Chronic Plasmodium brasilianum infections in wild Peruvian tamarins

PLoS One. 2017 Sep 13;12(9):e0184504. doi: 10.1371/journal.pone.0184504. eCollection 2017.

Abstract

There is an increased interest in potential zoonotic malarias. To date, Plasmodium malariae that infects humans remains indistinguishable from Plasmodium brasilianum, which is widespread among New World primates. Distributed throughout tropical Central and South America, the Callitrichidae are small arboreal primates in which detection of natural Plasmodium infection has been extremely rare. Most prior screening efforts have been limited to small samples, the use of low-probability detection methods, or both. Rarely have screening efforts implemented a longitudinal sampling design. Through an annual mark-recapture program of two sympatric callitrichids, the emperor (Saguinus imperator) and saddleback (Saguinus fuscicollis) tamarins, whole blood samples were screened for Plasmodium by microscopy and nested PCR of the cytochrome b gene across four consecutive years (2012-2015). Following the first field season, approximately 50% of the samples collected each subsequent year were from recaptured individuals. In particular, out of 245 samples from 129 individuals, 11 samples from 6 individuals were positive for Plasmodium, and all but one of these infections was found in S. imperator. Importantly, the cytochrome b sequences were 100% identical to former isolates of P. malariae from humans and P. brasilianum from Saimiri sp. Chronic infections were detected as evidenced by repeated infections (7) from two individuals across the 4-year study period. Furthermore, 4 of the 5 infected emperor tamarins were part of a single group spanning the entire study period. Overall, the low prevalence reported here is consistent with previous findings. This study identifies two new natural hosts for P. brasilianum and provides evidence in support of chronic infections in wildlife populations. Given that callitrichids are often found in mixed-species associations with other primates and can be resilient to human-disturbed environments, they could contribute to the maintenance of P. malariae populations if future work provides entomological and epidemiological evidence indicating human zoonotic infections.

MeSH terms

  • Animals
  • Animals, Wild
  • Chronic Disease
  • DNA, Protozoan / genetics
  • Female
  • Incidence
  • Malaria / epidemiology*
  • Malaria / parasitology
  • Malaria / veterinary*
  • Male
  • Monkey Diseases / epidemiology*
  • Monkey Diseases / parasitology
  • Peru / epidemiology
  • Phylogeny
  • Plasmodium / genetics
  • Plasmodium / isolation & purification
  • Polymerase Chain Reaction / veterinary
  • Saguinus / parasitology*
  • Sequence Analysis, DNA

Substances

  • DNA, Protozoan

Grants and funding

Funding for this work was provided by Field Projects International (www.fieldprojects.org), the American Society of Mammologists (www.mammalsociety.org), Sigma Xi Society (www.sigmaxi.org), The University of Missouri Trans World Airlines Scholarship Program, Whitney R. Harris World Ecology Center (www.umsl.edu/~hwec/), and The Des Lee Collaborative Vision at the University of Missouri-St. Louis. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.