[Skip to Navigation]
Sign In
Figure 1.  Coxscomb Chart Depicting the National Guideline Clearinghouse Extent of Adherence to Trustworthy Standards (NEATS) Score of Included Clinical Practice Guidelines
Coxscomb Chart Depicting the National Guideline Clearinghouse Extent of Adherence to Trustworthy Standards (NEATS) Score of Included Clinical Practice Guidelines

Different colors reflect the various components of the National Academy of Medicine (NAM) score. Higher rays represent higher-quality scores as assessed using the NEATS instrument, which measures adherence (on a scale ranging from 1 [low adherence] to 5 [high adherence]) to 12 NAM standards and includes 3 binary or categorical questions (response options yes, no, and/or unknown).11

Figure 2.  Heat Map Depicting Quality of Included Clinical Practice Guidelines
Heat Map Depicting Quality of Included Clinical Practice Guidelines

The heat map depicts clinical practice guideline (CPG) quality. The CPGs are ordered from highest quality to lowest quality (left to right). We assigned a score of 5 for yes (Y) responses (3 National Guideline Clearinghouse Extent of Adherence to Trustworthy Standards [NEATS] questions) and 0 for no (N) or unknown (UKN) responses (2 NEATS questions).

Table 1.  CPG Authorship by WHO Regiona
CPG Authorship by WHO Regiona
Table 2.  Direction of Recommendations for Pharmacologic Treatments of Hospitalized Patients With COVID-19a
Direction of Recommendations for Pharmacologic Treatments of Hospitalized Patients With COVID-19a
1.
Institute of Medicine.  Clinical Practice Guidelines We Can Trust. National Academies Press; 2011:1-300.
2.
Lohr  KN, Field  MJ. A provisional instrument for assessing clinical practice guidelines (Appendix B). In: Fields MJ, Lohr KN, eds.  Guidelines for Clinical Practice: From Development to Use. National Academies Press; 1992.
3.
Hayward  RS, Wilson  MC, Tunis  SR, Bass  EB, Rubin  HR, Haynes  RB.  More informative abstracts of articles describing clinical practice guidelines.   Ann Intern Med. 1993;118(9):731-737. doi:10.7326/0003-4819-118-9-199305010-00012 PubMedGoogle ScholarCrossref
4.
Liddle  J, Williamson  M, Irwig  L.  Method for Evaluating Research Guideline Evidence. New South Wales Health Department; 1996.
5.
Cluzeau  FA, Littlejohns  P, Grimshaw  JM, Feder  G, Moran  SE.  Development and application of a generic methodology to assess the quality of clinical guidelines.   Int J Qual Health Care. 1999;11(1):21-28. doi:10.1093/intqhc/11.1.21 PubMedGoogle ScholarCrossref
6.
Cluzeau  F, Burgers  J, Brouwers  M,  et al; AGREE Collaboration.  Development and validation of an international appraisal instrument for assessing the quality of clinical practice guidelines: the AGREE project.   Qual Saf Health Care. 2003;12(1):18-23. doi:10.1136/qhc.12.1.18 PubMedGoogle Scholar
7.
Fervers  B, Burgers  JS, Haugh  MC,  et al.  Predictors of high quality clinical practice guidelines: examples in oncology.   Int J Qual Health Care. 2005;17(2):123-132. doi:10.1093/intqhc/mzi011 PubMedGoogle ScholarCrossref
8.
Brouwers  MC, Kho  ME, Browman  GP,  et al; AGREE Next Steps Consortium.  AGREE II: advancing guideline development, reporting and evaluation in health care.   CMAJ. 2010;182(18):E839-E842. doi:10.1503/cmaj.090449 PubMedGoogle ScholarCrossref
9.
Brouwers  MC, Makarski  J, Kastner  M, Hayden  L, Bhattacharyya  O; GUIDE-M Research Team.  The Guideline Implementability Decision Excellence Model (GUIDE-M): a mixed methods approach to create an international resource to advance the practice guideline field.   Implement Sci. 2015;10:36. doi:10.1186/s13012-015-0225-1 PubMedGoogle ScholarCrossref
10.
Brouwers  MC, Spithoff  K, Kerkvliet  K,  et al.  Development and validation of a tool to assess the quality of clinical practice guideline recommendations.   JAMA Netw Open. 2020;3(5):e205535. doi:10.1001/jamanetworkopen.2020.5535 PubMedGoogle Scholar
11.
Jue  JJ, Cunningham  S, Lohr  K,  et al.  Developing and testing the Agency for Healthcare Research and Quality’s National Guideline Clearinghouse Extent of Adherence to Trustworthy Standards (NEATS) instrument.   Ann Intern Med. 2019;170(7):480-487. doi:10.7326/M18-2950 PubMedGoogle ScholarCrossref
12.
Dagens  A, Sigfrid  L, Cai  E,  et al.  Scope, quality, and inclusivity of clinical guidelines produced early in the COVID-19 pandemic: rapid review.   BMJ. 2020;369:m1936. doi:10.1136/bmj.m1936 PubMedGoogle Scholar
13.
Jin  YH, Cai  L, Cheng  ZS,  et al; Zhongnan Hospital of Wuhan University Novel Coronavirus Management and Research Team, Evidence-Based Medicine Chapter of China International Exchange and Promotive Association for Medical and Health Care (CPAM).  A rapid advice guideline for the diagnosis and treatment of 2019 novel coronavirus (2019-nCoV) infected pneumonia (standard version).   Mil Med Res. 2020;7(1):4. doi:10.1186/s40779-020-0233-6 PubMedGoogle Scholar
14.
National Health Commission of the People’s Republic of China.  Diagnostic and treatment protocol using traditional Chinese medicine.   Int J Acupuncture. 2020;14(1):7-12. doi:10.1016/j.acu.2020.04.002Google Scholar
15.
Alhazzani  W, Møller  MH, Arabi  YM,  et al.  Surviving sepsis campaign: guidelines on the management of critically ill adults with coronavirus disease 2019 (COVID-19).   Crit Care Med. 2020;48(6):e440-e469. doi:10.1097/CCM.0000000000004363 PubMedGoogle ScholarCrossref
16.
Thachil  J, Tang  N, Gando  S,  et al.  ISTH interim guidance on recognition and management of coagulopathy in COVID-19.   J Thromb Haemost. 2020;18(5):1023-1026. doi:10.1111/jth.14810 PubMedGoogle ScholarCrossref
17.
Flisiak  R, Horban  A, Jaroszewicz  J,  et al.  Management of SARS-CoV-2 infection: recommendations of the Polish Association of Epidemiologists and Infectiologists as of March 31, 2020.   Pol Arch Intern Med. 2020;130(4):352-357. doi:10.20452/pamw.15270PubMedGoogle Scholar
18.
Chawla  D, Chirla  D, Dalwai  S,  et al; Federation of Obstetric and Gynaecological Societies of India (FOGSI), National Neonatology Forum of India (NNF) and Indian Academy of Pediatrics (IAP).  Perinatal-neonatal management of COVID-19 infection: guidelines of the Federation of Obstetric and Gynaecological Societies of India (FOGSI), National Neonatology Forum of India (NNF), and Indian Academy of Pediatrics (IAP).   Indian Pediatr. 2020;57(6):536-548. doi:10.1007/s13312-020-1852-4 PubMedGoogle ScholarCrossref
19.
Mehta  Y, Chaudhry  D, Abraham  OC,  et al.  Critical care for COVID-19 affected patients: position statement of the Indian Society of Critical Care Medicine.   Indian J Crit Care Med. 2020;24(4):222-241. doi:10.5005/jp-journals-10071-23395 PubMedGoogle Scholar
20.
Zhai  Z, Li  C, Chen  Y,  et al; Prevention Treatment of VTE Associated with COVID-19 Infection Consensus Statement Group.  Prevention and treatment of venous thromboembolism associated with coronavirus disease 2019 infection: a consensus statement before guidelines.   Thromb Haemost. 2020;120(6):937-948. doi:10.1055/s-0040-1710019 PubMedGoogle ScholarCrossref
21.
Rajagopal  K, Keller  SP, Akkanti  B,  et al.  Advanced pulmonary and cardiac support of COVID-19 patients: emerging recommendations from ASAIOa living working document.   Circ Heart Fail. 2020;13(5):e007175. doi:10.1161/CIRCHEARTFAILURE.120.007175 PubMedGoogle Scholar
22.
Ramírez  I, De la Viuda  E, Baquedano  L,  et al.  Managing thromboembolic risk with menopausal hormone therapy and hormonal contraception in the COVID-19 pandemic: recommendations from the Spanish Menopause Society, Sociedad Española de Ginecología y Obstetricia and Sociedad Española de Trombosis y Hemostasia.   Maturitas. 2020;137:57-62. doi:10.1016/j.maturitas.2020.04.019 PubMedGoogle ScholarCrossref
23.
Reiter  RJ, Abreu-Gonzalez  P, Marik  PE, Dominguez-Rodriguez  A.  Therapeutic algorithm for use of melatonin in patients with COVID-19.   Front Med (Lausanne). 2020;7:226. doi:10.3389/fmed.2020.00226 PubMedGoogle ScholarCrossref
24.
Barnes  GD, Burnett  A, Allen  A,  et al.  Thromboembolism and anticoagulant therapy during the COVID-19 pandemic: interim clinical guidance from the anticoagulation forum.   J Thromb Thrombolysis. 2020;50(1):72-81. doi:10.1007/s11239-020-02138-z PubMedGoogle ScholarCrossref
25.
Llau  JV, Ferrandis  R, Sierra  P,  et al.  SEDAR-SEMICYUC consensus recommendations on the management of haemostasis disorders in severely ill patients with COVID-19 infection.   Rev Esp Anestesiol Reanim (Engl Ed). 2020;67(7):391-399. doi:10.1016/j.redar.2020.05.007 PubMedGoogle ScholarCrossref
26.
Lombardy Section Italian Society Infectious and Tropical Diseases.  Vademecum for the treatment of people with COVID-19. Edition 2.0, 13 March 2020.   Infez Med. 2020;28(2):143-152.PubMedGoogle Scholar
27.
Moores  LK, Tritschler  T, Brosnahan  S,  et al.  Prevention, diagnosis, and treatment of VTE in patients with coronavirus disease 2019: CHEST Guideline and Expert Panel Report.   Chest. 2020;158(3):1143-1163. doi:10.1016/j.chest.2020.05.559 PubMedGoogle ScholarCrossref
28.
Flisiak  R, Horban  A, Jaroszewicz  J,  et al.  Management of SARS-CoV-2 infection: recommendations of the Polish Association of Epidemiologists and Infectiologists: annex No. 1 as of June 8, 2020.   Pol Arch Intern Med. 2020;130(6):557-558. doi:10.20452/pamw.15424PubMedGoogle Scholar
29.
Kosior  DA, Undas  A, Kopeć  G,  et al.  Guidance for anticoagulation management in venous thromboembolism during the coronavirus disease 2019 pandemic in Poland: an expert opinion of the Section on Pulmonary Circulation of the Polish Cardiac Society.   Kardiol Pol. 2020;78(6):642-646. doi:10.33963/KP.15425PubMedGoogle ScholarCrossref
30.
Li  YH, Wang  MT, Huang  WC, Hwang  JJ.  Management of acute coronary syndrome in patients with suspected or confirmed coronavirus disease 2019: consensus from Taiwan Society of Cardiology.   J Formos Med Assoc. 2021;120(1 Pt 1):78-82. doi:10.1016/j.jfma.2020.07.017 PubMedGoogle Scholar
31.
Henderson  LA, Canna  SW, Friedman  KG,  et al.  American College of Rheumatology clinical guidance for multisystem inflammatory syndrome in children associated with SARS-CoV-2 and hyperinflammation in pediatric COVID-19: version 1.   Arthritis Rheumatol. 2020;72(11):1791-1805. doi:10.1002/art.41454 PubMedGoogle ScholarCrossref
32.
Rochwerg  B, Agarwal  A, Zeng  L,  et al.  Remdesivir for severe COVID-19: a clinical practice guideline.   BMJ. 2020;370:m2924. doi:10.1136/bmj.m2924 PubMedGoogle Scholar
33.
Goldenberg  NA, Sochet  A, Albisetti  M,  et al; Pediatric/Neonatal Hemostasis and Thrombosis Subcommittee of the ISTH SSC.  Consensus-based clinical recommendations and research priorities for anticoagulant thromboprophylaxis in children hospitalized for COVID-19-related illness.   J Thromb Haemost. 2020;18(11):3099-3105. doi:10.1111/jth.15073 PubMedGoogle ScholarCrossref
34.
Jin  YH, Zhan  QY, Peng  ZY,  et al; Evidence-Based Medicine Chapter of China International Exchange and Promotive Association for Medical and Health Care (CPAM); Chinese Research Hospital Association (CRHA).  Chemoprophylaxis, diagnosis, treatments, and discharge management of COVID-19: an evidence-based clinical practice guideline (updated version).   Mil Med Res. 2020;7(1):41. doi:10.1186/s40779-020-00270-8PubMedGoogle Scholar
35.
