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      Identifying wildlife reservoirs of neglected taeniid tapeworms: Non-invasive diagnosis of endemic Taenia serialis infection in a wild primate population

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          Abstract

          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.

          Author summary

          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.

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          Most cited references 88

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          Principles and practical application of the receiver-operating characteristic analysis for diagnostic tests.

          We review the principles and practical application of receiver-operating characteristic (ROC) analysis for diagnostic tests. ROC analysis can be used for diagnostic tests with outcomes measured on ordinal, interval or ratio scales. The dependence of the diagnostic sensitivity and specificity on the selected cut-off value must be considered for a full test evaluation and for test comparison. All possible combinations of sensitivity and specificity that can be achieved by changing the test's cut-off value can be summarised using a single parameter; the area under the ROC curve. The ROC technique can also be used to optimise cut-off values with regard to a given prevalence in the target population and cost ratio of false-positive and false-negative results. However, plots of optimisation parameters against the selected cut-off value provide a more-direct method for cut-off selection. Candidates for such optimisation parameters are linear combinations of sensitivity and specificity (with weights selected to reflect the decision-making situation), odds ratio, chance-corrected measures of association (e. g. kappa) and likelihood ratios. We discuss some recent developments in ROC analysis, including meta-analysis of diagnostic tests, correlated ROC curves (paired-sample design) and chance- and prevalence-corrected ROC curves.
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            Complete mitochondrial genomes of Taenia multiceps, T. hydatigena and T. pisiformis: additional molecular markers for a tapeworm genus of human and animal health significance

            Background Mitochondrial genomes provide a rich source of molecular variation of proven and widespread utility in molecular ecology, population genetics and evolutionary biology. The tapeworm genus Taenia includes a diversity of tapeworm parasites of significant human and veterinary importance. Here we add complete sequences of the mt genomes of T. multiceps, T. hydatigena and T. pisiformis, to a data set of 4 published mtDNAs in the same genus. Seven complete mt genomes of Taenia species are used to compare and contrast variation within and between genomes in the genus, to estimate a phylogeny for the genus, and to develop novel molecular markers as part of an extended mitochondrial toolkit. Results The complete circular mtDNAs of T. multiceps, T. hydatigena and T. pisiformis were 13,693, 13,492 and 13,387 bp in size respectively, comprising the usual complement of flatworm genes. Start and stop codons of protein coding genes included those found commonly amongst other platyhelminth mt genomes, but the much rarer initiation codon GTT was inferred for the gene atp6 in T. pisiformis. Phylogenetic analysis of mtDNAs offered novel estimates of the interrelationships of Taenia. Sliding window analyses showed nad6, nad5, atp6, nad3 and nad2 are amongst the most variable of genes per unit length, with the highest peaks in nucleotide diversity found in nad5. New primer pairs capable of amplifying fragments of variable DNA in nad1, rrnS and nad5 genes were designed in silico and tested as possible alternatives to existing mitochondrial markers for Taenia. Conclusions With the availability of complete mtDNAs of 7 Taenia species, we have shown that analysis of amino acids provides a robust estimate of phylogeny for the genus that differs markedly from morphological estimates or those using partial genes; with implications for understanding the evolutionary radiation of important Taenia. Full alignment of the nucleotides of Taenia mtDNAs and sliding window analysis suggests numerous alternative gene regions are likely to capture greater nucleotide variation than those currently pursued as molecular markers. New PCR primers developed from a comparative mitogenomic analysis of Taenia species, extend the use of mitochondrial markers for molecular ecology, population genetics and diagnostics.
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              Sero-epidemiological study of Taenia saginata cysticercosis in Belgian cattle.

