Clinical and Translational Oncology https://doi.org/10.1007/s12094-023-03219-0 RESEARCH ARTICLE Assessing the methodological strengths and limitations of the Spanish Society of Medical Oncology (SEOM) guidelines: a critical appraisal using AGREE II and AGREE‑REX tool Marilina Santero1 · Júlia de Mas1 · Berta Rifà1 · Inés Clavero1 · Irene Rexach1 · Xavier Bonfill Cosp1,2,3 Received: 11 May 2023 / Accepted: 16 May 2023 © The Author(s) 2023 Abstract Background The Spanish Society of Medical Oncology (SEOM) has provided open-access guidelines for cancer since 2014. However, no independent assessment of their quality has been conducted to date. This study aimed to critically evaluate the quality of SEOM guidelines on cancer treatment. Methods Appraisal of Guidelines for Research and Evaluation II (AGREE II) and AGREE-REX tool was used to evaluate the qualities of the guidelines. Results We assessed 33 guidelines, with 84.8% rated as “high quality”. The highest median standardized scores (96.3) were observed in the domain “clarity of presentation”, whereas “applicability” was distinctively low (31.4), with only one guideline scoring above 60%. SEOM guidelines did not include the views and preferences of the target population, nor did specify updating methods. Conclusions Although developed with acceptable methodological rigor, SEOM guidelines could be improved in the future, particularly in terms of clinical applicability and patient perspectives. Keywords Practice guidelines as topic · Cancer · Review · Medical oncology · Evidence-based medicine · Quality assessment Introduction on the evidence, and grading the strength of the recommen- dations [4]. All the process should be transparent, evidence- Published cancer research is increasing rapidly [1], and hav- based, and involve stakeholder input [5]. ing trustworthy health recommendations accessible is in The European Society for Medical Oncology (ESMO) high demand by guideline users [2]. For decision-makers, [6], the American Society of Clinical Oncology (ASCO) clinical practice guidelines (CPGs) have emerged to be a [7] and the Spanish Society of Medical Oncology (SEOM) reference to improve the quality of care by bringing together [8] guidelines are prepared and reviewed by leading experts the best available scientific evidence into specific recommen- and they provide a set of evidence-based recommendations dations to improve the quality of care [3]. Their development to serve as a guide for healthcare professionals and outline involves identifying and refining a subject area, forming a appropriate methods of treatment and care. Particularly, multidisciplinary panel of experts, conducting a systematic SEOM is a national, non-profit scientific society that pro- review of the evidence, formulating recommendations based motes studies, training, and research activities. SEOM wants to increase its role as a reference society, a source of opin- ion, and rigorous knowledge about cancer for all the agents * Marilina Santero involved, patients, and society in general [8]. The SEOM’s marilinasantero@gmail.com project to develop guidelines started in 2010 as a perceived 1 Universitat Autònoma Barcelona (UAB), Barcelona, Spain need by the Spanish oncologists, that required clinical prac- 2 Iberoamerican Cochrane Centre, Biomedical Research tice documents tailored to the peculiarities of the Spanish Institute Sant Pau (IIB Sant Pau), Barcelona, Spain healthcare system. Since 2014, open-access CPGs are avail- 3 CIBER Epidemiología y Salud Pública (CIBERESP), able to facilitate clinical practice providing an eminently Barcelona, Spain 13 Vol.:(0123456789) Clinical and Translational Oncology practical view of the most relevant considerations concern- file 1). Before starting the review process, we published a ing various cancer-related scenarios [9]. research protocol online in the Open Science Framework To date, no independent assessment of its quality has (OSF) repository [14]. been made, despite reports indicating that critical reviews of guidelines worldwide show they are not sufficiently robust Eligibility criteria [10, 11]. The quality of CPGs can be assessed using various tools, such as AGREE II and AGREE-REX, which evaluate We considered a definition for CPGs previously reported by the methodological quality, rigor, and transparency of guide- the Institute of Medicine (IOM) [15]. The inclusion criteria line development. These tools can help to identify areas for (all criteria required) were as follows: (a) CPGs for cancer improvement in CPGs and ensure that they are evidence- treatment; (b) supported by SEOM; (c) published in English, based and relevant to clinical practice. In this context, this or Spanish; and (d) published from 2014 onwards. study aims to critically assess the quality of CPGs on cancer Exclusion criteria (any criterion required) were: (a) CPGs treatment published by SEOM since 2014. on cancer prevention, screening, detection, diagnostic, mapping, staging, imaging, scanning, or follow-up without treatment recommendations; (b) CPGs not containing rec- Methods ommendations for specific cancer (pathology-related guide- lines); or (c) unavailable papers, surveys, audits, editorials, Study design letters to the editor, case reports or notes. This is a critical review of CPGs. We followed rigorous Literature search standards [12] and reported our results according to the Preferred Reporting Items for Systematic Review and Meta- In February 2022, we identified eligible CPGs through elec- Analysis (PRISMA) 2020 checklist [13] (Supplementary tronic searches on MEDLINE (via PubMed), the SEOM Fig. 1  PRISMA 2020 flowchart. From: Page MJ, McKenzie JE, atic reviews. BMJ 2021;372:n71. https://​doi.