Clinical practice guidelines for the diagnosis and management of Duchenne muscular dystrophy: a scoping review

Introduction: Our objective was to identify recent CPGs for the diagnosis and management of DMD and summarize their characteristics and reliability.

Methods: We conducted a scoping review of CPGs using MEDLINE, the Turning Research Into Practice (TRIP) database, Google Scholar, guidelines created by organizations, and other repositories to identify CPGs published in the last 5 years. Our protocol was drafted using the Preferred Reporting Items for Systematic Reviews and Meta-analyses for scoping reviews. To assess the reliability of the CPGs, we used all the domains included in the Appraisal of Guidelines Research and Evaluation II.

Results: We selected three CPGs published or updated between 2015 and 2020. All the guidelines showed good or adequate methodological rigor but presented pitfalls in stakeholder involvement and applicability domains. Recommendations were coherent across CPGs on steroid treatment, except for minor differences in dosing regimens. However, the recommendations were different for new drugs.

Discussion: There is a need for current and reliable CPGs that develop broad topics on the management of DMD and consider the challenges of developing recommendations for RDs.

1 Introduction

Duchenne muscular dystrophy (DMD) is a rare disease (RD) primarily affecting males due to its association with the X-linked chromosome (1, 2). DMD arises from a mutation in the DMD gene, leading to the absence or deficiency of the essential dystrophin protein (2). This genetic deficiency sets in motion a series of damaging processes within muscle cells, including oxidative stress injuries, imbalanced calcium regulation, and instability of the sarcolemma, these processes harm muscle cells, disrupt neuromuscular junction and abnormal differentiation of muscle satellite cells (2, 3). Collectively, these factors contribute to the progressive weakening and degeneration of muscles observed in individuals with DMD (2). The global prevalence and estimated birth prevalence of DMD are 7.1 and 19.8 male patients per 100,000 individuals, respectively (4). Unfortunately, many patients, especially in developing countries with inadequate standards of care, do not survive beyond their pediatric years (4).

For an RD such as DMD, the development of clinical practice guidelines (CPGs) involves multiple obstacles from evaluation and the synthesis of evidence to the formulation of recommendations and knowledge translation, and the data available may not be sufficient (5, 6). CPGs for the diagnosis and management of DMD could be useful as an aid to health care professionals for improving the quality of care and simultaneously reducing potentially harmful or ineffective interventions for patients (7). For RDs, CPGs are additionally useful for increasing transparency and allowing collaboration in improvements in patient care (8). For these reasons, guidelines for RDs must be prepared and provide recommendations with the best available evidence, even if it is considered insufficient.

Scoping reviews cover a broader field of review than systematic reviews (SRs); in addition, they can be used to qualitatively describe and evaluate the methodology of a CPG (9). Some similar papers were related to the diagnosis and treatment of liver tumors, diabetic macular edema and atopic dermatitis (10–12). Due to the importance of high-quality CPGs for RDs, it is necessary to evaluate them critically; thus, our objective was to identify CPGs for the diagnosis and management of DMD through an evaluation of methodology formulation and a comparison of clinical recommendations for a better application in clinical practice.

2 Materials and methods

We conducted a scoping review of CPGs for the diagnosis and management of DMD to assess their quality and compare their recommendations with a focus on developing countries. Our protocol was drafted using the Preferred Reporting Items for Systematic Reviews and Meta-analyses for scoping reviews (PRISMA-ScR) (13) and is available in the figshare database (www.prisma-statement.org/Extensions/ScopingReviews).

2.1 Search strategy

We performed a search to identify any potentially relevant documents from inception to February 2022 in databases (PubMed/MEDLINE, Scopus and Web of Science), guidelines formulated by organizations (National Institute for Health and Care Excellence [NICE], the Scottish Intercollegiate Guidelines Network [SIGN], Centro Nacional de Excelencia Tecnológica en Salud [CENETEC], Ministerio de Salud y Protección Social de Colombia [MINSALUD]) and repositories (Guidelines International Network (GIN) and SAGE, among others). This approach was selected as searches in databases alone may have a lower sensitivity compared to the inclusion of organizations (7). The investigation strategies were drafted by the research team and included terms related to DMD, diagnosis, and management and guideline filters. The search was conducted by three independent researchers (MC, AHR and MM).

