticercus-like larva with inverted parenchymatous portion, withdrawn scolex, and attenuated posterior end. The tegumental surface is transversely striated and exhibits inward folds (arrows). F) Histologic section of the Taenia martis tapeworm cyst showing morphologic characteristics also commonly seen in cysticercosis cysts caused by T. solium tapeworms. The syncytial bladder wall consists of a rugate external, a nucleated intermediate, and an internal reticular layer with lacunate branches of the excretory duct system. Filamentous extensions of contractile muscles project into the parenchyma, which is interspersed with a few calcareous corpuscles. In addition, the T. martis cyst shows a preponderance of uniformly organized, elongate and slender tegumental processes, which are usually not seen in histologic sections of cyst walls caused by T. solium tapeworms. Hematoxylin and eosin stain; objective magnification ×10.
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Citations
... To our knowledge, human T. martis cysticercosis has been reported for only 6 adults. Two cases involved a T. martis neurocysticercosis-like lesion (2,7), and the others involved the eye, peritoneum, and pouch of Douglas (3)(4)(5)(6). All 6 patients were immunocompetent women: 5 tended and ate from vegetable gardens, 5 lived in rural areas, and 3 were frequent hikers/dog owners. ...
... No specific serologic test is available for T. martis infection, and the extent of cross-reactivity between T. solium and T. martis antibodies in available serology tests is unknown. Serologic test results for the 6 adult patients showed mixed signals, including positive signals against Echinococcus multilocularis crude larval antigen extract (that could not be repeated in confirmatory assays) (5) and T. solium (2,5), although others have reported negative serologic test results for those parasites (3,4). Confirming the diagnosis requires detecting parasite DNA by PCR and sequencing to differentiate between Taenia species. ...
... Confirming the diagnosis requires detecting parasite DNA by PCR and sequencing to differentiate between Taenia species. The availability of differentiating molecular methods may have resulted in increased diagnoses of T. martis infections, possibly previously misdiagnosed as T. solium infections (3). ...
A neurocysticercosis-like lesion in an 11-year-old boy in the Netherlands was determined to be caused by the zoonotic Taenia martis tapeworm. Subsequent testing revealed that 15% of wild martens tested in that region were infected with T. martis tapeworms with 100% genetic similarity; thus, the infection source was most likely local.
... Cysticercosis of T. martis in rodents appears to occur throughout Europe with variable prevalence, while adult forms infect wild carnivores, mainly martens [4]. Cases of the larval stage have also been detected in humans [33][34][35][36] and non-human primates [37,38]. In 10 years of our research and 856 examined animals, only one small mammal (M. ...
Background
Hydatigera (Cestoda: Taeniidae) is a recently resurrected genus with the description of a new species, Hydatigera kamiyai, a cryptic entity within the Hydatigera taeniaeformis species complex. Rodents are intermediate hosts and correct taxonomic identification of H. taeniaeformis sensu lato (s.l.) species is difficult without the use of molecular methods. The aim of this study was to identify and explore the genetic diversity of Hydatigera and other taeniid species.
Methods
Ten different small mammals species (856 individuals) (Rattus rattus, three Apodemus, three Arvicolinae and three Soricidae species) were examined from 2013 to 2023. Captured animals were visually examined for cysts and visible lesions. Two markers were used for amplification and sequencing: cox1 and 12S rDNA.
Results
Molecular analysis of cysts and visible lesions revealed four taeniid species: Hydatigera kamiyai, H. taeniaeformis sensu stricto (s.s.), Taenia martis and T. crassiceps. Hydatigera kamiyai was found in Apodemus flavicollis, A. agrarius, Microtus arvalis and Crocidrua leucodon, while H. taeniaeformis s.s. is registered in R. rattus. Hydatigera kamiyai cox1 sequences clustered with European populations and showed at least 25 nucleotid differences compared to Asian, African, Australian and one of our isolates of H. taeniaeformis s.s acquired from a rat, followed by large sequence distances (9.4% to 12.9%), indicating clear molecular distinction of two species.
Conclusions
This is one of the few mitochondrial gene-based studies performed after the description of cryptic entities within the Hydatigera taeniaeformis s.l. complex and represents a valuable contribution to understanding of genetic diversity, host suitability and geographic distribution of these tapeworm species. Also, our study provides an important basis of molecular data from this part of Europe for further studies. We emphasize the importance of additional studies of intermediate hosts, especially rats from Europe and Apodemus spp. and voles from Asia and Africa.
