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INFRARED

THERMOGRAPHY ON
OCULAR SURFACE
TEMPERATURE: A
REVIEW
Jen Hong Tan, E. Y. K. Ng, U. Rajendra Acharya and Caroline Chee

Abstract - Body temperature is a good indicator of human health. Thermal imaging system
(thermography) is a noninvasive imaging procedure used to record the thermal patterns
using Infrared (IR) camera. It provides visual and qualitative documentation of
temperature changes in the vascular tissues, and is beginning to play an important role in
the field of ophthalmology. This paper deals with the working principle, use and
advantages of IR thermography in the field of ophthalmology. Different algorithms to
acquire the ocular surface temperature (OST), that can be used for the diagnosis of ocular
diseases are discussed.

Keywords – Eye, infrared, thermogram, temperature, cornea, ocular.

1. Introduction

Temperature has been used to investigate the physiological and pathological changes in
human body since 400 B.C. using different techniques. Galileo invented the thermoscope
in 17th century and then it evolved into modern mercury-in-glass thermometer,
radiometers for middle-ear temperature and disposable sterile thermocouple which is
widely used these days. Liquid crystals such as cholesteric esters, found in 1877 had the
property of changing color with temperatures, were used to display the distribution of
temperature on skin topographically. Such detectors were inexpensive, had relatively short
life span and may alter surface temperature due to large area of contact. Schlerian
photography enabled researchers to see the convection currents surrounding the body, but is
limited to the study of heat transfer around insulated clothing [1]. Except Schlerian
photography, most of the methods developed in past had limitations of either requiring
contact with subject or incapable of displaying distribution of temperature.

Infrared (IR) thermography is a non-contact and non-intrusive temperature measuring


technique, with an advantage of no alteration in the surface temperature and capable of
displaying real-time surface temperature distribution. It was first introduced by Lawson in
1956 to modern medicine and discovered the association of elevated skin temperature with
breast carcinoma [2] and later investigated the feasibility and potential of using IR
thermography as a tool to study breast lesions [3]. This technology has revolutionized the
field of temperature measurement in the last 50 years and is widely employed nowadays.

In the field of thermo-fluid dynamics IR thermography was applied to measure convective


heat fluxes, and for the comprehension of fluid dynamics phenomena on the flow field
behaviour over complicated body shapes [4]. The process of ice nucleation and ice
propagation in flowers of fruit trees and other frost sensitive plants were studied using IR
thermography in agriculture [5]. It was used for the measurement of size, depth and
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thermal resistance of materials and components [4], and also for environmental monitoring
such as sea, river pollution, information about indoor climate [6], inspection of plants and
assistance in the reduction of maintenance cost of mechanical equipment [4]. In polygraph
testing, a standard security procedure favoured by US government, IR thermography was
applied to perform facial image analysis [7].

In medical field, IR thermography has been used to assist in decision making in open heart
surgery due to its ability to provide real-time information [8]. It was also used for the
management of neuropathic pain [9,10] and the assessment of patient response to
chiropractic care by measuring the temperature gradient in clinical setting [11]. So far, IR
system has been used to diagnose breast cancer [12,13], rheumatism [1], skin lesion [14],
fever [15], impotence [16] and thyroid gland disease [17]. Currently, it has been applied to
ophthalmology to diagnose eye diseases [18].

The ocular anterior anatomy and physiology nowadays can be studied using a number of
ophthalmic imaging techniques: slit lamp biomicroscopy, confocal microscopy, corneal
topography, optical coherence tomography, computerized tomography, ultrasonic
biomicroscopy, and magnetic resonance imaging. These techniques are capable of providing
accurate description of anatomical features and help to diagnose the ocular diseases better.

Infrared thermography is renowned for its ability to detect the pathological and
physiological changes in the eye which are obscured or unreachable under anatomical
examination. A typical ocular thermogram of normal eye is shown in Fig. 1. It has been
used to study the inflammation of human lacrimal drainage system [19], dry eye [20],
carotid artery stenosis [21], glaucoma [22], unilateral exophthalmos [23], Tolosa–Hunt
syndrome [24], and ophthalmic post-herpetic neuralgia [25]. It was also used to diagnose
retinoblastoma in children [26] and vascular neuritis [27] of the optic nerve. The OST can
be used in the diagnosis of different ocular diseases.

Fig. 1. Typical thermogram of normal eye.

The invasive methods of measuring eye temperature require direct contact with human
cornea. Among the invasive measuring techniques, needle probe was mainly employed.
During measurement, needle probe acts as a cooling fin when inserted into the eye [28] and
error inevitably exists if the penetration depth is below 40 mm. Topical anesthesia is often
required, and this instilled solution often lowers OST. In addition, the penetration of
needle can be traumatic, which often induces further blood flow in eye and thus alters
OST. Hence, this invasive method, is not comfortable to the subjects and the reported
discrepancies in temperature in some cases can be up to 6°C [28].

Infrared thermometry and thermography can measure OST without causing trauma on
subjects. However, they are unable to measure the intraocular temperature. These

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techniques remotely measure the emitted IR radiation and acquire temperature data of a
specific surface. During measurement there will be no alteration in the surface temperature
and also the data collected is of higher precision. With this technology researchers are able
to study OST with greater ease, and accuracy.

2. The principles of infrared thermography on human eye

In general, IR thermography refers to the recording of temperature, or the distribution of


temperature utilizing infrared radiation emitted from a body surface, forming an image
called thermogram. The 2-D thermogram presents the distribution of temperature
distinctly unlike IR thermometry, which gives a single temperature value. IR thermography
also differs with IR photography, where in the latter records infrared radiation reflected
back from objects in the presence of some external infrared energy sources. The principle of
IR thermography on eye involves the physics of IR radiation and measurement of OST.
These concepts are discussed in the following sections.

