https://orcid.org/0009-0009-8161-8585
Figures
Abstract
Purpose
Radiotherapy imposes a significant physiological and psychological burden on gynaecological cancer patients. Prehabilitation is being increasingly used to prepare individuals for cancer treatment and improve their well-being and resilience. Whilst prehabilitation has demonstrated benefit for individuals undergoing cancer surgery, the structure, role and implementation of prehabilitation prior to radiotherapy are poorly defined and relatively unexplored. This scoping review aims to provide a comprehensive overview of the current literature regarding prehabilitation interventions for individuals with gynaecological cancer undergoing radiotherapy.
Methods
This review was conducted following the gold-standard Joanna Briggs Institute guidelines for scoping reviews. Literature searches were completed in October 2024 across: the Allied and Complementary Medicine Database; British Nursing Index; Cumulative Index to Nursing and Allied Health Literature; Cochrane library (Controlled trials and systematic reviews); Embase; Medical Literature Analysis and Retrieval System Online; and the Psychological Information Database. Grey literature searches were conducted via Google Scholar, Overton.io, and Trip Pro Medical Database.
Results
Ninety records met the inclusion criteria, pertaining to 56 studies. Cervical cancer was the most represented gynaecological cancer type across studies. A small number of multimodal prehabilitation studies were identified (n = 4). Studies evaluating unimodal interventions were more common, with nutritional interventions (n = 24) being the most frequent, followed by psychological (n = 22) and physical exercise (n = 6) interventions. There was considerable variation across studies in respect to intervention initiation, duration, delivery and outcome measures.
Conclusions
The physiological and psychological impacts of cancer diagnosis and treatment are closely entwined. Further development of multimodal prehabilitation to cohesively address these is an important area for future research. Studies evaluating exercise interventions are relatively unexplored in this patient population and the potential barriers to engagement must be considered. Future research should focus on complete and transparent reporting of interventions, with input from those with lived experience, and adopting a standardised set of outcome measures reported across all trials.
Citation: McGladrigan E, Wrench E, Dean E, O’Neil A, Ashmore L, Gaffney C (2025) Exploring prehabilitation interventions for patients with gynaecological cancer undergoing radiotherapy: A scoping review. PLoS ONE 20(3): e0319518. https://doi.org/10.1371/journal.pone.0319518
Editor: Ka Ming Chow, Chinese University of Hong Kong, HONG KONG
Received: August 16, 2024; Accepted: February 3, 2025; Published: March 13, 2025
Copyright: © 2025 McGladrigan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: "All relevant data are within the paper and its Supporting Information files."
Funding: This work contributes towards a PhD in Medicine for EM which is funded by the Lancaster Medical School Studentship fund
Competing interests: The authors have declared that no competing interests exist.
Introduction
Radiotherapy is a mainstay in the treatment of gynaecological malignancies and may be given as a primary treatment, in combination with chemotherapy, and in a neo-adjuvant or adjuvant setting, e.g., for patients receiving surgery [1]. Highly conformal external-beam radiotherapy and brachytherapy techniques have led to reduced morbidity and mortality [2]. However, these treatments still impose a significant physiological and psychosocial burden on patients [1,3].
Radiation-induced cellular death and injury, key to its anti-neoplastic mechanisms, cause adverse effects such as urinary tract and gastrointestinal injury which may present as radiation cystitis, diarrhoea, frequency, urgency, nausea, or bloating [1,2]. Whilst the acute toxicities generally resolve within 12 weeks of completing radiotherapy, many patients experience chronic side-effects that persist months or years later [2,4]. Most radiotherapy side effects are localised to the treatment area, yet fatigue is a commonly reported symptom that may occur acutely or persist long-term [5]. Cancer-related fatigue is characterised by physical, emotional, and/or cognitive tiredness, exhaustion, or weakness related to cancer and its treatment which can significantly alter daily living [5]. Disease and treatment-related burden can also profoundly impact a person’s sexual well-being. Brachytherapy, a technique requiring the insertion of an applicator into the vagina and uterus for prolonged periods, has been highlighted as a source of trauma and distress for gynaecological cancer survivors resulting from factors such as pain, vulnerability, anxiety, and loss of autonomy [6,7]. Unsurprisingly, the acute and chronic side-effects experienced by gynaecological cancer survivors have a profound impact on quality of life, affecting important aspects such as intimacy, social activities, and employment [3,8].
