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Recent advances in hyperspectral imaging for melanoma
detection
Thomas H. Johansen∗
, Kajsa Møllersen†
, Samuel Ortega‡
, Himar Fabelo‡
,
Aday Garcia‡
, Gustavo M. Callico‡
, Fred Godtliebsen∗
Article Type:
Advanced Review
Abstract
Skin cancer is one of the most common types of cancer. Skin cancers are classified as
non-melanoma and melanoma, with the first type being the most frequent and the second
type being the most deadly. The key to effective treatment of skin cancer is early
detection. With the recent increase of computational power, the number of algorithms to
detect and classify skin lesions has increased. The overall verdict on systems based on
clinical and dermoscopic images captured with conventional RGB cameras is that they do
not outperform dermatologists. Computer-based systems based on conventional RGB
images seem to have reached an upper limit in their performance, while emerging
technologies such as hyperspectral and multispectral imaging might possibly improve the
results. These types of images can explore spectral regions beyond the human eye
capabilities. Feature selection and dimensionality reduction are crucial parts of extracting
salient information from this type of data. It is necessary to extend current classification
methodologies to use all of the spatio-spectral information, and deep learning models
should be explored since they are capable of learning robust feature detectors from data.
There is a lack of large, high-quality datasets of hyperspectral skin lesion images, and there
is a need for tools that can aid with monitoring the evolution of skin lesions over time. To
understand the rich information contained in hyperspectral images, further research using
data science and statistical methodologies, such as functional data analysis, scale-space
theory, machine learning, and so on, are essential.
∗Department of Mathematics and Statistics, UiT The Arctic University of Norway
†Department of Community Medicine, UiT The Arctic University of Norway
‡Institute for Applied Microelectronics, University of Las Palmas de Gran Canaria
1
Introduction
Skin cancer is one of the most common types of cancer in humans, and in countries with
predominantly fair-skinned population the incidence trend for the past 30 years has been
increasing (American Cancer Society, 2018; Ferlay et al., 2013). Skin cancers are classified
as non-melanoma skin cancer (NMSC) and melanoma. NMSC is by far the most frequent,
whereas melanoma is the most deadly. In 2018 the reported number of new cases of NMSC
globally accounted for 5.8% of all new cancer cases, and accounting for 0.7% of all deaths.
New cases of melanoma was reported to account for 1.6% of new cancer cases, but notably
accounting for 0.6% of all deaths caused by cancer (Bray et al., 2018). The key to effective
treatment of skin cancer is early detection, before the cancer metastasizes. Non-metastasized
melanoma is reported to have a 5-year survival rate of 99%, whereas once it spreads to dis-
tant organs the survival rate drops to 20% (American Cancer Society, 2018). In dermatology
one of the most commonly taught diagnostic guidelines for classifying pigmented skin lesions
is the ABCD rule of dermatoscopy (Nachbar et al., 1994). The respective letters in the
acronym represent different features of a skin lesion; asymmetry, border, color, and differ-
ential structures. When using the ABCD rule to diagnose a skin lesion, a score is assigned
for each of the four features, and combined into a total score. The total score gives an
indication of the potential for malignancy, where higher scores mean greater potential for
malignancy. In clinical settings the reported sensitivity and specificity of the ABCD rule
ranges from 74–91.6% and 45–67%, respectively (Annessi, Bono, Sampogna, Faraggiana, &
Abeni, 2007; Unlu, Akay, & Erdem, 2014; Ahnlide, Bjellerup, Nilsson, & Nielsen, 2016).
Figure 1shows a few examples illustrating typical variation between different skin lesions.
Note the differences in the shapes, borders (and lack thereof), colors, etc.
2
Figure 1: Examples of melanoma and non-melanoma skin cancer taken in a clinical setting
from six different patients. These cases represent both non-melanoma and melanoma skin
cancer. The diagnoses of the lesions based on histopathology are as follows; 1) melanoma,
2) atypical melanocytic hyperplasia, 3) squamous cell carcinoma, 4) Bowen’s disease, 5) basal
cell carcinoma, 6) seborrheic keratosis.
Given the increasing trend in skin cancer prevalence, and the difficulty in detecting skin
cancer at an early stage, researchers across many fields have been working to both extend
and develop new diagnostic criteria and computational algorithms. For example the ABCD
rule of dermoscopy has been extended to ABCDE, where the E accounts for evolution of
the skin lesion over time (Abbasi et al., 2004). With the advent of machine learning and
the increasing access to vast, inexpensive computational power, several research groups have
been focusing on developing automated and semi-automated computational methods for
detecting and classifying skin lesions. While some recent advances have been developed
using conventional RGB (red, green and blue) imaging techniques (Esteva et al., 2017),
other researchers have been focusing on exploring new avenues of skin cancer classification
using multispectral and hyperspectral imaging techniques.
3
Figure 2: The image on the left is an example of a conventional, clinical image of a pigmented
skin lesion, whereas the image on the right is an example of dermoscopic image.
Computer systems for classification of pigmented skin lesions has been an active research
field for several decades. Early systems used conventional RGB images, but by the early
2000’s almost all systems used dermoscopic images (Rosado et al., 2003). See Figure 2for
examples of both types of images. A dermoscope is a simple device consisting of a magnifying
lens, a glass plate and a light source that allows the light to penetrate the uppermost layer
of the skin. It is commonly used by dermatologists. The overall verdict of systems based on
conventional and dermoscopic images is that they do not outperform dermatologists (Rosado
et al., 2003; Vestergaard & Menzies, 2008; Korotkov & Garcia, 2012). Deep learning has
been introduced to skin lesion classification, and although deep learning methods possibly
outperform traditional approaches (Codella et al., 2018), it has not outperformed the der-
matologist (Esteva et al., 2017). Multispectral imaging increases the amount of retrieved
information and various systems has been used for skin lesion classification. Whether this
increases the performance has not been established with certainty, since dermoscopic and
multispectral systems have not been tested on the same set of lesions, or under strictly sim-
ilar conditions. The conventional and dermoscopic systems seem to have reached an upper
limit for their performance, while emerging technologies such as hyperspectral imaging can
possibly increase the performance.
The main advantage of hyperspectral and multispectral imaging compared to conven-
4
tional imaging technologies is the possibility of exploring spectral regions beyond the hu-
man eye capabilities. Some materials present spectral features in the infrared spectral
range (Lachenal & Ozaki, 1999). Besides the spectral range, the use of hyperspectral images
is necessary when the material being analyzed presents narrow spectral features (Lee, Cohen,
Kennedy, Maiersperger, & Gower, 2004; Jet Propulsion Laboratory, California Institute of
Technology, n.d.). Such narrow spectral features cannot be detected using multispectral or
RGB images, and should therefore be measured using high spectral resolution instrumenta-
tion. Figure 3illustrates the difference in fidelity and richness of hyperspectral images in
comparison to conventional RGB images.
Figure 3: The conceptual difference between the information richness in a hyperspectral
cube and an RGB image. In the hyperspectral cube, each horizontal slice represents spatial
response for a discrete wavelength. For the RGB image each slice represents spatial infor-
mation across a range of wavelengths. Each of the red, green, and blue slices are calculated
based on the visual light spectrum associated with each respective color.
In this review we will report on the recent advances that specifically focus on detecting
skin cancer using multi- and hyperspectral images. We will start by giving a short description
of the review methodology. Then, we give a brief introduction to hyperspectral imaging and
point out how this imaging technique is being used in medicine, and specifically why it
is being used to classify skin cancer. Next, we focus on how feature selection is crucial for
5
extracting information of this type of data and thereafter we point out the need for extending
current classification methodologies to include the use of spatio-spectral information. Our
review finally gives some critical remarks and analysis of relevant published results before
we indicate important future research directions.
Review methodology
The goal of this review was to provide insight into recent advances in detection of skin
cancer using hyperspectral imaging systems in order to uncover what has been achieved,
and to understand what the key challenges are. Based on this we defined the following
inclusion criteria with the intention of only including recent, highly relevant, peer-reviewed
publications focusing on skin cancer detection using hyperspectral images;
•Peer-reviewed publication in journal or conference proceeding.
•Based on hyperspectral (or multispectral) images.
•Specifically dealing with skin lesion classification.
•Non-invasive data collection, i.e. in-vivo skin lesions.
•Published in recent years (2003–2018).
The inclusion of multispectral imaging systems was made based on preliminary searches,
which uncovered that most of the relevant skin cancer research has been done with these
systems. Although multispectral and hyperspectral systems are based on different concepts
and technologies, from the perspective of data analysis and pattern recognition, images
produced by these systems present similar benefits and challenges. Our initial threshold for
“recent” was 10 years, but because some very relevant studies were published more than 10
years ago, the threshold was increased to 15 years.