2.1 The physics of IR radiation

Any object, when its temperature is above absolute zero, emits electromagnetic radiation,
called thermal radiation. In physics, the amount of electromagnetic waves radiated by an
object is quantified by the term spectral radiance. It describes the amount of
electromagnetic waves emitted from a particular surface on the basis of per unit solid angle.
The idea of black body radiation forms the basis of the physics of thermal radiation, though
behaviours of many objects deviate from the ideal black body extensively.

When a black body is in equilibrium at temperature 𝑇 in an environment, it absorbs and


emits a specific continuous spectrum of wavelengths and intensities. The profile of the
emitted spectrum by a black body depends only on the temperature at equilibrium in an
environment and therefore the temperature of a black body is directly related to the
wavelengths of the light that it emits. According to Planck’s law, the spectral radiance, 𝐼 (in
watts per steradian per square meter) of electromagnetic radiation at all wavelengths, 𝜆 at
temperature 𝑇 from a black body as a function of wavelength is given by

2phc2 1 2 1
I (l, T ) = Wcm µm
(1) l5 e lkT
hc 1

where 𝑘 is the Boltzmann constant (1.381×10!!" J/K), ℎ is the Planck constant (6.626×
10!!" Js), 𝑐 is the speed of light (2.998×10! m/s) and 𝑇 is the absolute temperature.
Differentiating Planck’s law with respect to 𝜆 to look for the maximum radiation intensity,
the Wien’s displacement law is obtained

2898µK
lmax =
(2) T

which mathematically illustrates a common observation: as the temperature of an object


rises, the color of light emitted varies from infrared to red to orange. Given human body
temperature of 37°C, the emitted light peaks at 9.35 𝜇m which falls into the infrared
region.

Consider a small flat body radiating outward into a half-sphere under an temperature-
equilibrium environment, one can deduce Stefan–Boltzmann’s law from Eq. (1) and get

(3) j = sT 4

which states that for a black body the total energy radiated per unit surface area in a unit
time is directly proportional to the fourth power of the absolute temperature of the black
body.

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In reality, real objects are rarely a black body, though in certain spectral intervals they may
behave closed to the ideal black body. In most cases real object emits only part of the
radiation a black body emits at the same temperature and same wavelength. Denote
the amount of radiation emitted by real object as 𝐸! and 𝐸!" for the amount of radiation
emitted by black body, the emissivity is defined as

El
#=
(4) Ebl

and Eq. (3) can be rewritten for gray body with the knowledge of emissivity as

(5) j = #sT 4

2.2 The IR thermography system

Planck’s law, Wien’s displacement law, Stefan–Boltzmann’s law and the concept of
emissivity is the physics behind the working principle of an IR thermography system. An
IR thermography system in general consists of a camera (as shown in Fig. 2), with some
detachable optics, and a personal computer that controls the camera. In the camera there is
an IR detector, which absorbs the IR shining by the lenses and converts the IR signal into
electrical voltage or current for processing. The way a desired field of view is
projected and recorded on IR detector within the camera, is determined by the imaging
system.

Fig. 2. IR camera (VarioTHERM® head II,


http://www.infratec.de/fileadmin/downloads/pdf/Flyer_Variotherm_head_en_mail.pdf).

Generally, there are two main sorts of imaging system available to the IR thermography:
scanner (scanning array) and focal plane array. The focal plane array is superior to scanning
array in almost every aspect in terms of performance. Scanning array consists of linear
arrays, rastered across the desired field of view using one detector, two lenses, one
horizontal and one vertical deflection mirrors, to construct a 2-D image as illustrated in
Fig. 3a. Its working principle is analogous to a person looking at a view through narrow slit,
rastering both his/her head and slit in the direction perpendicular to the slit to build up 2-D
image. Focal plane array images a desired field of view without scanning, and it works
similar to a typical camera, in which the film captures the 2-D image directly projected by
the lens at image plane (Fig. 3b).

IR detectors of IR thermography consist of an array of elements reactive to IR. In the


broader field of IR thermology, there are two types of IR detectors: thermal and photonic.

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Thermal detectors such as microbolometer, pyroelectric detectors and Golay cells detect
heat generated by incidence of IR radiation and are not wavelength dependent. They are
commonly used in bolometers such as thermocouple and thermopile. They show slow
response time and low detection capability without the need for cooling. The photonic
detectors like quantum well infrared photodetector (QWIP) and mercury–cadmium–
telluride, are wavelength dependent, and can detect the temperature of a remote object’s
surface by measuring the amount of IR incidence of a specific range. Unlike thermal
detectors, they offer quicker response time and better detection performance, and therefore
are favourite as IR detector for focal plane array imaging system.

Fig. 3. a. Scanning array: 1. detector 2. lens 3. horizontal deflection mirror 4. Vertical deflection mirror 5. lens 6.
object 7. measuring spot. b. Focal plane array: 1. object with measuring spots 2. lens 3. detectors
(http://www.infratec.de).

Most of the photonic detectors operate only at cryogenic temperature, otherwise the
detected signal would be swamped by thermal noise. The IR thermography utilizing
imaging system of focal plane array can be of cooled or uncooled type. Most of these
detectors are cooled evaporatively, either by liquid helium, liquid nitrogen, thermal-electric
cooler, or Stirling cycle refrigerator. Though not common, in the latest technologies
microbolometer is used in focal plane array, which have lower cost and require no cooling.

