Case Reports in Veterinary Medicine

Case Reports in Veterinary Medicine / 2013 / Article

Case Report | Open Access

Volume 2013 |Article ID 719465 |

Jennifer N. Niemuth, Joni V. Allgood, James R. Flowers, Ryan S. De Voe, Brigid V. Troan, "Ventricular Habronemiasis in Aviary Passerines", Case Reports in Veterinary Medicine, vol. 2013, Article ID 719465, 6 pages, 2013.

Ventricular Habronemiasis in Aviary Passerines

Academic Editor: C. Gutierrez
Received29 Oct 2013
Accepted26 Nov 2013
Published22 Dec 2013


A variety of Habronematidae parasites (order Spirurida) have been described as occasional parasites of avian species; however, reports on passerines are relatively uncommon. From 2007 to 2008, 11 passerine deaths at The North Carolina Zoological Park in Asheboro, NC, USA, were associated with ventricular habronemiasis, which was determined to be the cause of death or a major contributing factor in 10 of the 11 individuals. The number and species affected were 5 Red-billed Leiothrix (Leiothrix lutea), 2 Japanese White-eye (Zosterops japonicus), 2 Golden-headed Manakin (Pipra erythrocephala), 1 Blue-grey Tanager (Thraupis episcopus), and 1 Emerald Starling (Coccycolius iris). Affected animals displayed nonspecific clinical signs or were found dead. The ventricular nematodes were consistent in morphology with Procyrnea sp. Koilin fragmentation with secondary bacterial and fungal infections was the most frequently observed pathologic lesion. Secondary visceral amyloidosis, attributed to chronic inflammation associated with nematodiasis, was present in 4 individuals. An insect intermediate host is suspected but was not identified. Native passerine species within or around the aviary may be serving as sylvatic hosts.

1. Introduction

Habronemiasis is used to describe infection by any of the genera of the family Habronematidae within the order Spirurida. The most well-known Habronematidae parasites, Draschia megastoma, Habronema muscae, and Habronema microstoma, are of minimal clinical significance as equine stomach parasites [1]. However, many members of the family Habronematidae (Odontospirura, Sicarius, Exsica, Procyrnea, Cyrnea, and Metacyrnea) are found in birds [2].

In nonpasserines, a variety of habronemes have been described as occasional parasites found within the proventriculus, ventriculus, and/or intestine. Reports are predominantly from Africa, Asia, and Australia and include buzzard, eagle, egret, falcon, fowl, hawk, hummingbird, kite, kiwi, owl, parrot, pigeon, tinamou, vulture, and woodpecker species [322]. With the exception of a lethal case in a black-backed woodpecker (Picoides arcticus), no host morbidity, mortality, or significant pathology is reported with habronemiasis in nonpasserines.

Reports on habronemiasis in passerines appear to be much less common. Habronema hyderabadensis was found in the proventriculus and ventriculus of Gracula (religiosa) intermedia in India [11], while habronemes from the genera Viguiera and Cyrnea have been reported in the ventriculus of Australian passerines [12]. Neither described any clinical significance. A case report from Germany [23] describes a series of cases of ventricular habronemiasis causing morbidity and mortality in Red-billed Leiothrix (Leiothrix lutea) and Bali Myna (Leucopsar rothschildi). A survey of American robins (Turdus migratorius) appears to be the only published record of North American passerine habronemiasis. Habronema sp. were recovered from the esophagus and proventriculus of 6 adult birds (3 males, 3 females) out of 62 surveyed [24].

This report describes two outbreaks of ventricular habronemiasis occurring in 2007 and 2008, which resulted in morbidity and mortality in passerines at The North Carolina Zoological Park, Asheboro, NC, USA.

2. Cases

2.1. Affected Animals

The R. J. Reynolds Forest Aviary at the North Carolina Zoological Park simulates tropical forest and displays approximately 36 species of exotic birds from Africa, Asia, Australia, Indonesia, and South America. The aviary sporadically houses native, rehabilitated, unreleasable passerine species. All birds complete at least a 30-day quarantine prior to introduction into the exhibit. While considered a closed system, native insects, reptiles, amphibians, and occasional birds have entered the habitat.

From March to October 2007 and May to September 2008, 11 passerine deaths were associated with habronemiasis. Five of the individuals were hatched at the North Carolina Zoological Park, while 6 were obtained from other institutions over time and had passed through quarantine. The number and species affected were 5 Red-billed Leiothrix (Leiothrix lutea), 2 Japanese White-eye (Zosterops japonicus), 2 Golden-headed Manakin (Pipra erythrocephala), 1 Blue-grey Tanager (Thraupis episcopus), and 1 Emerald Starling (Coccycolius iris). Gender and age of each individual are presented in Table 1.

