Russian Journal of Clinical Ophthalmology
ISSN 2311-7729 (Print), 2619-1571 (Online)

Thermography in posterior scleritis

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DOI: 10.32364/2311-7729-2020-20-4-204-208

A. Kawali, S. Sanjay, P. Mahendradas, R. Shetty

Narayana Nethralaya Eye Hospital, Bangalore, India


Aim: to evaluate the utility of thermography in posterior scleritis (PS).

Patients and Methods: this prospective observational case-control study included 6 patients with monolateral PS (study group) and 10 healthy volunteers (control group). Ocular surface temperature (OST) was measured in all participants using a non-contact thermal camera (FLIRTM) integrated onto a smartphone (CAT S 60). The difference in OST between the affected eye and the healthy (fellow) eye on thermograms (Δt)
was measured at each visit in both groups. Maximum (ΔtMax) and minimum (ΔtMin) Δt for each eye as well as the amplitude of fluctuations
(ampΔt) referred to as the difference between ΔtMax and ΔtMin were calculated for each eye. AmpΔt was compared between the groups.

Results: in a total of 6 PS patients, B-scan ultrasonography revealed the thickening of the posterior sclera. Choroidal folds (n=4), internal limiting membrane fold (n=2), subretinal fluid (n=3), and optic disc edema (n=2) were identified by eye fundus exam. At presentation, Δt was maximum in all PS patients and reduced unequally after starting treatment. Mean ampΔt was 1.21 °C (1.47–1.04 °C) in PS group and 0.44 °C (0.13–0.63 °C) in the control group. 3 out 6 PS patients were diagnosed with recurrences as demonstrated by OST spikes compared to previous measurements.

Conclusion: this article describes a novel technique of the measurement and monitoring of OST. It was demonstrated that PS is associated with the increase in OST measured by thermography. Further large-scale studies are needed to evaluate the potentialities of thermography for detecting occult or subclinical intraocular inflammation.

Keywords: ocular thermography, posterior scleritis, ocular surface temperature, eye temperature, occult inflammation.

For citation: Kawali A., Sanjay S., Mahendradas P., Shetty R. Thermography in posterior scleritis. Russian Journal of Clinical Ophthalmology. 2020;20(4):204–208. DOI: 10.32364/2311-7729-2020-20-4-204-208.



Background

The role of thermography in medicine is significant and well-known. This technique is widely applied in rheumatology, oncology, dermatology etc. [1–4]. In ophthalmology, the measurement of ocular surface temperature (OST) was previously uncommon since old-style thermographs implied contact measurements [5]. Thermistor and thermocouple measured the temperature between air and corneal surface. In addition, the probe itself provided a cooling effect [6]. Radiometric devices, e.g., bolometer, are non-contact but should be placed very close to the corneal surface thus provoking a negative patient’s reaction [7]. In 1968, R. Mapstone used a bolometer and revealed an increased corneal and periorbital skin temperature in a total of 53 patients with anterior uveitis [8]. Later on, he described thermographic patterns of the healthy eye and in various ocular diseases using an infrared camera [9].

As the non-contact ocular thermography evolved [10, 11], the importance of OST in dry eye disease (DED) and other ocular surface disorders, anterior uveitis etc. began to unravel [11-13]. It was demonstrated that OST reduces in DED [11]. In keratitis resulting from meibomian gland dysfunction, lower corneal temperature was also reported [13]. This phenomenon can be accounted for by increased tear film evaporation which cools ocular surface.

Various ocular inflammatory conditions can be diagnosed by routine slit lamp examination. However, in occult inflammation, e.g., in posterior scleritis (PS), more careful examinations are required. In some cases, the diagnosis is still challenging since clinical examination and B scan provide insufficient data. Ocular thermography which detects an elevated OST can help suggest an inflammation.

This technique is also useful in monitoring OST. Finally, in situations like lockdown when a patient cannot visit a doctor, this simple handheld non-contact device helps evaluate the severity of inflammation via telemedicine.

Therefore, our aim was to evaluate the utility of thermography in terms of identifying an elevated OST in verified PS and the fluctuations of OST during the follow-up after starting treatment.

Methods

This prospective observational case-control study was performed from May 2017 to May 2019. FLIR™ thermal camera integrated onto a Cat S 60™ mobile phone was used for thermography (thermal resolution 80 × 60,9 Hz, sensitivity 0.15°C). All measurements were performed in a single room of a tertiary eye center. The study was approved by the Institutional Review Board and conducted in accordance with the Helsinki Declaration.

