Journal Pre-proof Multimodal imaging of a choroidal granuloma as a first sign of tuberculosis Funda Ebru Aksoy, Cigdem Altan, Berna Basarir
PII:
S1572-1000(19)30458-2
DOI:
https://doi.org/10.1016/j.pdpdt.2019.101580
Reference:
PDPDT 101580
To appear in:
Photodiagnosis and Photodynamic Therapy
Received Date:
14 September 2019
Revised Date:
6 October 2019
Accepted Date:
15 October 2019
Please cite this article as: Aksoy FE, Altan C, Basarir B, Multimodal imaging of a choroidal granuloma as a first sign of tuberculosis, Photodiagnosis and Photodynamic Therapy (2019), doi: https://doi.org/10.1016/j.pdpdt.2019.101580
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CASE REPORT
Multimodal imaging of a choroidal granuloma as a first sign of tuberculosis
Funda Ebru Aksoy, MD*; Cigdem Altan, Assoc.Prof.*; Berna Basarir, Assoc.Prof*
Corresponding Author: Funda Ebru Aksoy, MD e-mail:
[email protected]
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*Istanbul Beyoglu Eye Education and Research Hospital, TURKEY.
HIGHLIGHTS
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We have no conflict of interest.
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Telephone: 00905052422826
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Address: Barbaros Mah. Veysi Paşa Sokak Atalar Sitesi 11.Blok Daire: 22 Koşuyolu7Istanbul
Choroidal granuloma of ocular Tuberculosis can be the first sign of Tuberculosis.
Choroidal granuloma in tuberculosis can be diagnosed with the use of OCT.
OCT-A may provide useful information about the retinal microvascular involvement in patients with choroidal tuberculoma.
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Abstract
Choroidal granuloma is rarely seen as the first sign of tuberculosis(TB). Here we report a case of a 34year old male with a choroidal mass which was associated with serous retinal detachment on EDIOCT and the “contact sign” between the neurosensory retina and the retinal pigment epithelium. We analysed the macular microvascular features of tuberculoma with Optical Coherence Tomography Angiography(OCTA). After 3 months of antituberculosis treatment, we observed the shrinkage of
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granuloma with permanent changes of macular microvasculature in deep capillary plexus and choriocapillaris. In conclusion, OCT-A may provide useful information about the retinal microvascular involvement in patients with choroidal tuberculoma.
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Key Words: Tuberculosis, choroidal granuloma, optical coherence tomography angiography
Introduction Posterior uveitis is the most common presentation of intraocular tuberculosis[TB], with lesions predominantly present in the choroid as focal, multifocal or serpiginous choroiditis, solitary or multiple choroidal nodules, choroidal granuloma [tuberculoma], neuroretinitis, subretinal abscess, endophthalmitis, panophthalmitis, and occlusive retinal vasculitis. The choroid is the most frequently
affected structure in ocular TB[1]. Choroidal granuloma of ocular TB clinically resembles other conditions such as central serous chorioretinopathy, choroidal metastases, melanoma of the choroid,
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and age-related macular degeneration.
Thus far, indocyanine green angiography [ICGA] has been accepted as the gold standard imaging
modality for the diagnosis choroidal granulomas[2]. In addition to this, enhanced-depth imaging optical coherence tomography [EDI-OCT] has been considered to be a useful technique for the
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visualization of these lesions, in vivo[3].
Salman et al. described features of a tubercular granuloma on spectral domain OCT [SD-OCT]. They
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revealed the 'contact sign' which was described as an attachment between the retina pigment epithelium-choriocapillaris layer and the neurosensory retina over the granuloma. This was also found
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to be associated with surrounding subretinal fluid[4].
Optical coherence tomography angiography [OCT-A] is a newly developed, non-invasive method for imaging of retinal and choroidal blood circulation without the need of a dye. This method allows us to
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get segmented en-face images[OCT angiograms] of blood flow in the superficial, intermediate and deep retinal capillary plexuses, the outer retina, the choriocapillaris and other areas of interest. It also can help us to visualize a detailed view of the retinal vasculature and shows the foveal microvascular
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abnormalities in patients with diabetic eye disease and other vascular occlusions.[5] In this report, we perform the quantitative analysis foveal microvasculature and blood flow in the in a
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case of subfoveal choroidal granuloma as the first sign of TB by using OCT-A. Case
A 34 year old male patient was admitted to our clinic with blurred vision in the right eye for 10 days. His visual acuity was finger counting from 2 meters in his left eye and 20/20 in the right eye according to the Snellen. Biomicroscopic examination revealed that there was +2 anterior chamber reaction and granulomatous keratic precipitates in the Arlt triangle in the left eye. Fundus examination showed that there was an elevated yellowish choroidal lesion at the macular region.
