Abstract
Purpose
There has been growing amount of evidence supporting the benefits of physical activity (PA) on oncological patients’ cancer-related health outcomes. Although guidelines on cancer rehabilitation are widely available, the varying quality and practical applicability limited the clinical application of PA recommendations. To assist the future development of guidelines, in this systematic review, we evaluated the quality and applicability of current cancer rehabilitation guidelines with PA recommendations and synthesized PA recommendations for the oncological population.
Methods
A systematic search was conducted in PubMed, CINAHL, PEDro, EMBASE, and guideline repositories to identify guidelines with PA recommendations for cancer patients from 1 May 2016 to 1 June 2022. The quality of included guidelines was appraised using the tools “Appraisal of Guidelines for Research and Evaluation II” (AGREE II) and AGREE-REX (Recommendation Excellence). PA recommendations were synthesized from the guidelines.
Results
Sixteen guidelines were extracted. The AGREE II domain “clarity of presentation” obtained the highest score, while “applicability” received the lowest, ranging from 33.33% to 98.58%. The AGREE-REX domains “values and preferences” and “implementability” generally scored lower and ranged from 45.83% to 74.17% and 55% to 88.33%, respectively. Eight high-quality guidelines were identified, and the included PA recommendations were extracted.
Conclusion
There were some disparities in the quality of the included guidelines. Methodological weaknesses were commonly observed in domains “applicability,” “values and preferences,” and “implementability”; particular attention should be given to these domains when developing future guidelines. Furthermore, this analysis indicated that more rigorous, high-quality studies are needed to generate evidence for supporting PA recommendations and provide guidance on research gaps in the field of cancer rehabilitation.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Cancer is a major global health issue and one of the leading causes of death in the world, placing a substantial economic burden on both the societal and individual levels [1, 2]. In 2020, an estimated 19.3 million new cancer cases and 10.0 million cancer-related deaths occurred worldwide [1]. With advancements in cancer diagnosis, prognosis, and treatment options, the cancer mortality rates in America have declined significantly between 1991 and 2019 by a total of 32% [3], and the number of cancer survivors has increased. The 2006 Institute of Medicine landmark report “From cancer patient to cancer survivor: Lost in transition [4]” highlighted the unique issues in survivorship care faced by all cancer survivors. The report presented the potential physical and psychosocial challenges caused by cancer and/or cancer treatment (including surgery, chemotherapy, radiation therapy, hormonal therapy, immunotherapy, or a combination of the above treatment options). Cancer-related impairments include but are not limited to cardiotoxicity [5], sarcopenia [6], cancer-related fatigue [7], lymphedema [8], pain, osteoporosis, and chemotherapy-induced peripheral neuropathy [9, 10]. They can occur during active cancer treatment (acute response) and persist after treatment (long-term effects) or appear months or years after treatment ends (latent effects) [11].
The positive role of PA has been profoundly researched in cancer-related impairments and survivorship. Physical activity refers to any bodily movement produced by skeletal muscles or requires muscular contraction and results in energy expenditure [12]. As early as 1938, animal experiments have demonstrated PA as an inhibitory factor to tumor growth. Nowadays, there has been large research effort devoted to investigating the role of PA in cancer survivors; many positive impacts have been shown including lowered cancer mortality risks and improved cancer-related health outcomes [13]. According to a systematic review [14], a combined resistance training with aerobic exercise program can reduce cancer-related fatigue and improve patients’ quality of life. A clinical trial suggested that active exercises prevented lymphedema in female breast cancer patients [15]. A high-quality controlled trial demonstrated that home-based aerobic exercise combined with supervised resistance training significantly reduced arthralgia associated with aromatase inhibitor therapy in breast cancer patients [16]. Emerging evidence suggests that exercise can harness the immune system to improve colorectal cancer survival rate [17, 18]. Given the promising effects of PA intervention in this patient population, an increasing number of initiatives for the integration of PA into cancer care continuum have been put forward [19].
Clinical practice guidelines (CPGs) are protocols developed based on systematic reviews of the current available evidence and the analyses of the benefits and harms. CPGs can assist clinicians with clinical decision-making and help identify gaps that may require further research [20]. Implementing good clinical practice guidelines could optimize clinical care quality while decreasing medical expenses and minimizing potential harm due to ineffective or unsafe interventions. Many guidelines and recommendations have supported PA intervention for cancer patients, but the wide variation in the quality of these guidelines may influence clinicians providing the optimal treatment for patients. At present, many quality assessment tools are frequently used to evaluate the guidelines [21]. As one of the most widely used instruments, the “Appraisal of Guidelines for Research and Evaluation (AGREE) II” was also recommended by WHO [22]. Numerous CPGs with PA recommendations for cancer patients have been appraised by this instrument and have met rigorous methodological quality criteria [23, 24]. However, previous studies [25] suggested that there may be a conflict between guideline methodologic quality and recommendation validity. Having high AGREE II scores does not guarantee that CPG recommendations are optimal, trustworthy, credible, or practical to implement, since some CPGs may have omitted common clinical situations or recommendations of uncertain clinical validity, which may affect the clinical application of recommendations [25, 26]. As a complementary tool to AGREE II, the Appraisal of Guidelines Research and Evaluation–Recommendations Excellence (AGREE-REX) was specifically developed to evaluate the clinical credibility and implementability of recommendations [26]. Therefore, the purpose of this review was to understand and appraise the quality of current CPGs with PA recommendations for cancer survivors and the clinical application of their recommendations using the AGREE II and AGREE-REX tools. In addition, we also wanted to identify research gaps through the synthesis of PA recommendations.
Materials and methods
Study design
We conducted a methodological appraisal of CPGs using the AGREE II and AGREE-REX instruments and reported our results according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement. The protocol was registered in the International Prospective Register of Systematic Reviews (PROSPERO) with the registration number CRD42021265329.
Search strategy
We conducted a systematic search for guidelines and employed three approaches to identify guidelines with PA recommendations for cancer survivors.
We searched electronic databases including PubMed, CINAHL, PEDro, and EMBASE. In addition, we supplemented database searches by a hand-search of guideline repositories. We also conducted a supplementary search by scanning the reference lists of review articles and relevant conference abstracts to identify eligible CPGs. A publication date limitation from 1 May 2016 to 1 June 2022 was set for all searches.
We adopted a combination of Medical Subject Headings (MeSH), free text terms, including “neoplasms, cancer, tumor, exercise, physical activity, rehabilitation, guideline, practice guideline, recommendation” as database search strategy. The detailed search strategies were provided in the Supplementary Table S1.
