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Ocular Onchocerca infections in two dogs in western United States
Veterinary Parasitology 90 (2000) 333–338
Short communication
Ocular Onchocerca infections in two dogs in western United States Mark L. Eberhard a,∗ , Ynes Ortega b , Sharon Dial c , Chris A. Schiller c , Alson W. Sears d , Ellis Greiner e a
e
Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Public Health Service, US Department of Health and Human Services, Atlanta, GA 30341-3724, USA b Veterinary Sciences Department, University of Arizona, Tucson, AZ, USA c ANTECH Diagnostics, Phoenix, AZ, USA d Sears Veterinary Hospital, Lancaster, CA, USA Department of Pathobiology, College of Veterinary Medicine, University of Florida, Gainesville, FL, USA Received 6 January 2000; accepted 30 March 2000
Abstract Two dogs, one from California and one from Arizona, were found to have aberrant infections caused by filarial nematodes of the genus Onchocerca. In both cases, the parasites are localized in or near the eye. In one case the worm was located in the cornea and was surgically removed. In the second case, a very marked granulomatous reaction was induced in the retrobulbar space, mimicking an abscess. This eye was enucleated. The worms in both instances were female, and were gravid, i.e. contained microfilariae in utero, indicating that a male worm(s) had been present and mating had occurred. The exact identity of the species of Onchocerca responsible cannot be determined, although the features observed are most like Onchocerca lienalis of cattle. These cases represent the fourth and fifth such cases reported from the US, and are especially interesting because of the unusual location of the worms, the small number of recognized cases, and the similarity to a recent zoonotic human infection. Published by Elsevier Science B.V. Keywords: Dog; Onchocercosis; Eye; Pathology
1. Introduction Various species of Onchocerca are common filarial infections in horses, cattle, and related ungulates. Several species, including Onchocerca gutturosa, Onchocerca lienalis, and ∗ Corresponding author. Tel.: +1-770-488-4419; fax: +1-770-488-4253. E-mail address: [email protected] (M.L. Eberhard)
0304-4017/00/$ – see front matter Published by Elsevier Science B.V. PII: S 0 3 0 4 - 4 0 1 7 ( 0 0 ) 0 0 2 5 2 - 1
334
M.L. Eberhard et al. / Veterinary Parasitology 90 (2000) 333–338
Onchocerca stilesi are known to occur in cattle in the US and Canada, while Onchocerca cervicalis has been reported from horses (Beaver et al., 1974; Eberhard, 1979; Levine, 1980). Although much more commonly reported in the eastern US, bovine and equine onchocercosis have been reported in the western US (Stannard and Cello, 1975; Munson et al., 1978; Polley, 1984). There are also occasional reports of Onchocerca infections in wild ungulates in North America, the most notable is Onchocerca cervipedis of deer (Wehr and Dickmans, 1935; Herman and Bischoff, 1946; Weinman et al., 1973). Dogs and other canids are not recognized to be natural hosts for any species of Onchocerca. However, in 1991, a dog in the Los Angeles, CA area was found to have an aberrant Onchocerca infection associated with the orbital fascia and eyelid (Orihel et al., 1991) and in 1993, two additional cases of Onchocerca were recognized in dogs, one from the Los Angeles, CA area and one from Utah (Gardiner et al., 1993). In both instances, the worms were associated with granulomatous nodules of the palpebral conjunctiva, third palpebra, and sclera. There are also three published reports of zoonotic Onchocerca infections in humans in the US and Canada, one of which involved the eye (Beaver et al., 1974; Ali-Khan, 1977; Burr et al., 1998). The zoonotic human infections and those aberrant infections in dogs were presumably the result of the bite by an insect vector harboring infective larvae of one of the aforementioned domestic animal species, but they could represent infection with unrecognized species naturally occurring in wild animals. This report describes two additional cases of unusual Onchocerca infections in dogs from the western US. 1.1. Case 1 An adult male Boxer-mix (dog 1) was observed at a veterinary clinic in Phoenix, Arizona because of acute erythema and swelling of the eye. The dog had spent its entire life in the Yuma, Arizona area. Examination revealed the presence of a living worm in the cornea. Under local anesthesia, a small incision was made and the worm extracted. A portion of the worm was available for detailed study. No information is available about either the use of heartworm prophylaxis or serologic status on this dog. The portion of specimen available for study was approximately 1 cm in length and had a maximum diameter of approximately 275 m. Neither the anterior nor posterior end of the worm was present. The portion of worm examined appeared to come from about the mid-body. The two features of the worm that were most prominent included the distinctive cuticle and the fact that the worm was gravid and contained microfilariae in utero. The cuticle had an outer layer composed of distinct ridges and an inner layer composed of striae; there were two striae per ridge, i.e. one under each ridge and one between adjacent ridges (Fig. 1A and B). The ridges were spaced about 25 m apart, they were relatively low about 2 m in height, and rounded in shape. The striae were prominent, thinner near the anterior end, and broader more posteriorly in the worm, and measured about 5–7 m thick and 10–12 m in length. In most areas, the cuticle measured 12–14 m in total thickness, although in some areas it measured up to 20 m in thickness. The second feature, as noted, was that developing microfilariae were present in the uteri (Fig. 1C), indicating that a male worm had been present and that mating had occurred.
