Chronic Postoperative Mycobacterium gordonae Endophthalmitis in a Patient with Phakic Intraocular Lens

Abstract

Methods: Case description of a 34 year old woman with chronic granulomatous anterior uveitis following implantation of a phakic anterior chamber intraocular lens (IOL). Aqueous humor was processed for bacterial, fungal culture, and PCR analysis.

Results: PCR for 16S ribosomal RNA universal primers was positive and Southern-blot for Propionibacterium spp was negative. Panfungal PCR was negative. Growth of a pigmented yellow colony was detected on Lowenstein-Jensen medium. The isolate was subsequently identified as Mycobacterium gordonae. The patient was treated for atypical mycobacteria as well as an intracameral injection of moxifloxacin, with resolution of inflammation and improvement in visual acuity.

Conclusions: This is the first reported case of Mycobacterium gordonae chronic postoperative endophthalmitis, and of chronic endophthalmitis following phakic IOL surgery. PCR and cultures were invaluable in making the diagnosis.

• Aqueous humor sample
• atypical mycobacteria
• chronic endophthalmitis
• mycobacterium gordonae
• phakic intraocular lens

Delayed-onset or chronic postoperative endophthalmitis is a well-known late complication of cataract surgery with IOL implantation, but it has not been reported after phakic intraocular lens surgery.1,2 Nontuberculous mycobacteria is an infrequent cause of delayed-onset postoperative endophthalmitis. We present a case of late-onset postoperative endophthalmitis caused by Mycobacterium gordonae after phakic intraocular lens surgery.

A 34-year-old woman presented to the uveitis clinic with an 8-month history of redness, blurred vision, and pain in her right eye. One year earlier she had undergone surgery for high myopia with the implantation of an angle-supported anterior chamber intraocular phakic lens in her right eye. Four months after surgery she developed blurred vision, redness, pain, and loss of vision. She was diagnosed with granulomatous anterior uveitis and treated with topical corticosteroids, antibiotics, and drops for ocular hypertension without improvement, and was referred to the Uveitis Clinic, University of Buenos Aires, Argentina, for a second opinion.

On examination, best-corrected visual acuity (BCVA) of the right eye was 20/80. IOP was 14 mmHg. Slit-lamp examination of the right eye revealed conjunctival and ciliary injection, multiple granulomatous keratic precipitates, anterior chamber (AC) inflammation with 2+ flare and 3+ cells, anterior synechiae, and whitish nodules over the phakic lens and the iris. The principal and the lateral corneal incision had nodules as well (Figure 1). There were no iris transillumination defects. Fundus examination revealed occasional vitreous cells, but was otherwise unremarkable. Examination of the left eye was unremarkable.

Figure 1. Whitish nodules and granulomatous deposits on IOL and iris.

Ultrasound biomicroscopy revealed the presence of granulomatous inflammation of the iris and nodules over the posterior layer of the cornea (Figure 2). A presumptive diagnosis of chronic postoperative endophthalmitis was made. An anterior chamber tap was performed to obtain intraocular fluid for culture and molecular biology studies.

Figure 2. Ultrasound biomicroscopy with nodules over the iris, intraocular lens, and posterior face of corneal incisions.

Aqueous humor was processed for bacterial and fungal culture, direct microscopy, and polymerase chain reaction (PCR) analysis. The sample was inoculated into blood agar, chocolate agar, Brucella blood agar, brain–heart infusion broth, Sabouraud's dextrose agar, and Lowenstein-Jensen medium. Smears were prepared from the aqueous humor aspirate for Gram staining and calcofluor-white and Ziehl-Neelsen stains. PCR was carried out using broad-range eubacterial primers targeting 16SrRNA; Southern blot testing for Propionibacterium spp. and panfungal genome targeting 28SrRNA were performed.3,4

Aqueous humor microscopy was negative. The broad-range eubacterial PCR was positive and Southern blot for Propionibacterium spp. was negative. Panfungal PCR was negative.

After 20 days, growth of a pigmented yellow colony was detected on Lowenstein-Jensen medium (Figure 3). The isolate was subsequently identified as Mycobacterium gordonae according to standard biochemical identification tests, including niacin accumulation, growth at 42 and 44 °C, pigmented production in light and dark, aryl sulfatase activity, catalase, nitrate reduction, and hydrolysis of Tween 80.

Figure 3. Mycobacterium gordonae smooth, round, and pigmented yellow colonies on a Lowenstein-Jensen slant tube.