Selection criteria
The eligibility of CPGs was identified according to the following criteria.
Inclusion criteria were as follows: ① CPGs published in English; ② recently published or updated from 1 May 2016 to 1 June 2022; ③ published in peer-reviewed scientific journals; ④ exclusive to adult (aged ≥ 18 years) cancer population; ⑤ provided specific PA intervention recommendations on at least one PA parameter (frequency, intensity, duration and/or type); and ⑥ provided recommendations and explicit methodology.
Exclusion criteria were as follows: ① did not include PA as part of intervention strategy; ② published or updated prior to 1 May 2016; ③ CPGs for pharmacological or rehabilitation interventions without PA recommendations; ④ received commercial funding; ⑤ provided recommendations for PA referrals; and ⑥ focused on cancer prevention other than cancer or cancer-related symptoms and impairments management.
Study selection
We first imported all results into Endnote (version X9, Clarivate Analytics) reference manager program, and eliminated duplicates using the software and manually. Two independent reviewers (X. Zhou, C.H. Li) scanned the remaining records against the titles and abstracts. For records that were considered potentially relevant, we retrieved the full-text guidelines following the inclusion and exclusion criteria. If any disagreement arose, a decision was made by discussion with a third reviewer (X.G. Lai).
Data extraction and summary
Data screening and extraction were performed by two authors (X. Zhou, C.H. Li). One author performed data extraction which was confirmed for consistency by a second author. A third independent author (X.G. Lai) adjudicated unresolved discrepancies. We extracted and summarized the relevant information on the CPGs and recommendations on specific PA interventions. Main characteristics of the CPGs were collected, including title, organization/author, country of origin, publication year, methodological approach, and its scope.
Quality appraisal of the CPGs
The quality of each included guideline was appraised using the evaluation tools AGREE II and AGREE-REX by trained reviewers. All the reviewers received the online AGREE II training and evaluated CPGs on melanoma from published review [27] using the AGREE-REX tool to familiarize themselves with the instrument and compare their scores.
Both tools were rated on a 7-point scale ranging from 1 (strongly disagree) to 7 (strongly agree). Disagreement among reviewers of > 2 points for each item was discussed and resolved by consensus. Domain scores were calculated by adding scores of the individual items in a domain and standardizing the sum as a percentage of the maximum possible score for that domain, i.e., (obtained score – minimum possible score) / (maximum possible score – minimum possible score).
Two trained reviewers (C.H. Li, W.Q. Hou) independently appraised the methodological quality of each guideline by the AGREE II instrument. The instrument comprised 23 items within 6 domains: scope and purpose (items 1–3), stakeholder involvement (items 4–6), rigor of development (items 7–14), clarity of presentation (items 15–17), applicability (items 18–21), and editorial independence (items 22–23).
The Consortium of AGREE II does not set minimum domain scores or patterns of scores across domains to differentiate between high quality and low quality [28]. In this study, based on cut-off scores reported in previous guideline appraisals [23, 27, 29], we chose a cut-off “score of at least 60% for rigor of development (domain 3) as well as 60% in at least two other domains as a quality threshold. Guidelines meeting the cut-off scores were then evaluated by AGREE-REX.
Complementary to AGREE II, AGREE-REX is an instrument used for evaluating the clinical credibility and implementability of the recommendations. AGREE-REX consists of 3 domains, including “clinical applicability (Domain 1), values and preferences (Domain 2) and implementability (Domain 3)” composed of 9 items that must be considered to ensure that guideline recommendations were of high quality. This instrument was used by five independent reviewers (X. Zhou, C.H. Li, W.Q. Hou, X.G. Lai, and L.W. Zhai).
Similar to AGREE II, AGREE-REX does not provide a standard threshold to differentiate between high quality and poor quality. In this study, we set the threshold to be 60% and identified high-quality guidelines when all domain scores were above the threshold.
Statistical analysis
All domain scores were calculated by adding the item scores in each domain and converting the number into a standardized percentage of the maximum score for that domain. We also listed mean (± standard deviation, SD) for analysis of the descriptive statistics. We used the intraclass correlation coefficient (ICC) with a two-way random effects model [30] to test the inter-rater agreement (measure agreement among reviewers). The degree of agreement (ICC) was classified according to Cicchetti (1994): poor (< 0.40), fair (0.40–0.59), good (0.60–0.74), or excellent (0.75–1.00) [31]. P < 0.05 was considered statistically significant. Statistical analyses were conducted using SPSS (version 24, IBM Corporation, Armonk, NY, USA).
Results
CPGs characteristics
The literature search of the databases and supplementary sources identified 5108 records. We reviewed 182 full-text articles for eligibility after removing the duplicates and screening the titles and abstracts and 16 CPGs that met selection criteria were included in this systematic review (Fig. 1). Reasons for exclusion (n = 166) are provided in Fig. 1. The fourteen CPGs included four for breast cancer [32,33,34,35], one for head and neck cancer [36], one for multiple myeloma [37], one for cancer survivorship [38], three for nutrition management and/or physical activity in cancer patients [39,40,41], and six for symptom or condition management [42,43,44,45,46,47]. Twelve CPGs were published in the USA, of which four CPGs were developed by the American Society of Clinical Oncology (ASCO) and four from National Comprehensive Cancer Network (NCCN). The remaining were published in the UK (n = 1), in Europe (n = 1), in Canada (n = 1), and in Germany (n = 1). The basic characteristics of the sixteen CPGs are shown in Table 1.
AGREE II
Scope and purpose
This domain assesses whether the guideline clearly described the main objectives, clinical questions, and target population. The guideline by Mohile et al. [44] scored the highest and fulfilled 100% of the criteria whereas the guideline [35] from Germany achieved only 41.67% (Fig. 2).
Stakeholder involvement
This domain evaluates whether the guideline was developed by appropriate stakeholders and represents the views of its intended users. Furthermore, it covers whether the guideline clearly defined its target users. Two ASCO guidelines [43, 44] achieved the highest score fulfilling 100% of the criteria, while the guideline [35] from Germany showed no consideration of the views of the other stakeholders such as patients, the public, payers, and policy-makers and therefore received a low score of 13.89%.
Rigor of development
This domain assesses the systematic methods used for gathering and synthesizing evidence, formulating recommendations, the expert external peer review process, and the procedure for updating the guideline. The mean score was 6.21 (± 1.49), with individual scores ranging from 34.38% to 98.96% (Supplementary Table S2). Most guidelines provided search strategies and clearly described the selection criteria except for the guideline from Germany [35]. Three guidelines [34, 35, 37] did not describe clear procedures for updates.