2.2 Study selection

To increase consistency among reviewers, the three independent researchers (MC, AHR and MM) who performed the study selection attended a workshop on how to identify CPGs. Thereafter, the three reviewers screened the titles and abstracts and selected the full-text articles of all the publications screened; disagreements were resolved by consensus with a fourth reviewer (CAD or VVR).

All the CPGs that met the following characteristics were included: 1) CPGs based on evidence from systematic reviews, 2) the scope of which was the diagnosis and/or management of DMD, that 3) had been published no more than seven years ago. CPGs were excluded if 1) they were not published in English or Spanish or 2) the primary aim was not to inform about clinical care.

2.3 Data extraction

A data charting form was developed in Excel software, and two independent researchers (AHR and MM) extracted the following characteristics from the CPGs: authors, year of publication, country, target users, guideline developers, whether there was patient participation, guideline review process and the system used to grade recommendations. Additionally, recommendations related to diagnosis or management were extracted for comparison. A third reviewer (CAD) resolved disagreements in extraction by consensus.

2.4 Assessment of quality

To assess the quality of the CPGs selected, we used all the domains included in the Appraisal of Guidelines Research and Evaluation II (AGREE-II) (14). Each guideline was rated by five researchers (MC, ARC, MM, GAG, PMB and FCE). A grade was assigned for each item on a 7-point scale, with a score of 1 indicating that the item met none of the criteria or was very poorly reported, and a score of 7 indicated that the item met all the criteria and was well reported. We used the mean of the five raters for each item and followed the AGREE-II instrument guideline to calculate the scores for each domain (14). When a difference in two or more points for each item was found, the item was discussed to achieve consensus; disagreements were resolved by consensus with a sixth reviewer (CAD). We considered a CPG to have high quality and good quality when the total score was >60% and >80%, respectively, and we used the same cutoff for each domain of the AGREE-II instrument based on previous studies (14).

3 Results

3.1 CPG search and selection

The search strategy identified 1330 original documents (databases: 1092, CPG-compiling agencies: 188, and CPG development organizations: 50). In the title and abstract screening, 18 documents from databases met the eligibility criteria for full text review. We selected four de novo CPGs on the scope of diagnosis and management of DMD published or updated between 2014 and 2022 (see Figure 1). Additionally, we found nine expert consensus statements.

Figure 1

Figure 1. Search flowchart for the scoping review following the PRISMA guidelines.

3.2 CPG characteristics

The CPGs were from England (developed by the National Institute for Health and Care Excellence [NICE]), the United States of America (developed by the American Academy of Neurology [AAN]), Colombia (developed by the Institute of Health Technology Evaluation of the Colombian Ministry of Health [IETS-MINSALUD]), and Australia (developed by the Australian National Health & Medical Research Council) (15–18). Two CPGs focused on recommendations for the diagnosis, treatment, and rehabilitation of DMD (15, 18), and one particularly focused its recommendations on nursing and other professional practices (15). The remaining two CPGs focused on treatment with ataluren (17) and corticosteroid therapy (16) (Table 1).

Table 1

Table 1. Characteristics of the clinical practice guidelines for the diagnosis and management of Duchenne muscular dystrophy.

In 2/4 CPGs, the guideline developers included physicians, neurologists, nurses, rehabilitation therapists, nutritionists, and other nonhealth care professionals, such as economists (15, 18). The remaining guidelines included physicians, neurologists, nurses, and specialists in technology evaluation (16, 17). Similarly, 2/4 CPGs described in detail the participation of patients or their representatives in the development of the guidelines (15, 18).

The Grading of Recommendations Assessment, Development and Evaluation (GRADE) system was employed in two of the CPGs (Colombian and Australian CPGs) (15, 18). The Australian CPG also used the Consensus-based Standards for the selection of health status Measurement Instruments (COSMIN) and the modified Delphi process (15). The two treatment CPGs included only evidence generated from clinical trials (16, 17); one included evidence generated from randomized controlled trials (RCTs) or observational studies (15), and the remaining CPG also included evidence from systematic reviews (18).

3.3 Expert consensus characteristics

The majority of consensus experts were from Europe. The objectives were related to treatment, diagnosis, follow-up and patient education. Most of the studies did not report any method of reaching a consensus. However, among those that did report this, the Delphi method was the most widely used. Three articles reported a systematic search in databases (19–21). Only two studies used some method to grade the evidence (19, 20) (Table 2).

Table 2

Table 2. Characteristics of expert consensus related to Duchenne muscular dystrophy.

