India Schneider-Crease 1 , * , Randi H. Griffin 1 , Megan A. Gomery 2 , Pierre Dorny 3 , 4 , John C. Noh 5 , Sukwan Handali 5 , Holly M. Chastain 5 , Patricia P. Wilkins 5 , Charles L. Nunn 1 , 6 , Noah Snyder-Mackler 1 , Jacinta C. Beehner 2 , 7 , Thore J. Bergman 7 , 8
13 July 2017
Despite the global distribution and public health consequences of Taenia tapeworms, the life cycles of taeniids infecting wildlife hosts remain largely undescribed. The larval stage of Taenia serialis commonly parasitizes rodents and lagomorphs, but has been reported in a wide range of hosts that includes geladas ( Theropithecus gelada), primates endemic to Ethiopia. Geladas exhibit protuberant larval cysts indicative of advanced T. serialis infection that are associated with high mortality. However, non-protuberant larvae can develop in deep tissue or the abdominal cavity, leading to underestimates of prevalence based solely on observable cysts. We adapted a non-invasive monoclonal antibody-based enzyme-linked immunosorbent assay (ELISA) to detect circulating Taenia spp. antigen in dried gelada urine. Analysis revealed that this assay was highly accurate in detecting Taenia antigen, with 98.4% specificity, 98.5% sensitivity, and an area under the curve of 0.99. We used this assay to investigate the prevalence of T. serialis infection in a wild gelada population, finding that infection is substantially more widespread than the occurrence of visible T. serialis cysts (16.4% tested positive at least once, while only 6% of the same population exhibited cysts). We examined whether age or sex predicted T. serialis infection as indicated by external cysts and antigen presence. Contrary to the female-bias observed in many Taenia-host systems, we found no significant sex bias in either cyst presence or antigen presence. Age, on the other hand, predicted cyst presence (older individuals were more likely to show cysts) but not antigen presence. We interpret this finding to indicate that T. serialis may infect individuals early in life but only result in visible disease later in life. This is the first application of an antigen ELISA to the study of larval Taenia infection in wildlife, opening the doors to the identification and description of infection dynamics in reservoir populations.
Although tapeworm parasites of the genus Taenia are globally distributed and inflict enormous socioeconomic and health costs on their hosts, which include humans, little is known about taeniid tapeworms that infect wildlife. This gap in knowledge prevents an assessment of the potential for these parasites to infect humans and production animals and is largely due to the difficulty of conducting standard diagnostic tests on wildlife. To address this gap, we adapted a standard diagnostic assay to be used with dried urine samples. We used urine from geladas, primates endemic to Ethiopia, which are frequently infected with the larval stage of a taeniid tapeworm and exhibit protuberant cysts during advanced infection. The use of this diagnostic test in a wild gelada population allowed us to detect that individuals can be infected without exhibiting observable cysts, and that some individuals may control infection in its early stages. This tool provides information about how a neglected tapeworm functions in a wildlife system and opens the door to the non-invasive identification of tapeworm reservoir hosts that may threaten humans.