Blood work-up revealed a normal angiotensin-converting enzyme titer and negative toxoplasma, syphilis and HIV serologies. QuantiFERON-TB test was positive and the enduration measured after purified protein derivative[PPD] skin testing was 20 mm. In OCT analysis there was a choroidal mass associated with a serous retinal detachment and 'the contact sign' which represents the adhesion zone between the retinal pigment epithelium– choriocapillaris layer and the neurosensory retina over the granuloma. Central foveal thickness was was 239 in normal eye and 248 in the affected eye. Fundus florescein angiography[FA] revealed early hypofluorescence and late hyperfluorescence at the macular region and the lesion showed early and
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late hypocyanescence on ICGA.[Figure 1 A-B]
We performed OCT-A [RTVue XR Avanti; Optovue, Fremont, CA] imaging with a scan size 6x6 mm. Evaluation with OCT-A at presentation revealed that flow area[FA] in choriocapillaris layer was slightly greater in the healthy eye than the affected eye.[19.76 mm2, 18.51 mm2,respectively].
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Superficial foveal avascular zone[FAZ] was 0.27 mm 2 in the right eye and 0.24 mm 2 in the affected eye, whereas deep FAZ was 0.28 mm 2 in normal eye and 0.35 mm 2 in the affected eye. We
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compared the vessel densities[VD] between two eyes and > 2 % considered as relevant difference[6]. Vessel density analysis showed that VD in superficial capillary plexus[SCP] was similar
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in both eyes. However, VD in deep capillary plexus[DCP] in all quadrants of parafoveal and perifoveal region were lower in the affected eye[Table 1].
The patient was consulted to pulmonary medicine department and no pulmonary or systemic
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involvement was detected. The lesion was accepted as isolated choroidal tuberculoma was retained and antituberculosis therapy[ATT] was given with doses of isoniazid 5 mg/kg, rifampin 10 mg/kg, ethambutol 15 mg/kg/day, and pyrazinamide 25–30 mg/kg/day. Oral corticosteroid [32 mg/day] was
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also added to ATT concomitantly. The patient was given intensive theraphy for two months and at least 18 months of consolidation theraphy with isoniazid and rifampin was planned. At the third
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month of treatment, granuloma and SRS was resorbed [Figure 2] and visual acuity was increased to 0.8 according to the Snellen. However, OCT-A imaging showed that FA in choriocapillaris layer of the affected eye was still diminished (19.77 mm2 in healthy eye and 18.15 mm2 in the affected eye) and deep retinal VD was still lower in the affected eye compared to the healthy eye[Table 1].
Discussion
There are only a few cases of choroidal granuloma in the literature being the presenting sign of TB[6]. In this report, we perform the quantitative analysis foveal microvasculature and blood flow in a case of subfoveal choroidal granuloma as the first sign of TB by using OCT-A.
Intraocular tuberculosis is an inflammatory choriocapillopathy documented with imaging and histopathologic studies. Indocyanine green angiography has been accepted as the gold standard imaging modality for the diagnosis choroidal granulomas[7]. Granuloma occupying full thickness of
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choroidal stroma remains hypocyanescent throughout the ICGA and commonly, the tubercular
granulomas detected on ICGA correspond to the lesions seen on EDI-OCT. Invernizzi et al. revealed
that measurements of choroidal granulomas on EDI-OCT could be useful in monitoring the response to treatment in patients with choroidal granulomas[4].
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Salman et al described a specific feature as the "contact sign" which is the attachment between the RPE–choriocapillaris layer and the neurosensory retina over the TB granuloma with the use of
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OCT[5]. In this case we also diagnosed TB with this finding and confirmed with PPD and QuantiFERON-TB tests. In EDI-OCT, we detected the boarders of hyporeflective granuloma and we
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also documented the lesion with the use of ICG. After 3 months of ATT, we revealed the shrinkage of granuloma and cessation of subretinal fluid in the OCT images.
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Diminished parafoveal VD in DCP were reported in the other retinal vascular diseases such as retinal vein occlusions and diabetic retinopathy with the use of OCT-A[8]. Khairallah et al performed qualitative analysis of retinal capillary perfusion on active phase of Behcet uveitis(BU) and reported that DCP is more severely impaired than SCP in the active phase of BU[9]. In our case, despite the healing and shrinkage of choroidal granuloma on EDI-OCT, OCT-A analysis showed that this DCP damage caused by TB granuloma was permanent. As cones prevail, macula has the highest oxygen consumption[6]. A cessation in blood flow from choriocapillaris due to macular choroidal granuloma could lead to high metabolic stress and microischemia. However foveal VD measurements were similar between two eyes. Possible reasons in the literature for this finding are that, 1) the wide variations in foveal VD in healthy eyes [10], 2) 1-mm ring around the fovea is a capillary-free
zone, and this measurement could be an artifact from the software overestimating the VD in this region[11]. Imaging techniques, such as FA and B-mode ultrasonography, can help us to exclude other diagnoses, especially intraocular tumors [e.g., melanoma] or infective abscesses [2]. However, in this case the diagnosis was confirmed by laboratory tests and specific OCT findings. In conclusion, OCT-A may provide useful information about the retinal microvascular involvement in patients with TB granuloma which supplements the findings of conventional FFA and ICGA in the
diagnosis and management of intraocular TB. Future studies with large sample sizes using OCTA may
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further enhance our understanding of the disease pathophysiology and natural history.