Ferreira  LL, Sampaio  DL, Chagas  ACP,  et al.  AMB guidelines: COVID-19. Rev Assoc Med Bras 2020.   Rev. Assoc. Med. Bras. 2020;66(suppl 2):17-21. doi:10.1590/1806-9282.66.S2.17Google ScholarCrossref
36.
Chekkal  M, Deba  T, Hadjali  S,  et al.  Prevention and treatment of COVID-19-associated hypercoagulability: recommendations of the Algerian Society of Transfusion and Hemobiology.   Transfus Clin Biol. 2020;27(4):203-206. doi:10.1016/j.tracli.2020.09.004 PubMedGoogle ScholarCrossref
37.
Flisiak  R, Parczewski  M, Horban  A,  et al.  Management of SARS-CoV-2 infection: recommendations of the Polish Association of Epidemiologists and Infectiologists. Annex no. 2 as of October 13, 2020.   Pol Arch Intern Med. 2020;130(10):915-918. doi:10.20452/pamw.15658 PubMedGoogle ScholarCrossref
38.
Abu-Raya  B, Migliori  GB, O’Ryan  M,  et al.  Coronavirus disease-19: an interim evidence synthesis of the World Association for Infectious Diseases and Immunological Disorders (WAIDID).   Front Med (Lausanne). 2020;7:572485. doi:10.3389/fmed.2020.572485 PubMedGoogle Scholar
39.
Mehta  Y, Chaudhry  D, Abraham  OC,  et al.  Critical care for COVID-19 affected patients: updated position statement of the Indian Society of Critical Care Medicine.   Indian J Crit Care Med. 2020;24(suppl 5):S225-S230. doi:10.5005/jp-journals-10071-23621 PubMedGoogle Scholar
40.
Foti  G, Giannini  A, Bottino  N,  et al; COVID-19 Lombardy ICU Network.  Management of critically ill patients with COVID-19: suggestions and instructions from the coordination of intensive care units of Lombardy.   Minerva Anestesiol. 2020;86(11):1234-1245. doi:10.23736/S0375-9393.20.14762-X PubMedGoogle ScholarCrossref
41.
Andrejak  C, Cottin  V, Crestani  B,  et al.  Guide for the management of patients with respiratory sequelae after a SARS-CoV-2 pneumonia: support proposals developed by the French-language Respiratory Medicine Society: version of 10 November 2020  [in French].  Rev Mal Respir. 2021;38(1):114-121. doi:10.1016/j.rmr.2020.11.009 PubMedGoogle ScholarCrossref
42.
Berlit  P, Bösel  J, Gahn  G,  et al.  “Neurological manifestations of COVID-19”—guideline of the German Society of Neurology.   Neurol Res Pract. 2020;2:51. doi:10.1186/s42466-020-00097-7 PubMedGoogle ScholarCrossref
43.
Henderson  LA, Canna  SW, Friedman  KG,  et al.  American College of Rheumatology clinical guidance for multisystem inflammatory syndrome in children associated with SARS-CoV-2 and hyperinflammation in pediatric COVID-19: version 2.   Arthritis Rheumatol. 2021;73(4):e13-e29. doi:10.1002/art.41616 PubMedGoogle ScholarCrossref
44.
Rochwerg  B, Agarwal  A, Siemieniuk  RA,  et al.  A living WHO guideline on drugs for COVID-19.   BMJ. 2020;370:m3379. doi:10.1136/bmj.m3379 PubMedGoogle Scholar
45.
Chen  X, Liu  Y, Gong  Y,  et al; Chinese Society of Anesthesiology, Chinese Association of Anesthesiologists.  Perioperative management of patients infected with the novel coronavirus: recommendation from the Joint Task Force of the Chinese Society of Anesthesiology and the Chinese Association of Anesthesiologists.   Anesthesiology. 2020;132(6):1307-1316. doi:10.1097/ALN.0000000000003301 PubMedGoogle ScholarCrossref
46.
Andrejak  C, Blanc  FX, Costes  F,  et al.  Guide for follow-up of patients with SARS-CoV-2 pneumonia: management proposals developed by the French-language Respiratory Medicine Society. Version of 10 May 2020  [in French].  Rev Mal Respir. 2020;37(6):505-510. doi:10.1016/j.rmr.2020.05.001 PubMedGoogle ScholarCrossref
47.
Donders  F, Lonnée-Hoffmann  R, Tsiakalos  A,  et al; Isidog Covid-Guideline Workgroup.  ISIDOG COVID-Guideline Workgroup. ISIDOG recommendations concerning COVID-19 and pregnancy.   Diagnostics (Basel). 2020;10(4):243. doi:10.3390/diagnostics10040243PubMedGoogle ScholarCrossref
48.
Tan  SHS, Hong  CC, Saha  S, Murphy  D, Hui  JH.  Medications in COVID-19 patients: summarizing the current literature from an orthopaedic perspective.   Int Orthop. 2020;44(8):1599-1603. doi:10.1007/s00264-020-04643-5 PubMedGoogle ScholarCrossref
49.
Zhang  Y, Coats  AJS, Zheng  Z,  et al.  Management of heart failure patients with COVID-19: a joint position paper of the Chinese Heart Failure Association & National Heart Failure Committee and the Heart Failure Association of the European Society of Cardiology.   Eur J Heart Fail. 2020;22(6):941-956. doi:10.1002/ejhf.1915 PubMedGoogle ScholarCrossref
50.
Solé  G, Salort-Campana  E, Pereon  Y,  et al; FILNEMUS COVID-19 study group.  Guidance for the care of neuromuscular patients during the COVID-19 pandemic outbreak from the French Rare Health Care for Neuromuscular Diseases Network.   Rev Neurol (Paris). 2020;176(6):507-515. doi:10.1016/j.neurol.2020.04.004 PubMedGoogle ScholarCrossref
51.
Cardenas  MC, Bustos  SS, Enninga  EAL, Mofenson  L, Chakraborty  R.  Characterising and managing paediatric SARSCoV-2 infection: learning about the virus in a global classroom.   Acta Paediatr. 2021;110(2):409-422. doi:10.1111/apa.15662 PubMedGoogle ScholarCrossref
52.
Miklowski  M, Jansen  B, Auron  M, Whinney  C.  The hospitalized patient with COVID-19 on the medical ward: Cleveland Clinic approach to management.   Cleve Clin J Med. Published online November 3, 2020. doi:10.3949/ccjm.87a.ccc064PubMedGoogle Scholar
53.
Yang  X, Liu  Y, Liu  Y,  et al.  Medication therapy strategies for the coronavirus disease 2019 (COVID-19): recent progress and challenges.   Expert Rev Clin Pharmacol. 2020;13(9):957-975. doi:10.1080/17512433.2020.1805315 PubMedGoogle ScholarCrossref
54.
Baller  EB, Hogan  CS, Fusunyan  MA,  et al.  Neurocovid: pharmacological recommendations for delirium associated with COVID-19.   Psychosomatics. 2020;61(6):585-596. doi:10.1016/j.psym.2020.05.013 PubMedGoogle ScholarCrossref
55.
Fang  F, Chen  Y, Zhao  D,  et al; Chinese Pediatric Society and the Editorial Committee of the Chinese Journal of Pediatrics.  Recommendations for the diagnosis, prevention, and control of coronavirus disease-19 in children: the Chinese perspectives.   Front Pediatr. 2020;8:553394. doi:10.3389/fped.2020.553394 PubMedGoogle Scholar
56.
Dobesh  PP, Trujillo  TC.  Coagulopathy, venous thromboembolism, and anticoagulation in patients with COVID-19.   Pharmacotherapy. 2020;40(11):1130-1151. doi:10.1002/phar.2465 PubMedGoogle ScholarCrossref
57.
Kronbichler  A, Effenberger  M, Eisenhut  M, Lee  KH, Shin  JI.  Seven recommendations to rescue the patients and reduce the mortality from COVID-19 infection: an immunological point of view.   Autoimmun Rev. 2020;19(7):102570. doi:10.1016/j.autrev.2020.102570 PubMedGoogle Scholar
58.
Ferreira  LL, Sampaio  DL, Chagas  ACP,  et al.  AMB guidelines: COVID 19. Rev Assoc Med Bras 2020.  2020;66(9):1179. doi:10.1590/1806-9282.66.9.1179.
59.
Aguilar  RB, Hardigan  P, Mayi  B,  et al.  Current understanding of COVID-19 clinical course and investigational treatments.   Front Med (Lausanne). 2020;7:555301. doi:10.3389/fmed.2020.555301 PubMedGoogle Scholar
60.
Costa  A, Weinstein  ES, Sahoo  DR, Thompson  SC, Faccincani  R, Ragazzoni  L.  How to build the plane while flying: VTE/PE thromboprophylaxis clinical guidelines for COVID-19 patients.   Disaster Med Public Health Prep. 2020;14(3):391-405. doi:10.1017/dmp.2020.195 PubMedGoogle ScholarCrossref
61.
Danthuluri  V, Grant  MB.  Update and recommendations for ocular manifestations of COVID-19 in adults and children: a narrative review.   Ophthalmol Ther. 2020;9(4):853-875. doi:10.1007/s40123-020-00310-5 PubMedGoogle ScholarCrossref
62.
Chivukula  RR, Maley  JH, Dudzinski  DM, Hibbert  K, Hardin  CC.  Evidence-based management of the critically ill adult with SARS-CoV-2 infection.   J Intensive Care Med. 2021;36(1):18-41. doi:10.1177/0885066620969132 PubMedGoogle ScholarCrossref
63.
World Health Organization. Clinical management of severe acute respiratory infection (SARI) when COVID-19 is suspected: interim guidance. March 13, 2020. Accessed April 24, 2021. https://apps.who.int/iris/handle/10665/331446
64.
Stamm  TA, Andrews  MR, Mosor  E,  et al.  The methodological quality is insufficient in clinical practice guidelines in the context of COVID-19: systematic review.   J Clin Epidemiol. 2021;135:125-135. doi:10.1016/j.jclinepi.2021.03.005 PubMedGoogle ScholarCrossref
65.
Kung  J, Miller  RR, Mackowiak  PA.  Failure of clinical practice guidelines to meet institute of medicine standards: two more decades of little, if any, progress.   Arch Intern Med. 2012;172(21):1628-1633. doi:10.1001/2013.jamainternmed.56 PubMedGoogle ScholarCrossref
66.
Reames  BN, Krell  RW, Ponto  SN, Wong  SL.  Critical evaluation of oncology clinical practice guidelines.   J Clin Oncol. 2013;31(20):2563-2568. doi:10.1200/JCO.2012.46.8371 PubMedGoogle ScholarCrossref
67.
Emergency Care Research Institute. US Agency for Healthcare Research and Quality launches new clinical guideline assessment tool through contract to ECRI Institute. November 16, 2017. Accessed April 24, 2021. https://www.ecri.org/press/ahrq-clinical-guideline-assessment-tool
68.
Brouwers  MC, Spithoff  K, Lavis  J, Kho  ME, Makarski  J, Florez  ID.  What to do with all the AGREEs? the AGREE portfolio of tools to support the guideline enterprise.   J Clin Epidemiol. 2020;125:191-197. doi:10.1016/j.jclinepi.2020.05.025 PubMedGoogle ScholarCrossref
69.
Fervers  B, Burgers  JS, Voellinger  R,  et al.  ADAPTE Collaboration. Guideline adaptation: an approach to enhance efficiency in guideline development and improve utilization.   BMJ Qual Saf. 2011;20(3):228-236. doi:10.1136/bmjqs.2010.043257PubMedGoogle ScholarCrossref
1 Comment for this article
EXPAND ALL
What Can Practicing Physicians Do to Improve their National Specialty Society's Evidence-based Practice Guidelines?
Florence Lecraw, M.D. | Andrew Young School of Policy Studies, Georgia State University
I thank the authors for the work entailed to determine if 32 clinical practice guidelines regarding the pharmacologic treatments for hospitalized patients with COVID-19 met the recommendations by National Academy of Medicine to ensure well derived evidence-based best practice. As a physician and patient, I have been concerned that many practice guidelines developed by national medical associations lacked a research methodologist. It is unfortunate that there are papers published in medical journals with data and analytical errors leading to misleading and even false conclusions. Methodologists can determine if the conclusion of papers investigated by the practice guideline task force was based on good data well analyzed. An expert research methodologist can educate the task force members why a certain paper should not be used in their recommendation for evidence-based best practice. However, due to this well analyzed study, I now know that there are other issues that make many practice guidelines suspect. To err is human, as the landmark Institute of Medicine report said. But guidelines that don't meet criteria for trustworthiness should be revised. At this time, trust in the scientific community by physicians and the public is sorely lacking. Transparency is the first step in rebuilding trust. I ask the readership of this journal to send this well-designed study to your national specialty leadership so they can determine if they are following NAM’s recommendations.
CONFLICT OF INTEREST: None Reported
READ MORE
Original Investigation
Medical Journals and Publishing
December 10, 2021