              A sero-epidemiological survey of Taenia saginata cysticercosis was carried out to determine the prevalence of the infection in cattle presented for slaughter in Belgium. Between November 1997 and June 1998, a total of 1164 serum samples were collected in 20 export abattoirs. Meat inspection was routinely carried out by veterinary inspectors. Serum samples were examined for circulating parasite antigen using a monoclonal antibody-based sandwich enzyme-linked-immunosorbent assay (Ag-ELISA). Thirty six serum samples (3.09%) were found positive in the Ag-ELISA, while by meat inspection on the same animals cysticerci were detected in only three carcasses (0.26%). Sero-prevalence was positively correlated with the age of the animals. The sero-prevalence found in this study was more than 10 times higher than the annual prevalence (0.26%) reported by the Institute for Veterinary Inspection. This study clearly indicates that the classical meat inspection techniques detect only a minor fraction of the carcasses infected with cysticerci.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: SoftwareRole: VisualizationRole: Writing – review & editing
                Role: InvestigationRole: Methodology
                Role: InvestigationRole: MethodologyRole: ResourcesRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: InvestigationRole: Methodology
                Role: InvestigationRole: Methodology
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: VisualizationRole: Writing – review & editing
                Role: Funding acquisitionRole: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: Funding acquisitionRole: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                13 July 2017
                July 2017
                : 11
                : 7
                Affiliations
                [1 ] Department of Evolutionary Anthropology, Duke University, Durham, North Carolina, United States of America
                [2 ] Department of Anthropology, University of Michigan, Ann Arbor, Michigan, United States of America
                [3 ] Department of Veterinary Medicine, Prince Leopold Institute of Tropical Medicine, Nationalestraat 155, Antwerp, Belgium
                [4 ] Department of Parasitology, Faculty of Veterinary Medicine, Salisburylaan 133, Merelbeke, Belgium
                [5 ] Department of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America
                [6 ] Duke Global Health Institute, Duke University, Durham, North Carolina, United States of America
                [7 ] Department of Psychology, University of Michigan, Ann Arbor, Michigan, United States of America
                [8 ] Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, United States of America
                University of Cambridge, UNITED KINGDOM
                Author notes

                The authors have declared that no competing interests exist.

                Article
                PNTD-D-17-00393
                10.1371/journal.pntd.0005709
                5526605
                28704366

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                Page count
                Figures: 3, Tables: 4, Pages: 18
                Product
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: IOS-1255974
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: BCS-0715179
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100006363, National Geographic Society;
                Award ID: 8989-11
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100006363, National Geographic Society;
                Award ID: 8100-06
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100003282, Primate Conservation;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100008647, Conservation International;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100009687, Nacey Maggioncalda Foundation;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100007134, Margot Marsh Biodiversity Foundation;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100005966, Leakey Foundation;
                Award Recipient :
                Long-term gelada research was supported by: the National Science Foundation (IOS-1255974, awarded to JCB, and BCS-0715179, awarded to TJB, https://www.nsf.gov), the Leakey Foundation ( https://leakeyfoundation.org, awarded to JCB), and the National Geographic Society (Gr. #8989-11, Gr. #8100-06, http://www.nationalgeographic.com, awarded to JCB). Support for project-specific fieldwork and laboratory analysis was provided by Primate Conservation, Inc. ( http://www.primate.org, awarded to ISC), Conservation International ( http://www.conservation.org, awarded to ISC), the Nacey Maggioncalda Foundation ( http://naceymagg.org, awarded to ISC), the Margot Marsh Biodiversity Foundation (awarded to ISC). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Anatomy
                Body Fluids
                Urine
                Medicine and Health Sciences
                Anatomy
                Body Fluids
                Urine
                Biology and Life Sciences
                Physiology
                Body Fluids
                Urine
                Medicine and Health Sciences
                Physiology
                Body Fluids
                Urine
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogenesis
                Host-Pathogen Interactions
                Medicine and Health Sciences
                Parasitic Diseases
                Research and Analysis Methods
                Immunologic Techniques
                Immunoassays
                Enzyme-Linked Immunoassays
                Biology and Life Sciences
                Organisms
                Animals
                Animal Types
                Wildlife
                Biology and Life Sciences
                Zoology
                Animal Types
                Wildlife
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Primates
                Medicine and Health Sciences
                Infectious Diseases
                Zoonoses
                Biology and Life Sciences
                Veterinary Science
                Veterinary Medicine
                Veterinary Diagnostics
                Custom metadata
                vor-update-to-uncorrected-proof
                2017-07-25
                Data and R source code are available on GitHub ( https://github.com/rgriff23/Gelada_parasites_elisa).

                Infectious disease & Microbiology

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