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ORIGINAL ARTICLE

Characterizing the role of


dermatologists in developing artificial
intelligence for assessment of skin
cancer: A systematic review
George A. Zakhem, MD, MBA,a Joseph W. Fakhoury, BS,b Catherine C. Motosko, MD,a and
Roger S. Ho, MD, MS, MPHa
New York, New York and Detroit, Michigan

Background: The use of artificial intelligence (AI) for skin cancer assessment has been an emerging topic
in dermatology. Leadership of dermatologists is necessary in defining how these technologies fit into
clinical practice.

Objective: To characterize the evolution of AI in skin cancer assessment and characterize the involvement
of dermatologists in developing these technologies.

Methods: An electronic literature search was performed using PubMed by searching machine learning or
artificial intelligence combined with skin cancer or melanoma. Articles were included if they used AI for
screening and diagnosis of skin cancer using data sets consisting of dermoscopic images or photographs of
gross lesions.

Results: Fifty-one articles were included, and 41% of these had dermatologists included as authors.
Articles that included dermatologists described algorithms built with more images versus articles that did
not include dermatologists (mean, 12,111 vs 660 images, respectively). In terms of underlying technology,
AI used for skin cancer assessment has followed trends in the field of image recognition.

Limitations: This review focused on models described in the medical literature and did not account for
those described elsewhere.

Conclusions: Greater involvement of dermatologists is needed in thinking through issues in data


collection, data set biases, and applications of technology. Dermatologists can provide access to
large, diverse data sets that are increasingly important for building these models. ( J Am Acad Dermatol
https://doi.org/10.1016/j.jaad.2020.01.028.)

Key words: artificial intelligence; computer vision; machine learning; melanoma; nevi; pigmented lesions;
skin cancer screening.

O ver the past decade, we have seen a sharp plethora of tasks we perform on a daily basis and is
increase in the use of artificial intelligence becoming an increasingly crucial part of the
(AI). This rise has been bolstered by conveniences of modern life. These technologies
an explosion in the generation of digital data, have also begun shaping the global economy and
substantial advances in computing hardware, and industries around the world; AI has become a part of
innovation in algorithm design.1 AI now underlies a crucial functions in the fields of finance, engineering,

From the Ronald O. Perelman Department of Dermatology, New School of Medicine, 240 E 38th St, Floor 12, New York, NY
York University School of Medicinea; and Wayne State Univer- 10016. E-mail: Roger.Ho@nyumc.org.
sity School of Medicine, Detroit.b Published online February 26, 2020.
Funding sources: None. 0190-9622/$36.00
Conflicts of interest: None disclosed. Ó 2020 by the American Academy of Dermatology, Inc.
Accepted for publication January 11, 2020. https://doi.org/10.1016/j.jaad.2020.01.028
Correspondence to: Roger S. Ho, MD, MS, MPH, The Ronald O.
Perelman Department of Dermatology, New York University

