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Isolation of Onchocerca lupi in Dogs and Black Flies, California, USA - Volume 21, Number 5—May 2015 - Emerging Infectious Disease journal - CDC

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Isolation of Onchocerca lupi in Dogs and Black Flies, California, USA - Volume 21, Number 5—May 2015 - Emerging Infectious Disease journal - CDC







Volume 21, Number 5—May 2015

Research

Isolation of Onchocerca lupi in Dogs and Black Flies, California, USA

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Hassan K. Hassan1, Shanna Bolcen1, Joseph Kubofcik, Thomas B. Nutman, Mark L. Eberhard, Kelly Middleton, Joseph Wakoli Wekesa, Gimena Ruedas, Kimberly J. Nelson, Richard Dubielzig, Melissa De Lombaert, Bruce Silverman, Jamie J. Schorling, Peter H. Adler, Thomas R. UnnaschComments to Author , and Emily S. Beeler
Author affiliations: University of South Florida, Tampa, Florida, USA (H.K. Hassan, S. Bolcen, T.R. Unnasch);National Institute of Allergy and Infectious Diseases, Bethesda, Maryland, USA (J. Kubofcik, T.B. Nutman);Centers for Disease Control and Prevention, Atlanta, Georgia, USA (M.L. Eberhard); San Gabriel Valley Mosquito and Vector Control District, West Covina, California, USA (K. Middleton, J.W. Wekesa, G. Ruedas, K.J. Nelson);University of Wisconsin, Madison, Wisconsin, USA (R. Dubielzig, M. De Lombaert); Complete Animal Eye Care, Sherman Oaks, California, USA (B. Silverman); Eye Clinic for Animals, San Diego, California, USA (J.J. Schorling);Clemson University, Clemson, South Carolina, USA (P.H. Adler); Los Angeles County Department of Public Health, Los Angeles, California, USA (E.S. Beeler)

Abstract

In southern California, ocular infections caused by Onchocerca lupi were diagnosed in 3 dogs (1 in 2006, 2 in 2012). The infectious agent was confirmed through morphologic analysis of fixed parasites in tissues and by PCR and sequencing of amplicons derived from 2 mitochondrially encoded genes and 1 nuclear-encoded gene. A nested PCR based on the sequence of the cytochrome oxidase subunit 1 gene of the parasite was developed and used to screen Simulium black flies collected from southern California for O. lupi DNA. Six (2.8%; 95% CI 0.6%–5.0%) of 213 black flies contained O. lupi DNA. Partial mitochondrial16S rRNA gene sequences from the infected flies matched sequences derived from black fly larvae cytotaxonomically identified as Simulium tribulatum. These data implicate S. tribulatum flies as a putative vector for O. lupi in southern California.
Onchocerca lupi is a zoonotic parasite capable of infecting dogs, cats, and humans. Human infection was first suspected in 2002, when a case of human subconjunctival filariasis was found to have a worm with morphology similar to that of O. lupi (1). Human infection was confirmed in 2011, when a subconjunctival nematode in the eye of a young woman in Turkey was identified by molecular methods as O. lupi (2). Overall, ≈10 confirmed or suspected human cases have been reported in Turkey (3,4), Tunisia (4), Iran (5), the southwestern United States (6), Crimea (1), and Albania (1). In most cases, clinical findings were similar, with a single immature worm found within a periocular mass. In the US case, a mature, gravid female worm was found within a mass in the cervical spinal canal of a young child in Arizona (6). The Centers for Disease Control and Prevention recently confirmed 5 additional cases in humans in the southwestern United States (M.L. Eberhard, unpub. data).
Several parasites of the genus Onchocerca are known to occur in North America, including 2 in cattle (O. gutturosa and O. lienalis) (7) and 1 in horses (O. cervicalis) (8). In addition, at least 2 parasites of the native cervid species (9) are known to be endemic to North America; at least 1 of these (O. cervipedis) has been identified in deer in California (10). Although most Onchocerca species are associated with ungulates, O. lupi is unique in that it is primarily associated with canids. The first report of O. lupi infection was in a wolf in Russia (11). In the past 20 years, ≈70 cases of O. lupi infection have been reported in domestic dogs in the United States, Greece, and Portugal (12–17). Probable cases also have been reported in Germany, Hungary, Switzerland, and Canada (16,18,19). Many affected dogs contained gravid female worms, presenting the possibility that canids may be a reservoir host for the parasite. The only additional species reported to have been infected were cats: 2 cases were documented in Utah, USA (20). Both cats were infected with gravid female worms, suggesting that cats also might be reservoir hosts. However, both cats also were infected with feline leukemia virus and probably were immunosuppressed and therefore not representative of most cats.
Thumbnail of Right eye of a dog with Onchocerca lupi infection, southern California, USA, 2012. The dog had severe conjunctival inflammation, corneal degeneration, and an elevated intraocular pressure of 31 mm Hg. Ultimately, enucleation was performed, and histology revealed Onchocerca adult worms.
Figure 1. Right eye of a dog with Onchocerca lupi infection, southern California, USA, 2004. The dog had severe conjunctival inflammation, corneal degeneration, and an elevated intraocular pressure of 31 mm Hg. Ultimately,...
In the United States, confirmed and probable O. lupi infection has been documented in at least 12 dogs (17) and 2 cats (20) since 1991. That 6 of the 12 cases in dogs were in southern California (17,21) highlights this area as a focus of infection. Clinical signs in dogs typically involve 0.3–0.7-cm periocular masses that contain adult worms. Infections may be associated with additional ocular pathology (Figure 1). The masses are typically subconjunctival or episcleral but can be found anywhere in the orbit (22).


The life cycle of O. lupi, including the vector and its primary reservoir host, remains unknown. Determining the vector is the critical step in preventing exposure. Black flies (Simulium spp.) and biting midges (Culicoides spp.) are vectors for other species of Onchocerca (23) and might be vectors for O. lupi. Black flies are routinely detected in certain areas of Los Angeles County, including a 29-km stretch of the Los Angeles River (http://www.glacvcd.org/), in the San Gabriel Valley area (http://sgvmosquito.org/), and in western areas of the county (http://www.lawestvector.org/). We report 3 additional O. lupi infections in dogs in southern California and present molecular evidence implicating the black fly species S. tribulatum as the possible vector for this parasite.

Mr. Hassan is a research associate in the Department of Global Health at the University of South Florida. His research interests focus on the development of novel diagnostic tests for, and the ecology of, vector-borne diseases, with an emphasis on human infections with Onchocerca spp.

Acknowledgments

This study was funded in part by the Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health (J.K. and T.B.N.).
S.B. worked on this project in partial fulfillment of her Master of Science in Public Health degree at the University of South Florida.

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Table

Technical Appendix

Suggested citation for this article: Hassan HK, Bolcen S, Kubofcik J, Nutman TB, Eberhard ML, Middleton K, et al. Isolation of Onchocerca lupi in dogs and black flies, California, USA. Emerg Infect Dis [Internet]. 2015 May [date cited]. http://dx.doi.org/10.3201/eid2105.142011
DOI: 10.3201/eid2105.142011
1These authors contributed equally to this article.
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