A European Robin (Erithacus rubecula) found dead in England had marked blepharitis and periocular alopecia associated with Aprocta cylindrica (Nematoda: Aproctidae) and concurrent mixed fungal infections. Aprocta cylindrica should be considered a differential diagnosis in periocular abnormalities of robins and other insectivorous, migratory passerines in Western Europe.
The European Robin (hereafter referred to as ‘robin,’ Erithacus rubecula, Order Passeriformes) is a common garden visitor in Britain (Mead 1984). Periocular alopecia has been reported, anecdotally, to be common in British robins (Mead 1984), and dermatophyte infection (of undetermined species) has been diagnosed in at least three cases (Mead 1984; V. Simpson and B.L. unpubl. data). Other pathogens with the potential to cause periocular disease in passerines include avipoxvirus, Mycoplasma and Chlamydia spp. (Thomas et al. 2007), Collyriclum faba (Trematoda; Literák et al. 2003), and Oxyspirura spp. (Nematoda: Thelaziidae) such as Oxyspirura petrowi, which has been detected in robins in Central Europe (Okulewicz 1984).
A dead adult male robin was submitted from a rural garden in Lincolnshire, eastern England (52°58′N, 0°30′W), in early May 2011. A postmortem examination was performed using standardized protocols (Lawson et al. 2012). The robin was moderately autolyzed and in thin body condition (bodyweight 18.9 g; the average bodyweight of 11 adult British robins in normal or fat body condition, received from 2005–12, was 20.1 g [B.L., K.M.B. unpubl. data]). The cause of death was judged to be trauma consistent with cat predation (missing feathers, penetrating wounds, fractures, and hemorrhage). In addition, the left eyelids were markedly swollen and alopecic (Fig. 1) with superficial dry, yellow material. The right eyelids were slightly swollen. In the left periocular subcutaneous space there was bright yellow, semifluid material and 10–15 cream-colored, threadlike nematodes. The small intestine contained approximately 20 acanthocephalan helminths with no associated gross lesions.
Microscopic examination of a smear of the subcutaneous purulent material revealed numerous branching, septate fungal hyphae. Routine cultures yielded a pure growth of Aspergillus fumigatus (identified on morphology) but no significant bacterial isolates. Further culture of this tissue on dermatophyte selective agar (BioMérieux UK Ltd., Hampshire, UK; in O2 at 25 C for 7 days) yielded a scant, pure growth of Chrysosporium keratinophilum (identified phenotypically by the Mycology Reference Laboratory, Public Health England, Bristol, UK). Routine cultures of liver and small intestinal content yielded no significant bacterial or fungal isolates. Tests of periocular tissue for Mycoplasma spp. (Diagnostic Pathology Service, University of Liverpool, Neston, UK) and avipoxvirus (as per Lawson et al., 2012), and of pooled periocular tissue and liver for Chlamydia spp. (Animal Health and Veterinary Laboratories Agency, Penrith, UK), were performed via PCR and all were all negative.
Histologic examination of the right and left eyelids and adnexa showed extensive granulomatous conjunctivitis and periophthalmitis with intralesional nematodes and intralesional fungal hyphae morphologically consistent with A. fumigatus. There were numerous nematodes within inflammatory exudate in the subconjunctival space (Fig. 2) and in what appeared to be fibrosed subconjunctival pockets of both eyes. The epidermis of both eyelids was hyperplastic and hyperkeratotic with many associated dermatophyte-like hyphae or pseudohyphae in the keratin layers. A third fungal species (a possible postmortem invader, resembling an oomycete such as Saprolegnia spp.) was visible histologically in the right periocular tissues. No significant histologic abnormalities were detected in the intestine, brain, heart, liver, or kidney.