In the period of August 20–23, 2018, we performed searches on Web of Science, PubMed,
Scopus, and Google Scholar. Search queries were specifically adapted to each search engine,
and based on the search criteria seen in Listing 1.
6
Listing 1: The search criteria used to construct search queries for Web of Science, PubMed,
Scopus, and Google Scholar.
(( m u lt is pe ct ra l AND classification) O R h y pe r sp ec t ra l ) AND
( i ma ge O R camera) AND
(skin O R melanoma) AND
(classification O R lesion OR cancer)
Our searches resulted in a collection of 86 peer reviewed publications that were potential
candidates for review based on their titles, keywords, and abstracts. After reading through
the initial collection of candidates, we ended up with 20 publications relevant for the review,
selected based upon our previously listed inclusion criteria. Figure 4shows a breakdown of
the number of publications per year, and a summary of all the reviewed publications can be
seen in Table 1.
Figure 4: The number of publications per year that matched our search queries and were
selected for review based on our inclusion criteria. From the plot we can see that the majority
of reviewed publications were published after 2011.
7
Publication Imaging System Wavelengths (nm) Bands Pixel Count
Tomatis et al. (2003) Custom 400–1040 17 —
Patwardhan et al. (2004) Nevoscope 580, 610 2 512×512
Patwardhan et al. (2005) Nevoscope 580, 610 2 512×512
Tomatis et al. (2005) SpectroShade 483–950 15 640×480
Carrara et al. (2007) SpectroShade 483–950 15 640×480
Kazianka et al. (2008) Custom — 300 640×480
Świtoński et al. (2010) VariSpec 410–710 21 —
Nagaoka et al. (2012) ImSpector V8E 380–780 124 512×512
Nagaoka et al. (2012) ImSpector V8E 380–780 124 512×512
Suárez et al. (2012) Custom 400–1100 — —
Nagaoka et al. (2013) ImSpector V8E 380–780 124 512×512
Quinzán et al. (2013) Custom 400–1100 71 640×480
Nagaoka et al. (2015) ImSpector V8E 450–750 124 1024×768
Zheludev et al. (2015) VTT/Revenio 500–885 76 320×240
Lorencs et al. (2016) Nuance EX 450–950 51 —
Song et al. (2016) MelaFind 430–950 10 1280×1024
Zherdeva et al. (2016) STC UI RAS 450–750 61 1920×1200
Stamnes et al. (2017) Custom 365–1000 10 —
Lihacova et al. (2018) Custom 405–964 4 —
Rey-Barroso et al. (2018) Custom 414–1613 14 512×512
Table 1: Summary of the publications included in the review. Publications denoted in bold
indicate that the research is based on hyperspectral images. The “—” entries indicate that
the information is not explicitly presented in the publication.
Hyperspectral imaging for skin cancer classification
Hyperspectral imaging has shown considerable potential as a non-invasive and non-ionizing
technique, supporting rapid acquisition and analysis of diagnostic information. Unlike con-
ventional RGB cameras, which are limited to capturing three bands in the electromagnetic
spectrum, hyperspectral imaging systems are capable of capturing hundreds of narrow bands
across the electromagnetic spectrum, both inside and outside the human visual spectral
8
range (Smith, 2012). Hyperspectral imaging has been widely used in remote sensing (Tuia,
Volpi, Copa, Kanevski, & Munoz-Mari, 2011), and has been applied in-vitro, ex-vivo and in-
vivo in different medical applications (Lu & Fei, 2014). For skin lesion classification, several
studies have been conducted using different types of hyperspectral and multispectral acquisi-
tion systems. Based on the reviewed publications listed in Table 1, most of the research effort
up until now has been based on multispectral systems. Some multispectral devices for skin
lesion analysis are commercially available, such as MelaFind (Elbaum et al., 2001; Kupetsky
& Ferris, 2013), and SIAscope (Moncrieff, Cotton, Claridge, & Hall, 2002), both operating in
the 400–1000 nm spectral range. We are currently not aware of any commercially available
hyperspectral imaging systems designed for skin lesion analysis.
Both multispectral and hyperspectral images are commonly represented as three-dimensional
matrices (or data cubes), where the first two axes represent the spatial coordinates, and the
third axis contains the spectral band measurements. There are two commonly used ap-
proaches to visualizing the information stored in a hyperspectral image. The first one is
to pick one or more pixels (spatial coordinates) and plotting their respective spectral band
measurements by wavelength. The other way is to visualize all pixels for one or more spectral
bands as individual grayscale or color-mapped images. See Figure 5for an example of both
types of visualization.
9
Figure 5: An example of what spectral curves for hyperspectral pixels can look like. The
plot on the left shows a representation of a hyperspectral reflectance image at an arbitrarily
chosen wavelength. On the right, the mean reflectance values are plotted, where the colors
of the curves correspond to the colored regions in the reflectance image. The mean curves
are calculated based on all pixels in each region.
There are several ways to capture both hyperspectral and multispectral images (Li et al.,
2013), but from the perspective of data science applications, how images are captured is
not crucial. However, what the captured image data represents is important. Both types
of images contain information that represents either absorption, reflectance, or radiance at
specific wavelengths across the electromagnetic spectrum. Measurements at discrete wave-
lengths is typically not performed, but measurements are instead performed across narrow
ranges of wavelengths referred to as spectral bands. Multispectral images are often captured
at specifically chosen spectral bands across the supported spectral range of the camera. In
many scenarios the chosen spectral bands are picked based on prior knowledge, such as
known absorption wavelengths of certain chemical compounds or similar. Other times the
spectral bands are chosen somewhat arbitrarily, or at evenly spaced intervals across the en-
tire spectral range. Commercial multispectral systems are typically capable of capturing
5–15 spectral bands across their supported spectral range. Because of spectral resolution
and how wavelengths are typically chosen, captured multispectral data should be considered
as consisting of discrete measurements. Hyperspectral images are captured with constant
10
sampling rate across the spectral range of the camera, and can have hundreds of spectral
bands depending upon the resolution of camera. Therefore, measurements in hyperspectral
images are often considered to be continuous, which means that each pixel in a hyperspectral
image can be said to represent a continuous spectral curve.
Before multispectral or hyperspectral images can be used as input to any classifier, sta-
tistical method, or other computational algorithm where images will be compared in some
sense, they need to be pre-processed. One very important pre-processing step is calibration
with respect to a known reference, typically an image of certified white reference material
captured. The image of the white reference is captured right before or after taking an image
of a skin lesion. This ensures that both images are captured under equivalent conditions.
Certified white references used with hyperspectral systems have known spectral response,
e.g. 99.9% reflectance, across the entire supported spectral range, and are often intended to
represent the maximum values measurable by a camera. In addition so-called “dark current”
or dark reference images are usually also captured as part of the calibration process. These
images can be captured by preventing light from hitting the camera sensor, and they there-
fore represent the minimum values measurable by a camera. An underlying assumption in
this process is that the following inequality is fulfilled,
0≤Idark < Iraw < Iwhite (1)
where Iraw is the raw image before calibration, Iwhite is the white reference image, and Idark
is the dark reference image.
A frequently used method for calibrating hyperspectral images is relative reflectance,
which in this context is performed by re-scaling spectral measurements from the skin lesion
image with respect to the two reference images (K. C. Lawrence, B. Park, W. R. Windham,
& C. Mao, 2003; W. Wang, Li, Tollner, Rains, & Gitaitis, 2012) captured under similar
conditions. The relative reflectance image can be expressed as
Ireflectance =Iraw −Idark
Iwhite −Idark
(2)
Given that the inequality in (1) is fulfilled, relative reflectance images will theoretically be
bounded in (0,1). This also implies that all calibrated images from the same camera system
11
are comparable in a fairly robust sense since the process reduces the effects of the camera
itself and the environment in which images are captured. Furthermore, images are scaled to
the same reference domain.
Another calibration technique used in some skin lesion classification research is the so-
called optical density (Zherdeva et al., 2016; Lorencs, Sinica-Sinavskis, Jakovels, & Mednieks,
2016). In the context of multispectral and hyperspectral images, optical density can be
defined as the logarithm of the ratio of a known reference image to the raw image,
IOD = logIreference
Iraw (3)
The reference image Ireference can be a white reference image, or an image of some other
reference material with known spectral characteristics.
In Rey-Barroso et al. (2018) a novel hyperspectral image calibration for skin analysis is
presented. The first innovation is to employ a neutral-gray color of an X-Lite ColorChecker
reference instead of a conventional certified white reference. The motivation is that this
reference material exhibits reflectance characteristics closer to that of human skin across the
spectral range. They also perform an additional calibration step designed to account for the
influence of healthy skin, reportedly boosting the effects of malignant tissue.
