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1 Editorial ISSN (Print) / ISSN: (Online) Urogenit Tract Infect 2019;14(1): Korean Translation of the GRADE Series Published in the BMJ, GRADE: An Emerging Consensus on Rating Quality of Evidence and Strength of Recommendations (A Secondary Publication) Translated by: Do Kyung Kim, Eu Chang Hwang 1, Ho Won Kang 2, Ja Yoon Ku 3, Hyun Jin Jung 4, Hong Wook Kim 5, Jae Hung Jung 6,7 ; Guideline Development Committee in the Korean Association of Urogenital Tract Infection and Inflammation Department of Urology, Soonchunhyang University Seoul Hospital, Soonchunhyang University College of Medicine, Seoul, 1 Department of Urology, Chonnam National University Medical School, Gwangju, 2 Department of Urology, Chungbuk National University College of Medicine, Cheongju, 3 Department of Urology, Pusan National University Hospital, Busan, 4 Department of Urology, Daegu Catholic University School of Medicine, Daegu, 5 Department of Urology, College of Medicine, Konyang University, Daejeon, 6 Department of Urology, 7 Institute of Evidence Based Medicine, Yonsei University Wonju College of Medicine, Wonju, Korea Clinical practice guidelines are statements that include recommendations intended to optimize patient care based on a systematic review of the evidence assessing the benefits and harm of alternative care options. Guideline developers should use an explicit, judicious, and transparent methodology to make trustworthy guidelines. Although there are a variety of frameworks that can help translate enormous medical knowledge into recommendations, the most widely adopted tool for grading the quality of evidence and making recommendations is GRADE (Grading of Recommendations, Assessment, Development and Evaluations). This article is the first translation of a series published in the BMJ with regard to the GRADE Approach for Evidence Based Clinical Practice Guideline Development to provide informative knowledge for moving from evidence to recommendations to Korean guideline developers. Copyright 2019, Korean Association of Urogenital Tract Infection and Inflammation. All rights reserved. This is an open access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Received: 1 April, 2019 Revised: 9 April, 2019 Accepted: 9 April, 2019 Correspondence to: Jae Hung Jung Department of Urology, Yonsei University Wonju College of Medicine, 20 Ilsan-ro, Wonju 26426, Korea Tel: , Fax: geneuro95@yonsei.ac.kr This article is the secondary publication (complete translation in Korean) of the aritlce originally published in the BMJ in English (GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. 2008;336:924-6). The Editorin-Chief of Urogenital Tract Infection decided to publish this secondary publication for the reader's sake, and it was approved by BMJ. BMJ Publishing Group take no responsibility for the accuracy of the translation from the published English language original and are not liable for any errors that may occur. 진료지침의근거수준과권고등급을평가하는방법은일관성이부족한것이현실입니다. 이논문에서는전세계적으로점차사용이확대되고있는 GRADE 방법론에대해논의하고자합니다. 2006년부터 BMJ ( 는 Instructions to Authors 에임상진료지침을투고할때증거의등급을평가하기위해 GRADE 방법론을이용하는것이바람직하다고권고하였습니다. 이논문은진료지침개발에있어근거수준및권고등급평가를위한통일된방법론의필요성및임상적중요성에대하여 GRADE 방법론을중심으로설명하고자합니다. GRADE 방법론은여러다른방법론에비하여장점을가지고있습니다 (Table 1 and Appendix 1) [1,2]. " 근거수준 " 이란무엇이며왜중요한가? 환자진료의최적화를위해서임상의사와환자는치료의원하는효과 (advantage) 와원하지않는효과 (disadvantage) 를반드시가늠해보아야합니다. 치료의원하는 / 원하지않는효과의추정치 (best estimate of expected advantage and disadvantage) 뿐만아니라추정치에대한확신도 ( 근거수준 ) 는의사결정에영향을미치게됩니다. 다시말하면중재효과의추정치크기 (estimate of the magnitude of intervention) 의임상적유용성은그추정치에대한우리의근거수준에달려있습니다. 보건의료관련전문가및전문학회등은근거수준을고려하지않는우를범하였습니다 [3]. 예를들면, 과거폐경기여성의 28