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marketing, and entertainment and has now begun to the full texts of 83 articles were assessed, of
find its way into medicine. which 51 were included in the final analysis (Fig 1
Computer visionda subset of AI that involves and Table I3-52). Overall, 41% of the included articles
computer recognition of imagesdin dermatology had dermatologists included as an author. Articles
has garnered substantial attention over the last that included dermatologists as authors described
2 years, as deep learning has allowed AI to approach algorithms built with a larger average image data set
dermatologist-level classification of skin cancer.2 versus articles that did not include dermatologists
However, the use of these (mean, 12,112 vs 660 images;
models in dermatology has standard deviation, 823 vs
been explored for decades. CAPSULE SUMMARY
28,187; median, 426 vs 304
In this review, we aim to images; interquartile range,
characterize the evolution of d
Artificial intelligence for evaluation of 199 to 866 vs 172.5 to 801,
the use of AI in skin cancer skin cancer has been an emerging topic respectively) (Fig 2). The
screening and assessment in dermatology; however, dermatologist number of publications,
and to characterize the involvement in designing and most common algorithms,
involvement of dermatolo- implementing these technologies has and relative distribution of
gists in developing these not been studied. articles including and not
models. d Dermatologists are underrepresented in including dermatologists
publications describing these among the authors were re-
METHODS technologies. Increased involvement and corded for each year (Fig 3).
An electronic literature leadership of dermatologists are Of the 12 convolutional neu-
search was performed on paramount to designing clinically ral networks identified in the
February 19, 2019, with the relevant and efficacious models. literature, 8 used transfer
PubMed database. Articles learning; the most common
published from inception pretrained models used were
through February 19, 2019, were included in the versions of Google’s Inception architecture (Google,
search. Search terms included machine learning or Mountain View, CA) (n = 3) and Microsoft’s ResNet
artificial intelligence combined with skin cancer or (n = 3). Forty five percent of the articles identified
melanoma. were published over the last 3 years.
Study selection was performed based on inclusion Of the publications identified, 70% did not list a
criteria consisting of (1) full-length trials, (2) use of dermatologist as an author. Of the 45 articles that
machine learning for screening and diagnosis of skin described the disease composition of the image set
cancer, and (3) use of data sets consisting of used for algorithm training, 70% reported a base rate
dermatoscopic images or photographs of gross of disease images of at least 30%, and 26% reported a
lesions. Studies were excluded on the following base rate of at least 50%. Of the 51 articles included,
criteria: (1) duplicate publications, (2) reviews, (3) 38 used data sets of dermoscopic images to train the
abstracts or presentations, (4) no use of artificial described algorithms, 12 used data sets of gross
intelligence, (5) use of imaging modalities other than images, and 1 used a combination of both. The
dermoscopy and gross photography, (6) use of country of origin for each author of the included
histopathologic images, (7) no diagnosis of lesions, articles was also recorded (Fig 4).
(8) not published in English, and (9) use of only
animal models. DISCUSSION
Titles and abstracts were assessed on these criteria Our findings suggest that machine learning
by 2 independent blinded reviewers (GAZ and JWF). algorithms for skin cancer assessment have followed
If the title or abstract did not include enough general trends in the field of image recognition. The
information to apply exclusion criteria, the full text trends we observed reflected technology advances
was assessed. The reviewers compared results, and in the field, as well as growing interest in and
any discrepancies were resolved by arbitration by adoption of these algorithms.
the senior author (RSH). The full text of the In terms of the technologies used to build the
remaining articles was reviewed in detail to algorithms, there appeared to be 3 eras of
determine eligibility based on the inclusion criteria. development in the literature. From 1994 to 2011,
algorithms were built primarily by using classical
RESULTS machine learning, such as logistic regressions,
During the initial search, 463 articles were Bayesian classifiers, and simple feedforward neural
reviewed. After the inclusion criteria were applied, networks. These algorithms were typically built with
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input images.53 However, this increase in publica-


Abbreviation used:
tions has been driven largely by teams of
AI: artificial intelligence nondermatologists.
This finding is of particular concern because,
based on the typical composition of the data sets
data sets of fewer than 1000 images, required human used, the models described are designed for use by
feature engineering based most commonly on the dermatologists. The majority of data sets used to train
ABCDEs of melanoma, and involved painstaking and test these models have a disease base rate
image preprocessing before model training. From between 30% and 50%, which would be appropriate
2011 to 2016, algorithms were built most commonly for a dermatologist using the model to assess
by using support vector machines, which are more higher-risk lesions. However, this same base rate, if
sophisticated, nonlinear classifiers. These systems used in the primary care setting or a patient-facing
typically had automated yet human-engineered app, could result in high rates of false positive
feature extraction and were trained with more screening results. Moreover, the majority of models
images, yet data sets still seldom consisted of more are built with dermoscopic images; dermoscopes are
than 1000 photos. much less likely to be available to a primary care
Over the last 2 years, AI in skin cancer assessment practitioner or patient than to a dermatologist.
has been radically affected by the revolution in deep Although decision support for dermatology is a
learning. Since 2017, there has been a sharp rise in viable use case for these technologies, it should be
the number of publications describing new models dermatologists, rather than data scientists, who
in the literature (Fig 3), and the majority have been define how this technology is used in the clinical
built using convolutional neural networksdmodels setting. A robust understanding of the clinical
consisting of several layers of simple algorithms that context is absolutely essential for effective
extract and assess features automatically to classify implementation of these technologies.

Fig 1. Search methodology and results of the literature search on artificial intelligence in skin
cancer screening.
Table I. Publications identified through systematic review of the literature

