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Posterior uveitis secondary to an African grey parrot bite

      In North America, approximately 25% of mycobacterial infections present with extrapulmonary manifestations, and only a fraction of those patients present with ocular tuberculosis (TB).
      Hematogenous spread of TB to the eye is more likely to occur than a primary exogenous infection and most commonly affects the uvea due to its high vascular content.
      • Albert D.M.
      • Raven M.L.
      Ocular tuberculosis.
      The diagnosis of ocular TB is often presumptive and based on the presence of characteristic clinical features in conjunction with imaging and laboratory investigations. Although TB is endemic in other countries, it is relatively uncommon in North America and is therefore a less common cause of uveitis.
      • Hong B.K.
      • Khanamiri H.N.
      • Bababeygy S.R.
      • Rao N.A.
      The utility of routine tuberculosis screening in county hospital patients with uveitis.
      • Abu El-Asrar A.M.
      • Abouammoh M.
      • Al-Mezaine H.S.
      Tuberculous uveitis.
      Mycobacterial infection through zoonotic transmission may pose a risk to human health.
      • Dhama K.
      • Mahendran M.
      • Tiwari R.
      • et al.
      Tuberculosis in birds: insights into the mycobacterium avium infections.
      We describe the first reported case of ocular manifestations after avian–human transmission of TB.
      A 50-year-old female was referred for evaluation of floaters in both eyes. Her past medical history was significant for uveitis in her right eye for 6 months, treated initially with prednisolone by another physician. Her best-corrected visual acuity was 20/63−1 OD and 20/25 OS. Slit lamp examination showed pigmented guttae on the corneal endothelium of the right eye. The anterior chamber of the right eye had cell grade of 0.5+ and flare grade of 1+. Examination of the lens revealed bilateral 1+ nuclear sclerosis. Dilated fundus examination revealed a blunted macular reflex and 2+ vitreous haze in the right eye, while the left eye was unremarkable and only demonstrated retinal pigment epithelial damage consistent with senile schisis (Fig. 1).
      Fig 1
      Fig. 1(A, B) Pseudocolour fundus images of the right and left eyes, respectively, demonstrating vitreous cells in the right eye, and an inferotemporal senile schisis in the left eye. (C,D) Green fundus autofluorescence images of the right and left eyes, respectively, demonstrating hypoautofluorescence associated with vitreous cells in the right eye and an inferotemporal area of hypoautofluorescence associated with retinal pigment epithelial damage from senile schisis in the left eye.
      Ultrawide field fluorescein angiography of the right eye revealed diffuse late perivascular and deep choroidal hyperfluorescence with disc leakage. In addition, macular hyperfluorescence with leakage was observed. In the left eye, ultrawide field fluorescein angiography revealed an inferotemporal area of staining without disc leakage (Fig. 2). Swept-source optical coherence tomography was performed and only demonstrated a fine epiretinal membrane and intraretinal fluid in the right eye (Fig. 2).
      Fig 2
      Fig. 2(A,B) Ultrawide field fluorescein angiography (5:00 min) of the right and left eyes, respectively, demonstrating late disc leakage and deep choroidal hyperfluorescence with leakage, as well as focal macular hyperfluorescence with leakage. Left eye shows inferotemporal staining in the area of retinal schisis. (C,D) Swept-source optical coherence tomography of the right and left eyes, respectively, demonstrating a fine epiretinal membrane with cystoid macular edema in the right eye and a normal left eye.
      On further history, it was revealed that the patient kept a pet African grey parrot. Bite wounds were seen on the patient's hands, which occurred throughout the year before her presentation in the clinic (Fig. 3).
      Fig 3
      Fig. 3(A) Photograph of the parrot bite wounds on the patient's right hand. A central healing eschar surrounded by an area of erythema (inset). (B) Photograph of the African grey parrot.
      The results of a complete uveitis work-up, including angiotensin converting enzyme, lysozyme, rapid plasma reagin, syphilis testing (fluorescent treponemal antibody absorption test), human leukocyte antigen-B27, rheumatoid factor, antidouble-stranded DNA, and Lyme antibody titres, were unremarkable. A purified protein derivative skin test was not performed, as the patient previously received the bacille Calmette-Guerin vaccination.
      Although inflammation in the anterior segment was responsive to topical steroids, the posterior segment inflammation persisted. Anterior chamber and vitreous taps were collected in the clinic and sent to a local public health laboratory for polymerase chain reaction (PCR) testing. Both samples were positive for Mycobacterium tuberculosis. QuantiFERON-TB Gold blood testing was also performed and was positive for M tuberculosis.
