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Radiation Therapy Induced-Erythema: Comparison of Spectroscopic Diffuse Reflectance Measurements and Visual Assessment

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Surveillance and assessment of radiation-induced erythema is an important aspect of managing skin toxicity in radiation therapy treated patients. Upon receiving the early fractions of radiation, an inflammatory response and vascular dilation takes place due to damage of basal cells in the skin’s epidermal layer. This process of skin reddening known as erythema. The gold standard used for assessing and grading erythema is visual assessment (VA) by an experienced clinician/ radiotherapist using toxicity scoring tools. This method is limited by the assessor’s experience, vision acuity, and the subjectivity of qualitative scores. An alternative optical technique to VA, is diffuse reflectance spectroscopy (DRS). A comparison between both techniques performance in detecting radiation therapy-induced erythema is demonstrated in this pilot study. The results evidenced that DRS is capable of detecting skin erythema before an expert eye could do so.
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Radiation therapy induced-erythema:
comparison of spectroscopic diffuse
reflectance measurements and visual
assessment
Ramy Abdlaty, Lilian Doerwald, Joseph Hayward, Qiyin
Fang
Ramy Abdlaty, Lilian Doerwald, Joseph Hayward, Qiyin Fang, "Radiation
therapy induced-erythema: comparison of spectroscopic diffuse reflectance
measurements and visual assessment," Proc. SPIE 10952, Medical Imaging
2019: Image Perception, Observer Performance, and Technology
Assessment, 109520H (4 March 2019); doi: 10.1117/12.2506306
Event: SPIE Medical Imaging, 2019, San Diego, California, United States
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Radiation Therapy Induced-Erythema:
Comparison of Spectroscopic Diffuse Reflectance
Measurements and Visual Assessment
Ramy Abdlaty 1, Lilian Doerwald 2, Joseph Hayward 2, Qiyin Fang 1.3
1 Biomedical Engineering, Military Technical College, Cairo, Egypt
2 Juravinski Cancer Centre, Hamilton Health Sciences, Ontario, Canada
3 Engineering Physics, McMaster University, Ontario, Canada
ABSTRACT
Surveillance and assessment of radiation-induced erythema is an important aspect of managing skin toxicity in
radiation therapy treated patients. Upon receiving the early fractions of radiation, an inflammatory response and
vascular dilation takes place due to damage of basal cells in the skin’s epidermal layer. This process of skin reddening
known as erythema. The gold standard used for assessing and grading erythema is visual assessment (VA) by an
experienced clinician/ radiotherapist using toxicity scoring tools. This method is limited by the assessor’s experience,
vision acuity, and the subjectivity of qualitative scores. An alternative optical technique to VA, is diffuse reflectance
spectroscopy (DRS). A comparison between both techniques performance in detecting radiation therapy-induced
erythema is demonstrated in this pilot study. The results evidenced that DRS is capable of detecting skin erythema
before an expert eye could do so.
Keywords: Radiation Therapy, Erythema, DRS, Visual Assessment
1- INTRODUCTION
Diverse biological, chemical, and physical interventions could provoke human skin to become erythematous.
One of the famous causes of skin to be erythematic is ultraviolet (UV) radiation in sun rays, (1,2) which progressively
damages the skin leading to skin cancer (SC) and photo aging (3). SC is basically two major categories: melanoma
skin cancer (MSC), and non-melanoma skin cancer (NMSC) (4). The lesion treatment for both categories is an
oncologist choice between surgery, radiation therapy, or a combination therapy (5). Surgery has no preference in facial
tumors and in old age patients (6). Consequently, a big ratio of SC patients is treated with local radiation therapy.
Radiotherapy points an ionizing radiation (X-rays photons/ electrons) onto sites of malignant tissue growth, in order
to induce DNA destruction within rapidly dividing tumor cells. Typically, the radiotherapy treatment plan is divided
into a set of sessions, wherein the patient receives a certain dose of ionizing radiation, called a fraction (7). The daily
radio therapeutic dose is confined between safe upper and effective lower limits quantified in Grey/ day (Gy/day) (8).
These limits are carefully considered to be far from inducing radiation side effects.