Classifier input
The underlying goal of classification is to organize observations into two or more labeled
classes. The classifier can be considered an algorithm that suggests a class affiliation based
on the input characteristics of the observation. For early detection of skin cancer, there
will typically only be two classes; malignant and benign. The classifier takes the skin lesion
image, or features extracted from the image, as input and gives a binary output indicating
whether the lesion is malignant or not.
The input to the classifier must contain information that makes it possible to discriminate
according to the different classes. In the skin cancer situation, this means that the input
must contain crucial properties of the skin lesion so that an image of a skin lesion can be
assigned the correct class in a very robust manner. Since the input of the classifier plays
such a crucial role, we will describe some important aspects of this for the skin cancer case.
12
Feature extraction, feature selection, and dimensionality reduction
As pointed out earlier, a set of characteristics or features must be extracted from the im-
age to construct a classifier. These features can be categorized into hand crafted features
and summary statistical features. A third category, machine learned features, will not be
discussed in this section since there are no deep learning classifiers yet for hyper- or multi-
spectral skin lesions. However we will discuss some aspects related to learning features from
data in later sections.
The hand crafted features aspire at mimicking some aspect that is known to be dis-
criminatory for lesion diagnosis, often inspired by, but not limited to, the ABCD rule of
dermoscopy (Nachbar et al., 1994). Several hyper- and multispectral systems apply hand
crafted features, exclusively or in combination with summary statistics features (Tomatis
et al., 2005; Carrara et al., 2007; Stamnes et al., 2017).
The summary statistics features are typically the mean, variance, entropy, etc., of the
pixel value for each spectral band. Common for these features, and also some of the hand
crafted features, is that the spatial information is not taken into account. Some systems use
only the mean pixel value (Zherdeva et al., 2016; Quinzán et al., 2013), others use a different
feature or a combination of summary statistics features (Lorencs et al., 2016; Lihacova et al.,
2018; Rey-Barroso et al., 2018; Patwardhan, Dhawan, & Relue, 2005; Nagaoka et al., 2015).
Each feature is calculated for each spectral band, and with a combination of a large set
of features and many bands, dimensionality reduction can improve the performance of the
system. With many spectral bands and/or features, some of the information is probably
redundant, but each feature and band adds noise. Dimensionality reduction will reduce
the noise and hence improve the classifier. If the number of images is small compared to
the dimensionality of the images in a dataset, which is often the case for hyperspectral
image datasets, a trained classifier will be unlikely to generalize well with regards to clas-
sifying samples not seen during training. The discriminatory power of a classifier initially
increases as the number of feature dimensions increases, but then begins to decrease as
the number of dimensions keeps increasing. This effect is often referred to as Hughes phe-
nomenon (Shahshahani & Landgrebe, 1994). Therefore dimensionality reduction is beneficial
13
even if it reduces the amount of discriminatory information. The three main strategies for
dimensionality reduction are band selection (Quinzán et al., 2013; Lorencs et al., 2016),
feature subset selection (Patwardhan et al., 2005; Rey-Barroso et al., 2018; Stamnes et al.,
2017), and principal component analysis (PCA) (Kazianka, Leitner, & Pilz, 2008; Carrara
et al., 2007; Tomatis et al., 2005). In spectral band selection and feature selection, a subset
of the original bands and/or features are selected. This can be done by selecting a subset of
bands, then the features are calculated for this subset (Quinzán et al., 2013; Lorencs et al.,
2016). It can also be done in combination (Rey-Barroso et al., 2018), where the features are
calculated for all bands and then the best band-feature pairs are selected, potentially keep-
ing all spectral bands. The advantage of the first approach is that the number of bands are
reduced, which can lead to a simpler camera construction in the future. In both approaches,
the interpretability is kept intact. When PCA is employed to reduce the spatial or spectral
dimensions, the result is a linear combination of features and spectral bands with different
positive and negative weights, and the interpretability of the resulting PCA features is to
some extent lost. It can be argued that interpretability is of lesser importance if the classifier
is accurate enough, but so far there are no systems with accuracies high enough to justify a
“black box” approach, given the potential fatal outcome of a misclassified melanoma.
Selecting optimal spectral bands
A promising approach for dimensionality reduction of hyperspectral images is to reduce the
number of spectral bands by selecting a subset of optimal wavelengths in a given hyper-
spectral image. This reduction can be performed by focusing on the spectral dimension of
the captured image. In hyperspectral imaging, two main approaches have been proposed
to reduce dimensionality; selection of spectral features or selection of spatial features (Dai,
Cheng, Sun, & Zeng, 2015). On the one hand, spectral feature selection can be based on
e.g. correlation analysis of the spectral bands. Reduction of the feature set can then be
achieved by selecting those bands that provide the most salient statistical information. Dif-
ferent search strategies have been proposed for spectral feature selection; complete, heuristic,
or random search. These search strategies have been used in conjunction with many algo-
rithms such as branch and bound (BB) (Nakariyakul & Casasent, 2007), PCA (Xing, Bravo,
14
Jancsók, Ramon, & De Baerdemaeker, 2005), artificial neural networks (ElMasry, Wang,
& Vigneault, 2009), and competitive adaptive re-weighted sampling (CARS) (Wu & Sun,
2013). On the other hand, spatial feature selection is focused on the selection of relevant
image characteristics (color, shape, etc.) to discriminate the spectral bands that contain
most information about the desired features. Investigations focusing on spectral and spatial
feature selection in hyperspectral images up until now have been very limited, likely due to
the small number of studies that have been carried out in the field of skin cancer detection
using hyperspectral images as a whole.
Practical implementation of a hyperspectral imaging system if often challenging due to
the complexity and cost of a hyperspectral camera capable of capturing several hundreds
of bands. Recent publications have addressed new strategies for obtaining a feasible and
practical technical solution by reducing the number of spectral bands or combining different
finite spectral bands. A direct consequence of the reduction of the total amount of infor-
mation processed, is the reduction of the computational requirements in a given algorithm.
Reducing the spectra can also enable algorithms to operate in near real-time. The common
approach up until now has been to obtain a hyperspectral image composed of hundreds of
bands and then analyze which bands provides more information to classify and differentiate
the skin tumor.
In Zherdeva et al. (2016) an experimental setup with hyperspectral images in the 450–
750 nm range is employed to discriminate between skin cancers. Based on analysis of the
collected images, it was determined that the most relevant differences between healthy tissue
and skin cancer are located in the spectral bands 530–570 nm and 600–700 nm. These bands
correspond to the absorption wavelengths of hemoglobin and melanin, respectively (Rubins,
Zaharans, L
,ihačova, & Spigulis, 2014). It has been reported that hemoglobin concentra-
tion and the ratio of melanin in skin lesion tissue can be important biological markers for
melanoma detection (MacKinnon, Vasefi, & Farkas, 2014; Vasefi et al., 2016).
A melanoma discriminator based on few spectral channels is proposed in Lorencs et
al. (2016). The spectral band selection principles are based on a correlation study of the
information contained between pixel values in optical density images of each pair of bands.
The triplet of spectral bands at 540 nm, 640 nm and 740 nm and at 540 nm, 640 nm and
15
840 nm were selected as they presented the highest correlation values.
The algorithms described represent promising approaches in achieving feasible technical
implementations for dermoscopic systems. Spectral band reduction, without degrading the
performance of classifying skin lesions, speeds up both training and inference of associated
algorithms and this can lead to near real-time operation of the overall system. This is an
important characteristic for practical applications in clinical settings.
It is worth mentioning that hyperspectral image feature selection applied to skin cancer
detection has been used in very few studies. Therefore, future investigation must be carried
out to demonstrate the conclusions reported in the initial studies. Furthermore, reported
applications of PCA on hyperspectral skin lesion images have not been focused on selecting
optimal spectral bands. By using PCA to reduce the spatial dimensionality, which means
applying PCA on each individual spectral band of an image, it should be possible to study
which spectral bands are most salient (Yamal et al., 2012).
The power of spatio-spectral information
Treating individual hyperspectral pixels in an image as independent observations from the
same patient has certain advantages and disadvantages, both in statistical methodologies
and machine learning. An immediate advantage is that an approach where individual pixels
are classified will yield much bigger datasets for both training and testing, even with quite
few images if they have large spatial dimensions. As an example, a small dataset consisting
of 10 multi- or hyperspectral images with 1000×1000 pixels, becomes a massive dataset
of 10 million observations in a pixel-wise scheme. Using a pixel-wise approach to detect
skin cancer has not been widely studied, but some research has been performed; skin lesion
segmentation based on a pixel-wise scheme was done in Świtoński, Michalak, Josiński, and
Wojciechowski (2010). One challenge of a pixel-wise scheme is how to balance the classes in
the dataset, and how to ensure the sub-division into training and test sets are distributed
in a representative way with respect to the original distribution, but still performed at
random. Another challenge is getting accurate labels at the pixel level, which means that for
each individual pixel a corresponding individual classification or diagnosis must be known.
