key: cord-1001029-shqu8z6n
authors: Zhou, Qi; Li, Qinyuan; Estill, Janne; Wang, Qi; Wang, Zijun; Shi, Qianling; Zhang, Jingyi; Zhang, Xiaobo; Mathew, Joseph L.; Smyth, Rosalind L.; Nurdiati, Detty; Fu, Zhou; Xu, Hongmei; Zheng, Xianlan; Zhao, Xiaodong; Lu, Quan; Liu, Hui; Xun, Yangqin; Li, Weiguo; Yang, Shu; Feng, Xixi; Wang, Mengshu; Lei, Junqiang; Luo, Xiaoping; Wu, Liqun; Lu, Xiaoxia; Lee, Myeong Soo; Zhao, Shunying; Chan, Edwin Shih-Yen; Qian, Yuan; Tu, Wenwei; Dong, Xiaoyan; Li, Guobao; Zhao, Ruiqiu; He, Zhihui; Zhao, Siya; Liu, Xiao; Li, Qiu; Yang, Kehu; Luo, Zhengxiu; Liu, Enmei; Chen, Yaolong
title: Methodology and experiences of rapid advice guideline development for children with COVID-19: responding to the COVID-19 outbreak quickly and efficiently
date: 2022-04-03
journal: BMC Med Res Methodol
DOI: 10.1186/s12874-022-01545-5
sha: fee1db049f0b0523e5e4a6b5b7eea6f08f65c375
doc_id: 1001029
cord_uid: shqu8z6n

BACKGROUND: Rapid Advice Guidelines (RAG) provide decision makers with guidance to respond to public health emergencies by developing evidence-based recommendations in a short period of time with a scientific and standardized approach. However, the experience from the development process of a RAG has so far not been systematically summarized. Therefore, our working group will take the experience of the development of the RAG for children with COVID-19 as an example to systematically explore the methodology, advantages, and challenges in the development of the RAG. We shall propose suggestions and reflections for future research, in order to provide a more detailed reference for future development of RAGs. RESULT: The development of the RAG by a group of 67 researchers from 11 countries took 50 days from the official commencement of the work (January 28, 2020) to submission (March 17, 2020). A total of 21 meetings were held with a total duration of 48 h (average 2.3 h per meeting) and an average of 16.5 participants attending. Only two of the ten recommendations were fully supported by direct evidence for COVID-19, three recommendations were supported by indirect evidence only, and the proportion of COVID-19 studies among the body of evidence in the remaining five recommendations ranged between 10 and 83%. Six of the ten recommendations used COVID-19 preprints as evidence support, and up to 50% of the studies with direct evidence on COVID-19 were preprints. CONCLUSIONS: In order to respond to public health emergencies, the development of RAG also requires a clear and transparent formulation process, usually using a large amount of indirect and non-peer-reviewed evidence to support the formation of recommendations. Strict following of the WHO RAG handbook does not only enhance the transparency and clarity of the guideline, but also can speed up the guideline development process, thereby saving time and labor costs. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12874-022-01545-5.

According to the World Health Organization (WHO), standard clinical practice guidelines (hereafter referred to as "standard guidelines") must be developed clearly and transparently following a rigorous methodology to obtain unbiased and high-quality recommendations and minimize the influence of conflicts of interest. The development of standard guidelines however will require on average about six months to two years to complete [1, 2] . Due to time constraints and the enormous input needed, developing standard guidelines is not the best way to assist decision-makers to rapidly make evidencebased decisions in a short period of time in case of public health emergencies. Thus, in 2006, the WHO introduced the concept and methodology of rapid advice guideline (RAG), which is characterized by short, scientific and standardized way of development. RAG aims to respond to potential public health emergencies or urgencies [3] . RAG has been proven successful with applications in several infectious diseases such as H5N1, HIV, and Ebola [4] [5] [6] .

