Systematic review of the tools and outcomes for the assessment of acute radiation dermatitis severity.

Introduction

Acute radiation dermatitis (ARD) is a commonly occurring side effect that presents in patients undergoing radiation therapy (RT) [ 1 ]. The incidence of ARD is notably high, with approximately 95 % of patients developing some manifestation of this condition within the first 90 days of initiating RT. Clinical presentation of ARD has a spectrum of signs including erythema, desquamation (both dry and moist), ulceration, and pruritus. Beyond its prevalence, ARD may significantly contribute to a deterioration in patients’ quality of life, often require adjustments to therapeutic regimens, such as disruption or discontinuation RT [ 2 , 3 ]. The pathophysiology of ARD is multifactorial, with treatment-related variables such as radiation dosage and concurrent systemic therapy, as well as patient-specific factors including smoking status, breast size, body mass index, radiation target site, and reirradiation all playing contributory roles in the severity of dermatologic reactions [ 4 ].

The multifaceted nature of ARD is reflected in the numerous types of tools utilized to measure ARD severity, which underscores the critical need for the standardization of these comprehensive assessment tools. Clinician-reported outcomes (CROs), such as the Radiation Therapy Oncology Group criteria (RTOG) and Common Terminology Criteria for Adverse Events (CTCAE), capture clinician reported evaluation of clinical presentation and physical symptoms using validated scales. Patient-reported outcomes (PROs), such as symptom-specific Visual Analogue Scales (VAS) and McGill Pain Questionnaire, capture the patient’s perspective on symptom burden and its impact on various dimensions of health and well-being. Mixed CRO/PRO instruments, such as the Radiation-Induced Skin Reaction Assessment Scale (RISRAS), amalgamate professional assessment with patient self-reporting to provide a more holistic evaluation. Additionally, quality of life (QoL) instruments, Dermatology Life Quality Index (DLQI),

European Organization for Research and Treatment of Cancer Quality of Life C30 (EORTC QLQ-C30), are a type of PRO that specifically assess the functional implications of ARD on daily living. Further, biophysical parameters (BPs) offer an objective quantification of skin traits affected by radiation exposure [ 5 , 6 ].

Despite the recognized importance of ARD assessment, the lack of standardization in measurement tools across clinical trials poses a significant barrier to comparative efficacy analyses and the optimization of management strategies. To date, no study has systematically addressed the harmonization of ARD measurement across CRO, PRO, CRO/PRO, QoL, and BP domains. The aim of this study was to critically evaluate published literature to identify the diverse array of tools and outcome measures currently employed in ARD assessment and determine the strength of evidence supporting use of the identified tools and measures, with the ultimate goal of informing standardization efforts for ARD assessment facilitating the comparability of clinical trials for improved RD management [ 7 ].

Materials and methods

Search strategy and selection criteria

The literature review employed in this study was the same as that reported in Behroozian et al. [ 8 ] with addition of an extended review through March 24, 2024. In summary, a literature systematic review was initially completed with the assistance of a medical librarian through OVID MEDLINE®, the Cochrane Central Register of Controlled Trials (CENTRAL), and Embase databases. Any relevant non-randomized studies and other publications (i.e., case reports, retrospective studies) during this period were also included. The search strategy is summarized in Appendix A.

All included articles were published in English (either abstract or full-text articles) and included in the analysis if they answered the research question according to the Population, Intervention, Comparison, Outcome (PICO) method [ 9 ]: P) patients treated with external beam RT for cancer; I) any form of intervention; C) standard of care, a form of placebo, another form of intervention, or no intervention use; and, O) the prevention or management of ARD and any ARD-related signs and symptoms. The research question was intentionally kept open-ended to maximize inclusion of randomized and non-randomized studies (i.e. prospective non-randomized studies, retrospective studies, case reports). Studies were excluded if they did not answer the research question, used animal or in vitro models, had insufficient information to answer the research question, had inaccessible full texts, only assessed chronic and late toxicities, or were in the accrual phase.

For the purposes of this systematic review, tools utilized in the assessment of ARD were extracted. Tools were defined as any measurement criteria that provided clinically relevant information about ARD severity: CROs, PROs, CRO/PROs, QoL, or BPs. Symptom outcomes examined were also noted. To align with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) process, multiple authors screened all titles and abstracts independently for eligibility [ 10 ]. When discrepancies were encountered, a third-party was consulted to determine inclusion. Subsequent full-text screening occurred, and data was extracted from those that met the inclusion criteria. The data was cross-checked for accuracy by an independent reviewer.