Graphical abstract
... Intermediate hosts get infected by oral intake of eggs and afterwards the metacestodic larva called cysticercus is mostly found in peritoneal (Brunet et al., 2014;Deplazes et al., 2019;Rudelius et al., 2017) and pleural (Deplazes et al., 2019) cavities, and rarely the central nervous system (CNS) (Brunet et al., 2015;Deplazes et al., 2016). Primates, including humans, can become dead-end hosts through accidental ingestion of eggs through contaminated food, water or soil (Brunet et al., 2015(Brunet et al., , 2014De Liberato et al., 2014;Eberwein et al., 2013;Koch et al., 2016;Mueller et al., 2020). In humans, few cases of cerebral (Brunet et al., 2014) and ocular T. martis cysticercosis (Eberwein et al., 2013) have been reported. ...
... Primates, including humans, can become dead-end hosts through accidental ingestion of eggs through contaminated food, water or soil (Brunet et al., 2015(Brunet et al., , 2014De Liberato et al., 2014;Eberwein et al., 2013;Koch et al., 2016;Mueller et al., 2020). In humans, few cases of cerebral (Brunet et al., 2014) and ocular T. martis cysticercosis (Eberwein et al., 2013) have been reported. ...
... We would like to contemplate possible scenarios for the introduction of T. martis infective stages into the lemur's enclosure: 1) soil or food contamination with eggs from free-ranging martens living in the vicinities. This possibility has been strongly suggested for a human case in Germany (Eberwein et al., 2013). In that report, the affected patient kept a vegetables garden in their backyard next to a forest in which martens lived and were sighted near the patient garden (Eberwein et al., 2013). ...
We present the case of Taenia martis metacestode infection in a white-headed lemur (Eulemur albifrons) from a zoological park. A post-mortem examination was conducted on the unexpectedly perished animal and focal granulomatous pneumonia with metacestodic tissue was discovered. Identification of T. martis was conducted through amplification and sequencing of a 12S rRNA gene fragment. We discuss the possible sources of infection and underline the importance of this infection in public health and conservation.
... Cysticerci of the mustelid tapeworm Taenia martis, a frequent cause of cysticercosis in rodents in Central Europe, normally settles in the pleural and peritoneal cavities (Brunet et al., 2015;Loos-Frank, 2000). However, there are reports of T. martis as the causative agent of human neurocysticercosis (Brunet et al., 2015;Eberwein et al., 2013). Interestingly, one case report refers to the removal of a T. martis-cysticercus from the eye of a woman living in a rural area near the city of Hanover (Koch et al., 2016). ...
Small rodents serve as intermediate or paratenic hosts for a variety of parasites and may participate in the transmission of these parasites into synanthropic cycles. Parasites with neuroinvasive stages, such as Toxoplasma gondii or Toxocara canis, can cause detrimental damage in the brain of intermediate or paratenic hosts. Therefore, the occurrence of neuroinvasive parasite stages was evaluated in brains of wild rodents captured in the city of Leipzig, Germany. In addition, a few specimens from the cities of Hanover, Germany, and Vienna, Austria were included, resulting in a total of 716 rodents collected between 2011 and 2016. Brains were investigated for parasitic stages by microscopic examination of native tissue, artificially digested tissue as well as Giemsa-stained digestion solution to verify positive results. Infective stages of zoonotic ascarids or other helminths were not detected in any sample, while coccidian cysts were found in 10.1% (95% CI: 7.9–12.5%; 72/716) of examined brains. The most abundant rodent species in the study was the bank vole (Myodes glareolus; Arvicolinae), showing an infection rate with cerebral cysts of 13.9% (95% CI: 11.0–17.8%; 62/445), while 2.7% (95% CI: 1.0–5.8%; 6/222) of yellow-necked mice (Apodemus flavicollis; Murinae) were infected. Generalized linear modelling revealed a statistically significant difference in prevalence between M. glareolus and A. flavicollis, significant local differences as well as an effect of increasing body mass on cyst prevalence. Coccidian cysts were differentiated by amplification of the 18S rRNA gene and subsequent sequencing. The majority of identifiable cysts (97.9%) were determined as Frenkelia glareoli, a coccidian species mainly circulating between M. glareolus as intermediate and buzzards (Buteo spp.) as definitive hosts. The zoonotic pathogen Toxoplasma gondii was confirmed in one M. glareolus originating from the city of Leipzig. Overall, it can be concluded that neuroinvasion of zoonotic parasites seems to be rare in M. glareolus and A. flavicollis.