4 Zakhem et al
Transfer
Dermatologists learning
included as Base Image type used for
authors? Images in rate of used to convolutional
Country of origin (number of data set, disease, train the neural network
Authors Year of authors dermatologists) n % algorithm Classification task Algorithm architecture Reference
3
Ercal et al 1994 United States No 326 56.13 Gross Classifies images as Feedforward artificial N/A
melanoma vs benign neural network
melanocytic lesions
4
Rubegni et al 2002 Italy Yes (4) 147 61.22 Dermoscopic Classifies images as Simple single-layer N/A
melanoma vs atypical perceptron artificial
nevus neural network
5
Stanley et al 2003 United States Yes (1) 258 50 Gross Classifies images as Fuzzy-logic color N/A
melanoma vs benign histogram analysis
lesion technique
6
Maglogiannis 2004 Greece No 17 41.18 Gross Classifies images as Support vector machine N/A
et al melanoma vs atypical
nevus
7
Maglogiannis 2005 Greece No 34 41.18 Gross Classifies images as Feedforward neural N/A
et al melanoma vs atypical network
nevus
8
Stoecker et al 2005 United States Yes (3) 512 32.23 Dermoscopic Classifies images as Neural network N/A
melanoma vs benign
melanocytic lesions
9
Stanley et al 2007 United States Yes (1) 226 50 Dermoscopic Classifies images as Relative color histogram N/A
melanoma vs atypical
nevus
10
Surowka et al 2007 Poland No 39 48.72 Dermoscopic Classifies images as Neural network N/A
melanoma vs atypical (multilayer
nevus perceptron-based
binary classifier),
support vector
machine, attributional
calculus
11

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Iyatomi et al 2008 Japan, United States Yes (4) 199 15.08 Dermoscopic Classifies images as Linear classifier N/A
melanoma vs benign
melanocytic lesions
12
Ruiz et al 2008 Spain No 110 d Dermoscopic Classifies images as Bayesian classifier and N/A
melanoma vs benign multilayer perceptron
melanocytic lesions artificial neural

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Khan et al 2009 Australia, Italy, Yes (5) 424 31.6 Dermoscopic Classifies images as Feedforward artificial N/A
United States melanoma vs benign neural network
melanocytic lesions
14
Gilmore et al 2010 Austria, Australia Yes (3) 199 50.75 Dermoscopic Classifies images as Support vector machine N/A
melanoma vs atypical
nevus
15
Surowka et al 2010 Poland No 158 49.37 Dermoscopic Classifies images as Attributional calculus N/A
melanoma vs atypical
nevus
16
Tenenhaus 2010 France No 180 d Dermoscopic Classifies images as Kernel logisticdpartial N/A
et al melanoma vs benign least-squares
melanocytic lesions multinomial
regression
17
Cheng et al 2012 United States Yes (2) 489 53.78 Dermoscopic Classifies images as BCC 3-layer multilayer N/A
vs benign lesion perceptron neural
network, direct neural
dynamic
programming
18
Garnavi et al 2012 Australia No 289 39.44 Dermoscopic Classifies images as Support vector machine, N/A
melanoma vs benign random forest, logistic
melanocytic lesions model tree, hidden
naive Bayes
19
Liu et al 2012 United Kingdom No 351 25.07 Dermoscopic Classifies images as Support vector machine N/A
melanoma vs benign
melanocytic lesions
20
Chang et al 2013 Taiwan Yes (3) 769 22.62 Gross Classifies images as 1 of Support vector machines N/A
19 distinct diagnoses
(14 benign, 5
malignant)
21
Cheng et al 2013 United States Yes (4) 114 30.7 Dermoscopic Classifies images as BCC Backpropagation neural N/A
vs benign lesion network
22
Liu et al 2013 United Kingdom No 307 73.62 Dermoscopic Classifies images as Support vector machine N/A
melanoma vs atypical
nevus
23
Lingala et al 2014 United States Yes (6) 866 19.98 Dermoscopic Classifies images as Support vector machines N/A
melanoma vs benign

Zakhem et al 5
melanocytic lesions
24
Riaz et al 2014 Portugal, Pakistan No 200 20 Dermoscopic Classifies images as Support vector machine N/A
melanoma vs benign
melanocytic lesions
Continued
Table I. Cont’d

6 Zakhem et al
Transfer
Dermatologists learning
included as Base Image type used for
authors? Images in rate of used to convolutional
Country of origin (number of data set, disease, train the neural network
Authors Year of authors dermatologists) n % algorithm Classification task Algorithm architecture Reference
25
Sabouri et al 2014 New Zealand, No 412 42.48 Gross Classifies images as Cascade classifier of 2 N/A
Sweden melanoma vs benign support vector
melanocytic lesions machines
26
Souza and 2014 Brazil No 762 74.67 Gross Classifies images as Paraconsistent artificial N/A
Abe melanoma vs benign neural network
melanocytic lesions
27
Ferris et al 2015 United States Yes (3) 426 50 Dermoscopic Classifies images as Decision forest (1000 N/A
malignant (including decision trees)
melanoma and NMSC)
vs benign lesions
28
Kaur et al 2015 United States Yes (1) 192 59.38 Dermoscopic Classifies images as Logistic regression N/A
melanoma vs benign
melanocytic lesions
29
Rastgoo et al 2015 Spain, France No 180 50 Dermoscopic Classifies images as Support vector machine, N/A
melanoma vs atypical gradient boosting,
nevus random forest
30
Shimizu et al 2015 Japan, United Yes (1) 964 28.22 Dermoscopic Classifies images as Layered linear classifiers N/A
States melanoma, benign
nevus, BCC, or SK
31
Jafari et al 2016 Iran, United States No 170 41.18 Gross Classifies images as Support vector machines N/A
melanoma vs benign
melanocytic lesions
32
Jaworek- 2016 Poland No 300 20 Dermoscopic Classifies images as Support vector machines N/A
Korjakowska melanoma or nevi,
et al recognizing 3
histotypes of benign
nevi
33
Jaworek- 2016 Poland No 200 35 Dermoscopic Classifies images as Support vector machines N/A

