• View in gallery

    Cytology of the peritoneal fluid from the pouch of Douglas showing multiple eosinophils. Papanicolaou stain, original magnification ×40.

  • View in gallery

    Histological section through the cystic tapeworm larva recovered from the patient’s peritoneum. The parasite’s spongy tissue is surrounded by a ruffled tegument. In the center, a sucker is visible and three hooklets. Hematoxylin and eosin stain, original magnification ×6.3.

  • View in gallery

    Histological detail of the metacestode’s tegument. Underneath the tegument, a thin layer of muscle fibers is found. Hematoxylin and eosin stain, original magnification ×25.

  • 1.

    Tappe D, Frosch M, Sako Y, Itoh S, Grüner B, Reuter S, Nakao M, Ito A, Kern P, 2009. Close relationship between clinical regression and specific serology in the follow-up of patients with alveolar echinococcosis in different clinical stages. Am J Trop Med Hyg 80: 792797.

    • Search Google Scholar
    • Export Citation
  • 2.

    Koch T, Schoen C, Muntau B, Addo M, Ostertag H, Wiechens B, Tappe D, 2016. Molecular diagnosis of human Taenia martis eye infection. Am J Trop Med Hyg 94: 10551057.

    • Search Google Scholar
    • Export Citation
  • 3.

    Tappe D, Berkholz J, Mahlke U, Lobeck H, Nagel T, Haeupler A, Muntau B, Racz P, Poppert S, 2016. Molecular identification of zoonotic tissue-invasive tapeworm larvae other than Taenia solium in suspected human cysticercosis cases. J Clin Microbiol 54: 172174.

    • Search Google Scholar
    • Export Citation
  • 4.

    Deplazes P, Eichenberger RM, Grimm F, 2019. Wildlife-transmitted Taenia and Versteria cysticercosis and coenurosis in humans and other primates. Int J Parasitol Parasites Wildl 9: 342358.

    • Search Google Scholar
    • Export Citation
  • 5.

    Eberwein P, Haeupler A, Kuepper F, Wagner D, Kern WV, Muntau B, Racz P, Agostini H, Poppert S, 2013. Human infection with marten tapeworm. Emerg Infect Dis 19: 11521154.

    • Search Google Scholar
    • Export Citation
  • 6.

    Rudelius M, Brehm K, Poelcher M, Spinner C, Rosenwald A, da Costa CP, 2017. First case of human peritoneal cysticercosis mimicking peritoneal carcinosis: necessity of laparoscopy and histologic assessment for the correct diagnosis. JMM Case Rep 4: e005097.

    • Search Google Scholar
    • Export Citation
  • 7.

    Brunet J et al. 2015. First case of human cerebral Taenia martis cysticercosis. J Clin Microbiol 53: 27562759.

  • 8.

    Ntoukas V, Tappe D, Pfütze D, Simon M, Holzmann T, 2013. Cerebellar cysticercosis caused by larval Taenia crassiceps tapeworm in immunocompetent woman, Germany. Emerg Infect Dis 19: 20082211.

    • Search Google Scholar
    • Export Citation
  • 9.

    Romig T, Kratzer W, Kimmig P, 1999. An epidemiological survey of human alveolar echinococcosis in southwestern Germany. Am J Trop Med Hyg 61: 566573.

    • Search Google Scholar
    • Export Citation
  • 10.

    Jensen B, Reuter S, Kratzer W, Naser K, Kaechele V, Kimmig P, Kern P, 2001. Long-term seropositivity against Echinococcus multilocularis in an epidemiological follow-up study in southwestern Germany (Römerstein). Infection 29: 310314.

    • Search Google Scholar
    • Export Citation
  • 11.

    Loos-Frank B, Zeyhle E, 1982. The intestinal helminths of the red fox and some other carnivores in southwest Germany. Z Parasitenkd 67: 99113.

    • Search Google Scholar
    • Export Citation
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

 

 

 

Case Report: Molecular Identification of Larval Taenia martis Infection in the Pouch of Douglas

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  • 1 Department of Tropical Medicine, Klinikum Würzburg Mitte gGmbH, Würzburg, Germany;
  • | 2 General Practioner, Wörth, Germany;
  • | 3 Gemeinschaftspraxis für Pathologie, Regensburg, Germany;
  • | 4 National Reference Center for Tropical Pathogens, Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany

ABSTRACT

Taenia martis is a tapeworm dwelling in the intestine of mustelids and a rare zoonotic cysticercosis pathogen in its larval stage. The metacestode is morphologically very similar to more prevalent cysticercosis parasites, such as the larvae of Taenia solium and Taenia crassiceps, and may be indistinguishable from other metacestodes on histological sections. However, the epidemiology of human T. martis infections is different, and for prognosis, prevention, and detection of natural parasite reservoirs, the species should be identified. We here report the molecular identification of a T. martis larva located in the pouch of Douglas in a female German patient who underwent surgery for endometriosis. This case represents the fifth human infection described worldwide; all previous cases were also in European women, involving the eye, brain, and the peritoneum.

