Lucie Lévêque
email: lucie.leveque@univ-eiffel.fr

Philippa Young
email: philippa.young2@wales.nhs.uk

Hantao Liu

Studying the Gaze Patterns of Expert Radiologists in Screening Mammography: A Case Study with Breast Test Wales

Keywords: medical imaging, screening mammography, visual attention, eye-tracking, saliency

Eye-tracking technology has become a widely used means to understand how radiologists perceive and interpret medical images, providing useful information that can help improve diagnostic accuracy. However, existing eyetracking studies in medical imaging remain limited due to the small number of stimuli and/or of subjects involved, and the lack of quantitative metrics to fully reveal readers' gaze behaviour. In this paper, we present the conduct of a larger scale eyetracking study, where seven expert radiologists were asked to read 196 mammogram images. Furthermore, we carry out an analyse various gaze metrics including fixation duration, saccade amplitude, as well as gaze deployment, which quantify radiologists' gaze behaviour.

I. INTRODUCTION

According to the World Health Organisation (WHO), breast cancer is the most common invasive cancer for women, and the second main cause of cancer death after lung cancer [START_REF]International Agency for Research on Cancer[END_REF]. Screening mammography uses low-dose X-ray imaging to detect early stage breast cancers, and so with a view to make treatment more successful for patients. However, lesion detection as conducted by human observers is prone to errors due to the inherent limitations of the human visual system (HVS). In radiology, estimates suggest that there may be up to a thirty percent miss rate and an equally high false-positive rate in some areas of the field [START_REF] Lee | Cognitive and System Factors Contributing to Diagnostic Errors in Radiology[END_REF]. It is therefore critical to better understand medical image perception and interpretation, and to use such knowledge to develop useful solutions to minimise errors in routine clinical practice [START_REF] Krupinski | Visual Scanning Patterns of Radiologists Searching Mammograms[END_REF]- [START_REF] Agrawal | Saliency Based Mass Dectection from Screening Mammograms[END_REF].

The eye-tracking technology has been used in the literature to reveal how medical professionals read radiological images in order to improve their speed and accuracy in diagnostic reading, as well as to inform clinical radiology training programmes [START_REF] Lévêque | State-of-the-Art: Eye-Tracking Studies in Medical Imaging[END_REF]- [START_REF] Lévêque | A Statistical Evaluation of Eye-Tracking Data on Screening Mammography: Effects of Expertise and Experience on Image Reading[END_REF]. Advanced eye-tracking systems have indeed been developed to reliably track and record the eye movements of image readers. Through the analysis of eyetracking data, useful information is provided that can help reveal visual search patterns and identify potential problems in radiological accuracy. In the literature, many eye-tracking studies have been undertaken in the field of radiology.

For instance, Kundel et al. [START_REF] Kundel | Using Gaze-Tracking Data and Mixture Distribution Analysis to Support a Holistic Model for the Detection of Cancers on Mammograms[END_REF] collected eye-tracking data from experienced mammographers, mammography fellows, and radiology residents who were asked to search for cancer in mammograms. The analysis focused on eye positions and attempted to find the percentage of cancer locations that were fixated within the initial viewing. The results suggested that the initial detection occurs before visual scanning takes place, as most of the cancer locations were fixated within the very first second of viewing. Voisin et al. [START_REF] Voisin | Predicting Diagnostic Error in Radiology via Eye-Tracking and Image Analytics: Preliminary Investigation in Mammography[END_REF] investigated the relationship between radiologists' gaze behaviour and diagnostic performance in the detection of lesions in mammogram images. The study recorded the eye movements of six readers who were asked to evaluate the likelihood of malignancy of forty cases of mammographic masses. By analysing various quantitative metrics derived from the eyetracking data, such as the number of fixations, the fixation duration, and the fixation/saccade ratio, their study showed that these gaze behaviour characteristics were highly correlated with radiologists' diagnostic errors.

