An evaluation of the reporting quality in clinical practice guidelines for hepatocellular carcinoma using the RIGHT checklist

Introduction

Hepatocellular carcinoma (HCC) ranks sixth among all types of cancer in new cases and is also the fourth leading cause of cancer-related death worldwide (1). The incidence of HCC varies globally and most of the cases occur in Asia and Africa, with China having a exceptionally high incidence (2). The high incidence of HCC in China is primarily due to the high prevalence of chronic hepatitis B virus (HBV) infection (3,4). While the five-year survival rate of patients with HCC is 18% in the United States, it is reported to be as low as 12% in China and other Asian countries (5,6). Over the past decade, new advances in the diagnosis and treatment have been developed due to the deepening understanding of the epidemiology, risk factors and molecular profiles of HCC (7). Correspondingly, new approaches to surveillance, diagnosis and treatment have shown their efficacy in managing patients with HCC and decreasing HCC related mortality (8-10). The incidence and mortality are affected by many factors, particularly the prevention, surveillance, diagnosis and management of HCC. The prevention of viral hepatitis can substantially reduce the occurrence of HCC, and the early detection of HCC can increase the chance of potentially curative treatment. However, the prevention and surveillance of HCC are substantially underutilized, even in countries with sufficient medical resources. The treatment of HCC can be complex and differs greatly depending on tumor burden, the severity of liver dysfunction, medical comorbidities, local expertise, and preferences of patients. Reasonable preventive measures, elimination of viral hepatitis, and active HCC surveillance and management are expected to significantly reduce the global burden of HCC within the next few decades. However, at present, in many countries HCC related morbidity and mortality are still increasing.

Clinical practice guidelines (CPGs) are collections of recommendations to guide, optimize, and establish norms for clinical practice. CPGs should be based on a systematic review of the literature, and rate the quality of evidence and strength of recommendations (11). In recent years, an increasing number of academic organizations and institutions worldwide have formulated guidelines to improve oncologists’ technical skills and knowledge and further the quality of medical treatment. However, the reporting quality of CPGs tends to be low (12,13). Checklists used to assist CPG developers can also be used to evaluate the quality of the guidelines. Two checklists, the appraisal of guidelines for research & evaluation (AGREE) for guideline development methodology and the Reporting Items for practice Guidelines in Healthcare (RIGHT) for reporting in guidelines, are commonly used in CPG development (14-16). The RIGHT statement has been used to assess the reporting quality of CPGs for different diseases (17-22). Currently, the reporting quality of HCC guidelines has not yet been systematically and comprehensively evaluated. The purpose of this review is to assess the reporting quality of the guidelines for HCC published between the years 2018 to 2020 to support more comprehensive, clear and transparent reporting in the future.

Methods

Literature search

We systematically searched Medline (via PubMed), Chinese Biomedical Literature Database (CBM), Wan Fang Database and Chinese National Knowledge Infrastructure (CNKI) for CPGs on HCC. We also searched the websites of the following guideline development organizations, governmental health agencies and oncological societies: World Health Organization (WHO), National Comprehensive Cancer Network (NCCN), Guidelines International Network (GIN), Scottish Intercollegiate Guidelines Network (SIGN), the National Institute for Health and Care Excellence (NICE), the European Society for Medical Oncology (ESMO), the American Society of Clinical Oncology (ASCO) and the Chinese Society of Clinical Oncology (CSCO).The search was restricted to the period January, 2018 to December 2020. The search terms for PubMed included liver neoplasms [MeSH], hepatic neoplasms [MeSH], cancer*, carcinoma*, neoplasm*, adenoma*, adenocarcinoma*, tumour*, tumor*, polyp* and malignant*, liver, hepatic, hepatocellular*, hepato-cellular*, hepatobiliary, Guideline, Practice Guideline, guideline*, guidance* and recommendation*. The complete PubMed search strategy is shown in Supplementary Appendix 1.

We included all CPGs on screening, surveillance, diagnosis, treatment, and up of HCC, published between 2018 and 2020 in English or Chinese.

We excluded translations and interpretations of guidelines, protocols of CPGs, older versions of CPGs when a more recent version was available, CPGs on other topics including recommendations related to HCC, and CPGs for which we were unable to retrieve the full texts.

