Notes on two species of Filaroides (Nematoda: Filaroididae) from carnivores in Texas, DB Pence

Tags: nematodes, Texas, nodules, hog-nosed skunk, spicules, bronchi, plasma cells, osleri, Filaroides mephitis Webster, host-parasite relationships, Conepatus mesoleucus, Filaroides milksi Whitlock, Metastrongyloidea, Filaroides, trachea, eosinophils, Museum of Texas Tech University, J. Zool, Filaroides Van Beneden, type specimens, species, Filaroides hirthi Georgi, Filaroides osleri, interstitial pneumonia, Texas Tech University Health Sciences Centers, bronchioles, granulomatous reaction, J. Parasitol, Cornell Vet, parenchyma, Helminthological Society, R. C. Anderson, Washington, Mephitis mephitis
Notes on Two Species of Filaroides (Nematoda: Filaroididae) from Carnivores in Texas DANNY B. PENCE Department of Pathology, Division of Comparative Pathology, Texas Tech University Health Sciences Centers, Lubbock, Texas 79409 ABSTRACT: The pathology and host-parasite relationships of two species of the genus Filaroides from west Texas carnivores are discussed. These are Filaroides milksi Whitlock, 1956 from the lungs of the hog-nosed skunk, Conepatus mesoleucus, and Filaroides osleri (Cobbold, 1879) Skrjabin, 1933 from the trachea and bronchi of the coyote, Cam's latrans. The lungs of the hog-nosed skunk infected with F. milksi were extremely congested, and there was a severe interstitial pneumonia surrounding numerous granulomatous foci containing adult and larval nematodes. This species is briefly redescribed from the hog-nosed skunk, which represents a new host record. Filaroides mephitis Webster, 1966 is considered a synonym of F. milksi. Also, the validity of Filaroides hirthi Georgi and and Anderson, 1975 is suspect. Filaroides osleri in the coyote presented as a mild to severe verminous bronchitis. Infections ranged from a small pinpoint nodule at the tracheal bifurcation to many large nodular lesions extending from the proximal % of the trachea into the anterior bronchi. Cellular reactions consisting of epithelioid cells, histiocytes, and a few eosinophils surrounded the entwined nematodes. A mild interstitial pneumonia and, in one instance, small parenchymal granulomas surrounding immature worms were observed in the lungs of some infected animals.
Studies on the helminth fauna of west Texas carnivorous mammals revealed infections in the coyote, Canis latrans, and hog-nosed skunk, Conepatus mesoleucus, with Filaroides osleri (Cobbold, 1879) Skrjabin, 1933 and Filaroides milksi Whitlock, 1956, respectively. The pathology, host-parasite relationships, and taxonomy of these species from their respective hosts are discussed. Materials and Methods Animals were routinely necropsied; nematodes removed and fixed in glacial acetic acid, and preserved in a mixture of 70% ethyl alcohol and 5% glycerine by volume. One cm square portions of lung parenchyma and small pieces of trachea from infected hosts were fixed in 10% buffered formalin. Sections were cut at 4-6 /x and stained with hematoxylin and eosin or Giemsa. In the following description all measurements are in microns unless otherwise indicated. Drawings were made with the aid of a Leitz drawing tube. Filaroides milksi Whitlock, 1956 NEW SYNONYMY: Filaroides mephitis Webster, 1966 (Can. J. Zool. 45: 145). DESCRIPTION (based on fragments of nu-
merous $ $ and 2 2 specimens): Filaroididae Schultz, 1951; Filaroides Van Beneden, 1858: long, slender, filiform nematodes. Cuticle smooth, without striations, very delicate, often detached from hypodermis. Buccal capsule very shallow, indistinct, not sclerotized. Four large papillae in outer circle, four smaller papillae in inner circle, amphids lateral. Esophagus muscular, simple. Excretory pore slightly posteriad to nerve ring. Posterior extremity of female with blunt tail, vulva close to anus without conspicuous vulvar inflation. Vagina muscular. Uteri paired, ovoviviparous, with hatched larvae. Male with very rudimentary bursa bearing two pairs large pedunculate, postanal papillae. Spicules similar, subequal, scimitar-shaped, without transverse striations, blunt-tipped (Fig. 1). Gubernaculum lightly sclerotized, % length of spicules. Eggs thin-shelled, with well-developed larvae. FEMALE (based on 10 specimens): One fragmented female 10.6 mm long, remaining specimens broken, total length undetermined. 82-94 (89) wide (maximum). Esophagus 122-140 (133) long. Nerve ring and excretory pore 65-88 (74) and 94-129 (109) from anterior extremity, respectively. Vulva and anus 76-82 (77) and 20-26 (23) from posterior extremity. Larvae 234-280 (254) long.
