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IEEE GEOSCIENCE AND REMOTE SENSING LETTERS
Developing an Index for Detection and
Identification of Disease Stages
Davoud Ashourloo, Ali Akbar Matkan, Alfredo Huete, Hossein Aghighi, and Mohammad Reza Mobasheri
Abstract—Spectral data have been widely used to estimate the
disease severity (DS) levels of different plants. However, such
data have not been evaluated to estimate the disease stages of
the plant. This study aimed at developing a spectral disease index
(SDI) that is able to identify the stages of wheat leaf rust disease
at various DS levels. To meet the aim of the study, the reflectance
spectra (350–2500 nm) of infected leaves with different symptom
fractions and DS levels were measured with a spectroradiometer.
Then, pure spectra of the different disease symptoms at the leaf
scale were analyzed, and a new function was developed to find
the wavelengths most sensitive to disease symptom fraction. The
reflectance spectra with highest sensitivity were found at 675 and
775 nm. Finally, the normalized difference of DS and the ratio
ρ675 /ρ775 was used as a new SDI to discriminate three different
levels of the disease stage at the canopy level. The suggested SDI
showed a promising performance to improve the detection disease
stages in precision plant protection.
Index Terms—Disease stages, disease symptoms, hyperspectral
reflectance, leaf rust, spectral disease index (SDI), wheat.
I. I NTRODUCTION
S PECTRAL data in the visible and near-infrared regions
have been utilized to estimate the disease severity (DS)
levels of infected leaves in precision crop protection [1]–[3].
Wheat leaf rust (WLR) is an important crop disease caused
by the Puccinia triticina fungus. This disease has five sporing
stages (uredospores, teliospores, basidiospores, spermatia, and
aeciospores) that uredospores, teliospores, and basidiospores
develop on the leaf surface [4]. In infected leaves, pustules
appear in a random scatter distribution as disease develops [4].
The WLR disease exhibits different symptoms [5], manifesting
themselves in yellow, orange, and dark brown colors. Finally,
the disease symptoms accrue and culminate in a dry leaf.
Yellow and orange colors show the initial stages (chlorosis),
while dark brown and dry leaves represent the final stages of
the WLR disease (necrosis) [5].
Manuscript received December 2, 2015; revised March 13, 2016; accepted
March 23, 2016.
D. Ashourloo, A. A. Matkan, and H. Aghighi are with the Remote Sensing
and GIS Center, Faculty of Earth Sciences, Shahid Beheshti University, Tehran
19839 63113, Iran (e-mail: d_ashourloo@sbu.ac.ir; a-matkan@sbu.ac.ir;
h_aghighi@sbu.ac.ir).
A. Huete is with the Plant Functional Biology and Climate Change Cluster,
University of Technology Sydney, Sydney, NSW 2007, Australia (e-mail:
Alfredo.Huete@uts.edu.au).
M. R. Mobasheri is with the Remote Sensing Group, Faculty of Geodesy and
Geomatics Engineering, K. N. Toosi University of Technology, Tehran 19697
64499, Iran (e-mail: mobasheri@kntu.ac.ir).
Color versions of one or more of the figures in this paper are available online
at http://ieeexplore.ieee.org.
Digital Object Identifier 10.1109/LGRS.2016.2550529
1545-598X © 2016 IEEE. Personal use is permitted, but republication/redistribution requires IEEE permission.
See http://www.ieee.org/publications_standards/publications/rights/index.html for more information.
1
Considering the importance of WLR disease and DS levels,
several attempts have been made over the past decade to detect
DS of WLR using spectral data. For example, some studies
employed classification and regression techniques for WLR
disease monitoring at the canopy scale [6], [7]. Another study
showed the potential of three spectral vegetation indices to
detect WLR from other types of rust disease at the leaf scale
[6]. These indices have been ranked on their accuracy to predict
DS levels of WLR [8]. In addition to previous approaches,
Ashourloo et al. [9] proposed two spectral disease indices
(SDIs) to detect WLR based on the analyses of spectra from
different disease symptoms using Fisher function and RGB
digital photographs. However, less attention has been made
toward estimation of the disease stages, and this has been a
neglected research area of disease detection using spectral data.
Therefore, the potential of spectral bands for estimating WLR
disease stages across DS levels needs to be studied.
In this research, we estimate disease stages by using pure
spectra of disease symptoms at various disease severities. The
disease severity (DS) of the WLR disease was investigated in
order to achieve two goals: 1) development of a new function
to find the most sensitive wavelengths to retrieve the disease
symptom fraction and 2) development of an index for the
precise determination of disease stages.