All identified records were imported into an EndNote library (version X9.1). Four investigators (Haiyang Chen; Ding Li; Jing Han; Yingxi Wu) screened the titles and abstracts of all records independently following the pre-defined inclusion and exclusion criteria. Full texts of articles deemed potentially relevant were then reviewed to determine eligibility. Disagreements between researchers were discussed and resolved through consensus or by consulting another researcher (Qiming Wang).

Data extraction

The eligible CPGs were given to two investigators (Xuan Wu; Ding Li) for assessment with the RIGHT checklist. The checklist contains 22 key items, some of which are divided further into sub-items, resulting in 35 items. The items are grouped into seven domains: basic information, background, evidence, recommendations, review and quality assurance, funding declaration and management of interests, and other information.

We assessed the adherence of the CPGs to each item on a dichotomous scale. “Reported” mean that the relevant information was provided, and “not reported” that the relevant information was completely missing. If an item did not apply to a particular guideline, it was assigned “not applicable (NA)”. Disagreements between the two investigators were discussed and unresolved matters were addressed by another investigator (Qiming Wang).

Statistical analysis

We calculated the proportions of guidelines compliant with each of the 35 RIGHT checklist items, the overall reporting rate, and the reporting rates for items within each domain. Reporting rates were calculated by dividing the number of items rated as “Reported” by the total number of items, weighting all items equally. We present the mean, standard error of the mean (SEM) and total range overall CPGs. Since our search strategy covered many Chinese-language databases, we compared the overall reporting quality between guidelines published in China versus the rest of the world using Student’s t test.

Results

Study selection

A total of 474 documents were identified in search of the literature databases. Eight additional documents were identified from the websites of guideline and oncology associations. After screening the full texts, 22 CPGs eventually met the inclusion criteria (Figure 1). Twenty (91%) CPGs were retrieved from literature databases, and two (9%) from websites of oncology associations (Table 1). Eight (36%) guidelines were developed in China; 5 (23%) in the United States; 2 (9%) in Europe (n=2); and 1 (5%) each in Canada, Saudi Arabia, India, Japan, Brazil, South Korea and Argentina. Five guidelines (23%) were published in 2018, 6 (27%) in 2019, and 11 (50%) in 2020.

Figure 1 Flowchart of the literature search.

Table 1 Characteristics of the included guidelines (23)
Full table

Reporting quality of the included guidelines

The overall reporting rates ranged from across the CPGs 31% to 91%, with a mean ± SEM of 56%±4%. Among them, the reporting rate of 11 (50%) guidelines was above 50%, of one guideline above 90% (Table 1). The mean reporting rates (ranges) of guidelines written in Chinese and English were 43% (37–49%) and 58% (31–91%), respectively. The mean overall reporting rate of CPGs from China was 49% (range, 37–91%), and of those from the rest of the world 59% (range, 31–86%; P=0.18).

Reporting quality within each domain

The mean ± SEM reporting proportions (ranges) in the seven RIGHT domains were 81%±3% (50–100%) for basic information, 58%±6% (13–100%) for background, 58%±6% (0–100%) for evidence, 59%±5% (14–100%) for recommendations, 34%±10% (0–100%) for review and quality assurance, 39%±4% (25–75%) for funding, declaration and management of interests and 23%±6% (0–100%) for other information (Figure 2).

Figure 2 The mean reporting rates in each domain of the RIGHT checklist. RIGHT, Reporting Items for practice Guidelines in Healthcare.

Reporting compliance of each item

The details of reporting quality of each item are summarized in Table 2. Twelve items (1a, 1c, 2, 3, 4, 5, 7b, 9b, 12, 13a, 13b and 13c) were sufficiently reported with a reporting proportion higher than 80%. Among them, item 1a was reported by all 22 CPGs (100%). Items 10b, 11a, 11b and 19a were also well reported, each having a reporting proportion ranging from 50% to 80%. Three items (7a, 10a and 15) were reported by half of the guidelines. Any of the guidelines did not report item 18b, and items 1b, 6, 8a, 8b, 9a, 14a, 14b, 14c, 16, 17, 18a, 19b, 20, 21, and 22 were also reported by less than 50% of the guidelines.