CASE REPORT

A 24-year-old female patient from southern Germany presented to her gynecologist with chronic lower abdominal pain and dysmenorrhea suggestive of endometriosis in October 2019. There were no medical preconditions. Apart from vacation trips to Italy, Austria, Croatia, Greece, and Spain there was no history of travel. The gynecological examination as well as routine laboratory parameters was unremarkable. Ultrasound showed a small amount of free fluid in the pouch of Douglas. She underwent diagnostic endoscopic laparoscopy showing multiple lesions suggestive of extensive endometriosis. For confirmation, biopsies from several foci were taken. The excised tissue specimens were fixed in formalin and routinely processed for histology. One of the specimens revealed structures suggestive of a parasitic infection, and the others were multiple endometriosis foci. Peritoneal lavage fluid showed a marked eosinophilia (Figure 1). Serological tests performed in two specialized laboratories showed positive screening tests for echinococcosis with Echinococcus multilocularis crude larval antigen extract ELISAs1 (index of 1.5, cutoff < 1.0; and 100 arbitrary units, cutoff < 10), but negative results with Echinococcus granulosus crude hydatid fluid antigen indirect hemagglutination assays (Fumouze, Levallois-Perret, France). Echinococcosis confirmatory assays (E. granulosus antigen B-ELISA, E. multilocularis EM10-ELISA,1 Em2plus-ELISA [Bordier Affinity Products, Crissier, Switzerland], and Echinococcus IgG Western blot [LDBIO Diagnostics, Lyon, France]) were negative. Taenia solium IgG ELISA (IBL International, Hamburg, Germany) was positive (41 arbitrary units, cutoff < 9), whereas the cysticercosis immunoblot (LDBIO Diagnostics) showed a borderline result with the presence of one 6–8 kDa band. In addition, an in-house Dirofilaria immitis crude adult antigen extract ELISA showed a weak positive result (16 arbitrary units, cutoff < 10). Because of the inconclusive serological findings, the patient was referred for further evaluation.

Figure 1.
Figure 1.

Cytology of the peritoneal fluid from the pouch of Douglas showing multiple eosinophils. Papanicolaou stain, original magnification ×40.

Citation: The American Journal of Tropical Medicine and Hygiene 103, 6; 10.4269/ajtmh.20-0782

Reassessment of the tissue sections showed a tegument, calcareous bodies, hooklets, and suckers characteristic for a larval tapeworm (Figures 2 and 3), and peritoneal cysticercosis was diagnosed. PCR targeting cestode cytochrome c oxidase subunit one gene2 was positive. Sequencing and BLAST analysis (www.ncbi.nlm.nih.gov/blast) of the 429-bp amplicon revealed 100% nucleotide similarity with the marten tapeworm Taenia martis. The highest sequence similarities were found with T. martis isolates from the human brain in France (100%; GenBank accession no. KP198618), from a marten in Italy (100%; GenBank no. FN547885), followed by isolates from a ring-tailed lemur living in an Italian zoological garden (99.8%; GenBank no. KJ459910), and from Myodes glareolus rodents from Denmark (99.8%; GenBank no. EU544553). Peritoneal cysticercosis of the pouch of Douglas with the larval stage of T. martis was diagnosed.

Figure 2.
Figure 2.

Histological section through the cystic tapeworm larva recovered from the patient’s peritoneum. The parasite’s spongy tissue is surrounded by a ruffled tegument. In the center, a sucker is visible and three hooklets. Hematoxylin and eosin stain, original magnification ×6.3.

Citation: The American Journal of Tropical Medicine and Hygiene 103, 6; 10.4269/ajtmh.20-0782

Figure 3.
Figure 3.

Histological detail of the metacestode’s tegument. Underneath the tegument, a thin layer of muscle fibers is found. Hematoxylin and eosin stain, original magnification ×25.

Citation: The American Journal of Tropical Medicine and Hygiene 103, 6; 10.4269/ajtmh.20-0782

After diagnostic laparoscopy had confirmed endometriosis as the cause of the lower abdominal pain, a therapeutic laparoscopy followed with resection of all endometriosis foci. No additional parasitic lesions were found in the resected tissue. On follow-up, the patient was asymptomatic. Because of the diagnosis of cysticercosis, cranial magnetic resonance imaging (cMRI) and ophthalmological examinations were performed, which were normal. Anthelminthic treatment with albendazole was offered but refused because of the desire to become pregnant.