The diagnosis of PS was verified using previously reported clinical and ultrasonographic criteria [14, 15]. The study enrolled the patients with unilateral PS who were followed-up using thermography for at least 4 consecutive visits. The patients who already received treatment and the patients with no clinical recovery were excluded from the study. The patients with bilateral PS were also excluded. Hospital healthcare workers were examined and included in the control group. The patients with ocular (other than PS) and systemic conditions which potentially affect OST measurements (e.g., DED, inflammatory disorders of the orbit and ocular adnexa, ocular ischemic syndrome, the history of recent sinusitis or fever) were excluded as well. Thermography was performed in the lack of contact lenses, mascara or other cosmetics. All participants were examined by a single ophthalmologist. Slit lamp exam and dilated fundus exam (indirect ophthalmoscopy) were performed by a single ophthalmologist in the same room using the same equipment in all participants. Thermography was performed 5 minutes after eye examination in the same room by the same ophthalmologist. Thermal camera (Cat S 60 smartphone) was placed close to a patient’s face (approximately one foot) in order that the face fully comes to the thermographic screen (the temples are on the edges of the screen, the forehead and the nose are visible in the thermograph, the eyes are in the center; see Fig. 1).


Рис. 1. Термография пациента № 6, первый визит. А — белый цвет на OD свидетельствует о повышенной ТГП по сравнению с OS. На экране справа — тепловая шкала от более низкой температуры (внизу) к более высокой (вверху). B — измерение проводилось в трех точка

The patients were asked to blink once just before taking a thermal snap. The same protocol was followed at each visit in all PS patients and healthy controls. Controls were examined every 5 days for 3 weeks (in total, 4 visits). The patients with clinically presumed PS underwent thermography and B-scan ultrasonography to measure the thickness of the posterior sclera and to verify the diagnosis. PS patients were prescribed with peroral non-steroidal anti-inflammatory drugs (NSAIDs) and/or peroral and topical steroids and immunomodulatory drugs on an as-needed basis. After starting the treatment, routine ocular examination and thermography were performed at each follow-up visit using the same protocol as described above.

The qualitative and quantitative analysis of thermographs was performed by a single researcher (see Fig. 1). The affected eye and the healthy (fellow) eye were compared based on OST as assessed by the “hot” and “cold” colors on thermographs using a color scale (see Fig. 1). OST difference between the affected and healthy eye was calculated (Δt) using a built-in mobile app “FLIR Tools”. In the control group, the difference between the eyes with the highest and the lowest OST measured at the first visit was regarded as Δt. The mean of three measurements in the points on a horizontal plane above each eye was calculated to obtain OST value for this eye (see Fig. 1). Maximum (ΔtMax) and minimum (ΔtMin) Δt for each eye as well as the amplitude of fluctuations (ampΔt) referred to as the difference between ΔtMax and ΔtMin were calculated for each eye (see Fig. 2).


Рис. 2. График изменения ТГП у пациента № 6 с ЗС, по- казывающий разницу температур (Δt) между пораженным и здоровым глазом, а также амплитуду колебаний (ampΔt) Fig. 2. Changes is OST in a patient with PS. The plot demonstrates the differences in OST (Δt)

Results

6 patients with PS (3 men and 3 women) and 10 healthy controls (2 men and 8 females) who met all eligibility criteria were enrolled. At presentation, mean age was 45.33 years (22-59 years) in the study group and 45.00 years (23-58 years) in the control group. All 6 PS patients complained of pain and 4 PS patients complained of low vision of the affected eye. Mild superior conjunctival congestion was reported in 4 PS patients. No other anterior segment diseases were revealed. Choroidal folds (n = 4), internal limiting membrane folds (n = 2), subretinal fluid (n = 3), and optic disc edema (n = 2) were identified by fundus examination. In a total of 6 PS patients, B-scan ultrasonography revealed the thickening of the posterior sclera (2.1-3.94 mm). Nodular PS diagnosed in three patients (see Fig. 3).


Рис. 3. В-сканирование пораженного глаза у пациента № 6 с ЗС; отмечается узловое утолщение задней склеры со скоплением жидкости в субтеноновом пространстве Fig. 3. B-scan of the affected eye (PS patient No. 6). Nodular thickening of the posterior sclera a

In patient 1, ΔtMax (during the active inflammation) was 1.77°C and ΔtMin (after the resolution) was 0.43°C. Therefore, ampΔt was 1.34°C. In patient 2, ΔtMax, ΔtMin, and ampΔt were 0.6°C, -0.4°C, and 1°C, respectively. AmpΔts for all PS patients were calculated based on Δt, ΔtMax, and ΔtMin values (see Table 1). AmpΔt was found to be lower in the control group than in the study group, i.e., 0.44°C (0.13-0.63°C) vs. 1.21°C (1.47-1.04°C). 3 out 6 PS patients were diagnosed with recurrences after steroid tapering as demonstrated by OST spikes compared to previous measurements.


