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Orbital and conjunctival nontuberculous mycobacteria infection

1 Department of Ophthalmology, Taipei City Hospital, Taipei, Taiwan
2 Department of Ophthalmology, Taipei City Hospital; Institute of Public Health, National Yang-Ming University, Taipei, Taiwan
3 Department of Ophthalmology, Taipei City Hospital; Department of Ophthalmology, National Taiwan University Hospital, Taipei, Taiwan

Date of Submission27-Feb-2022
Date of Acceptance05-Jun-2022
Date of Web Publication25-Aug-2022

Correspondence Address:
Zoe Tzu-Yi Chen,
Taipei City Hospital, No. 145, Zhengzhou Road, Datong District, Taipei City 10341
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/2211-5056.354534


A 64-year-old female developed refractory red-eye with itching and watery discharge 2 weeks after being injured by a comb in the left eye. It presented as diffuse pinkish thickening of the bulbar conjunctiva. Biopsy and histological examinations revealed granulomatous inflammation with microgranuloma. Acid-fast-positive bacilli were found within the tissue, which was identified by culture 5 weeks later as Mycobacterium Abscessus. The orbital computed tomography with contrast medium showed irregular enhancement with an ill-defined margin along the inferior sclera. Due to symptomatic and recurrent bulbar conjunctival thickening and abscess-like lesion formations, wide excision of the conjunctival and orbital granuloma with amniotic membrane transplantation was performed twice. Conjunctiva inflammation subsided after the surgical treatment was combined with 4 months of topical and parenteral antimycobacterial treatment. The presentation, diagnosis, and treatment of ocular nontuberculous mycobacterial (NTM) infection will be discussed in this article. NTM can cause infections of all adnexal and ocular tissues in patients with ocular trauma or surgical history. The pathological findings were granulomatous inflammation without true caseating. Periocular cutaneous, adnexal, and orbital NTM infections remain rare and require surgical debridement and long-term parenteral antibiotic therapy.

Keywords: Acid-fast stain, amniotic membrane transplantation, conjunctival nontuberculous mycobacterial, nontuberculosis mycobacterium

How to cite this URL:
Kuo CT, Chen YT, Tsai IL, Tsai CY, Chen ZT. Orbital and conjunctival nontuberculous mycobacteria infection. Taiwan J Ophthalmol [Epub ahead of print] [cited 2023 Mar 23]. Available from: https://www.e-tjo.org/preprintarticle.asp?id=354534

  Introduction Top

Nontuberculous mycobacteria (NTM), also known as atypical mycobacteria, are opportunistic pathogens that live in natural environments.[1] Since Runyon's microbiologic classification of mycobacteria was developed in 1959, NTM have become increasingly recognized as causes of systemic as well as ocular morbidity.[2] The incidence of NTM-associated disease has been increasing over the past few decades in Taiwan.[3] NTM can cause infections in all adnexal and ocular tissues, mostly by rapidly growing NTM: Mycobacterium chelonae (M. chelonae), M. abscessus, and M. fortuitum. Conjunctival NTM infection is very rare, however. To date, only five cases of NTM conjunctivitis have been published and discussed.[4],[5],[6],[7],[8] Here, we present a case with orbital and conjunctival NTM infection and further compare it with other published cases.