Since December 2019, a novel infectious disease (COVID-19) caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection has swept through the world, posing significant challenges to public health safety and healthcare delivery systems worldwide [7] . In such public health emergencies, guideline developers face great challenges in making urgent reasonable recommendations. Therefore, the development of a RAG is one of the effective ways to address this issue [1, 2, 8, 9] . On January 28, 2020, the development of the first international rapid advice guideline for management of children with COVID-19 (hereinafter referred to as the "RAG for children with COVID-19"), following the WHO RAG methodology and led by the National Clinical Research Center for Child Health and Disorders, was launched. RAG for children with COVID-19 was initiated by the contributions of the WHO Collaborating Center for Guideline Implementation and Knowledge Translation. It took three months from approving RAG to its publication [10, 11] . This guideline focuses on the management of children younger than 18 years infected with SARS-CoV-2, and covers screening, diagnosis, treatment, and patient education. The guideline has so far been translated into 20 languages and accepted into the Guidelines International Network library [12] . Based on the practical experience from the "RAG for children with COVID-19", the aim of this article is to summarize the methodological processes and experiences in the development of the RAG, and provides suggestions and reflections on the future development of RAGs.

The WHO suggests to consider five factors when deciding to develop a RAG rather than standard guideline, or to delay the development of guideline. If all these five aspects are met, the development of a RAG is considered necessary. Therefore, prior to the official launch of the RAG for children with COVID-19, the core members (CMs: Liu E, Smyth RL, Chen Y, Luo Z, Li W, Zhou Q and Ren L) of the RAG working group assessed the need and rationale for the development of the RAG for children with COVID-19 based on these five aspects suggested by the WHO [1] . Having found that all five criteria were met, they concluded that it was necessary to develop a RAG for children with COVID-19 ( Table 1) .

There are currently more than 60 manuals for the development of standard guidelines, including manuals issued by the Institute of Medicine (IOM), Canadian Medical Association (CMA), Scottish Intercollegiate Guidelines Network (SIGN), World Health Organization (WHO), American College of Physicians (ACP), and National Institute for Health and Care Excellence (NICE) [1, [26] [27] [28] [29] [30] . It generally takes one to two years to develop a standard guideline by following the methodology of these manuals [1, 26] . In response to public health emergencies, we need manuals that can shorten the time of guideline development. The GIN-McMaster guideline development checklist and the WHO RAG development handbook can help guideline developers complete a guideline in a short time [3, [31] [32] [33] . We compared the two manuals and finally chose the WHO RAG handbook 

Whether the public health event is an emergency or dangerous situation 1). Emergencies may be classified as natural, technological, or conflict related and may be of sudden onset (e.g., earthquakes, tsunamis, chemical crises) or more gradual onset (e.g., deteriorating situations in armed conflict, progressive disease outbreaks, drought, or food insecurities)

2). Using the rapid risk assessment of acute public health events manual to assess ''any outbreak or other rapidly evolving situation that may have negative consequences for human health and requires immediate assessment and action'' [13] .

On January 26, the WHO raised the global risk of the epidemic to "high risk" for the first time, with 2014 cases confirmed in 11 countries in the Americas, Oceania, Asia and Europe [14] Whether the public health event is novel 1). A new public health event (e.g., emerging infectious disease) or an event encountered previously but causing problems in a different context 2). If the contingency is not the first of its kind and relevant high-quality guideline already exists, it can be adopted directly or adapted to quickly address the health concern. (e.g., Ebola outbreak in the Democratic Republic of the Congo again in 2019, but by this time high-quality Ebola guidelines have been published, so there is no need to develop rapid advice guidelines for Ebola [15, 16] .)

On January 26, nucleic acid testing of the virus by Chinese researchers had revealed that the disease was caused by a novel coronavirus, that it was an outbreak of a new public health threat, and that there were no high-quality guidelines for children with this condition published at this time [17, 18] Duration of the public health event The purpose of the RAG is to provide urgently needed evidence-based recommendations that should be implemented within one to three months, and if an event is likely to last more than six months, then a standard guide may be the best approach

