DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Portable Rabies Virus Sequencing in Canine Rabies Endemic Countries Using the Oxford Nanopore MinION

Abstract

As countries with endemic canine rabies progress towards elimination by 2030, it will become necessary to employ techniques to help plan, monitor, and confirm canine rabies elimination. Sequencing can provide critical information to inform control and vaccination strategies by identifying genetically distinct virus variants that may have different host reservoir species or geographic distributions. However, many rabies testing laboratories lack the resources or expertise for sequencing, especially in remote or rural areas where human rabies deaths are highest. We developed a low-cost, high throughput rabies virus sequencing method using the Oxford Nanopore MinION portable sequencer. A total of 259 sequences were generated from diverse rabies virus isolates in public health laboratories lacking rabies virus sequencing capacity in Guatemala, India, Kenya, and Vietnam. Phylogenetic analysis provided valuable insight into rabies virus diversity and distribution in these countries and identified a new rabies virus lineage in Kenya, the first published canine rabies virus sequence from Guatemala, evidence of rabies spread across an international border in Vietnam, and importation of a rabid dog into a state working to become rabies-free in India. Taken together, our evaluation highlights the MinION’s potential for low-cost, high volume sequencing of pathogens in locations with limited resources.

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3];  [4];  [5];  [5];  [5];  [6];  [7];  [7];  [7];  [8];  [8];  [8];  [8]; ORCiD logo [9];  [9]; ORCiD logo [10]; ORCiD logo [11];  [12] more »;  [13];  [13];  [14];  [15];  [16]; ORCiD logo [17];  [3]; ORCiD logo [3];  [3] « less
  1. Centers for Disease Control and Prevention (CDC), Atlanta, GA (United States). National Center for Emerging and Zoonotic Infectious Diseases. Division of High-Consequence Pathogens and Pathology. Poxvirus and Rabies Branch
  2. Mission Rabies, Tonca, Panjim, Goa (India)
  3. Centers for Disease Control and Prevention (CDC), Atlanta, GA (United States). National Center for Emerging and Zoonotic Infectious Diseases. Division of High-Consequence Pathogens and Pathology. Poxvirus and Rabies Branch
  4. Directorate of Animal Health and Veterinary Services, Patto, Panjim, Goa (India). Disease Investigation Unit
  5. Vietnam Dept. of Animal Health, Hanoi (Vietnam)
  6. National Center for Veterinary Diseases, Hanoi (Vietnam)
  7. Sub-Dept. of Animal Health, Phú Thọ Province (Vietnam)
  8. Kenya Medical Research Inst., Nairobi (Kenya)
  9. Ministry of Health, Nairobi (Kenya). Ministry of Agriculture, Livestock and Fisheries. Zoonotic Disease Unit
  10. Univ. of Glasgow, Scotland (United Kingdom). Inst. of Biodiversity, Animal Health and Comparative Medicine
  11. Kenya Medical Research Inst., Nairobi (Kenya); Univ. of Nairobi (Kenya). Inst. of Tropical and Infectious Diseases; Washington State Univ., Pullman, WA (United States). Paul G. Allen School for Global Animal Health
  12. Ministry of Agriculture Livestock and Food, Guatemala City (Guatemala)
  13. National Health Lab., MSPAS, Villa Nueva (Guatemala)
  14. Centers for Disease Control, Nairobi (Kenya). Division of Global Health Protection
  15. University del Valle de Guatemala, Guatemala City (Guatemala)
  16. Centers for Disease Control, Guatemala City (Guatemala). Division of Global Health Protection
  17. Univ. of Edinburgh, Scotland (United Kingdom). Easter Bush Veterinary Centre
Publication Date:
Research Org.:
Oak Ridge Inst. for Science and Education (ORISE), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1817096
Grant/Contract Number:  
SC0014664
Resource Type:
Accepted Manuscript
Journal Name:
Viruses
Additional Journal Information:
Journal Volume: 12; Journal Issue: 11; Journal ID: ISSN 1999-4915
Publisher:
MDPI
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; rabies; lyssavirus; canine rabies elimination; portable sequencing; nanopore; MinION

