3. Results and Discussion
Our report represents the first unequivocally autochthonous case ofO. lupi , an agent of zoonotic onchocerciasis, in Texas, near the United States/Mexico border based on integrated histopathological, parasitological and molecular data.
Histologically, the most significant finding was the presence of corneal perforation with severe keratitis and anterior iris synechiae. Additionally, two long, filarioid nematodes were discovered embedded in the episcleral tissues. One of these parasites was degenerated and surrounded by granulomatous inflammation, while the other was intact and lacked surrounding inflammation. This specimen was a gravid, female nematode, suggesting a patent infection. The pattern of cuticular ridges of two inner striae within the space between two outer cuticular ridges observed on the specimens were morphologically consistent with O. lupi (Verocai et al., 2016) (Figure 1). Most likely, the dog was co-infected with heartworm, D. immitis , as a recent study, has shown that O. lupi infections are unlikely to generate false-positive results in commercial heartworm antigen tests (Sobotyk Oliveira, Savadelis, McLean, & Verocai, 2020).
The generated cox1 sequence was accessioned in GenBank (MW577256), and showed 99.9 – 100% maximum identity with O. lupi sequences available in GenBank. Phylogenetic analysis clustered the Texas isolate with all previous isolates from North America, and some European isolates, belonging to O. lupi “genotype 1” (99% bootstrap support; Figure 2) (Rojas, Salant, Yasur-Landau, Tsarfati, & Baneth, 2020).
Zoonotic onchocerciasis has been previously reported from a 10-year-old boy from Mission, Texas also in the Hidalgo County, who traveled to South Dakota, and slept in tents and cabins in New Mexico and Colorado, reported fishing in fresh water lakes near home, and had a pet dog with history of conjunctivitis and eye lesion of unknown etiology (Cantey et al., 2016). Altogether, the present canine case may suggest that this human infection may have been, in fact, acquired in Texas.
It is necessary to better understand the epidemiology of O. lupiin this newly recognized endemic area by screening dogs and cats from shelters using classical and molecular methods. In addition to companion animals and humans, coyotes (Canis latrans ) were reported infected and may serve as wild reservoirs in the western United States (Roe et al., 2020), and may also contribute to the epidemiology ofO. lupi in southern Texas, and neighboring Mexico. Other wild carnivores that are known or have postulated as O. lupi hosts such as wolves (Canis lupus ) and certain foxes (red fox,Vulpes vulpes ; swift fox, Vulpes velox ; kit fox,Vulpes macrotis ) are not present in southern Texas. However, the widely distributed gray fox (Urocyon cinereoargenteus ), is reported in this region, and across O. lupi endemic areas in North America, and therefore, should be assessed as potential reservoir host. Regarding the dipteran vectors, black flies (Simuliidae) have been considered the putative intermediate host for O. lupi (Hassan et al., 2015); however, biological confirmation remains necessary. Therefore, xenomonitoring in Texas could also involve screening of other dipterans, such as biting midges (Ceratopogonidae: Culicoides ) and sand flies (Psychodidae: Phlebotominae).
This unequivocal autochthonous O. lupi case in southern Texas suggests that this parasite is endemic to the region, and transmission may occur locally. In this case, it is postulated that O. lupicould have caused exophthalmos with secondary traumatic corneal ulceration and subsequent perforation. There is a need for epidemiological surveillance of companion animals, wildlife, and dipteran vectors along the United States/Mexico border. It is important to raise awareness of public health and medical specialists and authorities as humans in this region might be at risk of infection.