To improve the radiological reading practice, it is necessary to better understand how radiologists perform image search, detection and recognition tasks through the use of eye-tracking technology and gaze data analysis. In this paper, we present a new eye-tracking study in screening mammography with the following contributions.

• First, this study contains a large number of mammogram images with the aim to provide strong statistical evidence for the analysis of gaze behaviour. Note the existing studies often used a very limited number of stimuli.

• Second, rather than using the popular metrics, i.e., number of fixations and fixation duration to characterise the gaze behaviour, we propose to employ complementary information using the saccade amplitude.

• Third, we construct a gaze development representation, i.e., saliency map, to graphically quantify the gaze behaviour. This can also be used as a benchmark for the development of machine vision algorithms that can automatically predict radiologists' gaze patterns.

• Finally, the eye-tracking data will be made publicly available to the research community.

II. EYE-TRACKING EXPERIMENT

A. Stimuli

The set of stimuli used in our eye-tracking experiment is composed of 196 mammogram images of the mediolateral oblique (MLO) view, one of the standard views in mammographic imaging acquisition. The MLO view presents the most important projection as it allows depicting most breast tissues, e.g., the representation of the pectoral muscle on the MLO view is a key component in assessing the adequacy of the mammogram. The mammograms were extracted from 98 anonymised cases (note all cases were known to be lesion-free with a view to encourage the participants to consider all plausible clinical outputs) from the University Hospitals KU Leuven in Belgium. The original resolution of the mammograms was either 2080×2800 pixels or 2800×3518 pixels. All the images were linearly downscaled to 1080×1920 pixels to enable a controlled experiment. Fig. 1 illustrates examples of images used in our experiment.

B. Experimental Procedure

The eye-tracking experiment was conducted in a mammography reading room at Breast Test Wales, Cardiff, United Kingdom. The venue represented a controlled viewing environment with low surface reflectance and constant ambient light. The viewing distance was approximately sixty centimetres. A 19-inch LCD monitor was used to display the stimuli and was calibrated to the Digital Imaging and Communications in Medicine (DICOM): Greyscale Standard Display Function (GSDF) [START_REF] Samei | Assessment of Display Performance for Medical Imaging Systems[END_REF]- [START_REF]Digital Imaging and Communications in Medicine (DICOM) Part 14: Greyscale Standard Display Function[END_REF].

Firstly, the MLO view of the left breast was displayed for three seconds. It was then replaced by the MLO view of the right breast of the same patient, also displayed for three seconds. Once a participant had viewed both images, they would be prompted to answer the question "refer or not refer" by looking at one of these two options on the screen. This was meant to simulate the procedure of routine breast screening practice. Indeed, in routine, suspicious cases require further investigation. Fig. 2 illustrates the sequence of viewing.

The eye movements of the observers were recorded using a SensoMotoric Instrument (SMI) Red-m advanced eyetracker at a sampling rate of 250 Hz, using a nine-point calibration protocol.

C. Participants

Breast Test Wales (BTW) [12] is a Welsh organisation delivering the National Health Service Breast Screening Programme (NHSBSP). Every three years, women aged fifty to seventy years old are offered a screening mammography exam by the programme. There are three regional centres in Wales, i.e., Cardiff, Swansea, and Llandudno. Each centre has an important clinical team composed of various occupations, including radiologists, surgeons, breast physicians, pathologists, etc.

Seven expert radiologists from the Cardiff centre, having different degrees of experience in mammography (i.e., ranging from two to twenty-five years of experience), participated in the experiment. The radiologists were referred to as R1, R2, R3, R4, R5, R6, and R7, having, respectively, two, five, six, eight, ten, twenty, and twenty-five years of experience in mammogram reading.

III. EXPERIMENTAL RESULTS

Upon completion of the eye-tracking experiment, gaze information was extracted from the raw data using the SMI BeGaze Analysis software, including the number of fixations and saccades per image, their duration, and their coordinates.