Data collection and analysis

The relevant study factors extracted from the included articles were: sample size, publication year, study design (prospective or retrospective), type of trial (randomized or non-randomized), assessed outcomes, and the method used for ARD assessment. A quality of evidence assessment was completed following the Hadorn criteria for clinical trials (Appendix B) [ 11 ]. Studies determined to have no flaws or minor flaws were classified as having “adequate” quality of evidence, while those determined to have major flaws were classified as having “doubtful” quality of evidence.

Results

Search results

After conducting database searches, a total of 7,082 articles were identified ( Fig. 1 ). The removal of duplicates resulted in a remaining 5,635 articles. A total of 4,944 articles were excluded after abstract and title screening as they were not relevant to the PICO research question or they met one of the previously mentioned exclusion criteria, leaving 691 articles for full text screening. A total of 423 unique articles remained for inclusion in this analysis (227 randomized control trials (RCTs) and 196 non-randomized trials (NRTs). A total of 58 unique tools were identified in this search. A summary of key findings according to tool type is included in Fig. 2 and outcomes are listed in Table 1 . Individual tool quality of evidence based on study methodology can be found in Appendix C. Across all studies, 10 major disease site categories were noted. The top three sites included breast (62.7 %), head and neck (33.1 %), and gastrointestinal (8.3 %) regions. Further information regarding disease site breakdown can be found in Appendix D. Lastly, we observed treatment of patients from 46 different countries across all of the studies. Most studies were conducted in the United States of America (USA) (15.1 %), China (8.3 %), Italy (7.3 %), Canada (6.4 %), Germany (6.1 %), Iran (5.9 %), India (5.7 %), Japan (5.0 %), United Kingdom (UK) (4.3 %), and France (3.5 %), suggesting limited evidence for ARD assessment in low-resource countries. Further information regarding country breakdown can be found in Appendix E.

CROs

A total of 14 relevant CROs were identified (Appendix C). Most CROs (12/14, 85.7 %) were often used as primary outcome measures in clinical trials (Appendix C). However, the majority of CROs (12/14, 85.7 %) were used in less than five studies or were used in studies that could have considerations for improved methodology (12/14, 85.7 %) (Appendix C). The Radiation Dermatitis Severity Scoring Scale (RDS) and Visual Numerical Scale were used in studies with strong methodological approaches – 14.3 % (2/14) of all CRO tools (Appendix C). They were, however, used in three or fewer studies. The Radiation Therapy Organization Group (RTOG) and Common Terminology for Criteria for Adverse Events (CTCAE) were the most widely used CRO scoring tools, respectively appearing in 183 (116 RCTs) and 195 (81 RCTs) studies, ranging from studies that could be improved methodologically to those with robust methods (Appendix C). These commonly used instruments often had modified versions used across several trials. For example, the RTOG measure was modified to a 6-point scale (RTOG-Modified), which added the scores of 1.5 and 2.5 to help differentiate at lower scores based on visual assessment (Appendix C). Due to the diversity of trial settings and processes, a consensus on selecting a standard ARD CRO assessment tool could not be made.

PROs

A total of 17 relevant PRO tools were identified (Appendix C). The most commonly used PRO for ARD was the Visual Analogue Scale (VAS) which was reported in 39 (31 RCTs) studies (Appendix C). The McGill Pain Questionnaire – Short Form (MPQ), Skin Pain Inventory (SPI), Self-Reported Diary (0–10 scoring) and the Symptom Inventory adapted from MD Anderson Symptom Inventory, were all only used in strong methodological studies, however, were used in ≤ 2 studies – they represent 23.5 % of the PROs (4/17). Several PROs (17/17, 100 %) were used to measure secondary outcomes of interest, had less than 5 studies use them (14/17, 82.4 %), or were in studies with methodology limits (12/17, 70.6 %) (Appendix C). Thus, a consensus on choosing a standard PRO could not be reached for ARD assessment.