3.4 Assessment of quality

The AGREE-II domain scores for each guideline are shown in Table 3. The Colombian CPG had a high quality and showed the highest overall assessment score (mean: 97.9%; range: 95.8%-100%) (18). Additionally, the AAN (mean: 76.6%; range: 51.4%-90.2%) (16) and Australian CPGs (mean: 66%: range: 44%-87.5%) (15) showed good quality. The NICE (mean: 54.8%; range: 37.5%-75%) (17) guideline showed lower overall scores. Figure 2 graphically compares the AGREE-II domain scores of the included CPGs.

Table 3

Table 3. Quality appraisal of Clinical Practice Guidelines for Duchenne muscular dystrophy using the AGREE-II instrument.

Figure 2

Figure 2. AGREE-II domain scores for included CPGs. NICE (blue), AAN (orange), Colombian CPG (red), Australian CPG (yellow). 1: Scope and purpose; 2: Stakeholder involvement; 3: Rigor of development; 4: Clarity and presentation; 5: Applicability; 6: Editorial independence.

3.5 Diagnosis

Regarding CPG recommendations, the Colombian guideline had a wider scope and provided recommendations for the use of clinical criteria and the use of the measurement of serum creatinine kinase in the initial diagnostic approach for patients suspected of having DMD. Finally, the use of Western blotting, immunohistochemistry, and multiplex ligation-dependent probe amplification (MLPA) was recommended to confirm the diagnosis (18) (see Table 4).

Table 4

Table 4. Summary of recommendations in published CPGs for the diagnosis and treatment of DMD.

3.6 Pharmacological treatment

The three guidelines provided recommendations for pharmacological treatment (16–18). The Colombian CPG was broadest in scope and included recommendations for treatment with steroids, and creatine (18). The Colombian CPG recommended against the use of ataluren to reduce mortality, improve quality of life, and reduce dyspnea and fatigue (18). However, the NICE guideline evaluated the application of ataluren in patients 2 years and over who can walk, and gave a conditional recommendation in the context of a managed access agreement and other financial components that reduced the total costs to the National Institute of Health (17). Additionally, the Colombian CPG and AAN guidelines agreed on the use of prednisone or deflazacort to reduce mortality, to improve timed motor function and to reduce the progression of scoliosis (16, 18) (see Table 4).

3.7 Nursing and other allied health professions

The Australian CPG was the only one that provided recommendations related to health assessments and management strategies by nursing and other allied health professions for patients diagnosed with DMD. The key allied health professions relevant to this CPG were dietitians, occupational therapists, physiotherapists, social workers and speech pathologists. Among its main recommendations was support and prevention by multidisciplinary teams to achieve integral attention for DMD patients (15) (see Table 4).

4 Discussion

4.1 Main findings

We found a total of four CPGs, of which only one included recommendations for diagnosis and treatment; two CPGs, a practice guideline and a health technology assessment, were focused only on corticosteroid or ataluren therapy, respectively; and one CPG included recommendations about allied health and nursing practice for the assessment and management of DMD patients (15–18).

4.2 Assessment of quality

In relation to the quality of guideline development, the best performing CPG was the Colombian CPG, followed by the AAN and Australian CPGs (15, 16, 18). The NICE guideline showed low overall scores in the AGREE-II domains (17). The NICE guideline obtained a low score, probably due to its narrow objectives since it was mainly an evaluation of new technology (17). When analyzing the third domain (rigor of development), 2/4 CPGs achieved a very good score (> 80%) (16, 18). The other guides obtained good scores (>60%) (15, 17). Our results indicate that, in general, the CPGs had adequate methodological rigor, which could mean that they were based on the best available evidence identified from the SR process in addition to incorporating other multiple criteria, which was adequate to make trustworthy recommendations (27–29).

Another important aspect to consider is the system used to make recommendations. In this regard, 2/4 CPGs clearly described the methodology used step by step (Colombian and Australian guidelines) (15, 18). The AAN guideline reported the system used to grade recommendations but did not clearly describe the entire process. The application of a systematic review process guarantees the use of the best evidence but not the development of trustworthy recommendations from this evidence. GRADE is the most accepted approach for this, as it assesses the body of evidence using different criteria such as study design, risk of bias, imprecision, indirectness, inconsistency, and others to increase or reduce the certainty of evidence (30). This allows for a simple and transparent grading of recommendations that can effectively contribute to improving clinical practice, even in the scenario of limited evidence for RDs (31, 32).