A variety of side effects are induced by radiotherapy treatment in several body organs (9). One of the early
damaged organs, due to radiation, is the skin. The skin damage varies in severity from slight allergy, to intense
inflammation, and may reach skin burning or necrosis. The damage severity is majorly dependent on the disturbance
that takes place in the rate of compensating the dead cells. Beside compensation disturbance, radiation induces
inflammatory reaction due to destruction and dilation of capillaries in the dermis layer of the skin, and thus become
erythematous. Erythema is usually combined with edema since blood vessels’ permeability is changed. In conjunction
with erythema, hair growth is suppressed as the hair follicles enter a resting phase and thus stops generating new hairs.
The side effects of radiation reduce the patients’ quality of life since it may require different clothing style,
stop practicing favorite sports, beside regular use of moisturizing creams (10). The skin reactions to radiotherapy occur
in no less than nine tenth of all patients (11,12). It usually occurs within 1-4 weeks after the first fraction of radiation
(11). In the 24 hours period following the primary fraction, individual patients may show temporary erythema
surrounding the treated region, which becomes more observable along the rest of radiation sessions. The erythematous
side effect of radiotherapy does not only reduce patients’ quality of life, but also impedes the continuity of the
Medical Imaging 2019: Image Perception, Observer Performance, and Technology Assessment,
edited by Robert M. Nishikawa, Frank W. Samuelson, Proc. of SPIE Vol. 10952, 109520H
© 2019 SPIE · CCC code: 1605-7422/19/$18 · doi: 10.1117/12.2506306
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treatment plan, unless attentively monitored and precisely addressed (13). Erythema is not only accompanying
radiation therapy treatment, but also photodynamic therapy and plastic surgery.
Erythema research has garnered interest because its association with various cutaneous diseases and their
management. This interest fueled the innovation of precise techniques for quantifying erythema. From most to least
complex, the techniques are: spectroscopy, colorimetry/ photography, and visual assessment (VA) (13). VA is still the
current gold standard for erythema assessment in dermatology clinics (14,15). However, VA is a qualitative technique
for erythema evaluation as it accounts on human sensation and clinical experience. The subjectivity, differences in
visual perception, credence on human memory and language limit the reliability and repeatability of VA. As a result,
VA is necessary for rapid checking checking but far from quantitative assessment.
To achieve objective evaluation and precise documentation, colorimetry and digital photography were used.
These techniques measure the skin redness through reflection of light within the visible spectrum. For instance,
colorimetry techniques determine the object’s color by utilizing three sensors that each count photons with a specific
wavelength. The three specified wavelengths represent a standard color space such as the L*a*b* color system (16).
Digital photography has the advantage of being able to record and display erythema progression infinitely to experts
and trainees (17). Both techniques have been effectively used in several studies for sensing dermatological diseases
and symptoms including erythema (1721). One of the drawbacks of both techniques is the need for a standard
environment (illumination, color correction charts and poses (22)), as well as daily calibration to ensure high quality
inter-measurements (23). Moreover, both techniques are far from being able to precisely discriminate between
erythema in a time-series of measurements since they suffer from insufficient spectral resolution (2426).
Diffuse reflectance spectroscopy (DRS) measurements is an erythema assessment tool with better spectral
resolution. Unlike colorimetry and digital photography, DRS discriminates between skin color changes based on the
variation in the skin’s chromophores spectral profile (15,2734). The spectral profile provides quantitative information
out of the skin’s chromophores concentration. Thus, some commercial devices used DRS for detecting cutaneous
color changes. For instance, the T-Stat® (Spectros, Portola Valley, California) is used for that purpose; however, at
~$25,000 USD, it is too expensive for walk-in clinics to afford. The inexpensive instruments are ineffective among
clinicians because of poor interface, disappointing performance and reliability. Beside the steep cost of reliable DRS
instruments, trained technician is needed for their reoperation. For the former reasons, a former study by our group,
developed an inexpensive optical setup for acquiring DRS measurements, shown in Figure 1 (35). The setup reliably
functions in both the laboratory and the clinic.
Figure 1: A schematic diagram shows the DRS system used in the study. The optical setup is composed of a fiber-coupled white
LED light source to an integrating sphere input port. The diffusely reflected light is trapped inside the sphere except the photons
which reach the exit port. The former port is fiber coupled to a spectrophotometer. The captured photons within the spectral gate
are displayed and stored on the attached computer.