The period between diagnosis and treatment provides an opportunity for early engagement with prehabilitation activities that are designed to optimise patients’ physiological and psychological well-being and resilience [9]. Whilst unimodal exercise regimens have been used by some prior to surgery, prehabilitation is ideally delivered via a multimodal regimen comprising targeted exercise, nutrition and psychological interventions and support [9,10].
Prehabilitation benefits patients undergoing cancer surgery, including reduced complication severity and length of hospital stay [11–13] and prehabilitation interventions for gynaecological cancer patients prior to surgery have been explored in a recent scoping [14] and systematic review [15]. However, the evidence base for prehabilitation is highly variable and there is a comparative dearth of research for prehabilitation prior to non-surgical cancer treatments such as radiotherapy [16]. Additionally, the term prehabilitation is not used ubiquitously in the literature and has only become more frequently used in recent years [9] making it difficult to determine the true extent of the evidence base relating to prehabilitation in this population. Unlike surgery, radiotherapy treatment may be given over a period of weeks providing additional time for patients to participate in health optimising activities. As such, the timing and duration of prehabilitation is less clearly defined for individuals scheduled to undergo radiotherapy treatment. Furthermore, chemotherapy, surgery, radiotherapy, and the various combinations of these treatments all pose unique challenges that necessitate tailored support, meaning prehabilitation developed for surgical cohorts may not be the best approach for those treated with radiotherapy [17]. Therefore, it is of interest to explore prehabilitation in the context of individuals with gynaecological malignancies receiving radiotherapy. In particular, establishing: (1) what prehabilitation interventions are being delivered, (2) their underpinning rationale, (3) the point of delivery and duration of these interventions, and (4) what outcome measures are being reported within the literature. The objective of this scoping review is to provide a comprehensive overview of the current literature regarding prehabilitation interventions for gynaecological cancer patients undergoing radiotherapy.
Methods
Scoping reviews are a form of evidence synthesis ideal for identifying and mapping the breadth of evidence available for a given topic, clarifying key concepts and highlighting gaps in the literature [18]. They are particularly useful for examining emerging evidence where it is less clear if more precise questions, such as those regarding efficacy, can be asked and suitably addressed in a systematic review [19]. Unlike systematic reviews, the exploratory nature of a scoping review allows for broader research questions and is not intended to assess effectiveness or validity of studies [19].
The methodology for this scoping review was conducted following Joanna Briggs Institute (JBI) guidelines for scoping reviews [20] and reported in accordance with the Preferred Reporting Items for Systematic reviews and Meta-Analyses extension for Scoping Reviews (PRISMA-ScR) checklist [21] (S1 Checklist). The study protocol outlining the objectives, inclusion criteria and methods was registered a priori with the Open Science Framework (https://osf.io/jgrv3). This study was a scoping review of the literature and did not require ethical approval.
Preliminary searches of the Cochrane Database of Systematic Reviews, Open Science Framework, JBI Evidence Synthesis and Google were completed in December 2023 and no current or in-progress reviews on this topic for the specified patient population were identified. A subsequent search was conducted in January 2024, following the identification of a recently published scoping review addressing prehabilitation for radiotherapy. However, this review included studies evaluating prehabilitation in any adult patient undergoing radiotherapy, not limited by tumour site, and there were no studies specifically addressing gynaecological cancer. The research questions and inclusion criteria of this proposed review are sufficiently different to those addressed by Flores et al [22] to warrant a further scoping review.
Inclusion/exclusion criteria
As advised for scoping reviews, the inclusion criteria was developed using the Population, Concept and Context (PCC) framework [20].
We included prospective or retrospective studies that reported on or evaluated (1) prehabilitation for (2) adult (≥18 years old), female patients with a gynaecological malignancy prior to or during radiotherapy, with or without chemotherapy, (3) in any setting where care is provided or an intervention can be delivered to this population. We defined prehabilitation as an intervention prior to or during radiotherapy where unimodal addressed either physical, psychological or nutritional well-being and multimodal delivery was the combination of at least two different categories, e.g., physical and psychological. Preliminary searches indicated there were only a small number of studies evaluating multimodal interventions, as such the authors agreed that inclusion of unimodal prehabilitation interventions was necessary to suitably address the research questions and explore the breadth of prehabilitation literature in this population. Despite prehabilitation sitting within the broader context of health improvement, this review did not include studies focused primarily on smoking cessation, alcohol reduction or medication management, as they as are not encompassed by the primary prehabilitation interventions – tailored physical exercise, nutritional support and psychological support.