Clarity of presentation
This domain is related to whether the guidelines provided clear recommendations and whether important recommendations were easily identifiable. This domain achieved the highest mean score (6.52 ± 0.78), and the individual scores ranged from 75% [35] to 100% [44]. This suggested all the included guidelines performed well in the presentation and clarity of the recommendations.
Applicability
This domain considers facilitators and barriers to guideline implementation, including potential cost implications, and presents key monitoring criteria for adherence to the guideline. Across the guidelines, AGREE II scores were lowest in this domain, with a mean score of 5.26 (± 1.66). The guideline by Shapiro et al. [43] achieved the best score of 98.58%, while the guideline from Germany [35] and the ASCO guideline [42] paid limited attention to the applicability, scoring only 33.33% and 50%, respectively.
Editorial independence
This domain focuses on whether guidelines are developed independently or have any existing conflicts of interest. The mean score was 6.37 (± 1.03). All of the guidelines fulfilled the criteria and scored above 75% except for the guideline from the UK.
AGREE-REX
Clinical applicability
This domain evaluates whether the guideline is evidence-based and the extent to which the recommendations apply to the guideline’s target users in terms of the practice context and patient population. Among all the included guidelines, the AGREE-REX domain clinical applicability scored the highest with a mean score of 6.10 (± 0.82) (Supplementary Table S3), individual scores ranging from 68.89% [40] to 93.33% [33] (Fig. 3).
Values and preferences
This domain assesses whether the values and preferences of target users, patients, policy decision-makers, and guideline developers had been explored and considered in the development of the recommendations. This domain scored the lowest with individual scores ranging from 45.83% [34] to 74.14% [33] and seven guidelines scoring below 60%. Of the four items, the values and preferences of policy decision-makers and guideline developers had been omitted completely in several guidelines.
Implementability
This domain assesses the “purpose” and “local application and adoption” of the items. The mean score was 5.28 (± 1.11), with individual scores ranging from 55.00% to 88.33%. The NCCN guideline by Sanft et al. [38] scored the highest, at 88.33%. The NICE guideline [33] and the NCCN guideline by Swarm et al. [45] achieved 83.34%. Most guidelines paid limited attention to local application and adoption.
Among all, eight guidelines met the cut-off scores, achieving above 60% of all domains, and the NICE guideline earned the best scores in the three AGREE-REX domains, ranging from74.17% to 93.33%.
Summary of recommendations and levels of evidence
Fifteen of the sixteen guidelines met the cut-off scores of AGREE II, six of which provided PA intervention recommendations within a disease-specific context, and the remaining guidelines provided management recommendations for symptoms or functional impairments. Notably, two of the fourteen guidelines were published by specialized rehabilitation organizations, and one guideline endorsed by the Canadian Physiotherapy Association provided information specifically for physical therapists on the management of patients with multiple myeloma. PA recommendations, the level of evidence, and the strength of recommendation are outlined in Table 2. Method to collect the evidence, formulate recommendations, and articles type/number are outlined in Table 3.
Discussion
This study presents the first systematic review using AGREE II and AGREE-REX to appraise the quality of CPGs with physical activity recommendations for cancer patients. Sixteen guidelines were evaluated and eight guidelines published by ASCO, NCCN, NICE, and ESPN obtained high quality. This is likely due to the strict framework provided by these organizations, and the guideline makers had strictly adhered to the CPGs development process. For example, there is a representative from the ASCO Practice Guidelines Implementation Network (PGIN) and at least one patient representative in each expert panel of ASCO guidelines. Additionally, ASCO produces clinical tools and resources to assist with disseminating the recommendations contained in the guidelines. Based on the available clinical treatment resources, NCCN provides NCCN Framework, NCCN Harmonized Guidelines, and International Adaptations/Translations to extend the utility of the NCCN Guidelines. NICE incorporates economic evaluation in the development of guideline recommendations.
How might our findings impact CPGs development and future research?
Recommendations for guideline development
The potential benefits of clinical practice guidelines depend on the quality of the CPGs [28]. Ideally, guideline makers should strictly follow rigorous processes when developing CPGs. This review identified 16 relevant CPGs that showed acceptable quality in most AGREE II and AGREE-REX domains. Remarkably, some weaknesses have been revealed in AGREE II domain “applicability” and AGREE-REX domains of “values and preferences” and “implementability,” especially the items “values and preferences of policy/decision-makers” as well as “local application and adoption.” The lowest mean score (5.26 ± 1.66) was observed for the AGREE II domain “applicability,” and the evaluators gave low ratings (< 60%) to 4 out of 16 guidelines. Applicability refers to whether facilitators, barriers, and additional resources of the guideline application were presented and if monitoring or auditing criteria of the recommendations was provided. These parameters especially monitoring or auditing criteria were not clearly provided in most guidelines, which may explain the low values of this domain. However, ESPEN guideline did well in this domain, sufficiently providing all parameters [39]. The AGREE-REX domain “values and preferences” assesses whether the values and preferences of target users, patients, guideline developers, and policy decision-makers had been considered and how it influenced the recommendation formulation. Sackett [48] indicated that evidence‐based medicine should be equally based on service users’ values and expectations, individual clinical expertise, and the best available clinical evidence. Previous studies [49, 50] suggested that CPGs were more implementable when they considered patients’ and stakeholders’ values and preferences and provided information to support patient involvement in decision-making. However, most CPGs [32, 34, 37, 44] included in this study achieved low scores (< 50%) because there were missing information on the values and preferences of users, patients, guideline developers, and policy/decision-makers’ influenced on the recommendation formulation, which may ultimately influence the acceptability and adoption into clinical practice of PA recommendations. The findings are consistent with the previous studies [51,52,53]; many factors such as physical activity preferences (type, place, time), convenience (e.g., there is no travel to and from a hospital), cost, knowledge of physical activity guidelines, and accessibility to the program had led to a low level of PA adherence among cancer patients. For the AGREE-REX domain “implementability,” low values were consistently rated on item 9 “local application and adoption” in most included guidelines. This item assesses the suitability of the guideline recommendations for the setting, patient population, and/or the healthcare system in which they are being implemented. Professor Robbie Foy suggested that successful implementation of a guideline depends on both the national and local resources/action [54]. Most of the included guidelines did not consider resources at the local setting or adjust recommendations to tailor local adaptations when developing CPGs. This may further influence applicability to implement across the different local practice settings. Importantly, this consequence can be found in a systematic review involving ninety-eight studies and reported that barriers to cancer patients’ PA engagement included competencies of healthcare professional guidance, social support, and inaccessibility to fitness facilities [53]. However, NCCN guidelines are the notable exception. They provided NCCN Framework for Resource Stratification, NCCN Harmonized Guidelines targeting the regional resources, and International Adaptations/Translations to extend the utility of the NCCN Guideline internationally.