16
Acquiring accurate, fine-grained labels at the pixel level is currently not feasible, and this
means that training and testing supervised models with a pixel-wise scheme will be difficult.
The lack of published research using pixel-wise approaches to skin cancer detection might
be indicative of these challenges, suggesting that more research is needed in this area.
Although individual pixels can be treated as independent to some extent, in reality
neighboring pixels in an image are spatially dependent. By not accounting for this, models
and algorithms are deprived of salient information that could otherwise be used to improve
their classification performance. As an illustrative example, a dermatologist applying the
ABCD rule of dermoscopy will take into account all of the spatial information visible in
a dermoscope or dermoscopic image. If only presented with individual pixels, without the
spatial context, classifying the skin lesion would unquestionably be much more challenging.
Therefore, statistical methods and machine learning models should also be trained with the
same type of spatially-dependent data, either as full images or image patches.
Just like recent successful machine learning algorithms designed for clinical and der-
moscopic RGB images of skin lesions are trained on full images with all three color chan-
nels (Esteva et al., 2017), exploiting the full potential of hyperspectral images involves using
all of the spatial and spectral information encapsulated within the images. While this has
to some extent been done in other applications of hyperspectral imaging, such as remote
sensing (Makantasis, Karantzalos, Doulamis, & Doulamis, 2015; Chen, Zhao, & Jia, 2015;
Mughees, Ali, & Tao, 2017), we are not aware of any published research in the area of skin
cancer detection where all of the spatio-spectral information is used in a combined, fully
contextual approach. The most common practise up until now has been to use hand-crafted
features, summary statistics, and other lower-dimensional features. This can work reasonably
well in some cases, but most, if not all, such approaches are incapable of fully accounting for
the spatial and spectral context of detected patterns and features. Many deep learning mod-
els designed for image classification, e.g. convolutional neural networks (CNN) (Krizhevsky,
Sutskever, & Hinton, 2012), are specifically tailored to learn robust feature detectors from
data. The learned feature detectors (sometimes referred to as feature maps) have impor-
tant traits such as translation equivariance. In simplified terms, a feature detector that has
learned to detect e.g. eyes, will give the same activation response regardless of the spatial
17
location of the pixels comprising an eye, but if the pixels are spatially translated the acti-
vation will be translated respectively. For example, two activations of an “eye” feature in
an image is not enough to detect the presence of a face, but two such feature activations
in close, spatial proximity is a much stronger indication of a face. This is essentially how
most CNN-based models learn to detect objects by synthesizing feature detectors from one
layer into increasingly complex features in the next layer (Zeiler & Fergus, 2014). In Esteva
et al. (2017) they develop a deep learning model that detects and classifies skin lesions using
clinical and dermoscopic RGB images. One key component of their work is employing a
technique referred to as transfer learning (Pan & Yang, 2010). More specifically, they per-
form fine-tuning of a pre-trained CNN model using a large dataset of RGB-based clinical and
dermoscopic skin lesion images. Using this type of deep learning technique is feasible when
the modality of the dataset used to train the original model is equivalent to the modality of
the dataset used to perform the fine-tuning. No such pre-trained models for hyperspectral
images are publicly available. This is likely one of the primary reasons why there exists
no published research using deep learning methods on hyperspectral images for skin cancer
detection. A concrete example of the spatio-spectral information richness and variation is
depicted in Figure 6. From the figure it is clear that different physical properties of the lesion
are captured at different wavelengths. How to exploit this information is not immediately
obvious however. One suggestion is that such knowledge should be learned from data using
deep learning models as opposed to being captured by hand-crafted feature extractors, or
explicitly modeled in other ways.
18
Figure 6: Examples of the different information captured in hyperspectral images at different
wavelengths. Each image represents a reflectance image at a specific wavelength. Notice how
certain features appear and disappear at the various wavelengths. In particular, notice how
the small lesion visible near the right-most edge of the left image is almost invisible at higher
wavelengths, and at higher wavelengths, smaller sub-regions and structures in the central
lesion become visible.
Due to substantial differences in dataset modality, spatial dimensions, and number of
channels/bands, transfer learning based on models trained on RGB images is not directly
applicable to hyperspectral images. It has been shown feature detectors learned in the early
layers of CNNs trained on RGB images are sensitive to colors (Zeiler & Fergus, 2014). In
other words, these feature detectors have adapted to specific characteristics of RGB images,
which are not trivially transferable to hyperspectral images. Therefore we believe that any
model must either be trained from scratch, or novel RGB-to-hyperspectral transfer learning
techniques must be developed. The number of trainable parameters in the most frequently
used deep learning models designed for RGB images are in the order of 107, sometimes as high
as 108. The number of trainable parameters in the first layer will increase substantially when
the number of channels/bands in the images are increased by one or two orders of magnitude,
which is the case when going from RGB to hyperspectral images. Additionally, many of the
popular models are optimized for images with spatial dimensions around 250×250 pixels
and 3 color channels. Hyperspectral images used for skin cancer detection have much higher
spatial resolution and many more channels. Given these differences, model architectures
should be augmented for high-resolution hyperspectral images. Examples of such design
adjustments might include increasing the number of learned feature detectors in each layer
19
of the model, and increasing the total number of layers. Increasing the complexity of the
model translates into increasing the total number of trainable parameters.
Based on these observations, it is clear that training deep learning models for skin cancer
detection using hyperspectral images from scratch will be challenging given current tech-
niques and technology; it will require large amounts of computational power due to the high
dimensionality of the images, and the high number of parameters being optimized during
training. Training from scratch will also require sufficiently large datasets of high-quality,
domain-specific, and representative observations in order for the model to generalize well at
classification tasks. As far as we know, there are no publicly available datasets of hyperspec-
tral skin lesion images that are sufficiently large to train deep learning models for skin lesion
classification. The lack of publicly available datasets and pre-trained models are likely the
key challenges that explain the lack of published research on deep learning methods for skin
cancer detection using hyperspectral images.
Critical remarks and analysis of published results
In the context of cancer detection, the ideal system provides a class label for each image
in accordance with the actual pathology of the lesion in question. The gold standard for
skin lesion diagnosis is histopathology for excised lesions and dermoscopic evaluation for
non-excised lesions. Note that a non-biopsied lesion can only have a benign diagnosis, as
suspicion of malignancy automatically leads to excision and histopathological examination.
Due to the potential fatal consequences of misclassifying a melanoma as benign, even low
level of suspicion leads to excision.
A system that aims at clinical relevance must either have melanoma sensitivity close
to 100% combined with a reasonable specificity, or provide information that benefits the
physician in the decision on whether to excise the lesion in question. Both objectives have
shown to be hard to achieve, and so far no system can be said to have achieved either.
To predict the performance on future data, which do not have class labels, a system is
tested on either an independent test set or by the use of cross-validation. For the outcome
to be valid, the test set must be independent of all aspects of the system development,
20
from bandwidth selection to classifier parameter settings. In addition, the test set must be
large enough for the result to be generalizable, and reflect the population from where the
future data will be collected. These standards can be difficult to achieve due to the nature
of the problem at hand: hyperspectral cameras are expensive, require training to operate,
and melanomas are rare but fatal. This results in small datasets, and combined with high
dimensionality there is often not enough data for sufficient training and adequate testing.
The differences in imaging acquisition systems hinder combining different datasets.
Several publications report performance on the same set of data that were used to develop
the system (Zherdeva et al., 2016; Lihacova et al., 2018; Rey-Barroso et al., 2018; Kazianka
et al., 2008; Lorencs et al., 2016), which give highly optimistic results. This bias does not
only apply when the test set is used to train the classification algorithm itself, but applies
for all parts of system development, including bandwidth selection (Quinzán et al., 2013),
feature selection (Patwardhan et al., 2005; Stamnes et al., 2017), and post hoc threshold
settings for classification (Patwardhan et al., 2005; Nagaoka et al., 2015). The impact might
not be obvious, but it is indisputable (Smialowski, Frishman, & Kramer, 2010).
In an effort to overcome the limitations of a small dataset, cross-validation have been
used (Nagaoka et al., 2015; Quinzán et al., 2013), but when using the entire dataset for
bandwidth or feature selection, or parameter setting, the results are invalid.
It can be argued that incorrect use of statistical tools not necessarily disregards the
results altogether, but the drop in performance is usually dramatic. The performance of
MelaFind dropped from 85% specificity (Elbaum et al., 2001) to 9% specificity for near
100% sensitivity, when tested on a proper independent test set (Monheit et al., 2011). For
more examples, see Møllersen et al. (2015).