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Figures 1-3. Lateral and ventral views of spicule and gubernaculum from three described Filaroides species. 1. Filaroides milksi from Conepatus mesoleucus in Texas. 2. F. hirthi Georgi and Anderson, 1975 from beagle dog (Paratype, USNM Helm. Coll. No. 79243). 3. F. mephitis Webster, 1966 from Mephitis mephitis in Canada (USNM Helm. Coll. No. 61679). Copyright © 2011, The Helminthological Society of Washington
MALE (based on 10 specimens): One broken male 7.5 mm long, remainder of specimens fragmented, total length undetermined. 70-85 (79) wide (maximum). Esophagus 140-180 (153) long. Nerve ring and excretory pore 70-76 (73) and 94-123 (107) from anterior extremity, respectively. Cloacal opening 15-18 (17) from posterior extremity. Spicules 54-77 (65) long. Gubernaculum 1828 (23) long. HOSTS: Conepatus mesoleucus, hog-nosed skunk. One animal infected of six examined. LOCATION: Small bronchioles and parenchyma of lungs. LOCALITY: Six mi N, 16 mi W of Eden, Concho Co., Texas. Collected 11 November 1975 by M. Baird. DISPOSITION OF SPECIMENS: The Museum of Texas Tech University, Department of Medical Zoology, No. 1001 to 1025. PATHOLOGY: On necropsy, lungs were edematus, congested, not collapsed, and a mild pleuritis was evident. Hard, yellowish subpleural foci were evident in all lobes of the lungs. Blood and edema oozed from cut sections. Histologically, the entire parenchyma on all sections was extremely congested, edematous, and there was a severe interstitial pneumonia surrounding numerous granulomatous foci containing nematodes (Fig. 4). There was a perivasculitis of arterioles and veins and a perilymphangitis adjacent to these granulomas. This consisted predominately of lymphocytes and a few eosinophils. Adult and larval nematodes were predominantly localized in alveolar spaces and septa. Occasionally, they were found in terminal and secondary bronchioles. The granulomatous reaction consisted of epithelioid cells, plasma cells, lymphocytes, eosinophils, fibroblasts, and a few foreign body giant cells. There was only mild fibroplasia surrounding masses of F. milksi, Often this was absent in the vicinity of lesions with single or only a few nematodes. Terminal and secondary bronchioles presented with an eosinophilic peribronchiolitis, a bronchiolar exudate of epithelioid cells and lymphocytes, and hyperplasia of smooth muscle fibers. Nematodes in varying stages of maturity were observed ranging from gravid females to lar- vae. Larvae were most frequently observed in the parenchyma, but occasionally found in
bronchioles. There was little or no cellular reaction associated directly with larvae. Remarks Filaroides milksi has been previously reported from dogs in New York (Whitlock, 1956; Judd, 1960), Iowa (Peckham et al., 1960), Connecticut (Mills and Nieldsen, 1966), and Canada (Greenway and Stockdale, 1970), and the striped skunk, Mephitis mephitis, from Iowa (Levine et al., 1965). Filaroides mephitis was described as a distinct species by Webster (1966) from Mephitis mephitis in eastern Canada. Dyer (1970) also reported this species from the same host in North Dakota. This species was differentiated on the basis of larger size of the male (up to 24 mm versus 3.4-4.4 mm for F. milksi), larger spicules (48-60 in F. milksi versus 85.5--89.3 in F. mephitis), and presence of a prominent vulvar inflation in F. milksi. Specimens from the hog-nosed skunk in the present study appear intermediate in size (a single broken male measuring 7.5 mm), spicules 59-78 long, and females with only a slight to no inflation in the vulvar region. Examination of the type specimens of F. mephitis (USNM Helm. Coll. No. 61679 and 61680) revealed no morphological differences by which these species could be distinguished. Spicules of F. mephitis, although larger, appeared identical to those recovered from the hog-nosed skunk (Figs. 1, 3). Therefore, Filaroides mephitis Webster, 1966 is considered a synonym of F. milksi. Examination of type specimens of Filaroides hirthi Georgi and Anderson, 1975 revealed few morphological differences between specimens collected in the present study and this species. This species supposedly differed from F. milksi by (1) smaller size and (2) slightly stouter spicules with broader knobs for attachment of retractor muscles. Paratypes of F. hirthi (USNM Helm. Coll. No. 72943 and 72944) appear to be immature specimens. The spicules of the species reported as F. hirthi appear very similar to those observed herein from the hog-nosed skunk and those reported as F. mephitis by Webster (1966) (Figs. 1-3). Additionally, Hirth and Hottendorf (1973) in the original description of the pathology of this nematode stated the male was up to 6.0
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mm long and 90 wide, while the female ap- one third occasionally had a few nodules mea-
proached 10.0 mm long and 185 wide. This suring 1--3 mm in diameter. In the posterior
information was not included in the new spe- one third of the trachea at the bifurcation of
cies description of F. hirthi by Georgi and the bronchi and sometimes into the bronchi
Anderson (1975) who described living speci- themselves, the lesions became larger and more
mens as 2.3-3.2 mm long and 35-43 wide in numerous. Grossly, the lesions appeared as
the male and 6.6-13.0 mm long and 58-102 white to pink polypoid or sessile nodules just
wide in the female. Thus, both the spicules under the mucosa, 1--12 mm in diameter (Fig.
