Human Infection with Marten Tapeworm

To the Editor: Cysticercosis-like human infections with the tapeworm Taenia crassiceps, which infects foxes as terminal hosts, have been reported (1,2). We report a case of a cysticercosis-like eye infection caused by the tapeworm T. martis (marten tapeworm) in a woman. 
 
The patient was a 43-year-old German woman who sought care during July 2010, after 4 days of perceiving flashing lights in her visual field and a paracentral scotoma in her left eye. Visual acuity in both eyes was 20/20. Examination of the left fundus revealed a mobile subretinal tumor at the temporal upper retinal branch vessel with adjacent intraretinal and subhyaloid bleeding (Figure, panels A–C; Video). The subretinal tumor resembled a cestode larva. 
 
 
 
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 ... 
 
 
 
 
 
Video 
 
Taenia martis tapeworm cyst in woman with cysticercosis–like eye infection, before and after medical therapy. Although the cyst decreased in size after medical therapy, movements of the larva persisted. Video is 100 seconds long, taken with a ... 
 
 
 
The patient reported no other symptoms at that time. Laboratory evaluation found no eosinophilia or elevation of total IgE. Serologic testing results were negative for antibodies against the following parasites: Taenia solium, Echinococcus multilocularis, E. granulosus, Dirofilaria immitis, Strongyloides spp., and Toxocara canis. Fecal testing results were negative for worm eggs. Images from ultrasonography of the liver and magnetic resonance imaging of the head were unremarkable. The patient’s travel history included—in addition to southern European countries—trips to Nepal and Thailand 15 years previously. 
 
At the time of examination, the patient lived in a small village near Freiburg (im Breisgau) in southwestern Germany. She grew vegetables in the family garden, which was next to a forest. Her 3 children and husband did not report any health problems. For the past 6 years, the family had owned a dog, which received antiparasitic medications on a regular basis; recent checks for intestinal parasitic infection found no ova. 
 
The suspected cause of the woman’s illness was cysticercosis caused by the larva of T. solium; systemic antiparasitic therapy was started (albendazole 400 mg 2×/d, dexamethasone 20 mg/d). The size of the larva diminished (Figure, panel D; Video), but the patient remained symptomatic. Therefore, after 8 days of therapy, the cyst was removed by retinotomy. A few days later, peripheral retinal detachment occurred and was treated by a second vitrectomy and intravitreal gas injection. Because of the repeated gas tamponade, a gas cataract developed, which necessitated cataract surgery. At the end of March 2011, the patient’s visual acuity had returned to 20/20 in both eyes. 
 
The removed cyst showed the characteristic macroscopic and histologic features of a cysticercus bladder wall (Figure, panels E, F). To determine the exact species by using molecular methods, we isolated DNA from the cyst, conducted different PCRs selective for mitochondrial genes, determined the corresponding sequences, and used a BLAST search (3) to compare these sequences with publically available sequences. Sequences of the following mitochondrial genes were determined by using the given primers and later submitted to GenBank: small ribosomal subunit (primers 12S Taenia FF 5′-CACAGTGCCAGCATCYGCGGT-3′ and 12S Taenia RR 5′-GAGGGTGACGGGCGGTGTGTAC-3′, PCR product of 426 bp, GenBank accession no. {"type":"entrez-nucleotide","attrs":{"text":"JX415820","term_id":"407316738"}}JX415820); NADH dehydrogenase subunit 1 (primers: NAD1-FF 5′-ATTGGKTTATTTCAGAGTTTTTCTGATTTA-3′ and NAD1-RR 5′-CTCMCCATAATCAAATGGACTACG-3′, 394 bp, GenBank accession no. {"type":"entrez-nucleotide","attrs":{"text":"JX415819","term_id":"407316736"}}JX415819); and the cytochrome-c oxidase subunit 1 (determined by using previously published primers [4,5]; 376 bp, GenBank accession no. {"type":"entrez-nucleotide","attrs":{"text":"JX415821","term_id":"407316739"}}JX415821). All sequences showed highest identity with T. martis (99%–100%) but substantially lower identity with T. crassiceps (91%–97%) and T. solium (87%–89%) tapeworms. 
 