QoL

Of the 12 QoL measures identified, the most commonly used tools were Dermatology Life Quality Index (DLQI), European Organization for Research and Treatment of Cancer Quality of Life C30 (EORTC QLQ-C30), and Skindex-16, which were used in 19 (16 RCTs), 21 (16 RCTs), and 20 (17 RCTs) studies, respectively (Appendix C). Most QoL instruments (10/12, 83.3 %) measured secondary outcomes in the clinical trials, were utilized in < 5 studies (8/12, 66.7 %), or were in trials with methodological limitations (11/12, 91.7 %). The DLQI, EORTC-QLQ BR23, EORTC QLQC30, linear analog self-assessment (LASA), Skindex-16, and Skindex-29 were the only QoL measures utilized in at least one study with rigorous methods (i.e., high quality) (Appendix C). However, because all these tools were used in varying contexts with different levels of approaches, no consensus on a standard QoL tool for ARD assessment could be made.

Combined CRO/PROs

Of the three combined CRO/PRO tools identified, the most widely used tools were the Radiation-Induced Skin Reaction Assessment Scale (RISRAS) and the Skin Toxicity Assessment Tool (STAT) occurring in 31 (19 RCTs) and 9 (6 RCTs) studies respectively (Appendix C). Only RISRAS and STAT were used in at least one study with robust methodology (Appendix C). The Subjective, Objective, Management, and Analytic (SOMA) metric was used in one study as a secondary outcome measurement with limited methods (Appendix C). A consensus for a standard CRO/PRO measure for ARD assessment could not be made.

BPs

Of the 12 BPs that were identified, photography, reflectance spectrophotometry, and the corneometer (CM 820/825) were commonly used and reported in 36 (25 RCTs), 11 (10 RCTs), and 8 (8 RCTs) respectively (Appendix C). BP tools were mainly used as secondary outcome measures (11/12, 91.7 %), published in less than five studies (7/12, 58.3 %), or used in studies with limited methodological support (12/12, 100 %) (Appendix C). The highest quality methodology supported 58.3 % (7/12) of BP tools by having at least one high quality article use these tools, including colorimetry, corneometer (CM 820/825), erythema index/melanin index mexameter (MX18), infrared thermographic scanner, photography, reflectance spectrophotometry, and transepidermal water loss (TEWL) (Appendix C). Similarly, to all the other categories of tools discussed, no consensus could be made for BP tools on their utility for ARD assessment.

Outcomes

We noted 23 outcomes related to various symptoms and physical manifestations in the assessment of ARD severity ( Table 1 ). The most widely utilized outcomes included the following: burning, dry desquamation, edema/swollenness, erythema/redness, moist desquamation, necrosis/ulceration, pain, pruritus/itching, quality of life/wellbeing, and satisfaction/comfort/discomfort ( Table 1 ). Less commonly used outcomes included corneometry, dryness, fatigue, time/rate for healing, heat, pigmentation, moisture, mood, pulling/peeling of the skin, sebum content, the time/rate for RD/specific-grade dermatitis onset, tenderness, and trans -epidermal water loss ( Table 1 ). This is concurrent with the widespread use of the validated RTOG and CTCAE physician evaluation tools for ARD, both of which incorporate many of the aforementioned outcomes into their grading schemes when determining the degree of severity experienced by patients. Other non-validated tools and scales have also been shown to use similar outcome measures for ARD assessment ( Table 2 ). Twenty-two of the outcomes had a mode level of evidence of II and doubtful quality of evidence per the 1996 Hadorn criteria regarding the articles that used them [ 11 ]. Thus, consensus for outcome use based solely on the results of the literature search could not be reached and need further agreement on their use for ARD assessment through an expert panel.

Discussion

To the best of our knowledge, this systematic review is the first to compile a comprehensive list of tools and outcome measures for ARD severity. The systematic review process allowed us to capture 58 tools for ARD assessment from 227 RCTs and 196 NRTs. Although we were able to identify the most commonly used tools for ARD severity in their respective category (i.e., CRO = RTOG, CTCAE; PRO = VAS; QoL = DLQI, Skindex-16, EORTC QLQ-C30; CRO/PRO = RISRAS, STAT; BP = photography, reflectance spectrophotometry, and corneometer), we were unable to recommend a single tool that would comprehensively capture ARD severity.