M.L. Eberhard et al. / Veterinary Parasitology 90 (2000) 333–338
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Fig. 1. Onchocerca species recovered from the cornea of the eye of a dog in Arizona. (A) Longitudinal section of cuticle illustrating the outer cuticular ridges and inner cuticular striae. Scale bar=25 m; (B) longitudinal section of cuticle illustrating outer ridges and inner striae in a more posterior region of the worm. Scale bar=25 m; (C) photomicrograph of the middle region of the worm illustrating in utero microfilariae. Scale bar=25 m.
Based on the morphologic features of the worm, primarily the structure of the cuticle, the specimen most resembles O. lienalis from cattle (Beaver et al., 1974; Eberhard, 1979). 1.2. Case 2 A 1-year-old female Boston terrier (dog 2) was examined at a veterinary clinic in Lancaster, CA because of a mass in the retrobulbar space of the right eye. The dog had spent all of its life in the Lancaster area. A presumptive diagnosis of retrobulbar abscess was made and the eye enucleated. The dog had never been on heartworm preventative, and at the time of surgery, preoperative examination included a heartworm antigen test, which was negative. Histologic sections of the mass revealed a coiled, adult, gravid female filarial parasite (Fig. 2A). Six to eight sections of a single worm were present, including transverse and tangential sections. In transverse section (Fig. 2B) the worm measured between 260 and 300 m in maximum diameter. The cuticle was unevenly thick, measuring from 5–10 m in thickness, and had two distinct layers. Hypodermal tissue was not evident and the musculature was sparse and composed of wispy contractile elements. The worm was gravid as evidenced by the paired uteri full of microfilariae. A careful search of the surrounding tissue, including a small bit of skin contained in the sections, did not reveal any microfilariae except those in the uteri of the worm. In the tangential sections of worm, the presence of external ridges was noted (Fig. 2C). The ridges were rather low, measuring approximately 2 m in height, rounded in shape, and varied between 65 and 95 m apart. However, because of the tangential nature of the sections, the actual distance between ridges was exaggerated. The inner layer of the cuticle was composed of striae, but these were not clearly visible, and the number per ridge could not be determined. There appeared to be two ridges per striae — one under and one between adjacent ridges. Based on the morphologic features of the cuticle, the worm was identified as an Onchocerca species. The size, shape, and configuration of the ridges and striae suggested that this worm was also O. lienalis.
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M.L. Eberhard et al. / Veterinary Parasitology 90 (2000) 333–338
Fig. 2. Onchocerca species recovered from a granulomatous, retrobulbar lesion in the eye of a dog in California. (A) Panoramic view of the lesion and several sections of coiled worm. Scale bar=430 m; (B) transverse section of the worm, illustrating the degenerate state of the worm, paired uteri and thin cuticle. Scale bar=50 m; (C) high power magnification of the cuticle, in longitudinal section, illustrating the outer ridges and inner striae. Scale bar=25 m.