Таблица 1. Амплитуда колебаний Δt Table 1. Amplitude of Δt fluctuation

Discussion 

Elevated OST associated with ocular inflammation (other than PS) has been previously reported [13, 16]. PS is commonly underdiagnosed due to the lack of experience, occult inflammation or atypical presentations. Routine B-scan ultrasonography detects posterior scleral thickening that can be a masquerade syndrome without any inflammation. The pain that is often associated with PS varies from patient-to-patient and can occasionally be missing. OST measurements help clinicians suggest an inflammation. Our study demonstrated greater OST fluctuations in PS eyes compared to the fellow (healthy) eyes, i.e. OST increases in active inflammation and reduces to the baseline after its resolution. In addition, healthy eyes are also characterized by variable OST. However, these fluctuations are insignificant compared to affected eyes.

Inconsistency in OST measurements between the visits is a major challenge in terms of accuracy. To address this issue, we measured OST difference between the eyes using the same thermograph rather than OST of an individual eye during various visits using different thermographs. Therefore, we evaluated Δt rather than measuring OST of the affected eye only and monitoring its fluctuations. This approach helps avoid the dynamic biases resulting from the effects of external factors (i.e., atmospheric temperature changes, humidity, and radiation), patient factors (i.e., body temperature variability, ocular circulation), and instrumental factors (thermal camera provides variable OST measurements even in the same position). Δt measurements using the same thermograph can partially or totally eliminate these biases. In the control group, OST variability of each eye was significant between the visits. However, OST difference between the right and the left eye (Δt) was much less. Therefore, Δt is a relatively stable parameter to analyze the actual changes in OST between the visits.

Minor (less than 0.62 °C) OST difference between two eyes can occur even in healthy individuals [17]. Therefore, a unilateral disease can be suggested if OST difference between the eyes is more than 0.6°C. However, this is not always the case. Thus, in PS patient 4, ΔtMax was as low as 0.3°C. Meanwhile, this patient was diagnosed with an active inflammation. As the inflammation resolved, Δt reduced to -0.8°C thus demonstrating that the basal temperature of the affected eye was lower than that of the healthy eye. AmpΔt is a reliable indicator when monitoring OST in patients with unilateral ocular inflammation. Similarly, IOP fluctuations measured by non-contact tonometry were reported in healthy eyes. Any deviations from the normal ampΔt of OST measured by thermography should be considered abnormal and indicative of the inflammation. Mean ampΔt (0.44°C) was significantly lower in the control group than in the study group (1.2°C). Therefore, thermography which detects the increase in OST in verified PS can be used to monitor the inflammation.

The hallmarks of PS (i.e., sub-tenon’s fluid detected by B scan) are not obligatory present. Sometimes, it is difficult to document a local scleral thickening by B scan ultrasonography that can be a masquerade syndrome without any inflammation. Moreover, the lack of choroidal folds or subretinal fluid and mild or no pain make things more confusing. Thermography can differentiate between inflammatory and non-inflammatory conditions. Thus, in different inflammatory entities (e.g., choroidal granuloma and nodular PS), we hypothesize that nodular PS is characterized by higher OST compared to choroidal granuloma. This is accounted for by the thermal conduction of the sclera. Thermography is also useful for telemedicine in situations like lockdown to monitor PS patients. If one knows ampΔt of a certain patient, thermography can help diagnose the recurrence during a teleconsultation. Thermography which uses a handheld non-contact device is also considered a useful tool in bedridden patients or poorly cooperative children to identify occult inflammation. The interest in thermography and its application in many areas of medical practice rapidly grow in the era of the COVID pandemic.

Meanwhile, our study has the limitations, i.e., small sample size, unilateral PS, the use of low-resolution thermal camera, and single observer bias. Nonetheless, we have demonstrated that active occult inflammation (e.g., PS) is characterized by elevated OST. Therefore, the measurement of Δt and ampΔt is important. To our knowledge, this is the first effort to measure OST and to document its changes when monitoring PS patients. Large studies using a high-resolution ocular thermography camera are required to confirm our findings and to assess the usefulness of thermography in other occult ocular inflammatory diseases.


About the authors:


Ankush A. Kawali — MD, DNB, Consultant in Uveitis and Ocular Immunology Department, ORCID iD 0000-0002-5536-8051;


Srinivasan Sanjay — MBBS, DNB, Consultant in Uveitis and Ocular Immunology Department, ORCID iD 0000-0001-9756-1207;


Padmamalini Mahendradas — MBBS, DNB, Head of Uveitis and Ocular Immunology Department, ORCID iD 0000-0002-6137-8870;


Rohit Shetty — Head of Cornea and Refractive Surgery Department, ORCID iD 0000-0002-4556-1587.


Narayana Nethralaya Eye Hospital. 121/C, Chord Rd, Rajajinagar, Bengaluru, Karnataka, 560010, India.


Contact information: Ankush A. Kawali, e-mail: akawali332@gmail.com. Financial Disclosure: no author has a financial or property interest in any material or method mentioned. There is no conflict of interests. Received 23.05.2020. 


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