Adherence of Clinical Practice Guidelines for Pharmacologic Treatments of Hospitalized Patients With COVID-19 to Trustworthy Standards: A Systematic Review

Author Affiliations
  • 1Interdepartmental Division of Critical Care Medicine, Department of Medicine, Temerty Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada
  • 2Departments of Critical Care and Medicine, Unity Health Toronto, St Michael’s Hospital, Toronto, Ontario, Canada
  • 3Departments of Medicine, Critical Care Medicine, Pediatrics and Health Research Methods, Evidence, and Impact, McMaster University, Hamilton, Ontario, Canada
  • 4Li Ka Shing Knowledge Institute, St Michael’s Hospital, Toronto, Ontario, Canada
  • 5School of Medicine, Royal College of Surgeons, Dublin, Ireland
  • 6Department of Critical Care Medicine, London Health Sciences Centre, London, Ontario, Canada
  • 7Department of Medicine, Western University, London, Ontario, Canada
  • 8Physiotherapy and Division of Critical Care, St Joseph’s Healthcare, Hamilton, Ontario, Canada
  • 9School of Rehabilitation Science, Faculty of Health Science, McMaster University, Hamilton, Ontario, Canada
  • 10Hamilton Health Sciences, Hamilton, Ontario, Canada
  • 11Dalla Lana School of Public Health and the Institute of Health Policy, Management, and Evaluation, University of Toronto, Toronto, Ontario, Canada
  • 12Canadian Donation and Transplant Research Program, Ottawa, Ontario, Canada
  • 13Department of Anesthesiology, Université de Sherbrooke, Sherbrooke, Quebec, Canada
  • 14Department of Critical Care Medicine, Sunnybrook Health Sciences Centre, Toronto, Ontario, Canada
JAMA Netw Open. 2021;4(12):e2136263. doi:10.1001/jamanetworkopen.2021.36263
Key Points

Question  Do clinical practice guidelines (CPGs) that report on pharmacologic treatments of hospitalized patients with COVID-19 meet the National Academy of Medicine standards for trustworthiness?

Findings  In this systematic review of 32 CPGs of predominantly low quality, few reported funding sources or conflicts of interest, included a methodologist, described a search strategy or study selection process, or synthesized evidence. Although 14 CPGs (43.8%) made recommendations or suggestions for or against treatments, they infrequently rated the confidence in the quality of the evidence (6 [18.8%]), described potential benefits and harms (6 [18.8%]), or graded the strength of recommendations (5 [15.6%]).

Meaning  The findings of this study suggest that few COVID-19 CPGs meet National Academy of Medicine standards for trustworthy guidelines.

Abstract

Importance  The COVID-19 pandemic created the need for rapid and urgent guidance for clinicians to manage COVID-19 among patients and prevent transmission.

Objective  To appraise the quality of clinical practice guidelines (CPGs) using the National Academy of Medicine (NAM) criteria.