This letter is organized as follows. In Section I, a review of
the disease detection methods and the objective of this letter
are presented. The next section presents the experimental setup
and data collection. In Section III, the development procedure
for the new index is explained. In Section IV, the results based
on the developed index are explained in detail, and in Section V,
the conclusion is given.
II. E XPERIMENTAL S ETUP
In order to obtain robust and independent results, two cul-
tivars of wheat, namely, Bolani and Roshan, were selected.
These cultivars are vulnerable to WLR disease and are also
extensively planted in Iran. The experiment was performed in a
greenhouse located at the Iranian Research Institute of Plant
Protection, under fully controllable conditions. Spectral data
from healthy and infected samples were collected in order to
identify three different stages of WLR disease. In stage 1, the
leaf begins to show symptoms with yellow and orange colors
predominant. In stage 2, all of the symptoms are fully developed
and can be seen with similar proportion of colors. Stage 3
includes dry leaves in which the predominant symptoms show
as brown color.
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2 IEEE GEOSCIENCE AND REMOTE SENSING LETTERS
Fig. 1. Flowchart for estimation of WLR disease stages.
Fig. 2. (a) Illustrates the boxes used to plant wheat. (b) Using ASD spectrora-
diometer to measure infected leaf reflectance. (c) Different stages of WLR at a
similar disease severity.
In this letter, disease severity is the fraction of the infected
area to the total area. Infected leaves show different colors,
which are called disease symptoms and further change during
pathogeneses (disease symptom development). Also, disease
stage is the predominant disease symptom at the infected area.
Fig. 1 illustrates the flowchart for WLR disease stage estima-
tion. The input parameters were estimated based on a previous
algorithm developed by [9] at the leaf scale. The main steps of
the algorithm are shown at the right side of Fig. 1.
A. Cultivation and Pathogen Inoculation
The seeds were planted in boxes [120 cm wide × 120 cm
long × 40 cm high; Fig. 2(a)] and were grown at a temper-
ature of 15–20 ◦ C, a relative moisture more than 60%, and a
photoperiod of 16 h per day. Watering and fertilizing were done
under controlled conditions, according to the needs of the plant.
Inoculation was achieved by spraying the front and back of the
plants with a spore suspension from 15-cm distance. Inocula-
tion was performed at specific conditions (spore suspension of
0.6 mL per plant at a concentration of 6 × 105 spores/mL,
temperature of 15–16 ◦ C, and relative moisture more than
90%). Infected plants were transferred to a greenhouse and
grown at a temperature of 20–30 ◦ C, at a relative moisture of
90%, and with a photoperiod of 16 h per day. Cultivation was
conducted in 14 boxes, with 7 boxes for the Bolani and the
other 7 boxes for the Roshan. For each wheat cultivar, four
boxes were infected by spores, and three boxes were kept as
noninfected samples.
B. Spectral Data Collection at the Leaf Scale
To collect the spectral reflectance of the WLR, an ASD spec-
troradiometer (Analytical Spectral Device, Boulder, CO, USA)
was used. The spectra were collected in the 350–2500-nm
range with a bandwidth of 1–4 nm and the sensor field of
view of 25◦ . However, due to the water absorption effects on
the wavelengths beyond 1000 nm, we limited our analyses
from 450 to 1000 nm. A spectralon plate with a dimension of
40 × 40 cm was used as a reference, and also to improve
the measurement reflectance accuracy, a contact probe with a
leaf clip was employed. Spectral sampling was performed from
6 days after inoculation to 42 days. The reflectance spectrum
of each sample was measured five times, and their average was
considered as the reflectance spectrum of the sample. In this
experiment, 300 samples were collected from the leaves with
various amounts of disease symptoms. This data set was used
to estimate the pure spectra of the disease symptoms.
C. Spectral Data Collection at the Canopy Scale
The spectral data set was recorded by an ASD spectrora-
diometer at a height of 150 cm above the ground [Fig. 2(b)] and
with a footprint diameter of 66 cm. Then, a moving filter with a
frame-size of 17 data points and a second-order polynomial was
applied to smooth the spectrum which resulted from the average
of the five measurements collected for each sample [10]. The
processing was performed using MATLAB (Mathworks, Inc.).
Overall, 150 samples from canopy scale were used to detect
different stages of WLR disease.