In conclusion, this analysis shows there is substantial room for improvement in the following domains “applicability,” “values and preferences,” and “implementability” to facilitate the guideline implementation. It is essential to comprehensively consider the values and preferences of users, patients, policymakers, and guideline makers and provide advice or tools and resources to facilitate the implementation of the recommendations. In addition, providing a “Guideline Implementation Survey” and a clear “monitoring and auditing criteria” may facilitate application of guidelines. Furthermore, the transparency of the guideline development process should also be addressed.
Suggestions on study design
This study identified eight high-quality CPGs; notwithstanding, many studies that formed the exercise evidence base contained flaws in the study design. We reviewed the quality of studies included in 16 guidelines and summarized the main problems in their design as follows: ① small sample sizes, ② low adherence and high attrition rates, ③ short intervention durations, ④ observational studies or feasibility studies, and ⑤ serious inconsistency owing to various interventions and outcomes. For example, the trials in the ASCO guideline [42] “Management of chronic pain in survivors of adult cancers” presented with some limitations, such as pain as the secondary outcome, a small sample size, and different measurement tools. Some studies included in the CPA guideline [37] were retrospective design, and we also found that most of the latest research for patients with multiple myeloma are feasibility studies [55]. Future research must be conducted using large sample sizes, randomized design, and rigorous method to decrease the risk of bias. Community or home-based exercise mode combined with a web-based guidance is also needed so as to enhance exercise compliance in patients.
Opportunities for future research
Findings of a bibliometric analysis suggested that the overall trend of cancer rehabilitation publications is optimistic [56]. However, this literature study revealed the presenting research deficits in some areas of physical activity interventions: ① Researches were mostly performed on the breast cancer, prostate cancer, colorectal cancer, and lung cancer populations. Of the 16 included guidelines, up to 25% CPGs were tailored to breast cancer survivors; ② previous studies on cancer rehabilitation emphasized on the cognitive, behavioral, and psychological therapies, whereas research on the health effects of PA in cancer rehabilitation is lacking; ③ there is still minimal research exploring the safety, feasibility, and potential benefits of exercise in patients with advanced cancer and cachexia [57].
Therefore, future study efforts should be devoted to ①the effectiveness of PA interventions on a wider range of cancer population other than breast, lung, prostate, and colorectal cancer; ② the immediate and long-term benefits of different modalities of PA on the physical and mental fitness of cancer survivors; and ③ the optimal PA prescription (frequency, intensity, duration, or type) for different symptoms or functioning impairments management. The previous studies [58] suggest that the optimal effects of PA are dependent on the dose appropriate to the individual level of physical fitness and health status. The PA prescription should follow FITT principles: frequency, intensity, time, and type [59]. Some guidelines included in this review are lacking specific PA prescriptions; therefore, for further in-depth exploration of the benefits of PA for cancer patients, future research should continue to explore specific FITT principles tailored towards cancer patients; ④ future research must focus on the effect of exercise on clinical symptoms in patients with advanced cancer and cachexia, especially for sarcopenia and pain.
Recent studies [60, 61] have demonstrated that telehealth-based exercise prescription is both feasible and effective for cancer survivors during the COVID-19 pandemic. Multiple novel web-based exercise systems are emerging as an excellent option to provide individualized PA interventions for cancer survivors, such as breast cancer and prostate cancer [62, 63]. In addition, other factors such as cost-effectiveness, less expenditure on travel time, patients’ preference to home-based exercise, and less absence from work may be considered in favor of the patient [64]. Therefore, efforts should be performed to continue evaluating the value of web-based rehabilitation mode across the continuum of cancer care and survivorship.
Additionally, we also noted that some available evidence included in the CPGs suggested a potential benefit from exercise for some physical impairments or symptoms, yet latest evidence remain insufficient for a clear direction on recommendations. For example, exercise for chemotherapy-induced peripheral neuropathy in adult cancers with insufficient evidence to formulate a recommendation [65, 66]; Tai-Chi for depression with shallow evidence to support a recommendation [67, 68]; and yoga for chemotherapy-induced nausea and vomiting with insufficient data to support specific recommendations [69]. Therefore, future well-designed clinical trials are needed to confirm the effectiveness and safety of the PA interventions for treatment-related issues, especially chemotherapy-induced peripheral neuropathy, nausea, and cachexia.
What challenges are faced when integrating physical activity into oncology care?
There are numerous challenges in applying PA into routine oncology care practice. One solution to overcome the challenges is implementing practice guidelines. The potential benefits of guidelines depend on the quality [28]. In this review, we found some common issues in the content of selected guidelines not relating to methodological flaws. First, much of the guidelines covered information on medical management, while less information was relevant to non-pharmaceutical management. Professional guidance should be provided by experts in different disciplines; however, most expert panels which developed the selected guidelines [32, 33, 35, 39] did not consist of a rehabilitation specialist or exercise physiologist required during the development of PA recommendations. These existing problems may affect the process of integrating physical activity into routine oncology care practice. Hence, there is a compelling need to promote more collaboration between oncologists and rehabilitation specialists, establish multidisciplinary expert panels, improve the referral system, and eventually gain the recognition and promotion of PA intervention in oncology clinical setting. Besides, we also observed that most included CPGs did not provide relevant factors and resources to promote its successful dissemination, which may lower knowledge about PA guidelines in daily life. Previous studies demonstrated that most cancer patients did not know the PA guidelines, and providing more detailed knowledge regarding PA guidelines in the oncological setting was an important facilitators to motivate their PA participation [51, 70, 71]. This phenomenon was also reported among healthcare professionals[72]. It’s important to improve knowledge of PA guidelines in for narrowing the knowledge-to-practice gap. According to the AGREE-REX tool and relevant guidelines implementation projects [73, 74], we suggest that the PA guidelines promoting-strategies include the following: (1) Present information from the PA guidelines in an easy-to-understand format, such as developing PA guidelines for patients; (2) The PA guidelines for cancer patients should be sent to hospital decision-makers, managers, practitioners, and explained to them by the researchers; (3) provide routine training sessions and manual for healthcare professionals, education, and handbook for patients and their caregivers of PA guidelines; and (4) disseminate PA guidelines by holding public outreach events (public forums, reports, conferences, etc.).