Grey literature, conference proceedings, clinical trial protocols and records; and peer-reviewed qualitative, quantitative or mixed-methods publications, were all considered for inclusion. This breadth aligns with a scoping methodology and was considered important to fully gauge the variety of studies evaluating interventions for this population and the various aspects of applying these clinically. Social media posts, animal studies, blogs, and podcasts were excluded. Any relevant systematic or scoping reviews were excluded and hand-searched for primary studies that met the above criteria. Sources were excluded if they were not available in English language due to limited resources available for translation. The authors agreed that studies evaluating prehabilitation interventions in a broader population (e.g., a mixed population of individuals receiving radiotherapy, chemotherapy and/or surgery) would be considered for inclusion if there was sufficient separation in the results for the population of interest, in addition to ongoing clinical trials, as they could provide valuable insight into the review questions.
Search strategy
An initial search was conducted in Medical Literature Analysis and Retrieval System Online (MEDLINE) and Cumulative Index to Nursing and Allied Health Literature (CINAHL) with an adapted version of the terms used by Saggu et al [14]. The full search strategy was then developed using an analysis of text words contained within the titles and abstracts of retrieved papers and any index terms used to describe the articles. This search strategy was adapted and applied to each database including: Allied and Complementary Medicine Database (AMED) (Ovid and ProQuest Dialog); British Nursing Index (BNI) (ProQuest); CINAHL (EBSCO); Cochrane library (Controlled trials and systematic reviews); Embase (Ovid); MEDLINE (EBSCO); Psychological Information Database (PsycINFO) (EBSCO). Each search strategy was then peer reviewed by a research librarian and modified according to feedback. A search for grey literature was also conducted via Google Scholar, Overton.io, and Trip Pro Medical Database. Final searches were completed in October 2024. The full search strategies are available in the supplementary materials (S1 Table and S2 Table). Included sources and identified reviews were hand-searched for additional eligible articles.
Study selection
All identified records were uploaded to EndNote (Clarivate Analytics, PA, USA) and duplicates removed. The remaining abstracts were then uploaded to Rayyan (Qatar Computing Research Institute, Doha, Qatar) for title and abstract screening by the primary reviewer (EM) and the secondary screening was divided equally between two independent reviewers (ED and EW). The full-text screening for any potentially relevant sources were then screened in duplicate by the reviewers (EM, EW, ED or AON). Any conflicts were resolved by discussion between the relevant reviewers. A small number of sources (n = 8) were unable to be uploaded to Rayyan, the title and abstracts of each source were reviewed against the inclusion criteria and were found not to be relevant to the review.
Data charting
Relevant data were charted using a standardised form developed for this study by a reviewer (EM). This data extraction form was developed in accordance with JBI guidance [20] and piloted across different sources by two reviewers (EM and EW). Where multiple sources for the same studies were identified, the records were collated for data extraction to minimise risk of double counting [23]. A random sample (n = 8) were then verified by independent reviewers (ED or AON). Data items were extracted as published, including: title, author, year of publication, aims/purpose, population, study design, intervention type, comparator; and outcome measures, along with items from the Template for Intervention Description and Replication (TIDieR) checklist [24]. In the case of ongoing trials, all data items were extracted from available clinical trial records or published study protocols including planned intervention components and outcome measures. Authors were contacted for missing or additional information with a subsequent follow-up email after a minimum of two weeks, as necessary. Critical appraisal of the quality of included studies was not performed as this is not generally recommended for scoping reviews [19,21]. Data are presented in tabular and diagrammatic formats accompanied by a descriptive summary in a manner that aligns with the review objectives. Figures were prepared in GraphPad Prism 10 (GraphPad Software 2365 Northside Dr. Suite 560 San Diego, CA 92108) and the GNU Image Manipulation Programme (GIMP 2.10.38, gimp.org), unless otherwise stated.
Results
Study selection and descriptive characteristics of the studies
The systematic search identified 8,921 records (Fig 1). Following deduplication in EndNote, 6,835 titles and abstracts were screened against the inclusion criteria. A total of 234 records were then further assessed for eligibility, 90 were included pertaining to 56 studies.