Citation Formats

Gigante, Crystal M., Yale, Gowri, Condori, Rene Edgar, Costa, Niceta Cunha, Long, Nguyen Van, Minh, Phan Quang, Chuong, Vo Dinh, Tho, Nguyen Dang, Thanh, Nguyen Tat, Thin, Nguyen Xuan, Hanh, Nguyen Thi Hong, Wambura, Gati, Ade, Frederick, Mito, Oscar, Chuchu, Veronicah, Muturi, Mathew, Mwatondo, Athman, Hampson, Katie, Thumbi, Samuel M., Thomae, Byron G., de Paz, Victor Hugo, Meneses, Sergio, Munyua, Peninah, Moran, David, Cadena, Loren, Gibson, Andrew, Wallace, Ryan M., Pieracci, Emily G., and Li, Yu. Portable Rabies Virus Sequencing in Canine Rabies Endemic Countries Using the Oxford Nanopore MinION. United States: N. p., 2020. Web. doi:10.3390/v12111255.
Gigante, Crystal M., Yale, Gowri, Condori, Rene Edgar, Costa, Niceta Cunha, Long, Nguyen Van, Minh, Phan Quang, Chuong, Vo Dinh, Tho, Nguyen Dang, Thanh, Nguyen Tat, Thin, Nguyen Xuan, Hanh, Nguyen Thi Hong, Wambura, Gati, Ade, Frederick, Mito, Oscar, Chuchu, Veronicah, Muturi, Mathew, Mwatondo, Athman, Hampson, Katie, Thumbi, Samuel M., Thomae, Byron G., de Paz, Victor Hugo, Meneses, Sergio, Munyua, Peninah, Moran, David, Cadena, Loren, Gibson, Andrew, Wallace, Ryan M., Pieracci, Emily G., & Li, Yu. Portable Rabies Virus Sequencing in Canine Rabies Endemic Countries Using the Oxford Nanopore MinION. United States. https://doi.org/10.3390/v12111255
Gigante, Crystal M., Yale, Gowri, Condori, Rene Edgar, Costa, Niceta Cunha, Long, Nguyen Van, Minh, Phan Quang, Chuong, Vo Dinh, Tho, Nguyen Dang, Thanh, Nguyen Tat, Thin, Nguyen Xuan, Hanh, Nguyen Thi Hong, Wambura, Gati, Ade, Frederick, Mito, Oscar, Chuchu, Veronicah, Muturi, Mathew, Mwatondo, Athman, Hampson, Katie, Thumbi, Samuel M., Thomae, Byron G., de Paz, Victor Hugo, Meneses, Sergio, Munyua, Peninah, Moran, David, Cadena, Loren, Gibson, Andrew, Wallace, Ryan M., Pieracci, Emily G., and Li, Yu. Sun . "Portable Rabies Virus Sequencing in Canine Rabies Endemic Countries Using the Oxford Nanopore MinION". United States. https://doi.org/10.3390/v12111255. https://www.osti.gov/servlets/purl/1817096.
@article{osti_1817096,
title = {Portable Rabies Virus Sequencing in Canine Rabies Endemic Countries Using the Oxford Nanopore MinION},
author = {Gigante, Crystal M. and Yale, Gowri and Condori, Rene Edgar and Costa, Niceta Cunha and Long, Nguyen Van and Minh, Phan Quang and Chuong, Vo Dinh and Tho, Nguyen Dang and Thanh, Nguyen Tat and Thin, Nguyen Xuan and Hanh, Nguyen Thi Hong and Wambura, Gati and Ade, Frederick and Mito, Oscar and Chuchu, Veronicah and Muturi, Mathew and Mwatondo, Athman and Hampson, Katie and Thumbi, Samuel M. and Thomae, Byron G. and de Paz, Victor Hugo and Meneses, Sergio and Munyua, Peninah and Moran, David and Cadena, Loren and Gibson, Andrew and Wallace, Ryan M. and Pieracci, Emily G. and Li, Yu},
abstractNote = {As countries with endemic canine rabies progress towards elimination by 2030, it will become necessary to employ techniques to help plan, monitor, and confirm canine rabies elimination. Sequencing can provide critical information to inform control and vaccination strategies by identifying genetically distinct virus variants that may have different host reservoir species or geographic distributions. However, many rabies testing laboratories lack the resources or expertise for sequencing, especially in remote or rural areas where human rabies deaths are highest. We developed a low-cost, high throughput rabies virus sequencing method using the Oxford Nanopore MinION portable sequencer. A total of 259 sequences were generated from diverse rabies virus isolates in public health laboratories lacking rabies virus sequencing capacity in Guatemala, India, Kenya, and Vietnam. Phylogenetic analysis provided valuable insight into rabies virus diversity and distribution in these countries and identified a new rabies virus lineage in Kenya, the first published canine rabies virus sequence from Guatemala, evidence of rabies spread across an international border in Vietnam, and importation of a rabid dog into a state working to become rabies-free in India. Taken together, our evaluation highlights the MinION’s potential for low-cost, high volume sequencing of pathogens in locations with limited resources.},
doi = {10.3390/v12111255},
journal = {Viruses},
number = 11,
volume = 12,
place = {United States},
year = {Sun Nov 01 00:00:00 EDT 2020},
month = {Sun Nov 01 00:00:00 EDT 2020}
}