​org/​10.​1136/​bmj.​n71. Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The For more information, visit: http://​www.​prisma-​state​ment.​org/ PRISMA 2020 statement: an updated guideline for reporting system- 13 Clinical and Translational Oncology Table 1  Characteristics of included clinical practice guidelines by the Spanish Society of Medical Oncology (SEOM) (n = 33) Cancer type Guidelines [references] Collaborative developers Breast SEOM clinical guidelines in advanced and recurrent breast cancer (2018)* GEICAM, SOLTI [27, 60] SEOM clinical guidelines in early stage breast cancer (2018) [23, 55]* GEICAM, SOLTI SEOM clinical guidelines in hereditary breast and ovarian cancer (2019)* Sección SEOM de Cáncer Hereditario [38, 70] Cervical SEOM clinical guidelines for cervical cancer (2019)* [29, 82] GEICO Colorectal SEOM clinical guidelines for diagnosis and treatment of metastatic GEMCAD, TTD colorectal cancer (2018)* [33, 66] SEOM clinical guideline on hereditary colorectal cancer (2019)* [39, 65] Sección SEOM de Cáncer Hereditario SEOM-GEMCAD-TTD clinical guidelines for localized rectal cancer GEMCAD, TTD (2021)* [26, 59] Endometrial SEOM GEICO clinical guidelines on endometrial cancer (2021)*** [25, GEICO 57, 58] Gastrointestinal, Gastric or SEOM Clinical Guideline for gastrointestinal sarcomas (GIST) (2016) [48] GEIS gastroesophageal junction SEOM clinical guideline for the diagnosis and treatment of gastric cancer GEIS, GEMCAD, TTD (GC) and gastroesophageal junction adenocarcinoma (GEJA) (2019)*** [44,67–69] Glioblastoma SEOM clinical guidelines for diagnosis and treatment of glioblastoma GEINO (2017) [45] Glioma anaplastic [24, 56] SEOM clinical guidelines for anaplastic gliomas (2017)** [54, 83] GEINO Glioma low grade [54, 83] SEOM clinical guideline of diagnosis and management of low-grade GEINO glioma (2017)** Head and neck SEOM clinical guidelines for the treatment of head and neck cancer TTCC​ (2020)*** [46, 84, 85] Hepatic Diagnostic and treatment for hepatocellular carcinoma. Actualization of AEEH, AEC, GEMCAD, SERAM, the consensus document by AEEH, AEC, SEOM, SERAM, SERVEI and SERVEI, SETH, TTD SETH (2021)* [31, 62, 63] Kidney [40, 86–88] SEOM clinical guideline for treatment of kidney cancer (2019)*** [50, SOGUG​ 86–88] Lung SEOM clinical guidelines for the treatment of non-small cell lung cancer GECP (2018)* [42, 89] SEOM clinical guidelines for the treatment of small cell lung cancer GECP (SCLC) (2019) [30] Lymphoma SEOM clinical guidelines for the treatment of follicular non-Hodgkin’s GOTEL lymphoma (2015) [49] SEOM clinical guidelines for the treatment of Hodgkin’s lymphoma GOTEL (2015) [52] Medulloblastoma SEOM clinical guideline for management of adult medulloblastoma GEINO (2020) [41] Melanoma SEOM clinical guideline for the management of cutaneous melanoma GEM (2020)* [43, 90, 91] Mesothelioma SEOM clinical guidelines for the treatment of malignant pleural GECP mesothelioma (2020) [47] Nasopharynx SEOM TTCC clinical guideline in nasopharynx cancer (2021)* [53, 92] TTCC​ Neuroendocrine SEOM clinical guidelines for the diagnosis and treatment of gastroentero- GETNE pancreatic and bronchial neuroendocrine neoplasms (NENs) (2018)* [37, 93] Ovarian SEOM clinical guideline in ovarian cancer (2020)* [50, 94, 95] GEICO Pancreatic and biliary SEOM clinical guidelines for pancreatic and biliary tract cancer (2020)* GEMCAD, TTD [34, 96, 97] Prostate SEOM clinical guidelines for the treatment of advanced prostate cancer SOGUG​ (2020)*** [36, 98–100] Sarcoma SEOM Clinical Guideline of management of soft tissue sarcoma (2020)* GEIS [28, 61] 13 Clinical and Translational Oncology Table 1  (continued) Cancer type Guidelines [references] Collaborative developers Testicular SEOM clinical guidelines for the management of germ cell testicular GG, SGCCG​ cancer (2016) [22] Thymic SEOM GECP GETTHI Clinical Guidelines for the treatment of patients GECP, GETTHI with thymic epithelial tumors (2021) [51] Thyroid SEOM clinical guideline thyroid cancer (2019)* [32, 64] GETNE Urothelial bladder SEOM clinical guideline for treatment of muscle‑invasive and metastatic SOGUG​ urothelial bladder cancer (2018)*** [35, 101, 102] AEC Spanish Surgeons Association, AEEH Spanish Association for the Study of the Liver, GECP Spanish Lung Cancer Group, GEICAM Span- ish Foundation Research Group in Breast Cancer, GEICO Spanish Group for Ovary Cancer Investigation, GEINO Spanish Group for Neuro Oncology Investigation, GEIS Spanish Group for Research