Introduction

Ocular injury secondary to insect hairs, most often moth larvae and occasionally tarantulas, has been termed Ophthalmia Nodosa.¹ The responsible hairs, called urticating hairs or setae, from tarantulas are introduced to the eye after the spider uses its hind legs to flick them off its dorsal abdomen in response to a threat.² This is the first report of ocular injury due to tarantula hairs in the veterinary literature. The physician literature contains 13 cases of ocular injury due to tarantula hairs, supporting the rarity of this diagnosis in medicine.^3–14 The conjunctival tissue excised from the canine patient in this report also had fruiting bodies, hyphae, and microconidia associated with setae. The co-occurrence of these different foreign bodies warrants addition of fungal culture and cytology to work-up and possibly the addition of an anti-fungal agent in initial medical management. To the authors' knowledge, this report is also the first to propose a relationship between Aspergillus fungus and tarantulas of the Theraphosidae family—both in captivity and in the wild. Further research to elucidate this relationship is indicated. This case report describes the clinical presentation, medical and surgical treatment, and eventual diagnosis of keratoconjunctivitis and corneal ulceration in a rat terrier secondary to an unusual etiology.

Case Report

A 9 yr old neutered male rat terrier presented to a private veterinary ophthalmology practice with a 9 day history of acute onset blepharospasm and epiphora of the left eye (OS). Clinical signs were noticed by the owners immediately following an episode where the patient was seen digging in soil covered by dried leaves in northern Arizona.

Upon presentation, the patient was bright, alert, and responsive and weighed 8 kg. A physical examination revealed no abnormalities other than ocular. At a distance, the patient was noted to be markedly blepharospastic, suggesting pain in the OS. Marked serous discharge was present at the medial canthus OS and no gross abnormalities were seen in the right eye (OD). Complete ophthalmic examination was performed in both eyes (OU). Both eyes had positive menace response and dazzle reflex. A resting anisocoria was present with the left pupil being slightly miotic compared to the right pupil. The direct and indirect pupillary light reflexes were brisk and complete in the OD and sluggish and incomplete in the OS due to miosis. Schirmer tear test I^a values were measured at 18 mm/min in the OD and greater than 35 mm/min in the OS, a value consistent with increased lacrimation secondary to ocular irritation. Fluorescein stain^b and proparacaine^c 1% were applied topically to the OU. Slit-lamp^d biomicroscopy revealed no corneal or conjunctival abnormalities in the OD. However, examination of the OS revealed numerous brown to black linear foreign bodies measuring less than 0.5 mm penetrating the corneal epithelium and anterior corneal stroma. These were also present throughout the palpebral and bulbar conjunctiva. The conjunctiva was moderately to markedly hyperemic. A large, fluorescein-positive axial corneal epithelial ulceration was present. The region of cornea around the ulcer was edematous. Superficial neovascularization was present but had not yet reached the ulcer bed. No abnormalities of the lens or anterior vitreous were present in either eye, and the ocular fundus was normal in OU as assessed by indirect ophthalmoscopy^e. Intraocular pressures were normal at 20 mmHg in the OD and 19 mmHg in the OS, as measured by rebound tonometry^f.

Based on history and ophthalmic examination findings, corneal ulceration and conjunctivitis secondary to corneal and conjunctival foreign body was diagnosed. The foreign material was suspected to be of plant origin, specifically cactus glochids, based on local geography, high frequency of this type of injury in the region, and signs mostly consistent with cactus foreign body seen on clinical examination. Manual removal of foreign bodies under general anesthesia with use of an operating microscope^g and jewelers forceps^h was recommended and performed within hours of presentation. Preoperative bloodwork consisted of complete blood count and chemistry panel; the results were unremarkable. During the procedure, it was noted that the foreign bodies could not be extracted smoothly, as is typical of cactus glochids, despite moderate to marked manual traction. The foreign material instead fractured into smaller pieces that remained embedded in the conjunctival and corneal tissues. Excision of the palpebral conjunctiva with tenotomy scissorsⁱ was required to remove the foreign material in contact with the ulcerated cornea. A section of conjunctiva was collected on a cellulose surgical spear^j and placed into a sterile, red top tube^k along with a small amount of isopropyl alcohol. Due to extensive distribution of foreign material, it was impossible to remove all foreign bodies so many were left in the adnexal tissue. The patient recovered uneventfully from anesthesia and was discharged the same afternoon. Postoperatively, tobramycin^l was administered in the OS q 6 hr and artificial tear gel^m as needed to increase comfort. Postoperative medications also included twice daily oral administration of amoxicillin/clavulanic acidⁿ 62.5 mg, tramadol° 25 mg, and prednisone^p 2.5 mg.

