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      Evaluation of photography using head-mounted display technology (ICAPS) for district Trachoma surveys

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          Abstract

          Background

          As the prevalence of trachoma declines worldwide, it is becoming increasingly expensive and challenging to standardize graders in the field for surveys to document elimination. Photography of the tarsal conjunctiva and remote interpretation may help alleviate these challenges. The purpose of this study was to develop, and field test an Image Capture and Processing System (ICAPS) to acquire hands-free images of the tarsal conjunctiva for upload to a virtual reading center for remote grading.

          Methodology/Principal findings

          This observational study was conducted during a district-level prevalence survey for trachomatous inflammation—follicular (TF) in Chamwino, Tanzania. The ICAPS was developed using a Samsung Galaxy S8 smartphone, a Samsung Gear VR headset, a foot pedal trigger and customized software allowing for hands-free photography. After a one-day training course, three trachoma graders used the ICAPS to collect images from 1305 children ages 1–9 years, which were expert-graded remotely for comparison with field grades. In our experience, the ICAPS was successful at scanning and assigning barcodes to images, focusing on the everted eyelid with adequate examiner hand visualization, and capturing images with sufficient detail to grade TF. The percentage of children with TF by photos and by field grade was 5%. Agreement between grading of the images compared to the field grades at the child level was kappa = 0.53 (95%CI = 0.40–0.66). There were ungradable images for at least one eye in 199 children (9.1%), with more occurring in children ages 1–3 (18.5%) than older children ages 4–9 (4.2%) (χ 2 = 145.3, p<0.001).

          Conclusions/Significance

          The prototype ICAPS device was robust, able to image 1305 children in a district level survey and transmit images from rural Tanzania to an online grading platform. More work is needed to improve the percentage of ungradable images and to better understand the causes of disagreement between field and photo grading.

          Author summary

          Trachoma is the leading infectious cause of blindness worldwide, caused by the bacterium Chlamydia trachomatis. Programs targeting trachoma elimination in endemic regions largely rely on periodic prevalence surveys to monitor progress, but training field graders requires active cases, which is becoming challenging as prevalence declines. Photography of the tarsal conjunctiva with remote interpretation via telemedicine may serve as a more auditable, effective, and cost-efficient method for surveys. We developed and evaluated the Image Capture and Processing System (ICAPS), a smartphone-based, hands-free, head-mounted camera system (Samsung Galaxy S8 with custom app, Samsung Gear VR headset, and a Bluetooth-linked foot pedal trigger). The ICAPS was easy to use in challenging field conditions, was able to upload images from Tanzania and link images to field data. The percentage of TF was 5% by both field grade and photo grade, with agreement kappa = 0.53. Additional field training and enhanced certification of photographers may help reduce the proportion of ungradable images; further research on reasons for mismatch of grades between field and photo is needed.

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          Most cited references11

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          Global causes of blindness and distance vision impairment 1990-2020: a systematic review and meta-analysis.

          Contemporary data for causes of vision impairment and blindness form an important basis of recommendations in public health policies. Refreshment of the Global Vision Database with recently published data sources permitted modelling of cause of vision loss data from 1990 to 2015, further disaggregation by cause, and forecasts to 2020.
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            The Global Trachoma Mapping Project: Methodology of a 34-Country Population-Based Study

            ABSTRACT Purpose: To complete the baseline trachoma map worldwide by conducting population-based surveys in an estimated 1238 suspected endemic districts of 34 countries. Methods: A series of national and sub-national projects owned, managed and staffed by ministries of health, conduct house-to-house cluster random sample surveys in evaluation units, which generally correspond to “health district” size: populations of 100,000–250,000 people. In each evaluation unit, we invite all residents aged 1 year and older from h households in each of c clusters to be examined for clinical signs of trachoma, where h is the number of households that can be seen by 1 team in 1 day, and the product h × c is calculated to facilitate recruitment of 1019 children aged 1–9 years. In addition to individual-level demographic and clinical data, household-level water, sanitation and hygiene data are entered into the purpose-built LINKS application on Android smartphones, transmitted to the Cloud, and cleaned, analyzed and ministry-of-health-approved via a secure web-based portal. The main outcome measures are the evaluation unit-level prevalence of follicular trachoma in children aged 1–9 years, prevalence of trachomatous trichiasis in adults aged 15 + years, percentage of households using safe methods for disposal of human feces, and percentage of households with proximate access to water for personal hygiene purposes. Results: In the first year of fieldwork, 347 field teams commenced work in 21 projects in 7 countries. Conclusion: With an approach that is innovative in design and scale, we aim to complete baseline mapping of trachoma throughout the world in 2015.
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              Application of smartphone cameras for detecting clinically active trachoma