on Sarcoma, GEM Spanish Multidisciplinary Melanoma Group, GEMCAD Spanish Multidisciplinary Group for Digestive Cancer, GETNE Spanish Group for Neuroendocrine and Endocrine Tumors, GETTHI Spanish Group for Orphan and Infrequent Tumors, GG Germinal Oncologic Group, GOTEL Oncologic Group for treatment and study of lymphomas, SERAM Spanish Society of Medical Radiology, SERVEI Spanish Society of Vascular and Interventionist Radiology, SETH Spanish Society for Throm- bosis and Hemostasia, SGCCG​Spanish Germ Cell Cancer Group, SOGUG​: Spanish Oncology Genito Urinary Group, SOLTI Spanish Group for the study, treatment and other experimental strategies in solid tumors, TTCC​ Spanish Group for the Treatment of Head and Neck Tumors, TTD Digestive Tumor Treatment Group *thread **GPC + correction ***thread + correction website, and the Clinical and Translational Oncology Jour- clarity of presentation; (5) applicability; and (6) editorial nal website, an international journal where SEOM guide- independence. Each item, including the two global rating lines are published. The search strategy for MEDLINE is items, was rated on a 7-point scale (1—strongly disagree to presented in Supplementary file 2. 7—strongly agree). As a complement to AGREE II, only for the guidelines scored as “high quality”, we used the instru- Screening and data extraction ment AGREE-REX, a new tool designed in 2019 to evaluate and optimize the clinical credibility and implementability Two reviewers performed an independent title and abstract of CPGs recommendations [19, 20]. AGREE-REX includes screening and full text afterwards. A third reviewer solved three key quality domains: clinical applicability (domain 1), disagreements. We used ­Rayyan®, a free web-based software values and preferences (domain 2), and implementability tool for conducting reviews [16]. Two reviewers extracted (domain 3), comprising 9 items that must be considered to data independently from included guidelines, in a previ- ensure that guidelines recommendations are of high quality. ously piloted form. We extracted a minimum dataset con- This tool was used by the same three independent authors on sidering the general characteristics of included CPGs. Also, a 7-point scale (1—strongly disagree to 7—strongly agree). we extracted data for the development of a recommenda- Furthermore, the evaluator was asked about the recommen- tion mapping. The lack of agreements was resolved through dation of this guideline in the appropriate context or in the discussion until a consensus was reached. When we found reviewers’ context. All the assessments were performed more than one guideline for a specific cancer (also of differ- independently and blinded using an internally piloted data ent guideline versions), we decided to create a publication extraction spreadsheet in Microsoft Excel 2019. thread analyzing the CPGs as a whole with all its references. Statistical analysis Quality assessment As suggested by the AGREE II instructions, we calcu- Three independent reviewers assessed the quality of included lated domain scores as a sum of the average scores of CPGs using the AGREE II tool [17], developed by the Inter- individual items from all evaluators’ assessments in the national Appraisal of Guidelines, Research and Evaluation domains. Then, we expressed the total scores for each (AGREE) research team. The tool has become a widely used domain as a percentage of the maximum possible score for standard for evaluating the methodological quality and trans- that domain. Therefore, the range of possible scores was parency of CPGs internationally [18]. The reviewers rated 0–100%, representing the worst and best possible ratings 23 key items across six domains: (1) scope and purpose; for each domain, respectively. Each domain assessed with (2) stakeholder involvement; (3) rigor of development; (4) a score of ≥ 60% was considered effectively addressed. We 13 Clinical and Translational Oncology Table 2  AGREE II standardized domain scores: CPGs by SEOM (n= 33) Guidelines [references] Domain (%) Overall score Recommenda- Qualitya tion D1 D2 D3 D4 D5 D6 Breast (early stage) [23, 55] 87.0 33.3 64.6 88.9 19.4 75.0 4.3 ( +) high Breast (advanced) [27, 60] 81.5 40.7 61.1 85.2 26.4 75.0 4.3 (+ +) high Breast and ovarian [38, 70] 90.7 53.7 59.7 90.7 16.7 77.8 5.0 ( +) moderate Cervical [29, 82] 46.3 35.2 58.3 87.0 37.5 75.0 4.7 (+) low Colorectal (metastasic) [33, 66] 98.1 44.4 79.2 100 23.6 75.0 4.7 (+ +) high Colorectal (hereditary) [39, 65] 81.5 42.6 79.9 100 54.2 75.0 5.0 (+ +) high Endometrial [25, 57, 58] 57.4 46.3 77.8 88.9 34.7 75.0 5.7 (+ +) high Gastric and gastroesophageal junction [44, 77.8 48.1 55.6 81.5 15.3 75.0 4.3 ( +) moderate 67–69] Gastrointestinal sarcomas [48] 100.0 53.7 86.1 100 48.6 75.0 4.7 (+ +) high Glioblastoma [45] 92.6 63.0 77.1 100 77.8 75.0 4.7 (+ +) high Glioma (anaplasic) [24, 56] 83.3 40.7 63.9 92.6 11.1 75.0 6.0 (+ +) high Glioma (low grade) [54, 83] 92.6 59.3 72.2 100 27.8 75.0 5.0 (+ +) high Head and neck [46, 84, 85] 75.9 53.7 70.1 100 13.9 75.0 5.3 ( +) high Hepatocellular [31, 62, 63] 90.7 63.0 76.4 