Works referenced in this record:

Concepts in the pathogenesis of rabies
journal, September 2008


Nanopore sequencing and assembly of a human genome with ultra-long reads
journal, January 2018

  • Jain, Miten; Koren, Sergey; Miga, Karen H.
  • Nature Biotechnology, Vol. 36, Issue 4
  • DOI: 10.1038/nbt.4060

Immunization coverage required to prevent outbreaks of dog rabies
journal, February 1996


Rabies Situation in Cambodia
journal, September 2009


Emergence of Arctic-like Rabies Lineage in India
journal, January 2007

  • Nadin-Davis, Susan A.; Turner, Geoff; Paul, Joel P. V.
  • Emerging Infectious Diseases, Vol. 13, Issue 1
  • DOI: 10.3201/eid1301.060702

Community-based active surveillance for rabies in Machakos District, Kenya
journal, March 2000


A complete bacterial genome assembled de novo using only nanopore sequencing data
journal, June 2015

  • Loman, Nicholas J.; Quick, Joshua; Simpson, Jared T.
  • Nature Methods, Vol. 12, Issue 8
  • DOI: 10.1038/nmeth.3444

A Pan-Lyssavirus Taqman Real-Time RT-PCR Assay for the Detection of Highly Variable Rabies virus and Other Lyssaviruses
journal, January 2017


A molecular epidemiological study of rabies virus in central Ontario and western Quebec
journal, October 1994


Molecular epidemiology of canid rabies in Sudan: evidence for a common origin of rabies with Ethiopia
journal, September 2004


Next-generation sequencing in the clinic: are we ready?
journal, October 2012

  • Biesecker, Leslie G.; Burke, Wylie; Kohane, Isaac
  • Nature Reviews Genetics, Vol. 13, Issue 11
  • DOI: 10.1038/nrg3357

Phylogenetic analysis of nucleoprotein gene of dog rabies virus isolates from Southern India
journal, September 2009

  • Nagarajan, T.; Nagendrakumar, S. B.; Mohanasubramanian, B.
  • Infection, Genetics and Evolution, Vol. 9, Issue 5
  • DOI: 10.1016/j.meegid.2009.04.004

Reemerging Rabies and Lack of Systemic Surveillance in People’s Republic of China
journal, August 2009

  • Wu, Xianfu; Hu, Rongliang; Zhang, Yongzhen
  • Emerging Infectious Diseases, Vol. 15, Issue 8
  • DOI: 10.3201/eid1508.081426