and range of measurements are probably within 5). Often the anterior and posterior extremi-
the range of intraspecific variation of F. milksi. ties of numerous nematodes protruded from
Filaroides milksi is differentiated from F. the lesion. In more severe infections the ma-
mortis (Werner, 1782) Dougherty, 1943 and jority of the lesions were located in the tracheal
F. osleri principally by the smaller size of bifurcation with the larger adjacent lesions
the spicules which are 46--89 as compared to sometimes becoming confluent. They were
174-183 and 99-133 in the latter two species, confined to the ventral and ventrolateral as-
respectively (Levine et al., 1976). Addition- pects of the trachea and were raised as much
ally, the spicules of F. osleri have prominent as 5 mm above the mucosal surface. In no
transverse ridges, the tail of the female is instance were the lesions so numerous as to
rounded and the anus and vulva are very close. occlude the lumen of the trachea or bronchi.
Filaroides milksi differs from F. canadensis The lungs of infected animals showed no signs
Anderson, 1963 in that the distal ends of the of gross pathological changes.
spicules are not split and the gubernaculum Histologically, the size of the nodules cor-
is considerably larger (Anderson, 1963).
responded to the number of adult nematodes
present in the lesion. Smaller lesions contained
Filaroides osleri (Cobbold, 1879) Skrjabin, 1933
only a few nematodes and in some instances only a single worm. Occasionally, the ciliated
HOST RECORD: Canis latrans, coyote. Twenty four animals infected of 94 examined. LOCALITY: Benjamin, Knox Co., Texas; Ross and Adams Ranches, King Co., Texas; Beggs and Pitchford Ranches, Dickens Co., Texas. Collected by the author from September 1973 to November 1976. LOCATION: Trachea and bronchi forming nodular lesions under tracheal epithelium. DISPOSITION OF SPECIMENS: The Museum of Texas Tech University, Department of Medical Zoology, No. 1594-1673. PATHOLOGY: Animals less than 1 year of age were rarely infected (3/24) while the majority of cases were noted in animals over 2 years of age (15/24). The extent of pathological manifestations in the 24 infected coy-
columnar epithelium of the trachea was continuous over the lesion. Often this appeared to be absent with the surface of the lesion covered by a layer of connective tissue (Fig. 6). In all lesions the host reaction was substantial. Basically, the nodule consisted of masses of entwined adult and larval nematodes surrounded by plasma cells, lymphocytes, collagen, fibroblasts, neocapillaries, eosinophils, and a few histioeytes (Fig. 7). Usually the lesions did not progress beyond the level of the perichondrium. At the base of the nodules the mucous alveoli and tracheal glands were destroyed, and occasionally a few lymphocytes, plasma cells, and eosinophils were seen in tracheal tissue adjacent to the lesions. Histiologic sections of trachea and bronchi occasionally revealed first-stage larvae, and im-
otes varied considerably. Usually the anterior mature adults in the dilated lymphatics of
% of the trachea was not involved. The middle the bronchial and tracheal walls (Fig. 8).
Figures 4-5. Pathology of Filaroides species. 4. Histologic section of F. milksi in Conepatus mesoleucus. Note numerous adult and larval nematodes, peribronchiolar infiltration, hyperplasia of smooth muscle, and interstitial pneumonia. Hematoxylin and eosin. X 26. 5. Gross lesions of F. osleri in trachea of Canis latrans.