The patient, a final year teacher trainee, grew up and still lives in a small town in the east of the city of Regensburg in Bavaria, Germany. The patient used to eat unwashed strawberries from the garden of her aunt who lives nearby. Her aunt also grew vegetables and lettuce that she shared with the patient’s family. The patient used to pet her aunt’s dog but never owned a dog herself. For the past 3 years, the patient had a free-roaming cat. Deworming was performed once or twice per year. Martens have frequently been observed on the premises, leaving feces and causing significant damage to cars. The patient had never removed marten feces herself.

DISCUSSION

With the more widespread application of molecular diagnostic tests, more unusual zoonotic larval tapeworm infections are continuously detected.2,3 Accordingly, the detection of previous larval T. martis infections in humans was already attributed to these new molecular diagnostic strategies and probably does not represent an emergence of this zoonotic disease.4 In this report, we describe the fifth human infection worldwide with larval T. martis. All other human cases were also diagnosed molecularly and also occurred among European patients—three cases from Germany (two from the south5,6 and one from the north)2 and one case from eastern France.7 Adult marten tapeworms dwell in the intestine of mustelids (martens, badgers, and weasels) as definitive hosts and infective tapeworm eggs are released into the environment by host feces. The ingestion of tapeworm ova by intermediate hosts (voles, muskrats, and other rodents as natural hosts, and humans as accidental, dead-end intermediate hosts) is followed by hatching of oncospheres in the intestine and subsequent dissemination by the bloodstream. Eventually, the oncospheres develop into cysticerci in pleural and peritoneal cavities in the natural intermediate hosts. The cysticercus reaches a size of 6–32 mm.4

In humans, two eye infections with larval T. martis were reported2,3 and one cerebral cysticercosis case.7 Only recently, in 2017, one strikingly similar peritoneal infection of the pouch of Douglas with a T. martis larva was described.6 In contrast to human zoonotic Taenia crassiceps cysticercosis in which immunosuppression was seen in most of the patients with skin and muscle infection,8 none of the patients with T. martis cysticercosis exhibited signs of immunosuppression. So far, all five human T. martis cysticercosis cases were seen in women (aged 24, 36, 43, 44, and 70 years). Whether there is a gender association4 can be speculated when more cases emerge. In all cases, a single parasite was found, but an extensive MRI or computed tomography screening for additional lesions was apparently not performed in all patients. All four previous human T. martis cysticercosis cases were successfully managed with surgery and antiparasitic chemotherapy using albendazole (plus praziquantel in the cerebral case). The indication for antiparasitic treatment was intensively discussed with our patient but considered to be not compulsory based on the previous cases with singular lesions; because of the desire to become pregnant, the patient refused anthelminthic treatment with albendazole.

Of note, serological investigations showed cross-reactive antibodies to E. multilocularis and T. solium in our case of a peritoneal infection; in the previous peritoneal infection reported from Germany,6 cross-reactions to E. granulosus in an ELISA were described. In the cerebral infection,7 serology was weakly positive with T. solium antigens and immunofluorescence, but negative with Taenia saginata antigens, Echinococcus sp. by immunoblot, and E. multilocularis by Em2plus-ELISA. No serological cross-reactions for E. granulosus and E. multilocularis (crude antigen ELISAs), and T. solium (immunoblot) were seen in the eye infections.2,5 Apparently, when T. martis larvae are found in special anatomical compartments, such as the eye where immunological surveillance is naturally low, serological reactions are undetectable—at least when antigens of related parasites are used. By contrast, severe inflammation was seen in our case and a previously reported infection6 in the peritoneum. The main reason for referral of our patient was the fear of an E. multilocularis infection (alveolar echinococcosis). To which extent inapparent or abortive zoonotic cysticercosis cases contribute to positive serological echinococcosis screening assays remains open. Southern Germany is considered highly endemic for alveolar echinococcosis.9 In a seroepidemiological survey carried out in 1996 among 2,560 participants, 47 (1.8%) had a positive result in one of two crude antigen screening ELISAs but an unremarkable hepatic ultrasound.10 Of the study population, 13 showed a positive result in more specific E. multilocularis serological tests, but only one had a proven infection and three cases had suspicious liver lesions. Despite a comparably low incidence in the whole of Germany, alveolar echinococcosis is feared for its progressive larval growth and limited treatment options. Thus, as different larval tapeworm species have different epidemiological backgrounds and disease prognoses, molecular parasite species identification should be attempted.3

Stone martens are considered a synanthropic species and are commonly seen in the close vicinity of human dwellings. Fecal contamination of gardens and vegetable beds may not be unusual. A survey for helminth infections in carnivores in southern Germany demonstrated that 36% of the stone martens were infected with T. martis.11 It can be anticipated that human infections are due to ingestion of uncooked food, for example, vegetables or lettuce, contaminated with infective parasite ova from marten feces. Considering the abundance of martens around human dwellings and the high rates of martens infected with T. martis, inapparent or abortive human infections could be much more prevalent than reported. As a general preventive measure, thorough handwashing, careful cleaning of fruits and raw vegetables before consumption, and proper disposal of animal feces are strongly advisable, especially in areas with high marten populations.