A loop of mycobacteria grown on Lowenstein-Jensen medium was suspended in 500 μL of TE buffer (10 mM Tris, 1 mM EDTA; pH 8) and inactivated by boiling for 30 min. Template DNA was extracted by using a Wizard Genomic DNA Purification Kit (Promega) according to the manufacturer's instructions. Amplification of a 439-bp fragment from the heat-shock protein 65 (hsp65) gene with primers Tb11 (5′-ACCAACGATGGTGTGTCCAT) and Tb12 (5′-CTTGTCGAACCGCATACCCT) was performed according to the protocol described by Telenti et al.5 For PCR-RFLP assay (PRA), the 439-bp amplified product was digested with BstEII and HaeIII, and analyzed by electrophoresis on a 3% agarose gel. The gel was photographed on a UV transilluminator and restriction patterns were evaluated with the help of an algorithm (outlined on the Internet site app.chuv.ch/prasite/index.html) (Figure 4).5

Figure 4. PRA pattern of Mycobacterium gordonae in 3% agarose gel stained with ethidium bromide. M, molecular weight marker (50-bp ladder); 1, negative control; 2, BstEII 245/120/80 bp and HaeIII 160/140/70 bp; M. tuberculosis H₃R_V (ATCC 27294); 3, BstEII 235/210 bp and HaeIII 130/115 bp; M. gordonae isolate.

The isolated sample was subsequently identified as Mycobacterium gordonae by hsp65 PRA.

Systemic treatment for nontuberculous mycobacteria (NTM) with ethambutol, rifampicin and levofloxacin was started. The patient was referred to an internist for systemic assessment, where no systemic infection was found. The patient also received, 1 month after diagnosis, 2 intracameral injections of moxifloxacin (200 μg in 0.05 mL), 30 days apart.

M. gordonae susceptibility to clarithromycin, rifampin, amikacin, ciprofloxacin, ethambutol, moxifloxacin, trimethoprim-sulfamethoxazole, doxycycline, minocycline, and isoniazid was evaluated using the broth microdilution method of protocol M24-A2 of the Clinical and Laboratory Standards Institute (CLSI).6 The isolate was found to be susceptible to isoniazid, rifampin, clarithromycin, amikacin, ciprofloxacin, moxifloxacin, and trimethoprim-sulfamethoxazole, and resistant to ethambutol, doxycycline, and minocycline. At that time, ethambutol was discontinued.

All systemic therapy was stopped at month 4, because of unplanned pregnancy. Three months after the second intracameral injection and systemic treatment, BCVA in her right eye was 20/30, and she had no pain or redness. Anterior chamber inflammation, including the iris and corneal nodules, had completely resolved. Subsequent follow-up examinations over 12 months have been normal without recurrence of inflammation.

Environmental, atypical, or NTM are defined as mycobacteria other than Mycobacterium tuberculosis and Mycobacterium leprae. They are usually found in soil, dust, and water and are distinguished from M. tuberculosis and M. leprae by the fact that they are not obligate pathogens, but are true inhabitants of the environment.7 Over 100 species of NTM have been identified, but only around 15 are considered to be pathogenic, causing pulmonary, lymph node, skin, and disseminated disease in humans. Several reports from western countries have suggested that the incidence of NTM disease is increasing.8

NTM can cause intraocular infection and also infection of ocular adnexa, conjunctiva, cornea, and orbit.9 Ocular trauma or surgery can exogenously introduce these agents into ocular tissues. Classically, NTM have been divided into Runyon groups I–IV. Mycobacterium gordonae belongs to the group II scotochromogen phenotype, which produces yellow-orange pigment when exposed to light or in the dark.10

Mycobacterium gordonae can contaminate clinical samples from nonsterile sites, such as sputum, making it a problem for many laboratories working with respiratory samples.10 However, M. gordonae can cause clinical disease and was described as producing infections in cystic fibrosis patients, skin, catheter tunnel and exit site infections, granulomatous hypophysitis, colitis, cecum ulcers, and disseminated infections.11,12,13

In our case, Mycobacterium gordonae was isolated from intraocular fluids, taken under sterile conditions, and the sample was processed in a laboratory not related to a hospital, where no other M. gordonae was isolated. The clinical picture, the laboratory results, and the resolution with antibiotic treatment support the etiologic diagnosis. The UBM shows the granulomas located inside the eye, mostly over the surgical incisions, leaving no doubt as to the source of the intraocular contamination.

Late postoperative NTM endophthalmitis has been reported in just 15 cases.10 None of these cases followed phakic intraocular lens surgery, and none were caused by M. gordonae. Ramaswamy et al. presented a case of postoperative endophthalmitis due to Mycobacterium chelonae after an extracapsular cataract extraction and posterior chamber intraocular lens implantation. Direct smear and culture of aqueous aspirate were negative for bacteria, fungus, and mycobacteria. But when the eye worsened, a corneal scraping of the infiltrate at the cataract wound site revealed the presence of acid-fast bacilli and the culture identified a Mycobacterium chelonae subspecies abscessus.14

This case illustrates that delayed postoperative endophthalmitis caused by Mycobacterium gordonae can occur after phakic intraocular lens surgery and can present as a chronic granulomatous iridocyclitis. The laboratory results allowed us to make the etiologic diagnosis and to choose the appropriate therapy. This led to an effective control of the infection, leaving the eye without intraocular inflammation, with good final visual acuity and with the phakic IOL in place

Declaration of interest

The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.