Strengths and limitations
As with all systematic reviews, our review has several strengths. It is the first review of guidelines with PA recommendations for cancer patients using AGREE II and AGREE-REX instruments. We evaluated the quality and applicability of included CPGs, synthesized PA recommendations, which could guide future research. In this review, the study selection and data extraction were performed by two independent reviewers, and all included guidelines were assessed by five independent evaluators. Before this article, reviewers were trained to ensure the validity and reliability of the guideline evaluation. Our review team also consists of an expert who has experience in guidelines development.
There are some limitations in our review. First, albeit a comprehensive literature search strategy and covering grey literature, some CPGs may still be missed. Second, given that CPGs only published in English were included, there may be selection bias in our study. Finally, the methodological quality appraisal of guidelines may be somewhat subjective; AGREE II and AGREE-REX did not set defined thresholds to differentiate between high quality and low quality guidelines, we adopted cut-off scores based on previous studies in our review [27]. Other evaluators may interpret AGREE domains scores differently, so the results of AGREE II and AGREE-REX appraisal should be interpreted with discretion. The AGREE II and AGREE-REX only focus on the methodological quality and applicability of guidelines.
Conclusions
This review revealed several deficiencies in domains including “applicability,” “values and preferences” and “implementability,” so this study can serve as a baseline from which to benchmark future development and improvement of cancer rehabilitation guidelines. Furthermore, this analysis indicated that more rigorous, high-quality studies are needed to generate trial-based evidence for supporting PA recommendations and provide guidance on research gaps in the field of cancer rehabilitation.
References
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F (2021) Global cancer statistics 2020: Globocan estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71:209–249. https://doi.org/10.3322/caac.21660
Nekhlyudov L, Campbell GB, Schmitz KH, Brooks GA, Kumar AJ, Ganz PA, Von Ah D (2021) Cancer-related impairments and functional limitations among long-term cancer survivors: gaps and opportunities for clinical practice. Cancer 128(2):222–229. https://doi.org/10.1002/cncr.33913
Siegel RL, Miller KD, Fuchs HE, Jemal A (2022) Cancer statistics, 2022. CA Cancer J Clin 72:7–33. https://doi.org/10.3322/caac.21708
Maria Hewitt SG, Stovall E (2006) From cancer patient to cancer survivor: Advocacy, action, access and accountability: using public policy to advance the delivery of quality cancer care. Psychooncology 15:S9–S9
Herrmann J (2020) Adverse cardiac effects of cancer therapies: cardiotoxicity and arrhythmia. Nat Rev Cardiol 17:474–502. https://doi.org/10.1038/s41569-020-0348-1
Peixoto da Silva S, Santos JMO, Costa ESMP, Gil da Costa RM, Medeiros R (2020) Cancer cachexia and its pathophysiology: links with sarcopenia, anorexia and asthenia. J Cachexia Sarcopenia Muscle 11:619–635. https://doi.org/10.1002/jcsm.12528
Gerber LH (2017) Cancer-related fatigue: persistent, pervasive, and problematic. Phys Med Rehabil Clin N Am 28:65–88. https://doi.org/10.1016/j.pmr.2016.08.004
Gillespie TC, Sayegh HE, Brunelle CL, Daniell KM, Taghian AG (2018) Breast cancer-related lymphedema: risk factors, precautionary measures, and treatments. Gland Surg 7:379–403. https://doi.org/10.21037/gs.2017.11.04
Winters-Stone KM, Horak F, Jacobs PG, Trubowitz P, Dieckmann NF, Stoyles S, Faithfull S (2017) Falls, functioning, and disability among women with persistent symptoms of chemotherapy-induced peripheral neuropathy. J Clin Oncol 35:2604–2612. https://doi.org/10.1200/jco.2016.71.3552
Neo J, Fettes L, Gao W, Higginson IJ, Maddocks M (2017) Disability in activities of daily living among adults with cancer: a systematic review and meta-analysis. Cancer Treat Rev 61:94–106. https://doi.org/10.1016/j.ctrv.2017.10.006
Kline RM, Arora NK, Bradley CJ, Brauer ER, Graves DL, Lunsford NB, McCabe MS, Nasso SF, Nekhlyudov L, Rowland JH, Schear RM, Ganz PA (2018) Long-term survivorship care after cancer treatment - summary of a 2017 national cancer policy forum workshop. J Natl Cancer Inst 110:1300–1310. https://doi.org/10.1093/jnci/djy176
Caspersen CJ, Powell KE, Christenson GM (1985) Physical activity, exercise, and physical fitness: definitions and distinctions for health-related research. Public Health Rep 100:126–131
Friedenreich CM, Stone CR, Cheung WY, Hayes SC (2020) Physical activity and mortality in cancer survivors: a systematic review and meta-analysis. JNCI Cancer Spectr 4:pkz080. https://doi.org/10.1093/jncics/pkz080
Baguley BJ, Bolam KA, Wright ORL, Skinner TL (2017) The effect of nutrition therapy and exercise on cancer-related fatigue and quality of life in men with prostate cancer: a systematic review. Nutrients 9(9):1003.https://doi.org/10.3390/nu9091003
Oliveira MMF, Gurgel MSC, Amorim BJ, Ramos CD, Derchain S, Furlan-Santos N, Dos Santos CC, Sarian LO (2018) Long term effects of manual lymphatic drainage and active exercises on physical morbidities, lymphoscintigraphy parameters and lymphedema formation in patients operated due to breast cancer: a clinical trial. PLoS ONE 13:e0189176. https://doi.org/10.1371/journal.pone.0189176
Irwin ML, Cartmel B, Gross CP, Ercolano E, Li F, Yao X, Fiellin M, Capozza S, Rothbard M, Zhou Y, Harrigan M, Sanft T, Schmitz K, Neogi T, Hershman D, Ligibel J (2015) Randomized exercise trial of aromatase inhibitor-induced arthralgia in breast cancer survivors. J Clin Oncol 33:1104–1111. https://doi.org/10.1200/jco.2014.57.1547