For morphologic inspection, the periocular nematodes were cleared in beechwood creosote, mounted on glass microscope slides, examined under a high-power microscope (Olympus BH2, Olympus, Southend-on-Sea, UK, using 10× to 40× objectives, including interference phase), and measured using an ocular micrometer (Olympus). The nematodes measured (maximally) 15–20 mm long and 0.5 mm wide and were morphologically characteristic of Aprocta cylindrica (Nematoda: Aproctidae). The nematodes had a filarial form, rounded ends, an unadorned and transversely striated cuticle, a simple mouth, a short esophagus, and an intestine with black, granulate content. Females had no discernable anus and thick-walled eggs containing larvae without posterior spines, and males (smaller than females) had a spirally curved caudal end and boat-shaped, pointed spicules of roughly equal length (0.15–0.33 mm; Sonin 1974). The nematodes were accessioned into the Parasitic Worms Collection of the Department of Life Sciences, Natural History Museum (London, UK; accession NHMUK.2014.3.28.1-2). The intestinal acanthocephalan helminths were morphologically consistent with Plagiorhynchus cylindraceus (Crompton and Nickol 1985); this passerine parasite has previously been identified in robins in Britain, with no evidence of associated disease (E.H. unpubl. data).
This appears to be the first description of A. cylindrica in Western Europe. The Natural History Museum (London, UK) tentatively identified specimens received in the 1980s from a robin in Hampshire, England, as A. cylindrica; however, the parasites were adult females, precluding definitive identification (E.H. unpubl. data). Aprocta cylindrica has been detected in adult robins in Central and Eastern Europe and the southern Baltic (Jōgis 1974; Okulewicz 1984; Frantova 2002; Okulewicz and Sitko 2012). Robins appear to be the species most commonly parasitized by A. cylindrica in Europe (Okulewicz 1984; Frantova 2002). The nematode parasitizes a variety of passerines in Africa and Asia (Sonin 1974; Quentin et al. 1976; Vassiliadès 1980), and the migratory locust (Locusta migratoria) is believed to be an intermediate host (Quentin et al. 1976). Whether other invertebrates serve as intermediate hosts of A. cylindrica is unknown. The robin's susceptibility to A. cylindrica infection relates to its insectivorous diet and, possibly, also to certain anatomical features such as its large orbital cavities (Okulewicz and Sitko 2012).
How a robin in Britain was infected with A. cylindrica is uncertain. Central European robins are thought to acquire the infection when they overwinter in the Iberian Peninsula (although A. cylindrica has not been reported there), North Africa, and Asia Minor (Okulewicz and Sitko 2012). Most breeding robins are resident in Britain; however, migratory robins stop over in Britain while on spring passage from Iberia and North Africa to northeast Europe (Fennessy and Harper 2002). Migration between Central or Eastern Europe and Britain appears to occur very rarely (Fennessy and Harper 2002). Therefore, it seems most likely that this robin was a migrant that had overwintered in Iberia or North Africa and was either on return migration to northeast Europe or (less likely) had become disorientated on return migration to Central or Eastern Europe. The apparent pathogenicity of A. cylindrica in this case was consistent with observations by Okulewicz and Sitko (2012) of ocular and respiratory disease in three robins with periocular A. cylindrica infection. The risk A. cylindrica infection poses to other avian species in Britain is unknown.
The fungal infections were probably opportunistic, secondary to A. cylindrica infection. It is possible that the dermatophyte-like fungus visible in the keratinized skin was C. keratinophilum; however, there were too few distinctive histologic features to confirm its identity. Chrysosporium keratinophilum is keratinophilic and is a common commensal on avian plumage (Mandeel et al. 2011). Although C. keratinophilum has a low pathogenic potential, it may be an opportunistic pathogen in some instances (Chabasse et al. 1989).
Further investigations of wild bird mortalities are required to understand better the prevalence and significance of A. cylindrica and dermatophyte infections in British passerines. Aprocta cylindrica should be considered as a differential diagnosis in periocular abnormalities of robins and other insectivorous, migratory passerines in Western Europe.