Presently in the medical field IR thermography captures thermogram at wavelength range


of 8–12 𝜇m, which falls in the region of long-wave IR (LWIR). They are further
subdivided into a few bands [29,30]: near IR (NIR), from 0.7 to 1 𝜇m, short-wave IR
(SWIR), from 1 to 3 𝜇m, mid-wave IR (MWIR), from 3 to 5 𝜇m, long-wave IR (LWIR),
from 7 to 14 𝜇m, very long-wave IR (VLWIR), from 12 to 30 𝜇m. NIR and SWIR are
used in fiber optics telecommunications and long-distance communications, respectively;
guided missiles technology making use of IR heat is used in MWIR. The LWIR is the
region of ‘‘thermal imaging” which does not require external thermal source to obtain a
passive isotherm of the outside world. The IR thermography used for measurement of OST
obtains thermogram in LWIR.

2.3 The measured OST

Previous studies [31,32] have illustrated that the absorption bands of ocular tissues are
similar to water, which was opaque to far infrared. Water is found to have an emissivity of
1, and it behaves like black body radiator on IR spectral above 3 𝜇m. The emitted spectrum
falls in between 1 𝜇m and 30 𝜇m with a maximum distance at 9 𝜇m for ocular tissues,
under normal circumstances (32°C). Consequently, the spectrum radiated by any ocular

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tissues will be fully absorbed by ocular tissues anterior to it. In other words, the spectrum
emitted by vitreous will be absorbed by lens that is anterior to it.

The transmission in between cornea and tear film is slightly different. Though water
behaves similar to black body on IR spectrum above 3 𝜇m, for thin water layer the degree of
absorption depends on the thickness of layer. The transmittance of IR on spectrum 8 𝜇m to
13 𝜇m is about 30% when the layer thickness is 10 𝜇m. When the layer thickness was 40
𝜇m or above, the transmittance approximates to zero [33,34]; and tear film thickness was
found to be around 40 𝜇m [35]. Consequently, the spectrum radiated by cornea was also
wholly absorbed by tear film. The temperature of tear film was measured by thermography
during the evaluation of OST [34,36,37]. This study was performed using finite element
model of heat transfer in human eye [38].

A recent study [39] verified the above idea and showed that, OST was mainly related to
tear film stability, rather than other parameters such as central corneal thickness, corneal
curvature or depth of anterior chamber.

In clinical thermography, studies have indicated that an angle of viewing of curved


anatomical surface beyond 90° will lead to a reduction in measured temperature of 4°C or
more, due to the variation of emissivity at different angle of viewing. For the measurement
of OST by IR thermography, it is assumed that, the angle of viewing on any part of the
cornea and sclera during measurement with respect to the thermography is within 𝜋/4, so
that the error induced due to the variation of emissivity at different angle of viewing is
negligible. Furthermore, as the angle of view becomes greater, the amount of reflected
thermal radiation from anatomical surface increases and the error in temperature measured
grows. Such resultant error is found to be negligible for the case where angle of view falls
within  𝜋/4. Therefore, the OST measured can be comfortably taken as temperature of tear
film even after considerations of error incurred by angle of view and reflected thermal
radiation.

3. Methodologies in the study of OST

IR thermography captures temperatures and its variation over ocular surface. Generally, it is
either displayed in gray-scale or RGB color palette. RGB thermogram provides a better
visual representation of temperatures for direct inspection, which relies on users experience
and judgment during the study of OST. Gray-scale IR thermogram is useful in the
quantitative analysis of the OST.

OST is the temperature of a specific location acquired on corneal surface or some defined
region [19,23,40–43]. Usually, it is studied by comparisons on several regions in normal
and diseased eyes.

3.1 Manual measures in the acquisition of OST

Efron et al. have estimated the geometric centre of cornea, and measured surface
temperature at every 0.5 mm increments on either side of corneal surface horizontally [44].
In total there are 11 points running across the anterior surface, as illustrated in Fig. 4. The
method enables the study of temperature profile of OST, using a regression polynomial

(6) DT = ax2 + bx + c

where a = 0.01 °C/mm2, b = 0.003 °C/mm, c = 0.01 °C, and x is the distance from the
geometric centre of cornea in mm.

Morgan et al. have [21,36,45] approached the acquisition of OST by different method.
Five 10 × 10 boxes were placed in five different anatomical locations along horizontal
meridian running across the estimated centre of cornea as shown in Fig. 5. One was placed
at the estimated centre of cornea, two at the limbal position, and another two at the nasal
and temporal conjunctiva (2 mm from the limbus). The area of each box was approximately

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1 mm2. Mean OST was used for statistical analysis. In one of the studies [45], radial
temperature difference (RTD) was proposed to represent the variation in temperature
across the cornea. It is the temperature difference, in between the average temperature value
at the centre of cornea, and the mean temperature value of the sites of two limbal positions.

There were other similar measures to study OST. Instead of boxes, points were placed at
five different anatomical locations along the horizontal meridian. Five points were placed
on centre of cornea, internal and external canthus, half-way from the internal canthus and
nasal limbus, half-way from the temporal limbus and external canthus (Fig. 6) [46,47]. In
another scheme [48] five points equally placed along a horizontal line running through
centre of cornea, connecting medial and lateral canthi and those points were placed (Fig. 7).

In some studies either a squared 10 × 10 pixels box [42,49], or a squared 20 × 20 pixels box
[50] with an actual area of 3.3 mm2, or an area of 4 mm2 [20] or an encircled region of 4.4
mm diameter [51], or a small circle [52] at the centre of cornea were used to study OST.

A circular region was defined to estimate the centre of cornea and the radius of the circle
was either a fixed value [39] or was acquired by subjective judgment [25,53]. Purslow et al.
have recorded temperature data from 23 points across the anterior eye, as illustrated in Fig.
8, and this data was grouped into five regions for subsequent analysis: central, superior,
inferior, nasal, and temporal [54]. Tan et al. [55] have estimated the geometric centre of
cornea, and OST were measured by a total of 20 points across the anterior eye: geometric
centre of cornea, three points inferiorly and four points superiorly at 2 mm separation, six
points nasally and temporally at 2 mm separation, respectively [55] (Fig. 9). Chang et al.
[56] have studied Graves’ ophthalmopathy by acquiring local temperatures of lateral orbit
(reference point), upper eyelid, caruncle, medial conjunctiva, lateral conjunctiva, lower
eyelid, and cornea, as shown in Fig. 10.