D. Disease Severity and Disease Stage Measurement Using
RGB Camera
After recording the spectrum of each sample at the leaf and
canopy scales, a digital photograph was taken to measure DS
and disease stage of every sample. These measured parameters
were used as reference data for learning and evaluating the
results of the suggested methods. The digital photographs were
taken using an RGB digital camera with the following specifica-
tions: Canon Digital IXUS 85 IS; F-109 number: f/3.2; shutter
speed: 1/60. The photographs were transformed from RGB to
HIS to remove the effect of outdoor light intensity variations,
which was discussed in [11]. Then, DS was determined by
computing the proportion of the infected area to the total leaf
area, and disease stages were defined as the predominant dis-
ease symptom at the infected area. For example, Fig. 2(c) shows
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ASHOURLOO et al.: DEVELOPING AN INDEX FOR DETECTION AND IDENTIFICATION OF DISEASE STAGES
Fig. 3. Estimated reflectance spectra of healthy leaf and all other disease
symptoms of WLR disease [9].
three samples with similar DS (DS ≈ 0.45) and different
disease stages, including early, middle, and final stages. In the
early stage, the yellow color is predominant, and in the middle
stage, different symptoms can be seen. In contrast, the dry
area is predominant in the final stage. The healthy areas of the
infected leaves are illustrated in red color [the second row of
Fig. 2(c)].
III. D EVELOPMENT OF N EW I NDEX
A. Estimating Disease Symptom Pure Spectra and Disease
Severity (DS)
In this research, pure spectra of disease symptoms and DS
are the two main input parameters for estimating disease stages,
which was estimated based on the method developed in [9] as
follows.
The first step was to estimate the pure spectra of four dis-
ease symptoms and healthy area. Therefore, the proportions of
different disease symptoms which were extracted by an RGB
digital camera and the recorded spectra at the leaf scale were
used as input data sets of the model. Then, the pure spectra of
the different disease symptoms were estimated using spectral
mixture analysis and the least squares method. The output was
the spectral reflectance curves of the disease symptoms (Fig. 3).
The second step was developing an SDI based on the
pure spectra of disease symptoms. Particular wavelengths were
found, in which the reflectance values of different disease
symptoms are similar, while these reflectance values are highly
distinctive from the reflectance of the green area. To find the
suitable wavelengths, the Fisher function was used. This func-
tion increases the difference between two class means as well as
simultaneously decreases the difference between variances. The
two classes used for analysis in the Fisher function were healthy
(spectrum of healthy) and infected (spectra of four disease
symptoms) areas. Based on the result of the Fisher function,
two SDIs were suggested. The ratio of the reflectance values
at 605–455 nm was named leaf rust DS index 1 (LRDSI_1),
and the ratio of 695–455 nm was named leaf rust disease
severity index 2 (LRDSI_2). The correlations of LRDSI_1 and
LRDSI_2 with observed DS were 0.95 and 0.98, respectively.
Thus, in this study, LRDSI_2 was used to estimate the DS
levels [(1)], as this showed the higher correlation
ρ695
LRDSI_2 = 4.2 × − 0.38. (1)
ρ455
3
B. Detection of Disease Stages
In this letter, the sensitivity of different wavelengths to dis-
ease symptom development was considered. To find sensitive
wavelengths and regard them as input bands for disease stage
estimation, three conditions were defined as follows.
First, the reflectance (ρ) value increases or decreases as
disease symptoms develop from green to dry. Therefore, the
reflectance values of different symptoms from the lowest to the
highest values are green, yellow, orange, dark brown, and dry,
respectively. Also, the opposite order of the reflectance values
for the different disease symptoms can be true; the lowest to the
highest values are dry, dark brown, orange, yellow, and green,
respectively. This condition is defined as follows:
ρgreenλ > ρyellowλ > ρorangeλ > ρbrownλ > ρdryλ
or
ρgreenλ < ρyellowλ < ρorangeλ < ρbrownλ < ρdryλ .
Second, the reflectance value difference between the lowest
and highest symptoms is maximum
ρshighestλ − ρslowestλ
where ρshighestλ and ρslowestλ are the reflectance values of the
highest and lowest symptoms (s) at wavelength λ, respectively.
Based on the results of the first condition, one of the dry
or green symptoms is the highest, and another is the lowest.
Third, the differences in reflectance values of each symptom
of yellow, orange, and brown with respect to their subsequent
and following symptoms reach their maximum. In other words,
the differences in reflectance values of yellow from green
and orange symptoms, orange from yellow and dark brown
symptoms, and dark brown from orange and dry symptoms
at a specific wavelength are maximum. To get this condition,
the distance between the highest and lowest reflectance values
was divided into four equal segments. These four segments
were separated by three points. Each point is the ideal re-
flectance value of yellow, orange, and dark brown symptoms
for disease development detection. At a specific wavelength,
absolute values of distances for yellow, orange, and dark brown
from their ideal points were calculated. Then, the sum of the
absolute reflectance values for every wavelength was recorded.