98.1 31.9 75.0 5.0 (+ +) high Kidney [40, 86–88] 87.0 53.7 68.8 100 45.8 75.0 6.0 (+ +) high Lung (small cell) [30] 55.6 50.0 70.8 94.4 37.5 80.6 6.0 ( +) high Lung (non-small cell) [42, 89] 72.2 44.4 68.1 96.3 19.4 75.0 4.3 ( +) high Lymphoma (follicular non-Hodgkin) [49] 72.2 50.0 77.1 100 15.3 75.0 5.7 (+ +) high Lymphoma (Hodgkin) [52] 72.2 50.0 56.3 100 18.1 75.0 5.7 ( +) moderate Medulloblastoma [41] 90.7 50.0 75.0 98.1 40.3 75.0 6.0 (+ +) high Melanoma [43, 90, 91] 75.9 50.0 68.8 98.1 16.7 75.0 4.3 ( +) high Mesothelioma [47] 81.5 50.0 82.6 100 23.6 77.8 5.0 (+ +) high Nasopharynx [53, 92] 87.0 50.0 77.1 100 19.4 75.0 4.7 (+ +) high Neuroendocrine [37, 93] 88.9 53.7 74.3 100 33.3 75.0 5.7 (+ +) high Ovarian [50, 94, 95] 96.3 53.7 81.9 94.4 33.3 77.8 5.0 (+ +) high Pancreatic and biliary [34, 96, 97] 79.6 50.0 63.9 98.1 36.1 75.0 5.7 ( +) high Prostate [36, 98–100] 90.7 55.6 74.3 96.3 54.2 75.0 5.7 (+ +) high Rectal [26, 59] 87.0 46.3 83.3 100 25.0 75.0 5.3 (+ +) high Sarcoma [28, 61] 94.4 48.1 84.0 100 59.7 69.4 6.0 (+ +) high Testicular [22] 66.7 24.1 59.7 88.9 13.9 69.4 5.7 (+) moderate Thymic epithelial [51] 92.6 51.9 80.6 100 34.7 75.0 4.3 (+ +) high Thyroid [32, 64] 83.3 40.7 77.1 100 45.8 72.2 5.7 (+ +) high Urothelial bladder [35, 101, 102] 96.3 48.1 71.5 100 25.0 75.0 5.7 (+) high D1 Scope and purpose, D2 Stakeholder involvement, D3 Rigor of development, D4 Clarity of presentation, D5 Applicability, D6 Editorial inde- pendence a CPGs were considered as “high" quality if they scored ≥ 60% in at least three of six AGREE II domains, including domain 3. If three domains or more were assessed with a score of ≥ 60%, except domain 3, they were considered to be of “moderate” overall quality. CPGs scoring < 60% in two or more domains and < 50% in domain 3 were considered as “low" quality considered CPGs as “high quality” if they scored ≥ 60% We performed all statistical analyses in RStudio [21], in at least three of six AGREE II domains, including including boxplot and ggplot2 packages. Descriptive domain 3. If three domains or more were assessed with analyses were performed by estimators’ central tendency a score of ≥ 60%, except domain 3, they were considered and dispersion including mean and standard deviation to be of “moderate quality” overall quality. Finally, CPGs (SD) or median and interquartile ranges (IQR). We cal- scored < 60% in two or more domains and scored < 50% in culated inter-rater reliability using the average intraclass domain 3 were considered “low quality”. correlation coefficient (ICC) (two-way random mixed model), including the 95% confidence interval. ICC can 13 Clinical and Translational Oncology Items Guidelines, author year Domain 1 Domain 2 Domain 3 Domain 4 Domain 5 Domain 6 I1 I2 I3 I4 I5 I6 I7 I8 I9 I10 I11 I12 I13 I14 I15 I16 I17 I18 I19 I20 I21 I22 I23 Breast, Ayala 2018 7.0 5.7 6.0 3.7 1.0 4.3 3.3 3.3 7.0 5.3 5.7 6.3 7.0 1.0 7.0 6.0 6.0 2.0 3.0 2.3 1.3 4.0 7.0 Breast, Chacón López-Muñiz 2019 7.0 5.0 5.7 5.3 1.0 4.0 4.3 2.3 5.7 4.3 5.7 7.0 7.0 1.0 6.7 6.3 5.3 3.7 2.7 2.0 2.0 4.0 7.0 Breast and ovarian, González-Santiago 2019 7.0 6.7 5.7 5.3 1.3 6.0 4.3 5.3 5.0 4.0 4.7 5.3 7.0 1.0 7.0 6.0 6.3 1.7 4.0 1.3 1.0 4.3 7.0 Cervix, de Juan Ferré 2019 3.3 4.7 3.3 4.7 1.0 3.7 4.0 2.7 5.7 4.3 5.0 6.3 7.0 1.0 6.7 6.3 5.7 3.3 3.0 4.0 2.7 4.0 7.0 Colorectal, Gómez-España 2018 7.0 7.0 6.7 5.3 1.0 4.7 5.7 6.3 6.3 6.7 6.3 6.7 7.0 1.0 7.0 7.0 7.0 5.3 1.7 1.7 1.0 4.0 7.0 Colorectal, Guillén-Ponce 2019 5.0 6.7 6.0 5.0 1.0 4.7 6.0 6.7 6.7 5.7 6.7 6.7 7.0 1.0 7.0 7.0 7.0 6.0 5.0 5.0 1.0 4.0 7.0 Endometrial, Barretina-Ginesta 2021 7.0 6.3 6.7 4.7 1.0 5.7 5.0 5.7 6.3 6.7 6.7 7.0 7.0 1.0 6.7 6.7 5.7 4.7 4.3 2.3 1.0 4.0 7.0 Gastric and GE junction, Martín-Richard 2019 6.3 6.0 4.7 5.7 1.0 5.0 3.7 2.3 6.0 3.3 5.7 5.7 7.0 1.0 5.3 5.7 6.7 4.7 1.0 1.0 1.0 4.0 7.0 Gastrointestinal sarcomas, Poveda 2016 7.0 7.0 7.0 5.7 1.0 6.0 7.0 6.7 7.0 6.7 7.0 7.0 7.0 1.0 7.0 7.0 7.0 6.0 6.3 1.7 1.7 4.0 7.0 Glioblastoma, Martinez-Garcia 2017 7.0 6.0 6.7 6.7 1.0 6.7 4.3 6.7 6.7 6.3 6.3 6.7 7.0 1.0 7.0 7.0 7.0 6.3 6.7 3.3 6.3 4.0 7.0 Glioma, Balaña 2017 5.7 5.3 7.0 5.3 1.0 4.0 6.0 3.7 5.3 4.7 4.7 6.3 7.0 1.0 6.7 6.7 6.3 2.0 1.7 2.0 1.0 4.0 7.0 Glioma, Sepúlveda-Sánchez 2018 7.0 6.3 6.3 7.0 1.0 5.7 6.3 1.7 7.0 6.0 6.7 7.0 7.0 1.0 7.0 7.0 7.0 4.3 1.7 1.7 3.0 4.0 7.0 Head and neck, Mesia 2020 6.0 5.7 5.0 6.3 1.0 5.3 5.3 4.3 6.7 5.3 5.3 6.7 7.0 1.0 7.0 7.0 7.0 3.3 1.7 1.3 1.0 4.0 7.0 Hepatocellular, Reig 2021 7.0 6.0 6.3 6.7 1.7 6.0 5.0 5.0 6.7 7.0 7.0 6.0 7.0 1.0 7.0 7.0 6.7 3.7 3.3 3.7 1.0 4.0 7.0 Kidney, Lázaro 2019 7.0 6.0 5.7 6.0 1.0 5.7 4.7 2.3 7.0 5.3 6.7 7.0 7.0 1.0 7.0 7.0 7.0 4.7 2.3 5.0 3.0 4.0 7.0 Lung, Dómine 2019 3.0 5.3 4.7 5.0 2.0 5.0 4.7 5.7 5.7 5.0 6.7 6.3 7.0 1.0 6.7 6.7 6.7 5.0 4.7 1.7 1.7 4.7 7.0 Lung, Majem 2018 4.3 5.7 6.0 5.0 1.0 5.0 5.0 5.7 6.3 4.7 4.3 6.7 7.0 1.0 7.0 6.7 6.7 2.7 2.3 2.7 1.0 4.0 7.0 Lymphoma (follicular non-Hodgkin), Provencio 2019 5.0 5.7 5.3 5.7 1.0 5.3 7.0 5.3 5.7 5.7 6.3 7.0 7.0 1.0 7.0 7.0 7.0 2.3 2.3 2.0 1.0 4.0 7.0 Lymphoma (Hodgkin), Rueda Domiguez 2015 4.7 6.0 5.3 6.0 1.0 5.0 7.0 3.7 1.3 1.3 6.7 