2 Do Kyung Kim, et al. Korean Translation of GRADE Series 29 Table 1. Advantages of GRADE over other systems ㆍDeveloped by a widely representative group of international guideline developers ㆍClear separation between the quality of evidence and strength of recommendations ㆍExplicit evaluation of the importance of outcomes of alternative management strategies ㆍExplicit, comprehensive criteria for downgrading and upgrading the quality of evidence ratings ㆍTransparent process of moving from evidence to recommendations ㆍExplicit acknowledgment of values and preferences ㆍClear, pragmatic interpretation of strong versus weak recommendations for clinicians, patients, and policy makers ㆍUseful for systematic reviews and health technology assessments, as well as guidelines See also Appendix 1 (complete translate in Korean). 심혈관계위험을감소시킬수있다는믿음으로인해호르몬대체요법이권고되어왔습니다 [4]. 그러나, 이는일관되지않은결과를보고한관찰연구 (observational studies) 에기반한결과로이에대한근거수준은 매우낮음 (very low quality of evidence) 임이간과되었습니다 [5]. 결론적으로, 무작위대조임상연구 (randomized controlled trials) 에서호르몬대체요법이심혈관계위험을감소시키지못하고증가시킬수도있다는것이밝혀졌습니다 [6,7]. 또다른예로, 미국식품의약국 (US Food and Drug Administration) 은돌연사 (sudden death) 를초래할수있는무증상의심실성부정맥 (asymptomatic ventricular arrhythmia) 치료제인 encainide 와 flecainide 를허가하였습니다. 그러나, 이결정역시그약물들의효과에대한낮은근거수준 (low quality of evidence) 을고려하지않았으며마찬가지로, 무작위대조군연구에서두약물이급사의위험을증가시키는것으로보고되었습니다 [8]. 만약, 낮은근거수준에대한주의가있었다면수많은생명을구할수있었을것입니다. 높은질의근거수준을간과하는것역시같은문제를야기할수있습니다. 엄격히수행된무작위대조군연구들은혈전용해요법이심근경색으로인한사망률을감소시킬수있음을보고하였으나과거임상진료지침은 10년이상이를반영하지못하였습니다 [9]. 이러한실수를반복하지않기위하여근거수준에대하여이해하는것이도움이될것입니다. 진료지침개발자들은임상의사들에게어떻게근거수준을알려야하는가? GRADE 방법론은근거수준을 4가지등급 ( 높음 [high], 중등도 [moderate], 낮음 [low], 매우낮음 [very low]) 으로범주화함으로써임상의사가근거수준을명확히이해할수있도록도울수있을것입니다. 그러나근거수준은이렇게이분법적으로 나눌수없는경우도있을수있습니다. 하지만이러한근거수준분류의장점은단순함 (simplicity), 투명성 (transparency), 선명성 (vividness) 이라고할수있겠습니다. " 권고등급 " 은무엇이며왜중요한가? 진료지침은적은비용 (cost) 및환자불편감 (inconvenience) 과더불어중재의원하는효과 (benefits) 와원하지않는효과 (side effects) 의차이를증명한무작위대조군연구에기반할수있을것입니다. 예를들어, 천식이악화된환자에서단기간의경구용스테로이드의유용성이이런경우에해당할것입니다. 임상의사는이러한치료를아무런망설임없이시행할수있을것입니다. 또는, 진료지침은관찰연구에기반할수도있으며상당한중재부작용 (harms) 또는비용을수반할수도있습니다. 인공심장판막을가진임산부에게항혈전치료를결정하기위해서판막혈전증의발생감소정도와환자의불편감, 치료비용및태아기형발생위험을모두고려하여심사숙고하여야합니다. 임상의사는환자가자신의가치와선호도에따라치료의효과와부작용에대해신중하게가늠할수있도록도와야합니다. 그러므로진료지침은 1) 근거수준 높음 및원하는효과와원하지않는효과의차이가큰경우, 2) 원하는효과와원하지않는효과의차이가우열을가리기힘들거나불확실한경우인지를명시해야합니다. 간단하고투명한권고등급은이를효과적으로전달할수있을것입니다. GRADE 방법론은권고등급을 강한권고 (strong recommendation) 또는 약한권고 (weak recommendation) 로나누고있으나근거수준과마찬가지로권고등급역시이분법적으로나누기어려운점이있을수있습니다. 그러나명확한권고등급은진료지침에있어단점보다는장점이클것으로생각합니다. 우수한등급시스템에필수적인것은무엇인가? 항상근거수준과권고등급이일치하는것은아닙니다. 높은근거수준 (high quality of evidence) 이반드시강한권고를의미하는것은아니며, 강한권고역시낮은근거수준에기반할수있습니다. 예를들어명백한유발요인이없이심부정맥혈전증을처음으로경험한환자는항응고치료시행 1개월후에와파린의장기복용여부를결정해야합니다. 무작위대조군연구에따르면장기적인와파린복용은혈전증의재발위험을줄이지만출혈의위험과환자의불편이증가한다는단점이있습니다. 환자들은스스로의가치와선호도에따라치료를결정할수