The reported classification results with independent test sets are:
Publication Sensitivity (%) Specificity (%) # Melanomas # Lesions in Total
Song et al. (2016) 50 23 4 55
Nagaoka et al. (2015) 75 97 24 132
Tomatis et al. (2005) 80 90 41 1369
Carrara et al. (2007) 95 53 76 1208
21
The study of Song et al. (2016) tested MelaFind in a clinical setting, but contains only
4 melanomas, and the results are therefore not generalizable. The Nagaoka et al. (2015)
study consisted of 24 melanomas and 108 other skin lesions, but the lesions are from both
patients and volunteers, and can therefore not be said to reflect any future population.
Tomatis et al. (2005) had a large dataset with excised lesions consecutively collected, and in
addition non-excised lesions that were randomly collected in a clinical setting. Ideally, both
the excised and non-excised lesions should have been consecutively collected, but compared
to other datasets in the field of computer-aided skin lesion classification, this dataset has
high quality. The test set consisted of 41 melanomas and 306 non-melanomas, confirmed
by histopathology, and 1022 lesions that were diagnosed as benign without excision. When
using only the set of excised lesions, the specificity dropped to 77%, which clearly shows the
enormous impact that the inclusion criteria for the dataset can have on the result. Carrara
et al. (2007) reported in their study the sensitivity and specificity to whether a lesion should
be excised, with the dermatologist’s decision as ground truth. The numbers reported here are
according to melanoma/non-melanoma classes. Note the Tomatis et al. (2005) and Carrara
et al. (2007) studies use overlapping datasets and methods.
The reported performance of a system will vary from one test set to another due to its
random nature. The Clopper-Pearson confidence interval for the 95% sensitivity in the study
of Carrara et al. (2007) is 87-99%, which clearly demonstrates the need for large test sets
for reliable results.
The common practice of reporting of a single sensitivity-specificity pair makes compari-
son between systems impossible. The high specificity reported by Tomatis et al. (2005) drops
when the sensitivity is increased, as shown in their receiver operating characteristic (ROC)
curve, which shows the specificity as a function of sensitivity. The curve is not detailed
enough to extract the exact numbers. The reported 80% sensitivity of Tomatis et al. (2005),
which corresponds to missing 1 out of 5 melanomas, is not relevant for a system intended
for clinical use. A 95% sensitivity corresponds to missing 1 out of 20 melanomas, and might
still not be high enough. There is no consensus for a lower limit for acceptable melanoma
sensitivity, and therefore, to make comparisons between systems possible, the range of cor-
responding specificities for sensitivities from 95% to 100% should be reported. As shown in
22
Møllersen, Zortea, Schopf, Kirchesch, and Godtliebsen (2017), the criterion for comparing
different systems has huge impact on the resulting ranking. Summary performance measures
such as the area under the ROC curve (AUC), does not distinguish between the two types
of misclassifications; a system can have high AUC even if its ability to detect skin cancer is
poor. This is not suitable in settings where a false negative (misclassifying a melanoma as
benign) has much graver consequences than a false positive (misclassifying a benign lesion
as malignant).
Future research directions
Long-term goals
In recent years, early detection of skin cancer using RGB images has been research focus in a
large number of publications, see e.g., Oliveira, Papa, Pereira, and Tavares (2018). Although
the findings presented in Codella et al. (2018) and Esteva et al. (2017) are very promising,
they are still not able to outperform experienced dermatologists. Future research using RGB
images will likely suffer from effects equivalent to the law of diminishing returns, and because
of this additional information richness is crucial to boost classification results even further.
The ultimate goal is to obtain classification systems that can lower the number of deaths
caused by skin cancer significantly. A successful classification system will benefit from re-
search in the following two directions.
Firstly, there is a need to acquire a large quantity of high-quality data for all relevant
skin cancers to be able to develop a successful classification system. Any database for
clinical evaluation should be large enough to be able to provide good generalization, and
hence reflecting the high-variability of data. This generalization is even more challenging in
skin analysis, where the inter-patient variability across different pigmented skin lesions is also
influenced by the different skin phenotypes. By acquiring RGB and hyperspectral images for
all cases, it will also be possible to give a more objective answer to the proposed importance
of hyperspectral information. Clearly, it will take many years before a sufficient number
of datasets are available, but with such datasets available, the Common Task Framework
23
described by Donoho (2017) can be used to obtain the best possible classification systems.
After such results are available, clinical testing needs to be carried out before the whole
system can be put into use.
Secondly, patients can contribute to earlier detection of harmful skin lesions by keeping
an eye on the evolution of their skin lesions. A natural first step is therefore to design a
system that can be used for monitoring skin lesions. Ideally, such a system should be precise,
affordable, easy to use and interpretable. By designing a system like this, early detection of
skin cancer will hopefully be significantly improved since one of the reasons for skin cancer
related death is the lack of early treatment. A successful monitoring system may result in
earlier and more effective treatment, thereby reducing the number of deaths.
Short-term goals
Although there exist several papers (Qi, Xing, Foran, & Yang, 2011; Taghizadeh, Gowen, &
O’Donnell, 2011) that indicate that hyperspectral images contain information beyond RGB
images, it seems natural to start with careful analyses that show how much and in what way
hyperspectral information contributes in various types of classification algorithms. based in
both statistical methodologies and machine learning.
Spatial and hyperspectral information gives a natural link to spatio-temporal methods
and it is therefore natural to look into how such methods can be useful in the present
task. In particular, there are links to image sequences in other applications of medicine.
One example is fMRI where an important aim is to find areas of the brain connected to
specific tasks. This may, e.g. be crucial in connection with brain surgery. Similar ideas
could potentially be used to find “suspicious areas” that may be an indicator of a serious
change in a skin lesion. Research in this direction should be performed in close collaboration
with dermatologists, and may turn out to be well worthwhile since it could give rise to a
boost in early detection of skin cancer. Another possibility is to look for particular shapes
or features in the hyperspectral curves, thereby giving rise to important new features in a
future classification rule.
Clustering of the hyperspectral signatures that gives rise to specific RGB values will give
a potential link between RGB and hyperspectral images. This will give important knowledge
24
about how homogeneous such clusters are, and it may also lead to a better understanding
of the extra information obtained by hyperspectral signatures.
When the research community have gathered a large number of images, these datasets
may be used to learn the characteristics of each class. One important research area here would
be to see if hyperspectral images could be used to better distinguish between melanoma and
other types of skin cancer. This would be an extremely important result since melanomas
are fatal, whereas some types of non-melanoma skin lesions are considered harmless. Der-
matologists are able to distinguish these classes well, but this can be a very difficult task for
general practitioners.
Preliminary results (Li, Zhou, Liu, Wang, & Guo, 2015; Q. Wang, Wang, Zhou, Li,
& Wang, 2017; Ortega et al., 2018) indicate that pathology results can be improved both
with respect to precision and time using hyperspectral imaging. Further investigations are
needed to confirm this and to get a better understanding of how this new technology can be
beneficial for this purpose.
Analysis of dermatological hyperspectral images is in our opinion the most important
area for research in the near future. Monitoring the evolution of skin lesions over time is an
important part of such research. In addition, it is important to analyze hyperspectral images
using a large number of statistical tools, thereby gaining more knowledge about such data
and be in better position to design classification systems when sufficiently large datasets
become available.
For future classification systems, finding optimal data representation is a key to success.
Also known as feature learning, this is the task of finding a representation of the input that
will result in the best possible performance of the classification algorithm (Bengio, Courville,
& Vincent, 2013). In the application at hand, the skin lesion’s state is partially represented
by the curves measured by the hyperspectral camera. To this end, we seek a way to represent
the rich data contained in the skin lesion state that will result in a successful algorithm.
Using deep learning for reducing the dimensionality of hyperspectral images is believed to
be an important field of research. Instead of using methodologies based on variance analysis,
entropy, or other information measures, we suggest that learning robust lower-dimensional
representations of the data using e.g. deep autoencoders (Hinton & Salakhutdinov, 2006)
25
could lead to better classification performance. The spatio-spectral information encoded in
hyperspectral images is complex, and it is not immediately obvious that conventional meth-
ods such as PCA are sufficiently capable of capturing this. Furthermore, learning shared
representations might make it feasible to combine hyperspectral skin lesion datasets (Ngiam
et al., 2011). Researching the potential gains of using deep learning approaches for dimen-
sionality reduction could yield extremely important results.
The incorporation of scale-space ideas can also be explored in obtaining an efficient state
space representation. Scale-space theory is a framework for representing signals on multiple
scales, developed by the computer vision, image processing and signal processing communi-
ties. Scale-space ideas could be used to select tuning parameters in the FDA approach. For a
basis expansion representation of hyperspectral curves, for instance, several key parameters
(e.g. bandwidth, degree of the derivative) must be selected (Chaudhuri & Marron, 2000).
As the representation may be very sensitive to these parameters, scale-space methods can
provide useful insight. For instance, SiZer is a visual tool to examine when the derivative of
a scatterplot-smoother is significantly negative, possibly zero or significantly positive across
a range of smoothing bandwidths (Chaudhuri & Marron, 1999).