Song M, Chan AT (2018) The potential role of exercise and nutrition in harnessing the immune system to improve colorectal cancer survival. Gastroenterology 155:596–600. https://doi.org/10.1053/j.gastro.2018.07.038
Gustafson MP, Wheatley-Guy CM, Rosenthal AC, Gastineau DA, Katsanis E, Johnson BD, Simpson RJ (2021) Exercise and the immune system: taking steps to improve responses to cancer immunotherapy. J Immunother Cancer 9(7):e001872.https://doi.org/10.1136/jitc-2020-001872
Dempsey PC, Friedenreich CM, Leitzmann MF, Buman MP, Lambert E, Willumsen J, Bull F (2020) Global public health guidelines on physical activity and sedentary behavior for people living with chronic conditions: a call to action. J Phys Act Health 18:76–85. https://doi.org/10.1123/jpah.2020-0525
Graham R, Mancher M, Miller Wolman D, Greenfield S, Steinberg E. (Eds.). (2011) Institute of medicine committee on standards for developing trustworthy clinical practice, guidelines. In Clinical practice guidelines we can trust. Washington (DC): National Academies Press (US). Available from: https://www.ncbi.nlm.nih.gov/books/NBK209546/
Brouwers MC, Florez ID, McNair SA, Vella ET, Yao X (2019) Clinical practice guidelines: tools to support high quality patient care. Semin Nucl Med 49:145–152. https://doi.org/10.1053/j.semnuclmed.2018.11.001
Dans AL, Dans LF (2010) Appraising a tool for guideline appraisal (the agree ii instrument). J Clin Epidemiol 63:1281–1282. https://doi.org/10.1016/j.jclinepi.2010.06.005
Shallwani SM, King J, Thomas R, Thevenot O, De Angelis G, Aburub AS, Brosseau L (2019) Methodological quality of clinical practice guidelines with physical activity recommendations for people diagnosed with cancer: a systematic critical appraisal using the agree ii tool. PLoS ONE 14:e0214846. https://doi.org/10.1371/journal.pone.0214846
Stout NL, Santa Mina D, Lyons KD, Robb K, Silver JK (2021) A systematic review of rehabilitation and exercise recommendations in oncology guidelines. CA Cancer J Clin 71:149–175. https://doi.org/10.3322/caac.21639
Nuckols TK, Lim YW, Wynn BO, Mattke S, MacLean CH, Harber P, Brook RH, Wallace P, Garland RH, Asch S (2008) Rigorous development does not ensure that guidelines are acceptable to a panel of knowledgeable providers. J Gen Intern Med 23:37–44. https://doi.org/10.1007/s11606-007-0440-9
Brouwers MC, Spithoff K, Kerkvliet K, Alonso-Coello P, Burgers J, Cluzeau F, Férvers B, Graham I, Grimshaw J, Hanna S, Kastner M, Kho M, Qaseem A, Straus S, Florez ID (2020) Development and validation of a tool to assess the quality of clinical practice guideline recommendations. JAMA Netw Open 3:e205535. https://doi.org/10.1001/jamanetworkopen.2020.5535
Steeb T, Hayani KM, Förster P, Liegl R, Toussaint F, Schlaak M, Berking C, Heppt MV (2020) Guidelines for uveal melanoma: a critical appraisal of systematically identified guidelines using the agree ii and agree-rex instrument. J Cancer Res Clin Oncol 146:1079–1088. https://doi.org/10.1007/s00432-020-03141-w
Brouwers MC, Kho ME, Browman GP, Burgers JS, Cluzeau F, Feder G, Fervers B, Graham ID, Grimshaw J, Hanna SE, Littlejohns P, Makarski J, Zitzelsberger L (2010) Agree ii: advancing guideline development, reporting and evaluation in health care. CMAJ 182:E839-842. https://doi.org/10.1503/cmaj.090449
Hoffmann-Eßer W, Siering U, Neugebauer EAM, Lampert U, Eikermann M (2018) Systematic review of current guideline appraisals performed with the appraisal of guidelines for research & evaluation ii instrument-a third of agree ii users apply a cut-off for guideline quality. J Clin Epidemiol 95:120–127. https://doi.org/10.1016/j.jclinepi.2017.12.009
Hallgren KA (2012) Computing inter-rater reliability for observational data: an overview and tutorial. Tutor Quant Methods Psychol 8:23–34. https://doi.org/10.20982/tqmp.08.1.p023
Cicchetti DV (1994) Guidelines, criteria, and rules of thumb for evaluating normed and standardized assessment instruments in psychology. Psychol Assess 6:284–290
Greenlee H, DuPont-Reyes MJ, Balneaves LG, Carlson LE, Cohen MR, Deng G, Johnson JA, Mumber M, Seely D, Zick SM, Boyce LM, Tripathy D (2017) Clinical practice guidelines on the evidence-based use of integrative therapies during and after breast cancer treatment. CA Cancer J Clin 67:194–232. https://doi.org/10.3322/caac.21397
National Institute for Health and Care Excellence (2018) Early and locally advanced breast cancer: Diagnosis and management (NG101). ISBN-13: 978-1-4731-3008-1. Available from: https://www.ncbi.nlm.nih.gov/books/NBK519155/
Davies C, Levenhagen K, Ryans K, Perdomo M, Gilchrist L (2020) Interventions for breast cancer–related lymphedema: clinical practice guideline from the academy of oncologic physical therapy of APTA. Phys Ther 100:1163–1179. https://doi.org/10.1093/ptj/pzaa087
Ditsch N, Untch M, Kolberg-Liedtke C, Jackisch C, Krug D, Friedrich M, Janni W, Müller V, Albert U-S, Banys-Paluchowski M, Bauerfeind I, Blohmer J-U, Budach W, Dall P, Diel I, Fallenberg Eva M, Fasching Peter A, Fehm T, Gerber B, Gluz O (2020) Ago recommendations for the diagnosis and treatment of patients with locally advanced and metastatic breast cancer: update 2020. Breast Care 15:294–309. https://doi.org/10.1159/000508736
Cohen EE, la Monte SJ, Erb NL, Beckman KL, Sadeghi N, Hutcheson KA, Stubblefield MD, Abbott DM, Fisher PS, Stein KD, Lyman GH, Pratt-Chapman MLACS (2016) American cancer society head and neck cancer survivorship care guideline. CA A Cancer J Clin 66(3):203–239
Jeevanantham D, Rajendran V, McGillis Z, Tremblay L, Larivière C, Knight A (2021) Mobilization and exercise intervention for patients with multiple myeloma: clinical practice guidelines endorsed by the Canadian physiotherapy association. Phys Ther 101(1):pzaa180.https://doi.org/10.1093/ptj/pzaa180
Natioinal Comprehensive Cancer Network (NCCN). NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines®) Survivorship. Version 1.2022. Accessed at. https://www.nccn.org/professionals/physician_gls/pdf/survivorship.pdf
