Ways of measuring peripheral neuropathy severity and its association with retinopathy in patients with diabetes: A scoping review protocol

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A systematic review of the literature on the methods of measuring the severity of DPN and the association of the results of each method with diabetic retinopathy would contribute positively to the above developments. Methods The intended scoping review will be aligned, in combination, with the frameworks proposed by Arksey and O’Malley, the Preferred Reporting Items for Systematic Review and Meta-Analysis extension for Scoping Reviews (PRISMA-ScR), and the framework proposed by Peters et al. in 2015. The PubMed, Embase, Scopus, Web of Science, CINAHL, and ProQuest databases will be searched, as well as the ClinicalTrials.gov registry. The search strategy will include the following sequence of Boolean terms and operators: (“retinopathy” OR “eye disease” OR “eye disease” OR “maculopathy” OR “retinal” OR “macular”) AND “neuropathy” and for the title/abstract or abstract only “severity” AND (“diabetes” OR “diabetic”). The yielded publications will be screened according to criteria. This will be followed by data extraction, synthesis and presentation of results, discussion and conclusions. Discussion The different ways of measuring the severity of peripheral neuropathy identified in the previous literature will be discussed, as well as the association of neuropathy and/or its severity with retinopathy in patients with diabetes. The main aim of the discussion will be to elucidate the role of different methods of measuring the severity of DPN and its association with retinopathy. Registration The protocol has been registered on the international platform of registered systematic review and meta-analysis protocols (INPLASY). Inplasy protocol 2024100017. doi: 10.37766/inplasy2024.10.0017. 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F1000Research 2025, 14 :66 ( https://doi.org/10.12688/f1000research.160468.1 ) NOTE: If applicable, it is important to ensure the information in square brackets after the title is included in all citations of this article. Close Copy Citation Details Export Export Citation Sciwheel EndNote Ref. Manager Bibtex ProCite Sente EXPORT Select a format first Track Share ▬ ✚ Study Protocol Ways of measuring peripheral neuropathy severity and its association with retinopathy in patients with diabetes: A scoping review protocol [version 1; peer review: awaiting peer review] Aristomenis Kossioris https://orcid.org/0000-0002-1674-1984 1 , Stylianos Kandarakis 2 , Spyridon Doumazos 2 , Petros Petrou 2 Aristomenis Kossioris https://orcid.org/0000-0002-1674-1984 1 , Stylianos Kandarakis 2 , Spyridon Doumazos 2 , Petros Petrou 2 PUBLISHED 10 Jan 2025 Author details Author details 1 Ophthalmology Outpatient Clinics, General Hospital of Athens, “G. Gennimatas”, Athens, 11527, Greece 2 First Ophthalmology Clinic, Medical School, National and Kapodistrian University of Athens, Athens, 11527, Greece Aristomenis Kossioris Roles: Conceptualization, Investigation, Methodology, Project Administration, Writing – Original Draft Preparation, Writing – Review & Editing Stylianos Kandarakis Roles: Methodology, Resources, Validation, Writing – Original Draft Preparation, Writing – Review & Editing Spyridon Doumazos Roles: Resources, Visualization, Writing – Original Draft Preparation Petros Petrou Roles: Methodology, Supervision, Validation, Writing – Review & Editing OPEN PEER REVIEW REVIEWER STATUS AWAITING PEER REVIEW This article is included in the Eye Health gateway. This article is included in the HEAL1000 gateway. Abstract Introduction Recent advances in elucidating the pathogenetic mechanisms of diabetic peripheral neuropathy (DPN) and improvements in clinical trial design have reinvigorated the potential for agents developed in preclinical studies to be translated into new therapeutic agents, as well as highlighting the need for improved and effective means of measuring neuropathy in preclinical and clinical research. A systematic review of the literature on the methods of measuring the severity of DPN and the association of the results of each method with diabetic retinopathy would contribute positively to the above developments. Methods The intended scoping review will be aligned, in combination, with the frameworks proposed by Arksey and O’Malley, the Preferred Reporting Items for Systematic Review and Meta-Analysis extension for Scoping Reviews (PRISMA-ScR), and the framework proposed by Peters et al. in 2015. The PubMed, Embase, Scopus, Web of Science, CINAHL, and ProQuest databases will be searched, as well as the ClinicalTrials.gov registry. The search strategy will include the following sequence of Boolean terms and operators: (“retinopathy” OR “eye disease” OR “eye disease” OR “maculopathy” OR “retinal” OR “macular”) AND “neuropathy” and for the title/abstract or abstract