2. Discussion The parasites found in these two dogs clearly belong in the genus Onchocerca, and morphologically, are very similar to the previously described cases (Orihel et al., 1991; Gardiner et al., 1993). Interestingly, the infections in these five dogs were all localized in or near the eye and seem to represent the same species of parasite, all have occurred in the western US. Whether these infections can be attributed to O. lienalis, or possibly O. stilesi, both parasites of cattle that have low ridges and typically two striae per ridge (O. stilesi can have two or three striae per ridge) cannot be stated unequivocally. They definitely do not represent species such as O. gutturosa of cattle or O. cervicalis of horses, both of which have prominent ridges and more numerous striae (four to five) per ridge (Beaver et al., 1974; Eberhard, 1979). The overall cuticle thickness of the latter two later species is also much greater. Another possibility that cannot be excluded is that the Onchocerca spp. in these canine infections represent a species normally infecting some wildlife host, such as deer, elk, big horn sheep, or other ungulate. Deer, moose and reindeer in Europe are infected with a number of species of Onchocerca (Bain and Schulz-Key, 1974; Bain et al., 1979; Bain and Rehbinder, 1986). Whether these infections occur in North America is unknown, but a single species, O. cervipedis, is recognized to be a common infection in deer in the western US (Wehr and Dickmans, 1935; Herman and Bischoff, 1946; Weinman et al., 1973). The description given for the cuticle of O. cervipedis does not match that reported for the worms recovered from dogs. It would seem that further study of the parasites of wildlife may be needed to clarify whether or not the parasite found in dogs is caused by an Onchocerca spp. of domestic or wild ungulates. It is particularly noteworthy that three zoonotic Onchocerca infections have been reported in humans from North America, including a recent case in a resident of Colorado (Burr
M.L. Eberhard et al. / Veterinary Parasitology 90 (2000) 333–338
337
et al., 1998). In that case, a female worm was removed from the cornea, much as in dog 1 of the present report. The species of worm recovered from the human cases in the US and Canada could not be established definitively; however, the cuticle in those cases was much thicker, had very prominent cuticular ridges, and bore four to five striae per ridge, making them clearly distinct from the species reported in dogs. The zoonotic species infecting humans, therefore, is not the same species as the parasite causing aberrant infections in dogs. Why these accidental Onchocerca infections seem to localize in the eye of dogs is puzzling. Onchocerca infections, as adult stages in their natural hosts, are not recognized to typically or preferentially localize in or near the eye. It may be that masses on or around the eye, or the presence of a worm within the eye, gain a lot of attention from both dog owners and veterinarians whereas localization of small granulomatous masses elsewhere in the body could easily go unrecognized or ignored, especially if these tended to resolve on their own over time. Both previous reports of Onchocerca infections in dogs remarked about the possibility of establishing experimental Onchocerca infections in dogs. This, of course, would represent a significant breakthrough in onchocercosis research. As a direct result of the recognition of the first case of Onchocerca being recovered from dogs, a specific study to address the potential of dogs to serve as experimental models was undertaken. Three groups of three dogs each were inoculated with infective larvae of Onchocerca volvulus (human origin), O. lienalis (cattle origin) or O. cervicalis (horse origin). All of the animals were observed for 15 months, skin snips from various sites on the body were obtained beginning at 7 months postinoculation. Careful examination of the eye, socket, and orbit were conducted monthly. At the end of the study, a complete necropsy was performed on all dogs, with particular attention to searching for adult worms and/or nodules, not only around the eye but also elsewhere in the body. No evidence of infection could be documented in any of the inoculated dogs (M. Eberhard, D. Abraham, J. Lok, unpublished data). These results emphasize our very meager understanding of what the overriding host factors are that account for zoonotic infections in humans or aberrant infections in animals. At the very least, we now recognize at least five cases of unusual Onchocerca infection in dogs, all being localized in or around the eye and occurring in the western US. A report of an Onchocerca infection under the sclera of the eye of a wolf in Russia bears mentioning. The parasite was given the name, Onchocerca lupi (Rodonaja, 1967) but the taxonomic validity has not been accepted (Muller, 1979). Based on the descriptions provided (Rodonaja, 1967; Demiaszkiewicz and Matsaberidze, 1991), the cuticular morphology of O. lupi is similar to that seen in the five cases reported from dogs in the US. It is likely that the same species of parasite may be responsible for all of these infections in canids, but the evidence is still strong that this is not a natural infection of canids, but rather, as stated before, represents an unusual infection acquired from an intermediate host that fed on some other animal living in the same area. If the parasite in question is indeed O. lienalis of cattle, the distribution of that species in the US is widespread and not restricted to the western states. Therefore, clinicians in other areas of the US should be alert to the possibility of Onchocerca infections in dogs and consider this in the differential diagnosis of ocular or periocular nodules in dogs, and possibly other companion animals.