... In Europe, T. martis has been observed in martens and rodents in Italy, Germany, The Netherlands, Belgium, Spain, Poland, Belarus and Switzerland [3][4][5]. So far, to our knowledge, only three cases of human T. martis cysticercosis have been reported worldwide [6][7][8]. Cysticercosis manifested in the brain or in the eye as a solitary lesion. In our case, the patient also presented with a solitary lesion; however, not in the brain or eye but in the peritoneum like in the natural intermediate host reservoir. ...
Introduction. Correct diagnosis of peritoneal infectious disease can be extremely difficult due to non-specific clinical features. Thus, careful assessment with thorough histopathological work-up is essential. Here, we report the first case of human peritoneal cysticercosis mimicking peritoneal carcinosis.
Case presentation. The patient presented with recurring ascites and a tumour in the Douglas cavity accompanied by elevated tumour markers. There were no signs of systemic infection. On laparoscopy, the tumour was resected completely. Histology revealed a granulomatous reaction and a diagnosis suspicious of tuberculosis was made. Only after additional sections, avital cestode-fragments were visible and Taenia martis DNA was detected. Further staging by computerized tomography scan of the lung and brain turned out negative and the patient recovered quickly.
Conclusion. Laparoscopy and histopathological examination can be extremely helpful for correct diagnosis and management in uncertain recurrent ascites. This case clearly demonstrates that orphan infectious diseases should also be considered. Only complete histopathological examination with serial sections and additional molecular testing can lead to the appropriate diagnosis.
... In particular, it has been described to occur in more than 40% of red foxes in the Slovak Republik [54] and larval stages have been found in rodents of the species A. agrarius and M. glareolus [55]. T. martis has recently been considered to be an emerging infectious disease since it has been recognized to rarely cause infections of the eye and the brain in humans [56,57] and to cause severe to fatal infections in non-human primates [58,59]. The ITS-2 sequences obtained from four specimen here show a remarkably high diversity. ...
Rodents are important intermediate and paratenic hosts for carnivore parasites, including the important zoonotic agents Toxoplasma, Echinococcus and Toxocara. Monitoring of such parasites in rodents can be used to detect increasing risks for human and veterinary public health. Rodents were trapped at four sites in Berlin, two near the city center, two at the periphery. PCRs were conducted to detect Coccidia (target ITS-1) and specifically Toxoplasma gondii (repetitive element) in brain and ascarids (ITS-2) in muscle or brain tissue. During necropsies, metacestodes were collected and identified using ITS-2 and 12S rRNA PCRs. An ELISA to detect antibodies against Toxocara canis ES antigens was performed. Within the 257 examined rodents, the most frequently observed parasite was Frenkelia glareoli predominantly found in Myodes glareolus. T. gondii was only detected in 12 rodents and Microtus spp. (although strongly underrepresented) had a significantly increased chance of being positive. Neither Echinococcus nor typical Taenia parasites of dogs and cats were found but Mesocestoides litteratus and Taenia martis metacestodes were identified which can cause severe peritoneal or ocular cysticercosis in dogs, primates and humans. Using PCR, the ascarids T. canis (n = 8), Toxocara cati (4) and Parascaris sp. (1) were detected predominantly in muscles. Seroprevalence of T. canis was 14.2% and ELISA was thus more sensitive than PCR to detect infection with this parasite. Non-parametric multidimensional scaling and cluster analysis revealed that parasite communities could be grouped into an urban and a peri-urban cluster with high frequency of ascarid-positive rodents in urban and high frequency of F. glareoli in peri-urban sites. Prevalence rates of parasites in rodents with potential impact for human or veterinary public health are considerable and the monitoring of transmission cycles of carnivore parasites in intermediate rodent hosts is recommended to estimate the health risks arising from wild and domesticated carnivores.
... Rare cases of carnivore-transmitted cysticercosis caused by, for example, T. crassiceps (Heldwein et al., 2006;Flammer et al., 2014) and T. martis (Brunet et al., 2015;Eberwei et al., 2013), have been documented in people in Europe. Furthermore, several lethal T. martis (Brunet et al., 2014;De Liberato et al., 2014) and T. crassiceps infections were reported recently for lemurs in zoos (Luzon et al., 2010). ...
