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Filarial tenosynovitis caused by Pelecitus species (Spirurida, Filarioidea, Onchocercidae) in the legs of a channel-billed toucan (Ramphastos vitellinus).

Abstract. An adult channel-billed toucan (Ramphastos vitellinus), imported from Surinam, South America, 18 months earlier, was found dead in its cage. At necropsy, the hock joints were swollen bilaterally and had a reduced range of motion. Small curled worms were present in subcutaneous tissue around the joints, with edema and fibrin formation. These worms were classified as the filarioid nematode, Pelecitus species. Blood-borne microfilariae were seen in cytologic impression smears of the lung and the leg lesions.

Key words: filarioid nematodes, Pelecitus species, tenosynovitis, avian, channel-billed toucan, Ramphastos vitellinus

Clinical Report

An adult channel-billed toucan (Ramphastos vitellinus) was found dead in its cage and was submitted for necropsy. The bird had been imported from Surinam, South America, 18 months earlier and had been housed in a breeding facility in the Netherlands. The bird was caged in a heated indoor enclosure with access to an outside flight pen. It had been vaccinated against Yersinia pseudotuberculosis (Pseudovac, Department of Veterinary Pathology, Utrecht University Utrecht, The Netherlands) 3 months earlier. No clinical problems were observed. At necropsy, the bird was in poor body condition, with several broken flight feathers and no subcutaneous, abdominal, or coronary fat tissue. The right ventricle of the heart was dilated and the coronary vessels were congested. The kidneys were dark brown and congested. The esophagus, proventriculus, and gizzard were empty except for a small amount of bile fluid, and the koilin layer was stained green-yellow. The duodenum and other parts of the small intestines were filled with orange-yellow mucoid contents. Some undigested plant fibers were found in the rectum and cloaca along with droppings. The rest of the digestive tract and the respiratory system appeared normal.

The hock joints were swollen bilaterally, with subcutaneous edema and visible fibrin formation. The range of motion appeared reduced. Several small curled nematodes were visible within the subcutaneous tissue of the hock joints (Fig 1 a and b); these were closely associated with the flexor tendons and the joint capsule but were not inside the synovial cavity. In addition, nematodes were visible in the metatarsophalangeal joints and the footpads. Impression smears from the liver, spleen, lungs, and rectum were prepared and stained with a quick stain (Hemacolor, Merck, Darmstadt, Germany). In addition, smears were prepared from the lesions of the hocks. Tissue samples from all parenchymal organs as well as both entire legs were collected and fixed in 10% buffered formalin. Tissues were processed routinely after paraffin embedding, cut to thin 4-[micro]-thick sections, and stained with hematoxylin and eosin and with Prussian Blue for iron. Numerous worms, approximately 1-cm long, were collected from subcutaneous tissues and fixed in 70% ethanol with added 10% glycerin for parasitologic examination.

On cytologic examination, brown pigmentation (hemosiderin) was present in the spleen, and several microfilariae were identified in the lungs. Numerous microfilariae, foamy macrophages, and heterophilic granulocytes were seen in stained smears of edema fluid from the leg lesions. On histologic examination, one transverse section of a worm with eggs was found in the liver. Many aggregates of macrophages loaded with brown pigment that stained positive for iron (hemosiderin) were present in the spleen. No major pathologic changes were identified in other organs. In the subcutis of the hock and tarsometatarsus, as well as in the edema fluid, many microfilariae (Fig 1c) and sections of adult nematodes (Fig 1d and e) were seen. There was a very extended fibrinous response as well as areas with cellular infiltrates (lymphocytes, macrophages, and granulocytes). The nematodes were classified as Pelecitus species (Spirurida, Filarioidea, Onchocercidae). The probable cause of death of the toucan was cachexia and hypoglycemia due to deceased mobility and anorexia that resulted from verminal tendovaginitis and cellulitis caused by the nematodes.

[FIGURE 1 OMITTED]

Discussion

Approximately 160 species of filarioid nematodes are known to parasitize birds. (1) All genera of avian filarioids are classified in the family Onchocercidae, and 16 genera are recognized. Avian filarioids produce microfilariae that are either blood borne or skin inhabitating. (1) The life cycles of avian filarioids follow the standard filarioid pattern; these invariably involve a vertebrate definitive host and an invertebrate intermediate host, the latter referred to as the vector. (1) Adult male and female worms mate in the vertebrate, and the females produce microfilariae that enter the host's blood or skin. (1) Upon ingestion by a hematophagous arthropod, development proceeds to a so-called sausage stage, then to the second stage, and finally to the infective third stage. (1) Infective third-stage larvae migrate to the head and mouthparts of the arthropod and, while the arthropod feeds, break out of these locations and onto the vertebrate's skin. (1) Given conditions of suitable moisture, they quickly enter the puncture wound made by the arthropod and gain entrance to the vertebrate's body. (1) In the vertebrate, development continues to the fourth larval stage and finally the fifth or adult stage of development. (1)