DateSpeciesSexAgeCause of deathOther/associated lesions

3/28/2007L. lutea M10 yrsHepatic amyloidosisVentricular habronemiasis
6/18/2007L. lutea F7 yrsHepatic amyloidosisVentricular habronemiasis with secondary bacterial ventriculitis; ovarian amyloidosis
6/19/2007T. episcopus F2 yrsTraumaVentricular habronemiasis with secondary bacterial ventriculitis
7/23/2007Z. japonicus M7 yrsVentricular habronemiasisSecondary fungal ventriculitis
7/23/2007P. erythrocephala N/A13 daysVentricular habronemiasisSecondary bacterial and fungal ventriculitis
7/23/2007L. lutea F2 yrsVentricular habronemiasisSecondary bacterial and fungal ventriculitis
8/13/2007P. erythrocephala N/A40 daysVentricular habronemiasisSecondary bacterial ventriculitis
10/5/2007L. lutea F7 yrsVentricular habronemiasisSecondary bacterial ventriculitis; hepatic amyloidosis
5/10/2008C. iris M4 yrsVentricular habronemiasisSecondary bacterial ventriculitis; hepatic, splenic, and renal amyloidosis
8/16/2008L. lutea M11 yrsVentricular habronemiasisSecondary bacterial and fungal ventriculitis
9/2/2008Z. japonicus F8 yrsVentricular habronemiasisSecondary bacterial and fungal ventriculitis; pulmonary aspergillosis; polyoma nephritis; and myocarditis

2.2. Clinical Examination, Gross Pathology, and Microscopy

The deaths of 10 individuals were spontaneous: 8 were found dead, 1 individual died in-hand during examination, and 1 individual died en route to treatment. The eleventh individual was humanely euthanized because of declining quality of life.

Before death, a majority of affected individuals ( ) displayed nonspecific clinical signs associated with illness in birds, such as depression or lethargy, perching low or on the ground, and/or a fluffed appearance. After death, 7 individuals (5 with other clinical signs) were noted to be in thin to emaciated body condition (body condition scores ranging from 1 to 2 out of 5 for the 6 individuals given a score).

All individuals were stored at 4°C until postmortem examination and necropsy by a veterinarian. On gross examination, 8 individuals were found to have visible nematodes associated with the koilin layer or within the lumen of the ventriculus or intestinal tract. Four individuals had gross hepatomegaly. Thickened, irregular, or friable koilin was noted in 3 individuals.

Nematodes were preserved in 70% ethanol for identification. Representative specimens were cleared and temporarily mounted in an alcohol and glycerine solution. Habronematidae taxonomy and identification follow those of Chabaud [2].

Whole nematode specimens recovered from the ventriculus of a C. iris were consistent in morphology with Procyrnea sp. As with Chabaud’s [2] key, our specimen had weakly developed teeth near the anterior border of the pseudolabia. Median teeth and a cylindrical, chitinous buccal cavity (Figure 1(a)) were present. The male had a distinct copulatory spicule (Figure 1(b)) and a tail of the spirurid type with 9 preanal papillae, 4 postanal papillae, and a terminal group of papillae and phasmids. The uteri of females were filled with thick-shelled, larvated eggs (Figure 1(c)). Although the quality and number of specimens examined for identification were not adequate for confident speciation, our specimens were similar in appearance and measurement to Procyrnea mansioni [16, 23].

2.3. Histopathology

Samples of brain, lung, kidney, liver, and gastrointestinal tract were collected for histopathology from each individual. Spleen, heart, skeletal muscle, gonads, pancreas, and thyroid were collected from some individuals. The samples were fixed in 10% neutral buffered formalin. Fixed samples were embedded in paraffin wax; 5 μm serial sections were made and then stained with hematoxylin and eosin (H&E) stain. When applicable, additional staining with acid fast, trichrome, Sirius red, periodic acid Schiff, Grocott’s methenamine silver stain, or Congo red (pre- and post-acid digestion with 0.5% potassium permanganate and 0.3% sulfuric acid) was performed. Board-certified veterinary pathologists performed histopathologic examinations.

Histologically, Procyrnea sp. parasites were found between the koilin and mucosal layers of the ventriculus (Figure 2(a)) and occasionally within the lumen of the proventriculus, ventriculus, or intestinal tract. A thin cuticle, polymyarian, coelomyarian musculature, lateral cords, complete digestive tract, pseudocoelom, and a tripartite esophagus were identified on cross-section. Numerous oval, thick-shelled, embryonated eggs were present within the uterus (Figure 2(c)).

