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

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.
PMID
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Authors

Mayor MeshTerms

Endemic Diseases

Keywords
Journal Title plos neglected tropical diseases
Publication Year Start




PMID- 28704366
OWN - NLM
STAT- MEDLINE
DA  - 20170713
DCOM- 20170731
LR  - 20170731
IS  - 1935-2735 (Electronic)
IS  - 1935-2727 (Linking)
VI  - 11
IP  - 7
DP  - 2017 Jul
TI  - Identifying wildlife reservoirs of neglected taeniid tapeworms: Non-invasive
      diagnosis of endemic Taenia serialis infection in a wild primate population.
PG  - e0005709
LID - 10.1371/journal.pntd.0005709 [doi]
AB  - 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.
FAU - Schneider-Crease, India
AU  - Schneider-Crease I
AUID- ORCID: http://orcid.org/0000-0002-2699-5304
AD  - Department of Evolutionary Anthropology, Duke University, Durham, North Carolina,
      United States of America.
FAU - Griffin, Randi H
AU  - Griffin RH
AD  - Department of Evolutionary Anthropology, Duke University, Durham, North Carolina,
      United States of America.
FAU - Gomery, Megan A
AU  - Gomery MA
AD  - Department of Anthropology, University of Michigan, Ann Arbor, Michigan, United
      States of America.
FAU - Dorny, Pierre
AU  - Dorny P
AD  - Department of Veterinary Medicine, Prince Leopold Institute of Tropical Medicine,
      Nationalestraat 155, Antwerp, Belgium.
AD  - Department of Parasitology, Faculty of Veterinary Medicine, Salisburylaan 133,
      Merelbeke, Belgium.
FAU - Noh, John C
AU  - Noh JC
AD  - Department of Parasitic Diseases and Malaria, Centers for Disease Control and
      Prevention, Atlanta, Georgia, United States of America.
FAU - Handali, Sukwan
AU  - Handali S
AD  - Department of Parasitic Diseases and Malaria, Centers for Disease Control and
      Prevention, Atlanta, Georgia, United States of America.
FAU - Chastain, Holly M
AU  - Chastain HM
AD  - Department of Parasitic Diseases and Malaria, Centers for Disease Control and
      Prevention, Atlanta, Georgia, United States of America.
FAU - Wilkins, Patricia P
AU  - Wilkins PP
AD  - Department of Parasitic Diseases and Malaria, Centers for Disease Control and
      Prevention, Atlanta, Georgia, United States of America.
FAU - Nunn, Charles L
AU  - Nunn CL
AD  - Department of Evolutionary Anthropology, Duke University, Durham, North Carolina,
      United States of America.
AD  - Duke Global Health Institute, Duke University, Durham, North Carolina, United
      States of America.
FAU - Snyder-Mackler, Noah
AU  - Snyder-Mackler N
AD  - Department of Evolutionary Anthropology, Duke University, Durham, North Carolina,
      United States of America.
FAU - Beehner, Jacinta C
AU  - Beehner JC
AD  - Department of Anthropology, University of Michigan, Ann Arbor, Michigan, United
      States of America.
AD  - Department of Psychology, University of Michigan, Ann Arbor, Michigan, United
      States of America.
FAU - Bergman, Thore J
AU  - Bergman TJ
AD  - Department of Psychology, University of Michigan, Ann Arbor, Michigan, United
      States of America.
AD  - Department of Ecology and Evolutionary Biology, University of Michigan, Ann
      Arbor, Michigan, United States of America.
LA  - eng
PT  - Journal Article
DEP - 20170713
PL  - United States
TA  - PLoS Negl Trop Dis
JT  - PLoS neglected tropical diseases
JID - 101291488
RN  - 0 (Antigens, Helminth)
SB  - IM
MH  - Animals
MH  - Antigens, Helminth/urine
MH  - *Endemic Diseases
MH  - Enzyme-Linked Immunosorbent Assay/*methods
MH  - Ethiopia/epidemiology
MH  - Female
MH  - Male
MH  - Prevalence
MH  - Primate Diseases/*diagnosis/*epidemiology
MH  - ROC Curve
MH  - Sensitivity and Specificity
MH  - Taenia/*isolation & purification
MH  - Taeniasis/diagnosis/epidemiology/*veterinary
MH  - Theropithecus/parasitology
MH  - Urine/*parasitology
EDAT- 2017/07/14 06:00
MHDA- 2017/08/02 06:00
CRDT- 2017/07/14 06:00
PHST- 2017/04/07 [received]
PHST- 2017/06/12 [accepted]
PHST- 2017/07/25 [revised]
AID - 10.1371/journal.pntd.0005709 [doi]
AID - PNTD-D-17-00393 [pii]
PST - epublish
SO  - PLoS Negl Trop Dis. 2017 Jul 13;11(7):e0005709. doi:
      10.1371/journal.pntd.0005709. eCollection 2017 Jul.