only “severity” AND (“diabetes” OR “diabetic”). The yielded publications will be screened according to criteria. This will be followed by data extraction, synthesis and presentation of results, discussion and conclusions. Discussion The different ways of measuring the severity of peripheral neuropathy identified in the previous literature will be discussed, as well as the association of neuropathy and/or its severity with retinopathy in patients with diabetes. The main aim of the discussion will be to elucidate the role of different methods of measuring the severity of DPN and its association with retinopathy. Registration The protocol has been registered on the international platform of registered systematic review and meta-analysis protocols (INPLASY). Inplasy protocol 2024100017. doi: 10.37766/inplasy2024.10.0017. READ ALL READ LESS Keywords Peripheral neuropathy, Severity, Retinopathy, Patients with diabetes, Scoping review. Corresponding Author(s) Aristomenis Kossioris ( [email protected] ) Close Corresponding author: Aristomenis Kossioris Competing interests: No competing interests were disclosed. Grant information: The author(s) declared that no grants were involved in supporting this work. Copyright: © 2025 Kossioris A 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 work is properly cited. How to cite: Kossioris A, Kandarakis S, Doumazos S and Petrou P. Ways of measuring peripheral neuropathy severity and its association with retinopathy in patients with diabetes: A scoping review protocol [version 1; peer review: awaiting peer review] . F1000Research 2025, 14 :66 ( https://doi.org/10.12688/f1000research.160468.1 ) First published: 10 Jan 2025, 14 :66 ( https://doi.org/10.12688/f1000research.160468.1 ) Latest published: 10 Jan 2025, 14 :66 ( https://doi.org/10.12688/f1000research.160468.1 ) Introduction Diabetes mellitus, or simply “diabetes”, is a syndrome with a heterogeneous and multifactorial substrate. It is characterized by a disorder of carbohydrates, fat, and protein metabolism due to insulin deficiency. This deficiency may be complete, partial, or relative. Relative insulin deficiency is when, despite elevated levels in the blood, insulin is not sufficient to meet metabolic needs due to inhibition of its action in peripheral tissues (insulin resistance). The main expression of metabolic disturbance in diabetes is an increase in blood glucose levels. 1 Diabetes and its complications are now a major public health issue globally, with the number of people diagnosed increasing. 2 , 3 According to the International Diabetes Federation (IDF), the number of individuals diagnosed with diabetes in 2013 was estimated to be 381.3 million. Projections indicate that this figure will rise to 519.9 million by 2035, representing a 55% increase. 2 In patients diagnosed with diabetes, inadequate glycemic control can lead to microvascular complications, including peripheral diabetic neuropathy (DPN) (encompassing sensory, motor, and autonomic nerve fibers, and thus multiple organ systems) nephropathy, and retinopathy. 4 , 5 The microvascular alterations in retinal blood vessels resulting from diabetes constitute the disease entity called “diabetic retinopathy” (DR), which occurs worldwide in 30-40% of people with type 2 diabetes and is considered one of the main causes of partial vision loss and the leading cause of blindness in the working-age population (20-60 years) in developed countries (DR currently accounts for 4.8% of all cases of blindness). 6 , 7 Among people with diabetes, an overall prevalence analysis 8 showed that 35% had any type of diabetic retinopathy, 7% had proliferative retinopathy, 7% had macular edema, and 10% had sight-threatening retinopathy. Although all prevalences, which increased with duration of diabetes, poor glycemic control, and poor blood pressure control, were observed to be higher in patients with type 1 diabetes than in those with type 2 diabetes 9 the number of patients with type 2 diabetes far exceeds that of patients with type 1 diabetes. Therefore, patients with type 2 diabetes represent a larger proportion of patients with DR. 10 Nearly 50% of people with diabetes develop diabetic neuropathy, a disabling condition that can affect any part of the nervous system. The prevalence of diabetic neuropathy with pain can be as high as 15-30% but approaches 60% in some populations of persons with diabetes. It is a late finding in type 1 diabetes but can be found early in type 2 diabetes. 11 The motor and sensory nerves of the peripheral nervous system, since they are outside the central nervous system (CNS) and far from the protection of the blood-brain barrier, are particularly sensitive to harmful/toxic substances, such as substances resulting from diabetes and e.g. chemotherapeutic agents, as well as being a conduit to the CNS for the transport of viruses and neurotoxins. 12 Protein glycation and the polyol pathway are the main causes of peripheral neuropathy in people with diabetes. 