  Case Report Top

A 64-year-old female started to suffer from redness as well as itchy and watery discharge in the left eye 2 weeks after being injured by a comb in the left eye. She had been treated with conventional topical antihistamine and corticosteroids under the tentative diagnosis of allergic reaction, but the treatment failed to resolve the problem. Slit-lamp examination revealed a thickened and pinkish conjunctiva with a mass-like lesion, started inferiorly at first, but it later extended circumferentially [Figure 1]a. The cornea was intact and remained clear. The anterior chamber was free of cells, and the vitreous was clear. The best-corrected visual acuity was 20/20 in both of her eyes. The intraocular pressure was 15.5 mmHg in the right eye and 17.7 mmHg in the left eye. Hertel's exophthalmoscopy measured 17 mm for the right eye and 18 mm for the left eye. The orbital computed tomography (CT) left eye revealed an irregular-shaped, precontrast high-density lesion; enhancement was noted along the inferior sclera, and after contrast medium injection, the sclera could be identified separately from the lesion in the images [Figure 2]a and [Figure 2]b. The pinkish thickening of conjunctiva responded very poorly to medical treatment. Furthermore, the drug penetrance of topical medication was limited. Besides, the area of the lesion extended from the inferior bulbar conjunctiva (from 4 o'clock to 9 o'clock) to the superior bulbar conjunctiva that it became encircled entirely. The rapid growing warrants further confirmation for pathology results. Therefore, an incisional biopsy 1 month later was performed, and it revealed a granulomatous inflammation with microgranuloma. Some acid-fast-positive bacilli were found within the tissue without caseous necrosis [Figure 1]b. No pulmonary involvement was detected, based on the chest X-ray and the sputum culture. Rifampicin 400 mg, isoniazid 320 mg, pyrazinamide 1000 mg, and ethambutol 800 mg daily were given to the patient under the suspicion of tuberculosis infection for 5 weeks. In response to this, only a mild and generalized weakness was documented as adverse effect. The best-corrected vision, the color function tests, and the hepatorenal functions remained normal during the use of the anti-tuberculous medications.
Figure 1: (a) Circumferential pinkish conjunctival thickening with nodular elevations. (b) Histopathological exam showed acid-fast-positive bacilli (arrow)

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Figure 2: (a) Orbital CT scan, coronal view. Orbital extension of lesion inferior to the sclera (arrows). The scleral contour could be identified separately from the lesion. (b) Orbital CT scan, sagittal view. It showed an irregular-shaped lesion inferior to the orbit with precontrast high density (arrows). (c) orbital lesion diminished after 4-month treatment. CT: Computed tomography

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Five weeks after the surgery, the culture revealed M. abscessus. As a result, the medication was shifted to oral ciprofloxacin 500 mg daily and topical amikacin with 50 mg/mL four times a day. However, a few abscesses formed in the lower part of the bulbar conjunctiva, and the conjunctival thickening persisted despite the medication. Therefore, we decided to perform an excision of the involved conjunctiva and tenon capsule. The conjunctival culture was obtained at the site of abscess after gently removal of the conjunctival epithelium. During the excision, the underlying sclera was found to be intact. Amniotic membrane transplantation was arranged simultaneously to avoid a large area of bare sclera and enhance early epithelialization. Pathologic report revealed small abscesses formation with granulation tissue. There were no microorganisms found later. After treatment for 4 months with topical and oral antibiotics, the conjunctiva inflammation gradually subsided [Figure 3] and the CT scan [Figure 2]c showed that the orbital lesion had diminished. There were no prominent complications detected and no recurrence was found within 5 years of follow-up examinations.
Figure 3: After 4-month treatment of topical and oral antibiotics, conjunctiva inflammation gradually subsided, (a) initial presentation, note the abscess formation in the inferior bulbar conjunctiva (asterisk) and conjunctival nodular formations (arrow). (b) one month after the first excision, and (c) four months after the second excision, parenteral ciprofloxacin and topical amikacin treatment

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  Discussion Top

To the best of our knowledge, there are only five cases reported of NTM conjunctivitis –M. chelonae conjunctivitis and scleritis following vitrectomy,[4] M. abscessus nodular conjunctivitis after scleral tunnel incision and phacoemulsification,[5] bacillary angiomatosis with cytomegaloviral and mycobacterial infections of the palpebral conjunctiva in an acquired immunodeficiency syndrome (AIDS) patient,[6] conjunctival granuloma with NTM growth after contact lens use or contact with parrot,[7] and M. abscessus keratoconjunctivitis in a Sjögren's syndrome patient.[8] In the five cases mentioned above, the first two cases were associated with ocular surgery and had subacute to chronic conjunctival injection. These cases exhibited irritation and epiphora for 6 months and 4 years, respectively, before diagnosis. The former case featured a diffuse conjunctival injection, and in the latter case a localized conjunctival nodule noted. The case of the patient with AIDS showed an opportunistic infection, which my mean that immunocompromised individuals may be more susceptible to mixed infections. The patients in other cases had no major trauma, ocular surgery, and were not immunocompromised. The cause may be associated with wearing contact lens and decreased tear film that resulted in minor ocular trauma or impaired ocular surface immune function, respectively. In our case of the 64-year-old female, the conjunctival lesion developed 2 weeks after the trauma occurred. The conjunctiva was injected and thickened with palpable nodules within the conjunctiva were noted during operation with the sclera spared. In brief, risk factors such as trauma, immunocompromise, and disruption of the ocular surface's defense mechanism may have been related to NTM conjunctivitis.