The patient was reexamined five times in the subsequent 3 mo. On all but the last occasion, foreign material could still be visualized in the ocular adnexa of the OS in diminishing quantities. At the third recheck examination, which was 5 wk after initial presentation and surgery, the corneal ulcer was smaller but still retained fluorescein dye. Within the stroma beneath a nonulcerated region of cornea, a nebular white infiltrate could be visualized. Despite re-epithelialization of the majority of the corneal defect, the patient had marked epiphora and appeared to be more painful than at the prior surgical recheck examinations. Based on lack of complete resolution with prior medical treatment, appearance of stromal infiltrate, and increased discomfort, an antifungal^q medication was prescribed for topical application q 8 hr. Collection of cytology and culture was discussed but not performed to avoid further disruption of corneal epithelium and additional owner expense. Resolution of clinical signs occurred approximately 3 mo after date of injury with prolonged medical management and surgical excision.

The conjunctival tissue that was surgically excised on the day of initial presentation was examined via light microscopy at low power. The tissue was stored in a sterile red-top tube with alcohol since surgery; no staining or histological preparation of tissue was done. The tissue appeared transparent with a brownish hue, possibly due to use of dilute povidone iodine^r used to prepare the eye for surgery. Throughout the tissue sample, numerous round, purple-colored structures associated with transparent linear structures that had a slight green hue could be seen. Additionally, multiple hollow, brown-colored, linear structures with external sharp, thorn-like protuberances were seen diffusely throughout tissue sample (Figures 1A, B).

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Identification of the foreign material was pursued. Based on morphologic appearance and the environment where the injury occurred, the brown barbed structures were speculated to be setae from a New World tarantula of the Theraphosidae family. The Arizona Blond was considered most likely, but over 30 species of tarantula can be found in Arizona.^2,15 Microscopic examination of known Arizona Blond hair samples collected at the Phoenix Zoo and consultation with an entomologist specializing in arthropod setae injuries confirmed these structures to be tarantula hairs, specifically urticating setae (Andrea Battisti, PhD, University of Padua, email communication, October 2013).^2,18 The remaining structures that underlie the central seta in the tissue sample seen in Figure 1B were morphologically identified as fruiting bodies (red arrow), microconidia (red star), and hyphae (open arrow) of Aspergillus spp. The tarantula hair samples collected from the zoo were also evaluated for the presence of fungal organisms; Aspergillus was morphologically identified and grown on culture. Unfortunately, the exact species could not be determined.

Discussion

Corneal ulceration associated with corneal and conjunctival foreign material is common in the canine patient. This, however, is the first report in the veterinary literature of keratoconjunctivitis with corneal ulceration secondary to injury from tarantula hairs. To the authors' knowledge, it is also the first report in the scientific literature to document the presence of Aspergillus associated with tarantula setae both in a natural environment and in a zoo setting.

The human literature includes thirteen cases of ocular injury suspected to be secondary to tarantula hairs.^3–14 In all but one, the patient was a male, ranging in age from 9 to 29 yr old, handling a pet tarantula. Resolution of clinical signs with use of topical corticosteroids was reported to occur in as little as 2 wk, but, most often, resolution was achieved in a time period closer to 12 mo. One patient required a pars plana vitrectomy for resolution of clinical signs. Injury was noted at all layers of the eye in these reports and is attributed to the barbed structure of setae that effectively promotes migration and prevents removal. Aside from the technical difficulty of removing setae, there is evidence from a study of 543 human patients with ocular injury due to caterpillar setae that removal does not reduce the risk of intraocular penetration, which can occur as late as 6 mo after injury.¹⁶ Caterpillar setae from this particular species have a nearly-identical structure to tarantula setae (Andrea Battisti, PhD, University of Padua, email communication, October 2013).¹⁷ Etiologic diagnosis in patients with tarantula-hair-induced ocular injury was based on history of exposure to a tarantula, most commonly a household pet. There are no reports of concurrent fungal infection secondary to tarantula hairs in the human eye.