Arends J, Bachmann P, Baracos V, Barthelemy N, Bertz H, Bozzetti F, Fearon K, Hütterer E, Isenring E, Kaasa S, Krznaric Z, Laird B, Larsson M, Laviano A, Mühlebach S, Muscaritoli M, Oldervoll L, Ravasco P, Solheim T, Strasser F, de van der Schueren M, Preiser JC (2017) Espen guidelines on nutrition in cancer patients. Clin Nutr 36:11-48. https://doi.org/10.1016/j.clnu.2016.07.015
Rock CL, Thomson CA, Sullivan KR, Howe CL, Kushi LH, Caan BJ, Neuhouser ML, Bandera EV, Wang Y, Robien K, Basen-Engquist KM, Brown JC, Courneya KS, Crane TE, Garcia DO, Grant BL, Hamilton KK, Hartman SJ, Kenfield SA, Martinez ME, Meyerhardt JA, Nekhlyudov L, Overholser L, Patel AV, Pinto BM, Platek ME, Rees-Punia E, Spees CK, Gapstur SM, McCullough ML (2022) American cancer society nutrition and physical activity guideline for cancer survivors. CA Cancer J Clin 72:230–262. https://doi.org/10.3322/caac.21719
Ligibel JA, Bohlke K, May AM, Clinton SK, Demark-Wahnefried W, Gilchrist SC, Irwin ML, Late M, Mansfield S, Marshall TF, Meyerhardt JA, Thomson CA, Wood WA, Alfano CM (2022) Exercise, diet, and weight management during cancer treatment: Asco guideline. J Clin Oncol 40:2491–2507. https://doi.org/10.1200/jco.22.00687
Paice JA, Portenoy R, Lacchetti C, Campbell T, Cheville A, Citron M, Constine LS, Cooper A, Glare P, Keefe F, Koyyalagunta L, Levy M, Miaskowski C, Otis-Green S, Sloan P, Bruera E (2016) Management of chronic pain in survivors of adult cancers: American society of clinical oncology clinical practice guideline. J Clin Oncol 34(27):3325–3345
Shapiro CL, Van Poznak C, Lacchetti C, Kirshner J, Eastell R, Gagel R, Smith S, Edwards BJ, Frank E, Lyman GH, Smith MR, Mhaskar R, Henderson T, Neuner J (2019) Management of osteoporosis in survivors of adult cancers with nonmetastatic disease: Asco clinical practice guideline. J Clin Oncol 37:2916–2946. https://doi.org/10.1200/jco.19.01696
Mohile SG, Dale W, Somerfield MR, Schonberg MA, Boyd CM, Burhenn PS, Canin B, Cohen HJ, Holmes HM, Hopkins JO, Janelsins MC, Khorana AA, Klepin HD, Lichtman SM, Mustian KM, Tew WP, Hurria A (2018) Practical assessment and management of vulnerabilities in older patients receiving chemotherapy: Asco guideline for geriatric oncology. J Clin Oncol 36:2326–2347. https://doi.org/10.1200/jco.2018.78.8687
Natioinal Comprehensive Cancer Network (NCCN). NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines®) Adult cancer pain. Version 2.2022. Accessed at https://www.nccn.org/professionals/physician_gls/pdf/pain.pdf
Natioinal Comprehensive Cancer Network (NCCN). NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines®) Antiemesis. Version 2.2022. Accessed at https://www.nccn.org/professionals/physician_gls/pdf/antiemesis.pdf
Natioinal Comprehensive Cancer Network (NCCN). NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines®) Cancer-related fatigue. Version 2.2022. Accessed at https://www.nccn.org/professionals/physician_gls/pdf/fatigue.pdf
Sackett DL, Rosenberg WM, Gray JA, Haynes RB, Richardson WS (1996) Evidence based medicine: what it is and what it isn’t. BMJ 312:71–72. https://doi.org/10.1136/bmj.312.7023.71
van der Ham AJ, van Erp N, Broerse JE (2016) Monitoring and evaluation of patient involvement in clinical practice guideline development: lessons from the multidisciplinary guideline for employment and severe mental illness, the netherlands. Health Expect 19:471–482. https://doi.org/10.1111/hex.12370
Florez ID, Brouwers MC, Kerkvliet K, Spithoff K, Alonso-Coello P, Burgers J, Cluzeau F, Férvers B, Graham I, Grimshaw J, Hanna S, Kastner M, Kho M, Qaseem A, Straus S (2020) Assessment of the quality of recommendations from 161 clinical practice guidelines using the appraisal of guidelines for research and evaluation-recommendations excellence (agree-rex) instrument shows there is room for improvement. Implement Sci 15:79. https://doi.org/10.1186/s13012-020-01036-5
Hardcastle SJ, Maxwell-Smith C, Kamarova S, Lamb S, Millar L, Cohen PA (2018) Factors influencing non-participation in an exercise program and attitudes towards physical activity amongst cancer survivors. Support Care Cancer 26:1289–1295. https://doi.org/10.1007/s00520-017-3952-9
Smith L, Croker H, Fisher A, Williams K, Wardle J, Beeken RJ (2017) Cancer survivors' attitudes towards and knowledge of physical activity, sources of information, and barriers and facilitators of engagement: a qualitative study. Eur J Cancer Care (Engl) 26(4):e12641.https://doi.org/10.1111/ecc.12641
Elshahat S, Treanor C, Donnelly M (2021) Factors influencing physical activity participation among people living with or beyond cancer: a systematic scoping review. Int J Behav Nutr Phys Act 18:50. https://doi.org/10.1186/s12966-021-01116-9
Nice implementation strategy group. Accessed at https://www.nice.org.uk/about/what-we-do/into-practice/resources-help-put-guidance-into-practice
McCourt O, Fisher A, Ramdharry G, Roberts AL, Land J, Rabin N, Yong K (2020) Percept myeloma: a protocol for a pilot randomised controlled trial of exercise prehabilitation before and during autologous stem cell transplantation in patients with multiple myeloma. BMJ Open 10:e033176. https://doi.org/10.1136/bmjopen-2019-033176
Stout NL, Alfano CM, Belter CW, Nitkin R, Cernich A, Lohmann Siegel K, Chan L (2018) A bibliometric analysis of the landscape of cancer rehabilitation research (1992–2016). J Natl Cancer Inst 110:815–824. https://doi.org/10.1093/jnci/djy108
Roeland EJ, Bohlke K, Baracos VE, Bruera E, Del Fabbro E, Dixon S, Fallon M, Herrstedt J, Lau H, Platek M, Rugo HS, Schnipper HH, Smith TJ, Tan W, Loprinzi CL (2020) Management of cancer cachexia: Asco guideline. J Clin Oncol 38:2438–2453. https://doi.org/10.1200/jco.20.00611