Due to frequent cases of alveolar echinococcosis (AE) in captive primates in Europe, 141 samples of food, which consists mostly of vegetables and fruits, were investigated for contamination with egg-DNA of taeniids. Each sample consisted of at least 40 heads of lettuce as well as various vegetables and fruits. The samples were purchased at different times of the year: either from September to November (autumn), originating from greenhouses or fields in the Basel region in the North of Switzerland, or in April and May (spring) when fruit and vegetables are sourced from throughout Europe from various wholesalers. Each sample was washed, and the washing water sieved through mesh apertures of 50 μm and 21 μm, respectively. The debris, including taeniid eggs, collected on the 21 μm sieve were investigated by a multiplex PCR-analysis followed by direct sequencing. In 17 (18%) of the 95 samples collected in autumn, taeniid-DNA was detected (Taenia hydatigena in four, T. ovis in three, T. polyacantha in two and Hydatigera (Taenia) taeniaeformis in five cases). Similarly, in 13 (28%) of the 46 samples collected during spring taeniid-DNA was detected (Echinococcus granulosus s.l. in two, T. crassiceps in one, T. hydatigena in two, T. multiceps/T. serialis in two, T. saginata in one and H. taeniaeformis in five cases). Although DNA of E. multilocularis was not found specifically in this study, the detection of other fox taeniids reveals that vegetables and fruit fed to the primates at the Zoo Basel at different times of the year and from different origin are contaminated with carnivore's faeces and therefore act as a potential source of AE infections.
... Cysticercosis, a zoonotic parasitic disease due to tissue invasion of larval Taenia species, is in the vast majority of human cases caused by the pork tapeworm Taenia solium. 1 However, other Taenia species with different reservoirs and epidemiology, such as Taenia crassiceps and Taenia martis, may also cause human cysticercosis, but much more rarely. [2][3][4][5] The larval stages share a highly similar morphology, and they might be virtually indistinguishable on histological sections. 6 Still, for prognosis, prevention, and detection of parasite reservoirs, the species responsible for human disease should be determined. ...
... Tissue sections of the specimen showed a characteristic tapeworm tegument (Figure 1), and ophthalmological cysticercosis was diagnosed. Polymerase chain reaction targeting cestode cytochrome c oxidase subunit 1 (cox 7 ), 12S rDNA, 4 and nicotinamide adenine dinucleotide-dehydrogenase subunit 1 (NAD1) 4 was positive. After sequencing of the 418-, 461-, and 440-bp amplicons, basic local alignment search tool analysis (www .ncbi.nlm.nih.gov/blast) ...
... 8 Human infection with T. martis, where the human serves as dead-end intermediate host, is very rarely seen and only two cases have been reported so far. 4,5 In 2010, the first described human infection with larval T. martis had occurred in a 43-year-old woman living in a small village in southwest Germany. 4 The patient had complained of flashing light sensations in her left eye, and a T. martis larva had been found subretinally similar to our case. ...
Taenia martis, a tapeworm harbored in the intestine of mustelids, is a rarely encountered zoonotic cysticercosis pathogen. The larval stage closely resembles the Taenia solium cysticercus, but the natural host and thus the epidemiology of the disease is different. We here report a human eye infection diagnosed molecularly in a previously healthy female German patient. The case represents the third human infection described worldwide; the two previous cases were also European, involving eye and brain.
... Various other zoonotic tapeworm species, which are propagated in different predator-prey cycles, have been described as causes of human cysticercosis (3)(4)(5)(6). Tapeworm larvae have a highly similar morphology. Histologically the species are often indistinguishable. ...
Rarely, zoonotic Taenia species other than Taenia solium cause human cysticercosis. The larval stages are morphologically often indistinguishable. We therefore investigated 12 samples of suspected human cysticercosis cases at the molecular level and surprisingly identified one Taenia crassiceps and one Taenia serialis (coenurosis) infection, which were caused by tapeworm larvae normally infecting rodents and sheep via eggs released from foxes and dogs. © 2015, American Society for Microbiology. All Rights Reserved.
... Neurocysticercosis caused by T. crassiceps or T. multiceps is less common yet should be considered in the differential diagnosis of CNS infections. T. martis cysticercosis was recently reported for the very first time in a human eye (5). ...
Taenia martis is a tapeworm affecting mustelids, with rodents serving as intermediate hosts. The larval stage (cysticercus) has before been found only rarely in humans or primates. We hereby describe a case of cerebral T. martis cysticercosis in a French immunocompetent patient, confirmed by DNA analyses of biopsy material.
Copyright © 2015, American Society for Microbiology. All Rights Reserved.