Ocular injury and inflammation due to insect hairs is sometimes labeled Ophthalmia Nodosa in the human literature. The term originated in 1904 and was used to describe initiation of granulomatous nodules on uveal and conjunctival tissue secondary to contact with caterpillar hairs.¹ Multiple past and present reports of ocular injury caused by caterpillar hairs exist in the physician literature and the term has been adapted to describe any type of ocular inflammatory reaction to insect hairs (setae) or plant material. Before the availability of topical corticosteroids, patients suffering from Ophthalmia Nodosa were at risk for developing a devastating endophthalmitis, which led to enucleation.¹⁸ This outcome has not been confirmed in the veterinary medical literature.

Setae are specialized hairs on the dorsal abdomen of some tarantulas in densities that range from hundreds to tens of thousands per square millimeter.² The term urticating hair is often applied to the setae of New World tarantulas, specifically the family Theraphosidae, which are known to use their hind legs to flick these hairs toward perceived threats.^2,18 There are four types of urticating hairs described; often, more than one type is found on an individual tarantula.² The Arizona Blond tarantula is known to carry at least four distinct types of hair, including at least two urticating types.² The sample from our patient contained type III hairs, which have been shown to be capable of penetration to a depth of 2 mm or more in less than 30 min.² Migration is worsened by rubbing, a commonly observed response to ocular foreign bodies.² There has been much speculation over the mechanism for inflammation caused by setae. The consensus in the human literature seems to be mechanical irritation or a granulomatous hypersensitivity reaction, although these hypotheses have not yet been proven.¹⁸ The inflammation may be a reaction to the protein composition of setae that is recognized as foreign by the immune system of mammals. Setae are composed of chitin, which is itself known to be proinflammatory, but it is also known to provoke an antibody-mediated response and an indirect T-cell mediated response by stimulation of chitinases from macrophages.¹⁸ Finally, it has also been theorized that tarantula setae may contain a toxin-like protein that induces the extreme inflammatory reaction and discomfort created by contact with these hairs. This has been proven in the caterpillar setae and the hypothesis is currently being investigated in Italy (Andrea Battisti, PhD, University of Padua, email communication, October 2013).

While the source of ocular injury in the patient described in this report was unexpected, the presence of Aspergillus associated with the setae was also unanticipated. None of the cases reported in the human literature describe an associated fungal infection with this type of ocular injury, though many describe the presence of white stromal infiltrates.^3–14 The authors of this report believed this was likely due to the fact that pet tarantulas were the source of human ocular injury, unlike our patient, who encountered a spider in its natural environment where this fungus would be abundant. Hairs from an Arizona Blond tarantula were collected at the Phoenix Zoo to aid in setae identification for this case; these hairs were also submitted for fungal culture and identification (Figure 1A). The culture from the Arizona Blond zoo tarantula hairs was also positive for Aspergillus, a very unexpected finding. Unfortunately, Aspergillus cultured from these hairs could not be further speciated.

There are likely many explanations for this finding, but simple contamination of the sample was unlikely due to the sampling process. Hairs were collected by gently rubbing the spider's dorsal abdomen with a cytobrush^s from a newly opened package and placing the brush immediately in a sterile red-top tube^k. Tarantulas at the zoo are kept indoors in regularly cleaned, plastic containers filled with sterilized sand intended for use in sandboxes. While it is certainly possible that the substrate or diet could be the source of this fungus, our findings suggest that Aspergillus may be a commensal organism found in association with tarantula hairs irrespective of the environment.