Thus, molecular methods unequivocally identified the larva as that of a T. martis tapeworm. T. martis tapeworms (cestodes) live and produce eggs in the intestines of definitive hosts, weasels (family Mustelidae), which also includes pine martens, stone martens, polecats, badgers, wolverines, and stoats (6). The intermediate hosts are prey animals of the definitive hosts, such as arvicoline (voles and muskrats) or murid rodents. When intermediate hosts ingest eggs, cysticerci develop in the pleural and peritoneal cavities. T. martis tapeworms probably occur worldwide wherever suitable definitive and intermediate hosts are present (6,7). A study in southwest Germany reported that 36% of stone martens were infected with T. martis tapeworms (6). 
 
Although nearly all patients who had cysticercosis-like infections caused by T. crassiceps tapeworms were immunosuppressed (1,2), we found no signs of immunosuppression in the patient reported here. The only identified risk factor for this patient was consumption of homegrown vegetables, which could have been contaminated by marten feces. 
 
The clinical and histologic appearance of the organism in this patient suggested cysticercosis caused by a T. solium tapeworm. However, the specific diagnosis of T. martis tapeworm infection was possible only by use of molecular methods. Thus, human infections with T. martis and other animal tapeworms might occur at times but might be misdiagnosed as T. solium cysticercosis. For therapy, the rules and considerations are probably the same as those for T. solium cysticercosis, as described (8,9). Concerning antiparasitic therapy, one must be aware of possible complications caused by intraocular immunologic reactions. As demonstrated by the case reported here, surgical removal of a subretinal larva is connected with the risk for retinal detachment and cataract formation. The identification of the responsible tapeworm is useful for epidemiologic reasons, for determining the source of infection. We therefore suggest using molecular methods to determine the exact species of parasites removed from human tissue.