To our knowledge, this is the first documentation of a Pelecitus infection in a channel-billed toucan. Pelecitus species are probably the most broadly distributed genus of filarioid nematodes in birds, with reports from 17 avian orders. (1) Pelecitus species infection was previously reported from a Maximilian's parrot (Pionus maximiliana) with a cystic lesion of the hock joints. (2) The parrot died of bacterial septicemia and pyogranulomatous hepatitis but not of the parasitism. (2) Pizarro et al (3) reported Pelecitus species infection of the cervical subcutaneous tissue in a pigeon. They concluded that the death was caused by coinfection with Trichomonas species but not filariosis itself. (3) Although originally reported as Pelecitus species infection of the peritracheal tissues in pigeons, the filarioid nematodes that were reported by Pizarro et al (3) and Rutherford and Black (4) are likely to be misidentifications of species of Lemdana or Eulimdana (subfamily Lemdaninae). (1) Oniki et al (5) reported Pelecitus helieinus infection in 13 neotropical rain forest avian species that belong to 7 families and 2 orders. They collected the worms from live birds that had been caught to be banded and described that the infected sites were frequently hock and foot joints. The joints of these parasitized wild birds were swollen and red, often with a hole in the skin with oozing blood, especially if the bird had scratched the wound. (5) Seven different species of Pelecitus were also reported by Pinto and Noronha (6) from foot pad and tendons of feet in 19 Brazilian wild bird species. Pinto et al (7) reported Pelecitus species infection of psittacine birds.

Pelecitus species have been described in many nonavian hosts. (8-10) Pelecitus species are probably the only filarioids that parasitize both avian and nonavian hosts. (1) Chilton et al (9) showed that one species of Pelecitus can infect more than one host species. The intermediate hosts of all Pelecitus species are not fully known. Normally, bloodsucking insects such as tabanids serve as intermediate hosts. In American coots (Fuliea americana), lice were found as vectors. Development of Pelecitus fulieaeatrae to the third stage in the chewing louse Pseudomenopon pilosum (Mallophaga: Amblycera) was described by Bartlett and Anderson. (11) However, mosquitoes have been reported as the intermediate host of Pelecitus species in birds. (1)

Some Pelecitus species have skin-inhabiting microfilariae. (12) In this toucan, we found blood-borne microfilariae on impression smears of the lungs. The exact development life cycle of Pelecitus species in their definitive host is uncertain. Subadult fourth-stage worms were present 20 days after infection in the tibiotarsal joints of the host in an experimental infection of American coots with P fulicaeatrae. (11) Pelecitus Julicaeatrae of coots also produce long-lived, skin-inhabiting microfilariae, but adult worms become reproductively senescent. (13) The short life span of adults in Eulimdana species and reproductive senescence in P Julicaeatrae ensure that the skin will not become saturated with large numbers of microfilariae, which would probably be harmful to mallophagan vectors that remain on the host and are continually exposed to microfilariae while feeding. (13) In Pelecitus species, as in many other filarioids, the time span for maturation from microfilariae into adult worms can take 7 months or longer. (12) Although it is likely that the toucan that we describe became infected in Surinam, the possibility of acquiring the infection in The Netherlands cannot be excluded.

Although an antemortem diagnosis of Pelecitus species has been reported, (5,14) diagnosis is often made when adult worms are found during necropsy. (1,15) Fine needle aspiration of leg lesions may reveal microfilariae. (14) In a suspect case in a live bird, blood samples can be helpful. (1,16) The hematocrit centrifuge technique enables detection of microfilariae in a wet mount preparation. (1) Blood smear samples have been used for investigating the prevalence of microfilariae in wild birds, but the species or even genus microfilariae could not be identified. (17,18) Speciation of filarids is based mainly on descriptions of adult worms, and descriptions based only on microfilariae are discouraged. (1)

There is no effective drug treatment for Pelecitus infection. (15) Because dead worms may initiate inflammatory responses and lesions that adversely affect normal physiologic function, drugs that kill adult worms in situ may lead to more severe consequences than those posed by the original infection. (1) In a yellow-collared macaw (Ara auricollis) with lameness due to Pelecitus species infection, therapy with ivermectin and corticosteroids was unsuccessful, and the problem was resolved by surgically removing the adult worms from subcutaneous tissues. (19)

Acknowledgments: We thank Herman Cremers, Utrecht, The Netherlands, for his expertise and review of the parasitologic descriptions in this manuscript.

References

(1.) Bartlett CM. Filarioid nematodes. In: Atkinson CT, Thomas N J, Hunter DB, eds. Parasitic Diseases of Wild Birds. Ames, IA: Wiley-Blackwell; 2008:439-462.