Our findings are similar to a previously published literature showing low level evidence for robustness of tools specific for ARD severity. Behroozian et al. found doubtful quality and level of evidence in the studies’ robustness of methodology with varying levels of reliability regarding intra- and inter-rater scoring [ 12 ] upon examination of 13 skin toxicity tools used to score radiation dermatitis of breast cancer patients in 12 published studies [ 12 ]. Additionally, Schnur et al. (2011) published a systematic review of patient reported outcomes for measurement of breast cancer-related radiation dermatitis and found little standardization amongst trials in their approach to quantifying patient perspectives, often times having tools be limited in their focus to one QoL modality such as physical health [ 13 ]. Our results further confirm the lack of accepted consensus in ARD severity measurement underscoring the need for a gold standard measurement tool that incorporates clinician and patient perspectives, impact on QoL, and objective biophysical parameters. This sentiment is comparably echoed in Behroozian et al. where they reported that ARD assessment could not be designated to a single gold standard tool due to lack of sufficient evidence, and that further investigation is required [ 12 ]. Furthermore, our key findings indicate no recommendation for a single tool could be made based on the literature review. Many of the tools were utilized in studies having low level quality of evidence or only used in a limited number of studies. Although we were not able to collapse the evidence to a single ARD severity tool, we were able to identify strong tools within each of our categories (CRO, PRO, CRO/PRO, QoL, BP) which may facilitate future development of a new comprehensive tool for ARD severity.

To ensure optimal ARD patient care, the ability to make inter-trial comparisons of treatments is important. Tool and outcome consistency across studies is thus critical to achieve this end. As the current literature shows, there was extensive variability in the outcomes measured and tools used. Some studies used validated measurement tools while others utilized self-made, non-validated internal tools. ARD outcomes studied were also variable in their assessment across trials. This lends itself to making comparisons of interventions and management between studies difficult as the degree of benefit becomes harder to appreciate. Lam et al. (2020) noted divergence in radiation dermatitis assessment consistency between CROs and PROs whereby patients were more likely to disclose symptoms such as acute breast pain and late breast shrinkage whereas physicians were more likely to report these symptoms as acute breast edema [ 14 ]. Behroozian et al. found contrasts between clinician- and patient-reported ARD symptoms where clinicians tended to underreport the severity of symptoms when compared to patient groups [ 15 ]. To rectify this discordance, a tool which incorporates both clinician and patient perspectives was suggested [ 15 ]. With our findings, this increased variability in ARD assessment highlights the need for an international gold standard ARD assessment tool that is consensus-informed.

The limitations of our study include tool and outcomes quality interpretation and inclusion of only English language published studies. The 1996 Hadorn criteria to evaluate research study quality was used by previously by the Multinational Association for Supportive Care in Cancer (MASCC) for clinical practice guidelines for mucositis and radiation dermatitis [ 11 ]. However, there are limitations associated with its use in this review including the disproportionate focus on specific methodological flaws of the trial and its broad criteria [ 11 ]. Tool and outcomes quality interpretation was limited by the shortcomings of the trials that utilized the tool or measured the specific outcome, which potentially underscored those used in a limited number of trials. Further, only studies published in English language were reviewed. We did not use software to translate non-English articles to bypass errors in translation; thus, missing studies that were relevant to the research question could have been overlooked along with non-English tools for ARD. The systematic review underscores the considerable variability in the tools and outcome measures employed in assessing ARD severity, which presents a challenge for establishing standardized protocols across clinical trials. This lack of uniformity not only hampers the comparability of results across studies but also complicates the development of a universally accepted, gold-standard assessment tool. Given the broad range of instruments identified, from clinician-reported outcomes to biophysical parameters, the findings highlight the urgent need for more rigorous, high-quality research to validate these tools and assess their reliability in diverse clinical settings. Such efforts are essential for improving the consistency of ARD management and ensuring that patients receive the best possible care based on the most reliable data. However, our study is critical as it undertakes a comprehensive evaluation of the tools and outcome measures currently used to assess ARD, an endeavor that has significant implications for patient care. The discovery that the most frequently used tools lack high-quality evidence to support their use highlights a significant gap in ARD management.

This lack of standardized, validated assessment instruments impedes consistent patient care and makes it difficult to compare outcomes across different studies or treatment regimens. Consequently, this study's findings call for enhanced research efforts, particularly through high-quality randomized controlled trials, to develop and validate effective assessment tools. Future research should focus not only on validating existing tools but also on integrating clinician and patient perspectives, as well as objective biophysical measures, into a unified assessment framework. This approach could facilitate the development of a new, more robust tool that can serve as the gold standard for ARD assessment, ultimately leading to more effective and personalized treatment strategies for patients undergoing RT.