              The WHO is committed to eliminating trachoma as a public health concern by 2020.1 Since decisions for mass treatment are determined by the prevalence of clinical trachoma in a community, efficient and accurate methods for monitoring clinical activity remain a priority.2 However, reliability of clinical examination is poor and disagreement between graders is common.3 Photography of the conjunctiva could reduce variability and improve accuracy of trachoma surveillance. Currently, research studies use single-lens reflex (SLR) cameras to validate field grading.4 Yet, SLR cameras are expensive and require substantial field training to operate, and thus few trachoma programmes have adopted this technology. A simpler, more affordable camera may increase uptake of this diagnostic technique. In view of growing applications of mobile technology,5 we examined the use of smartphone imaging in trachoma. During a recent programme, Partnership for the Rapid Elimination of Trachoma (PRET study) visit in Niger, we performed the clinical examination, SLR, and smartphone photography of the everted right upper tarsal conjunctiva in 61 study participants.4 Study participants, aged 6 months to 5 years, were from four villages, each of which had received a mass azithromycin distribution one year prior. Clinical examinations were performed by a PRET-certified examiner with 2.5× magnifying loupe and a flashlight. Examiners used the simplified WHO grading scheme, which classifies follicular trachoma (TF) as the presence of at least five follicles ≥0.5 mm in diameter on the upper tarsal conjunctiva, and trachomatous inflammatory-intense (TI) as papillary hypertrophy and inflammatory thickening obscuring over half of the deep tarsal vessels.6 SLR photographs were taken by a PRET-certified photographer with a handheld Nikon D-40, with a 105 mm f/2.8D AF Macro Nikkor Autofocus lens, using manual settings with the flash engaged. Smartphone images, captured immediately after the SLR photo, were taken with an iPhone four camera using autofocus and without flash in order to minimise glare from the phone's screen. Photos were systematically cropped and resized to match the approximate size of the conjunctiva in the SLR images. Three PRET-certified trachoma graders reviewed the photographs independently and in random order within one sitting and without discussion. Latent Class Analysis was performed to assess test performance with both cameras and field grades given the absence of a gold standard. Sensitivities and specificities for the latent gold standard were obtained for (i) SLR photography; (ii) smartphone photography and; (iii) clinical field grades. For clinical activity, field grades had similar sensitivity to SLR photos, but higher specificity than both cameras. SLR photos were moderately more sensitive and more specific than the iPhone photos (table 1). While iPhone photos were the least sensitive for TF, compared with both the SLR photos and field grades, iPhone photos were the most sensitive for TI. However, iPhone photos were moderately less specific than both field grades and SLR photos. Table 1 Sensitivity, specificity and inter-grader reliability (κ) for trachoma grading (N=61) Active trachoma (TF and/or TI) TF TI Grade assigned N (%)  iPhone 25 (41.0%) 11 (18.0%) 16 (26.2%)  SLR 24 (39.3%) 20 (32.8%) 11 (18.0%)  Field grade 23 (37.7%) 20 (32.8%) 11 (18.0%) Sensitivity  iPhone 78% (63.9–95.3) 41% (26.1–94.4) 91% (82.4–99.4)  SLR 81% (69.0–95.4) 88% (68.0–94.3) 76% (50.5–94.4)  Field grade 81% (66.7–95.6) 88% (68.0–95.0) 76% (53.7–93.8) Specificity  iPhone 91% (80.8–100.0) 91% (83.1–100.0) 91% (83.1–100.0)  SLR 97% (89.2–100.0) 98% (88.2–100.0) 96% (90.8–99.4)  Field grade 100% (97.5–100.0) 98% (87.5–100.0) 96% (90.7–99.3) Inter-grader reliability  iPhone 0.86 (0.80–0.90) 0.63 (0.57–0.73) 0.83 (0.73–0.86)  SLR 0.78 (0.63–0.83) 0.76 (0.71–0.81) 0.65 (0.55–0.71) SLR, single lens reflex; TF, follicular trachoma; TI, trachomatous inflammatory-intense. The iPhone demonstrated moderate inter-grader reliability (table 1). iPhone inter-grader reliability was higher than SLR for active and TI grades. Inter-grader reliability was the highest for clinically active trachoma with the iPhone photographs. iPhones were less reliable for TF than SLR photos, but more reliable for TI. The advantages of photographic examinations include reproducible grading by centres of expertise, auditability, and increased accessibility to official graders. We were unable to demonstrate that the iPhone could be used in lieu of SLR photography, which has been considered costly. However, updates to the camera with newer smartphone models, an external lens attachment, and lighting adjustments could soon make smartphones a viable alternative to SLR photography. The ability to both share images through cellular data and capture relevant information electronically could dramatically facilitate accurate and efficient methods for diagnosis and treatment of blinding trachoma.
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                Author and article information