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M.L. Eberhard et al. / Veterinary Parasitology 90 (2000) 333–338
References Ali-Khan, Z., 1977. Tissue pathology and comparative microanatomy of Onchocerca from a resident of Ontario and other enzootic Onchocerca species from Canada and the USA. Ann. Trop. Med. Parasitol. 71, 469–482. Bain, O., Rehbinder, C., 1986. Onchocerca alcis n. sp., parasite of the moose Alces alces in Sweden. Ann. Parasitol. 61, 447–455. Bain, O., Schulz-Key, H., 1974. The species of Onchocerca in the red deer: redescription of O. flexuosa (Wedl, 1856) and description of O. tubingensis sp. n. and O. tarsicola n. sp. Trop. Parasitol. 25, 437–449. Bain, O., Rehbinder, C., Perry, G., 1979. Occurrence of Onchocerca tarsicola Bain and Schulz-Key, 1974, in reindeer. Ann. Parasitol. 54, 263–265. Beaver, P.C., Horner, G.S., Bilos, J.Z., 1974. Zoonotic onchocerciasis in a resident of Illinois and observations on the identification of Onchocerca species. Am. J. Trop. Med. Hyg. 23, 595–607. Burr, W.E., Brown, M.F., Eberhard, M.L., 1998. Zoonotic Onchocerca (Nematoda: Filarioidea) in the cornea of a Colorado resident. Ophthalmology 105, 1494–1497. Demiaszkiewicz, A.W., Matsaberidze, G.V., 1991. New details on the morphology of Onchocerca lupi. Wiad. Parazytol. 37, 255–259 (in Polish). Eberhard, M.L., 1979. Studies on the Onchocerca (Nematoda: Filarioidea) found in cattle in the United States. 1. Systematic of O. gutturosa and O. lienalis with a description of O. stilesi sp. n. J. Parasitol. 65, 379–388. Gardiner, C.H., Dick, E.J., Meininger, A.C., Lozano-Alarcon, F., Jackson, P., 1993. Onchocerciasis in two dogs. J.A.V.M.A. 203, 828–830. Herman, C.M., Bischoff, A.I., 1946. The foot worm parasite of deer. California Fish and Game 32, 182–190. Levine, N.D., 1980. Nematode Parasites of Domestic Animals and Man, 2nd Edition. Burgess Publishing Co., Minneapolis, pp. 344–409. Muller, R., 1979, Identification of Onchocerca. Problems in the identification of parasites and their vectors. In: Proceedings of the 17th Symposium of the British Society for Parasitology, Blackwell Scientific Publications, Oxford, pp. 175–206. Munson, A.H., Archer, J.N., Dyer, J.E., 1978. Bovine onchocerciasis in Mountain and Pacific states. Am. J. Vet. Res. 39, 1073–1074. Orihel, T.C., Ash, L.R., Holshuh, H.J., Santenelli, S., 1991. Onchocerciasis in a California dog. Am. J. Trop. Med. Hyg. 44, 513–517. Polley, L., 1984. Onchocerca in horses from western Canada and northwestern US: an abattoir survey of the prevalence of infection. Can. Vet. J. 25, 128–129. Rodonaja, T.E., 1967. A new species of nematode, Onchocerca lupi sp. nov., from Canis lupus cubanensis. Soobshcheniya Akademii Nauk, Gruzinksaya S.S.R., Vol. 45, pp. 715–719 (in Russian). Stannard, A.A., Cello, R.M., 1975. Onchocerca cervicalis infection in horses from the western United States. Am. J. Vet. Res. 36, 1029–1031. Wehr, E.E., Dickmans, G., 1935. New nematodes (Filariidae) from North America ruminants. Zoologischer Anzeiger 110, 202–208. Weinman, C.J., Anderson, J.R., Longhurst, W.M., Connolly, G., 1973. Filarial worms of Columbian black-tailed deer in California. 1. Observations in the vertebrate host. J. Wildlife Dis. 9, 213–220.
