Biting midges (Diptera: Ceratopogonidae) as putative vectors of zoonotic Onchocerca lupi (Nematoda: Onchocercidae) in northern Arizona and New Mexico, southwestern United States

Chandler C Roe; Olivia Holiday; Kelly Upshaw-Bia; Gaven Benally; Charles H D Williamson; Jennifer Urbanz; Guilherme G Verocai; Chase L Ridenour; Roxanne Nottingham; Morgan A Ford; Derek P Lake; Theodore A Kennedy; Crystal M Hepp; Jason W Sahl

doi:10.3389/fvets.2023.1167070

Biting midges (Diptera: Ceratopogonidae) as putative vectors of zoonotic Onchocerca lupi (Nematoda: Onchocercidae) in northern Arizona and New Mexico, southwestern United States

Front Vet Sci. 2023 May 15:10:1167070. doi: 10.3389/fvets.2023.1167070. eCollection 2023.

Authors

Chandler C Roe^{1

2}, Olivia Holiday³, Kelly Upshaw-Bia³, Gaven Benally³, Charles H D Williamson¹, Jennifer Urbanz⁴, Guilherme G Verocai⁵, Chase L Ridenour^{1

2

6}, Roxanne Nottingham¹, Morgan A Ford⁷, Derek P Lake¹, Theodore A Kennedy⁷, Crystal M Hepp^{1

2

6}, Jason W Sahl¹

Affiliations

¹ The Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, AZ, United States.
² School of Informatics, Computing, and Cyber Systems, Northern Arizona University, Flagstaff, AZ, United States.
³ Navajo Nation Veterinary Management Program, Window Rock, AZ, United States.
⁴ Eye Care for Animals, Scottsdale, AZ, United States.
⁵ Department of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX, United States.
⁶ Pathogen and Microbiome Division, Translational Genomics Research Institute, Flagstaff, AZ, United States.
⁷ U.S. Geological Survey, Southwest Biological Science Center, Flagstaff, AZ, United States.

Abstract

Onchocerca lupi (Rodonaja, 1967) is an understudied, vector-borne, filarioid nematode that causes ocular onchocercosis in dogs, cats, coyotes, wolves, and is also capable of infecting humans. Onchocercosis in dogs has been reported with increasing incidence worldwide. However, despite the growing number of reports describing canine O. lupi cases as well as zoonotic infections globally, the disease prevalence in endemic areas and vector species of this parasite remains largely unknown. Here, our study aimed to identify the occurrence of O. lupi infected dogs in northern Arizona, New Mexico, and Utah, United States and identify the vector of this nematode. A total of 532 skin samples from randomly selected companion animals with known geographic locations within the Navajo Reservation were collected and molecularly surveyed by PCR for the presence of O. lupi DNA (September 2019-June 2022) using previously published nematode primers (COI) and DNA sequencing. O. lupi DNA was detected in 50 (9.4%) sampled animals throughout the reservation. Using positive animal samples to target geographic locations, pointed hematophagous insect trapping was performed to identify potential O. lupi vectors. Out of 1,922 insects screened, 38 individual insects and 19 insect pools tested positive for the presence of O. lupi, all of which belong to the Diptera family. This increased surveillance of definitive host and biological vector/intermediate host is the first large scale prevalence study of O. lupi in companion animals in an endemic area of the United States, and identified an overall prevalence of 9.4% in companion animals as well as multiple likely biological vector and putative vector species in the southwestern United States. Furthermore, the identification of these putative vectors in close proximity to human populations coupled with multiple, local zoonotic cases highlight the One Health importance of O. lupi.

Keywords: Ceratopogonidae; Onchocerca lupi; biting midges; nematodes; prevalence.