The global SARS outbreak lasted almost 8 months from the first case to the complete eradication, the MERS outbreak has lasted 5 years, and SARS-CoV-2 belongs to the same coronavirus genus as SARS-CoV and MERS-CoV. COVID-19 epidemic can also be expected to last for some time, so it is feasible to develop rapid advice guidelines within 1 to 3 months of the outbreak [19] The need to urgently address the problem of uncertainty In the event of a public health emergency, there is significant controversy among health care professionals about certain issues or aspects that need to be resolved in the short term. (e.g., the use of glucocorticoids in the treatment of COVID 

Whether it can be rapidly and widely implemented Before developing RAGs, it is important to consider the various factors involved in their implementation, such as the breadth and acceptability of the target population, their integration into national health policy systems, and their rapid implementation Yes SARS-CoV-2 is highly contagious and the entire population is susceptible. The total number of children in the world stands at 2 billion, and children, as a vulnerable group, are of great concern [23, 24] . In addition, countries threatened by the epidemic have elevated the prevention and control of COVID-19 to the highest national priority and have promulgated various health policies to prevent and control the disease [25] , so that COVID- [37, 38] ; and 3) children, especially those under 6 years of age, are also not necessarily able to express themselves clearly enough [39] . The PRs were involved in the voting process for recommendations and providing feedback on the full text of the guideline.

To ensure clarity and transparency in the development of the RAG, all participants were required to declare any potential conflicts of interest that may be relevant to the RAG [40, 41] . One CM (Li W) collected the conflicts of interest declaration forms among all members participating in the development of the RAG through email. Participants were required to declare any financial, professional and other interests that may be related to the RAG. The declared conflict of interests was reviewed by the CMs (Liu E, Chen Y, Li W, Zhou Q). Based on the assessment of conflict of interests, we limited the participation of experts with potential conflict of interests in the core work or excluded them from the overall development of the guideline. All disclosures and conflicts of interest management decisions have been publicly reported [42, 43] .

The RAG was registered on the International Practice Guidelines Registry Platform (registration No. IPGRP-2020CN008). The protocol was published on March 26 of 2020 [11] .

Four CMs (Liu E, Chen Y, Li W, Zhou Q) conducted a scoping review of the published literatures related to COVID-19, and developed the initial clinical questions related to children with COVID-19 [44] . After two rounds of discussions among three CMs (Liu E, Smyth RL, Li W) and clinical experts working in the frontline of infectious disease prevention, 26 clinical questions were identified for further assessment of their importance ( Table 2) . On February 2, 2020, one CM (Li W) sent a clinical questionnaire to 33 GDG members by email. All experts scored each question from 1 to 7 according to its importance (1: the question is not important at all and should not be included in the guideline; 7: the question is extremely important and must be included in the guideline). Twenty-seven (81.8%) of the invited 33 GDG members completed the questionnaire. On February 7, 2020, two CMs (Li W, Zhou Q) prioritized the clinical questions according to the questionnaire scores and modified the questions based on the feedback from the GDG. After considering the score ranking and discussing the feedback, six CMs (Liu E, Smyth RL, Chen Y, Luo Z, Li W, Zhou Q) reached an agreement and included ten clinical questions (Table 2) . and their synonyms, as well as terms related to specific the topic of each review. We developed the search strategy in cooperation with an experienced medical information retrieval specialist [5, 56] . The first searches were completed on 28 February 2020. Later, due to the length of the development process of the RAG, the searches were updated on March 31, 2020. In addition, the RRG also manually searched SSRN (https:// www. ssrn. com/ index. cfm/ en/), medRxiv (https:// www. medrx iv. org/) and bioRxiv (https:// www. biorx iv. org/) preprint platforms and Google Scholar, and tracked references of the included studies.

Since another high-quality rapid review on the same topic was published, the rapid review on quarantine to control COVID-19 was discontinued on 8 April 2020 [45, 57] . Finally, the RRG completed 13 rapid reviews (see Additional file 2). The GRADE method was used to grade the evidence from the results of the rapid reviews [45, 58] . The detailed grading results were reported in the published articles. The questions and supporting evidence from the rapid reviews is shown in Table 3 .