Table 2 The details of reporting quality
Full table

Discussion

We identified 22 CPGs on HCC published during the years 2018–2020 worldwide. All except two guidelines were found through the searches of literature databases. Thus, medical literature databases should be the primary source when searching for guidelines on HCC. The number of CPGs for HCC published annually increased every year during the three years.

The reporting quality was found highly variable. Half of the included guidelines adhered to less than half of the RIGHT checklist items, showing a need for improvement. However, we found one guideline, developed by the Shanghai Association of Chinese Integrative Medicine, which had particularly high adherence to RIGHT and could thus be used as an example of how to report CPGs (41). Moreover, the domains of basic information, evidence and recommendations tended to be well reported. In contrast, reporting of items related to funding, declaration and management of interests, and review and quality assurance, was insufficient, consistent with the findings of previous studies in other guidelines (13,46).

The reporting compliance for individual items also varied substantially between the items. The reasons for the low reporting rate of certain items is essential to developing strategies to improve the reporting quality of the guidelines. Only eight guidelines (36%) reported the year of publication of the guideline in the title (RIGHT item 1b). If a guideline describes the year of publication in the title, it will be easy for researchers and practitioners to receive the updated guidelines containing the latest evidence. However, due to the lack of compliance standards and training related to guideline development, many guideline developers may have been unaware of the importance of this item. In contrast, all except two guidelines described the focus of the guideline appropriately in the title (item 1c). A clear presentation of the focus in the title makes it easy and fast for researchers and practitioners to identify the appropriate guideline for their needs from the database.

Four guidelines (18%) did not include an executive summary of the recommendations (item 2). Summarizing the recommendations can be meaningful for users who can quickly obtain the critical information without the need to seek the relevant information in the main text of the guideline. The rationale or explanation of the recommendations was reported by only about one-third of the CPGs. The accurate description of the rationale can be essential for a thorough understanding and balancing of the “pros and cons” of different interventions in the target population.

In clinical practice, clinicians need to make decisions that consider the context of the individual patient and situation. Therefore, high-quality guidelines should provide sufficient information about the applicability of the recommendations in specific clinical situations (47). We also found that the specific approaches or methods used to elicit or identify value and preferences or resource implications were poorly reported. Similar findings were also observed in other guideline evaluations regarding other topics (21,48). Generally, the methodological quality relies on documented information, and reporting quality can to some extent also mirror the methodological quality (49). Thus, guideline developers must pay attention to the rationale and explanation of the recommendations when drafting the guidelines.

Both RIGHT items (16 and 17) related to the review and quality assurance were reported by less than 40% of the guidelines. Undergoing an independent review and a quality assurance process will enhance the rigor of development and editorial independence, ultimately making the CPGs more convincing. It is also worth noting that the funding source and declaration of interest were reported in most guidelines. However, the role of funder(s) in the different stages of guideline development and the dissemination and implementation of the recommendations (item 18b), and the management of interests were poorly reported. A possible reason for the lack of declaration of the role of the funders may be that guideline developers are not always directly involved in the dissemination or implementation of guidelines: this is often the responsibility of health care authorities or professional societies (50). But without transparent management of interests, the independence of guideline development will be questionable. Previous studies evaluating the reporting quality of guideline in other topics, for example integrative medicine and chronic kidney disease, also found deficiencies in reporting in these domains (51,52). Strengthening review and quality assurance, and a thorough and transparent declaration and management of conflicts of interest and funding sources is an effective way to improve the quality of current guidelines.

Strengths and limitations

This is to our knowledge the first article to assess the reporting quality of guidelines for HCC based on the RIGHT statement. We carried out strict quality control during the evaluation process. However, our study also has some weaknesses. As we only searched English- and Chinese-language databases, the number of included CPGs was small and did not cover guidelines for HCC in other languages, which may potentially lead to selection bias.

Questions to be further discussed and considered

Question 1: What impact do you think the low reporting quality of clinical practice guidelines on hepatocellular carcinoma will have on clinicians and clinical practices?