At a specific wavelength, as the sum of absolute reflectance
values decreases, the reflectance values of different disease
symptoms become suitable for disease symptom development
detection. This wavelength can be used to identify disease
symptom development. The third condition has been presented
as follows:
n−1 
   
 ρshighestλ − ρslowestλ 
ρsλ − ρslowest + (s − 1) 
 λ
(n − 1) 
s=1
where n is the number of symptoms and s is the disease
symptoms. s − 1 and n − 1 have been used to ignore ρshighestλ
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4 IEEE GEOSCIENCE AND REMOTE SENSING LETTERS
Fig. 4. Values of different wavelengths so as to detect disease stages of WLR
disease.
and ρslowestλ , respectively. With regard to the three suggested
conditions, (2) is presented
⎛ ⎞
⎜ ρshighestλ −ρslowestλ ⎟ (DS = 1 and N (ρ675 /ρ775 ) = 0.58), and the difference value
w(λ)=⎜
⎝ n−1 

⎟.
 ρshighest −ρslowest ⎠
ρsλ − ρslowestλ +(s−1) λ
(n−1)
λ
 and N (ρ675 /ρ775 ) = 0.3), and the difference value will be 0.2.
s=1
(2)
The proposed function is maximized when the difference
between the green and dry reflectance values is high and the
denominators are minimized. If the reflectance value of each
disease symptom is close to its ideal value, the denominator
will be minimized.
IV. R ESULTS AND D ISCUSSION
The proposed function was calculated for all wavelengths
from 450 to 1000 nm. Wavelengths with a high function value
have more potential and greater sensitivity to disease symptom
development. As Fig. 4 shows, the reflectance values at 675
and 775 nm show the maximum values of the function. At
675 nm, as the disease symptoms develop, the reflectance
values increase too. At this wavelength, the dry and green
symptoms have the highest and lowest values of reflectance,
respectively. As Fig. 3 shows, the reflectance value order at
775 nm is the opposite of 675 nm, and the green and dry
symptoms have the highest and lowest values, respectively.
Therefore, the ratio of ρ675 /ρ775 was used to detect the disease
stages. Since the range of DS is between 0 and 1, the value
of ρ675 /ρ775 was normalized between 0 and 1. In order to
normalize ρ675 /ρ775 , the maximum and minimum values of
ρ675 /ρ775 are needed. The values of ρ675 /ρ775 for the green
and dry symptoms are 0.71 and 0.13, respectively
 development was evaluated under two different conditions as
  ρ675
− min ρ675
ρ675 ρ775 ρ775
N =
. (3)
ρ775 max ρ775 − min ρρ675
ρ675
775
In the remainder of this research, N (ρ675 /ρ775 ) denotes the
normalized value of ρ675 /ρ775 . Based on the disease progress,
DS ≥ N (ρ675 /ρ775 ).
When the entire leaf is affected and dried by the disease
(DS = 1 and N (ρ675 /ρ775 ) = 1), then DS = N (ρ675 /ρ775 )
and DS − N (ρ675 /ρ775 ) = 0.
The high value of the difference shows the beginning symp-
toms of the disease. For example, when the leaf is yellow
(DS = 1 and N (ρ675 /ρ775 ) = 0.25), then the difference value
of DS = 1 and N (ρ675 /ρ775 ) reaches 0.75. As disease symp-
toms develop, the difference value decreases. Then, two other
Fig. 5. Reflectance of different infected leaves with various disease severity
and disease symptoms.
conditions were considered: first, the whole leaf is brown
will be 0.42. Second, half of the leaf is brown (DS = 0.5
The DS values are different in both conditions (1 and 0.5);
however, their disease stages are similar, and brown is the
predominant symptom. This problem can be solved by dividing
the difference of DS and N (ρ675 /ρ775 ) by the sum of the DS
and N (ρ675 /ρ775 ). The results will be similar for the first and
second conditions, and the normalized difference values will
be 0.26 [(1−0.58)/(1+0.58)] and 0.25 [(0.5−0.3)/(0.5−0.3)],
respectively. The results show that the normalized difference
has more potential to detect the disease stage at a specific DS.