Based on the ten clinical questions and supporting evidence from rapid reviews, six CMs (Liu E, Smyth RL, Chen Y, Luo Z, Zhou Q, Li W) initially drafted ten recommendations. The relevant materials and questionnaires were sent to the GDG members by email in electronic format, and also to the two children's guardians in paper versions. The preferences and values of the two children's guardians and clinical experts were consistent. Two rounds of Delphi survey were conducted on February 24, 2020 and February 28, 2020, respectively, and we voted on the recommendations. The consensus criterion was that at least 70% of the invited panelists agreeing on the recommendation [45, 60] . After each round of Delphi survey, the core group discussed the feedback, revised the recommendations and also disclosed the feedback to the panel members before the next round. Detailed expert feedback can be found in Additional file 3.

A total of nine recommendations reached consensus in the first round of Delphi survey, leaving only one recommendation to be determined (Recommendation #3: CT scan should not be used routinely in the diagnosis of COVID-19 in children, although it may be helpful in monitoring children who develop severe respiratory symptoms). Six CMs (Liu E, Smyth RL, Luo Z, Chen Y, Zhou Q, Li W) revised the wording and rationale of the recommendations based on the first round of Delphi survey. Afterwards, a second round of Delphi survey was conducted for two recommendations: recommendation #3 for which consensus was not reached in the first round, and recommendation #6 (Recommendation #6: systemic glucocorticoids should not be used routinely for children with COVID-19. Only low-dose and short-duration systemic glucocorticoid therapy can be used for children with severe COVID-19 in the context of clinical trials). The recommendation was divided into two sub-recommendations (a. We recommend against using systemic glucocorticoids for children with COVID-19 routinely; b. We suggest a low dose and a short duration for severe COVID-19 children only when over inflammatory reaction or in the context of clinical trials) after feedback from the first round. Consensus were reached for both recommendations, resulting in a total of ten recommendations being finally included in the RAG. The panelists made a total of 181 comments during the two rounds of Delphi survey ( Table 4) .

According to the Reporting Items for Practice Guidelines in Healthcare (RIGHT) reporting checklist, the RAG development process, clinical questions, recommendations, evidence summary and research gaps, two CMs (Zhou Q, Li W) drafted the first version of the RAG [45, 61] . Four other CMs (Liu E, Luo Z, Smyth RL, Chen Y) made secondary revisions to the content and expression. The revised version of the RAG was reviewed by four invited experts. We selected the external reviewers to ensure a balanced representation of different specialties (one external reviewer was specialized in health policy and guideline methodology, two in pediatric respiratory medicine, and one in pulmonary and critical care medicine), 2geographical regions (one reviewer from the WHO, UK, Chinese mainland and Hong Kong, China 2)We recommend parents to obtain information from print media, authorities and official agencies rather than social media(1D)

3)We recommend parents to provide their children with suitable health education to improve the awareness on infectious diseases and teach their children not to discriminate people from areas affected by the epidemic 1D) 94% (Consensus) 8 14 We recommend parents to obtain information regularly from academic and official resources rather than social media. (1D) each) and genders (one female, three male). All external experts were requested to complete a conflicts of interest form, to identify any factual errors and to comment on the clarity of the language and contextual issues. Finally, the core members discussed and revised the guidelines based on the external reviewers' comments.

In summary, the development of the RAG by a group of 67 researchers from 11 countries took 50 days from the official commencement of the work (January 28, 2020) to submission (March 17, 2020) . The process took another 50 days from submission to acceptance, resulting in a total duration of 100 days (Table 5 ). In addition, to ensure real-time communication, the development of the RAG was intensively discussed in online meetings almost every week from February 1st to March 7th. A total of 21 meetings between the CM and the RRG were held throughout the RAG development process with a total duration of 48 h (average 2.3 h per meeting) and an average of 16.5 participants attending (Table 6 ).