11 The diagnosis of DPN is based on exclusion, where the presence or absence of symptoms and signs of nerve dysfunction, the duration of the disease, and the degree of glycaemic control are considered. 13 It should be highlighted that for patients with diabetes, it is not enough to determine whether they have peripheral neuropathy, the severity of neuropathy must also be determined. The more severe the DPN, the more severe the impairment of activities of daily living. 14 Often, there are differences between diagnostic criteria in clinical care and in clinical research. 5 In clinical practice, the diagnosis of DPN, and the determination of its severity, is made after careful clinical examination with the application of at least two neurological tests. 15 According to Boulton et al., 16 these two tests would include the Semmes-Weinstein 10g monofilament and a second test. The wide measurement range and excellent reliability make the biothesiometer a valuable, after the 10g monofilament, research and clinical tool for quantifying sensory loss. 17 , 18 In cases where the clinical features are atypical, electrophysiological tests (nerve conduction tests and electromyography -EMG-), as well as specialized neurological evaluation are necessary for the diagnosis of diabetic neuropathy. 5 Recent advances in elucidating the pathogenetic mechanisms of diabetic neuropathy and improvements in clinical trial design have reinvigorated the potential for agents developed in preclinical studies to be translated into new therapeutic agents, as well as highlighting the need for improved and effective means of measuring neuropathy in preclinical and clinical research. 19 The systematic investigation of the literature regarding the methods of measuring the severity of DPN and the association of the results of each method with diabetic retinopathy would contribute positively to the efforts to improve the methods/means of measuring neuropathy and predicting retinopathy, as well as, consequently, other microvascular complications of diabetes. A preliminary search for existing systematic or scoping reviews in the literature on the association between DPN and retinopathy (in Scopus, Web of Science, 20 and PubMed), as well as for registered in registers, as listed by Pieper and Rombey, 21 on such linking protocols of systematic or scoping reviews, in April 2024, was conducted. The search terms, in the databases, were for the records’ title (“retinopathy” OR “eye disease” OR “maculopathy” OR “retinal” OR “macular”) AND “neuropathy” and for the title/abstract or abstract only “severity” AND (“diabetes” OR “diabetic”), while in the registers the same terms in a single sequence, all or part of them together -in particular, consecutively the terms of the first Boolean sequence up to the first ‘AND’- if the register did not provide the possibility to search with a Boolean sequence, without distinction between search by title or by title/abstract or abstract only. The team of researchers who undertook the searches considered that the above sequence of terms and Boolean operators was sufficient/satisfactory quantitatively and qualitatively and that it prevented the generation of results noise. 22 Figure 1 shows the search/screening process, in the registers PROSPERO (Specific to systematic reviews), Research Registry, INPLASY, OSF Registries (Generic), and protocols.io, 21 of protocols (possibly) relevant to the association between diabetic peripheral neuropathy and diabetic retinopathy. A screening of the found protocols was performed by two researchers, AK and PP, to determine whether they were relevant to the proposed literature review. Table 1 presents the results of the above search/screening process. In particular, one protocol was found, by Wang et al., 23 whose although its topic “oversees” 24 the proposed literature review the protocol does not mention anything about including how to measure the severity of peripheral neuropathy, as well as mentioned only two databases (PubMed and Embase) to be searched for articles. Based on the above, it was concluded that is limited, if any, evidence regarding already existing scoping reviews on ways of measuring peripheral neuropathy severity and its association with retinopathy in patients with diabetes. Figure 1. Flowchart of the search process for existing protocols relevant to the proposed scoping review. Table 1. Protocols potentially relevant to the association of diabetic peripheral neuropathy and diabetic retinopathy found. Register Number of protocols found potentially relevant to the association between diabetic peripheral neuropathy and diabetic retinopathy Protocol(s) found INPLASY 1 Wang et al. 23 Methods Methodological framework The structure of the proposed scoping review will be aligned, in combination, with the frameworks proposed by Arksey and O’Malley, 25 , 26 the Preferred Reporting Items for