4.3 Stakeholder involvement

On the one hand, stakeholders are defined as “individuals, organizations, or communities that have a direct interest in the process and outcomes of a project, research, or policy” (33). In CPGs, the patients are of particular importance, as they are affected by the diseases, and the outcomes investigated are a key component in the applicability of the guidelines. Patients can help to identify research questions and important issues in their health care and include perspectives from different settings (16, 34, 35). Nevertheless, we found that 2/4 CPGs reported in detail the participation of the patients in the review of the scope, identification and grading of outcomes and in the review of the draft (Colombian and Australian CPGs) (15, 18). Both guidelines achieved a score >60% in this domain.

Regarding the other guidelines, the NICE guideline includes a patient advocate as a specialized technologies evaluation committee member (36). Additionally, the process manual to develop clinical practice guidelines of the AAN recommends including at least one patient in formulating the clinical question and review of the draft (37). However, we did not find details of the participation of patients and/or their representatives in the DMD guidelines developed by these institutions (16, 17). The NICE and AAN guidelines probably did not obtain adequate quality scores in the stakeholder involvement domain due to their limited scope or because a professional association developed them.

4.4 Clarity, presentation, and editorial independence

Most of the guidelines reported easily identifiable, specific, and unambiguous recommendations. This helps in the uptake of guidelines by target professionals and patients (38). In addition, the Colombian CPG presented a flowchart for patients with suspected DMD and for treatment with steroids and deflazacort (18).

The editorial independence domain is important because funding and conflicts of interest (CoIs) can introduce bias in developing recommendations (39). We found that the CPGs were supported by transparent institutions that reported financing. However, not all the guidelines described how potential CoIs influenced and how they were controlled for in the elaboration of the recommendations, which is a common limitation (40, 41).

4.5 Diagnosis and treatment recommendations

Only the Colombian CPG included diagnosis in its scope and therefore included recommendations regarding the types of diagnostic tests available for DMD. In addition, it mentioned an economic evaluation within the CPG, recommending the use of Western blotting, followed by immunohistochemistry and finally MLPA. However, given that different techniques may be available in each country, factors such as training and standardization should be involved in deciding the techniques required for diagnosing DMD (31).

Two CPGs recommended corticosteroids as the standard of care for DMD due to their significant benefits (16, 18). Nevertheless, glucocorticoids (prednisone and deflazacort) are associated with notorious adverse effects (AEs), such as weight gain, cushingoid appearance, growth retardation/failure to thrive, behavioral changes, fractures due to osteoporosis, cataracts, and skin fragility (40, 42). For this reason, intermittent therapy has been investigated as an alternative; unfortunately, one randomized controlled trial did not show significant improvement the comparison between daily and intermittently 10 days on and 10 days off (43). Despite this, due to an outdated state of the available evidence, the Colombian CPG recommends intermittent therapy when the patient develops AEs (17, 18), whereas the AAN CPG considers that the evidence is insufficient (16). Additionally, new alternatives are currently under investigation, such as vamorolone, a steroid analog, where doses of 2 and 6 mg/kg per day showed improvements in multiple functional end points over the 24-week treatment period (44).

Ataluren, a small orally bioavailable molecule that induces ribosomal read-through of nonsense mutations, was conditionally approved by the European Medicines Agency in 2015 (45), but in 2023 recently recommended non-renewal of authorization Translarna (ataluren) (46); besides, has not yet been approved by the Food and Drug Administration (47). Since the Colombian CPG was developed in 2014, it did not include the two new RCTs on ataluren (48, 49). This could explain why this CPG recommended against treatment with ataluren (18). Although Ataluren treatment is controversial, ongoing studies are recruiting patients for long-term efficacy and safety. In addition, the drug has demonstrated better benefits than placebo, and with standard of care is even better, albeit with limited evidence (50, 51). For example, the NICE guideline concluded that ataluren represents an acceptable option only in the context of a managed access agreement (MAA) based on clinical results (17, 52). However, by certain organizations exist restriction for the use of the innovative technology when it is expensive and exist uncertainty about it effectiveness and security. Consequently, patients with DMD are left without appropriate treatment options (53–55).