Fig. 4. Methodology by Efron et al. in the acquisition Fig. 5. Methodology by Morgan et al. in the acquisition
of OST [44] of OST [21,36,45]

Fig. 6. Methodology by Galassi et al. in the acquisition Fig. 7. Methodology by Sodi et al. in the acquisition of
of OST [46,47]. OST [48].

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Fig. 8. Methodology by Purslow et al. in the Fig. 9. Methodology by Tan et al. in the acquisition of
acquisition of OST [54]. OST [55].

Fig. 9. Methodology by Chang et al. in the acquisition of OST [56].

3.2 Semi-automated method in the acquisition of OST

A semi-auto method was developed to acquire OST on thermogram using standard


procedure [57], as shown in Fig. 11. Thermogram of eye (in OEM data format) was
converted to gray-scale jpeg file. Then the image was manually cropped to consist only of
eye, and resized to a standard size of 400 × 200 pixels. An algorithm to detect the circular
cornea was proposed, with corneal radius being one-fourth of the length of the entire eye.
Temperature profile in the middle of the cornea was plotted, as illustrated in Fig. 12.

Fig. 11. Methodology by Acharya et al. in the acquisition of OST [57].

The variation in temperature over the cornea was used to study temperature deviation along
cornea (TDC)

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TDC = Â f (x, y) f ( x, y + 1)
(7) y

Fig. 12. Pixel profile across the cornea (corresponds to temperature profile of cornea).

3.3 Automated method in the acquisition of OST

An automated method to acquire OST was developed [58,59], as illustrated in Fig. 13. In
that method, localization of eye and cornea was achieved by snake algorithm and target
tracing function [58] without any manual intervention. Genetic algorithm was utilized
to perform search for minimum on target tracing function.

Snake [60] is an active contour consisting of a series of points (dubbed snake points),
moving under forces of gradient vector flow (GVF) [61] to lock onto nearby edges, and
thereby delineates the shape of eye if its initial contour is of appropriate shape and placed in
some suitable locations. GVF, an intense force field pushing snake contour to reach its
minimum in an energy functional (proposed by Kass et al.), is derived from edge map. In
the automated method, the algorithm acquires edge map by applying Gaussian blur on the
ocular thermogram (gray-scale image).

Fig. 13. Methodology by Tan et al. in the acquisition of OST [58,59].

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For a snake locking into the desired feature, it requires the snake to be initially placed
closed to the feature of interest, and the shape of the snake must be carefully selected. In
fact, even in some more sophisticated methods such as spline-based shape matching [62],
diffusion snakes [63], and active shape models [64], these deformable template matching
techniques are local optimizers and require good initial position or clean image to avoid
incorrect localization [65]. In other words, for some applications user is required to select
location for placement of initial contour, also the size or the shape of contour, in order to
get the correct localization. There were cases where user has to monitor the expansion or
convergence of snake.

The eye in ocular thermogram is not fixed at the centre of the image, and may appear
anywhere in the image. For some eyes which have smaller size, they occupy just some part
of the image instead of most of the spaces in thermogram. Given these circumstances, local
optimizers are not a viable option if any user initialization is to be avoided.

In the automated method, the problem is overcome by using a target tracing function.
Target tracing function evaluates a number of converged snakes, and from them only a few,
or probably just one of them correctly localize the eye. The converged snake which gives
target tracing function the lowest value, is the snake that accurately localizes the eye. In
other words, the algorithm performs a search for minimum on target tracing function to get
the right snake to correctly localize the eye. Genetic algorithm is utilized to perform this
search process.

The radius and the centre of cornea are derived from the final resultant snake points. The
centre of cornea is the same as centroid of the snake, and radius of cornea is acquired on the
ground of the snake points with the use of a formula derived [66]. Fig. 13 shows result of
the automatic detection of eye and cornea using genetic snake algorithm.

4. Application of IR thermography to ocular studies

In ophthalmology, IR thermography has been applied to study ocular physiologies, ocular


diseases and surgery. Several correlations between OST and a number of physiological and
pathological changes in eye have been studied with greater ease through IR thermal
imaging. The OST is not only affected by physiological and pathological changes in eye,
but also some of the external factors.

Room temperature was shown to influence OST [39,67]; a rise in 1 °C room temperature
may lead to an increase of 0.15 °C to 0.2 °C in OST [68,69]. The OST was reported to
decrease with an increase in the air flow [70], therefore uniform room temperature and
humidity are required to minimize the discrepancies in studies of OST.

It was reported that, OST increases when an eye is infected with anterior uveitis [36,71],
and indicates a negative correlation for carotid artery stenosis [19,67,72]. The degree of
hyperemia in bulbar conjunctiva (examined in terms of grade of redness using McMonnies
scale) were positively correlated to OST [73]. It is in agreement among most of the
investigators that, a large inter-ocular temperature difference indicates the presence of eye
disease.

4.1 Studies of ocular physiologies

Mapstone described thermographic patterns in normal, ischemic and hyperemic eyes using
Bofor IR camera system [40]. Wachtmeister also conducted a similar study, investigating
both normal and diseased eyes [41]. He found out that, the affected eye was warmer than
the normal eye for anterior and posterior diseases.

Since then a number of researchers looked into the application of IR thermography as a


diagnostic tool, to detect eye diseases using thermal asymmetry [74]. They have compared
thermogram of both sides at the orbito-ocular region and concluded that, ocular disease will

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be present, if a difference of 0.5 °C exists in between the left and right eye. However, this
method was shown to be incorrect [74]. In one study involving 96 normal subjects, half of
them exhibited asymmetry at orbito-ocular region [74]. Hence symmetry alone, may not be
a good tool to differentiate normal and diseased eye. Some characteristic patterns of
symmetry in orbito-ocular thermogram was proposed for normal and pathological
eyes [74].