Evidence Review  A search of MEDLINE, EMBASE, and the Cochrane Central Register of Controlled Trials to December 14, 2020, and a search of related articles to February 28, 2021, that included CPGs developed by societies or by government or nongovernment organizations that reported pharmacologic treatments of hospitalized patients with COVID-19. Teams of 2 reviewers independently abstracted data and assessed CPG quality using the 15-item National Guideline Clearinghouse Extent of Adherence to Trustworthy Standards (NEATS) instrument.

Findings  Thirty-two CPGs were included in the review. Of these, 25 (78.1%) were developed by professional societies and emanated from a single World Health Organization (WHO) region. Overall, the CPGs were of low quality. Only 7 CPGs (21.9%) reported funding sources, and 12 (37.5%) reported conflicts of interest. Only 5 CPGs (15.6%) included a methodologist, described a search strategy or study selection process, or synthesized the evidence. Although 14 CPGs (43.8%) made recommendations or suggestions for or against treatments, they infrequently rated confidence in the quality of the evidence (6 of 32 [18.8%]), described potential benefits and harms (6 of 32 [18.8%]), or graded the strength of the recommendations (5 of 32 [15.6%]). External review, patient or public perspectives, or a process for updating were rare. High-quality CPGs included a methodologist and multidisciplinary collaborations involving investigators from 2 or more WHO regions.

Conclusions and Relevance  In this review, few COVID-19 CPGs met NAM standards for trustworthy guidelines. Approaches that prioritize engagement of a methodologist and multidisciplinary collaborators from at least 2 WHO regions may lead to the production of fewer, high-quality CPGs that are poised for updates as new evidence emerges.

Trial Registration  PROSPERO Identifier: CRD42021245239

Introduction

Clinical practice guidelines (CPGs) should be systematically developed statements and recommendations that articulate the roles for diagnostic tests and treatments to inform clinician and patient decisions. The process for creating guidelines affects CPG quality. In turn, CPG quality affects patient care, safety, and health care equality. In 2011, the National Academy of Medicine (NAM) (formerly known as the Institute of Medicine)1 published a report stipulating that CPG recommendations should be supported by a systematic review of the evidence and highlighted 8 criteria for assessing the trustworthiness of CPGs.

Many instruments and scorecards have been developed to evaluate CPG quality.2-11 The Appraisal of Guidelines for Research and Evaluation (AGREE) II tool8 is the most widely used CPG appraisal tool. The scope of the AGREE II tool targets all components of a CPG report, emphasizing features that enhance its internal validity. The AGREE Recommendation Excellence tool,9 a supplement to the AGREE II tool, highlights 9 items in 3 themes that focus on the quality of the CPG recommendations and the justifications that underpin them. The AGREE Recommendation Excellence tool ascertains whether CPGs are credible and implementable by assessing their internal consistency. Notwithstanding, the AGREE II and AGREE Recommendation Excellence appraisal tools do not directly address the NAM criteria for trustworthy CPGs or consider the perspectives of different stakeholder groups involved in CPG development. More recently, the US Agency for Healthcare Research and Quality developed the National Guideline Clearinghouse Extent of Adherence to Trustworthy Standards (NEATS) instrument 11 (eMethods in Supplement 1) to provide a standardized approach to assess CPG quality. The NEATS tool explicitly evaluates the NAM criteria and assesses CPGs from a broad and multidisciplinary perspective.

The COVID-19 pandemic created the need for rapid and urgent guidance for clinicians to manage COVID-19 among patients and prevent transmission, but methodological rigor has been variable across CPGs.12 We systematically reviewed published CPGs reporting pharmacologic treatments for hospitalized patients with COVID-19 and evaluated their quality and trustworthiness using the NEATS instrument. We hypothesized that CPGs created and disseminated during the pandemic have important methodological weaknesses that affect their quality and trustworthiness.

Methods
Study Design

We systematically reviewed published CPGs addressing pharmacologic treatments for hospitalized patients with COVID-19. An ethics review was not obtained for this secondary analysis of published data.

Data Sources and Searches

We searched MEDLINE, EMBASE, and the Cochrane Central Register of Controlled Trials (to December 14, 2020) and conducted a search of related articles (to February 28, 2021) to identify updates. Two reviewers (M.L. and J.S.) independently screened all titles and abstracts of citations for eligibility. Disagreements were resolved by consensus or in discussion with a third reviewer (K.E.A.B.).

Study Selection

Eligible CPGs were investigator led, sponsored or produced by a national or international scientific organization or government or nongovernment organization related to global health, and reported on pharmacologic treatments of hospitalized patients with COVID-19 and its complications. Pharmacologic interventions referred to treatments dispensed by hospital pharmacies, with an identifiable molecular structure. We included all versions of published CPGs. We did not apply language restrictions. We excluded CPGs produced for regional or local use (eg, hospital-based), nonpharmacologic interventions, medications not dispensed by a hospital pharmacy (eg, herbal remedies, homeopathic medications), and CPGs that focused on treatments for specific populations (ie, obstetrical populations hospitalized with COVID-19).

Data Abstraction

Fifteen reviewers (K.E.A.B., M.L, J.S., K.H., D.G., M.E.K., D.C., J.O.F., M.O.M., M.D., D.C., F.D., A.A., N.K.J.A., and B.R.), working independently and in duplicate, abstracted data pertaining to CPG publications (dates of submission, acceptance, and publication online and in print), geographical representation of collaborators using World Health Organization (WHO) regions, CPG sponsorship (professional society, government or nongovernment agency, or other), funding (monetary or nonmonetary), and scope (international, national, state/province, or other). Reviewers recorded the patient populations addressed (hospitalized, ward, intensive care unit, or other) and assessed whether CPGs had a formal conflict of interest (COI) policy and declared COIs (financial, nonfinancial, or both). They noted whether patient and/or public perspectives were sought or incorporated. For each pharmacologic intervention, appraisers documented outcomes of interest and the direction of the recommendation statement (for or against or no recommendation), the strength of the recommendation, and the certainty of the evidence.

Quality Assessment

Working in pairs, reviewers appraised the quality of included CPGs using the NEATS instrument11 (eMethods in Supplement 1). Disagreements were resolved by consensus or in discussion with a third reviewer (K.E.A.B.).

Data Synthesis and Analysis

We collated data in Excel, version 2016 (Microsoft Corporation), to characterize CPGs, NEATS scores, and the direction of recommendation or suggestion statements (for, against, or no recommendation) for each pharmacologic treatment described in included CPGs. The NEATS instrument includes 3 binary or categorical items reflecting adherence to the NAM standard: assessing disclosure of funding (yes or no), multidisciplinary representation (yes, no, or unknown), and inclusion of a methodologist on the guideline panel (yes, no, or unknown) in CPG panels and 12 Likert scales. Reviewers rated adherence (on a scale ranging from 1 [low adherence] to 5 [high adherence]) to 12 NAM standards reflecting disclosure/management of COIs, inclusion of patient and public perspectives, use of systematic review of the evidence (separate items for reporting search strategy, study selection, and synthesis of the evidence), a process for making recommendations (separate items for reporting grading or rating of the quality or strength of evidence, reporting benefits and harms of recommendations, including evidence summary supporting recommendations, and rating the strength of recommendations), generation of specific and unambiguous recommendations, procurement of external reviews, and inclusion of a prespecified process to update the CPG.

We tabulated results to highlight the evolution of evidence over time for each pharmacologic intervention addressed by 3 or more CPGs. We characterized and compared recommendations for use of each specific pharmacologic intervention by assessing whether a recommendation or suggestion was made for or against its use or whether no recommendation for its use was made. In assessing the consistency between CPGs for each pharmacologic treatment, we prioritized the direction of the recommendation over the strength of the recommendation.

We depicted quality scores for each element of the NEATS instrument for each included CPG using a Coxcomb chart (Figure 1). We illustrated the quality ratings of all included CPGs using a heat map (Figure 2). To summarize binary and categorical data in the NEATS assessment in both figures, we assigned a score of 5 for yes and 0 for no or unknown responses.

Results
CPG Identification and Quality Assessment

From 2226 citations, the reviewers screened 51 full texts and identified 32 eligible CPGs.13-44 We excluded 19 CPGs (eFigure in Supplement 1).45-63 Of the 32 included CPGs, 3 (9.4%)15,38,40 reported on pharmacologic treatments for critically ill patients specifically, and the remainder reported on treatments for hospitalized patients with COVID-19. Fifteen CPGs (46.9%) were international15,16,20,21,23,24,27,31-34,36,38,43,44 and 17 (53.1%) were national.13,14,17-19,22,25,26,28-30,35,37,39-42 Most CPGs (25 [78.1%]) had sponsorship from 1 or more national societies, and few CPGs (3 [9.4%])14,23,34 had sponsorship from government, nongovernment, or not-for-profit agencies (4 [12.5%]).13,32,38,44 Seven CPGs (21.9%)13,20,23,30-32,34 explicitly reported their funding sources (eTable 1 in Supplement 1). Guidelines predominantly included authors from a single WHO region (20 [62.5%]) and mostly emanated from America or Europe (Table 1). Overall, few CPGs met most of the NAM standards for trustworthiness as assessed by the NEATS instrument (Figure 1 and eTable 2 in Supplement 1).

Funding and Panel Composition

Eighteen CPGs (56.3%) explicitly disclosed funding information.13,15,18,20-24,26,27,30-32,34,38,39,42,44 Twenty CPGs (62.5%)13,15,17,18,20,21,23,24,27-30,32,34,35,37,38,40,43,44 included multidisciplinary guideline panels, and 5 guideline panels (15.6%)13,15,32,34,44 included a methodologist.