We have translated this guideline into the following 20 languages: English, Chinese, Japanese, Russian, German, French, Italian, Vietnamese, Thai, Spanish, Arabic, Portuguese, Polish, Czech, Romanian, Burmese, Hungarian, Hebrew, Hindi, Turkish and Malay. The guideline is indexed in the International Practice Guidelines Registry Platform (IPGRP, http:// www. guide lines-regis try. org/ news/ 141), the Guidelines International Network (GIN, https://g-i-n. net/ get-invol ved/ resou rces/), and the Emergency Care Research Institute (ECRI, https:// guide lines. ecri. org/ profi le/ 1868) databases. In addition, we contacted the editor-in-chief in advance and discussed publication strategies to ensure a rapid publication (e.g., taking the fast track option, and fast recruitment of peerreviewers). Considering the differences in health policies and systems, resources, feasibility and equity across the countries, through above strategies, we will assist countries and regions to adopt or adapt the guidelines into their local context.

There is still a lack of effective manuals on how to update the RAG to the standard guideline. Therefore, our working group has proposed the following update plan: 1) According to the WHO guideline handbook [1] , when a public health event lasts longer than six months, it should be considered to develop a standard version of the guidelines, and we therefore will update the RAG; 2) The evidence evaluation group will continuously monitor Table 5 Actual versus planned completion time of the development of RAG NA Not Applicable a Production of a rapid review in two phases: phases I (Feb 11-Feb 1), just completed the evidence summary sheet; phases II (Feb 16-Apr 14), drafted rapid reviews full-text and submit to journal

Start to work Jan 28-Jan 28 (One day) Jan 28-Jan 28 (One day) 0

Write protocol Jan 29-Jan 29 (One day) Jan 29-Feb 3 (Six days) 5

Invite panelists Jan 30-Feb 2 (Four days) Jan 29-Feb 3 (Six days) 2

Declare conflicts of interests Jan 30-Feb 2 (Four days) Jan 30-Feb 5 (Four days) 0 [62]; 4) We will invite new clinical experts and methodologists to participate in the updating of the guideline if necessary; 5) We will monitor the updating of existing RAG on COVID-19 and use their experience to guide the updating of our guideline; and 6) The updated guideline will be reported in accordance with the CheckUp checklist [63] .

As shown in Table 5 , it took 50 days to complete the entire development process of the RAG from launch of the guideline to submission to a medical journal. This was 20 days longer than the planned schedule (one month). Two weeks of this time was spent on the identification of clinical questions (proposing clinical questions, selecting the initial clinical questions, prioritizing questions, and formatting them in PICO format). Because COVID-19 is an emerging infectious disease that was poorly understood in children and even adults when this work was started, it was extremely challenging to select the top ten clinical questions at the beginning of the development of the RAG. First, there was a severe paucity of literature in children on COVID-19 at that time. Second, the limited number of pediatric cases were all contacts of infected adults, and the transmission routes and dynamics among the children themselves or through other sources (e.g. contaminated surfaces) were unknown. Third, the RAG development groups had no frontline clinicians with relevant clinical experience of the natural history of the disease. Fourth, as an international RAG, the clinical questions needed to be applicable to a wide and heterogeneous target population around the world. The health systems and policies of each country need to be taken into consideration in the process of identifying clinical issues, and the importance of clinical issues vary from country to country. For example, during the survey of clinical questions, the experts proposed the question "who should be tested for nucleic acid at the beginning of an outbreak?". Health policies in some countries have been very clear on this issue (China's policy is to provide free nucleic acid testing to all persons who show clinical signs and have had close contact with a confirmed case [64] ). But in most countries, only a limited number of people could be tested in the early stages of the pandemic because of the lack of nucleic acid testing kits.

The RAG was supported by 13 rapid reviews that incorporated evidence from studies of COVID-19, SARS and MERS. Table 3 shows only two of the ten recommendations were fully supported by direct evidence for COVID-19, three recommendations were supported by indirect evidence only, and the proportion of COVID-19 studies among the body of evidence in the remaining five recommendations ranged between 10 and 83%. Moreover, only one of the recommendations was fully supported by direct evidence from children with COVID-19, and for seven recommendations there was almost no direct evidence from children with COVID-19.

The RAG aims to provide instructional recommendations in the short term, and therefore studies available as preprints were used to support the evidence. Table 3 shows that six of the ten recommendations used COVID-19 preprints as evidence support, and up to 50% of the studies with direct evidence on COVID-19 were preprints. The RAG recommendations may have been influenced by the variable quality of the underpinning evidence, which may challenge the reliability of the guideline.