7.0 7.0 1.0 7.0 7.0 7.0 1.7 1.7 2.0 3.0 4.0 7.0 Medulloblastoma, Luque 2020 7.0 6.3 6.0 6.0 1.0 5.0 5.3 5.7 6.7 5.0 6.7 6.7 7.0 1.0 6.7 7.0 7.0 5.3 4.7 2.7 1.0 4.0 7.0 Melanoma, Majem 2020 5.7 6.0 5.0 6.0 1.0 5.0 4.7 5.3 6.0 5.0 5.3 6.7 7.0 1.0 7.0 6.7 7.0 3.3 2.0 1.7 1.0 4.0 7.0 Mesotelioma, Nadal 2020 5.0 6.3 6.3 5.0 1.0 6.0 7.0 6.7 6.3 5.7 7.0 7.0 7.0 1.0 7.0 7.0 7.0 3.7 3.3 1.7 1.0 4.3 7.0 Nasopharynx, Rueda Dominguez 2021 7.0 6.3 5.3 5.7 1.0 5.3 5.7 5.3 7.0 5.3 6.7 7.0 7.0 1.0 7.0 7.0 7.0 3.3 2.3 2.0 1.0 4.0 7.0 Neuroendocrine, González-Flores 2018 7.0 6.3 5.7 6.0 1.0 5.7 5.3 3.3 6.7 6.7 6.7 7.0 7.0 1.0 7.0 7.0 7.0 3.0 3.3 4.7 1.0 4.0 7.0 Ovarian, Redondo 2020 7.0 6.7 6.7 5.3 1.0 6.3 5.3 7.0 7.0 6.7 6.3 7.0 7.0 1.0 7.0 7.0 6.0 5.0 4.3 1.7 1.0 4.3 7.0 Pancreatic and biliary, Gómez-España 2020 5.3 6.3 5.7 5.3 1.7 5.0 3.7 3.0 5.7 5.7 6.0 6.7 7.0 1.0 6.7 7.0 7.0 4.7 2.3 2.3 3.3 4.0 7.0 Prostate, González del Alba 2020 7.0 6.3 6.0 6.3 1.0 5.7 5.7 4.3 6.3 6.0 6.7 6.7 7.0 1.0 6.7 6.7 7.0 5.7 3.3 6.0 2.0 4.0 7.0 Rectal, Capdevila 2021 5.7 6.3 6.7 5.0 1.0 5.3 6.0 7.0 7.0 6.3 6.7 7.0 7.0 1.0 7.0 7.0 7.0 2.3 5.7 1.0 1.0 4.0 7.0 Sarcoma, de Juan Ferré 2020 7.0 6.3 6.7 5.3 2.0 4.3 7.0 6.7 6.7 6.7 6.7 6.7 7.0 1.0 7.0 7.0 7.0 6.3 6.3 3.0 2.7 3.3 7.0 Testicular, Aparicio 2016 7.0 3.0 5.0 3.3 1.0 3.0 4.7 2.0 6.0 3.3 5.7 7.0 7.0 1.0 7.0 6.3 5.7 1.0 3.0 1.0 2.3 3.3 7.0 Thymic epithelial, Remon 2021 7.0 6.0 6.7 6.0 1.0 5.3 6.7 7.0 6.7 5.7 6.0 6.7 7.0 1.0 7.0 7.0 7.0 4.3 4.7 2.3 1.0 4.0 7.0 Thyroid, Gallardo 2019 7.0 5.7 5.3 4.7 1.0 4.7 6.3 5.3 6.7 5.7 6.3 6.7 7.0 1.0 7.0 7.0 7.0 4.0 4.3 4.3 2.3 3.7 7.0 Urothelial bladder, González del Alba 2018 7.0 6.7 6.7 5.3 1.0 5.3 4.3 6.7 5.7 5.3 6.0 6.3 7.0 1.0 7.0 7.0 7.0 2.7 2.3 4.0 1.0 4.0 7.0 be interpreted as follows, 0–0.2 (poor agreement); 0.3–0.5 Results (fair agreement); 0.5–0.75 (moderate agreement); 0.75–0.9 (strong agreement); and > 0.9 (almost perfect agreement). The PRISMA statement flow diagram (Fig. 1) depicts the flow of information through the different phases of our criti- cal review. Finally, 208 relevant references remained for the full-text review, and 69 met the inclusion criteria for detailed 13 Clinical and Translational Oncology ◂Fig. 2  AGREE II item scores of included clinical practice guide- of development), the standardized scores ranged from 55.6 lines by the Spanish Society of Medical Oncology (SEOM) (n = 33). to 86.1 (median = 74.3), and 28 of the CPGs scored above I1—The overall objective(s) of the guideline is (are) specifically described; I2—The health question(s) covered by the guideline is 60.0%. The CPG for gastrointestinal sarcomas (GIST) [48] (are) specifi- cally described; I3—The population (patients, pub- obtained the highest scores, fulfilling 100% of the criteria in lic, etc.) to whom the guideline is meant to apply is specifically two domains, and > 85.0% in domain 3. described; I4—The guide- line development group includes indi- Figure 2 summarizes the item scores of AGREE II. viduals from all the relevant professional groups; I5—The views and preferences of the target population (patients, public, etc.) have been SEOM´s guidelines did not include in their development sought; I6—The target users of the guideline are clearly defined; I7— the views and preferences of the target population as can be Systematic methods were used to search for evidence; I8—The crite- inferred from item 5 (1–2, lowest scores). Moreover, they did ria for selecting the evidence are clearly described; I9—The strengths not clarify the updating methods either, so all obtained the and limitations of the body of evidence are clearly described; I10— The methods for formulating the recommendations are clearly worst score on the Likert scale in item 14 [45]. Also, items described; I11—The health benefits, side effects, and risks have been 18–21 regarding applicability scored in most cases lower considered in formulating the recommendations; I12—There is an than 4. Specifically, item 21, which refers to monitoring and explicit link between the recommendations and the supporting evi- audit criteria, has a median score of 1.7, being the guideline dence; I13—The guideline has been externally reviewed by experts prior to its publication; I14—A procedure for updating the guideline about glioblastoma the only one with a high score (6.3) in is provided; I15—The recommendations are specific and unambigu- this item [45]. ous; I16—The different options for management of the condition or Table 3 summarizes the standardized domain scores of health issue are clearly presented; I17—Key recommendations are AGREE-REX. Considering only the 28 high-quality CPGs easily identifiable; I18—The guideline provides advice and/or tools on how the recommendations can be put into practice; I19—The the mean overall AGREE-REX score was 48.5 (SD 11.0) guideline describes facilitators and barriers to its application; I20— with variability in performance across the individual 9 items. The potential resource impli- cations of applying the recommenda- The overall average score of the recommendations was 4.2 tions have been considered; I21—The