The associated koilin layer was frequently fragmented and admixed with aggregates of fibrin, necrotic cell debris, and inflammatory cells (Figure 2(b)). Ventriculitis was severe in 5 individuals, moderate in 2 individuals, and mild in 4 individuals. In 10 of the 11 affected individuals, secondary bacterial infections and/or fungal infections (consistent with Candida albicans) were identified. Mucosal ulceration was occasionally noted.

Four of the adult animals, including 3 of the 5 L. lutea and the single C. iris, also had visceral amyloidosis verified by Congo red staining (Figure 2(d)). Amyloidosis in the 3 L. lutea was moderate to severe, while the amyloidosis in the C. iris was mild. Amyloid deposits were most commonly found within hepatic sinusoids but were also identified in ovarian, splenic, and renal tissue. Loss of Congo red staining after acid digestion with 0.5% potassium permanganate and 0.3% sulfuric acid was consistent with reactive, serum amyloid-associated (SAA) secondary amyloidosis.

Severe ventricular habronemiasis was determined to be the cause of death in 8 of the 11 individuals (Table 1) and a major contributing factor in the death of 2 individuals with severe hepatic amyloidosis. A single individual died of trauma.

3. Discussion

Unlike the low pathogenicity often seen with equine gastric and nonpasserine avian habronemiasis, increased morbidity and mortality were associated with ventricular habronemiasis of passerines at the North Carolina Zoological Park. Ventricular habronemiasis in these individuals caused chronic ventriculitis and resulted in poor body condition and death. Disruption of the protective koilin layer of the ventriculus led to inflammation and increased susceptibility to secondary bacterial and fungal infections. Similar koilin disruption and large bacterial colonies were noted in the black-backed woodpecker [20], but no inflammatory reaction or change in the koilin layer was reported by Ehrsam et al. [23] for German cases of ventricular habronemiasis in L. lutea and L. rothschildi.

Amyloidosis in birds usually occurs in the liver, spleen, and/or kidneys [25]. It is typically of the SAA type and is associated with chronic infectious disease [25]. Given the absence of other inflammatory lesions, amyloidosis was attributed to chronic ventriculitis caused by nematode infestation. The overrepresentation of L. lutea in cases of amyloidosis could denote species-specific variation in amyloid formation in response to chronic inflammation.

Antemortem direct fecal smears and sodium nitrate fecal flotations had been negative for spirurid nematodes. The eggs of the equine Habronema and Draschia spp. tend not to float well in fecal flotation solutions and are fragile, thus making them hard to find [1]. A combination filtration and centrifugation method is described by Ehrsam et al. [23] and could be attempted in the future.

Given the use of fly intermediates by equine habronememes, the clustering of cases during warm months, and the omnivorous habits of the species affected, an insect intermediate is suspected in this case. Maggots used in diets in the aviary were unlikely to be the intermediate as they are obtained from a commercial source and have been analyzed by a parasitologist and were negative for nematode larvae. Rehabilitated, unreleasable, native passerines introduced to the aviary undergo the same quarantine procedures as exotic aviary species prior to introduction to the general population including prophylactic deworming, typically with a single dose of ivermectin. However, while the aviary is technically a closed environment, native insects, reptiles, amphibians, and occasional birds still get into the exhibit. Efforts to identify an insect intermediate have been unsuccessful and collection and necropsy of native passerines found dead within the zoological park have not identified a sylvatic host. Reported intermediate hosts of Procyrnea pileata include pillbugs (Armadillidium vulgare) and earwigs (Euborellia annulipes) [20], while the German cockroach (Blattella germanica) has been experimentally infected with Cyrnea colini [23]. These insect species or close relatives could be foraged by birds within the aviary. If an intermediate host is identified, xenodiagnosis may be an effective antemortem diagnostic tool and biologic control using parasitoid wasps could be considered if the insect intermediate is Musca sp. [1, 26].

For companion and aviary birds, treatment with oral fenbendazole given daily for 3–5 days, pyrantel pamoate given orally and repeated after 14 days, or ivermectin has been successful at eliminating nematode infections [27]. Treatment with oral fenbendazole, repeated after 14 days, has been reported to be an effective option in raptors [4]. Equine cases are typically treated with a single dose of ivermectin or moxidectin [1, 26, 28, 29].