COVID-19 is a global pandemic and the research evidence is growing rapidly. Some of the original studies included in the rapid reviews were retracted for various reasons, resulting in the data being updated again during the production of the rapid review. For example, two studies included in the rapid review for the clinical question #4 ("Should Antiviral drugs such as ribavirin, interferon, remdesivir (GS-5734), lopinavir /ritonavir or oseltamivir be used to treat children with COVID-19?") were withdrawn, a controlled study on favipiravir was temporarily removed from Engineering on April 1 [65] , and another non-randomized controlled trial of hydroxychloroquine was withdrawn from the International Journal of Antimicrobial Agents on April 3rd due to not meeting the industry consensus criteria [66] . Because of the withdrawal of these studies, the rapid reviews had to be updated and revised.

The registration and publication of the protocol determines in advance the steps and methodology to be followed in developing the RAG according to the WHO handbook. Thorough development and documentation of the methodology, key issues and outcomes reduces the bias in the formulation of recommendations and minimizes the risk of inducing randomness into decisionmaking. In addition to the above, the registration of the guideline helps to increase the transparency of the development process, avoid duplication, enhance the credibility of the guidelines, and facilitate their dissemination and implementation.

The collection and integration of parents' preferences and values to form recommendations will help families fully understand the pros and cons of various treatment options, so that they have a stronger sense of acceptance and willingness to participate in clinical decision-making. Consideration of families' preferences and values can thus improve patient compliance, maximize patient benefits, and improve their clinical outcomes [67] . Therefore, the RAG conducted a recommendation survey process that incorporated two guardians of children scoring our recommendations and providing relevant feedback.

Clinical questions are the starting point for guideline development that determine the scope of evidence to be retrieved and evaluated at a later stage. Clinical questions also determine the content of the final recommendations [68] . Due to the urgency of the COVID-19 public health situation, solving all clinical problems at once was not possible, so we conducted a Delphi survey to rank clinical problems by a representative group of experts, and finalized 10 key clinical questions for clinicians fighting the epidemic in the frontline.

The development of guidelines must consider the best currently available research evidence to ensure that the recommendations are comprehensive and objective. Rapid reviews can synthesize the available research evidence on the same topic in a short duration of time, and thus reduce the risk of bias and ultimately improve the reliability and accuracy of decision making. Our guideline was accompanied by 13 rapid reviews to support the development of recommendations.

It is well known that strict adherence to guideline development manuals and the protocol can enhance the transparency and clarity and ensure the quality and credibility of the guideline [69] . In this particular case, we did not use other standard handbooks due to time constraints. We registered a protocol, and followed the protocol and the WHO RAG manual in every step of the development process. The manual is specifically intended for rapid advice guidelines, and contains several aspects that help to carry out the development in a rapid and efficient manner. The recommendations of the WHO RAG handbook differs from the standard guideline development in the following ways:1) The method of rapid systematic review production is used instead of the traditional development process of systematic reviews in evidence synthesis, which helps to save a lot of time in document screening, evaluation and synthesis; 2) Online meetings are used instead of face-to-face meetings, which saves time, administrative workload and resources of both the organizers and the attending experts; and 3) the WHO RAG handbook requires all members of the expert group to prioritize the preparation of the guidelines, postpone other non-urgent matters, and provide efficient feedback around the rapid development of the guidelines, which guarantees a rapid turnaround time of thefeedback and response.

In order to respond to public health emergencies, the development of a RAG requires a clear and transparent formulation process, and usually uses a large amount of indirect and non-peer-reviewed evidence to support the formation of recommendations. Strictly following the WHO RAG handbook does not only enhance the transparency and clarity of the guideline, but also speeds up the guideline development process, thereby saving time and resources.

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We thank Amir Qaseem for giving comments to the first draft. 

The online version contains supplementary material available at https:// doi. org/ 10. 1186/ s12874-022-01545-5.Additional file 1.

Additional file 3.