Efron et al. have used a wide-field color-coded infrared imaging device, to observe the
variation in temperature across the ocular surface and the temporal stability of the central
cornea temperature [44]. They have observed the presence of ellipsoidal isotherms, with a
major horizontal axis for most cases, concentric on a temperature apex that was slightly
inferior to the geometric centre of the cornea in most of the OST [44]. Limbus was found
to be 0.45 °C warmer than geometric centre of cornea, and the rate of corneal cooling after
a blink was positively correlated to the amount of time an eye can remain open.

Another study similar to Efron et al. was conducted to show that limbus was 0.23–0.43 °C
warmer than the geometric centre of cornea [55]. All subjects recruited were Chinese,
illustrating ‘bowl-shaped’ horizontal OST profile and ‘spoon-shaped’ vertical OST profile
[55]. It was shown that Chinese eyes have lower tear volume and tear stability compared to
Caucasian eyes [75–78]. These findings suggested brown eyes in general have lower
temperature at limbus compared to blue eyes [55].

OST was shown to be decreasing by -0.01 °C per year throughout life, and this rate of
reduction increases after middle age [79]. It was revealed that, 95% normal subjects showed
an inter-ocular temperature difference of less than 0.62 °C and more than 0.62 °C for
disease subjects [36].

Human lacrimal drainage system and the effect of non-contact corneal esthesiometer
(NCCA) air stimulus were also investigated [42]. The anatomy and patency of human
lacrimal drainage system were usually examined using radionucleotide lacrimal scanning
and dacryocystography. But, the subjects were exposed to radiations due to these
techniques. Raflo et al. have employed IR thermography together with lacrimal irrigation,
for the purpose of visualizing tear ducts in control and patients with obstructive epiphora
[80].

Corneal innervation has a number of specialized nerve types: mechano-sensory, polymodal,


mechano-heat and ‘cold’ neurons. Traditional methods of assessing corneal nerve function,
such as using nylon thread of fine metal wire cause trauma to cornea. NCCA was proposed
as a new method to stimulate corneal nerves utilizing controlled air pulse, though the mode
of stimulation was unclear to researchers.

Murphy et al. have conducted a study to investigate the mode of stimulation by NCCA and
concluded that, the rate of change in corneal surface temperature was due to the principal
mode of stimulation by NCCA [42]. In other words, during stimulation both A
𝜕  (mechano-sensory) and C (temperature) fibers are likely to respond to air-pulse stimulus
signals from C fibers.

Dynamic IR imaging was used in the NCCA stimulation study, and the corneal surface
temperature was measured in a sequence of 32 images with 0.25 s in between each image of
subjects after exposure to air-pulse stimulus [42]. In another recent study, dynamic IR
imaging was utilized to investigate the relationship between OST and some physical
parameters of anterior eye, such as corneal topography, corneal thickness, bulbar hyperemia,
and tear film stability [39]. Initial OST after blinking was found to be correlated with body
temperature and tear film stability, as assessed by non-invasive breakup time.

4.2 Studies of ocular diseases and surgery

Exophthalmos is a bulging or protruding eyeball. It is a medical condition that is often seen


in severe thyroid eye disease (Graves’ ophthalmopathy), an auto-immune inflammatory
disorder which affects the orbit of the eye, in patients with or without thyroid disorder. A

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number of different cases such as left endocrinal exophthalmos, metastasis of left orbit were
subjectively assessed with IR thermography [23]. The number of subjects in each case was
too small to perform the statistical analysis [23].

In a later study, IR thermal imaging was utilized to determine the inflammatory state and
follow-up effect of methylprednisolone pulse therapy in patients with Graves’
ophthalmopathy [56]. Local temperatures such as lateral orbit (which is defined as a
reference point), upper eyelid, caruncle, medial conjunctiva, lateral conjunctiva, lower eyelid
and cornea were measured in patients with Graves’ ophthalmopathy and normal control
subjects. Clinical activity score and local temperatures in some 11 patients were also
measured before and after methylprednisolone pulse therapy. The study showed that,
temperature difference between lateral orbit and other target area such as caruncle, medial
conjunctiva, lateral conjunctiva and lower eyelid of Graves’ ophthalmopathy patients were
significantly higher than those of normal subjects [56]. Positive correlation (correlation
coefficient = 0.8, n = 22) was found in between the difference in the sum of the
temperatures before and after treatment, and the change in clinical activity score. The IR
thermal imaging was thought to be helpful in evaluating the follow-up effect of
methylprednisolone pulse therapy [56].

In some other studies, the effect of corneal temperature on the insudation of lipoprotein
and its mobility within corneal tissue were studied with IR thermography [43]. They found
that, the local capillary permeability was increased when the regional differences in
temperature was greater, bringing lipoprotein insudation preferentially into this warmer
corneal region and making it less mobile and relatively inert [43].

Studies on ocular diseases and surgery were conducted, with the aid of IR thermography on
post-herpetic neuralgia (PHN), photorefractive keratectomy (PRK) and dry eye. In patients
with Herpes Zoster Ophthalmicus (HZO), it was shown that the affected eye was warmer
than the fellow eye, giving a large inter-ocular difference in temperature [81]. However, for
patients with established PHN the affected side was colder than the other side [81].
Another study indicated that for the affected side in PHN the entire ocular surface was cool
with a loss of isotherms [25] and reduction in corneal sensitivity of more than 50% [23].