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These were sometimes surrounded by lymphocytes, plasma cells, and a few eosinophils. Occasionally, there was a mild hyperplasia of lymph nodes adjacent to these lesions. The lung parenchyma of infected animals in most instances was normal. Several of the animals had a mild interstitial pneumonia, probably unrelated to the F. osleri infection. In the most severe case of F. osleri observed in the coyote, there was a moderate degree of insterstitial pneumonia with congestion and edema most severe near the hilus of the lung. A few granulomatous lesions were scattered throughout the parenchyma. These contained larval nematodes, presumably F. osleri, usually surrounded by an intense reaction of lymphocytes, plasma cells, eosinophils, and a few histiocytes. Remarks Specimens from the coyote collected in this study conform in all respects to previous descriptions of F. osleri infections in dogs, coyotes, and wolves. Filaroides pararostratus described from nodules in the trachea of the dog in Mexico City by Flores-Barroeta (1955) is probably a synonym of F. osleri. Spicules of this species were only 88 long compared to 99--113 for F. osleri, as reported by Olsen and Bracken (1959). Specimens collected from the coyote in the present study had spicules measuring 91--115 (mean 94; 30 specimens; 10 worms from 3 animals, respectively). The prominent transverse ridges on the blade of the spicules as noted by Olsen and Bracken (1959) should serve to differentiate this species from others of the genus. Clarification of the status of F. pararostratus must await careful comparison with F. osleri. Discussion The taxonomy, host--parasite relationships, and distribution of the genus Filaroides in North American carnivores are poorly understood. Their small size, location, and few good
taxonomic characteristics for species differentiation adds to the confusion. Additionally, both the species reported herein demonstrate considerable meristic variability in key characters used in differentiation. Thus, F. mephitis Webster is regarded as a synonym of F. milksi, while the validity of F. hirthi Georgi and Anderson and F. pararostratus FloresBarroeta is in question. Filaroides milksi is reported from dogs in several areas of southern Canada and the eastern United States; Mephitis mephitis in southern Canada, Iowa, and North Dakota; and Conepatus mesoleucus in west Texas. Examination of numerous specimens of other skunks from the same locality, including Spilogale gracilis, Mephitis mephitis, and Mephitis macroura, in west Texas failed to reveal infections with this nematode. Additionally, numerous other carnivores examined from the same area were not infected. Filaroides osleri is apparently cosmopolitan in the dog (Levine, 1968). Coyotes and wolves are reported infected with this species in Alberta (Holmes and Podesta, 1970) and Minnesota (Erickson, 1944). Thornton et al. (1974) previously reported this species from South Texas coyotes. The lesions produced by F. milksi in the hog-nosed skunk appeared similar to those described by Levine et al. (1965) in the eastern striped skunk and by Judd (1960), Peckham et al. (1960), Mills and Nielsen (1966), Greenway and Stockdale (1970), and Hirth and Hottendorf (1973) from the dog. The differences were less granulomatous response surrounding the worms, more severe peribronchiolar infiltration and hyperplasia of smooth muscle, and a more severe interstitial pneumonia with congestion and edema in the parenchyma. Although Babero (1960) noted that Filaroides sp. in Louisiana skunks was highly pathogenic, he failed to describe the lesions. Likewise, lesions attributable to F. mephitis (= F. milksi) were not described by Webster (1966) or Dyer (1970). Judging
Figures 6-8. Pathology of Filaroides osleri in Cam's latrans. 6. Histological section of F. osleri nodule on trachea. Note numerous adult nematodes surrounded by granulation tissue. Hematoxylin and eosin. X 26. 7. Cellular reaction consisting of histiocytes, eosinophils, fibroblasts, plasma cells, and lymphocytes from tracheal nodule. Hematoxylin and eosin. X 320. 8. Section of trachea with small lesion on mucosa containing F. osleri and immature adult in lymphatics (arrow). Hematoxylin and eosin. X 26.