guideline presents monitoring out of 7 (SD 0.6). The domain 1 “clinical applicability” got and/ or auditing criteria; I22—The views of the funding body have not influenced the content of the guideline; I23—Competing interests the highest scores (mean 75.8, SD 14.3) and the domain of guideline development group members have been recorded and 2 “values and preferences” got the lowest (mean 26.0, SD addressed 12.2). AGREE-REX items that scored the highest were “2. Applicability to Target Users” (mean 6.2; SD 0.7), and “1. Evidence” (mean 5.8; SD 0.5), while the lowest scores were analysis (excluded studies are presented in Supplementary observed for the item “5. Values and Preferences of Patients/ file 3). After considering the subsequent updates of the same Population” (mean 1.6; SD 1.1), and item “6. Values and CPGs, a total of 33 CPGs were included [22–54]. Preferences of Policy/Decision-Makers” (mean 1.6; SD 1.4). Table 1 presents the characteristics of the reviewed CPGs. We identified 25 cancer types. Colorectal and breast can- cer were the locations with more publications. On average, SEOM published seven guidelines per year. The year that Discussion witnessed the highest production was 2015 (13 guidelines), while 2017 had the lowest production (no guidelines pub- Overall, this critical review provides a thorough analysis lished). Among the identified guidelines, 28 had been pub- of the quality of CPGs published by the Spanish Society lished over three years ago. of Medical Oncology on cancer treatment along the last Table 2 summarizes the standardized domain scores of nine years. The study also identified the characteristics of the AGREE II and the overall quality rating of the CPGs. the guidelines, including the types of cancer covered and As per the pre-defined criteria of this study, 84.8% of CPGs the timeline of their publication. Ultimately, 33 guidelines (28) were considered “high quality” [23–28, 30–33, 39, were included and assessed, with 28 (85.0%) of those being 45, 55–66], 12.0% of CPGs (4) were assessed as “moder- considered “high quality” according to pre-defined criteria; ate quality” [22, 38, 44, 52, 67–70] and 3.0% CPGs (1) however, their applicability was found to be poor. One of were considered as “low quality” [29]. A moderate agree- the main strengths of the guidelines is the domain “clarity ment was present across all appraisers in this study (aver- of presentation”, in which it achieved the highest possible age measures ICC = 0.6; 95% CI 0.4, 0.7). Among the scores, whereas domain “applicability” was distinctively low six domains of AGREE II in all guidelines, four median (31.4), with only one of the CPGs scoring above 60.0%. scores were rated ≥ 60 (domains 1, 3, 4, and 6). The high- SEOM’s guidelines did not include in their formulation the est median standardized scores (96.3) were observed in views and preferences of the target population. Moreover, domain 4 (clarity of presentation), whereas domain 5 they did not specify the updating methods either. (applicability) was distinctively low (31.4), with only one Our results are pointing out that the SEOM is producing of the CPGs scoring above 60%. Regarding domain 3 (rigor CPGs that meet established standards for methodological 13 Clinical and Translational Oncology rigor. Being high scored in “clarity of presentation” is there are no search results that indicate whether ASCO or encouraging because it suggests that the SEOM is effec- ESMO have conducted critical appraisals of the quality tively communicating its recommendations to clinicians and of guidelines in cancer. One study used the AGREE tool patients. This result is particularly noteworthy given that to assess the quality of oncology guidelines developed in clear and understandable guidelines are essential for their different countries [77]. Another study used the AGREE effective implementation in clinical practice, ensuring that II tool to assess the methodological quality of clinical the recommendations are specific and unambiguous, the dif- practice guidelines with physical activity recommenda- ferent options for management of the condition or health tions for people diagnosed with cancer [76]. The results issues are clearly presented, and key recommendations are of these studies showed a heterogeneous quality of exist- easily identifiable [73]. ing guidelines in cancer, indicating a need for improve- However, it is concerning that guidelines scored low ment in the development and reporting of guidelines. in “applicability” because it suggests that may not be as useful for clinicians and patients as they could be. Previ- Strengths and limitations ous research indicates that for clinical guidelines to have an actual impact on processes and ultimately outcomes of Our research has multiple strengths. We implemented a thor- care, they need to be not only well developed and based ough search strategy to locate SEOM guidelines, and utilized on scientific evidence but also disseminated and imple- a standardized and globally recognized guidelines appraisal mented in ways that ensure they are actually