A rise in the temperature was reported during the PRK treatment [49]. Studies have shown
that, at 38.7 °C 50% of corneal collagens denature and a complete denaturation was reached
at 40 °C [82]. The studies were conducted to investigate whether the temperature for
denaturation of corneal collagen on corneal surface was routinely reached throughout the
PRK operation [49]. OST was found to reach the threshold at which the corneal collagen
denatures during treatment and there was no correlation reported in between any surgical
parameters and temperature changes.

It was reported that subjects with dry eye showed greater OST and radial temperature
difference than normal subjects [45]. During cooling of ocular surface, the dry eye subjects
showed faster rate of cooling than normal eye [20]. It was in agreement with other
investigators that dry eye patients have higher evaporation rate [83,84]. The effect of
conjunctival hyperemia associated with dry eyes seems to outweigh the cooling effect given
by the increased evaporation, hence dry eyes were found to have higher OST [45].

However, in another studies it was shown that the centre part of corneal temperature of dry
eyes was lower than normal eyes, though mean OST was not evaluated [53]. Similar studies
conducted by research group in Japan [50,85], showed that central corneal temperature in
dry eye patients were higher than normal control groups. Such differences were attributed
to the different population of dry eye patients recruited in studies [53].

Besides, Craig et al. have also indicated that, the temperature variation factor and mean
osmolality were higher in dry eye groups than control subjects [53]. Temperature variation
factor was found to be inversely correlated to central corneal temperature. Hence, the ocular
surface having higher variation in temperature tends to have lower central corneal
temperature.

dx.doi.org/10.1016/j.infrared.2009.05.002
13

Corneal surface temperature decreases exponentially after eye opens, and it asymptotically
approaches a constant value after some time [50]. This can be modeled by the following
formula:

kt
(8) T (t) = ( T0 T• ) e + T•

In which 𝑇 is the corneal surface temperature after the eye opens for a period of 𝑡. 𝑇! is the
temperature immediately the eye opens; T1 is the corneal surface temperature at
equilibrium; 𝑘 is the temperature coefficient. By measuring temperature values within a box
of 20 × 20 pixels, or 3.3  mm! , placed at the centre of cornea over a period of 30 s, it was
found that for normal blinking the mean 𝑘 value in dry eye patients (5.6 ± 2.9 per s) was
significantly less than in normal control subjects (9.3 ± 5.0 per s) [50]. It was suggested that
𝑘 value might reflect tear film stability [34].

A later studies employed principle similar to the one mentioned above to diagnose dry eye
using IR thermography. Twenty six normal and 82 dry eye patients were recruited in that
studies. An encircled region having diameter of 4.4 mm (22 pixels) was positioned at the
centre of eye to acquire OST [51]. The study showed that, the diagnosis of dry eye patients
was accurate with a sensitivity of 79%, specificity of 75% with 0.841 area under ROC
(receiver operating characteristics) curve 0.42 °C/s [51].

Furthermore, dry eye was studied in conjunction with the treatment of acupuncture and IR
thermography to determine the effect of acupuncture [86]. It was reported that acupuncture
affects the temperature of the pre-corneal tear film, and lowers the temperature at the
middle of cornea.

Some studies have suggested a correlation in between OST and ocular blood flow. In
monkeys, intraocular pressure (IOP) was found inversely related to ocular perfusion
pressure and ocular temperature [87]. Corneal temperature was determined to be positively
correlated to the ipsilateral values of end diastolic velocity (in left and right eyes,
respectively), and it also positively correlates to the resistivity index of left and right eyes,
respectively; interocular difference in corneal temperature was positively correlated with the
difference in end diastolic velocity, and was found to be negatively correlated with resistivity
index [88]. The above study was done with IR thermometer instead of IR thermographer
[88].

Galassi et al. have evaluated the OST of patients with primary open-angle glaucoma
(POAG) and control group through IR thermography [46]. They have investigated the
correlation between OST, IOP and retrobulbar hemodynamics in conjunction with the use
of color Doppler imaging (CDI). Temperatures of five anatomical points (internal and
external canthus, half-way from the internal canthus and nasal limbus, centre of the cornea,
half-way from the temporal limbus and external canthus) of POAG patients were found to
be lower than of healthy control group. These temperatures were significantly correlated to
resistivity index [46]. Their results highlight the influence of retrobulbar hemodynamics on
OST [46]. In other study, higher OST was observed for central retinal vein occlusion
(CRVO) compared to normal subjects and lower OST was shown for ischemic CRVO eyes
compared to non-ischemic ones [48].

The effects of two glaucoma surgeries, namely deep sclerectomy and trabeculectomy, on
bulbar hemodynamics and corneal surface temperature were investigated [47]. Corneal
surface temperature was acquired [46]. Three months after operation, the corneal surface
temperature increased in both type of surgeries, and a negative correlation between
postoperative changes in ophthalmic artery resistivity index and corneal surface temperature
was observed in both types of surgeries [47]. They have suggested that IR thermography
was useful in the evaluation of vascular outcome of glaucoma surgery [47].

The cataract patients with an anterior capsulotomy, had corneal temperature significantly
higher not only just after the surgery, but also at the 30th-day after the operation [89]. The
length of surgery lasted for more than 40 min, and IR thermometer was used in the study.
No follow-up investigation with IR thermographer was done to elucidate further detail.

dx.doi.org/10.1016/j.infrared.2009.05.002
14

IR thermography was employed to analyze and compare different cataract surgery


procedures based on the phacoemulsification system. In one of the studies,
phacoemulsification probes from Alcon Legacy AdvanTec, Bausch & Lomb Millennium
and AMO sovereign WhiteStar were placed in air, and testing condition was set in a way
such that a corneal burn might be produced during cataract surgery [90]. It was found that,
Millennium and Sovereign WhiteStar generated more heat and therefore led to higher
temperature than Legacy AdvanTec phacoemulsification system [90].