After the initial diagnosis of habronemiasis, four of the affected L. lutea and the C. iris were treated symptomatically or prophylactically with either pyrantel pamoate (22 mg/kg by mouth repeated every 10 days for 2-3 doses) or fenbendazole (50 mg/kg by mouth every 24 hours for 1–6 days repeated at variable intervals). These treated birds died within 2 months after their last anthelminthic treatment. However, the small sample size, variation in dosing regimes, and lack of regular repeated dosing preclude any conclusions about anthelminthic efficacy or parasite resistance.

In future outbreaks, prophylactic deworming of all affected species with single doses of ivermectin or moxidectin during the summer months may prove to be more efficacious and practical for the free-flight aviary setting. Increased insect pest control and preventing entry of native avian species into the habitat may also help in the reduction or management of outbreaks.


The authors thank Judy Hunt for her assistance in compiling medical records.


  1. D. D. Bowman, Georgis' Parasitology for Veterinarians, Elsevier/Saunders, St. Louis, Mo, USA, 9th edition, 2009.
  2. A. G. Chabaud, “Spirurida,” in Keys to the Nematode Parasites of Vertebrates: Archival Volume, R. C. Anderson, A. G. Chabaud, and S. Willmott, Eds., pp. 334–382, CABI, Cambridge, Mass, USA, 2009. View at: Google Scholar
  3. A. C. Chandler, “A new spiruroid nematode, Habronema americanum, from the Broad-Winged Hawk, Buteo platypterus,” Journal of Parasitology, vol. 27, no. 2, pp. 184–185, 1941. View at: Google Scholar
  4. J. C. Chebez and R. F. Aguilar, “Order falconiformes (Hawks, Eagles, Falcons, Vultures),” in Biology, Medicine, and Surgery of South American Wild Animals, M. E. Fowler and Z. S. Cubas, Eds., pp. 115–124, Iowa State University Press, Ames, Iowa, USA, 2001. View at: Google Scholar
  5. S. A. Smith, “Parasites of birds of prey: their diagnosis and treatment,” Seminars in Avian and Exotic Pet Medicine, vol. 5, no. 2, pp. 97–105, 1996. View at: Google Scholar
  6. M. P. Illescas Gomez, M. Rodriguez Osorio, and F. Aranda Maza, “Parasitation of falconiform, strigiform and passeriform (Corvidae) birds by helminths in Spain,” Research and Reviews in Parasitology, vol. 53, no. 3-4, pp. 129–135, 1993. View at: Google Scholar
  7. A. A. Kocan and L. N. Locke, “Some helminth parasites of the American bald eagle,” Journal of wildlife diseases, vol. 10, no. 1, pp. 8–10, 1974. View at: Google Scholar
  8. V. Agrawal, “On a new avian nematode, Habronema (Aviabronema) hrishii sp. nov. from the intestine of Milvus migrans (Kite),” Transactions of the American Microscopical Society, vol. 84, no. 4, pp. 573–576, 1965. View at: Google Scholar
  9. E. Gendre, “Sur quelques espèces d'Habronema parasites de oiseaux,” Actes de la Société Linnéenne de Bordeaux, vol. 74, pp. 112–133, 1922. View at: Google Scholar
  10. R. Ortlepp, “On Habronema murrayi n. sp. from the barn owl, Tyto alba,” Onderstepoort Journal of Veterinary Science and Animal Industry, vol. 3, pp. 351–355, 1934. View at: Google Scholar
  11. S. M. Ali, “On some new nematodes (Habronematinae) from birds in hyderabad, India, and the relationships of the genus Habronema,” Journal of Helminthology, vol. 35, no. 1-2, pp. 1–48, 1961. View at: Google Scholar
  12. P. M. Mawson, “Habronematinae (Nematoda: Spiruridae) from Australian birds,” Parasitology, vol. 58, no. 4, pp. 745–767, 1968. View at: Google Scholar
  13. R. M. Pinto, J. J. Vicente, and D. Noronha, “Nematode parasites of Brazilian accipitrid and falconid birds (Falconiformes),” Memorias do Instituto Oswaldo Cruz, vol. 89, no. 3, pp. 359–362, 1994. View at: Google Scholar
  14. W. C. Clark, “Procyrnea kea sp. nov. (Habronematidae: Spirurida: Nematoda) from the New Zealand Kea (Nestor notabilis Gould, 1865) (Aves: Psittaciformes),” Journal of the Royal Society of New Zealand, vol. 8, no. 3, pp. 323–328, 1978. View at: Google Scholar