Concluding remarks
Recent advances in hyperspectral imaging for skin cancer detection show great promise, and
we believe that further research can lead to a significant reduction in the number of deaths
caused by skin cancer. However, there are still many open research questions that must
be addressed, such as what are the benefits of training classifiers with hyperspectral skin
lesion images as opposed to clinical and dermoscopic images of skin lesions captured with
conventional RGB cameras. To answer this, large, high-quality datasets of skin lesion images
need to be collected using both hyperspectral and conventional RGB cameras. Importantly,
both types of images need to be collected from all observed skin lesions in order to make it
possible to perform e.g. statistical analysis, and to compare classification algorithms trained
on both types of images. Once enough data has been collected, the data can be analyzed
using statistical methodologies such as functional data analysis, multivariate analysis, etc.
26
Furthermore, classification algorithms can be trained using conventional statistical model-
based methodologies and more recent developments based on deep learning approaches. How
to architect and optimize algorithms and models for skin cancer detection using hyperspectral
imaging needs to be discovered by further research. Hyperspectral imaging is widely used
in other fields of research such as remote sensing, and such research should provide a good
foundation on which to build future research efforts towards skin cancer detection.
For reported performance results of classification systems to be valid and reliable, to ease
comparison between systems, and to ensure that the clinical aspect is not ignored, we have
the following recommendations for data collection and statistical analysis of the results:
1. Use an independent test set, not cross-validation.
2. Report specificities for sensitivities from 95% to 100%.
3. Collect data in a clinical-like setting, with clearly stated inclusion and exclusion criteria.
The data should be collected consecutively to reflect the underlying distribution of the
population in question (e.g., hospital patients, primary care patients, etc.).
4. Report confidence intervals for the sensitivities.
5. If the available dataset is too small for independent test set, other aspects of the system
such as spectral band selection or feature selection can be reported instead.
For a more detailed list that will increase the quality of a study even further, see Rosado
et al. (2003).
Funding information
This work has been supported in part by the Canary Islands Government through the ACIISI
(Canarian Agency for Research, Innovation and the Information Society), ITHACA project
“Hyperspectral Identification of Brain Tumors” under Grant Agreement ProID2017010164
and it has been partially supported also by the Spanish Government and European Union
(FEDER funds) as part of support program in the context of Distributed HW/SW Platform
for Intelligent Processing of Heterogeneous Sensor Data in Large Open Areas Surveillance
Applications (PLATINO) project, under contract TEC2017-86722-C4-1-R. Additionally, this
work was completed while Samuel Ortega was beneficiary of a pre-doctoral grant given by
27
the “Agencia Canaria de Investigacion, Innovacion y Sociedad de la Información (ACIISI)”
of the “Conserjería de Economía, Industria, Comercio y Conocimiento” of the “Gobierno de
Canarias”, which is part-financed by the European Social Fund (FSE) (POC 2014–2020, Eje
3 Tema Prioritario 74(85%)). Finally, this work has been also supported in part by the 2016
PhD Training Program for Research Staff of the University of Las Palmas de Gran Canaria.
The project has also partially been funded by grant A33020 from Tromsø Forskningsstif-
telse.
Research resources
The camera prototype used for capturing the hyperspectral images used in our example
figures was provided by Revenio Research Oy.
Acknowledgements
We would like to thank Dr. Herbert Kirchesch for his help in collecting all of the conventional
RGB images and hyperspectral images used in our example figures.
References
Abbasi, N. R., Shaw, H. M., Rigel, D. S., Friedman, R. J., McCarthy, W. H., Osman, I., . . .
Polsky, D. (2004). Early Diagnosis of Cutaneous Melanoma. JAMA,292 (22).
doi:10.1001/jama.292.22.2771
Ahnlide, I., Bjellerup, M., Nilsson, F., & Nielsen, K. (2016). Validity of ABCD Rule of
Dermoscopy in Clinical Practice. Acta Dermato Venereologica,96 (3), 367–372.
doi:10.2340/00015555-2239
American Cancer Society. (2018). Cancer Facts and Figures 2018. Retrieved from
https://www.cancer.org/research/cancer-facts-statistics/all-cancer-facts-
figures/cancer-facts-figures-2018.html
28
Annessi, G., Bono, R., Sampogna, F., Faraggiana, T., & Abeni, D. (2007). Sensitivity,
specificity, and diagnostic accuracy of three dermoscopic algorithmic methods in the
diagnosis of doubtful melanocytic lesions. Journal of the American Academy of
Dermatology,56 (5), 759–767. doi:10.1016/j.jaad.2007.01.014
Bengio, Y., Courville, A., & Vincent, P. (2013). Representation Learning: A Review and
New Perspectives. IEEE Transactions on Pattern Analysis and Machine Intelligence,
35 (8), 1798–1828. doi:10.1109/TPAMI.2013.50
Bray, F., Ferlay, J., Soerjomataram, I., Siegel, R. L., Torre, L. A., & Jemal, A. (2018).
Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality
worldwide for 36 cancers in 185 countries. CA: A Cancer Journal for Clinicians,
00 (00), 1–31. doi:10.3322/caac.21492
Carrara, M., Bono, A., Bartoli, C., Colombo, A., Lualdi, M., Moglia, D., . .. Marchesini, R.
(2007). Multispectral imaging and artificial neural network: mimicking the
management decision of the clinician facing pigmented skin lesions. Physics in
Medicine and Biology,52 (9), 2599–2613. doi:10.1088/0031-9155/52/9/018
Chaudhuri, P. & Marron, J. S. (1999). SiZer for Exploration of Structures in Curves.
Journal of the American Statistical Association,94 (447), 807–823.
doi:10.1080/01621459.1999.10474186
Chaudhuri, P. & Marron, J. S. (2000). Scale space view of curve estimation. The Annals of
Statistics,28 (2), 408–428. doi:10.1214/aos/1016218224
Chen, Y., Zhao, X., & Jia, X. (2015). Spectral–Spatial Classification of Hyperspectral Data
Based on Deep Belief Network. IEEE Journal of Selected Topics in Applied Earth
Observations and Remote Sensing,8(6), 2381–2392.
doi:10.1109/JSTARS.2015.2388577
Codella, N. C. F., Gutman, D., Celebi, M. E., Helba, B., Marchetti, M. A., Dusza, S. W.,
. .. Halpern, A. (2018). Skin lesion analysis toward melanoma detection: A challenge
at the 2017 International symposium on biomedical imaging (ISBI), hosted by the
international skin imaging collaboration (ISIC). In 2018 IEEE 15th International
Symposium on Biomedical Imaging (ISBI 2018) (pp. 168–172).
doi:10.1109/ISBI.2018.8363547
29
Dai, Q., Cheng, J.-H., Sun, D.-W., & Zeng, X.-A. (2015). Advances in Feature Selection
Methods for Hyperspectral Image Processing in Food Industry Applications: A
Review. Critical Reviews in Food Science and Nutrition,55 (10), 1368–1382.
doi:10.1080/10408398.2013.871692
Donoho, D. (2017). 50 Years of Data Science. Journal of Computational and Graphical
Statistics,26 (4), 745–766. doi:10.1080/10618600.2017.1384734
Elbaum, M., Kopf, A. W., Rabinovitz, H. S., Langley, R. G., Kamino, H., Mihm, M. C., . ..
Wang, S. (2001). Automatic differentiation of melanoma from melanocytic nevi with
multispectral digital dermoscopy: A feasibility study. Journal of the American
Academy of Dermatology,44 (2), 207–218. doi:10.1067/mjd.2001.110395
ElMasry, G., Wang, N., & Vigneault, C. (2009). Detecting chilling injury in Red Delicious
apple using hyperspectral imaging and neural networks. Postharvest Biology and
Technology,52 (1), 1–8. doi:10.1016/j.postharvbio.2008.11.008
Esteva, A., Kuprel, B., Novoa, R. A., Ko, J., Swetter, S. M., Blau, H. M., & Thrun, S.
(2017). Dermatologist-level classification of skin cancer with deep neural networks.
Nature,542 (7639), 115–118. doi:10.1038/nature21056
Ferlay, J., Soerjomataram, I., Ervik, M., Dikshit, R., Eser, S., Mathers, C., .. . Bray, F.