3 30 Do Kyung Kim, et al. Korean Translation of GRADE Series 있기때문에, 임상진료지침개발자는높은근거수준에도불구하고 ( 무작위대조군연구에기반한 ) 약한권고를내릴수도있을것입니다. 전문가의견 (expert opinion) 을근거 (evidence) 로서분류하는것역시혼란을야기합니다. 증거의질이높거나낮은것에상관없이모든근거의해석에는판단 (judgement) 이필요합니다. 전문가의견은사례보고및적절하게수행되지않은관찰연구와마찬가지로매우낮은근거수준으로평가되어야할것입니다. 근거수준과권고등급의단순한분류시스템 (grading system) 은환자, 임상의사및정책결정자에게사용을용이하게만들수있으며근거수준및권고등급의상세하고명쾌한기준은진료지침을보다투명하게만들것입니다 [2]. 지금까지많은분류시스템이사용되어왔으나시스템의복잡성으로인해이를임상진료현장에사용하기에는많은제약이있습니다 [2]. 또한다양한시스템을임상의사가모두이해하는것은효율적이지않을뿐더러실제로임상의사는이것을위해할애할시간이없습니다. GRADE 방법론은현재세계보건기구 (World Health Organization), 미국내과학회 (American College of Physicians), 미국흉부학회 (American Thoracic Society), UpToDate ( 및코크란연합 (Cochrane Collaboration) 등전세계유수의기관에서 진료지침개발에사용되고있습니다. GRADE 방법론은어떻게근거수준을분류하는가? GRADE 방법론은근거수준을 높음, 중등도, 낮음 및 매우낮음 으로단순하고투명하게분류합니다 (Table 2 and Appendix 2) [1]. 무작위대조군연구는근거수준 높음 에서출발하여다음의이유로중등도, 낮음, 매우낮음순으로낮아질수있습니다. ㆍ비뚤림위험 (risk of bias) ㆍ비일관성 (inconsistency) ㆍ비직접성 (indirectness) ㆍ비정밀성 (imprecision) ㆍ출판비뚤림 (publication bias) 관찰연구 ( 예 : 코호트 [cohort study] 및환자대조군연구 [case control study] 는증거의질이 낮음 으로출발하지만만일중재효과의크기가크거나 (very large effect), 교란변수가효과의크기를낮추거나 (all plausible biases would decrease the magnitude of an apparent treatment effect), 양-반응관계 (dose-response relation) 가있다면근거수준의등급을높일수있습니다. Table 2. Quality of evidence and definitions ㆍHigh quality Further research is unlikely to change our confidence in the estimate of effect ㆍModerate quality Further research is likely to have an important impact on our confidence in the estimate of effect and may change the estimate ㆍLow quality Further research is very likely to have an important impact on our confidence in the estimate of effect and is likely to change the estimate ㆍVery low quality Any estimate of effect is very uncertain See also Appendix 2 (complete translate in Korean). GRADE 방법론은어떻게권고등급을분류하는가? GRADE 방법론은 강함 (strong) 및 약함 (weak) 두가지등급의권고사항을제공합니다 ( 진료지침개발패널은 약함 대신 조건부 [conditional] 또는 임의 [discretionary] 와같은용어를선호할수있음 ). 중재의효과가위해보다명확히크거나작은경우진료지침개발패널은강한권고를제시하는반면, 만약낮은근거수준이거나효과가위해와거의비슷한 Table 3. Factors that affect the strength of a recommendation Factor Examples of strong recommendations Examples of weak recommendations Quality of evidence Many high quality randomized trials have shown the benefit of inhaled steroids in asthma Only case series have examined the utility of pleurodesis in pneumothorax Uncertainty about the balance between desirable and undesirable effects Aspirin in myocardial infarction reduces mortality with minimal toxicity, inconvenience, and cost Warfarin in low risk patients with atrial fibrillation results in small stroke reduction but increases the bleeding risk and causes substantial inconvenience Uncertainty or variability in values and preferences Uncertainty about whether the intervention represents a wise use of resources Young patients with lymphoma will invariably place a higher value on the life prolonging effects of chemotherapy than on the treatment toxicity The low cost of aspirin as a prophylaxis against stroke in patients with transient ischemic attacks See also Appendix 3 (complete translate in Korean). Older patients with lymphoma may not place a higher value on the life prolonging effects of chemotherapy than on the treatment toxicity The high cost of clopidogrel and of combination dipyridamole and aspirin as prophylaxis against stroke in patients with transient ischemic attacks