A. Analysis of the Fixations

Fixations are the most common feature when analysing eye movements. A fixation has been defined by SMI's software using the dispersal and duration-based algorithm as established in [START_REF] Salvucci | Identifying Fixations and Saccades in Eye-Tracking Protocols[END_REF], with the minimum fixation threshold being set to 100 ms. The fixation duration has been widely used as a quantitative metric to analyse the viewing behaviour of human subjects.

In radiology, readers with different degrees of experience (e.g., experts and novices) can be characterised by their average gaze/fixation duration [START_REF] Krupinski | Visual Scanning Patterns of Radiologists Searching Mammograms[END_REF]. Fig. 3 shows the mean duration of fixations over all stimuli used in our experiment for each of the seven radiologists. In this figure, two clusters can be clearly observed, a first cluster including R1, R2, R3, R4 and R5, and a second cluster including R6 and R7. It can be also seen from Fig. 3 that "senior" radiologists, i.e., R6 and R7, having more than twenty years of experience in mammography, had shorter fixations than "junior" radiologists (i.e., ≤ 10 years of experience in mammography). The observed difference was further analysed using statistical hypothesis testing, i.e., an ANOVA (Analysis of Variance) was performed. The results of the statistical test show that there is a significant difference between the two groups of radiologists (i.e., p-value < 0.05). The results also show that there is a statistically significant difference (i.e., p-value < 0.05) between the two "senior" radiologists, i.e., R6 and R7. The radiologist who has twenty-five years of experience had the shortest fixation duration.

B. Analysis of the Saccades

Saccades can be defined as quick and simultaneous movements happening between fixations [START_REF] Meur | Saccadic Model of Eye Movements for Free-Viewing Condition[END_REF]. The saccade amplitude represents the Euclidian distance between two consecutive fixations, and is expressed in degree of visual angle [START_REF] Meur | Visual Attention Saccadic Models Learn to Emulate Gaze Patterns from Childhood to Adulthood[END_REF]. Fig. 4 illustrates the distribution of saccade amplitude averaged over all stimuli for the senior radiologists on the one hand, and for the junior radiologists on the other.

One can notice from Fig. 4 a peak of saccade amplitude between one and three degrees of visual angle for both groups. Contrary to the senior radiologists, the junior present very few saccades with an amplitude bigger than ten degrees of visual angle. Concretely, this means that, in general, radiologists show very short trajectories between two fixated points and, therefore, seem to focus their gaze in a relatively small region of interest.

C. Analysis of the Gaze Deployment

The collected eye-tracking data were also used to generate saliency maps, i.e., topographic representations indicating conspicuousness of scene location [START_REF] Privitera | Algorithms for Defining visual Regions-of-Interest: Comparison with Eye Fixations[END_REF]- [START_REF] Liu | Visual Attention in Objective Image Quality Assessment: Based on Eye-Tracking Data[END_REF]. To create a saliency map, each fixation location gives rise to a greyscale patch simulating the foveal vision of the human visual system. The activity of a given patch is modelled as a Gaussian distribution, where the standard deviation approximates the size of the human fovea [START_REF] Liu | Visual Attention in Objective Image Quality Assessment: Based on Eye-Tracking Data[END_REF]. A saliency map SM can thus be calculated as follows:

𝑆𝑀 ! (𝑘, 𝑙) = ) exp (- " #$% /x & -𝑘0 ' + /𝑦 # -𝑙0 ' σ ' ) (1)
where SMi(k,l) corresponds to the saliency map of the stimulus Ii (xj,yj) corresponds to the spatial coordinates of the j-th fixation (j = 1…T), with T being the total number of fixations over all observers; and σ corresponds to the standard deviation of the Gaussian (i.e., two degrees of visual angle). Fig. 5 illustrates the saliency maps (the brighter the regions, the higher the saliency) created from our eyetracking data for two sample patient cases, for the "junior" and "senior" radiologists, respectively. It can be observed from the figure that the "senior" radiologists tend to produce a more concentrated saliency map than the "junior" radiologists, whose gaze is more dispersed. This suggests that there is a strong agreement between "senior" radiologists.