Elucidating the phylodynamics of endemic rabies virus in eastern Africa using whole-genome sequencing
journal, January 2015

  • Brunker, Kirstyn; Marston, Denise A.; Horton, Daniel L.
  • Virus Evolution, Vol. 1, Issue 1
  • DOI: 10.1093/ve/vev011

Molecular Epidemiology of Reemergent Rabies in Yunnan Province, Southwestern China
journal, September 2014

  • Zhang, Hai-Lin; Zhang, Yu-Zhen; Yang, Wei-Hong
  • Emerging Infectious Diseases, Vol. 20, Issue 9
  • DOI: 10.3201/eid2009.130440

Bat Rabies in Guatemala
journal, July 2014


Present and Potential Future Distribution of Common Vampire Bats in the Americas and the Associated Risk to Cattle
journal, August 2012


The Feasibility of Canine Rabies Elimination in Africa: Dispelling Doubts with Data
journal, February 2010


Assessing the burden of human rabies in India: results of a national multi-center epidemiological survey
journal, January 2007

  • Sudarshan, M. K.; Madhusudana, S. N.; Mahendra, B. J.
  • International Journal of Infectious Diseases, Vol. 11, Issue 1
  • DOI: 10.1016/j.ijid.2005.10.007

Epidemiologic and Historical Relationships among 87 Rabies Virus Isolates as Determined by Limited Sequence Analysis
journal, August 1992

  • Smith, J. S.; Orciari, L. A.; Yager, P. A.
  • Journal of Infectious Diseases, Vol. 166, Issue 2
  • DOI: 10.1093/infdis/166.2.296

SeqKit: A Cross-Platform and Ultrafast Toolkit for FASTA/Q File Manipulation
journal, October 2016


Response to a Rabies Epidemic, Bali, Indonesia, 2008–2011
journal, April 2013

  • Putra, Anak Agung Gde; Hampson, Katie; Girardi, Janice
  • Emerging Infectious Diseases, Vol. 19, Issue 4
  • DOI: 10.3201/eid1904.120380

A review of room temperature storage of biospecimen tissue and nucleic acids for anatomic pathology laboratories and biorepositories
journal, March 2014


Multi-site evaluation of the LN34 pan-lyssavirus real-time RT-PCR assay for post-mortem rabies diagnostics
journal, May 2018


Evaluation of rabies virus characterization to enhance early detection of important rabies epizootic events in the United States
journal, January 2020

  • Pieracci, Emily G.; Chipman, Richard B.; Morgan, Clint N.
  • Journal of the American Veterinary Medical Association, Vol. 256, Issue 1
  • DOI: 10.2460/javma.256.1.66

Rabies virus isolates of India – Simultaneous existence of two distinct evolutionary lineages
journal, October 2014

  • Reddy, R. V. Chandrasekhar; Mohana Subramanian, B.; Surendra, K. S. N. L.
  • Infection, Genetics and Evolution, Vol. 27
  • DOI: 10.1016/j.meegid.2014.07.014

MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013

  • Katoh, K.; Standley, D. M.
  • Molecular Biology and Evolution, Vol. 30, Issue 4
  • DOI: 10.1093/molbev/mst010

Rapid in-country sequencing of whole virus genomes to inform rabies elimination programmes
journal, January 2020


Molecular Epidemiology of Rabies Virus Isolates in India
journal, September 2006

  • Nagarajan, T.; Mohanasubramanian, B.; Seshagiri, E. V.
  • Journal of Clinical Microbiology, Vol. 44, Issue 9
  • DOI: 10.1128/JCM.00801-06

Performance of neural network basecalling tools for Oxford Nanopore sequencing
journal, June 2019


Predicting the local dynamics of epizootic rabies among raccoons in the United States
journal, November 2000

  • Childs, J. E.; Curns, A. T.; Dey, M. E.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 25
  • DOI: 10.1073/pnas.240326697

MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform
journal, July 2002


Epidemiological and clinical features of human rabies cases in Bali 2008-2010
journal, April 2012

  • Susilawathi, Ni M.; Darwinata, Agus E.; Dwija, Ida BNP
  • BMC Infectious Diseases, Vol. 12, Issue 1
  • DOI: 10.1186/1471-2334-12-81

The real cost of sequencing: higher than you think!
journal, January 2011


National Borders Effectively Halt the Spread of Rabies: The Current Rabies Epidemic in China Is Dislocated from Cases in Neighboring Countries
journal, January 2013


Emerging Technologies for the Detection of Rabies Virus: Challenges and Hopes in the 21st Century
journal, September 2009

  • Fooks, Anthony R.; Johnson, Nicholas; Freuling, Conrad M.
  • PLoS Neglected Tropical Diseases, Vol. 3, Issue 9
  • DOI: 10.1371/journal.pntd.0000530

Portable devices and mobile instruments for infectious diseases point-of-care testing
journal, April 2017


Cross-border spread, lineage displacement and evolutionary rate estimation of rabies virus in Yunnan Province, China
journal, June 2017


Eliminating canine rabies, the principal source of human infection: What will it take?
journal, May 2013


The status of rabies in Ethiopia: A retrospective record review
journal, December 2010

  • Deressa, A.; Ali, A.; Bayene, M.
  • Ethiopian Journal of Health Development, Vol. 24, Issue 2
  • DOI: 10.4314/ejhd.v24i2.62961

Host Phylogeny Constrains Cross-Species Emergence and Establishment of Rabies Virus in Bats
journal, August 2010


Recent Emergence and Spread of an Arctic-Related Phylogenetic Lineage of Rabies Virus in Nepal
journal, November 2013


The Phylogeography of Rabies in Grenada, West Indies, and Implications for Control
journal, October 2014


Public Veterinary Medicine: Public Health: Rabies surveillance in the United States during 2018
journal, January 2020

  • Ma, Xiaoyue; Monroe, Ben P.; Cleaton, Julie M.
  • Journal of the American Veterinary Medical Association, Vol. 256, Issue 2
  • DOI: 10.2460/javma.256.2.195

Rabies re-examined
journal, June 2002

  • Rupprecht, Charles E.; Hanlon, Cathleen A.; Hemachudha, Thiravat
  • The Lancet Infectious Diseases, Vol. 2, Issue 6
  • DOI: 10.1016/S1473-3099(02)00287-6

Enzootic and Epizootic Rabies Associated with Vampire Bats, Peru
journal, September 2013

  • Condori-Condori, Rene Edgar; Streicker, Daniel G.; Cabezas-Sanchez, Cesar
  • Emerging Infectious Diseases, Vol. 19, Issue 9
  • DOI: 10.3201/eid1909.130083

Molecular Inferences Suggest Multiple Host Shifts of Rabies Viruses from Bats to Mesocarnivores in Arizona during 2001–2009
journal, June 2012


Genetic Polymorphism in the Rabies Virus Nucleoprotein Gene
journal, June 1995


Molecular characterization of rabies virus isolates from Mexico: implications for transmission dynamics and human risk.
journal, October 1999

  • Orciari, L. A.; Loza-Rubio, E.; Smith, J. S.
  • The American Journal of Tropical Medicine and Hygiene, Vol. 61, Issue 4
  • DOI: 10.4269/ajtmh.1999.61.587

Mapping and phasing of structural variation in patient genomes using nanopore sequencing
journal, November 2017

  • Cretu Stancu, Mircea; van Roosmalen, Markus J.; Renkens, Ivo
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/s41467-017-01343-4

The real cost of sequencing: scaling computation to keep pace with data generation
journal, March 2016


Control of rabies in Jaipur, India, by the sterilisation and vaccination of neighbourhood dogs
journal, September 2006


Molecular epidemiology of rabies virus circulating in domestic animals in India
journal, July 2018