4 Do Kyung Kim, et al. Korean Translation of GRADE Series 31 경우약한권고를제시합니다. 근거수준이외에도몇가지다른요인들이권고의등급에영향을미칠수있습니다 (Table 3 and Appendix 3) [1]. CONFLICT OF INTEREST No potential conflict of interest relevant to this article was reported. AUTHOR CONTRIBUTIONS D.K.K.: translating the article, and drafting the manuscript, E.C.H.: providing clinical and methodological advices in translation, H.W.K.: helping to translate and draft the manuscript, J.Y.K., H.J.J., and H.W.K.: providing clinical advices in translation, J.H.J.: contacting BMJ editorial office to get the approval, helping to translate and draft the manuscript, and final approval. ORCID Do Kyung Kim, Eu Chang Hwang, Ho Won Kang, Ja Yoon Ku, Hyun Jin Jung, Hong Wook Kim, Jae Hung Jung, REFERENCES 1. Guyatt GH, Oxman AD, Vist GE, Kunz R, Falck-Ytter Y, Alonso- Coello P, et al.; GRADE Working Group. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ 2008;336: Atkins D, Eccles M, Flottorp S, Guyatt GH, Henry D, Hill S, et al.; GRADE Working Group. Systems for grading the quality of evidence and the strength of recommendations I: critical appraisal of existing approaches The GRADE Working Group. BMC Health Serv Res 2004;4: Lacchetti C, Guyatt G. Therapy and validity: surprising results of randomized controlled trials. In: Guyatt G, Rennie D, editors. Users' guides to the medical literature: a manual for evidencebased clinical practice. Chicago: American Medical Association; American College of Physicians. Guidelines for counseling postmenopausal women about preventive hormone therapy. Ann Intern Med 1992;117: Humphrey LL, Chan BK, Sox HC. Postmenopausal hormone replacement therapy and the primary prevention of cardiovascular disease. Ann Intern Med 2002;137: Hulley S, Grady D, Bush T, Furberg C, Herrington D, Riggs B, et al. Randomized trial of estrogen plus progestin for secondary prevention of coronary heart disease in postmenopausal women. Heart and Estrogen/progestin Replacement Study (HERS) Research Group. JAMA 1998;280: Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 2002;288: Echt DS, Liebson PR, Mitchell LB, Peters RW, Obias-Manno D, Barker AH, et al. Mortality and morbidity in patients receiving encainide, flecainide, or placebo. The Cardiac Arrhythmia Suppression Trial. N Engl J Med 1991;324: Antman EM, Lau J, Kupelnick B, Mosteller F, Chalmers TC. A comparison of results of meta-analyses of randomized control trials and recommendations of clinical experts. Treatments for myocardial infarction. JAMA 1992;268:240-8.

5 32 Do Kyung Kim, et al. Korean Translation of GRADE Series Appendix 1. GRADE의장점ㆍ전세계적으로대표되는국제진료지침개발자그룹에의해개발ㆍ근거수준 (quality of evidence) 과권고등급 (strength of recommendation) 의명확한분리ㆍ대안적치료전략의결과의중요성에대한명확한평가ㆍ근거수준등급을낮추거나높이기위한명확하고포괄적인기준ㆍ근거 (evidence) 에서권고 (recommendation) 로의투명한이행과정ㆍ환자의가치 (value) 및선호도 (preference) 의명확한제공ㆍ임상의사, 환자및정책입안자에대한권고등급의명확하고실용적인해석ㆍ체계적문헌고찰, 의료기술평가및진료지침개발에유용성 Appendix 2. 근거수준 (quality of evidence) ㆍ높음 (high) 추가연구가효과추정치 (estimate of effect) 에대한우리의신뢰도 (confidence) 를바꿀가능성이매우낮음ㆍ중등도 (moderate) 추가연구가효과추정치에대한우리의신뢰에중요한영향을미칠수있으며추정치를변경시킬수도있음ㆍ낮음 (low) 추가연구가효과추정치에대한우리의신뢰에중요한영향을미칠가능성이매우높으며추정치를변경시킬것으로예상됨ㆍ매우낮음 (very low) 효과추정치는매우불확실함 Appendix 3. 권고등급에영향을미치는요인요인 강한권고 약한권고 근거수준 (quality of evidence) 천식환자에서흡입스테로이드의효과에대한많은무작위대조군연구 폐기흉환자에서흉막유착술 (pleurodesis) 의효과에대한사례보고만이존재 원하는효과 (desirable effects) 와원하지않는효과 (undesirable effects) 심근경색증에서 aspirin의효과 ( 사망률을낮추면서약제독성, 불편및비용이적음 ) 심방세동의위험이낮은환자에서 warfarin은뇌졸중감소효과는적으나출혈위험을높일수있으며환자불편을유발함 가치 (values) 와선호 (preferences) 젊은림프종환자들은치료독성보다는화학요법의수명연장효과에더높은가치를둘수있음 고령의림프종환자는화학요법의수명연장효과보다는치료독성에더높은가치를둘수있음 비용 (costs or resources) 일시적인뇌졸중환자에서 aspirin 사용은비용이적게듦 일시적인뇌졸중환자에서 clopidogrel 과 dipyridamole 및 aspirin 병용요법은비용이많이듦

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