An oral bait vaccination approach for the Tasmanian devil facial tumor diseases

ABSTRACT

Introduction: The Tasmanian devil (Sarcophilus harrisii) is the largest extant carnivorous marsupial. Since 1996, its population has declined by 77% primarily due to a clonal transmissible tumor, known as devil facial tumor (DFT1) disease. In 2014, a second transmissible devil facial tumor (DFT2) was discovered. DFT1 and DFT2 are nearly 100% fatal.

Areas covered: We review DFT control approaches and propose a rabies-style oral bait vaccine (OBV) platform for DFTs. This approach has an extensive safety record and was a primary tool in large-scale rabies virus elimination from wild carnivores across diverse landscapes. Like rabies virus, DFTs are transmitted by oral contact, so immunizing the oral cavity and stimulating resident memory cells could be advantageous. Additionally, exposing infected devils that already have tumors to OBVs could serve as an oncolytic virus immunotherapy. The primary challenges may be identifying appropriate DFT-specific antigens and optimization of field delivery methods.

Expert opinion: DFT2 is currently found on a peninsula in southern Tasmania, so an OBV that could eliminate DFT2 should be the priority for this vaccine approach. Translation of an OBV approach to control DFTs will be challenging, but the approach is feasible for combatting ongoing and future disease threats.

KEYWORDS:

• Devil
• transmissible tumor
• wild immunology
• allograft
• viral vector
• conservation immunology
• oral bait vaccine
• neoantigen

Article highlights

• Tasmanian devils get cancer at higher rates than most other species.

• The wild devil population has been reduced by 77% over the last 23 years due primarily to the emergence of a transmissible cancer, the devil facial tumor (DFT1).

• The emergence of a second transmissible tumor (DFT2) further threatens the long-term survival of this species.

• There are currently no effective interventions for reducing or controlling the impact of DFT1 or DFT2 on a broad scale, and few tools are in place to rapidly combat future disease outbreaks.

• We propose a rabies-style oral bait vaccine (OBV) as a safe and effective method for eliminating DFTs and this option must be explored to support the long-term survival of this iconic, endemic, endangered species.

• Tasmanian devils are the world’s largest carnivorous marsupial after the human-driven extinction of the Tasmanian tiger (Thylocanus cyanochalus) several decades ago. Fear of failure should not impede the exploration of innovative strategies to save this iconic species.

Author contributions

A S Files conceived the ideas and designed methodology; A S Files, S R Johnson, GS Liu collected the data; A S Files and E J Files led the writing of the manuscript. A Gilbert and S R Johnson provided expert insight on rabies bait vaccines. A B Lyons, A L Patchett, and R J Pye provided insights on DFT vaccine research. S Fox, D Pemberton, and R J Pye provided expert knowledge on the Tasmanian devil, current management practices and the history of DFTs and management of the disease and the devil. All authors contributed critically to the drafts and gave final approval for publication.

Acknowledgments

We would like to thank Chrissie Ong for comments on the manuscript and Jocelyn Darby, Alana De Luca, and Ahab Kayigwe for comments on the project.

Declaration of interest

The authors have an expression of interest for a related project pending with the Commonwealth Scientific and Industrial Research Organisation – Australian Animal Health Laboratory – Science©Merit Access Program. The authors have received funding from the Save the Tasmanian Devil Program for related projects. The authors have received funding for related projects from the Australian Research Council. Authors Flies, Lyons, and Patchett are currently participating in the CSIRO ON Prime program to further develop this project.

Reviewer disclosures

Peer reviewers on this manuscript have no relevant financial or other relationships to disclose.

Additional information

Funding

The authors have received funding from the University of Tasmania to develop the oral bait vaccine described in this manuscript. ARC Discovery Early Career Researcher Award # DE180100484, ARC Linkage Project # LP0989727, ARC Discovery Project # DP130100715, University of Tasmania Foundation Dr Eric Guiler Tasmanian Devil Research Grant through funds raised by the Save the Tasmanian Devil Appeal, University of Tasmania College of Health and Medicine Research Enhancement Program.