  15. S. Zhang, J. Song, and L. Zhang, “Three species of Procyrnea Chabaud, 1958 (Nematoda: Habronematoidea: Habronematidae) from raptors in Beijing, China, with descriptions of two new species,” Journal of Natural History, vol. 45, no. 47-48, pp. 2915–2928, 2011. View at: Publisher Site | Google Scholar
  16. J. C. Quentin, C. Seureau, and C. Railhac, “Biological cycle of Cyrnea (Procyrnea) mansoni Seurat, 1914, a habronemid nematode parasite of birds of prey in Togo,” Annales de Parasitologie Humaine et Comparee, vol. 58, no. 2, pp. 165–175, 1983. View at: Google Scholar
  17. J. Vercruysse, E. A. Harris, R. A. Bray, M. Nagalo, M. Pangui, and D. I. Gibson, “A survey of gastrointestinal helminths of the common helmet guinea fowl (Numida meleagris galeata) in Burkina Faso,” Avian Diseases, vol. 29, no. 3, pp. 742–745, 1985. View at: Google Scholar
  18. E. A. Harris, “Two new nematodes parasitic in the kiwi in New Zealand,” Bulletin of the British Museum of Natural History, vol. 28, no. 5, pp. 199–205, 1975. View at: Google Scholar
  19. L. Zhang, D. R. Brooks, and D. Causey, “Procyrnea chabaud, 1958 (Nematoda: Habronematoidea: Habronematidae) in birds from the Area de Conservación Guanacaste, Costa Rica, including descriptions of 3 new species,” Journal of Parasitology, vol. 90, no. 2, pp. 364–372, 2004. View at: Publisher Site | Google Scholar
  20. R. B. Siegel, M. L. Bond, R. L. Wilkerson et al., “Lethal Procyrnea infection in a black-backed woodpecker (Picoides arcticus) from California,” Journal of Zoo and Wildlife Medicine, vol. 43, no. 2, pp. 421–424, 2012. View at: Google Scholar
  21. W. R. Davidson, L. T. Hon, and D. J. Forrester, “Status of the genus Cyrnea (Nematoda: Spiruroidea) in wild Turkeys from the southeastern United States,” Journal of Parasitology, vol. 63, no. 2, pp. 332–336, 1977. View at: Google Scholar
  22. G. W. Foster, J. M. Kinsella, E. L. Walters, M. S. Schrader, and D. J. Forrester, “Parasitic helminths of red-bellied woodpeckers (Melanerpes carolinus) from the Apalachicola National Forest in Florida,” Journal of Parasitology, vol. 88, no. 6, pp. 1140–1142, 2002. View at: Google Scholar
  23. H. Ehrsam, S. K. Spillmann, and K. Wolff, “Nematodes (Procyrnea mansioni, Spirurida) as a cause of stomach changes in Chinese nightingales (Leiothrix lutea) and Rothschild's mynah birds (Leucopsar rothschildi),” Schweizer Archiv für Tierheilkunde, vol. 127, no. 10, pp. 665–670, 1985. View at: Google Scholar
  24. R. L. Slater, “Helminths of the Robin, Turdus migratorius Ridgway, from Northern Colorado,” The American Midland Naturalist, vol. 77, no. 1, pp. 190–199, 1967. View at: Google Scholar
  25. K. E. Roertgen and K. H. Johnson, “Amyloidosis,” in Noninfectious Diseases of Wildlife, A. Fairbrother, L. N. Locke, and G. L. Hoff, Eds., pp. 194–202, Iowa State University Press, Ames, Iowa, USA, 1996. View at: Google Scholar
  26. R. K. Schuster and S. Sivakumar, “A xenodiagnostic method using Musca domestica for the diagnosis of gastric habronemosis and examining the anthelmintic efficacy of moxidectin,” Veterinary Parasitology, vol. 197, no. 1-2, pp. 176–181, 2013. View at: Google Scholar
  27. I. Langlois, “The anatomy, physiology, and diseases of the avian proventriculus and ventriculus,” Veterinary Clinics of North America, vol. 6, no. 1, pp. 85–111, 2003. View at: Publisher Site | Google Scholar
  28. A. A. Cutolo, A. T. D. Santos, and S. M. Allegretti, “Field study on the efficacy of an oral 2% ivermectin formulation in horses,” Revista Brasileira de Parasitologia Veterinaria, vol. 20, no. 2, pp. 171–175, 2011. View at: Google Scholar
  29. A. J. Costa, O. F. Barbosa, F. R. Moraes et al., “Comparative efficacy evaluation of moxidectin gel and ivermectin paste against internal parasites of equines in Brazil,” Veterinary Parasitology, vol. 80, no. 1, pp. 29–36, 1998. View at: Publisher Site | Google Scholar

Copyright © 2013 Jennifer N. Niemuth et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

More related articles

 PDF Download Citation Citation
 Download other formatsMore
 Order printed copiesOrder

Related articles