4.6 Nursing and other allied health professions

DMD is a disease characterized by progressive muscle degeneration and functional losses. Thus, it is important to develop supportive and prevention recommendations by multidisciplinary teams to achieve integral attention for DMD patients (56). However, we found only one CPG, the Australian CPG (15), that focused on health issues not covered by guidelines aimed at diagnosis and/or medical treatment. This guideline had a broad scope, including dietary counseling, rehabilitation, respiratory function, behavioral or learning difficulties management, etc. In addition, the users of the guideline were professionals from different areas of health. This type of scope is novel but very important for the proper care of DMD patients. Further studies could include its conceptual framework within the development methodology.

4.7 Expert consensus

Most experts agreed with CPGs about the recommendations for diagnosis and treatment. Apart from these, some suggested that family education can help address the problem of stigma at home and in society (25). Additionally, they indicated regular nutritional monitoring and diet adjustments (20).

4.8 Formulating recommendations for rare diseases

The paucity of evidence is a serious concern for RDs. The CPGs we identified based their recommendations on systematic reviews of clinical trials and cost-effectiveness studies. They did not use other types of evidence, such as observational studies for treatment, real-world data, or qualitative or narrative studies, which are important in the field of RDs (5, 31). Furthermore, RD studies, when available, may have multiple limitations (31). Some of these limitations include the rarity of RCTs, study heterogeneity, and challenges in patient enrollment, among others (31, 54).

Researchers have developed methodologies for eliciting and synthetizing evidence for CPGs on RDs. The RARE-Best Practices Working Group shares methodological knowledge for guideline development in the field of RDs (31, 32). First, intentional and systematic gathering of observational evidence from experts is a more efficient and transparent alternative to informal “around the table discussion” by guideline panels (5). Additionally, indirect evidence from other diseases and access to a patient registry of the target disease to complement published evidence with low certainty is a feasible alternative (5). Finally, in this context, qualitative research could be a feasible source of information (5). However, these registries were not implemented in the CPGs identified, as they were published previously or did not incorporate the GRADE methodology. Future guidelines should consider these recommendations during development because they can increase reliability.

4.9 Limitations

One of our study limitations was that only guidelines published in English or Spanish were collected, and thus, our findings may not be representative of CPGs published in other languages. Although most organizations publish their guidelines in English, one of the CPGs was excluded because it was only available in Chinese. Further studies should consider evaluating the quality of CPGs published in other languages. Although the CPGs originated from high-income countries, exist different population in patients with DMD around the world with disparities in healthcare access, medication and accurate diagnosis availability. It is imperative to consider this heterogeneity in DMD populations when its developing EBG to incorporate implementation considerations (57).

4.10 Conclusions

We performed a scoping review of CPGs for DMD, identifying four guidelines: one for the diagnosis and management of DMD, two for ataluren and corticosteroid therapy, and one focused on allied health professionals and nursing. In addition, nine expert consensuses were identified. All the guidelines showed high or good performance in the rigor of development. Recommendations were coherent across CPGs on steroid treatment, except for minor differences in dosing regimens. However, there was disagreement regarding the use of ataluren, mainly due to the absence of evidence at the time of publication. Finally, no diagnostic or treatment guidelines have been published or actualized in the last 5 years, and we recommend updating the existing guidelines and implementing a reliable methodology in their development.

Author contributions

MM: Conceptualization, Formal analysis, Methodology, Writing—original draft, Writing—review & editing. AR-C: Conceptualization, Formal analysis, Methodology, Writing—original draft, Writing—review & editing. FC-E: Conceptualization, Formal analysis, Investigation, Methodology, Writing—original draft, Writing—review & editing. AH-R: Investigation, Methodology, Writing—original draft. GA-G: Investigation, Methodology, Validation, Writing—original draft. MC-L: Investigation, Methodology, Writing—original draft. PM-B: Data curation, Validation, Writing—original draft. VV-R: Formal analysis, Investigation, Methodology, Software, Validation, Writing—original draft, Writing—review & editing. PM-E: Supervision, Validation, Visualization, Writing—original draft, Writing—review & editing. CA-D: Conceptualization, Funding acquisition, Investigation, Project administration, Resources, Validation, Visualization, Writing—original draft, Writing—review & editing.

Funding

The authors declare that no financial support was received for the research, authorship, and/or publication of this article.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Abbreviations

SAGE, Strategic Advisory Group of Experts; AGREE-II, Appraisal of Guidelines for Research and Evaluation II; MLPA, Multiplex ligation-dependent Probe Amplification; MAA, Managed Access Agreement; RCTs, Randomized Controlled Trials.

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