  • Manjunatha Reddy, Gundallhalli Bayyappa; Krishnappa, Sumana; Vinayagamurthy, Balamurugan
  • VirusDisease, Vol. 29, Issue 3
  • DOI: 10.1007/s13337-018-0478-9

Molecular Epidemiology of Rabies in Vietnam
journal, September 2007


Stray dog population demographics in Jodhpur, India following a population control/rabies vaccination program
journal, October 2010


Determining the post-elimination level of vaccination needed to prevent re-establishment of dog rabies
journal, December 2019


Real-time, portable genome sequencing for Ebola surveillance
journal, February 2016

  • Quick, Joshua; Loman, Nicholas J.; Duraffour, Sophie
  • Nature, Vol. 530, Issue 7589
  • DOI: 10.1038/nature16996

The role of viral evolution in rabies host shifts and emergence
journal, October 2014


Processes Underlying Rabies Virus Incursions across US–Canada Border as Revealed by Whole-Genome Phylogeography
journal, September 2017

  • Trewby, Hannah; Nadin-Davis, Susan A.; Real, Leslie A.
  • Emerging Infectious Diseases, Vol. 23, Issue 9
  • DOI: 10.3201/eid2309.170325

MinION-based long-read sequencing and assembly extends the Caenorhabditis elegans reference genome
journal, December 2017

  • Tyson, John R.; O'Neil, Nigel J.; Jain, Miten
  • Genome Research, Vol. 28, Issue 2
  • DOI: 10.1101/gr.221184.117

Synchronous cycles of domestic dog rabies in sub-Saharan Africa and the impact of control efforts
journal, April 2007

  • Hampson, Katie; Dushoff, Jonathan; Bingham, John
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 18
  • DOI: 10.1073/pnas.0609122104

Implementation of an Intersectoral Program to Eliminate Human and Canine Rabies: The Bohol Rabies Prevention and Elimination Project
journal, December 2012

  • Lapiz, Stella Marie D.; Miranda, Mary Elizabeth G.; Garcia, Romulo G.
  • PLoS Neglected Tropical Diseases, Vol. 6, Issue 12
  • DOI: 10.1371/journal.pntd.0001891

Elimination of Dog-Mediated Human Rabies Deaths by 2030: Needs Assessment and Alternatives for Progress Based on Dog Vaccination
journal, February 2017

  • Wallace, Ryan M.; Undurraga, Eduardo A.; Blanton, Jesse D.
  • Frontiers in Veterinary Science, Vol. 4
  • DOI: 10.3389/fvets.2017.00009

Host Switching in Lyssavirus History from the Chiroptera to the Carnivora Orders
journal, September 2001


Effective Control of an Outbreak of Rabies in Memphis and Shelby County, Tennessee
journal, September 1950

  • Tierkel, Ernest S.; Graves, Lloyd M.; Tuggle, H. G.
  • American Journal of Public Health and the Nations Health, Vol. 40, Issue 9
  • DOI: 10.2105/AJPH.40.9.1084

Vaccinate-assess-move method of mass canine rabies vaccination utilising mobile technology data collection in Ranchi, India
journal, December 2015


The Next-Generation Sequencing Revolution and Its Impact on Genomics
journal, September 2013


Paralytic rabies after a two week holiday in India
journal, September 2005


Rabies control initiative in Tamil Nadu, India: a test case for the ‘One Health’ approach
journal, December 2011


Molecular Phylodynamic Analysis Indicates Lineage Displacement Occurred in Chinese Rabies Epidemics between 1949 to 2010
journal, July 2013


Use of filter paper (FTA®) technology for sampling, recovery and molecular characterisation of rabies viruses
journal, March 2007


Overview of rabies in the Americas
journal, July 2005


Antigenic variants of rabies virus
journal, July 1980

  • Wiktor, Tj; Koprowski, H.
  • Journal of Experimental Medicine, Vol. 152, Issue 1
  • DOI: 10.1084/jem.152.1.99

Analysis on factors related to rabies epidemic in China from 2007–2011
journal, April 2012