Expert opinion: Dr. Vishal G. Shelat

Low reporting quality may impact the reliability of the guidelines. Many busy clinicians may feel obliged to comply with the guidelines due to trust in professional societies and organizations that make guidelines. Thus, if guidelines are poor of quality, it can impact safety and lead to harm. For example, 60% of clinicians responded that they would comply with guidelines recommending high dose steroids in patients with acute spinal cord injury, despite only 6% feel that it should be the standard of care (53,54). Fear of malpractice and professional censure can test individual clinician professional resilience to deviate from guidelines. One may feel more safe just blindly following the guideline, though morally it is not the right choice. Thus, the quality of reporting must be robust so that patients are not harmed. Kung et al. have studied a random sample of clinical practice guidelines archived on the National Guideline Clearinghouse (NGC) website and reported poor compliance with Institute of Medicine (IOM) standards (55). Our study confirms that scientific community continues to deviate from meeting high reporting standards despite awareness of such limitations. Personal conflicts, financial interests, scientific progress, or personal gain from authorship could be the reasons behind the lack of rigor and low-scientific quality of HCC guidelines. Our study cannot answer these questions and more evidence is required before any recommendations can be made. It remains individual moral responsibility to contribute scientific evidence in guideline and the process of guideline development. If conflict is perceived, recusal from guideline workgroup may be the best recourse.

Expert opinion: Dr. Francisco Tustumi

Low reporting quality clinical practice guidelines on hepatocellular carcinoma are propensity to every kind of bias. Consequently, these low-quality guidelines may induce clinicians to manage hepatocellular carcinoma based on poorly evidenced data regarding prognostication, diagnosing, investigation, or therapy. Poor quality guidelines lead to poor decision-making and inadequate use of resources (including utilization of liver grafts, diagnostic tests, expenses, time, and human resources).

Expert opinion: Dr. Sanjaya K. Satapathy

Traditional clinical guidelines consider only what is best for the patient and have explicitly not considered cost to the society. The suboptimal reporting of clinical practice guidelines on HCC will have spiraling effect on the clinicians and clinical practices, leading to a significant increase in healthcare burden.

Expert opinion: Dr. Koo Jeong Kang

The key for high reporting quality of clinical practice guideline is that it should provide the best benefit of survival and safety with highest quality of life when the patient was treated according to the guideline. And the guideline should be simple and algorithmic. The problem of the treatment guideline for hepatocellular carcinoma is that the patient status is not simple. Most of the HCC is developed in various diseased liver, viral hepatitis, alcoholics and fatty liver disease. And also the staging system of the HCC is not simple. There are various different staging systems.

EASL guideline is the most commonly mentioned in literature and academic society with higher reporting quality, even though the guideline is still not acceptable in some situations, intermediate to advanced staged HCC in particular. EASL guideline for both diagnosis and treatment is referred with higher quality, especially the algorithm for treatment strategy. It is very well formulated based on combined performance status, liver function as well as tumor stage according to BCLC stage. However, it is still applied in only 42.4% in Korean Primary Liver Cancer Registry (56). There was relatively low adherence to the guideline in patients with BCLC stage B or C HCC. The doctors who involved in in this study believe that the results and highlighted trends in the characteristics of HCC will contribute to improve the management of this disease.

Another aspect of the reason of low reporting quality may be caused that the guideline developed earlier is not revised and updated with high quality reports showing better survival benefit applied with other treatment modalities than the guideline (57,58).

Question 2: What do you think the most important aspects needed for developing high-quality clinical practice guidelines on hepatocellular carcinoma are?

Expert opinion: Dr. Vishal G. Shelat

The two crucial aspects needed for developing high-quality clinical practice guidelines on HCC are: high-quality scientific evidence, and professional governance of guideline development workgroups. As existing scientific literature is the backbone of guideline development, high-quality of data that is reliable and generalizable must be reported. To generate such data, clinicians must conduct scholarly activities alongside clinical practice. Such scholarly work should be performed by collaborative networks of basic scientists and clinicians, so that bench research is timely translated to bedside practice. It is essential that the latest evidence is incorporated into guidelines and this is continually reviewed. Professional organizations should recruit guideline members on the basis of scientific repute and not based on hierarchy or leadership roles in the organization. The guideline workgroup members should not be under the influence that could impair their judgment or decisions in critical analysis and evaluation of scientific evidence. Ideally, all members should be familiar with skills needed for critical appraisal of literature, and provided access and time to perform their role. Individual roles and responsibilities must distribute in mirco-teams so that individual members don’t make assumptions that ‘someone else is going to do this ….’. Individual motivation, accountability and empowerment of all members is integral to high-quality guidelines. In addition, independent external and impartial review of the final manuscript by key opinion leaders or content experts is important to ensure that any possible blind-spots of guideline workgroup are identified, and corrected.