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from the severe reactions and heavy infections in the hog-nosed skunk in Texas and the case described from the striped skunk in Iowa by Levine et al. (1966), this nematode is highly pathogenic to skunks. The effect of this species on wild skunk populations remains to be determined. Apparently F. osleri is not highly pathogenic to coyotes. Although the lesions are similar to those reported in the dog (Mills and Nielsen, 1966; Mills, 1967; Dorrington, 1968) and dingo (Dunsmore and Burt, 1972), the infection apparently does not reach the intensity nor produce the severe effects as reported in the latter species. In no instance was an infection in the coyote noted in this study or by Thornton et al. (1974) in which there were sufficient nodular lesions to block the trachea or bronchi, thus suffocating the animal. Although a mild interstitial pneumonia was noted in several coyotes, in only one instance was this probably attributable to F. osleri infection in the trachea. Histologically, the only difference in lesions from the coyote as compared to those in the dog was the abundance of eosinophils. The effects of this species on the morbidity and mortality of coyote populations is apparently insignificant. Acknowledgments The authors expresses sincere appreciation to Messrs. Larry Conner, Wyman Meinzer, and Mark Baird, who provided many of the coyotes and skunks examined in this study. Literature Cited Anderson, R. C. 1963. Further studies on the taxonomy of metastrongyles (Nematoda: Metastrongyloidea) of Mustelidae in Ontario. Can. J. Zool. 41: 801-809. Babero, B. B. 1960. A survey of parasitism in skunks (Mephitis mephitis) in Louisiana, with observations on pathological damages due to helminthiasis. J. Parasitol. 46(Suppl.): 26-27. Dorrington, J. E. 1968. Studies on Filaroides osleri infestation in dogs. Onderstepoort J. Vet. Res. 35: 225-285. Dunsmore, J. P., and R. J. Burt. 1972. Filaroides osleri in dingoes in southeasternAustralia. Aust. Vet. J. 48: 548-551. Dyer, W. G. 1970. Helminths of the striped skunk, Mephitis mephitis Schreber, in North Dakota. Proc. Helminthol. Soc. Wash. 37: 92-93.
Erickson, A. B. 1944. Helminths of Minnesota Canidae in relation to food habits, and a host list and key to the species reported from North America. Am. Midi. Nat. 32: 358-372. Flores-Barroeta, L. 1955. Helmintos de los Perros Cam's familiaris y gatos Felis catus en la Ciudad de Mexico. An. Esc. Nac. Cienc. Biol. Mexico City 8: 159-202. Georgi, J. R., and R. C. Anderson. 1975. Filaroides hirthi sp. n. (Nematoda: Metastrongyloidea) from the lung of the dog. J. Parasitol. 61: 337-339. Greenway, J. A., and P. H. Stockdale. 1970. A case tentatively diagnosed as Filaroides milksi in a dog. Can. Vet. J. 11: 203-204. Hirth, R. S., and G. H. Hottendorf. 1973. Lesions produced by a new lungworm in beagle dogs. Vet. Pathol. 10: 385-407. Holmes, J. C., and R. Podesta. 1968. The helminths of wolves and coyotes from the forested regions of Alberta. Can. J. Zool. 46: 1193-1204. Jubb, K. V. 1960. The lesions caused by Filaroides milksi in a dog. Cornell Vet. 50: 319325. Levine, N. D. 1968. Nematode parasites of domestic animals and man. Burgess Publ. Co., Minneapolis. 600 p. Levine, N. D., V. Ivens, J. R. Reilly, and J. Simon. 1965. Filaroides milksi (Nematoda: Filaroididae) in the lungs of a striped skunk, Mephitis mephitis. J. Parasitol. 51: 628-630. Mills, J. H. L. 1967. Filaroidiasis in the dog: A review. J. Small Anim. Pract. 8: 37-43. Mills, J. H. L., and S. W. Nielsen. 1966. Canine Filaroides osleri and Filaroides milksi infection. J. Amer. Vet. Med. Assoc. 149: 56-63. Olsen, O. W., and F. K. Bracken. 1959. Lungworm, Filaroides osleri, in a dog in Colorado. J. Am. Vet. Med. Assoc. 134: 330334. Peckham, J. D., J. S. Guldner, and R. L. Winegarden. 1960. The lungworm Filaroides milksi, in Iowa dog. Iowa State Univ. Vet. 22: 129-131, 152, 163. Thornton, J. E., R. R. Bell, and M. J. Rear- don. 1974. Internal parasites of coyotes in southern Texas. J. Wildl. Dis. 10: 232-236. Webster, W. A. 1966. Filaroides mephitis n. sp. (Metastrongyloidea: Filaroididae) from the lungs of eastern Canadian skunks. Can. J. Zool. 45: 145-147. Whitlock, J. H. 1956. A description of a new dog lungworm Filaroides milksi n. sp. (Nematoda, Metastrongyloidea). Wien. Tieraerztl. Monatsschr. 43: 730-738.
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