used by clini- tool (AGREE II). While our study is not the first to critically cians [71, 72]. Implementation science frameworks have appraise guidelines [11, 20], it is noteworthy that we are one been used to address challenges in implementing clinical of the few studies to use the AGREE-REX tool (developed practice guidelines [72]. Also, SEOM's guidelines did not in 2019) for assessing cancer guidelines. Furthermore, to include the views and preferences of the target population the best of our knowledge, this is one of the first independ- or specify the updating methods indicates that there is ent evaluations of the quality of cancer treatment guidelines room for improvement in the guidelines development pro- from a scientific society, which adds to the significance of cess. Incorporating patient perspectives into guidelines our findings. development can improve the relevance and applicability Nevertheless, there are also some limitations to our study of guidelines to clinical practice [73]. Specifying updat- that need to be acknowledged. First, our study only assessed ing methods is also important to ensure that guidelines the methodological quality of the SEOM guidelines and remain up-to-date and reflect the latest evidence [5]. did not evaluate their impact on clinical practice or patient Our critical review used both AGREE II and AGREE- outcomes. Second, while AGREE II and AGREE-REX are REX, tools used to evaluate practice guidelines, but recognized appraisal tools, they do have limitations, and with different focuses. AGREE II is designed to assess therefore, their application alone may not fully encompass the methodological quality and transparency of practice all aspects of guidelines quality. Third, we should not be guidelines, while AGREE-REX is designed to evaluate assumed that having a rigorous methodology means that the clinical credibility and implementability of prac- all issues have been dealt with exhaustively and accurately. tice guidelines [17, 20]. AGREE-REX is a complement Some recommendations could not be sufficiently detailed to AGREE II, rather than an alternative, and provides a to guide treatment decisions in specific situations, such as blueprint for practice guideline development and report- advanced cancer, end of life, elderly, and comorbidities. ing. Although scoring high in AGREE II is essential, it Fourth, we cannot assume that clinicians’ adherence to these does not guarantee that recommendations are optimal for guidelines is high, so having high-quality guidelines does targeted users nor the optimal implementation of the rec- not necessarily mean that clinicians are making the right ommendations [19]. In our review, we found that recom- decisions, as many studies previously reported [78–80]. mendations from guidelines scored as “high quality” on Finally, due to the nature of the study design, our results AGREE II, did not align with the values and preferences are limited to the time period of guidelines publication and of their target users, whether they be patients or policy do not account for any subsequent updates or changes to the makers, according to AGREE-REX. This result has been guidelines. previously reported elsewhere [20]. In this context, we It is worth considering the potential redundancy with consider that guidelines that are developed without con- other cancer treatment guidelines developed by international sidering the values and preferences may not be relevant organizations or societies. While our study focuses on the or applicable to their needs, which can lead to poor adher- SEOM guidelines, it is important to acknowledge that other ence and outcomes. guidelines exist that may provide valuable insights and rec- Finally, there have been several critical appraisals ommendations. It is worth reflecting on the extent to which of the quality of guidelines in cancer [20, 74–76], but these guidelines, taken individually, contribute different 13 Clinical and Translational Oncology Table 3  AGREE-REX Guidelines [references] Domain (%) Mean score (SD) standardized domain scores: CPGs by SEOM (n= 28) D1 D2 D3 Clinical Values and Imple- applicability preferences mentability Breast (early stage) [23, 55] 77.8 45.8 65.5 63.0 (0.2) Breast (advanced) [27, 60] 72.2 30.6 51.7 41.3 (0.1) Colorectal (metastasic) [33, 66] 85.2 54.2 20.7 53.4 (0.0) Colorectal (hereditary) [39, 65] 96.3 25.0 38.0 53.1 (0.4) Endometrial [25, 57, 58] 35.2 19.4 27.6 27.4 (0.1) Gastrointestinal sarcomas [48] 92.6 12.5 0.0 35.0 (0.5) Glioblastoma [45] 98.2 27.8 13.8 46.6 (0.5) Glioma (anaplasic) [24, 56] 64.8 5.6 34.5 35.0 (0.3) Glioma (low grade) [54, 83] 87.0 34.7 58.6 60.1 (0.3) Head and neck [46, 84, 85] 59.3 26.4 58.6 48.1 (0.2) Hepatocellular [31, 62, 63] 92.6 56.9 82.8 77.4 (0.2) Kidney [40, 86–88] 77.8 26.4 44.8 49.7 (0.3) Lung (small cell) [30] 88.9 29.1 31.0 49.7 (0.3) Lung (non-small cell) [42, 89] 64.8 9.7 0.0 24.8 (0.3) Lymphoma (follicular non-Hodgkin) [49] 70.4 45.8 62.1 59.4 (0.1) Medulloblastoma [41] 79.6 27.8 62.1 56.5 (0.3) Melanoma [43, 90, 91] 85.2 40.3 55.1 60.2 (0.2) Mesothelioma [47] 92.6 27.8 0.0 40.1 (0.5) Nasopharynx [53, 92] 75.9 29.2 62.1 55.7 (0.2) Neuroendocrine [37, 93] 64.8 19.4 41.4 41.9 (0.2) Ovarian [50, 94, 95] 94.5 37.5 17.2 49.7 (0.4) Pancreatic and biliary [34, 96, 97] 66.7 27.8 44.8 46.4 (0.2) Prostate [36, 98–100] 72.2 34.7 44.8 50.6 (0.2) Rectal [26, 59] 74.1 12.5 37.9 41.5 (0.3) Sarcoma [28, 61] 75.9 29.2 17.3 40.1 (0.3) Thymic epithelial [51] 75.9 27.8 69.0 57.6 (0.3) Thyroid [32, 64] 55.6 27.8 69.0 50.8 (0.2) Urothelial bladder [35, 101, 102] 87.0 18.1 27.6 44.2 (0.4) Domain 1 “Clinical applicability”: Items 1. Evidence, 2. Applicability to Target Users, 3. Applicability to Patients/Population; Domain 2 “Values and Preferences”: Items 4. Values and Preferences of Target Users, 5. Values and Preferences of Patients/Population, 6. Values and Preferences of Policy/Decision-makers, 7. Values and Preferences of Guideline Developers; Domain 3 “Implementability”: Items 8. Purpose, 9. Local application and Adoption. nuances and perspectives on cancer treatment and manage- of SEOM's guidelines and highlight areas where improve- ment. In light of this, it is worth asking whether a policy of ment can be made to enhance their relevance and adapting guidelines [81] might be a more efficient approach usefulness. than the development of new guidelines from scratch. Such an approach could help to reconcile the differences between guidelines and promote the uptake of best practices across Conclusions multiple contexts. SEOM guidelines on cancer treatment have been devel- Implications for practice and research oped with acceptable methodological rigor although they have some drawbacks that could be improved in the future, Overall, this review emphasizes the importance of pro- such as clinical applicability and items regarding patient ducing high-quality and applicable CPGs in oncology to views and preferences as well as unmeeting policies. guide clinical practice and improve patient outcomes. The findings provide insights into the strengths and limitations 13 Clinical and Translational Oncology Supplementary Information The online version contains supplemen- 9. Rodriguez CA, Martín M. SEOM guidelines 2015: a new era in tary material available at https://d​ oi.o​ rg/1​ 0.1​ 007/s​ 12094-0​ 23-0​ 3219-0. the collaboration with the Spanish Cancer Research Cooperative Groups. Clin Transl Oncol. 2015;17:937–8. Funding Open Access Funding provided by Universitat Autònoma 10. Barry HC, Cosgrove L, Slawson DC. Where clinical practice Barcelona (UAB). Marilina Santero is funded by Instituto de Salud guidelines go wrong. Am Fam Phys. 2022;105:350–2. Carlos III through the contract "FI19/00335” (Co-funded by European 11. Alonso-Coello P, Irfan A, Sola I, Gich I, Delgado-Noguera M, Social Fund "Investing in your future"). Rigau D, et al. The quality of clinical practice guidelines over the last two decades: a systematic review of guideline appraisal Data availability statement The data used in this study is available studies. BMJ Qual Saf. 2010. https://​doi.​org/​10.​1136/​qshc.​2010.​ upon request. Interested researchers can contact the corresponding 042077. author for access to the data. 12. Johnston A, Kelly SE, Hsieh S-C, Skidmore B, Wells GA. Sys- tematic reviews of clinical practice guidelines: a methodological Declarations guide. J Clin Epidemiol. 2019;108:64–76. 13. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Conflict of interest The authors declare that they have no competing Mulrow CD, et al. The PRISMA 2020 statement: an updated interests related to this work and they did not receive any funding for guideline for reporting systematic reviews. PLoS Med. 2021;18: this work. e1003583. 14. Santero M, de Mas J, Rexach I, Marín IC, Rifa B, Bonfill X, Ethical approval (Research involving human participants and/or ani‑ et al. Quality assessment of clinical practice guidelines from the mals) and Informedconsent Not applicable. Spanish Society of Medical Oncology (SEOM). 2022. Open Sci Framework. https://​doi.​org/​10.​17605/​OSF.​IO/​6BZFN. Open Access This article is licensed under a Creative Commons Attri- 15. Graham R, Mancher M, Wolman DM, Greenfield S, Steinberg E. bution 4.0 International License, which permits use, sharing, adapta- Committee on standards for developing trustworthy clinical prac- tion, distribution and reproduction in any medium or format, as long tice guidelines; institute of medicine. Clinical practice guidelines as you give appropriate credit to the original author(s) and the source, we can trust. 2011. provide a link to the Creative Commons licence, and indicate if changes 16. Ouzzani M, Hammady H, Fedorowicz Z, Elmagarmid A. were made. The images or other third party material in this article are Rayyan—a web and mobile app for systematic reviews. Syst Rev. included in the article's Creative Commons licence, unless indicated 2016;5:210. otherwise in a credit line to the material. If material is not included in 17. Brouwers MC, Kho ME, Browman GP, Burgers JS, Cluzeau F, the article's Creative Commons licence and your intended use is not Feder G, et al. 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