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Korjakowska micromelanoma vs
benign nevus
34
Kefel et al 2016 Algeria, United Yes (5) 1378 29.32 Dermoscopic Classifies images as BCC Logistic regression N/A
States vs benign lesion
35
Nasr-Esfahani 2016 Iran, United States No 170 41.12 Gross Classifies images as Convolutional neural No transfer
et al melanoma vs benign network learning

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melanocytic lesions
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36
Premaladha 2016 India No 992 d Dermoscopic Classifies images as Deep learningebased No transfer
et al melanoma vs benign neural network, learning
lesion support vector
machine, hybrid
Adaboost
37
Sabbaghi 2016 Australia No 814 21.38 Dermoscopic Classifies images as Stacked sparse encoder No transfer
et al melanoma vs atypical of bag of features learning
nevus
2
Esteva et al 2017 United States Yes (3) 129,405 d Gross and Classifies images as 1 of Convolutional neural Inception
dermoscopic 757 distinct disease network version 3
classes composed of architecture
2032 diagnoses
38
Gareau et al 2017 United States Yes (5) 120 50 Dermoscopic Classifies images as Q-learning, 13 machine N/A
melanoma vs atypical learning algorithms
nevus
39
Munia et al 2017 United States No 170 1.12 Gross Classifies images as Support vector machine, N/A
melanoma vs benign k-nearest neighbor,
melanocytic lesions decision tree, random
forest
40
Xie et al 2017 China, United No 600 33.33 Dermoscopic Classifies images as Neural network N/A
States melanoma vs benign ensemble of fuzzy
lesion neural networks
41
Yu et al 2017 China No 1279 29.63 Dermoscopic Classifies images as Fully convolutional Unnamed
melanoma vs benign residual network architecture
lesion (segmentation)/very trained on
deep residual network ImageNet
(classification)
42
Gautam et al 2018 India No 294 46.94 Gross Classifies images as Random forest (best of 4 N/A
melanoma vs benign different types)
melanocytic lesions
43
Gilmore et al 2018 Australia Yes (1) 250 66 Dermoscopic Classifies images as Support vector machine, N/A
melanoma vs atypical random forest, linear
nevus regression
Haenssle et al 2018 France, Germany, Yes (9) [100,000 20 Dermoscopic Classifies images as Convolutional neural Inception 44

United States melanoma or nevus, network version 4


recognizing 8 architecture

Zakhem et al 7
histotypes of
melanoma and 12
histotypes of nevus
Continued
Table I. Cont’d

8 Zakhem et al
Transfer
Dermatologists learning
included as Base Image type used for
authors? Images in rate of used to convolutional
Country of origin (number of data set, disease, train the neural network
Authors Year of authors dermatologists) n % algorithm Classification task Algorithm architecture Reference
45
Han et al 2018 Korea Yes (4) 16,684 d Gross Classifies images as 1 of Convolutional neural Microsoft
12 distinct diagnoses network ResNet-152
(8 benign and 4
malignant)
46
Li et al 2018 China No 2600 18.88 Dermoscopic Classifies images as Convolutional neural No transfer
melanoma vs benign network learning
melanocytic lesions
47
Mahbod et al 2018 Austria, United No 2787 20.02 Dermoscopic Classifies images as Convolutional neural AlexNet,
Kingdom, Sweden melanoma, benign network VGGNet,
nevus, or SK ResNet
48
Rebouças Filho 2018 Brazil, India No 3100 d Dermoscopic Classifies images as Multilayer perceptron N/A
et al melanoma vs benign
lesion
49
Wahba et al 2018 Egypt, United States No 1200 50 Dermoscopic Classifies images as Support vector machine, N/A
melanoma, BCC, multilayer perceptron
nevus, or benign
keratocytic lesion
50
Walker et al 2018 Israel, United States No 482 50 Dermoscopic Classifies images as Convolutional neural Inception
malignant (including network version 2
melanoma and NMSC) architecture
vs benign lesions
51
Yu et al 2018 Korea, United States Yes (4) 724 48.34 Dermoscopic Classifies images as Convolutional neural Unnamed
melanoma vs benign network architecture
melanocytic lesions trained on
ImageNet
52
Yu et al 2018 China, United States No 1279 19.39 Dermoscopic Classifies images as Convolutional neural ResNet
melanoma vs benign network
lesion