The research question of the current study is: “Could DRS be considered an alternative to visual assessment
in quantifying skin erythema?” To reach an answer, a preliminary study was planned to examine the feasibility of the
custom-made DRS system for addressing the progress of erythema on SC patients referred to radiation therapy
treatment. For comparison purposes, the same patients were simultaneously visually assessed by two expert
radiotherapists. The following reasons motivated this study: (1) DRS measurements are noninvasive ones, low-cost
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and user-friendly technique; (2) DRS is an objective method and does not require special expertise to operate; and
finally (3) DRS quantitatively measures changes in skin’s chromophores concentration associated with erythema.
2- MATERIALS AND METHODS
2.1 Study protocol
The clinical study protocol and consent were accepted by the Hamilton Integrated Research Ethics Board (HiREB)
responsible for research studies within McMaster University and affiliated regional healthcare institutions (Hamilton
Health Science and St. Joseph’s Healthcare Hamilton). All the participating subjects, in the study, signed the consent
received a schedule of the treatment and study sessions. The participants were instructed not to use any topical agent
or skin dressing, unless instructed by their oncologist, in which case they should also inform the study’s main
investigator. The study setup preparation, patient recruitment, and clinical work continued for six months.
2.2 Patients recruitment
In this study, we recruited eight patients. The patients were diagnosed with skin cancer and radiation therapy was their
way for treatment. The patient’s age ranged from 56 to 88 years (median = 79 years). Daily radiation fraction doses
ranged from 250 cGy (5000/20) up to 425 cGy (4250/10). Five patients, out of eight, completed the study successfully
till the end. The other three patients’ data were ignored according to exclusion criteria (the first patient (P01) quit the
treatment before completion, P05 initially had a high degree of skin redness, while P07 had an uneven treatment site
which would compromise the reproducibility of DRS measurements). The demographic data of the applicable five
patients is displayed in Table 1. The recruited patients have non-melanoma skin cancer (NMSC), either basal cell
carcinoma (BCC) or squamous cell carcinoma (SCC), and received at least 10 radiation fractions. The lesions in the
recruited patients were either in the arm, the leg, or the face.
Once the region of treatment/ interest (ROI) is determined, by the oncologist, it is marked in order to ensure
high precision in providing the radiation dose every day. The radiotherapist would usually use markers of different
colors such red, green, or blue. Patients may prefer to be marked with red marker for cosmetic reasons. However, in
our study, the recruited patients were marked with green or blue marker. The reason for selecting other markers than
red is to avoid any interference between the red marking and the radiation-induced erythema. For our experiments,
one or two location{s) within the ROI is/are selected by the radiotherapist to be the daily position for DRS
measurement acquisition. Identifying ROI is the radiotherapist’s decision. Two spots, within ROI, were used for DRS
measurements. The reason for using two spots instead of one is reducing the possibility of holding measurements
because of severe skin reactions such as dry and wet desquamation. Again, One or two spot(s), out of ROI, is/are
decided by the radiotherapist to act as the control region for measurement. The control region provides a baseline from
which to measure the alteration in skin optical properties due to radiation treatment.
Table 1: Demographic data of the recruited skin cancer subjects along the length of the study
Patient
Gender
Age
Histology
Radiation
type
Bolus
Dose
(cGy)
Fractions
Site
1
Female
88
SCC
Electrons
1.5 cm
5000
20
Left tibia
2
Female
56
BCC
X-rays
-
5000
20
Left fore- arm
3
Male
68
BCC
X-rays
-
4250
10
Left cheek
4
Male
85
BCC
Electrons
1 cm
4250
10
Right ear
5
Male
75
SCC
X-rays
-
4250
10
Left temple
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Figure 2: displays the region of interest (ROI) for a patient (P04). The patient has a basal cell carcinoma (BCC) in her left fore-
arm. The patient’s ROI is surrounded by a red marker. Two circles, blue and black, were selected by the radiotherapist to be the
positions of reflectance measurements on the patient’s skin. The green circle is selected as a control region since it is located in the
same arm but does not receive any radiation through the time of treatment. The size of the circles is matching the size of the
integrating sphere detection port.