Short communication
Ocular Onchocerca infections in two dogs in western United States Mark L. Eberhard a,∗ , Ynes Ortega b , Sharon Dial c , Chris A. Schiller c , Alson W. Sears d , Ellis Greiner e a
e
Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Public Health Service, US Department of Health and Human Services, Atlanta, GA 30341-3724, USA b Veterinary Sciences Department, University of Arizona, Tucson, AZ, USA c ANTECH Diagnostics, Phoenix, AZ, USA d Sears Veterinary Hospital, Lancaster, CA, USA Department of Pathobiology, College of Veterinary Medicine, University of Florida, Gainesville, FL, USA Received 6 January 2000; accepted 30 March 2000
Abstract Two dogs, one from California and one from Arizona, were found to have aberrant infections caused by filarial nematodes of the genus Onchocerca. In both cases, the parasites are localized in or near the eye. In one case the worm was located in the cornea and was surgically removed. In the second case, a very marked granulomatous reaction was induced in the retrobulbar space, mimicking an abscess. This eye was enucleated. The worms in both instances were female, and were gravid, i.e. contained microfilariae in utero, indicating that a male worm(s) had been present and mating had occurred. The exact identity of the species of Onchocerca responsible cannot be determined, although the features observed are most like Onchocerca lienalis of cattle. These cases represent the fourth and fifth such cases reported from the US, and are especially interesting because of the unusual location of the worms, the small number of recognized cases, and the similarity to a recent zoonotic human infection. Published by Elsevier Science B.V. Keywords: Dog; Onchocercosis; Eye; Pathology
1. Introduction Various species of Onchocerca are common filarial infections in horses, cattle, and related ungulates. Several species, including Onchocerca gutturosa, Onchocerca lienalis, and ∗ Corresponding author. Tel.: +1-770-488-4419; fax: +1-770-488-4253. E-mail address: [email protected] (M.L. Eberhard)
0304-4017/00/$ – see front matter Published by Elsevier Science B.V. PII: S 0 3 0 4 - 4 0 1 7 ( 0 0 ) 0 0 2 5 2 - 1
334
M.L. Eberhard et al. / Veterinary Parasitology 90 (2000) 333–338
Onchocerca stilesi are known to occur in cattle in the US and Canada, while Onchocerca cervicalis has been reported from horses (Beaver et al., 1974; Eberhard, 1979; Levine, 1980). Although much more commonly reported in the eastern US, bovine and equine onchocercosis have been reported in the western US (Stannard and Cello, 1975; Munson et al., 1978; Polley, 1984). There are also occasional reports of Onchocerca infections in wild ungulates in North America, the most notable is Onchocerca cervipedis of deer (Wehr and Dickmans, 1935; Herman and Bischoff, 1946; Weinman et al., 1973). Dogs and other canids are not recognized to be natural hosts for any species of Onchocerca. However, in 1991, a dog in the Los Angeles, CA area was found to have an aberrant Onchocerca infection associated with the orbital fascia and eyelid (Orihel et al., 1991) and in 1993, two additional cases of Onchocerca were recognized in dogs, one from the Los Angeles, CA area and one from Utah (Gardiner et al., 1993). In both instances, the worms were associated with granulomatous nodules of the palpebral conjunctiva, third palpebra, and sclera. There are also three published reports of zoonotic Onchocerca infections in humans in the US and Canada, one of which involved the eye (Beaver et al., 1974; Ali-Khan, 1977; Burr et al., 1998). The zoonotic human infections and those aberrant infections in dogs were presumably the result of the bite by an insect vector harboring infective larvae of one of the aforementioned domestic animal species, but they could represent infection with unrecognized species naturally occurring in wild animals. This report describes two additional cases of unusual Onchocerca infections in dogs from the western US. 1.1. Case 1 An adult male Boxer-mix (dog 1) was observed at a veterinary clinic in Phoenix, Arizona because of acute erythema and swelling of the eye. The dog had spent its entire life in the Yuma, Arizona area. Examination revealed the presence of a living worm in the cornea. Under local anesthesia, a small incision was made and the worm extracted. A portion of the worm was available for detailed study. No information is available about either the use of heartworm prophylaxis or serologic status on this dog. The portion of specimen available for study was approximately 1 cm in length and had a maximum diameter of approximately 275 m. Neither the anterior nor posterior end of the worm was present. The portion of worm examined appeared to come from about the mid-body. The two features of the worm that were most prominent included the distinctive cuticle and the fact that the worm was gravid and contained microfilariae in utero. The cuticle had an outer layer composed of distinct ridges and an inner layer composed of striae; there were two striae per ridge, i.e. one under each ridge and one between adjacent ridges (Fig. 1A and B). The ridges were spaced about 25 m apart, they were relatively low about 2 m in height, and rounded in shape. The striae were prominent, thinner near the anterior end, and broader more posteriorly in the worm, and measured about 5–7 m thick and 10–12 m in length. In most areas, the cuticle measured 12–14 m in total thickness, although in some areas it measured up to 20 m in thickness. The second feature, as noted, was that developing microfilariae were present in the uteri (Fig. 1C), indicating that a male worm had been present and that mating had occurred.