Disclosure of COIs and Inclusion of Patient and Public Perspectives

We identified 12 CPGs (37.5%)13,15,17,20,23,27,28,32,37,40,42,44 with high adherence (score of 4 or 5) to the NAM standard to disclose actual or potential financial COIs and report how COIs were incorporated or managed in the CPG development process. Eight CPGs (25.0%)21,22,29-31,34,38,43 had intermediate adherence (score of 3) and 12 CPGs (37.5%)14,16,18,19,24-26,33,35,36,39,41 had low adherence (score of 1 or 2) to this NAM standard.

Only 2 CPGs (6.3%)32,44 adhered (both with a score of 5) to the requirement to seek the views of patients, surrogates, advocates, and/or the public who represent those that have experience with the disease, its treatment, or its complications or those who could be affected by the CPG. These individuals could be integrated into the CPG development group or engaged in other ways or at various points in CPG development.

Inclusion of a Systematic Review of the Evidence

Six CPGs (18.8%)18,20,27,32,34,44 adhered (score of 4 or 5) to the requirement to describe their search strategy in detail, including a listing of the databases searched, summary of the search terms used, and the start and end date covered by the search. Five CPGs (15.6%)18,27,32,34,44 adhered (score of 4 or 5) to the requirement to describe the study selection, including the number of studies identified and a summary of inclusion and exclusion criteria. Five CPGs (15.6%)15,27,32,34,44 adhered (score of 4 or 5) to the requirement to provide a synthesis of the evidence from the selected studies in the form of a detailed description of the body of evidence or as evidence tables or both.

Recommendations

Six CPGs (18.8%)15,20,27,32,34,44 adhered (score of 4 or 5) to the requirement to provide a grade or rating of the level of confidence or certainty in the quality or strength of the evidence underpinning each recommendation. Similarly, 6 CPGs (18.8%)15,23,27,32,34,44 adhered (all with a score of 5) to the requirement to provide a clear description of the potential benefits and harms and link this information to specific recommendations. The same 6 CPGs15,23,27,32,34,44 adhered (score of 4 or 5) to the requirement to have an explicit link to a summary of the relevant evidence and link this information directly to recommendations. Five CPGs (15.6%)15,27,32,34,44 adhered (score of 4 or 5) to the standard to rate the strength of the recommendations (strong or conditional/weak) based on a clear and well-described evidence-to-recommendation scheme that took into account the balance between benefits and harms, available evidence, and their confidence in the underlying evidence (quantity, quality, and consistency). Fourteen CPGs (43.8%)15,18,20,22-24,26,27,30,32,34,36,39,44 adhered (score of 4 or 5) to the requirement to make specific and unambiguous recommendations that stated which actions should or should not be taken in specific situations or populations, and, where recommendations were vague or underspecified, clearly described the rationale for making recommendations.

External Review and Plans for Updating

Only 3 CPGs (9.4%)32,34,44 adhered (score of 4 or 5) to the requirement to describe an external review process by specifying (name and description) relevant stakeholders (ie, scientific and clinical experts, organizations, agencies, patients, and representatives) and a process for external review. Only 2 CPGs (6.3%; both with a score of 5)32,44 had a prespecified procedure to update the CPG that included the time frame for updating, the process by which a decision would be made to update the CPG, and a description of how the update would be conducted.

We depict the total NEATS score for each included CPG in a heat map in Figure 2. Common features of the highest-quality CPGs (n = 5)15,27,32,34,44 were that they were multidisciplinary and included collaborators from at least 2 WHO regions. Four of these 5 highest-quality CPGs15,32,34,44 included a methodologist in their guideline panel.

Direction of Recommendations for Pharmaceutical Interventions

Table 2 depicts the evolution and direction of recommendations over time for each pharmacologic intervention reported by 3 or more CPGs in chronologic order. Clinical practice guidelines consistently recommended or suggested use of supportive (ie, vasopressors, inotropes) and prophylactic treatments (venous thromboembolism or deep venous thrombosis prophylaxis, histamine receptor antagonists, or proton pump inhibitors) for hospitalized patients with COVID-19. Notwithstanding, we noted relatively inconsistent recommendations for most pharmacologic treatments identified (empirical antibiotics, azithromycin, corticosteroids, hydroxychloroquine or chloroquine, lopinavir or ritonavir, remdesivir, tocilizumab, interferon, favipiravir, and oseltamivir) in the included CPGs.

Clinical practice guideline recommendations evolved during the period of our review to recommend or suggest the use of corticosteroids for hospitalized patients with COVID-19 (Table 2). Conversely, CPGs evolved from largely recommending or suggesting use of hydroxychloroquine or chloroquine, lopinavir or ritonavir, remdesivir, and tocilizumab to recommending or suggesting against their use for hospitalized patients with COVID-19 during the period covered by our review.

Discussion

In this systematic review of CPGs evaluating pharmacologic treatments for hospitalized patients with COVID-19, we found that few CPGs met the NAM standards for trustworthiness as assessed by the NEATS instrument.1,11 Although nearly two-thirds of CPGs included multidisciplinary guideline panels, fewer than 20% of CPG panels included a methodologist. Only 37.5% of CPGs had a detailed disclosure of actual or potential COIs. Few CPGs (6.3%) included patient and public perspectives. Fewer than 20% of included COVID-19–related CPGs described their search strategy, a process for study selection, or provided a synthesis of the evidence. Although nearly half of CPGs made suggestions or recommendations for or against treatments, fewer than 20% of CPGs provided a grade or rating of the level of confidence in or certainty with the quality or strength of the evidence, offered a clear description of the potential benefits and harms with links to specific recommendations, or rated the strength of the recommendations using a clear grading scheme. Fewer than 10% of CPGs underwent external review and even fewer described a process for updating. The overall quality of CPGs, as assessed by the NEATS score, was low. Multidisciplinary panels that included a methodologist and collaborators from at least 2 WHO regions were features of high-quality COVID-19 CPGs.

The rate at which CPGs pertaining to the management of COVID-19 in various settings (outpatient, inpatient, or intensive care unit) have been published is unprecedented. During a pandemic specifically, there is a high demand for early, systematically developed statements that reflect best practices based on available evidence to guide the practice of health care professionals. Nonetheless, strong methodologic standards for CPGs are essential to avoid promulgating useless or potentially harmful treatments and wasting health care resources.64 Overall, most included CPGs in our study failed to meet NAM standards and consequently were at increased risk of bias. Although producing high-quality guidelines may be viewed as impractical during a pandemic, this review identified features of high-quality COVID-19–related CPGs using the NEATS instrument. Although most high-quality CPGs tended to be published later in the pandemic, a high-quality CPG in our review was published in March 2020.15 Moreover, we noted that updates of CPGs published earlier in the pandemic tended to be of higher quality than the parent documents (Figure 2). Improvement of CPG quality over time may reflect accumulating knowledge, clinical experience, or lead-time bias.

Our findings align with other assessments of nonpandemic and pandemic CPG quality.12,64-66 From 130 randomly selected CPGs from the National Guideline Clearinghouse, Kung et al65 found that the median number of NAM standards satisfied was 8 of 18 (44.4% [IQR, 36.1%-52.8%]). The authors noted that fewer than half of their included CPGs and one-third of CPGs produced by subspecialty societies met more than 50% of the NAM standards.65 Similar to our study, others have shown that fewer than half of CPGs provided information regarding COIs,12,65 few CPGs included patients or patient representatives,12,64-66 and the CPGs rarely included a process for updating.64,66 The present review adds to the literature by documenting that fewer than 20% of CPGs included a systematic review or adhered to the International Organization for Standardization to generate recommendations for care. Although several CPGs in our review (14 of 32 [43.8%]) made suggestions or recommendations for or against treatments, they infrequently provided a grade or rating of the level of confidence or certainty regarding the quality or strength of the evidence (6 of 32 [18.8%]), offered a clear description of the potential benefits and harms (6 of 32 [18.8%]), or rated the strength of the recommendations using a clear grading scheme (5 of 32 [15.6%]). As such, the guidance statements from most CPGs included in our review were not optimally informed by the key dimensions of evidence on pharmacologic interventions for COVID-19. Contrary to a review of oncology CPGs,66 most CPGs in our review did not undergo external peer review. Similar to our study, an earlier review of 19 COVID-19–specific CPGs12 found that the overall quality of CPGs was poor; lacked detail; had inconsistent recommendations, even for the same intervention; and did not provide explicit linkage between the evidence and generating recommendations. Recently, Stamm et al64 evaluated the quality of 188 general COVID-19 CPGs published from February 1 to April 27, 2020, using the AGREE II tool. The CPGs in this review were largely (83%) based on informal consensus without clear evidence summaries and scored highest for scope and purpose (89%) and lowest (25%) for rigor of development. The latter finding may relate to the paucity of evidence available early in the pandemic. Unlike previous COVID-19 CPG reviews,12,64 we limited our review to pharmacologic treatments for COVID-19, included CPGs with broad potential reach (authored by societies and government or nongovernment organizations), and appraised quality using the NEATS (vs AGREE II) instrument. Taken together, systematic reviews of CPG quality have identified that most CPGs were of low overall methodologic quality and tended to make recommendations that promoted more interventions as opposed to more effective interventions.