MinION Analysis and Reference Consortium: Phase 2 data release and analysis of R9.0 chemistry
journal, January 2017


The origin and phylogeography of dog rabies virus
journal, November 2008


Point-of-care molecular diagnostic systems — past, present and future
journal, October 2005


Surveillance guidelines for disease elimination: A case study of canine rabies
journal, May 2013

  • Townsend, Sunny E.; Lembo, Tiziana; Cleaveland, Sarah
  • Comparative Immunology, Microbiology and Infectious Diseases, Vol. 36, Issue 3
  • DOI: 10.1016/j.cimid.2012.10.008

Antigenic and genetic divergence of rabies viruses from bat species indigenous to Canada
journal, April 2001


The Epidemiology of fox Rabies in Europe
journal, January 1980


Complex Epidemiology of a Zoonotic Disease in a Culturally Diverse Region: Phylogeography of Rabies Virus in the Middle East
journal, March 2015

  • Horton, Daniel L.; McElhinney, Lorraine M.; Freuling, Conrad M.
  • PLOS Neglected Tropical Diseases, Vol. 9, Issue 3
  • DOI: 10.1371/journal.pntd.0003569

Spatio-temporal Analysis of the Genetic Diversity of Arctic Rabies Viruses and Their Reservoir Hosts in Greenland
journal, July 2016


One million dog vaccinations recorded on mHealth innovation used to direct teams in numerous rabies control campaigns
journal, July 2018


Large-Scale Phylogenomic Analysis Reveals the Complex Evolutionary History of Rabies Virus in Multiple Carnivore Hosts
journal, December 2016


Canu: scalable and accurate long-read assembly via adaptive k -mer weighting and repeat separation
journal, March 2017

  • Koren, Sergey; Walenz, Brian P.; Berlin, Konstantin
  • Genome Research, Vol. 27, Issue 5
  • DOI: 10.1101/gr.215087.116

Ecology and evolution of rabies virus in Europe
journal, October 1999


Commercialization of microfluidic point-of-care diagnostic devices
journal, January 2012

  • Chin, Curtis D.; Linder, Vincent; Sia, Samuel K.
  • Lab on a Chip, Vol. 12, Issue 12
  • DOI: 10.1039/c2lc21204h

MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016

  • Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
  • Molecular Biology and Evolution, Vol. 33, Issue 7
  • DOI: 10.1093/molbev/msw054

Analysis of Rabies in China: Transmission Dynamics and Control
journal, July 2011


Molecular Diversity of Rabies Viruses Associated with Bats in Mexico and Other Countries of the Americas
journal, May 2006


Characterization of an antigenic determinant of the glycoprotein that correlates with pathogenicity of rabies virus.
journal, January 1983

  • Dietzschold, B.; Wunner, W. H.; Wiktor, T. J.
  • Proceedings of the National Academy of Sciences, Vol. 80, Issue 1
  • DOI: 10.1073/pnas.80.1.70

Imported Episodic Rabies Increases Patient Demand for and Physician Delivery of Antirabies Prophylaxis
journal, June 2010


Zika virus in the Americas: Early epidemiological and genetic findings
journal, March 2016

  • Faria, N. R.; Azevedo, R. d. S. d. S.; Kraemer, M. U. G.
  • Science, Vol. 352, Issue 6283
  • DOI: 10.1126/science.aaf5036

Difficulties in estimating the human burden of canine rabies
journal, January 2017


Barriers to dog rabies vaccination during an urban rabies outbreak: Qualitative findings from Arequipa, Peru
journal, March 2017

  • Castillo-Neyra, Ricardo; Brown, Joanna; Borrini, Katty
  • PLOS Neglected Tropical Diseases, Vol. 11, Issue 3
  • DOI: 10.1371/journal.pntd.0005460

Control and prevention of canine rabies: The need for building laboratory-based surveillance capacity
journal, June 2013


Rabies virus glycoprotein. II. Biological and serological characterization
journal, June 1977