Systematic Review and Meta-Analysis extension for Scoping Reviews (PRISMA-ScR), 26 , 27 as well as the framework proposed by Peters et al. 26 , 28 The scoping review framework proposed by Arksey and O’Malley 25 , 26 is an approach to organising literature/information that has been used by many (literature) researchers in recent years. The aim of this approach is to map the existing literature on a topic, as well as to identify key concepts and gaps in the original research data. Arksey and O’Malley’s 25 , 26 framework includes five main stages: • The first stage is to identify the question to be investigated in the literature • The second stage is the identification of relevant studies (in this step the search strategy is applied to identify the diverse literature sources) • The third stage concerns the selection/screening process of the studies by applying inclusion and exclusion criteria • The fourth stage is the data mapping of the studies, based on the data extracted from the studies, and • The fifth, and final stage which involves the classification, summarizing reporting of the results from the examination of the extracted data. The Preferred Reporting Items for Systematic Review and Meta-Analysis extension for Scoping Reviews (PRISMA-ScR) provides a standardized reporting framework that is thoroughly tailored to the specific objectives and methodology of scoping reviews. The development of PRISMA-ScR was driven by the need for clarity and transparency in reporting for scoping reviews. It includes a 22-point checklist that helps researchers/authors to present the results of their, secondary, research more comprehensively. These 22 points are also designed to facilitate the development of scoping review protocols. 26 , 27 This scoping review protocol has been registered on the international platform of registered systematic review and meta-analysis protocols (INPLASY). Inplasy protocol 2024100017. doi: 10.37766/inplasy2024.10.0017. Scoping review stages/sections The stages/sections of the intended scoping review will be as follows 25 – 28 : • Research question identification • Relevant literature identification • Studies selection • Data extraction • Summary, synthesis and reporting of results • Results discussion • Limitations, and • Conclusions Research question identification The research question identification for this scoping review was based on the PCC (population, concept, context) model 26 , 29 , 30 : “What evidence is there regarding ways of measuring the severity of peripheral neuropathy and its association with retinopathy in people with diabetes?”. In order to optimally address the above research question, it was divided into four main sub-objectives, which during the writing of the intended scoping review will be further analyzed/partitioned, based on the framework of Clark et al. 30 : • To map the ways of measuring the severity of peripheral neuropathy and its association with retinopathy in patients with diabetes in the context of the literature • To determine the types of peripheral neuropathy severity assessment methods (subjective type - e.g. VASs for neuropathic pain - vs objective type - e.g. clinical/physical examinations etc.) • To identify the type of nerve fibers, if the test is of an objective type, which is the aim of each way of measuring the severity of neuropathy, and • To describe of the link between the severity of peripheral neuropathy and retinopathy, if the latter is negotiated in the relevant article/book chapter. Relevant literature identification The selection of databases or registries for the intended scoping review, was made based on the recommendations of Gusenbauer and Haddaway, 31 as well as Bramer et al. 32 Given the required search accuracy for term-based searches, we rejected Google Scholar. Also, given the availability of subscription databases, we did not limit the search to open access options only. The search systems selected for the proposed scoping review were 31 : • PubMed • Embase • Scopus • Web of Science • CINAHL, and • ProQuest. ClinicalTrials.gov registry will also be searched. The search strategy will include the following Boolean sequence with the following terms and operators: (“retinopathy” OR “eye disease” OR “eye disease” OR “maculopathy” OR “retinal” OR “macular”) AND “neuropathy” and for the title/abstract or abstract only “severity” AND (“diabetes” OR “diabetic”). Whether the terms with the operators are searched for the title/abstract or only for the abstract will depend on the search capabilities provided by the database or the clinical trials registry. Regarding the Embase database, since there was no active subscription from a university in Greece, the country where the proposed scoping review will be conducted, for the academic year 2023-2024, the help of scientific staff from the Rutgers University, New Jersey, USA was requested and accepted (see acknowledgments section). Studies selection Eligibility criteria The proposed scoping review will be guided by the “population, concept, context” framework of Peters et al. 26 , 29 , 30 The “population, concept, context” framework is presented in Table 2 , which is a modified table based on the publication of Clark et al. 30 Table 2. “Population, concept, context” framework and objectives of the intended scoping review. 