M.L. Eberhard et al. / Veterinary Parasitology 90 (2000) 333–338
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Fig. 1. Onchocerca species recovered from the cornea of the eye of a dog in Arizona. (A) Longitudinal section of cuticle illustrating the outer cuticular ridges and inner cuticular striae. Scale bar=25 m; (B) longitudinal section of cuticle illustrating outer ridges and inner striae in a more posterior region of the worm. Scale bar=25 m; (C) photomicrograph of the middle region of the worm illustrating in utero microfilariae. Scale bar=25 m.
Based on the morphologic features of the worm, primarily the structure of the cuticle, the specimen most resembles O. lienalis from cattle (Beaver et al., 1974; Eberhard, 1979). 1.2. Case 2 A 1-year-old female Boston terrier (dog 2) was examined at a veterinary clinic in Lancaster, CA because of a mass in the retrobulbar space of the right eye. The dog had spent all of its life in the Lancaster area. A presumptive diagnosis of retrobulbar abscess was made and the eye enucleated. The dog had never been on heartworm preventative, and at the time of surgery, preoperative examination included a heartworm antigen test, which was negative. Histologic sections of the mass revealed a coiled, adult, gravid female filarial parasite (Fig. 2A). Six to eight sections of a single worm were present, including transverse and tangential sections. In transverse section (Fig. 2B) the worm measured between 260 and 300 m in maximum diameter. The cuticle was unevenly thick, measuring from 5–10 m in thickness, and had two distinct layers. Hypodermal tissue was not evident and the musculature was sparse and composed of wispy contractile elements. The worm was gravid as evidenced by the paired uteri full of microfilariae. A careful search of the surrounding tissue, including a small bit of skin contained in the sections, did not reveal any microfilariae except those in the uteri of the worm. In the tangential sections of worm, the presence of external ridges was noted (Fig. 2C). The ridges were rather low, measuring approximately 2 m in height, rounded in shape, and varied between 65 and 95 m apart. However, because of the tangential nature of the sections, the actual distance between ridges was exaggerated. The inner layer of the cuticle was composed of striae, but these were not clearly visible, and the number per ridge could not be determined. There appeared to be two ridges per striae — one under and one between adjacent ridges. Based on the morphologic features of the cuticle, the worm was identified as an Onchocerca species. The size, shape, and configuration of the ridges and striae suggested that this worm was also O. lienalis.
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M.L. Eberhard et al. / Veterinary Parasitology 90 (2000) 333–338
Fig. 2. Onchocerca species recovered from a granulomatous, retrobulbar lesion in the eye of a dog in California. (A) Panoramic view of the lesion and several sections of coiled worm. Scale bar=430 m; (B) transverse section of the worm, illustrating the degenerate state of the worm, paired uteri and thin cuticle. Scale bar=50 m; (C) high power magnification of the cuticle, in longitudinal section, illustrating the outer ridges and inner striae. Scale bar=25 m.