The characteristics and details of the included studies are summarised in Tables 1–6. The 56 studies were categorised as multimodal (n = 4) [25–33], physical/exercise (n = 6) [34–42], psychological (n = 22) [43–79], and nutritional (n = 24) [80–114]. The studies were conducted in Australia (n = 4), Brazil (n = 2), Canada (n = 2), Chile (n = 1), China (n = 5), England (n = 1), France (n = 2), Finland (n = 1), Germany (n = 2), Italy (n = 1), India (n = 8), Japan (n = 1), Republic of Korea (n = 1), Mexico (n = 4), Myanmar (n = 1), Norway (n = 2), Spain (n = 5), Sweden (n = 2), Thailand (n = 2), Turkey (n = 1), and the USA (n = 8). Several ongoing clinical trials were included (n = 10) [28,36,39,43,51,72,73,91,102,108] and the earliest included record was published in 1958 [104]. Sources included peer-reviewed journal articles (n = 50), conference abstracts (n = 13), clinical trial records (n = 20), peer-reviewed study protocols (n = 4), a pre-print author manuscript (n = 1) and dissertations (n = 2). Cervical cancer was the most highly represented gynaecological cancer type across study populations, however, studies also included endometrial, uterine, vaginal, vulval, ovarian and fallopian tube malignancies (Fig 2).
What interventions are being reported in the literature?
Multimodal.
Studies evaluating multimodal prehabilitation utilised multidisciplinary teams to address the complex needs of their target population including: dieticians; physiotherapists; radiation oncologists; and prehabilitation exercise specialists (Table 3). Some of the studies also utilised early referrals or input from mental health services or social work teams within their prehabilitation interventions [25,28,32]. Kaliamurthi et al. [27] provided cervical cancer patients with a programme consisting of counselling, nutritional support and physiotherapy. Only one study did not specifically mention including a physical exercise element, this was targeted to patients undergoing brachytherapy so the intervention focused on carbohydrate loading, pain control and psychosocial support [32]. RadBone [28] is an ongoing clinical trial that utilises the resources of an established prehabilitation service to provide tailored exercise, nutritional and psychological support in combination with a targeted musculoskeletal health package.
Unimodal – Physical/Exercise.
Of the six studies reporting on a unimodal physical exercise intervention, only two implemented a physical activity programme that resemble those more commonly used in prehabilitation prior to surgery. Of these, one was a case study providing a completely tailored exercise intervention for an individual during treatment [37] and the other is an ongoing clinical trial involving a variety of patient groups undergoing radiotherapy using an activity tracker-based programme [36]. Two single-arm (pre-post) interventional studies focused on teaching pelvic floor muscle exercises (PFMEs) and encouraging participants to perform these exercises at home facilitated by educational materials and/or pre-recorded instructions [35,38]. The final category of physical interventions was targeted towards post-surgical patients prior to adjuvant treatment. These studies focus on prophylactic complex physiotherapy including manual lymphatic drainage, skin care, use of compression stockings, and functional exercises that could be performed at home [34,39].
Unimodal – Psychological.
The majority of studies addressing psychological wellbeing (n = 17) [43,51,54,56,58–65,67–69,71,72] incorporated relaxation and stress reduction techniques such as controlled breathing exercises, aromatherapy, progressive muscle relaxation, guided imagery, videos, music, meditation, mindfulness, and stress management coaching. Three of which also evaluated the effect of the complementary therapies: healing touch [54], reiki [43], and reflexology with aromatherapy [62]. In the PeNTAGOn trial, and an earlier pilot study [69], Schofield et al. [68] used both specialist nurses and matched peers to deliver a tailored psychoeducational intervention that involved elements of relaxation combined with timely delivery of information and support, to address patients’ concerns and psychosexual needs. Kpoghomou et al. [70] and Varre et al. [53] also provided nurse-led counselling to support and manage patients’ psychological and psychosexual wellbeing, whereas, Jeffries et al. [52] favoured a small group approach with taught elements and peer discussion facilitated by healthcare professionals. In their ongoing trial, Oluloro et al. [73] are evaluating the implementation of virtual support groups hosted by a trained peer-support and specialist co-facilitators to promote group conversation and discussion of structured topics including mental well-being, finances and family dynamics. The support group intervention is also being compared against enhanced care including more targeted written information and a 1:1 support intervention with a peer trained by the Endometrial Cancer American Network for African-Americans [73].
Unimodal – nutritional.