30 Criteria Characteristics Population • Patients with type 1 or type 2 diabetes, of any age • Diagnosis of peripheral neuropathy, as well as retinopathy of any type Concept Studies with various ways of measuring the severity of peripheral neuropathy which they link/associate with retinopathy Context Samples of patients from all possible settings (community, primary health care, secondary health care, tertiary health care) The population will include patients with type 1 or 2 diabetes, without age restriction, with diagnosed peripheral neuropathy, as well as with diagnosed retinopathy of any type. Inclusion criteria Studies or book chapters that will be original studies of any research design, published in the English language at any date. To be eligible, the full text of the publication must also be directly accessible to the authors through university subscriptions. Exclusion criteria Articles or book chapters will be excluded if: • Are not original studies • They are review publications • They are not written in English, and • They are not readily available from the library systems of the universities from which the reviewers come. Screening process To achieve the screening of publications by the two reviewers (AK and PP), first the titles/abstracts of the records resulting from the databases/registries will be checked to exclude duplicate records, as well as records that appear multiple times in the results of the databases/registries. The titles/abstracts of the publications will then be checked to exclude those that are reviews. Then, after checking also the titles/abstracts, those records that are publications in a language other than English will be excluded and, finally, the remaining records that will be left will be checked for their full text to determine whether they are relevant to the topic/question of the proposed scoping review. If there is disagreement during the screening process about whether to include a publication, a third reviewer will be consulted, whose name will be mentioned in the ScR publication. The screening process will be detailed in the article of the proposed scoping review, as well as an illustration will be provided that will capture the process with a flowchart. Data extraction • From the yielded articles based on the search strategy and screening process mentioned in the “Relevant literature identification” section, the following data will be extracted: • The name(s) of the authors • The publication’s country of origin (based on the first author) • The research design • The quality of the sample (the study’s subjects) • The peripheral neuropathy assessment method • The type of nerve fibers targeted by the assessment method • The way the severity of peripheral neuropathy is classified (if mentioned in the publication) • The way of associating with retinopathy, and • The way of classifying the retinopathy severity (if reported in the publication). The identification of the nerve fibers targeted by each method of assessing the severity of peripheral neuropathy will be done according to Jin et al. 19 and Davalos et al. 33 The extracted data will be passed to an.xlsx spreadsheet. Summary, synthesis and reporting of results The main results of the proposed scoping review will be reported narratively, as well as presented in aggregate based on the data for extraction listed above, in a table. Discussion of the results After reporting the results narratively and in a table, a discussion of the results will follow. The different ways of measuring the severity of peripheral neuropathy identified, based on previous literature, will be discussed, as well as the association of neuropathy and/or its severity with retinopathy, in patients with diabetes. The main objective of the discussion will be to elucidate the role of different ways of measuring the severity of peripheral neuropathy with its association with retinopathy. Limitations The proposed scoping review aims to explore/clarify the role of different ways of measuring the severity of peripheral neuropathy with its association with retinopathy. This objective is relatively broad and not somewhat specific. This fact may lead to results that will be difficult to draw clear conclusions. Conclusions Conclusions will be drawn in line with the objective(s) of the proposed scoping review and will be based on the results. Following the conclusions, recommendations for future research will be made, which will include suggestions for conducting systematic reviews, with more specific questions to be explored, 28 with or without meta-analysis, based on the knowledge gaps identified from the results. 