Zubin Maslov P, Schulman A, Lavie CJ, Narula J (2018) Personalized exercise dose prescription. Eur Heart J 39:2346–2355. https://doi.org/10.1093/eurheartj/ehx686
Thompson PD, Arena R, Riebe D, Pescatello LS (2013) ACSM’s new preparticipation health screening recommendations from ACSM’s guidelines for exercise testing and prescription, ninth edition. Curr Sports Med Rep 12:215–217. https://doi.org/10.1249/JSR.0b013e31829a68cf
Wu F, Rotimi O, Laza-Cagigas R, Rampal T (2021) The feasibility and effects of a telehealth-delivered home-based prehabilitation program for cancer patients during the pandemic. Curr Oncol 28:2248–2259. https://doi.org/10.3390/curroncol28030207
Avancini A, Trestini I, Tregnago D, Wiskemann J, Lanza M, Milella M, Pilotto S (2020) Physical activity for oncological patients in covid-19 era: no time to relax. JNCI Cancer Spectrum 4(6):pkaa071.https://doi.org/10.1093/JNCICS/PKAA071
Evans HE, Forbes CC, Galvão DA, Vandelanotte C, Newton RU, Wittert G, Chambers S, Vincent AD, Kichenadasse G, Girard D, Brook N, Short CE (2021) Usability, acceptability, and safety analysis of a computer-tailored web-based exercise intervention (exercise guide) for individuals with metastatic prostate cancer: multi-methods laboratory-based study. JMIR Cancer 7:e28370. https://doi.org/10.2196/28370
Ariza-Garcia A, Lozano-Lozano M, Galiano-Castillo N, Postigo-Martin P, Arroyo-Morales M, Cantarero-Villanueva I (2019) A web-based exercise system (e-cuidatechemo) to counter the side effects of chemotherapy in patients with breast cancer: randomized controlled trial. J Med Internet Res 21:e14418. https://doi.org/10.2196/14418
May AM, Bosch MJ, Velthuis MJ, van der Wall E, Steins Bisschop CN, Los M, Erdkamp F, Bloemendal HJ, de Roos MA, Verhaar M, Ten Bokkel HD, Peeters PH, de Wit GA (2017) Cost-effectiveness analysis of an 18-week exercise programme for patients with breast and colon cancer undergoing adjuvant chemotherapy: the randomised pact study. BMJ Open 7:e012187. https://doi.org/10.1136/bmjopen-2016-012187
Kanzawa-Lee GA, Larson JL, Resnicow K, Smith EML (2020) Exercise effects on chemotherapy-induced peripheral neuropathy: a comprehensive integrative review. Cancer Nurs 43:E172-e185. https://doi.org/10.1097/ncc.0000000000000801
Guo S, Han W, Wang P, Wang X, Fang X (2022) Effects of exercise on chemotherapy-induced peripheral neuropathy in cancer patients: a systematic review and meta-analysis. J Cancer Surviv.https://doi.org/10.1007/s11764-022-01182-3
Zeng Y, Xie X, Cheng ASK (2019) Qigong or tai chi in cancer care: an updated systematic review and meta-analysis. Curr Oncol Rep 21:48. https://doi.org/10.1007/s11912-019-0786-2
Cai Q, Cai SB, Chen JK, Bai XH, Jing CX, Zhang X, Li JQ (2022) Tai chi for anxiety and depression symptoms in cancer, stroke, heart failure, and chronic obstructive pulmonary disease: a systematic review and meta-analysis. Complement Ther Clin Pract 46:101510. https://doi.org/10.1016/j.ctcp.2021.101510
Kothari TO, Jakhar SL, Bothra D, Sharma N, Kumar HS, Baradia MR (2019) Prospective randomized trial of standard antiemetic therapy with yoga versus standard antiemetic therapy alone for highly emetogenic chemotherapy-induced nausea and vomiting in South Asian population. J Cancer Res Ther 15:1120–1123. https://doi.org/10.4103/jcrt.JCRT_860_16
Avancini A, Tregnago D, Rigatti L, Sartori G, Yang L, Trestini I, Bonaiuto C, Milella M, Pilotto S, Lanza M (2020) Factors influencing physical activity in cancer patients during oncological treatments: a qualitative study. Integr Cancer Ther 19:1534735420971365. https://doi.org/10.1177/1534735420971365
Maxwell-Smith C, Zeps N, Hagger MS, Platell C, Hardcastle SJ (2017) Barriers to physical activity participation in colorectal cancer survivors at high risk of cardiovascular disease. Psychooncology 26:808–814. https://doi.org/10.1002/pon.4234
Alderman G, Semple S, Cesnik R, Toohey K (2020) Health care professionals’ knowledge and attitudes toward physical activity in cancer patients: a systematic review. Semin Oncol Nurs 36:151070. https://doi.org/10.1016/j.soncn.2020.151070
Doré I, Plante A, Bedrossian N, Montminy S, St-Onge K, St-Cyr J, Pomey MP, Charpentier D, Pettigrew L, Brisson I, Saad F, Tournoux F, Raynault MF, Mes-Masson AM, Gauvin L (2022) Developing practice guidelines to integrate physical activity promotion as part of routine cancer care: a knowledge-to-action protocol. PLoS ONE 17:e0273145. https://doi.org/10.1371/journal.pone.0273145
Fu L, Zhang X, Hu Y, Lu Z, Yang Y, Huang M, Li Y, Zhu F, Wang Y, Huang Z (2022) Distress management in cancer patients: guideline implementation based on can-implement. Int J Nurs Sci 9:187–195. https://doi.org/10.1016/j.ijnss.2022.02.006
Acknowledgements
We acknowledge AGREE Enterprise for technical support.
Author information
Authors and Affiliations
Contributions
Conceptualization: Yi Zhu and Xue Zhou. Methodology: Xue Zhou and Yujie Yang. Formal analysis: Xue Zhou, Conghui Li, Weiqian Hou, Xigui La, and Liwen Zhai. Investigation: Xue Zhou, Yujie Yang, and Conghui Li. Writing—original draft preparation: Xue Zhou. Writing—review and editing: Yi Zhu, Yujie Yang, and Shanshan Gu. Supervision: Yi Zhu. Project administration: Yi Zhu. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Ethics approval
The study is a systematic review of published material; therefore, ethics approval was not required.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Xue Zhou and Yujie Yang are the co-first authors.
Supplementary information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhou, X., Yang, Y., Li, C. et al. What information can we gain from the quality appraisal of guidelines with physical activity recommendations for cancer patients?A systematic review using the AGREE II and AGREE-REX tools. Support Care Cancer 31, 97 (2023). https://doi.org/10.1007/s00520-022-07567-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00520-022-07567-5