Twelve (50%) of the studies evaluating nutritional interventions were randomised, placebo-controlled trials. Several of these studies focused on the introduction of probiotics or synbiotics (prebiotics and probiotics) into the participants’ diets. The strain and combination of bacteria used, varied between studies including: Lactobacillus casei DN-114 001 with standard starters Streptococcus thermophilus and Lactobacillus delbrueckii subsp. Bulgaricus [88]; Lactobacillus acidophilus LA-5 and Bifidobacterium animalis subsp. lactis BB-12 [93]; Lactiplantibacillus plantarum HEAL9 and 299 [81]; Lactobacillus acidophilus with Bifidobacterium bifidum [82]; Lactobacillus acidophilus (NCDO 1748) [97]; and Lactobacillus acidophilus NCFM, Bifidobacterium lactis Bi-07 with blue agave inulin [85]. Garcia-Peris et al. [86] instead opted for a mixture of prebiotics, inulin and fructo-oligosaccharide, to stimulate proliferation of Lactobacillus spp and Bifidobacterium spp populations.
Two studies provided patients with Omega-3 supplements, with Chitapanarux et al. [83] additionally including arginine and glutamine into their supplement regimen. Whereas, Muecke et al. [96] and Yang et al. [106] provided selenium supplements to cervical cancer patients. Some focused on modifying factors through dietary changes, such as no or low-residue (little to no fibre) [104]; anti-inflammatory [112]; low fat and lactose [110]; or low fermentable oligosaccharides, disaccharides, monosaccharides and polyols (FODMAP) [100] diets. Other studies included glutamine [105], hydrolysed rice bran [90], oral resistant starch [99], immunonutrient [108] or elemental [84] supplements. One ongoing trial is evaluating the effect of time-restricted eating compared to nutritional counselling during radiotherapy [91,107].
What are the rationales underpinning these interventions?.
Any identified theories and/or rationales for each study are outlined in Tables 3-6. More broadly, multimodal interventions were introduced to improve outcomes and prevent or reduce treatment-related morbidity. Edbrooke et al. [25] identified that gynaecological cancer patients require increased emotional and social support due to high-levels of distress. They highlighted that their target patient population did not meet nutritional and exercise recommendations and had expressed the need for external motivation to drive behavioural changes [25]. Therefore, they used a multidisciplinary team to provide psychological, nutritional and exercise support underpinned by HealthChange® methodologies with features such as pedometers and text prompts to provide additional motivation [25].
Lymphoedema is a chronic process, experienced by many gynaecological cancer survivors, that is associated with physical, psychosocial and financial burden [34,39,115]. Daggez et al. [34] and Zou et al. [39] both utilise a technique that is currently used for the conservative management of lower extremity lymphoedema but introduced it in a prophylactic setting. The exercise program used by Daggez et al. [34] was chosen specifically to induce muscle function and promote lymphatic drainage. Adjuvant radiotherapy is a risk factor for lymphoedema therefore the studies included, or intend to include, post-surgical patients scheduled for radiotherapy. Similarly, as radiotherapy is also considered a risk factor for pelvic floor dysfunction, Jagdish et al. [38] and Sacomori et al. [35] adopted pelvic floor strengthening techniques more commonly used in a rehabilitation setting but initiated them prior to radiotherapy as a preventative measure. Hauth et al. [36] acknowledged that whilst a personal supervised physical activity programme is desirable for prehabilitation, it is not always feasible due to cost, geographical limitations and resources. Instead, they designed a physical activity programme that can be carried out at home, is less resource intensive, and more easily implemented into a busy radiotherapy workflow [36]. The ongoing Onkofit II trial [36] uses a wearable activity tracker to monitor patient activity and provide a motivational element to the intervention. Interestingly, when developing a physical activity programme, Tórtola-Navarro et al. [37] altered their exercise prescription relative to the timing of treatment, reducing the intensity of physical activity in the days following chemotherapy to account for the anticipated increase in side-effects experienced by the patient.