Our patient was initially treated with empirical antimycobacterial agents due to positive acid-fast bacilli found by conjunctival an incisional biopsy. While waiting for culture results, faster diagnostic modalities, such as polymerase chain reaction (PCR) and interferon-gamma release essay (IGRA) may help differentiate between Mycobacterium tuberculosis (MTB) and NTM in these circumstances. Meanwhile, the IGRA tests such as T-SPOT.TB and QuantiFERON-TB Gold are effective ways to detect MTB infection.[9] PCR tests for NTM were not performed for this patient because it was not available in our hospital at the time of diagnosis. However, with the improvement of diagnostic tools, this procedure is now a standard diagnostic modality for us. In terms of IGRA test, because of it is not covered by the National Health Insurance in Taiwan, our patient did not receive this examination.

Chaurasia et al. reported six cases with chronic conjunctivitis caused by MTB.[10] Three of these patients had conjunctival nodular or nodular-ulcerative mass, two patients had conjunctival ulcerations, and one patient had chronic papillary conjunctivitis. Jennings et al. reported a case with MTB as showing chronic red eye with thickened, erythematous conjunctiva overhanging the corneal limbus.[11] With variable conjunctival presentations, all mycobacterium conjunctivitis cases share the same chronicity and positive acid-fast stain. However, in cases where the causative organism is established, proper antibiotics should be administered. The treatments for MTB also differ from NTM. Normally, MTB conjunctivitis is treated with standard anti-TB treatment and may be combined with a topical or oral steroid.[12]

Because of the relative resistance of it to available antibiotics, multidrug parenteral therapy continues to be the mainstay of treatment for more serious ocular and adnexal infections caused by NTM. Slow-growing NTM such as Mycobacterium avium complex, Mycobacterium haemophilum, Mycobacterium kansasii, Mycobacterium malmoense, Mycobacterium marinum, Mycobacterium simiae, and Mycobacterium xenopi are sensitive to the agents typically used to treat M. tuberculosis infections, whereas rapidly growing NTM such as Mycobacterium chelonae, Mycobacterium abscessus, and Mycobacterium fortuitum are sensitive to macrolides, fluoroquinolones, and aminoglycosides.[13],[14] The site of infection determines the route of antibiotic administration. Topical amikacin therapy is widely used for NTM infection. Periocular cutaneous, adnexal, and orbital NTM infections remain rare and require surgical debridement and long-term parenteral antibiotics therapy. Chu et al. reported that M. abscessus and M. massiliense are the two most identified species of NTM ocular infections in Taiwan.[14] Both of these species have similar characteristics, including resistance to fluoroquinolones and susceptibility to amikacin, though they vary in terms of clarithromycin resistance. Accordingly, we switched from anti-tuberculosis drugs to oral ciprofloxacin and topical amikacin once the culture was shown to be M. abscessus.

Surgical excisions were performed in our case for the following reasons. First, the response to the medication for infection control was poor, excision of the conjunctiva has been reported as successful for infection control,[15],[16] and to explore the possibility of scleral involvement. In our case, the area involved had extended posteriorly into the orbit inferiorly. Multiple abscesses developed diffusely and result in a gradually worsened of the condition. The case proved to be resistant to medical controls alone. Second, for drug penetrance, benzalkonium chloride has been used as an absorption promoter,[17] which was absent in fortified amikacin solution. We could see the area involved by using contrast enhancement on the CT scan [Figure 2]a and [Figure 2]b. Although we gave the patient systemic antibiotic treatment, the drug penetrance of topical amikacin was still uncertain. Therefore, a decision was made to perform surgical debridement.