2. Discussion The parasites found in these two dogs clearly belong in the genus Onchocerca, and morphologically, are very similar to the previously described cases (Orihel et al., 1991; Gardiner et al., 1993). Interestingly, the infections in these five dogs were all localized in or near the eye and seem to represent the same species of parasite, all have occurred in the western US. Whether these infections can be attributed to O. lienalis, or possibly O. stilesi, both parasites of cattle that have low ridges and typically two striae per ridge (O. stilesi can have two or three striae per ridge) cannot be stated unequivocally. They definitely do not represent species such as O. gutturosa of cattle or O. cervicalis of horses, both of which have prominent ridges and more numerous striae (four to five) per ridge (Beaver et al., 1974; Eberhard, 1979). The overall cuticle thickness of the latter two later species is also much greater. Another possibility that cannot be excluded is that the Onchocerca spp. in these canine infections represent a species normally infecting some wildlife host, such as deer, elk, big horn sheep, or other ungulate. Deer, moose and reindeer in Europe are infected with a number of species of Onchocerca (Bain and Schulz-Key, 1974; Bain et al., 1979; Bain and Rehbinder, 1986). Whether these infections occur in North America is unknown, but a single species, O. cervipedis, is recognized to be a common infection in deer in the western US (Wehr and Dickmans, 1935; Herman and Bischoff, 1946; Weinman et al., 1973). The description given for the cuticle of O. cervipedis does not match that reported for the worms recovered from dogs. It would seem that further study of the parasites of wildlife may be needed to clarify whether or not the parasite found in dogs is caused by an Onchocerca spp. of domestic or wild ungulates. It is particularly noteworthy that three zoonotic Onchocerca infections have been reported in humans from North America, including a recent case in a resident of Colorado (Burr
M.L. Eberhard et al. / Veterinary Parasitology 90 (2000) 333–338
337
et al., 1998). In that case, a female worm was removed from the cornea, much as in dog 1 of the present report. The species of worm recovered from the human cases in the US and Canada could not be established definitively; however, the cuticle in those cases was much thicker, had very prominent cuticular ridges, and bore four to five striae per ridge, making them clearly distinct from the species reported in dogs. The zoonotic species infecting humans, therefore, is not the same species as the parasite causing aberrant infections in dogs. Why these accidental Onchocerca infections seem to localize in the eye of dogs is puzzling. Onchocerca infections, as adult stages in their natural hosts, are not recognized to typically or preferentially localize in or near the eye. It may be that masses on or around the eye, or the presence of a worm within the eye, gain a lot of attention from both dog owners and veterinarians whereas localization of small granulomatous masses elsewhere in the body could easily go unrecognized or ignored, especially if these tended to resolve on their own over time. Both previous reports of Onchocerca infections in dogs remarked about the possibility of establishing experimental Onchocerca infections in dogs. This, of course, would represent a significant breakthrough in onchocercosis research. As a direct result of the recognition of the first case of Onchocerca being recovered from dogs, a specific study to address the potential of dogs to serve as experimental models was undertaken. Three groups of three dogs each were inoculated with infective larvae of Onchocerca volvulus (human origin), O. lienalis (cattle origin) or O. cervicalis (horse origin). All of the animals were observed for 15 months, skin snips from various sites on the body were obtained beginning at 7 months postinoculation. Careful examination of the eye, socket, and orbit were conducted monthly. At the end of the study, a complete necropsy was performed on all dogs, with particular attention to searching for adult worms and/or nodules, not only around the eye but also elsewhere in the body. No evidence of infection could be documented in any of the inoculated dogs (M. Eberhard, D. Abraham, J. Lok, unpublished data). These results emphasize our very meager understanding of what the overriding host factors are that account for zoonotic infections in humans or aberrant infections in animals. At the very least, we now recognize at least five cases of unusual Onchocerca infection in dogs, all being localized in or around the eye and occurring in the western US. A report of an Onchocerca infection under the sclera of the eye of a wolf in Russia bears mentioning. The parasite was given the name, Onchocerca lupi (Rodonaja, 1967) but the taxonomic validity has not been accepted (Muller, 1979). Based on the descriptions provided (Rodonaja, 1967; Demiaszkiewicz and Matsaberidze, 1991), the cuticular morphology of O. lupi is similar to that seen in the five cases reported from dogs in the US. It is likely that the same species of parasite may be responsible for all of these infections in canids, but the evidence is still strong that this is not a natural infection of canids, but rather, as stated before, represents an unusual infection acquired from an intermediate host that fed on some other animal living in the same area. If the parasite in question is indeed O. lienalis of cattle, the distribution of that species in the US is widespread and not restricted to the western states. Therefore, clinicians in other areas of the US should be alert to the possibility of Onchocerca infections in dogs and consider this in the differential diagnosis of ocular or periocular nodules in dogs, and possibly other companion animals.