REFERENCES

  • 1.

    Tappe D, Frosch M, Sako Y, Itoh S, Grüner B, Reuter S, Nakao M, Ito A, Kern P, 2009. Close relationship between clinical regression and specific serology in the follow-up of patients with alveolar echinococcosis in different clinical stages. Am J Trop Med Hyg 80: 792797.

    • Search Google Scholar
    • Export Citation
  • 2.

    Koch T, Schoen C, Muntau B, Addo M, Ostertag H, Wiechens B, Tappe D, 2016. Molecular diagnosis of human Taenia martis eye infection. Am J Trop Med Hyg 94: 10551057.

    • Search Google Scholar
    • Export Citation
  • 3.

    Tappe D, Berkholz J, Mahlke U, Lobeck H, Nagel T, Haeupler A, Muntau B, Racz P, Poppert S, 2016. Molecular identification of zoonotic tissue-invasive tapeworm larvae other than Taenia solium in suspected human cysticercosis cases. J Clin Microbiol 54: 172174.

    • Search Google Scholar
    • Export Citation
  • 4.

    Deplazes P, Eichenberger RM, Grimm F, 2019. Wildlife-transmitted Taenia and Versteria cysticercosis and coenurosis in humans and other primates. Int J Parasitol Parasites Wildl 9: 342358.

    • Search Google Scholar
    • Export Citation
  • 5.

    Eberwein P, Haeupler A, Kuepper F, Wagner D, Kern WV, Muntau B, Racz P, Agostini H, Poppert S, 2013. Human infection with marten tapeworm. Emerg Infect Dis 19: 11521154.

    • Search Google Scholar
    • Export Citation
  • 6.

    Rudelius M, Brehm K, Poelcher M, Spinner C, Rosenwald A, da Costa CP, 2017. First case of human peritoneal cysticercosis mimicking peritoneal carcinosis: necessity of laparoscopy and histologic assessment for the correct diagnosis. JMM Case Rep 4: e005097.

    • Search Google Scholar
    • Export Citation
  • 7.

    Brunet J et al. 2015. First case of human cerebral Taenia martis cysticercosis. J Clin Microbiol 53: 27562759.

  • 8.

    Ntoukas V, Tappe D, Pfütze D, Simon M, Holzmann T, 2013. Cerebellar cysticercosis caused by larval Taenia crassiceps tapeworm in immunocompetent woman, Germany. Emerg Infect Dis 19: 20082211.

    • Search Google Scholar
    • Export Citation
  • 9.

    Romig T, Kratzer W, Kimmig P, 1999. An epidemiological survey of human alveolar echinococcosis in southwestern Germany. Am J Trop Med Hyg 61: 566573.

    • Search Google Scholar
    • Export Citation
  • 10.

    Jensen B, Reuter S, Kratzer W, Naser K, Kaechele V, Kimmig P, Kern P, 2001. Long-term seropositivity against Echinococcus multilocularis in an epidemiological follow-up study in southwestern Germany (Römerstein). Infection 29: 310314.

    • Search Google Scholar
    • Export Citation
  • 11.

    Loos-Frank B, Zeyhle E, 1982. The intestinal helminths of the red fox and some other carnivores in southwest Germany. Z Parasitenkd 67: 99113.

    • Search Google Scholar
    • Export Citation

Author Notes

Address correspondence to Dennis Tappe, Bernhard Nocht Institute for Tropical Medicine, Bernhard-Nocht-St. 74, Hamburg 20359, Germany. E-mail: tappe@bnitm.de

Authors’ addresses: Andreas Mueller, Department of Tropical Medicine, Klinikum Würzburg Mitte gGmbH, Würzburg, Germany, E-mail: andreas.mueller@kwm-klinikum.de. Gerhard Förch, General Practioner, Wörth, Germany, E-mail: info@hausarztpraxis-woerth.de. Jozef Zustin, Gemeinschaftspraxis für Pathologie, Regensburg, Germany, E-mail: jozefzustin@t-online.de. Birgit Muntau, Gerlind Schuldt, and Dennis Tappe, National Reference Center for Tropical Pathogens, Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany, E-mails: muntau@bnitm.de, gerlind.schuldt@bnitm.de, and tappe@bnitm.de.

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