As the aim was to determine the disease stage at a specific DS,
the normalized difference of DS and N (ρ675 /ρ775 ) was used
as a new index to determine the health of wheat leaves infected
by the WLR disease (4). This new SDI was named normalized
leaf rust healthy index (NLRHI). NLRHI is between 0 and
0.73 for healthy and dry leaves, respectively. In (4), as the
disease develops and brown and dry symptoms become pre-
dominant in the infected area, the index values approach 0.
However, high values of the index represent the conditions
when the initial symptoms are predominant. Based on (4), the
potential of the suggested index depends on the accuracy of DS
and sensitivity of wavelengths to disease symptom development
DS − ρρ675
NLRHI =
775
. (4)
DS + ρ775 ρ675
The potential of the presented index in disease symptom
follows.
First, it is the ability to estimate different disease stages
in two infected leaves under similar DS levels. Second, it is
the potential to estimate similar disease stages in two infected
leaves, while they have different DS levels. So as to show
the potential of NLRHI, six samples of infected leaves with
a variety of DS levels and disease stages were chosen. The
spectra and disease symptom fractions of these samples are
shown in Fig. 5 and Table I, respectively. Samples a and b
have similar values of DS levels (around 0.2), while their
disease stages are different, and dry and yellow symptoms are
predominant symptoms in the a and b samples, respectively. As
stated before, yellow is the initial, and dry is the final stages of
the WLR disease. As Table I shows, NLRHI distinguishes this
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ASHOURLOO et al.: DEVELOPING AN INDEX FOR DETECTION AND IDENTIFICATION OF DISEASE STAGES
TABLE I
F RACTION OF D ISEASE S YMPTOMS FOR D IFFERENT I NFECTED L EAVES
TABLE II
C ONFUSION M ATRIX FOR E STIMATION OF D ISEASE S TAGES
difference between the two samples. The NLRHI values of a
and b samples are 0.59 and 0.23, respectively. The index value
of 0.59 for sample a shows the initial stages of the disease in
comparison with 0.23 for sample b. Also, e and f are the same
as a and b in having similar DS levels and different disease
stages. NLRHI properly shows the disease stages, and the index
values are 0.21 and 0.59 for e and f samples, respectively.
Although the DS level of sample c is one and a half of sample d,
they have similar disease stages. Based on Table I, the NLRHI
values are 0.4 and 0.37 for c and d samples, respectively. On
the other hand, the DS level of sample f is triple of b, and
dry symptoms are predominant in both samples. The NLRHI
values for both of them are close to each other, b is 0.23, and
f is 0.21. These values for NLRHI demonstrated the ability
of the presented index to detect disease stages. The afore-
mentioned examples clarified that NLRHI not only is able to
distinguish the disease stage at similar DS levels, but also it is
possible to estimate the same disease stage at different DS
levels. Therefore, NLRHI can be used as a new SDI in precision
plant protection. Finally, accuracy assessment of the index
values in the identification of disease stages was determined
at three levels based on the defined thresholds in the confusion
matrix shown in Table II, and the kappa and overall accuracy
were 0.78 and 0.68, respectively.
It has been reported that each disease symptom of WLR has
its own structure [12]. Based on the results obtained in this
research, the visible and near-infrared regions are suitable in
detecting the disease stages at canopy scales. This study has
shown the potential of SDIs, developed at the leaf scale, to be
used at the canopy scale [13]. Leaf optical properties, plant
structure, leaf area index, canopy gaps, litter, and soil back-
ground are important parameters which affected the collected
spectra at leaf and canopy scales [14]. Thus, the next step is to
consider the effect of the atmosphere and imaging systems on
the index accuracy. Moreover, it must be noted that independent
data sets from the other cultivar of wheat and fungus disease
with different symptoms are required to evaluate and improve
the suggested index.
5
V. C ONCLUSION
The proposed SDI showed high accuracy and sensitivity in
discriminating disease stages at a certain DS. This investiga-
tion, carried out with a developed new function applied over
the 450–1000-nm range, has revealed little spectral distinction
of disease symptoms between the beginning and end of the red-
edge region. Furthermore, there are large differences between
the reflectance spectra of the disease symptoms at 675 and
775 nm. Disease estimation is faced with much difficulty in
the early stages due to the slight development of the disease
and the spectral similarity between the yellow and noninfected
areas. Nevertheless, the proposed SDI has high accuracy in the
early stage detection of infected areas. In addition, suggested
SDI reduces data dimensionality and speeds up the disease
estimation rate. It must be noted that the proposed index needs
to be tested on various sensors and different varieties of wheat
in order to be used in precision plant protection.
ACKNOWLEDGMENT
The authors would like to thank the anonymous reviewers for
their comments which helped in improving this letter.
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