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References Ali-Khan, Z., 1977. Tissue pathology and comparative microanatomy of Onchocerca from a resident of Ontario and other enzootic Onchocerca species from Canada and the USA. Ann. Trop. Med. Parasitol. 71, 469–482. Bain, O., Rehbinder, C., 1986. Onchocerca alcis n. sp., parasite of the moose Alces alces in Sweden. Ann. Parasitol. 61, 447–455. Bain, O., Schulz-Key, H., 1974. The species of Onchocerca in the red deer: redescription of O. flexuosa (Wedl, 1856) and description of O. tubingensis sp. n. and O. tarsicola n. sp. Trop. Parasitol. 25, 437–449. Bain, O., Rehbinder, C., Perry, G., 1979. Occurrence of Onchocerca tarsicola Bain and Schulz-Key, 1974, in reindeer. Ann. Parasitol. 54, 263–265. Beaver, P.C., Horner, G.S., Bilos, J.Z., 1974. Zoonotic onchocerciasis in a resident of Illinois and observations on the identification of Onchocerca species. Am. J. Trop. Med. Hyg. 23, 595–607. Burr, W.E., Brown, M.F., Eberhard, M.L., 1998. Zoonotic Onchocerca (Nematoda: Filarioidea) in the cornea of a Colorado resident. Ophthalmology 105, 1494–1497. Demiaszkiewicz, A.W., Matsaberidze, G.V., 1991. New details on the morphology of Onchocerca lupi. Wiad. Parazytol. 37, 255–259 (in Polish). Eberhard, M.L., 1979. Studies on the Onchocerca (Nematoda: Filarioidea) found in cattle in the United States. 1. Systematic of O. gutturosa and O. lienalis with a description of O. stilesi sp. n. J. Parasitol. 65, 379–388. Gardiner, C.H., Dick, E.J., Meininger, A.C., Lozano-Alarcon, F., Jackson, P., 1993. Onchocerciasis in two dogs. J.A.V.M.A. 203, 828–830. Herman, C.M., Bischoff, A.I., 1946. The foot worm parasite of deer. California Fish and Game 32, 182–190. Levine, N.D., 1980. Nematode Parasites of Domestic Animals and Man, 2nd Edition. Burgess Publishing Co., Minneapolis, pp. 344–409. Muller, R., 1979, Identification of Onchocerca. Problems in the identification of parasites and their vectors. In: Proceedings of the 17th Symposium of the British Society for Parasitology, Blackwell Scientific Publications, Oxford, pp. 175–206. Munson, A.H., Archer, J.N., Dyer, J.E., 1978. Bovine onchocerciasis in Mountain and Pacific states. Am. J. Vet. Res. 39, 1073–1074. Orihel, T.C., Ash, L.R., Holshuh, H.J., Santenelli, S., 1991. Onchocerciasis in a California dog. Am. J. Trop. Med. Hyg. 44, 513–517. Polley, L., 1984. Onchocerca in horses from western Canada and northwestern US: an abattoir survey of the prevalence of infection. Can. Vet. J. 25, 128–129. Rodonaja, T.E., 1967. A new species of nematode, Onchocerca lupi sp. nov., from Canis lupus cubanensis. Soobshcheniya Akademii Nauk, Gruzinksaya S.S.R., Vol. 45, pp. 715–719 (in Russian). Stannard, A.A., Cello, R.M., 1975. Onchocerca cervicalis infection in horses from the western United States. Am. J. Vet. Res. 36, 1029–1031. Wehr, E.E., Dickmans, G., 1935. New nematodes (Filariidae) from North America ruminants. Zoologischer Anzeiger 110, 202–208. Weinman, C.J., Anderson, J.R., Longhurst, W.M., Connolly, G., 1973. Filarial worms of Columbian black-tailed deer in California. 1. Observations in the vertebrate host. J. Wildlife Dis. 9, 213–220.