Original stimulus "Senior" radiologists "Junior" radiologists Fig. 5. Illustration of the saliency maps constructed for two patient cases for the "junior" and "senior" radiologists. The brighter the regions, the higher the saliency.

IV. CONCLUSIONS

In this paper, we carried out a large-scale eye-tracking experiment with mammogram images. Seven expert radiologists from Breast Test Wales participated in the study. A statistical analysis of fixations and saccades, as well as a study of gaze deployment, revealed that there is a significant difference in gaze behaviour between radiologists working in the same environment depending on their degrees of experience. The findings can inform further study on the development of tailored image processing algorithms to optimise individual performance.

Fig. 1 .

 1 Fig. 1. Illustration of four sample stimuli from two patient cases (each case contains the MLO views of the left and right breasts) used in our eye-tracking experiment.

Fig. 2 .

 2 Fig. 2. Illustration of the experimental procedure: (a) MLO view of a left breast, (b) MLO view of the corresponding right breast, and (c) the question asked after viewing (a) and (b).

Fig. 3 .

 3 Fig.3. Illustration of the mean fixation duration, over all fixations recorded for all test stimuli, for each radiologist. The cluster circled by red colour corresponds to "junior" radiologists, whereas the cluster circled by blue colour corresponds to "senior" radiologists. Error bars indicate a 95% confidence interval.

Fig. 4 .

 4 Fig. 4. Illustration of the distribution of the saccade amplitude over all stimuli used in our experiment for: (a) the senior radiologists, and (b) the junior radiologists.


Gauthier Hulot

Jean-Michel Leger

Lasse B N Clausen

Florian Deconinck

Pierdavide Coïsson

Pierre Vigneron

Patrick Alken

Arnaud Chulliat

Christopher C Finlay

Alexander Grayver

J M Léger

A V Kuvshinov

N Olsen

E Thébault

T Jager

F Bertrand

T Häfner

NanoMagSat, a 16U nanosatellite constellation high

An optimal and scalable mission concept

Recovering the Magnetospheric Field (E2E simulations)

NanoMagSat does much better than Swarm, at recovering the field up to SH degree 3 with 1.5 h resolution thanks to the "criss-crossing" of 60° inclined orbits.

Combining NanoMagSat with Swarm would also be very beneficial, illustrating the potential complementarity of the two constellations.

NanoMagSat in summary

A nanosatellite constellation to investigate Earth's magnetic field and ionospheric environment in a unique way.

A mission ensuring continuity in the monitoring of Earth's magnetic field and ionospheric environment.

A mission ensuring continuity in the monitoring of Earth's magnetic field and ionospheric environment. A nanosatellite constellation to investigate Earth's magnetic field and ionospheric environment in a unique way.

A stepping stone for a space network of observatories with international scalability.

NanoMagSat in summary

NanoMagSat programmatic history and status

  Initiating a low-cost scalable collaborative constellation solution for very long-term observations (extending to space the Intermagnet network of magnetic observatories) An innovative orbital configuration A 3-year lifetime constellation composed of 3x16U Cubesats at 575 km initial altitude State of the art compact payloads • 2 dual-frequency GNSS • A multi-Needle Langmuir Probe (m-NLP) • A High Frequency Magnetometer (HFM) • A Miniaturized Absolute Magnetometer (MAM) with a set of two Star Cameras (STR) • 1 satellite at 60° inclination • 1 satellite at 60° inclination offset by 90°-RAAN • 1 satellite in near-polar orbit • Targeting recovery of fast planetary changes in core, ionospheric and magnetospheric fields, also improving recovery of crustal and oceanic signals • To investigate fast core dynamics, solar-terrestrial interactions, crust and deep Earth properties and possible signatures of climate change Taking advantage of the innovative constellation First family of objectives: Earth's magnetic field 4 Hulot et al., NanoMagSat, a 16U Nanosatellite Constellation High-Precision Magnetic Project, EGU21-14660, EGU, Online, 27/04/2021 Swarm recovered Swarm residuals Recovering fast core waves (E2E simulations) Core waves with 14 (top), 7 (middle) and 3.5 (bottom) months periods can be recovered by NanoMagSat and not by Swarm ., NanoMagSat, a 16U Nanosatellite Constellation High-Precision Magnetic Project, EGU21-14660, EGU, Online, 27/04/2021 Daily models can also be recovered by NanoMagSat and not by Swarm, thanks to the much better LT coverage Hulot et al., NanoMagSat, a 16U Nanosatellite Constellation High-Precision Magnetic Project, EGU21-14660, EGU, Online, 27/04/2021