A few reports of an association between presence of Aspergillus and arthropods can be found in the scientific literature. A report of fungi cultured from 1,687 wild arthropods collected over a 2 yr period found approximately 40% of arthropods cultured positive for Aspergillus spp.¹⁹ Another study reported a few incidences of Aspergillus on flies living around livestock.²⁰ A third study that collected 180 arthropods found in document archives in Portugal reports 16 positive cultures for Aspergillus.²¹ All of these reports speculate that the Aspergillus originated from an environmental source and was not a commensal organism. They do, however, substantiate the idea that arthropods can act as vectors for fungi, such as Aspergillus. While our single report cannot prove that Aspergillus lives as a commensal organism on tarantulas in every environment, it certainly suggests that fungi may not originate solely from environmental elements. It is also possible that Aspergillus spp. are so ubiquitous that it may be reasonable to find it in an environment consisting of a plastic container filled with sterilized sand and kept indoors.

The final diagnosis of keratoconjunctivitis secondary to tarantula hairs was made based on multiple factors including patient history and signalment, the environment where injury occurred, and the characteristics of the linear foreign bodies. The foreign material visualized in the ocular tissues was originally presumed to be glochids, small spines from a cactus of the Opuntieae family.²² Based on the authors' clinical experience, cactus material accounts for the majority of ocular injury due to foreign body in veterinary patients in the desert Southwest. The brown color of the foreign bodies in our patient, however, was inconsistent with most glochids, which appear clear to yellow in color. Glochids are also generally much larger than setae—4 to 8 mm compared to 0.3 to 1 mm (Figure 2). In addition, the inability to easily remove the foreign structures from the conjunctiva and absence of obvious cacti in environment where injury occurred led us to consider other types of foreign material.

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Signalment and history were also considered when arriving at the etiologic agent in this case report, as it is in the physician literature. The rat terrier is specifically bred to hunt vermin in underground burrows, putting it at high risk for this type of injury.²³ The type of tarantula suspected in this particular case, the Arizona Blond, is known to live in underground burrows in northern Arizona. They are seen most often in the summer months, which is the mating season, and also the season when the injury occurred in our patient. This species is considered docile and generally requires significant provocation to induce this type of defensive response. It is easy to imagine a terrier bred to hunt small prey inciting this level of provocation.²²

While consideration of tarantula hair as the causative agent was based on multiple factors, its final identity was based on expert opinion and microscopic comparison with known samples. Unfortunately, no diagnostic test is available for this particular etiologic agent in human or veterinary patients. One possible diagnostic approach could be use of an assay to detect chitin. As previously mentioned, setae contain chitin, a protein not present in mammalian tissue.¹⁸ This, however, would not have been useful in our tissue sample due to the presence of fungi, which also contain chitin.

Conclusion

In summary, this case report characterizes keratoconjunctivitis with corneal ulceration in a rat terrier due to Theraphosidae tarantula setae for the first time in the veterinary literature. In areas with native tarantula populations or households with pet tarantulas, this should be a differential for a patient presenting with acute onset blepharospasm and epiphora, especially if foreign material can be visualized in the cornea and adnexa. This is also the first report to document the presence of Aspergillus in association with tarantula hairs from the same species of tarantula living in very different environments. This suggests the possibility of a relationship between this fungus and tarantulas, and it also highlights the possibility of setae acting as vectors for fungal infection. Further research is needed to elucidate this relationship. This finding also suggests that cytology and fungal culture should be considered in the diagnostic workup of any case of ophthalmic injury suspected to be caused by tarantula setae. In particularly severe injuries or in cases where resolution is absent or delayed with antibacterial treatment, it may also be appropriate to start empirical topical antifungal treatment while waiting for culture results. This case report contains some unique findings and a new differential diagnosis for veterinary patients presenting with corneal ulcer and conjunctivitis. It also highlights the importance of re-evaluating diagnoses if the clinical picture has inconsistencies or if response to treatment does not proceed as expected. While it has been the experience of these authors that cactus glochids and spines make up the vast majority of corneal and conjunctival foreign bodies in veterinary patients in the desert Southwest, it is important to consider that tarantula setae can cause very similar clinical signs and may warrant different diagnostic and treatment strategies.