                Contributors
                Role: Formal analysisRole: InvestigationRole: Project administrationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: SoftwareRole: Writing – original draftRole: Writing – review & editing
                Role: ValidationRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: SoftwareRole: Writing – review & editing
                Role: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                8 November 2021
                November 2021
                : 15
                : 11
                : e0009928
                Affiliations
                [1 ] Dana Center for Preventive Ophthalmology, Wilmer Eye Institute, Baltimore, Maryland, United States of America
                [2 ] Larner College of Medicine, University of Vermont, Burlington, Vermont, United States of America
                [3 ] Kongwa Trachoma Project, Kongwa, Tanzania
                [4 ] Ministry of Health–Community Development, Gender, Elderly and Children, Dodoma, Tanzania
                [5 ] RTI International, Washington DC, United States of America
                University of Buea, CAMEROON
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0001-6106-3177
                https://orcid.org/0000-0001-7847-3914
                https://orcid.org/0000-0001-7663-6759
                https://orcid.org/0000-0002-1030-2884
                Article
                PNTD-D-21-00629
                10.1371/journal.pntd.0009928
                8601615
                34748543
                4be8bdcd-8b72-41e0-b400-996be4d30bdb
                © 2021 Naufal et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 5 May 2021
                : 19 October 2021
                Page count
                Figures: 4, Tables: 4, Pages: 15
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000200, United States Agency for International Development;
                Award ID: 7200AA18CA00040
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000057, National Institute of General Medical Sciences;
                Award ID: P20GM103644
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000910, Conrad N. Hilton Foundation;
                Award ID: 17332
                Award Recipient :
                Funded by: Seeing is Believing Foundation
                Award Recipient :
                Grants provided by the United States Agency for International Development (7200AA18CA00040), National Institute of General Medical Sciences (P20GM103644), The Conrad N. Hilton Foundation (17332) and the Seeing is Believing Foundation. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Anatomy
                Head
                Eyes
                Medicine and Health Sciences
                Anatomy
                Head
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                Biology and Life Sciences
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                Eyes
                Medicine and Health Sciences
                Anatomy
                Ocular System
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                Medicine and Health Sciences
                Medical Conditions
                Infectious Diseases
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                Trachoma
                Medicine and Health Sciences
                Medical Conditions
                Eye Diseases
                Trachoma
                Medicine and Health Sciences
                Ophthalmology
                Eye Diseases
                Trachoma
                Medicine and Health Sciences
                Medical Conditions
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                Trachoma
                Biology and Life Sciences
                Anatomy
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                Engineering and Technology
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                Research and Analysis Methods
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                Custom metadata
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                2021-11-18
                All relevant data are within the manuscript and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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