Instruments that appraise CPG quality provide stakeholders with a metric to evaluate and select the most rigorously developed CPGs with the goal of improving patient care, safety, and outcomes. The AGREE II checklist focuses on assessment of the quality and reporting of CPGs in 6 domains (scope and purpose, stakeholder involvement, rigor of development, clarity of presentation, applicability, and editorial independence) but does not address the clinical validity of CPG recommendations. By contrast, the 15-item NEATS instrument assesses adherence to NAM standards. The NEATS tool has been shown to have high interrater reliability (weighted κ = 0.73) and external validity.11 To ensure consistency and reliability of judgments, 2 trained personnel assess each CPG using the NEATS tool at the National Guideline Clearinghouse. Subsequently, these assessments are shared with CPG developers to enhance the accuracy and completeness of NEATS quality summaries. This feedback loop provides guideline developers with a benchmark to compare their processes against the NAM standards and an opportunity to clarify their methods.67 Several authors64,68 have noted that the additional rigor required to adhere to these standards may come at the cost of increased complexity, expertise, money, and time to CPG completion, most of which are in short supply during a pandemic. Future research is needed to compare appraisal tools, understand how to create CPGs that are ready for implementation, and aid stakeholders (clinicians, patients, and the public) to be informed CPG consumers.

Several strategies might enhance the development of trustworthy CPGs, even in the setting of a pandemic. First, CPG panels should include participation of a methodologic expert (eg, an epidemiologist, biostatistician, health services researcher). Their expertise adds to decisions regarding study design and the potential for bias and influence on study findings, methods to minimize bias in the conduct of systematic reviews, use of quantitative methods, conduct of qualitative synthesis, and issues related to data collection and management.11 Second, approaches that prioritize broad collaborations that engage multidisciplinary stakeholders who work together and share expertise and resources and are from at least 2 WHO regions may be optimal and lead to the production of fewer but higher-quality CPGs that are poised for updates as new evidence emerges. This approach could not only limit duplication of efforts but also limit publication of inconsistent recommendations. As opposed to de novo CPG development, local and regional groups should consider appraising and adapting existing high-quality CPGs to their practice context using the ADAPTE process.69 This 3-stage process includes start-up (assessment of skills and resources required), adaptation (selection of specific questions and CPG retrieval, quality assessment, selection, and compilation), and end stage (seeking opinions of decision makers affected by CPG, CPG revision, and finalization).69 Inherent to the ADAPTE process is access to CPGs and availability of local expertise in CPG appraisal. Adaptation to the clinical context is an important consideration, because most CPGs in our review were sponsored by societies with infrastructure and expertise and few were developed in low- and middle-income countries. Third, journal editors and peer reviewers should mandate use of 1 or more CPG appraisal tools at the time of manuscript submission to ensure publication of high-quality and trustworthy CPGs.

Strengths and Limitations

Our review has several strengths. Unlike prior reviews of COVID-19–related CPGs, we limited our review to pharmacologic treatments for hospitalized patients with COVID-19, included CPGs with broad potential reach (sponsored by societies and government or nongovernment organizations), and appraised CPG quality using the NEATS (vs AGREE II) instrument. To our knowledge, this is the first report to use the NEATS instrument to appraise CPG quality outside of the National Guideline Clearinghouse. We prioritized use of the NEATS tool because it had undergone rigorous development and testing and is aligned with NAM standards for trustworthy CPGs. We performed a comprehensive search and reviewed citations, abstracted data, and assessed quality in duplicate to limit ascertainment bias.

Our review also has some limitations. First, we limited our search to CPGs that were published in peer-reviewed journals. Second, we did not contact CPG authors to verify the methodologic aspects of their respective guidelines. Consequently, our assessment of methodologic expertise may be an underestimate, limited by reporting of this information in CPGs. Third, we did not have specific information pertaining to whether the included CPGs underwent peer review (regular, expedited, or absent) or were appraised using a quality checklist or other tool by authors at the time of submission. Notwithstanding, these points highlight the need for high publication standards even in the unique circumstances posed by a pandemic.

Conclusions

Few COVID-19 CPGs met NAM standards for trustworthy guidelines. Approaches that prioritize engagement of a methodologist and multidisciplinary collaborators from at least 2 WHO regions may lead to the production of fewer, high-quality CPGs that are poised for updates as new evidence emerges.

Back to top
Article Information

Accepted for Publication: September 14, 2021.

Published: December 10, 2021. doi:10.1001/jamanetworkopen.2021.36263

Open Access: This is an open access article distributed under the terms of the CC-BY License. © 2021 Burns KEA et al. JAMA Network Open.

Corresponding Author: Karen E. A. Burns, MD, MSc (Epid), Unity Health Toronto, St Michael’s Hospital, 30 Bond St, 4-045 Donnelly Wing, Toronto, Ontario, Canada M5B 1W8 (karen.burns@unityhealth.to).

Author Contributions: Dr Burns had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Concept and design: Burns, Laird, Stevenson, Kho, Friedrich, Meade, Duffett, Adhikari, Noh, Rochwerg.

Acquisition, analysis, or interpretation of data: Burns, Laird, Stevenson, Honarmand, Granton, Kho, Cook, Friedrich, Meade, Duffett, Chaudhuri, Liu, D’Aragon, Agarwal, Adhikari, Rochwerg.

Drafting of the manuscript: Burns, Laird, Stevenson, Noh.

Critical revision of the manuscript for important intellectual content: All authors.

Statistical analysis: Burns, Duffett, Liu, Rochwerg.

Administrative, technical, or material support: Burns, Laird, Stevenson, Cook, Friedrich, Chaudhuri, Agarwal, Rochwerg.

Supervision: Burns, Meade, Rochwerg.

Conflict of Interest Disclosures: Dr Burns reported holding a career award from the Physician Services Incorporated Foundation. Dr Kho reported receiving grants from Canada Research Chairs outside the submitted work. Dr Adhikari reported serving as chair for COVID-19 guideline panels convened by the World Health Organization. No other disclosures were reported.

Group Information: The Academy of Critical Care: Development, Evaluation, and Methodology (ACCADEMY) collaborators are listed in Supplement 2.

Additional Contributions: David Lightfoot, MISt, Unity Health Toronto, St Michael’s Hospital, assisted in conducting the literature searches. Mr Lightfoot did not receive remuneration for his assistance.