2.3- Study Methods
The study daily measurements were scheduled before the irradiation session for each patient. On each day one out of
two radiotherapists, involved in the study, scores and documents her assessment of the ROI, and the second do the
same using digital captured images, as shown in Figure 3. The patient’s ROI is graded using a scoring chart ranges in
degrees from 0 to 4 as exhibited in Table 2 (15).
Table 2: Erythema visual grading scores
Erythema
grade
No
erythema
Very faint
erythema
Faint
erythema
Bright
erythema
Very bright
erythema
Score
0
1
2
3
4
Figure 3: RGB images of the treatment site for patient number 4 in row (P04) showing a typical time sequence (date is tagged) of
progressive skin reaction over the radiation therapy plan. Starting at the top left, the images correspond to treatment days number
5, 6, 7, 8, 9, 11, 12, 14, 16, 19, and 20. The skin ROI exposed to radiation exhibited a marked increase in erythema (skin redness)
over time.
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To ensure the replicability of DRS measurements, a clinic chair-bed was used to position the patient. For calibration
purposes, two diffuse reflectance targets whose reflectance are 99% and 2% (SRS-99-010, and SRS-02-010
Labsphere, North Sutton, New Hampshire) were simultaneously measured before use on each subject. The high
reflectance standard normalizes the patient’s measurement, relative to the room environment, while the low reflectance
target accounts for the background noise (15,36).
To give more details regarding the DRS system, a brief will be presented regarding the system components.
The primary component is the light source which is selected, since the spectral absorption peaks of oxy- and
deoxyhemoglobin (37,38), to emit light within the visible light spectra. An LED source was chosen to illuminate the
ROI because of the stable emission in the visible spectra. The LED source is transmitted via Radiometric Fiber coupled
source (Newport, Irvine, California) to provide a precisely steady luminance within the visible range. The
spectrophotometer, used for detecting skin reflectance, is selected to be highly sensitive and efficient at differentiating
close spectral features. The whole system components were constrained in size, and weight to facilitate portability.
For the former purpose, the Ocean Optics (Dunedin, Florida) was utilized for developing the system of the study. One
essential reason for selecting this spectrophotometer is the relatively long range of operation, 340-1000 nm, that
includes UV-VIS, and NIR spectra. In addition, it is portable in size (< 150 mm3), and has wide integration time (3
ms < t < 60 s). The fibers used for light transmission specifications were SMA 905 with 0.22 NA, and 400 µm. The
fiber specifications were identified in order to collect the maximum possible light. The integrating sphere was custom
developed in the laboratory and the details are published elsewhere (13).
3- EXPERIMENTS AND RESULTS
3.1 DRS measurements and processing
The diffuse reflectance data was computed by processing the acquired visible spectra measurements obtained from
the patients. Simply, the dark noise was removed from the raw spectral measurement (𝑴𝑹𝑶𝑰) by subtracting the low
reflectance standard target measurement (𝑴𝒍𝒐𝒘 ). The effect of unevenly distributed illumination was neutralized by
normalizing the ROI measurement to a high reflectance white standard target (𝑴𝒉𝒊𝒈𝒉 ). Both the white standard target
and the dark noise measurements were accomplished in the same conditions of the ROI. Hence, the skin ROI
reflectance (𝑹𝑹𝑶𝑰) was computed as follows:
𝑹𝑹𝑶𝑰 =𝑴𝑹𝑶𝑰 − 𝑴𝑙𝑜𝑤
𝑴𝑖𝑔− 𝑴𝑙𝑜𝑤
(1)
Using the low reflectance standard target, instead of capturing measurements for a dark background, is
advantageous in reducing variability in measurements due to the changes of ambient light. The wide integration time
of the spectrometer enabled measurements far from saturation. Three measurements were collected each turn, either
for skin or the reflectance standards. The three measurements were averaged to reduce noise and human error. The
integrating sphere detection port was protected by a layer of tight dressing (Tegaderm™ film, 3M Health Care, St.
Paul, Minnesota) against dirt and contamination. A new dressing layer was used for each individual to verify
decontamination. The individual’s layer was unchanged until the high and low standards’ measurements were
collected, so as not to alter the acquired data.