•

  G N S S s ig n a ls G N S S si gn al s W hi st le r si gn al • With new ways of sensing the ionosphere below the satellites and monitoring in situ meter to km scale dynamics and energy input Taking advantage of an innovative compact payload • Targeting ionospheric plasma density dynamics • Combining standard GNSS techniques • To investigate Space weather phenomena that affect radio and GNSS signals, and improve science and operational ionospheric models 8 Second family of objectives: Ionospheric environment Hulot et al., NanoMagSat, a 16U Nanosatellite Constellation High-Precision Magnetic Project, EGU21-14660, EGU, Online, 27/04/2021 Monitoring the ionosphere below NanoMagSat • These propagate through the ionosphere with a dispersion that allows sensing the ionospheric plasma below the satellites 9 Take advantage of ELF Whistlers produced by lightning, detected by the MAM (scalar) and HFM (vector) magnetometers (2 kHz) • Providing information in regions not covered by ionosonde or GNSS techniques • Also allowing investigations of whistlers in general • Complementing local m-NLP measurements Hulot et al., NanoMagSat, a 16U Nanosatellite Constellation High-Precision Magnetic Project, EGU21-14660, EGU, Online, 27/04/2021 IRI model prediction on 22/02/14 Principle illustrated using Swarm B ASM (250 Hz magnetic scalar Burst mode, left) and 1 Hz Langmuir Probe data (below) on 22/02/2014 Investigating in-situ small scale plasma variability Moen, J., et al. (2008), doi:10.1029/2012GL051407 • First joint measurements of electron density and magnetic signals at high frequencies (2 kHz) • to access meter to km scale plasma variability and associated electrical currents • using a multi-Needle Langmuir Probe (m-NLP), only flown so far on sounding rockets and the NorSat-1 nano-satellite, and the High Frequency Magnetometer (HFM), which NorSat-1 fails to have ICI-2 sounding Rocket NorSat-1 nano-satellite 10 Hulot et al., NanoMagSat, a 16U Nanosatellite Constellation High-Precision Magnetic Project, EGU21-14660, EGU, Online, 27/04/2021

12

  Hulot et al., NanoMagSat, a 16U Nanosatellite Constellation High-Precision Magnetic Project, EGU21-14660, EGU, Online, 27/04/2021

•

  Currently: Consortium (Open Cosmos, CEA-Leti, IPGP, Univ. of Oslo) in dialogue phase with ESA • Second Quarter of 2021: ESA industrial Policy Committee (IPC) to approve • September 2021: KO of RRA -> NanoMagSat moving forward towards implementation -> Teams and institutions from over 16 countries expressed interest and support -> Science consolidation activities (expanding science team and scope of mission, consultation of user community, running more E2E simulations) to move forward in parallel to RRA. -> Do not hesitate to contact us: gh@ipgp.fr

Hulot et al., NanoMagSat, a 16U Nanosatellite Constellation High-Precision Magnetic Project, EGU21-14660, EGU, Online, 27/04/2021

Hulot et al., NanoMagSat, a 16U Nanosatellite Constellation High-Precision Magnetic Project, EGU21-14660, EGU, Online, 27/04/2021