(2013). GLOBOCAN 2012 v1.0, cancer incidence and mortality worldwide: IARC
cancerbase no. 11 [internet]. International Agency for Research on Cancer. Retrieved
from http://globocan.iarc.fr
Hinton, G. E. & Salakhutdinov, R. R. (2006). Reducing the Dimensionality of Data with
Neural Networks (tech. rep. No. 5786). doi:10.1126/science.1127647
Jet Propulsion Laboratory, California Institute of Technology. (n.d.). Airborne Visible
InfraRed Imaging Spectrometer (AVIRIS) - Imaging Spectroscopy. Retrieved from
https://aviris.jpl.nasa.gov/aviris/imaging%7B%5C_%7Dspectroscopy.html
K. C. Lawrence, B. Park, W. R. Windham, & C. Mao. (2003). Calibration of a pushbroom
hyperspectral imaging system for agricultural inspection. Transactions of the ASAE,
46 (2). doi:10.13031/2013.12940
30
Kazianka, H., Leitner, R., & Pilz, J. (2008). Segmentation and classification of
hyper-spectral skin data. Data Analysis, Machine Learning and Applications,
245–252. doi:10.1007/978-3-540-78246-9_29
Korotkov, K. & Garcia, R. (2012). Computerized analysis of pigmented skin lesions: A
review. Artificial Intelligence in Medicine,56 (2), 69–90.
doi:10.1016/j.artmed.2012.08.002
Krizhevsky, A., Sutskever, I., & Hinton, G. E. (2012). ImageNet classification with deep
convolutional neural networks. In Advances in neural information processing systems
25 (nips 2012). doi:10.1145/3065386
Kupetsky, E. A. & Ferris, L. K. (2013). The diagnostic evaluation of MelaFind
multi-spectral objective computer vision system. Expert Opinion on Medical
Diagnostics,7(4), 405–411. doi:10.1517/17530059.2013.785520
Lachenal, G. & Ozaki, Y. (1999). Advantages of near infrared spectroscopy for the analysis
of polymers and composites. Macromolecular Symposia,141 (1), 283–292.
doi:10.1002/masy.19991410123
Lee, K.-S., Cohen, W. B., Kennedy, R. E., Maiersperger, T. K., & Gower, S. T. (2004).
Hyperspectral versus multispectral data for estimating leaf area index in four
different biomes. Remote Sensing of Environment,91 (3-4), 508–520.
doi:10.1016/j.rse.2004.04.010
Li, Q., He, X., Wang, Y., Liu, H., Xu, D., & Guo, F. (2013). Review of spectral imaging
technology in biomedical engineering: achievements and challenges. Journal of
Biomedical Optics,18 (10). doi:10.1117/1.JBO.18.10.100901
Li, Q., Zhou, M., Liu, H., Wang, Y., & Guo, F. (2015). Red Blood Cell Count Automation
Using Microscopic Hyperspectral Imaging Technology. Applied Spectroscopy,69 (12),
1372–1380. doi:10.1366/14-07766
Lihacova, I., Bolochko, K., Plorina, E. V., Lange, M., Lihachev, A., Bliznuks, D., &
Derjabo, A. (2018). A method for skin malformation classification by combining
multispectral and skin autofluorescence imaging. In J. Popp, V. V. Tuchin, & F. S.
Pavone (Eds.), Biophotonics: Photonic solutions for better health care vi
(Vol. 1068535, p. 113). SPIE. doi:10.1117/12.2306203
31
Lorencs, A., Sinica-Sinavskis, J., Jakovels, D., & Mednieks, I. (2016). Melanoma-nevus
discrimination based on image statistics in few spectral channels. Elektronika ir
Elektrotechnika,22 (2), 66–72. doi:10.5755/j01.eie.22.2.12173
Lu, G. & Fei, B. (2014). Medical hyperspectral imaging: a review. Journal of Biomedical
Optics,19 (1). doi:10.1117/1.JBO.19.1.010901
MacKinnon, N., Vasefi, F., & Farkas, D. L. (2014). Toward in vivo diagnosis of skin cancer
using multimode imaging dermoscopy: (I) clinical system development and validation.
8947 (1). doi:10.1117/12.2041818
Makantasis, K., Karantzalos, K., Doulamis, A., & Doulamis, N. (2015). Deep supervised
learning for hyperspectral data classification through convolutional neural networks.
In 2015 ieee international geoscience and remote sensing symposium (igarss)
(Vol. 2015-Novem, pp. 4959–4962). IEEE. doi:10.1109/IGARSS.2015.7326945
Møllersen, K., Kirchesch, H., Zortea, M., Schopf, T. R., Hindberg, K., & Godtliebsen, F.
(2015). Computer-Aided Decision Support for Melanoma Detection Applied on
Melanocytic and Nonmelanocytic Skin Lesions: A Comparison of Two Systems Based
on Automatic Analysis of Dermoscopic Images. BioMed Research International,2015,
1–8. doi:10.1155/2015/579282
Møllersen, K., Zortea, M., Schopf, T. R., Kirchesch, H., & Godtliebsen, F. (2017).
Comparison of computer systems and ranking criteria for automatic melanoma
detection in dermoscopic images. PLoS ONE,12 (12).
doi:10.1371/journal.pone.0190112
Moncrieff, M., Cotton, S., Claridge, E., & Hall, P. (2002). Spectrophotometric
intracutaneous analysis: a new technique for imaging pigmented skin lesions. British
Journal of Dermatology,146 (3), 448–457. doi:10.1046/j.1365-2133.2002.04569.x
Monheit, G., Cognetta, A. B., Ferris, L., Rabinovitz, H., Gross, K., Martini, M., . . .
Gutkowicz-Krusin, D. (2011). The Performance of {MelaFind}: A Prospective
Multicenter Study. Archives of Dermatology,147 (2), 188–194.
doi:10.1001/archdermatol.2010.302
Mughees, A., Ali, A., & Tao, L. (2017). Hyperspectral image classification via
shape-adaptive deep learning. In 2017 ieee international conference on image
32
processing (icip) (Vol. 2017-Septe, pp. 375–379). IEEE.
doi:10.1109/ICIP.2017.8296306
Nachbar, F., Stolz, W., Merkle, T., Cognetta, A. B., Vogt, T., Landthaler, M., . . .
Plewig, G. (1994). The {ABCD} rule of dermatoscopy. {H}igh prospective value in
the diagnosis of doubtful melanocytic skin lesions. Journal of the American Academy
of Dermatology,30 (4), 551–559. doi:10.1016/S0190-9622(94)70061-3
Nagaoka, T., Kiyohara, Y., Koga, H., Nakamura, A., Saida, T., & Sota, T. (2015).
Modification of a melanoma discrimination index derived from hyperspectral data: A
clinical trial conducted in 2 centers between March 2011 and December 2013. Skin
Research and Technology,21 (3), 278–283. doi:10.1111/srt.12188
Nagaoka, T., Nakamura, A., Kiyohara, Y., & Sota, T. (2012). Melanoma screening system
using hyperspectral imager attached to imaging fiberscope. Proceedings of the Annual
International Conference of the IEEE Engineering in Medicine and Biology Society,
EMBS,30, 3728–3731. doi:10.1109/EMBC.2012.6346777
Nagaoka, T., Nakamura, A., Okutani, H., Kiyohara, Y., Koga, H., Saida, T., & Sota, T.
(2013). Hyperspectroscopic screening of melanoma on acral volar skin. Skin Research
and Technology,19 (1), 290–296. doi:10.1111/j.1600-0846.2012.00642.x
Nagaoka, T., Nakamura, A., Okutani, H., Kiyohara, Y., & Sota, T. (2012). A possible
melanoma discrimination index based on hyperspectral data: A pilot study. Skin
Research and Technology,18 (3), 301–310. doi:10.1111/j.1600-0846.2011.00571.x
Nakariyakul, S. & Casasent, D. P. (2007). Adaptive branch and bound algorithm for
selecting optimal features. Pattern Recognition Letters,28 (12), 1415–1427.
doi:10.1016/j.patrec.2007.02.015
Ngiam, J., Khosla, A., Kim, M., Nam, J., Lee, H., & Ng, A. Y. (2011). Multimodal Deep
Learning. In Proceedings of the 28th international conference on machine learning
(icml-11) (pp. 689–696).
Oliveira, R. B., Papa, J. P., Pereira, A. S., & Tavares, J. M. R. S. (2018). Computational
methods for pigmented skin lesion classification in images: review and future trends.
Neural Computing and Applications,29 (3), 613–636. doi:10.1007/s00521-016-2482-6
33
Ortega, S., Fabelo, H., Camacho, R., de la Luz Plaza, M., Callico, G. M., & Sarmiento, R.
(2018). Detecting brain tumor in pathological slides using hyperspectral imaging.