References
1.
Institute of Medicine.  Clinical Practice Guidelines We Can Trust. National Academies Press; 2011:1-300.
2.
Lohr  KN, Field  MJ. A provisional instrument for assessing clinical practice guidelines (Appendix B). In: Fields MJ, Lohr KN, eds.  Guidelines for Clinical Practice: From Development to Use. National Academies Press; 1992.
3.
Hayward  RS, Wilson  MC, Tunis  SR, Bass  EB, Rubin  HR, Haynes  RB.  More informative abstracts of articles describing clinical practice guidelines.   Ann Intern Med. 1993;118(9):731-737. doi:10.7326/0003-4819-118-9-199305010-00012 PubMedGoogle ScholarCrossref
4.
Liddle  J, Williamson  M, Irwig  L.  Method for Evaluating Research Guideline Evidence. New South Wales Health Department; 1996.
5.
Cluzeau  FA, Littlejohns  P, Grimshaw  JM, Feder  G, Moran  SE.  Development and application of a generic methodology to assess the quality of clinical guidelines.   Int J Qual Health Care. 1999;11(1):21-28. doi:10.1093/intqhc/11.1.21 PubMedGoogle ScholarCrossref
6.
Cluzeau  F, Burgers  J, Brouwers  M,  et al; AGREE Collaboration.  Development and validation of an international appraisal instrument for assessing the quality of clinical practice guidelines: the AGREE project.   Qual Saf Health Care. 2003;12(1):18-23. doi:10.1136/qhc.12.1.18 PubMedGoogle Scholar
7.
Fervers  B, Burgers  JS, Haugh  MC,  et al.  Predictors of high quality clinical practice guidelines: examples in oncology.   Int J Qual Health Care. 2005;17(2):123-132. doi:10.1093/intqhc/mzi011 PubMedGoogle ScholarCrossref
8.
Brouwers  MC, Kho  ME, Browman  GP,  et al; AGREE Next Steps Consortium.  AGREE II: advancing guideline development, reporting and evaluation in health care.   CMAJ. 2010;182(18):E839-E842. doi:10.1503/cmaj.090449 PubMedGoogle ScholarCrossref
9.
Brouwers  MC, Makarski  J, Kastner  M, Hayden  L, Bhattacharyya  O; GUIDE-M Research Team.  The Guideline Implementability Decision Excellence Model (GUIDE-M): a mixed methods approach to create an international resource to advance the practice guideline field.   Implement Sci. 2015;10:36. doi:10.1186/s13012-015-0225-1 PubMedGoogle ScholarCrossref
10.
Brouwers  MC, Spithoff  K, Kerkvliet  K,  et al.  Development and validation of a tool to assess the quality of clinical practice guideline recommendations.   JAMA Netw Open. 2020;3(5):e205535. doi:10.1001/jamanetworkopen.2020.5535 PubMedGoogle Scholar
11.
Jue  JJ, Cunningham  S, Lohr  K,  et al.  Developing and testing the Agency for Healthcare Research and Quality’s National Guideline Clearinghouse Extent of Adherence to Trustworthy Standards (NEATS) instrument.   Ann Intern Med. 2019;170(7):480-487. doi:10.7326/M18-2950 PubMedGoogle ScholarCrossref
12.
Dagens  A, Sigfrid  L, Cai  E,  et al.  Scope, quality, and inclusivity of clinical guidelines produced early in the COVID-19 pandemic: rapid review.   BMJ. 2020;369:m1936. doi:10.1136/bmj.m1936 PubMedGoogle Scholar
13.
Jin  YH, Cai  L, Cheng  ZS,  et al; Zhongnan Hospital of Wuhan University Novel Coronavirus Management and Research Team, Evidence-Based Medicine Chapter of China International Exchange and Promotive Association for Medical and Health Care (CPAM).  A rapid advice guideline for the diagnosis and treatment of 2019 novel coronavirus (2019-nCoV) infected pneumonia (standard version).   Mil Med Res. 2020;7(1):4. doi:10.1186/s40779-020-0233-6 PubMedGoogle Scholar
14.
National Health Commission of the People’s Republic of China.  Diagnostic and treatment protocol using traditional Chinese medicine.   Int J Acupuncture. 2020;14(1):7-12. doi:10.1016/j.acu.2020.04.002Google Scholar
15.
Alhazzani  W, Møller  MH, Arabi  YM,  et al.  Surviving sepsis campaign: guidelines on the management of critically ill adults with coronavirus disease 2019 (COVID-19).   Crit Care Med. 2020;48(6):e440-e469. doi:10.1097/CCM.0000000000004363 PubMedGoogle ScholarCrossref
16.
Thachil  J, Tang  N, Gando  S,  et al.  ISTH interim guidance on recognition and management of coagulopathy in COVID-19.   J Thromb Haemost. 2020;18(5):1023-1026. doi:10.1111/jth.14810 PubMedGoogle ScholarCrossref
17.
Flisiak  R, Horban  A, Jaroszewicz  J,  et al.  Management of SARS-CoV-2 infection: recommendations of the Polish Association of Epidemiologists and Infectiologists as of March 31, 2020.   Pol Arch Intern Med. 2020;130(4):352-357. doi:10.20452/pamw.15270PubMedGoogle Scholar
18.
Chawla  D, Chirla  D, Dalwai  S,  et al; Federation of Obstetric and Gynaecological Societies of India (FOGSI), National Neonatology Forum of India (NNF) and Indian Academy of Pediatrics (IAP).  Perinatal-neonatal management of COVID-19 infection: guidelines of the Federation of Obstetric and Gynaecological Societies of India (FOGSI), National Neonatology Forum of India (NNF), and Indian Academy of Pediatrics (IAP).   Indian Pediatr. 2020;57(6):536-548. doi:10.1007/s13312-020-1852-4 PubMedGoogle ScholarCrossref
19.
Mehta  Y, Chaudhry  D, Abraham  OC,  et al.  Critical care for COVID-19 affected patients: position statement of the Indian Society of Critical Care Medicine.   Indian J Crit Care Med. 2020;24(4):222-241. doi:10.5005/jp-journals-10071-23395 PubMedGoogle Scholar
20.
Zhai  Z, Li  C, Chen  Y,  et al; Prevention Treatment of VTE Associated with COVID-19 Infection Consensus Statement Group.  Prevention and treatment of venous thromboembolism associated with coronavirus disease 2019 infection: a consensus statement before guidelines.   Thromb Haemost. 2020;120(6):937-948. doi:10.1055/s-0040-1710019 PubMedGoogle ScholarCrossref
21.
Rajagopal  K, Keller  SP, Akkanti  B,  et al.  Advanced pulmonary and cardiac support of COVID-19 patients: emerging recommendations from ASAIOa living working document.   Circ Heart Fail. 2020;13(5):e007175. doi:10.1161/CIRCHEARTFAILURE.120.007175 PubMedGoogle Scholar
22.
Ramírez  I, De la Viuda  E, Baquedano  L,  et al.  Managing thromboembolic risk with menopausal hormone therapy and hormonal contraception in the COVID-19 pandemic: recommendations from the Spanish Menopause Society, Sociedad Española de Ginecología y Obstetricia and Sociedad Española de Trombosis y Hemostasia.   Maturitas. 2020;137:57-62. doi:10.1016/j.maturitas.2020.04.019 PubMedGoogle ScholarCrossref
23.
Reiter  RJ, Abreu-Gonzalez  P, Marik  PE, Dominguez-Rodriguez  A.  Therapeutic algorithm for use of melatonin in patients with COVID-19.   Front Med (Lausanne). 2020;7:226. doi:10.3389/fmed.2020.00226 PubMedGoogle ScholarCrossref
24.
Barnes  GD, Burnett  A, Allen  A,  et al.  Thromboembolism and anticoagulant therapy during the COVID-19 pandemic: interim clinical guidance from the anticoagulation forum.   J Thromb Thrombolysis. 2020;50(1):72-81. doi:10.1007/s11239-020-02138-z PubMedGoogle ScholarCrossref
25.
Llau  JV, Ferrandis  R, Sierra  P,  et al.  SEDAR-SEMICYUC consensus recommendations on the management of haemostasis disorders in severely ill patients with COVID-19 infection.   Rev Esp Anestesiol Reanim (Engl Ed). 2020;67(7):391-399. doi:10.1016/j.redar.2020.05.007 PubMedGoogle ScholarCrossref
26.
Lombardy Section Italian Society Infectious and Tropical Diseases.  Vademecum for the treatment of people with COVID-19. Edition 2.0, 13 March 2020.   Infez Med. 2020;28(2):143-152.PubMedGoogle Scholar
27.
Moores  LK, Tritschler  T, Brosnahan  S,  et al.  Prevention, diagnosis, and treatment of VTE in patients with coronavirus disease 2019: CHEST Guideline and Expert Panel Report.   Chest. 2020;158(3):1143-1163. doi:10.1016/j.chest.2020.05.559 PubMedGoogle ScholarCrossref
28.
Flisiak  R, Horban  A, Jaroszewicz  J,  et al.  Management of SARS-CoV-2 infection: recommendations of the Polish Association of Epidemiologists and Infectiologists: annex No. 1 as of June 8, 2020.   Pol Arch Intern Med. 2020;130(6):557-558. doi:10.20452/pamw.15424PubMedGoogle Scholar
29.
Kosior  DA, Undas  A, Kopeć  G,  et al.  Guidance for anticoagulation management in venous thromboembolism during the coronavirus disease 2019 pandemic in Poland: an expert opinion of the Section on Pulmonary Circulation of the Polish Cardiac Society.   Kardiol Pol. 2020;78(6):642-646. doi:10.33963/KP.15425PubMedGoogle ScholarCrossref
30.
Li  YH, Wang  MT, Huang  WC, Hwang  JJ.  Management of acute coronary syndrome in patients with suspected or confirmed coronavirus disease 2019: consensus from Taiwan Society of Cardiology.   J Formos Med Assoc. 2021;120(1 Pt 1):78-82. doi:10.1016/j.jfma.2020.07.017 PubMedGoogle Scholar
31.
Henderson  LA, Canna  SW, Friedman  KG,  et al.  American College of Rheumatology clinical guidance for multisystem inflammatory syndrome in children associated with SARS-CoV-2 and hyperinflammation in pediatric COVID-19: version 1.   Arthritis Rheumatol. 2020;72(11):1791-1805. doi:10.1002/art.41454 PubMedGoogle ScholarCrossref
32.
Rochwerg  B, Agarwal  A, Zeng  L,  et al.  Remdesivir for severe COVID-19: a clinical practice guideline.   BMJ. 2020;370:m2924. doi:10.1136/bmj.m2924 PubMedGoogle Scholar
33.
Goldenberg  NA, Sochet  A, Albisetti  M,  et al; Pediatric/Neonatal Hemostasis and Thrombosis Subcommittee of the ISTH SSC.  Consensus-based clinical recommendations and research priorities for anticoagulant thromboprophylaxis in children hospitalized for COVID-19-related illness.   J Thromb Haemost. 2020;18(11):3099-3105. doi:10.1111/jth.15073 PubMedGoogle ScholarCrossref
34.
Jin  YH, Zhan  QY, Peng  ZY,  et al; Evidence-Based Medicine Chapter of China International Exchange and Promotive Association for Medical and Health Care (CPAM); Chinese Research Hospital Association (CRHA).  Chemoprophylaxis, diagnosis, treatments, and discharge management of COVID-19: an evidence-based clinical practice guideline (updated version).   Mil Med Res. 2020;7(1):41. doi:10.1186/s40779-020-00270-8PubMedGoogle Scholar