(2.) Greve JH, Graham DL, Nye RR. Tenosynovitis caused by Pelecitus calamiformis (Nematoda: Filarioidea) in the legs of a parrot. Avian Dis. 1982;26(2):431-436.

(3.) Pizarro M, Villegas P, Rodriguez A, Rowland GN. Filariasis (Pelecitus sp.) in the cervical subcutaneous tissue of a pigeon with trichomoniasis. Avian Dis. 1994;38(2):385-389.

(4.) Rutherford DM, Black H. Letter: Pelecitus, a peritracheal nematode in the pigeon. N Z Vet J. 1974;22(8):147.

(5.) Oniki Y, Kinsella JM, Willis EO. Pelecitus helicinus Railliet & Henry, 1910 (Filarioidea, Dirofilariinae) and other nematode parasites of Brazilian birds. Mem Inst Oswaldo Cruz. 2002;97(4):597-598.

(6.) Pinto RM, Noronha D. Analysis of Brazilian species of Pelecitus Railliet & Henry (Nematoda, Filarioidea) with the establishment of new records. Rev Bras Zool. 2003;20(2):361-364.

(7.) Pinto RM, Vicente JJ, Noronha D. Nematode parasites of Brazilian psittacid birds, with emphasis on the genus Pelecitus Railliet & Henry, 1910. Mem Inst Oswaldo Cruz. 1993;88(2):279-284.

(8.) Jimenez-Ruiz FA, Gardner SL, Cervantes FA, Lorenzo C. A new species of Pelecitus (Filarioidea: Onchocercidae) from the endangered Tehuantepec jackrabbit Lepus flavigularis. J Parasitol. 2004; 90(4):803-807.

(9.) Chilton NB, Beveridge I, Andrews RH, Spratt DM. Apparent lack of genetic variation within Pelecitus romeri (Nematoda: Filarioidea) from three Australian species of macropodid marsupial. Int J Parasit. 1992;22(7):1023-1027.

(10.) Portas TJ, Spratt DM, Rose KA. Microfilaraemia associated with Pelecitus roemeri in a western grey kangaroo (Macropus fuliginosus). Aust Vet J. 2005; 83(6):353-354.

(11.) Bartlett CM, Anderson RC. Pelecitus fulicaeatrae (Nematoda: Filarioidea) of coots (Gruiformes) and grebes (Podicipediformes): skin-inhabiting microfilariae and development in Mallophaga. Can J Zool. 1987;65(11):2803-2812.

(12.) Bartlett CM, Anderson RC. Mallophagan vectors and the avian filarioids: new subspecies of Pelecitus fulicaeatrae (Nematoda: Filarioidea) in sympatric North American hosts, with development, epizootiology, and pathogenesis of the parasite in Fulica americana (Aves). Can J Zool. 1989;67(11):2821-2833.

(13.) Anderson RC, Bartlett CM. Ephemerality and reproductive senescence in avian filarioids. Parasitol Today. 1994;10(1):33-35.

(14.) Greiner EC, Ritchie BW. Parasites. In: Ritchie BW, Harrison G J, Harrison LR, eds. Avian Medicine: Principles and Application. Lake Worth, FL: Wingers Publishing; 1994:1007-1029.

(15.) Morishita TY, Schaul JC. Parasites of birds. In: Baker DG, ed. Flynn's Parasites of Laboratory Animals'. Ames, IA: Blackwell Publishing; 2007:217-301.

(16.) Dissanaike AS, Fernando MA. Pelecitus galli n. sp. from the Malayan jungle fowl Gallus gallus spadicus. J Helminth. 1974;48(3): 199-203.

(17.) Bennett GF, White EM, Williams NA. Additional observations on the blood parasites of Ugandan birds. J Wildl Dis'. 1977;13(3):251-257.

(18.) Forrester D J, Greiner EC, McFarland RW. Blood parasites of some columbiform and passeriform birds from Chile. J Wildl Dis. 1977;13(1):94-96.

(19.) Allen JL, Kollias GV, Greiner EC, Boyce W. Subcutaneous filaxiasis (Pelecitus sp.) in a yellow-collared macaw (Ara auricollis). Avian Dis. 1985;29(3):891-894.

Seyed Ahmad Madani, DVM, DVSc, and Gerry M. Dorrestein, DVM, PhD

From the Department of Clinical Sciences, Faculty of Veterinary Medicine, University of Tehran, 16539-48458 Tehran, Iran (Madani); and Diagnostic Pathology Laboratory, NOIVBD, Wintelresedijk 51, 5507 PP Veldhoven, The Netherlands (Dorrestein).
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Author:Madani, Seyed Ahmad; Dorrestein, Gerry M.
Publication:Journal of Avian Medicine and Surgery
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Geographic Code:4EUNE
Date:Mar 1, 2012
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