Human Infection with Marten Tapeworm
To the Editor: Cysticercosis-like human infections with the tapeworm Taenia crassiceps, which infects foxes as terminal hosts, have been reported (1,2). We report a case of a cysticercosis-like eye infection caused by the tapeworm T. martis (marten tapeworm) in a woman.
The patient was a 43-year-old German woman who sought care during The patient reported no other symptoms at that time. Laboratory evaluation found no eosinophilia or elevation of total IgE. Serologic testing results were negative for antibodies against the following parasites: Taenia solium, Echinococcus multilocularis, E. granulosus, Dirofilaria immitis, Strongyloides spp., and Toxocara canis. Fecal testing results were negative for worm eggs. Images from ultrasonography of the liver and magnetic resonance imaging of the head were unremarkable. The patient's travel history included-in addition to southern European countries-trips to Nepal and Thailand 15 years previously.
At the time of examination, the patient lived in a small village near Freiburg (im Breisgau) in southwestern Germany. She grew vegetables in the family garden, which was next to a forest. Her 3 children and husband did not report any health problems. For the past 6 years, the family had owned Figure. Spoligotype and 24-loci MIRU-VNTR typing results for Mycobacterium tuberculosis complex isolates recovered from 3 patients with multidrug-resistant tuberculosis (TB). Patient A (index case-patient), Burma-born man with TB, incarcerated in Singapore correctional facility; patient B, Singapore-born man with HIV infection and TB, who transported prisoners in Singapore; patient C, Singapore-born man with HIV infection and TB, who shared cell with patient A. MIRU-VNTR, mycobacterial interspersed repetitive units-variable number tandem repeat.
All material published in Emerging Infectious Diseases is in the public domain and may be used and reprinted without special permission; proper citation, however, is required. a dog, which received antiparasitic medications on a regular basis; recent checks for intestinal parasitic infection found no ova.
The suspected cause of the woman's illness was cysticercosis caused by the larva of T. solium; systemic antiparasitic therapy was started (albendazole 400 mg 2×/d, dexamethasone 20 mg/d). The size of the larva diminished (Figure, panel D; Video), but the patient remained symptomatic. Therefore, after 8 days of therapy, the cyst was removed by retinotomy. A few days later, peripheral retinal detachment occurred and was treated by a second vitrectomy and intravitreal gas injection. Because of the repeated gas tamponade, a gas cataract developed, which necessitated cataract surgery. At the end of March 2011, the patient's visual acuity had returned to 20/20 in both eyes.
The removed cyst showed the characteristic macroscopic and histologic features of a cysticercus bladder wall ( Figure, panels E, F). To determine the exact species by using molecular methods, we isolated DNA from the cyst, conducted different PCRs selective for mitochondrial genes, determined the corresponding sequences, and used a BLAST search (3) to compare these sequences with publically available sequences. Sequences of the following mitochondrial genes were determined by using the given primers and later submitted to GenBank: small ribosomal subunit (primers 12S Taenia FF 5′-CACAGTGCCAGCAT-CYGCGGT-3′ and 12S Taenia RR 5′-GAGGGTGACGGGCGGTGT-GTAC-3′, PCR product of 426 bp, GenBank accession no. JX415820); NADH dehydrogenase subunit 1 (primers: NAD1-FF 5′-ATTGGKT-TATTTCAGAGTTTTTCTGATT-TA-3′ and NAD1-RR 5′-CTCMC-CATAATCAAATGGACTACG-3′, 394 bp, GenBank accession no. JX415819); and the cytochrome-c oxidase subunit 1 (determined by using previously published primers  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. [4,5]; 376 bp, GenBank accession no. JX415821). All sequences showed highest identity with T. martis (99%-100%) but substantially lower identity with T. crassiceps (91%-97%) and T. solium (87%-89%) tapeworms.
Thus, molecular methods unequivocally identified the larva as that of a T. martis tapeworm. T. martis tapeworms (cestodes) live and produce eggs in the intestines of definitive hosts, weasels (family Mustelidae), which also includes pine martens, stone martens, polecats, badgers, wolverines, and stoats (6). The intermediate hosts are prey animals of the definitive hosts, such as arvicoline (voles and muskrats) or murid rodents. When intermediate hosts ingest eggs, cysticerci develop in the pleural and peritoneal cavities. T. martis tapeworms probably occur worldwide wherever suitable definitive and intermediate hosts are present (6,7). A study in southwest Germany reported that 36% of stone martens were infected with T. martis tapeworms (6).
Although nearly all patients who had cysticercosis-like infections caused by T. crassiceps tapeworms were immunosuppressed (1,2), we found no signs of immunosuppression in the patient reported here. The only identified risk factor for this patient was consumption of homegrown vegetables, which could have been contaminated by marten feces.
The clinical and histologic appearance of the organism in this patient suggested cysticercosis caused by a T. solium tapeworm. However, the specific diagnosis of T. martis tapeworm infection was possible only by use of molecular methods. Thus, human infections with T. martis and other animal tapeworms might occur at times but might be misdiagnosed as T. solium cysticercosis. For therapy, the rules and considerations are probably the same as those for T. solium cysticercosis, as described (8,9). Concerning antiparasitic therapy, one must be aware of possible complications caused by intraocular immunologic reactions. As demonstrated by the case reported here, surgical removal of a subretinal larva is connected with the risk for retinal detachment and cataract formation. The identification of the responsible tapeworm is useful for epidemiologic reasons, for determining the source of infection. We therefore suggest using molecular methods to determine the exact species of parasites removed from human tissue.

Letters
Letters commenting on recent articles as well as letters reporting cases, outbreaks, or original research are welcome. Letters commenting on articles should contain no more than 300 words and 5 references; they are more likely to be published if submitted within 4 weeks of the original article's publication. Letters reporting cases, outbreaks, or original research should contain no more than 800 words and 10 references. They may have 1 Figure or Table and should not be divided into sections. All letters should contain material not previously published and include a word count.