      The patient was subsequently referred to an infectious disease clinic for complete work-up and treatment. Chest radiograph and computed tomography were both negative for pulmonary TB. The intensive phase of her treatment lasted 2 months and involved administration of isoniazid, rifampin, pyrazinamide, and ethambutol. She remained on isoniazid and rifampin for an additional 10 months.
      She was treated with a dexamethasone intravitreal implant (Ozurdex) twice during the first 6 months of follow-up for management of cystoid macular edema. Her visual acuity after resolution was 20/32 OD and 20/25 OS.
      Ocular TB may present with involvement of the inside of the eye (uvea, retina, optic nerve), the surface of the eye (cornea, sclera, conjunctiva), or its surroundings (orbit, eyelids).
      • Goyal J.L.
      • Jain P.
      • Arora R.
      • Dokania P.
      Ocular manifestations of tuberculosis.
      Particularly, tuberculous uveitis is most commonly seen and may be acquired through direct mycobacterial infection of the eye, hematogenous spread of bacteria, or an immune-mediated hypersensitivity reaction from a remote or systemic TB infection.
      • Albert D.M.
      • Raven M.L.
      Ocular tuberculosis.
      Tuberculous uveitis is a vision-threatening disease, thereby necessitating prompt diagnosis and treatment to reduce morbidity.
      Confirming TB as the cause of a patient's uveitis can be challenging. More often, the patient is treated based on a presumptive diagnosis with a high index of clinical suspicion.
      • Abu El-Asrar A.M.
      • Abouammoh M.
      • Al-Mezaine H.S.
      Tuberculous uveitis.
      • Ang M.
      • Chee S.-P.
      Controversies in ocular tuberculosis.
      In patients with chronic, unexplained uveitis, the presence of risk factors for TB, signs of systemic TB infection, and the exclusion of other potential causes of granulomatous uveitis should prompt suspicion for TB.
      • Abu El-Asrar A.M.
      • Abouammoh M.
      • Al-Mezaine H.S.
      Tuberculous uveitis.
      • Ang M.
      • Chee S.-P.
      Controversies in ocular tuberculosis.
      Investigations, including vitreous tap for a suspected intraocular infection, may support a diagnosis of TB but may not be conclusive. Cultures and staining for acid-fast bacilli from an aqueous or vitreous sample require a large sample volume, have a low yield, and take a long time to complete.
      • Ang M.
      • Chee S.-P.
      Controversies in ocular tuberculosis.
      • Damato E.M.
      • Angi M.
      • Romano M.R.
      • Semeraro F.
      • Costagliola C.
      Vitreous analysis in the management of uveitis.
      Nucleic acid amplification of an ocular sample can be affected by several factors, including the method of DNA extraction and the number of targets used for amplification.
      • Ang M.
      • Chee S.-P.
      Controversies in ocular tuberculosis.
      Systemic steroids are not typically used alone in the management of infectious uveitis, as their immunosuppressive effects can cause the existing TB to flare.
      • Goyal J.L.
      • Jain P.
      • Arora R.
      • Dokania P.
      Ocular manifestations of tuberculosis.
      After 3 months of multidrug systemic anti-TB therapy, the vitreous inflammation resolved; however, resolution of the macular edema was limited and posed a threat to permanent vision loss. Infectious disease specialists were consulted, and it was determined that the patient would benefit from local dexamethasone therapy to control ocular inflammation during concurrent TB treatment.
      It is uncertain how the patient's African grey parrot became infected with TB initially. Several mycobacterium species are known to affect birds, and there have been few reports of avian–human transmission of Mycobacterium avium.
      • Bradbury F.C.S.
      • Young J.A.
      Human pulmonary tuberculosis due to avian tubercle bacilli; report of a case.
      • Kincade G.F.
      Avian tuberculosis in the human.
      The African grey parrot is a known carrier of M tuberculosis and may acquire the bacteria through close contact with their owners, although it is not considered a primary host.
      • Washko R.M.
      • Hoefer H.
      • Kiehn T.E.
      • Armstrong D.
      • Dorsinville G.
      • Frieden T.R.
      Mycobacterium tuberculosis infection in a green-winged macaw (Ara chloroptera): report with public health implications.
      • Schmidt V.
      • Schneider S.
      • Schlomer J.
      • Krautwald-Junghanns M.E.
      • Richter E.
      Transmission of tuberculosis between men and pet birds: a case report.
      A veterinarian consultation facilitated a tracheal swab from the parrot, which was found to be positive for TB by PCR. In this case, the bite wounds on the patient's hands provided a portal of entry for the pathogen.
      This is the first case describing avian–human transmission of TB leading to ocular manifestations. Ocular TB may be diagnosed clinically and in conjunction with laboratory tests that confirm the presence of the bacteria. As seen in our case, imaging with optical coherence tomography and fluorescein angiography, in combination with a thorough history, facilitates an accurate diagnosis.

      Footnotes and Disclosure

      The authors have no proprietary or commercial interest in any materials discussed in this article.

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