27 , 28 Authors’ contributions Aristomenis Kossioris wrote the introduction section of the topic under examination, part of the methodology, as well as did a preliminary search of databases and protocol registers for existing publications on the topic under examination. Stylianos Kandarakis wrote part of the methods section, helped sorting the protocols found, wrote part of the discussion, and made editorial and grammatical corrections. Spyridon Doumazos helped sorting the protocols found, wrote the limitations section, as well as made editorial and grammatical corrections. Petros Petrou contributed to the search strategy planning, wrote part of the methodology, as well as had overall supervision of the project. Ethics and consent Ethical approval and consent were not required. Data availability No data are associated with this article. Extended data Zenodo: So far selected for the scoping review articles/draft file with the process of sorting the articles from the selected search systems/Completed PRISMA ScR fillable checklist. Doi: 10.5281/zenodo.14599226 https://zenodo.org/records/14599226 . 34 This project contains the following extended data: • ScR extracted data_draft 1.xlsx Data is available under the terms of the CC0. Reporting guidelines Zenodo: PRISMA ScR checklist and flowchart for “So far selected for the scoping review articles/draft file with the process of sorting the articles from the selected search systems/Completed PRISMA ScR fillable checklist”. Doi: 10.5281/zenodo.14599226 . 34 Data are available under the terms of the Creative Commons Zero (CC0). Acknowledgments Granted that there was not any active subscription to the Embase database from the universities in Greece, the country that the proposed scoping review will be conducted/completed, during the planning/writing of the present protocol, the help of Yingting Zhang, MLS, AHIP-D, Robert Wood Johnson Library of the Health Sciences, Rutgers University, New Jersey, USA, was requested and accepted. Ms. Yingting Zhang did the search on the Embase database. References 1. Hellenic Diabetes Association: Diabetic patient management guidelines. Athens: Hellenic Diabetes Association; 2019. 2. 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Wang W, Wu Y: Prediction models for diabetic retinopathy development in type 2 diabetes mellitus patients: a systematic review. Inplasy Protocol. 2022; 30089. Publisher Full Text 24. Squire L, Berg D, Bloom FE, et al. : Fundamental neuroscience. 4th ed.San Diego: Academic Press; 2012. 25. Arksey H, O’Malley L: Scoping studies: towards a methodological framework. Int. J. Soc. Res. Methodol. 2005; 8 (1): 19–32. Publisher Full Text 26. Westphaln KK, Regoeczi W, Masotya M, et al. : From Arksey and O’Malley and beyond: customizations to enhance a team-based, mixed approach to scoping review methodology. MethodsX. 2021; 8 : 101375. Publisher Full Text 27. Tricco AC, Lillie E, Zarin W, et al. : PRISMA extension for scoping reviews (PRISMA-ScR): checklist and explanation. Ann. Intern. Med. 2018; 169 (7): 467–473. PubMed Abstract | Publisher Full Text 28. Peters MD, Godfrey CM, Khalil H, et al. : Guidance for conducting systematic scoping reviews. JBI Evid. Implement. 2015; 13 (3): 141–146. 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Davalos L, Stino A, Smith AG: Diagnostic techniques for diabetic peripheral neuropathy.Boulton AJM, editor. Diabetic neuropathy: advances in pathophysiology and clinical management. Cham: Springer; 2023; pp. 93–112. 34. Kossioris A: So Far Selected for the Scoping Review Articles/draft File with the Process of Sorting the Articles from the Selected Search Systems/completed PRISMA Scr Fillable Checklist. Zenodo. 2025. Publisher Full Text Comments on this article Comments (0) Version 1 VERSION 1 PUBLISHED 10 Jan 2025 ADD YOUR COMMENT Comment Author details Author details 1 Ophthalmology Outpatient Clinics, General Hospital of Athens, “G. Gennimatas”, Athens, 11527, Greece 2 First Ophthalmology Clinic, Medical School, National and Kapodistrian University of Athens, Athens, 11527, Greece Aristomenis Kossioris Roles: Conceptualization, Investigation, Methodology, Project Administration, Writing – Original Draft Preparation, Writing – Review & Editing Stylianos Kandarakis Roles: Methodology, Resources, Validation, Writing – Original Draft Preparation, Writing – Review & Editing Spyridon Doumazos Roles: Resources, Visualization, Writing – Original Draft Preparation Petros Petrou Roles: Methodology, Supervision, Validation, Writing – Review & Editing Competing interests No competing interests were disclosed. Grant information The author(s) declared that no grants were involved in supporting this work. Article Versions (1) version 1 Published: 10 Jan 2025, 14:66 https://doi.org/10.12688/f1000research.160468.1 Copyright © 2025 Kossioris A et al . 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