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BCC, Basal cell carcinoma; N/A, not applicable; NMSC, nonmelanoma skin cancer; SK, seborrheic keratosis.

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VOLUME jj, NUMBER j

Fig 2. Comparison of image data set size in publications with and without dermatologist
involvement.

Dermatologist input is also paramount to improve only 10,015 standardized clinical images of skin
model efficacy for other reasons, notably the lesions,55 which is likely too small to build a reliable
procurement and validation of larger and more decision-support system. Moreover, this data set
diverse data sets of images with which to train appears to contain exclusively images taken of
and validate models. In our review, we found light-skinned patients, such that a model trained on
that the models described in publications with this data set would likely be less effective for patients
dermatologist authorship were built with a higher of color. If models trained with biased data sets are
average number of images. Moreover, the 3 eventually used in clinical practice, existing outcome
publications in the literature describing models built disparities56,57 could be exacerbated58; furthermore,
with tens of thousands of images involved extensive it could be difficult for dermatologists to recognize
collaboration with dermatology departments. the cause of this phenomenon without active
The number of images used in model training has involvement in procuring training data sets and
become one of the most important factors in developing these models.
developing the latest generation of deep learning In the field at large, advances in computing
models. Whereas the performance of classic hardware, increased generation of digital data, and
machine learning models plateaus after a threshold algorithm improvements have been the biggest
number of images, deep learning performance scales drivers of the deep learning revolution1; however,
efficiently with the amount of input data (Fig 5).54 in dermatology, the increased availability and
Currently, the largest open-source data set contains improved usability of tools to build deep learning
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Fig 3. Number of computer vision publications in dermatology and with dermatologist


involvement by year. CML, Classical machine learning; CNN, convolutional neural network;
SVM, support vector machine.

Fig 4. Normalized global distribution of dermatology computer vision authorship. This figure
shows the number of authors per country normalized to country population.64 In terms of
absolute numbers, the most authors were affiliated with institutions in the United States
(117 authors), followed by China and South Korea (13 authors each), the United Kingdom
(12 authors), and Australia (10 authors).

models may have been the more relevant catalyst for increasingly routine as the next generation of
this new era in computer vision. For example, open machine learning products are used to develop
source tools, such as Google’s Tensorflow and models without any coding from the user.61-63
Inception architecture,59,60 have greatly simplified Instead, the skill sets necessary to build practical
the coding necessary to build these models. In applications of this technology are shifting; critically
fact, performing machine learning will become thinking through issues in data collection, potential
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would likely be described in the literature when fully


developed as part of a potential US Food and Drug
Administration approval process or to raise clinician
awareness. In addition, coauthorship is not a
completely reliable surrogate in determining the
extent of dermatologist involvement. Meaningful
participation in these projectsdincluding extensive
involvement in designing studies, curating and
validating data, and determining the optimal clinical
setting for usedis difficult to assess, and a reliable
surrogate for this has not been described. However,
we believe that having no dermatologist among the
authors is an extremely reliable surrogate for a lack
of meaningful involvement by dermatologists.
We were unable to compare and assess model
Fig 5. Comparison of the performance and size of data sets
efficacy in this review, largely because of a lack of
among deep learning and classical machine learning homogeneity in reporting metrics and target
models. With classical machine learning algorithms, such variables of the models. We observed a lack of
as logistic regressions, decisions trees, and simple standardization in the reporting of accuracy metrics,
feedforward artificial neural networks, model performance and we believed we were unable to assess potential
eventually plateaus as the amount of data used in training distortion of model efficacy caused by overfitting or
increases. With deep learning, performance scales efficiently data leakage. We were unable to compare clinical
with more data. For this reason, access to larger data sets of outcomes, because nearly all models were tested
imagesdand therefore involvement of dermatologists and exclusively with retrospective clinical images. We
dermatology departmentsdhas become increasingly impor- encourage the development of guidelines on metric
tant to train artificial intelligence for skin cancer screening.
reporting to facilitate the assessment of future
publications in this area.
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