Due to the extended excision of the conjunctiva, the large area of scleral exposure was a major concern. In the previous literatures, modalities such as amniotic membrane transplantation[18],[19] and conjunctival autograft[20],[21] could be used for ocular surface reconstruction. We applied amniotic membrane transplantation to enhance epithelization. Furthermore, the amniotic membrane was reported as having a possible positive effect on reducing the microbial count.[22] It was also applied to prevent symblepharon and fornix shortening due to extended excision into the inferior orbital cavity. As a result of these treatments, the patient recovered well after surgery and there was no evidence of recurrence in the next 5-year follow-ups.

  Conclusion Top

For those with refractory conjunctivitis presenting as a thickening of the conjunctiva with nodular formation, conjunctival NTM infection should be considered as one of the differential diagnoses. These patients may have an ocular trauma or surgical history. An orbital CT is needed to provide a surgical plan when an orbital involvement is suspected. PCR and IGRA tests may provide earlier detection of NTM before the culture result. The pathologic findings were granulomatous inflammation without true caseation; therefore, topical and parenteral antibiotics accompanied by surgical management were recommended in this situation.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient has given her consent for her images and other clinical information to be reported in the journal. The patient understands that name and initials will not be published and due efforts will be made to conceal identity, but anonymity cannot be guaranteed.

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Conflicts of interest

The authors declare that there are no conflicts of interests of this paper.

  References Top

van Ingen J, Boeree MJ, Dekhuijzen PN, van Soolingen D. Environmental sources of rapid growing nontuberculous mycobacteria causing disease in humans. Clin Microbiol Infect 2009;15:888-93.  Back to cited text no. 1
Runyon EH. Identification of mycobacterial pathogens utilizing colony characteristics. Am J Clin Pathol 1970;54:578-86.  Back to cited text no. 2
Lai CC, Tan CK, Chou CH, Hsu HL, Liao CH, Huang YT, et al. Increasing incidence of nontuberculous mycobacteria, Taiwan, 2000-2008. Emerg Infect Dis 2010;16:294-6.  Back to cited text no. 3
Margo CE, Pavan PR. Mycobacterium chelonae conjunctivitis and scleritis following vitrectomy. Arch Ophthalmol 2000;118:1125-8.  Back to cited text no. 4
Merani R, Orekondy S, Gottlieb T, Janarthanan P, McCarthy S, Karim R, et al. Postoperative Mycobacterium abscessus nodular conjunctivitis. Clin Exp Ophthalmol 2008;36:371-3.  Back to cited text no. 5
Edmonson BC, Morris WR, Osborn FD. Bacillary angiomatosis with cytomegaloviral and mycobacterial infections of the palpebral conjunctiva in a patient with AIDS. Ophthalmic Plast Reconstr Surg 2004;20:168-70.  Back to cited text no. 6
Jeng CJ, Hsiao CH, Hu FR, Hou YC. Nontuberculous mycobacterial conjunctival granuloma detected by nested polymerase chain reaction. J Formos Med Assoc 2014;113:760-1.  Back to cited text no. 7
Shumway C, Aggarwal S, Park ST, Wade M, Kedhar S. Complicated case of Mycobacterium abscessus conjunctivitis in Sjögren's syndrome. Am J Ophthalmol Case Rep 2020;19:100765.  Back to cited text no. 8
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Chaurasia S, Ramappa M, Murthy SI, Vemuganti GK, Fernandes M, Sharma S, et al. Chronic conjunctivitis due to Mycobacterium tuberculosis. Int Ophthalmol 2014;34:655-60.  Back to cited text no. 10
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Shakarchi FI. Ocular tuberculosis: Current perspectives. Clin Ophthalmol 2015;9:2223-7.  Back to cited text no. 12
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  [Figure 1], [Figure 2], [Figure 3]


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