References [1] Gupta V, Shoughy SS, Mahajan S, et al. Clinics of ocular tuberculosis. Ocul Immunol Inflamm. 2015;23:14–24. [2] Herbort CP, LeHoang P, Guex-Crosier Y. Schematic interpretation of indocyanine green angiography in posterior uveitis using a standard angiographic protocol. Ophthalmology 1998;105: 432–440. [3] Invernizzi A, Mapelli C, Viola F, et al. Choroidal granulomas visualized by enhanced depth imaging optical coherence tomography. Retina. 2015;35:525–531.
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[4]. Salman A, Parmar P, Rajamohan M, Vanila CG, Thomas PA, Jesudasan CAN. Optical coherence tomography in choroidal tuberculosis. Am J Ophthalmol. 2006;142[1]:170–172.
[5] De Carlo, T. E., Romano, A., Waheed, N. K., & Duker, J. S. [2015]. A review of optical coherence
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tomography angiography [OCTA]. International Journal of Retina and Vitreous, 1[1], 5.
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[6] Arej, Nicolas, Ali Fadlallah, and Elias Chelala. "Choroidal tuberculoma as a presenting sign of tuberculosis." International medical case reports journal 9 [2016]: 365.
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[7] De Luigi G, Mantovani A, Papadia M, et al. Tuberculosis related choriocapillaritis [multifocalserpiginous choroiditis]: follow-up and precise monitoring of therapy by indocyanine green angiography. Int Ophthalmol. 2012;32:55–60.
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[8] Couturier A, Mané V, Bonnin S, et al. Capillary plexus anomalies in diabetic retinopathy on optical coherence tomography angiography. Retina 2015;35:2384–2391.
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[9] Khairallah, M., Abroug, N., Khochtali, S., et al., [2017]. Optical coherence tomography angiography in patients with Behcet uveitis. Retina, 37[9], 1678-1691.
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[10] Tsai G, Banaee T, Conti FF, Singh RP. Optical Coherence Tomography Angiography in Eyes with Retinal Vein Occlusion. J Ophthalmic Vis Res. 2018;13(3):315–332. doi:10.4103/jovr.jovr_264_17 [11] Coscas, F., Sellam, A., Glacet-Bernard, A., et al. (2016). Normative data for vascular density in superficial and deep capillary plexuses of healthy adults assessed by optical coherence tomography angiography. Investigative ophthalmology & visual science, 57(9), OCT211-OCT223.
Figure legends
Figure 1 A: Fundus photograph and EDI-OCT of the eye with TB choroidal granuloma.[Arrows showing
Figure 1 B: ICGA images of the the eye wih choroidal granuloma.
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the borders of TB granuloma]
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EDI-OCT: Enhanced depth optical coherence tomography, ICGA:Indocyanin green angiography,
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TB:Tuberculosis
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Figure 2: After 3 months of ATT, EDI-OCT revealing the shrinkage of TB granuloma. EDI-OCT: Enhanced depth optical coherence tomography, ATT: Antituberculosis treatment, TB:Tuberculosis
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Table
Table 1: Optical Coherence Tomography Angiography of Macular Microvascular Features of the eye with TB choroidal granuloma and contralateral eye.
Table 1 : Optical Coherence Tomography Angiography of Macular Microvascular Features of the eye with TB choroidal granuloma and contralateral eye Eye with choroidal granuloma Before ATT After ATT
43.4 40.8 46.2 36.2 47.5
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43.0 44.4 41.9 36.4 46.4
50.0 50.5 49.4 22.3 53.9
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48.9 48.4 49.4 22.5 49.8
Contralateral eye
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51.2 51.1 51.3 23.3 50.7
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Capillary Vessel Densities (%) Superficial VD Whole image Superior-Hemi Inferior-Hemi Fovea Parafovea Deep VD Whole image Superior-Hemi Inferior-Hemi Fovea Parafovea
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TB: Tuberculosis, VD:Vessel density, ATT:Antituberculosis treatment
50.2 48.8 51.7 36.9 54.3