Three different cataract surgeries performed in vivo with phacoemulsification


(phacoemulsification with the traditional Sovereign system without WhiteStar technology,
phacoemulsification with the Sovereign WhiteStar system, and phacoemulsification
through micro incision cataract surgery with the bimanual Sovereign WhiteStar system)
were compared using IR thermography [91]. Among these three techniques
phacoemulsification through micro incision cataract surgery with the bimanual Sovereign
WhiteStar system was determined to have the lowest thermal impact on eye [91]. In
another study, intraoperative thermal levels at wound site were studied, with Sovereign
WhiteStar system and Legacy AdvanTec and NeoSoniX system. Legacy AdvanTec and
NeoSoniX system produced grater mean temperature change at wound site and higher
mean peak temperatures in patients [92]. These studies showed that IR thermography has
facilitated effective analysis on cataract surgery with phacoemulsification.

4.3 Studies of non-ocular diseases

Carotid artery stenosis (CAS) was investigated, using color-coded infrared ocular
thermography [21]. They have shown that, the OST was negatively correlated with the
degree of CAS and the relative difference in CAS (CAS of right eye minus that of left eye)
was also negatively correlated with the relative difference in OST (OST of right eye minus
that of left eye). They have concluded that the circle of Willis and the other anastomoses
within the brain are not able to compensate for the reduction in blood flow and hence led
to a cooler eye on the affected side [21].

5. Discussion

IR thermography is an efficient tool not only to capture temperatures of corneal surface, but
also to detect and visualize any subtle changes on the OST. Eye is a delicate organ and
highly susceptible to external variations. The non-intrusiveness of this technique has
encouraged many researchers to use this method to study ocular physiology, instead of
other imaging techniques and methods for measuring the OST.

Zeiss pioneered the use of thermometry in the measurement of ocular temperature [93].
However, Mapstone [32] had first introduced IR thermal imaging into the field of
ophthalmology. Since its inception, several researchers have looked into thermal asymmetry
or anomalies in thermal distribution, both on the eyes and region surrounding the eyes.
They have tried to establish diagnostic criteria from these asymmetry and anomalies. Due
to the poor resolution of IR thermal imaging at that time, the eye on thermogram was not
clearly discernible. Hence, it was not possible to propose diagnostic criteria based on these
asymmetry and anomalies. Due to the rapid advancement in the IR thermography, more
detailed thermal distribution of the anterior eye can be obtained. The better technology has
prompted researchers to focus their studies on the thermographic pattern of the anterior
eye, instead of the entire orbito-ocular region. The horizontal temperature profile passing
through the geometric centre of eye was illustrated, and more recently, the vertical
temperature profile is also described.

Finite element analysis on human eye has shown that, the centre of the corneal surface has
the lowest temperature [94]. However, experimental studies showed that the coolest point
on the cornea is slightly inferior to the geometric centre of cornea [36,44,55], and this
observation was evident in most of the normal subjects [44]. Researchers suggested that the

dx.doi.org/10.1016/j.infrared.2009.05.002
15

presence of upper eyelid, which is a source of heat, shifted the temperature apex (the coolest
point) inferiorly instead of being at the centre of cornea.

Besides, the shape of isotherms predicted by finite element analysis was not the same as the
experimental studies. The presence of eyelid has made the isotherms as an elliptical shape,
instead of a circular shape [94].

So far thermographic pattern of normal subjects’ OST have been reported. But for other
ocular diseases the corresponding thermographic pattern has not been reported. Subjective
assessment was the only method employed on studies of OST of diseased eye conducted
during 1970s and 1980s; for later studies, mean temperatures on one or several sites (in this
context, a site refers to a point or an area) over the anterior eye were utilized to study ocular
diseases.

From the viewpoint of image processing, when one acquires mean temperature, standard
deviation or median over a region or an area on ocular thermogram, he/she is in fact
acquiring some first-order spatial statistics of texture analysis on the thermal image. As an
example, to obtain the mean temperature in the above case, the average pixel intensity over
the region is calculated and converted to the corresponding temperature. The average pixel
intensity is the first-order spatial statistics.

Often researchers employed mean temperature as a measure to get a ‘‘middle” or ‘‘expected”


temperature value of the site of interest, and made comparison with the corresponding
value obtained from normal subjects. Texture analysis was not actually considered in their
studies. But in coming future such technique may prove to be an alternative approach to
effectively study thermographic pattern of normal and diseased eye, other than descriptively
or quantitatively accounting the pattern of isotherms.

The study of OST on IR thermogram needs more analysis tools and efforts to deliver better
diagnostic value. It is known that eye thermogram lacks corneal boundary, which is clearly
visible in optical image. This makes the quantification of corneal temperature (or OST) a
difficult task to achieve due to the difficulty in corneal localization, and this problem is
approached with numerous methods as introduced in Section 3 and summarized in Table 1.

For manual acquisition of OST, the centre of cornea is located by subjective judgment, by
placing few boxes or points at other locations with respect to the centre [20,42,49,50,52].
In some other studies, a circular region was defined at the centre of cornea. These methods
do not indicate the actual corneal temperature and accuracy depends on the number and
position of the boxes.

Semi-automated method is an improved method. It provides a set of rules and procedures


to define and locate cornea, though in some cases there is some slight error in accuracy with
regard to the location of corneal region. However, human intervention is required before
the start of the proposed algorithm to crop the eye exactly in the proper location.

The snake algorithm coupled with target tracing function [58] localizes the cornea and eye
automatically. This recent method can be used to evaluate the OST and hence the eye
diseases. And the acquired temperature profile (similar to Fig. 12) can be used as tool to
diagnose the ocular diseases.

