SURVEILLANCE FOR AN EMERGENT HOOF DISEASE IN ELK (CERVUS ELAPHUS) IN THE US PACIFIC WEST SUPPLEMENTED BY 16S RRNA GENE AMPLICON SEQUENCING

Abstract: A novel hoof disease of elk (Cervus elaphus) was described in southwestern Washington, US, in 2008 and was subsequently diagnosed in an adjacent area in northwestern Oregon in 2014. The disease, currently referred to as treponeme-associated hoof disease (TAHD), is characterized by lesions ranging from mild erosions, to severe ulcers with underrunning of the hoof capsule and heel-sole junction, to overgrown and avulsed hoof capsules. Histologically, lesions exhibit epithelial erosion or ulceration, suppurative inflammation, and the presence of argyrophilic spirochetes. We used data collected by the Washington Department of Fish and Wildlife and Oregon Department of Fish and Wildlife from 2008 to 2017 as reference for disease distribution. We then conducted enhanced surveillance in 2018–20 by obtaining 164 submissions from four US Pacific West states. We detected TAHD for the first time in Idaho and northern California, as well as in multiple counties in Washington and Oregon where it had not been previously reported. Given the unexpectedly broad disease distribution, continued surveillance is warranted to determine the full geographic extent of TAHD. From samples of 22 elk, we investigated 16S rRNA gene amplicon sequencing as a technique that could be used to supplement TAHD surveillance. Operational taxonomic units of the family Spirochaetaceae were identified in 10 of 12 histologically diagnosed TAHD-positive cases and two of 10 TAHD-negative cases. Phyla Spirochaetae (P<0.008), Fusobacteria (P<0.006), and Tenericutes (P<0.01) were overrepresented in samples from TAHD-positive feet when compared with TAHD-negative elk. A unique spirochete, PT19, was detected in hooves of 11 elk and from at least one elk in each state. Results support the use of 16S rRNA gene amplicon sequencing as a reliable and informative tool to supplement investigations into distribution and etiology of this presumed polybacterial disease.

[1]  Paulína Marčeková,et al.  The Presence of Treponema spp. in Equine Hoof Canker Biopsies and Skin Samples from Bovine Digital Dermatitis Lesions , 2021, Microorganisms.

[2]  M. Alsaaod,et al.  Detection of treponemes in digital dermatitis lesions of captive European bison (Bison bonasus) , 2021, PloS one.

[3]  P. Richards,et al.  The dysbiosis of ovine foot microbiome during the development and treatment of contagious ovine digital dermatitis , 2020, Animal microbiome.

[4]  Daniel A. Grear,et al.  The ecology of chronic wasting disease in wildlife , 2019, Biological reviews of the Cambridge Philosophical Society.

[5]  Nicholas A. Be,et al.  Putative parapoxvirus-associated foot disease in the endangered huemul deer (Hippocamelus bisulcus) in Bernardo O’Higgins National Park, Chile , 2019, PloS one.

[6]  Christopher L. Jerde,et al.  High-Throughput Sequencing for Understanding the Ecology of Emerging Infectious Diseases at the Wildlife-Human Interface , 2019, Front. Ecol. Evol..

[7]  Steven D. Miller,et al.  The Expectations and Challenges of Wildlife Disease Research in the Era of Genomics: Forecasting with a Horizon Scan-like Exercise. , 2019, The Journal of heredity.

[8]  T. Besser,et al.  Treponeme-Associated Hoof Disease of Free-Ranging Elk (Cervus elaphus) in Southwestern Washington State, USA , 2018, Veterinary pathology.

[9]  L. Lenzi,et al.  16S rRNA amplicon sequencing reveals a polymicrobial nature of complicated claw horn disruption lesions and interdigital phlegmon in dairy cattle , 2018, Scientific Reports.

[10]  J. Pikula,et al.  White-nose syndrome detected in bats over an extensive area of Russia , 2018, BMC Veterinary Research.

[11]  M. Palmer,et al.  Experimental Transmission of Bovine Digital Dermatitis to Sheep: Development of an Infection Model , 2018, Veterinary pathology.

[12]  M. D. de Jong,et al.  Digital Dermatitis in dairy cattle: The contribution of different disease classes to transmission. , 2017, Epidemics.

[13]  Lalanika M. Abayasekara,et al.  Detection of bacterial pathogens from clinical specimens using conventional microbial culture and 16S metagenomics: a comparative study , 2017, BMC Infectious Diseases.

[14]  P. Myer,et al.  Evaluation of 16S rRNA amplicon sequencing using two next-generation sequencing technologies for phylogenetic analysis of the rumen bacterial community in steers. , 2016, Journal of microbiological methods.

[15]  J. Foster,et al.  Application of genetics and genomics to wildlife epidemiology , 2016 .

[16]  Paul J. McMurdie,et al.  DADA2: High resolution sample inference from Illumina amplicon data , 2016, Nature Methods.

[17]  D. Alt,et al.  The etiology of digital dermatitis in ruminants: recent perspectives , 2015, Veterinary medicine.

[18]  L. E. Sullivan,et al.  Isolation of Digital Dermatitis Treponemes from Hoof Lesions in Wild North American Elk (Cervus elaphus) in Washington State, USA , 2014, Journal of Clinical Microbiology.

[19]  G. Phillips,et al.  Deep Sequencing Analysis Reveals Temporal Microbiota Changes Associated with Development of Bovine Digital Dermatitis , 2014, Infection and Immunity.

[20]  K. Mansfield,et al.  SEVERE HOOF DISEASE IN FREE-RANGING ROOSEVELT ELK (CERVUS ELAPHUS ROOSEVELTI) IN SOUTHWESTERN WASHINGTON, USA , 2014, Journal of wildlife diseases.

[21]  T. Jensen,et al.  Interdigital dermatitis, heel horn erosion, and digital dermatitis in 14 Norwegian dairy herds. , 2013, Journal of dairy science.

[22]  M. Boyé,et al.  Targeting the Treponemal Microbiome of Digital Dermatitis Infections by High-Resolution Phylogenetic Analyses and Comparison with Fluorescent In Situ Hybridization , 2013, Journal of Clinical Microbiology.

[23]  Robert C. Edgar,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2001 .

[24]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[25]  C. Hart,et al.  Treponema pedis sp. nov., a spirochaete isolated from bovine digital dermatitis lesions. , 2009, International journal of systematic and evolutionary microbiology.

[26]  C. Hart,et al.  Three unique groups of spirochetes isolated from digital dermatitis lesions in UK cattle. , 2008, Veterinary microbiology.

[27]  J. Parmley.  Essentials of Disease in Wild Animals , 2006 .

[28]  J. Clarridge,et al.  Impact of 16 S rRNA Gene Sequence Analysis for Identification of Bacteria on Clinical Microbiology and Infectious Diseases , 2004 .