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Volume 30, Number 9—September 2024
Research Letter
Thelazia callipaeda Eyeworms in American Black Bear, Pennsylvania, USA, 2023
Suggested citation for this article
Abstract
We identified a Thelazia callipaeda eyeworm in an American black bear in Pennsylvania, USA, on the basis of its morphological features and molecular analysis. Our finding highlights emergence of a T. callipaeda worm sylvatic transmission cycle in the United States.
Thelaziosis is an emerging zoonotic disease caused by nematodes of the genus Thelazia (Spirurida, Thelazioidea). In the United States, 3 zoonotic species have been identified: Thelazia gulosa (1), T. californiensis (2), and most recently T. callipaeda (3). In Asia and Europe, T. callipaeda is considered the main agent of thelaziosis in humans, domestic animals, and wild animals (4). Over the past decade, the geographic distribution and prevalence of T. callipaeda infection has increased worldwide in scale and intensity (4). The first autochthonous case in the United States was reported in 2018 in a domestic dog (Canis lupus familiaris) from New York with a history of unilateral epiphora and blepharospasm. Since then, additional cases in domestic dogs and cats have been reported, predominately from the northeastern United States (3,5).
T. callipaeda eyeworms are found in the conjunctival sac and lacrimal duct of the definitive host. They are transmitted when a male zoophilic secretophagous Phortica variegata fly ingests first-stage larvae from the host’s lachrymal secretions. In the vector, the first-stage larvae develop to the infective third-stage larvae in the testes, migrate to the mouthparts, and are transferred to another host during subsequent feeding on lachrymal secretions (4).
The role of wildlife in the epidemiology and emergence of T. callipaeda eyeworms is not completely known. In Europe, cases of T. callipaeda eyeworm infection have been detected in a wide range of hosts, including wild carnivores, omnivores, and lagomorphs (6,7). Wild canids, particularly red foxes (Vulpes vulpes), seem to play a large role in maintaining the sylvatic cycle in thelaziosis-endemic areas of Europe (7). However, knowledge of the sylvatic transmission cycle of T. callipaeda eyeworms, along with their environmental and anthropogenic factors, remains limited. Considering the emergence of those zoonotic nematodes in non–thelaziosis-endemic areas and the need for more information about their ecology and epidemiology in the United States, we report a case of T. callipaeda eyeworm infection in an American black bear (Ursus americanus) and identify a new geographic location of transmission.
In November 2023, an adult, female American black bear was legally harvested in Coolbaugh Township, Monroe County, Pennsylvania. During processing of the bear for taxidermy preparation, multiple linear nematodes were observed behind the third eyelid. Nematodes were extracted and submitted for identification. Two additional harvested bears from Monroe and Pike Counties, Pennsylvania, were also reported to have similar ocular nematode infections, but specimens from those bears were not collected.
We identified 9 female and 4 male adult nematodes from the bear as T. callipaeda on the basis of morphologic and morphometric features (8). The nematodes were characterized by the presence of a cup-shaped buccal capsule and cuticular transverse striations, as well as the location of the vulvar opening anterior to the esophageal-intestinal junction on the female worms (Figure 1). Female nematodes were 1.16–1.46 cm long and 0.36–0.42 mm wide; male worms were 0.82–1.06 cm long and 0.31–0.42 mm wide. The number of transverse cuticular striations ranged from 160 to 400/mm in the cephalic, midbody, and caudal regions.
We extracted genomic DNA from a midbody fragment of a female adult worm and amplified, sequenced, and analyzed the partial cytochrome oxidase c subunit I (cox1) gene, as previously described (2). We generated a 623-bp cox1 sequence (GenBank accession no. PP739308), which showed 99%–100% maximum identity with T. callipaeda sequences available in GenBank. Phylogenetic analysis was performed by using the maximum-likelihood method and confirmed the taxonomic identification of T. callipaeda. The isolate clustered with all previous isolates from domestic animals in North America and with some isolates from Europe (Figure 2), indicating circulation of the newly introduced pathogen in wildlife habitats and transmission from domestic animals to wildlife.
The presence of adult T. callipaeda eyeworms in an American black bear suggests the establishment of a sylvatic transmission cycle in the United States and expansion of the number of definitive host species used by the zoonotic nematode. In the past decade, wild carnivores have been identified as primary definitive hosts associated with the sylvatic cycle in thelaziosis- endemic and non–thelaziosis-endemic areas of Europe and Asia (7). American black bears are the most widely distributed species of bear in North America, inhabiting diverse regions throughout Mexico, Canada, and the United States (9). Given the bears’ extensive geographic distribution and frequent and close interaction with humans and pets (10), thelaziosis in the black bear population raises concerns about the rapidly increasing incidence and geographic range of T. callipaeda eyeworms in the United States. Although further research into the extent to which black bears play a role in the maintenance of the sylvatic cycle and transmission of T. callipaeda eyeworms is needed, the presence of the zoonotic nematode in such a wide range of hosts implicates exposure and risk for transmission to threatened and endangered species and direct or indirect risk for transmission to humans and domestic animals.
Dr. Sobotyk is an assistant professor of clinical parasitology and director of the Clinical Parasitology Laboratory at the University of Pennsylvania, Philadelphia, PA. Her research focuses on zoonotic helminth infections in domestic and wild animals and improvement and development of diagnostic techniques for detecting parasitic infections of veterinary and public health relevance.
Acknowledgment
We thank the Pennsylvania Game Commission and Dillon Gruver for their continued support. We also acknowledge Shawn Lamparter’s Wildlife Design for recognition and prompting submission of the specimens.
References
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Figures
Suggested citation for this article: Sobotyk C, Dietrich J, Verocai GG, Maxwell L, Niedringhaus K. Thelazia callipaeda eyeworms in American black bear, Pennsylvania, USA, 2023. Emerg Infect Dis. 2024 Sep [date cited]. https://doi.org/10.3201/eid3009.240679
Original Publication Date: August 14, 2024
Table of Contents – Volume 30, Number 9—September 2024
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Please use the form below to submit correspondence to the authors or contact them at the following address:
Caroline. Sobotyk, University of Pennsylvania, School of Veterinary Medicine, Matthew J. Ryan Veterinary Hospital, Rm 4034, 3900 Delancey St, Philadelphia, PA 19104-6051, USA
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