Biomedical Optics Express,9(2), 818. doi:10.1364/BOE.9.000818
Pan, S. J. & Yang, Q. (2010). A survey on transfer learning. IEEE Transactions on
Knowledge and Data Engineering,22 (10), 1345–1359. doi:10.1109/TKDE.2009.191
Patwardhan, S. V. & Dhawan, A. P. (2004). Multi-spectral imaging and analysis for
classification of melanoma. Conference proceedings : ... Annual International
Conference of the IEEE Engineering in Medicine and Biology Society. IEEE
Engineering in Medicine and Biology Society. Conference,1, 503–6.
doi:10.1109/IEMBS.2004.1403204
Patwardhan, S. V., Dhawan, A. P., & Relue, P. A. (2005). Monte Carlo simulation of
light-tissue interaction: Three-dimensional simulation for trans-illumination-based
imaging of skin lesions. IEEE Transactions on Biomedical Engineering,52 (7),
1227–1236. doi:10.1109/TBME.2005.847546
Qi, X., Xing, F., Foran, D. J., & Yang, L. (2011). Comparative performance analysis of
stained histopathology specimens using RGB and multispectral imaging. (Vol. 7963).
doi:10.1117/12.878325
Quinzán, I., Sotoca, J. M., Latorre-Carmona, P., Pla, F., García-Sevilla, P., & Boldó, E.
(2013). Band selection in spectral imaging for non-invasive melanoma diagnosis.
Biomedical Optics Express,4(4), 514. doi:10.1364/BOE.4.000514
Rey-Barroso, L., Burgos-Fernández, F., Delpueyo, X., Ares, M., Royo, S., Malvehy, J., .. .
Vilaseca, M. (2018). Visible and Extended Near-Infrared Multispectral Imaging for
Skin Cancer Diagnosis. Sensors,18 (5), 1441. doi:10.3390/s18051441
Rosado, B., Menzies, S., Harbauer, A., Pehamberger, H., Wolff, K., Binder, M., &
Kittler, H. (2003). Accuracy of Computer Diagnosis of Melanoma: A Quantitative
Meta-analysis. Archives of Dermatology,139 (3), 361–367.
doi:10.1001/archderm.139.3.361
Rubins, U., Zaharans, J., L
,ihačova, I., & Spigulis, J. (2014). Multispectral
Video-Microscope Modified for Skin Diagnostics. Latvian Journal of Physics and
Technical Sciences,51 (5), 65–70. doi:10.2478/lpts-2014-0031
34
Shahshahani, B. M. & Landgrebe, D. A. (1994). The Effect of Unlabeled Samples in
Reducing the Small Sample Size Problem and Mitigating the Hughes Phenomenon.
IEEE Transactions on Geoscience and Remote Sensing,32 (5), 1087–1095.
doi:10.1109/36.312897
Smialowski, P., Frishman, D., & Kramer, S. (2010). Pitfalls of supervised feature selection.
Bioinformatics,26 (3), 440–443. doi:10.1093/bioinformatics/btp621
Smith, R. B. (2012). Introduction to Hyperspectral Imaging. Retrieved June 26, 2018, from
https://www.microimages.com/documentation/Tutorials/hyprspec.pdf
Song, E., Grant-Kels, J. M., Swede, H., D’Antonio, J. L., Lachance, A., Dadras, S. S., . . .
Rothe, M. J. (2016). Paired comparison of the sensitivity and specificity of
multispectral digital skin lesion analysis and reflectance confocal microscopy in the
detection of melanoma in vivo: A cross-sectional study. Journal of the American
Academy of Dermatology,75 (6), 1187–1192.e2. doi:10.1016/j.jaad.2016.07.022
Stamnes, J. J., Ryzhikov, G., Biryulina, M., Hamre, B., Zhao, L., & Stamnes, K. (2017).
Optical detection and monitoring of pigmented skin lesions. Biomedical Optics
Express,8(6), 2946. doi:10.1364/BOE.8.002946
Suárez, I. Q., Carmona, P. L., García-Sevilla, P., Boldo, E., Pla, F., Jiménez, V. G., .. .
de Lucía, G. P. (2012). Non-invasive Melanoma Diagnosis using Multispectral
Imaging. In Proceedings of the 1st international conference on pattern recognition
applications and methods (January, pp. 386–393). SciTePress - Science.
doi:10.5220/0003843803860393
Świtoński, A., Michalak, M., Josiński, H., & Wojciechowski, K. (2010). Detection of Tumor
Tissue Based on the Multispectral Imaging. (Vol. 1732, pp. 325–333).
doi:10.1007/978-3-642-15907-7_40
Taghizadeh, M., Gowen, A. A., & O’Donnell, C. P. (2011). Comparison of hyperspectral
imaging with conventional RGB imaging for quality evaluation of Agaricus bisporus
mushrooms. Biosystems Engineering,108 (2), 191–194.
doi:10.1016/j.biosystemseng.2010.10.005
35
Tomatis, S., Bono, A., Bartoli, C., Carrara, M., Lualdi, M., Tragni, G., & Marchesini, R.
(2003). Automated melanoma detection: Multispectral imaging and neural network
approach for classification. Medical Physics,30 (2), 212–221. doi:10.1118/1.1538230
Tomatis, S., Carrara, M., Bono, A., Bartoli, C., Lualdi, M., Tragni, G., .. . Marchesini, R.
(2005). Automated melanoma detection with a novel multispectral imaging system:
Results of a prospective study. Physics in Medicine and Biology,50 (8), 1675–1687.
doi:10.1088/0031-9155/50/8/004
Tuia, D., Volpi, M., Copa, L., Kanevski, M., & Munoz-Mari, J. (2011). A Survey of Active
Learning Algorithms for Supervised Remote Sensing Image Classification. IEEE
Journal of Selected Topics in Signal Processing,5(3), 606–617.
doi:10.1109/JSTSP.2011.2139193
Unlu, E., Akay, B. N., & Erdem, C. (2014). Comparison of dermatoscopic diagnostic
algorithms based on calculation: The ABCD rule of dermatoscopy, the seven-point
checklist, the three-point checklist and the CASH algorithm in dermatoscopic
evaluation of melanocytic lesions. The Journal of Dermatology,41 (7), 598–603.
doi:10.1111/1346-8138.12491
Vasefi, F., MacKinnon, N., Saager, R., Kelly, K. M., Maly, T., Booth, N., . . . Farkas, D. L.
(2016). Separating melanin from hemodynamics in nevi using multimode
hyperspectral dermoscopy and spatial frequency domain spectroscopy. Journal of
Biomedical Optics,21 (11), 114001. doi:10.1117/1.JBO.21.11.114001
Vestergaard, M. E. & Menzies, S. W. (2008). Automated diagnostic instruments for
cutaneous melanoma. Seminars in cutaneous medicine and surgery,27 (1), 32–36.
Wang, Q., Wang, J., Zhou, M., Li, Q., & Wang, Y. (2017). Spectral-spatial feature-based
neural network method for acute lymphoblastic leukemia cell identification via
microscopic hyperspectral imaging technology. Biomedical Optics Express,8(6),
3017. doi:10.1364/BOE.8.003017
Wang, W., Li, C., Tollner, E. W., Rains, G. C., & Gitaitis, R. D. (2012). A liquid crystal
tunable filter based shortwave infrared spectral imaging system: Calibration and
characterization. Computers and Electronics in Agriculture,80, 135–144.
doi:10.1016/j.compag.2011.09.003
36
Wu, D. & Sun, D.-W. (2013). Application of visible and near infrared hyperspectral
imaging for non-invasively measuring distribution of water-holding capacity in salmon
flesh. Talanta,116, 266–276. doi:10.1016/j.talanta.2013.05.030
Xing, J., Bravo, C., Jancsók, P. T., Ramon, H., & De Baerdemaeker, J. (2005). Detecting
Bruises on ‘Golden Delicious’ Apples using Hyperspectral Imaging with Multiple
Wavebands. Biosystems Engineering,90 (1), 27–36.
doi:10.1016/j.biosystemseng.2004.08.002
Yamal, J.-M., Zewdie, G. A., Cox, D. D., Neely Atkinson, E., Cantor, S. B., MacAulay, C.,
. . . Follen, M. (2012). Accuracy of optical spectroscopy for the detection of cervical
intraepithelial neoplasia without colposcopic tissue information; a step toward
automation for low resource settings. Journal of Biomedical Optics,17 (4).
doi:10.1117/1.JBO.17.4.047002
Zeiler, M. D. & Fergus, R. (2014). Visualizing and Understanding Convolutional Networks.
(pp. 818–833). doi:10.1007/978-3-319-10590-1_53
Zheludev, V., Pölönen, I., Neittaanmäki-Perttu, N., & Averbuch, A. (2015). Biomedical
Signal Processing and Control Delineation of malignant skin tumors by hyperspectral
imaging using diffusion maps dimensionality reduction. Biomedical Signal Processing
and Control,16, 48–60. doi:10.1016/j.bspc.2014.10.010
Zherdeva, L. A., Bratchenko, I. A., Myakinin, O. O., Moryatov, A. A., Kozlov, S. V., &
Zakharov, V. P. (2016). In vivo hyperspectral imaging and differentiation of skin
cancer. 10024, 100244G. doi:10.1117/12.2246433
37