3.2- Erythema Index computation
The use of Dawson indices is a familiar approach for quantitative estimation of the skin color changes due to disease
progression (26), or medical treatment (39). Dawson derived his erythema index (DEI) formula based on the
assumption that the relation between the hemoglobin optical absorption in the range of 510-610 nm and the erythema
scores is proportional. Dawson found that the area under the curve for the hemoglobin absorption, if a baseline is
determined, is the parameter related to the skin erythema variation and calculated as follows:
𝑫𝑬𝑰 = 𝟓𝟎 ∗ [𝟐𝒓 + 𝟑(𝒒 + 𝒔)− 𝟒(𝒑 + 𝒕)]
(2)
The terms, p, q, r, s, and t are the symbols expressing the logarithm of the reciprocal of the 𝑹𝑹𝑶𝑰 (LRR)
computed at five predetermined wavelengths 510, 540, 560, 580, and 610 nm, respectively. Following the
measurements, Dawson’s relative erythema index (DEIr) is computed to assess the skin color change. The term DEIr
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is equivalent to the difference in DEIc values between two skin sites, one of which is the treated site while the other is
the control (non-treated) site. By this subtraction, the effect of the melanin presence in the skin considered.
Figure 4 is a plot of DEIr calculated from the spectral data obtained using the DRS system for each day of
the 20 treatments for patient P04. The DEIr was calculated relative to normal skin to reduce daily variations of skin
optical properties. Figure 5 is a plot of the daily erythema scores assigned by the clinician by visual inspection (gold
standard). Note the clinician scored visible erythema (above zero) for the first time on day 4, whereas the EI increased
since Day 1.
Figure 4: displays the computed relative erythema index, using Dawson erythema index, for one of the recruited patients. The
displayed results are for a patient who received 20 treatment sessions along 4 weeks.
Figure 5: displays the average clinical scores for the same patient (P04), in Figure 4, assigned by the expert radiotherapist using
the assessment criteria for erythema.
3.0164
12.0969
19.7941
28.1939
19.0826
14.5543
20.5285
27.9167
32.4293
39.1208
30.9857
28.9127
31.2189
39.7544
37.6534
37.8487
30.9896
28.6329
31.7051
35.3118
0
5
10
15
20
25
30
35
40
45
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20
RELATIVE ERYTHEMA INDEX
TREATMENT DAYS
000
1 1
2
1
22222
3 3 3 3 3 3 3 3
0
1
2
3
4
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
CLINICIAN VISUAL SCORE
TREATMENT DAYS
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4- CONCLUSION
Based on the results for the 5 patients, we found that 2 out 5 had an increasing clinician scores, however,
DEIr scores displayed no particular trend after the first week of treatment. The other 3 patients had overall increasing
clinician scores that agree with the DEIr scores over the course of treatment. The advantage of computing DEIr is the
early detection of erythema compared with visual assessment by the radiotherapist. This was proved as all DEIr scores
started to increase from the baseline measurement on the first day of treatment. Thus, erythema index based on DRS
measurements is more sensitive to erythema change than VA. To sum, we suggest that radiotherapists use inexpensive
portable DRS systems in order not only to objectively score erythema, but also to detect skin reactions next to radiation
therapy treatment before being visibly apparent to the clinician.
The results of this preliminary study demonstrate the potential of using DRS technique in the clinical settings
of dermatology clinics. Extended research effort needs to be exerted to certify the reliability of the DRS system with
more patient recruited in the ongoing study. Some enhancements in the original study methodology have been planned
to streamline DRS measurements on skin cancer patients seen in clinic, as well as to verify accurate daily DRS data
acquisition. The second phase of the ongoing study is currently taking place.
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... Different stages of tumor progression require different types of surgical treatment, including breastconserving surgery (BCS) and Radical Mastectomy (RM). Modified radical mastectomy (MRM) is widely used in clinical practice for the treatment of breast cancer to ensure surgical efficacy while reducing surgical damage and improving the patient's quality of life [2]. Specifically, MRM has become a cornerstone of breast cancer treatment in China. ...
... Manual delineation of OARs and CTVs for RT is a laborious task for clinicians, which requires not only experience but also physical exertion. Repetitive work for long periods can lead to reduced productivity and even errors on the part of clinicians [2]. In this case, automatic segmentation algorithms serve as a useful tool for reducing the workload of clinicians and producing highly consistent results. ...
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