Expert opinion: Dr. Francisco Tustumi

Practice guidelines on hepatocellular carcinoma should preferably use systematic review tools for selecting, extracting, synthetizing, critical appraisal, and reporting. Guidelines should clearly summarize the evidence by reporting the certainty of any statement so that decision-makers could know the strength of the evidence.

Expert opinion: Dr. Sanjaya K. Satapathy

High quality clinical practice guidelines on HCC need to consider RIGHT checklist items carefully with special attention for funding, declaration and management of interests, and external review and quality assurance. These items specifically appear to be neglected in majority of the HCC guidelines reported so far in the past 3 years.

Expert opinion: Dr. Koo Jeong Kang

For higher reporting quality of clinical practice guideline, it should be simply formulated from by systematic review of very well analyzed and summarized of the evidence based data by experts in different specialties. Also, it should be simple and easily applicable to individual patient following well-designed algorithm. Although the guideline is very well described after comprehensive analytic works by experts who have various kinds of specialties, the descriptive guideline without well formulated algorithm is not well used in practice. The ideal guideline should provide both safety and survival when it was applied to individual patient. If the tumor board members in an institution believe that their own practice provides better survival benefit than the guidelines, they will go their own way.

Question 3: How do you think conflicts of interest in the guidelines should be handled?

Expert opinion: Dr. Vishal G. Shelat

The ethical basis for professional obligation in medicine is the principle of primacy to patient welfare. Thus, patient’s best interest must be the primary consideration of the guideline development workgroup. In my opinion, the best way to manage conflicts is by recusal. Only if necessary for a particular member to be included in the guideline, then disclosure of conflict is mandatory. Problems rarely follow disclosure, but often from the discovery of non-disclosure. For example, the HCC practice guideline from Korean presented the disclosure of conflict of interest, not only presented the specific personnel information including names and affiliations, but also their contribution in the process of forming the guideline, which can increase reliability and protect the rights of patients better (35).

Expert opinion: Dr. Francisco Tustumi

Every conflict of interest should be clearly stated.

Expert opinion: Dr. Sanjaya K. Satapathy

Guideline developers with conflicts of interest such as relationships with the pharmaceutical industry could potentially be biased while formulating their recommendations (59). It is vital to have appropriate disclosure of financial conflicts of interest for authors of CPGs and a formal process for discussing these conflicts before CPG development should be formed.

Expert opinion: Dr. Koo Jeong Kang

It is very difficult issue. There is no way except declaration of every developer or organization of the guideline regarding the conflict of interest with funding sources.

Conclusions

The reporting quality of guidelines for HCC was suboptimal. Particularly the declaration of funding and the quality assurance process was rarely reported. We encourage using the RIGHT statement when developing high-quality CPGs for HCC to ensure that the recommendations and their background information are clearly transparently reported.

Acknowledgments

The authors appreciate the academic support from the AME Reporting Guideline Collaborative Group.

Funding: This work was supported by a project cosponsored by Henan Province Health and Youth Subject Leader Training Project (No. [2020]60) and the Excellent Young Talent Cultivation Project of Henan Health Science and Technology Innovation Talents (No. YXKC2020046). It was also supported by Henan International Joint Laboratory of drug resistance and reversal of targeted therapy for lung cancer (No. [2021]10). The funders had no role in the study design, data collection, an analysis, decision to publish, or manuscript preparation.

Footnote

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://dx.doi.org/10.21037/atm-21-2611). SKS has served as a speaker for Intercept, Alexion, Dova, as an advisory board member for Gilead, Intercept, Bayer and has received research funding from Novartis, Fibronostics Gilead, Biotest, Genfit, Conatus, Intercept, Shire, Exact Sciences, Eananta, Dova, Bayer. SKS is an employee of Northwell Health. The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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