Conclusions

In conclusion, the diversity of existing literature has allowed for the compilation of an array of tools and measurements used in the assessment of ARD. This systematic review evaluated the quality of evidence supporting 58 different subjective and objective tools including clinician-reported outcomes, patient-reported outcomes, combined CRO/PROs, quality of life instruments, and biophysical parameters. The following were the most widely used tools in their respective categories: CROs (RTOG, CTCAE), PROs (VAS), CROs/PROs (RISRAS, STAT), QoL (DLQI, Skindex-16, EORTC QLQ-C30), and BPs (photography, reflectance spectrophotometry, corneometry). Overall, no strong recommendation for one single tool for ARD severity could be made based on published literature alone; however, our findings have identified the strongest ARD severity tools currently employed in ARD clinical trials, which provides preliminary insight for future development of a new comprehensive ARD severity tool. Based on these findings, MASCC conducted a Delphi consensus survey study with an expert panel to recommend evidence-based tools and outcomes for ARD severity assessment.

Availability of data and material (data transparency)

Research data are stored in an institutional repository and may be shared upon request to the corresponding author.

CRediT authorship contribution statement

Partha Patel: Data curation, Formal analysis, Investigation, Methodology, Project administration, Writing – original draft, Writing – review & editing. Syed Minhaj Rahman: Methodology, Project administration, Writing – review & editing. Tara Behroozian: Conceptualization, Data curation, Methodology, Project administration, Writing – review & editing. Samuel Finkelstein: Data curation, Formal analysis, Investigation, Writing – review & editing. Lauren Kanee: Formal analysis, Investigation, Writing – review & editing. Elwyn Zhang: Formal analysis, Investigation, Writing – review & editing. Suvam Banerjee: Formal analysis, Investigation, Writing – review & editing. Michele Aquilano: Formal analysis, Investigation, Writing – review & editing. Pierluigi Bonomo: Conceptualization, Methodology, Writing – review & editing. Raymond J. Chan: Conceptualization, Methodology, Writing – review & editing. Edward Chow: Conceptualization, Methodology, Resources, Software, Writing – review & editing. Adrian Wai Chan: Data curation, Formal analysis, Investigation, Methodology, Writing – review & editing. Jennifer Yin Yee Kwan: Data curation, Formal analysis, Investigation, Methodology, Writing – review & editing. Shing Fung Lee: Data curation, Formal analysis, Investigation, Methodology, Writing – review & editing. Henry Wong: Data curation, Formal analysis, Investigation, Methodology, Writing – review & editing. Corina van den Hurk: Conceptualization, Methodology, Project administration, Writing – review & editing. Mark Trombetta: Formal analysis, Investigation, Project administration, Writing – review & editing. Julie Ryan Wolf: Conceptualization, Methodology, Project administration, Resources, Software, Supervision, Writing – original draft, Writing – review & editing.

Acknowledgements

Additional coauthors: Gemma Caro, MD (Dermatology-Ente Ospedaliero Cantonale (EOC), Ospedale Regionale Bellinzona e Valli, Bellinzona, Switzerland); Dominic Chun Wan Chan, MD (Department of Oncology, Princess Margaret Hospital, HKSAR, China); Satoshi Hirakawa, MD (Department of Supportive Care in Cancer, Seirei Hamamatsu General Hospital, Hamamatsu, Japan); Gustavo Nader Marta, MD, PhD (Radiation Oncology, Hospital Sírio-Libanês, Sao Paulo, Brazil); Robert Miller, MD (Mayo Clinic, Rochester, Minnesota, 55905, US); Jolien Robijns, PhD (Hasselt University, Faculty of Medicine & Life Sciences-Linburg Clinical Research Center, Hasselt, Belgium).

Funding

No funding was provided for the completion of this paper. JRW and CvdH are chair and vice chair of the MASCC Oncodermatology Study Group, respectively. All authors are members of the MASCC Oncodermatology Study Group.

. Search strategy

Appendix B − Hadorn et al, 1996 criteria to evaluate research quality 10

Appendix C − level of evidence for each tool per Hadorn criteria

. Disease site Prevalence Rates

. The prevalence rate of countries across included studies

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