Eye is a delicate organ, and ocular IR thermography brings no harm to subjects’ eye under
study or diagnosis. But it is unable to provide thermal information and description of
anatomical features beneath the anterior eye. Unlike ultrasound imaging, IR thermography
cannot provide description (or image) on the posterior segment of eye, nor can it accurately
determine the size and location of uveal melanoma which computed tomography is capable
of. However, IR thermal imaging does not emit ionizing radiation as computed
tomography does, or generate high-frequency acoustic wave, expose part of body to
powerful magnetic field and infrared light. It passively receives IR radiation emitted by
subjects, and does not cause any discomfort either through contact with instrument or
expose the eye to any electromagnetic and acoustic wave.

dx.doi.org/10.1016/j.infrared.2009.05.002
16

IR thermal imaging is able to detect pathological changes in eyes which are obscured under
examination by other imaging techniques and methods. It was reported that, for mild
inflammation it may not be observed under examination of slit lamp biomicroscope since
the changes were too subtle but sufficient to cause a measurable increase in OST [55].

The IR thermal imaging is non-invasiveness and is an excellent diagnostic tool. As an


example, the diagnosis of dry eye syndrome mainly based on measurement of tear film
production, such as Schirmer test, tear breakup time method, and Rose Bengal staining
method. However, Schirmer test requires contact with eye and the use of topical anesthesia,
tear breakup time method requires patients to hold their eye for a long time, and often it is
not easy to do so, and Rose Bengal staining method is an invasive method, patients can feel
uncomfortable. The diagnosis of dry eye syndrome using IR thermal imaging has none of
the above problems.

IR Thermography can be extensively used as an effective noninvasive ocular temperature


measuring tool. The advancement in this area offers a great potential to study and measure
OST with greater ease and precision. This enables researchers to look into various aspects
in the field of ophthalmology, and understand ocular physiology and diseases. However, to
establish IR thermography as a tool to diagnose ocular diseases requires more robust
automatic cornea localization and the use of sophisticated tools, such as image analysis, and
statistical analysis.

dx.doi.org/10.1016/j.infrared.2009.05.002
Table 1
Summary of methods used to estimate OST.

Types of
Studies OST Methods Main findings
acquisition
Efron et al. manual 11 points running across the anterior surface average difference in temperature between the GCC and the limbus is
[44] 0.450C

Morgan et al. manual 5 10x10 boxes placed in 5 different anatomical In [21], a significant negative correlation was found between OST and
[21; 36; 45] locations along horizontal meridian running the degree of CAS [21]
across the estimated centre of cornea In [36], 95% normal subjects were found to have interocular
temperature differences between -0.57 and 0.620C [36]
In [45], dry eye patients were found to have greater mean OST than
normal subjects, and RTD was also found to be greater in dry eye group
[45]

Galassi et manual 5 points placed on centre of cornea, internal For all 5 points temperature of patients of POAG are lower than
al.[46; 47] and external canthus, half-way from the temperature of healthy control group [46]
internal canthus and nasal limbus, half-way A negative correlation between postoperative changes in ophthalmic
from the temporal limbus and external artery resistivity index and corneal surface temperature was observed 3
canthus months after deep sclerectomy and trabeculectomy surgeries.

Sodi et al.[48] manual 5 points equally placed along a horizontal line In central retinal vein occlusion (CRVO) eyes and in fellow, non-
running through centre of cornea, connecting affected eyes, OST values were lower than in controls [48]
medial and lateral canthi

Murphy et manual a squared 10x10 pixels box placed at the In [42], The principal mode of corneal nerve stimulation, by the NCCA
al.[42], Betney centre of cornea air pulse, was the rate of temperature change of the corneal surface [42]
et al.[49] In [49], no correlation was demonstrated between the surgical
parameters and either absolute temperature of relative temperature
changes [49]

Mori et al.[50] manual a squared 20x20 pixels box placed at the the rate of decline in corneal temperature for normal blinking in patients
centre of cornea with dry eye was significantly less than that in normal subjects [50]

Chiang et al. manual an encircled region of 4.4mm diameter (22 diagnostic of dry eye using infrared thermal imager system has reached a
[51] pixels) sensitivity of 79.3%, a specificity of 75 [51]

Ng et al.[52] manual a small circle placed at the centre of cornea OST was found to decrease with age at a rate of 0.03830C per year [52]

Cardona et al. manual a circular region centred at the corneal centre In [25], patients with HZO in acute stage were found to show high
[25], Purslow inter-ocular temperature differences, with the affected side being
and Wolffsohn warmer than the other side [25]
[39], Craig et In [39], strong positive correlations were found in between initial OST
al.[53] and both body (forehead) temperature and tear film stability [39]
In [53], dry eye patients were found to have lower central cornea
temperature and higher mean osmolality [53]

Purslow et al. manual 23 points placed across the anterior eye OST is greater with hydrogel and greater still with silicone hydrogel
[54] contact lenses in situ, regardless of modality of wear [54]

Tan et al. [55] manual 20 points placed across the anterior eye, lined Vertical OST profile was noted to be a 'spoon-shaped'; for Chinese the
up in the shape of “+” average difference in temperature between the GCC and the limbus is
0.230C ~0.430C [55]

Chang et al. manual acquire local temperatures of lateral orbit, Temperature difference between lateral orbit and 3 other target areas
[56] upper eyelid, caruncle, medial conjunctiva, (caruncle, medial conjunctiva, lateral conjunctiva and lower eyelid) of
lateral conjunctiva, lower eyelid and cornea GO patients were found significantly higher than those of normal
subjects [56]

Acharya et al. Semi-auto image was manually cropped to consist only of average OST and temperature deviation across the cornea decreases with
[57] eye, the cornea was then detected by age [57]
algorithm developed

Tan et al. [58] automated The eye was localized by using genetic snake The algorithm was able to localize 90% of IR ocular thermogram [58]
algorithm, and the corneal diameter and
location were derived from the resultant snake
points
18

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