35.
Ferreira  LL, Sampaio  DL, Chagas  ACP,  et al.  AMB guidelines: COVID-19. Rev Assoc Med Bras 2020.   Rev. Assoc. Med. Bras. 2020;66(suppl 2):17-21. doi:10.1590/1806-9282.66.S2.17Google ScholarCrossref
36.
Chekkal  M, Deba  T, Hadjali  S,  et al.  Prevention and treatment of COVID-19-associated hypercoagulability: recommendations of the Algerian Society of Transfusion and Hemobiology.   Transfus Clin Biol. 2020;27(4):203-206. doi:10.1016/j.tracli.2020.09.004 PubMedGoogle ScholarCrossref
37.
Flisiak  R, Parczewski  M, Horban  A,  et al.  Management of SARS-CoV-2 infection: recommendations of the Polish Association of Epidemiologists and Infectiologists. Annex no. 2 as of October 13, 2020.   Pol Arch Intern Med. 2020;130(10):915-918. doi:10.20452/pamw.15658 PubMedGoogle ScholarCrossref
38.
Abu-Raya  B, Migliori  GB, O’Ryan  M,  et al.  Coronavirus disease-19: an interim evidence synthesis of the World Association for Infectious Diseases and Immunological Disorders (WAIDID).   Front Med (Lausanne). 2020;7:572485. doi:10.3389/fmed.2020.572485 PubMedGoogle Scholar
39.
Mehta  Y, Chaudhry  D, Abraham  OC,  et al.  Critical care for COVID-19 affected patients: updated position statement of the Indian Society of Critical Care Medicine.   Indian J Crit Care Med. 2020;24(suppl 5):S225-S230. doi:10.5005/jp-journals-10071-23621 PubMedGoogle Scholar
40.
Foti  G, Giannini  A, Bottino  N,  et al; COVID-19 Lombardy ICU Network.  Management of critically ill patients with COVID-19: suggestions and instructions from the coordination of intensive care units of Lombardy.   Minerva Anestesiol. 2020;86(11):1234-1245. doi:10.23736/S0375-9393.20.14762-X PubMedGoogle ScholarCrossref
41.
Andrejak  C, Cottin  V, Crestani  B,  et al.  Guide for the management of patients with respiratory sequelae after a SARS-CoV-2 pneumonia: support proposals developed by the French-language Respiratory Medicine Society: version of 10 November 2020  [in French].  Rev Mal Respir. 2021;38(1):114-121. doi:10.1016/j.rmr.2020.11.009 PubMedGoogle ScholarCrossref
42.
Berlit  P, Bösel  J, Gahn  G,  et al.  “Neurological manifestations of COVID-19”—guideline of the German Society of Neurology.   Neurol Res Pract. 2020;2:51. doi:10.1186/s42466-020-00097-7 PubMedGoogle ScholarCrossref
43.
Henderson  LA, Canna  SW, Friedman  KG,  et al.  American College of Rheumatology clinical guidance for multisystem inflammatory syndrome in children associated with SARS-CoV-2 and hyperinflammation in pediatric COVID-19: version 2.   Arthritis Rheumatol. 2021;73(4):e13-e29. doi:10.1002/art.41616 PubMedGoogle ScholarCrossref
44.
Rochwerg  B, Agarwal  A, Siemieniuk  RA,  et al.  A living WHO guideline on drugs for COVID-19.   BMJ. 2020;370:m3379. doi:10.1136/bmj.m3379 PubMedGoogle Scholar
45.
Chen  X, Liu  Y, Gong  Y,  et al; Chinese Society of Anesthesiology, Chinese Association of Anesthesiologists.  Perioperative management of patients infected with the novel coronavirus: recommendation from the Joint Task Force of the Chinese Society of Anesthesiology and the Chinese Association of Anesthesiologists.   Anesthesiology. 2020;132(6):1307-1316. doi:10.1097/ALN.0000000000003301 PubMedGoogle ScholarCrossref
46.
Andrejak  C, Blanc  FX, Costes  F,  et al.  Guide for follow-up of patients with SARS-CoV-2 pneumonia: management proposals developed by the French-language Respiratory Medicine Society. Version of 10 May 2020  [in French].  Rev Mal Respir. 2020;37(6):505-510. doi:10.1016/j.rmr.2020.05.001 PubMedGoogle ScholarCrossref
47.
Donders  F, Lonnée-Hoffmann  R, Tsiakalos  A,  et al; Isidog Covid-Guideline Workgroup.  ISIDOG COVID-Guideline Workgroup. ISIDOG recommendations concerning COVID-19 and pregnancy.   Diagnostics (Basel). 2020;10(4):243. doi:10.3390/diagnostics10040243PubMedGoogle ScholarCrossref
48.
Tan  SHS, Hong  CC, Saha  S, Murphy  D, Hui  JH.  Medications in COVID-19 patients: summarizing the current literature from an orthopaedic perspective.   Int Orthop. 2020;44(8):1599-1603. doi:10.1007/s00264-020-04643-5 PubMedGoogle ScholarCrossref
49.
Zhang  Y, Coats  AJS, Zheng  Z,  et al.  Management of heart failure patients with COVID-19: a joint position paper of the Chinese Heart Failure Association & National Heart Failure Committee and the Heart Failure Association of the European Society of Cardiology.   Eur J Heart Fail. 2020;22(6):941-956. doi:10.1002/ejhf.1915 PubMedGoogle ScholarCrossref
50.
Solé  G, Salort-Campana  E, Pereon  Y,  et al; FILNEMUS COVID-19 study group.  Guidance for the care of neuromuscular patients during the COVID-19 pandemic outbreak from the French Rare Health Care for Neuromuscular Diseases Network.   Rev Neurol (Paris). 2020;176(6):507-515. doi:10.1016/j.neurol.2020.04.004 PubMedGoogle ScholarCrossref
51.
Cardenas  MC, Bustos  SS, Enninga  EAL, Mofenson  L, Chakraborty  R.  Characterising and managing paediatric SARSCoV-2 infection: learning about the virus in a global classroom.   Acta Paediatr. 2021;110(2):409-422. doi:10.1111/apa.15662 PubMedGoogle ScholarCrossref
52.
Miklowski  M, Jansen  B, Auron  M, Whinney  C.  The hospitalized patient with COVID-19 on the medical ward: Cleveland Clinic approach to management.   Cleve Clin J Med. Published online November 3, 2020. doi:10.3949/ccjm.87a.ccc064PubMedGoogle Scholar
53.
Yang  X, Liu  Y, Liu  Y,  et al.  Medication therapy strategies for the coronavirus disease 2019 (COVID-19): recent progress and challenges.   Expert Rev Clin Pharmacol. 2020;13(9):957-975. doi:10.1080/17512433.2020.1805315 PubMedGoogle ScholarCrossref
54.
Baller  EB, Hogan  CS, Fusunyan  MA,  et al.  Neurocovid: pharmacological recommendations for delirium associated with COVID-19.   Psychosomatics. 2020;61(6):585-596. doi:10.1016/j.psym.2020.05.013 PubMedGoogle ScholarCrossref
55.
Fang  F, Chen  Y, Zhao  D,  et al; Chinese Pediatric Society and the Editorial Committee of the Chinese Journal of Pediatrics.  Recommendations for the diagnosis, prevention, and control of coronavirus disease-19 in children: the Chinese perspectives.   Front Pediatr. 2020;8:553394. doi:10.3389/fped.2020.553394 PubMedGoogle Scholar
56.
Dobesh  PP, Trujillo  TC.  Coagulopathy, venous thromboembolism, and anticoagulation in patients with COVID-19.   Pharmacotherapy. 2020;40(11):1130-1151. doi:10.1002/phar.2465 PubMedGoogle ScholarCrossref
57.
Kronbichler  A, Effenberger  M, Eisenhut  M, Lee  KH, Shin  JI.  Seven recommendations to rescue the patients and reduce the mortality from COVID-19 infection: an immunological point of view.   Autoimmun Rev. 2020;19(7):102570. doi:10.1016/j.autrev.2020.102570 PubMedGoogle Scholar
58.
Ferreira  LL, Sampaio  DL, Chagas  ACP,  et al.  AMB guidelines: COVID 19. Rev Assoc Med Bras 2020.  2020;66(9):1179. doi:10.1590/1806-9282.66.9.1179.
59.
Aguilar  RB, Hardigan  P, Mayi  B,  et al.  Current understanding of COVID-19 clinical course and investigational treatments.   Front Med (Lausanne). 2020;7:555301. doi:10.3389/fmed.2020.555301 PubMedGoogle Scholar
60.
Costa  A, Weinstein  ES, Sahoo  DR, Thompson  SC, Faccincani  R, Ragazzoni  L.  How to build the plane while flying: VTE/PE thromboprophylaxis clinical guidelines for COVID-19 patients.   Disaster Med Public Health Prep. 2020;14(3):391-405. doi:10.1017/dmp.2020.195 PubMedGoogle ScholarCrossref
61.
Danthuluri  V, Grant  MB.  Update and recommendations for ocular manifestations of COVID-19 in adults and children: a narrative review.   Ophthalmol Ther. 2020;9(4):853-875. doi:10.1007/s40123-020-00310-5 PubMedGoogle ScholarCrossref
62.
Chivukula  RR, Maley  JH, Dudzinski  DM, Hibbert  K, Hardin  CC.  Evidence-based management of the critically ill adult with SARS-CoV-2 infection.   J Intensive Care Med. 2021;36(1):18-41. doi:10.1177/0885066620969132 PubMedGoogle ScholarCrossref
63.
World Health Organization. Clinical management of severe acute respiratory infection (SARI) when COVID-19 is suspected: interim guidance. March 13, 2020. Accessed April 24, 2021. https://apps.who.int/iris/handle/10665/331446
64.
Stamm  TA, Andrews  MR, Mosor  E,  et al.  The methodological quality is insufficient in clinical practice guidelines in the context of COVID-19: systematic review.   J Clin Epidemiol. 2021;135:125-135. doi:10.1016/j.jclinepi.2021.03.005 PubMedGoogle ScholarCrossref
65.
Kung  J, Miller  RR, Mackowiak  PA.  Failure of clinical practice guidelines to meet institute of medicine standards: two more decades of little, if any, progress.   Arch Intern Med. 2012;172(21):1628-1633. doi:10.1001/2013.jamainternmed.56 PubMedGoogle ScholarCrossref
66.
Reames  BN, Krell  RW, Ponto  SN, Wong  SL.  Critical evaluation of oncology clinical practice guidelines.   J Clin Oncol. 2013;31(20):2563-2568. doi:10.1200/JCO.2012.46.8371 PubMedGoogle ScholarCrossref
67.
Emergency Care Research Institute. US Agency for Healthcare Research and Quality launches new clinical guideline assessment tool through contract to ECRI Institute. November 16, 2017. Accessed April 24, 2021. https://www.ecri.org/press/ahrq-clinical-guideline-assessment-tool
68.
Brouwers  MC, Spithoff  K, Lavis  J, Kho  ME, Makarski  J, Florez  ID.  What to do with all the AGREEs? the AGREE portfolio of tools to support the guideline enterprise.   J Clin Epidemiol. 2020;125:191-197. doi:10.1016/j.jclinepi.2020.05.025 PubMedGoogle ScholarCrossref
69.
Fervers  B, Burgers  JS, Voellinger  R,  et al.  ADAPTE Collaboration. Guideline adaptation: an approach to enhance efficiency in guideline development and improve utilization.   BMJ Qual Saf. 2011;20(3):228-236. doi:10.1136/bmjqs.2010.043257PubMedGoogle ScholarCrossref
×