Psychological interventions aimed to reduce stress and help patients cope with the complex psychological burden associated with treatment and disease. Relaxation techniques were favoured by researchers due to their safety, accessibility, low-cost and effectiveness amongst similar populations in the literature [60,63,65,67,71]. De Oliveira Santana et al. [67] used virtual reality technology to provide a more immersive guided-imagery experience that can be applied in a clinical environment to overcome physical barriers of accessing nature. Of the studies focused specifically on patients receiving brachytherapy, interventions promoting relaxation and pain reduction were particularly prevalent due to the high levels of discomfort and distress experienced by patients. Chi et al. [56] introduced combined audiovisual stimulation to modify pain perception and maximise the anxiolytic effects of both music and guided imagery. The music was chosen with consideration of the literature suggesting a slow, constant rhythm with predictable dynamics and harmonic consonance at a tempo, similar to the resting human heart rate, was optimal for relaxation [56]. In a similar study, Lim [71] prioritised music based on individual preference and projected nature videos onto the ceiling to ensure the participant could engage with the intervention whilst lying on the therapy bed. Several studies particularly emphasised the relevance of mind-body connection as a core element of the intervention to promote relaxation [51,59,62,64,67,72]. Tagliaferri et al. [58] took a multidisciplinary approach to assess the needs of brachytherapy patients from different perspectives and developed a number of interventions and recommendations to address the needs and concerns expressed by patients. As an example, they allowed patients to select music and relaxing videos to create a relaxing environment; altered language used to reduce stressful trigger words for patients; provided an information booklet in a timely manner prior to the treatment to facilitate shared decision making; and increased staff presence in the interventional room to decrease feelings of isolation [50,58].
The prevalence of physical and psychosexual concerns following radiotherapy and the complexities of compliance with rehabilitative strategies, such as vaginal dilation, prompted researchers to counteract this with timely intervention strategies. Bergin et al. [69] and Schofield et al. [68] took a psychoeducational approach to improve coping, and reduce the psychological impact of treatment. The nurse-led consultations were included to provide tailored information at relevant timepoints throughout treatment to improve patient recall and involved elements such as radiotherapy department orientation to enhance patients’ sense of preparedness [68,69]. Peer support was a key component of the intervention to help patients make sense of their journey and provide social support [68,69]. Similarly, Jeffries et al. [52] developed a psychoeducational intervention, underpinned by a behaviour change model, involving groups of peers to normalise patient experience and overcome attitudinal barriers to care strategies. Kpoghomou et al. [70] introduced a programme in response to the lack of support patients are currently given regarding their sexual concerns, aiming to reduce side effects through supportive and educational measures.
Many of the nutritional interventions aimed to prevent or reduce the adverse gastrointestinal effects experienced by gynaecological patients, such as radiation enteritis, due to the impact on quality of life and treatment tolerability. Radiotherapy can disrupt the gut microbiota and cause intestinal inflammation and injury. A number of studies cited the positive effects of probiotics in patients with other inflammatory bowel conditions and theorised that probiotics may correct dysbiosis, improve or maintain intestinal barrier function, and/or offer beneficial immunomodulatory effects [81,82,88,93,97]. Whilst probiotic strains varied between studies, generally they were chosen due to safety and/or benefit in previous studies. Dietary changes and recommendations were often implemented to reduce or modify factors that may influence gastrointestinal toxicities. Bye et al. [110] theorised a low-fat, low-lactose diet would reduce diarrhoea during treatment by minimising faecal bile salt excretion and fluid accumulation within the intestinal lumen. However, they also highlighted that inadequate nutrition could impact healing so included compensatory measures and tailored advice to achieve sufficient energy intake and minimise weight loss. More recently, Soto-Lugo and colleagues [100] evaluated a low FODMAP diet to explore if gastrointestinal toxicity could be managed more effectively by modifying multiple factors rather than a single dietary element. Both Aredes et al. [103] and Medina-Jiménez et al. [95] aimed to reduce malnutrition and fat-free mass loss due to their association with treatment toxicity and poor outcomes. Aredes et al. [103] provided patients with nutritional risk omega-3 and nutritional formula supplements whereas Medina-Jiménez et al. [95] opted for a tailored nutritional intervention with individual counselling due to the reported benefits of this approach in other radiotherapy patient populations compared to standard recommendations.
What are the timings and duration of these interventions?.
Interventions were broadly divided between those beginning prior to radiotherapy (external-beam or brachytherapy) (n = 27) and those initiated at the point of or shortly after beginning radiotherapy (n = 29) (Fig 3). Point of intervention and duration was variable and difficult to determine for some studies due to ambiguous reporting. Most spanned the radiotherapy treatment period with some continuing for longer. The timings of individual studies are outlined in Tables 3-6, the duration of the interventions and number of sessions varied depending on factors such as treatment length (e.g., brachytherapy alone compared to chemoradiotherapy) and use of familiarisation periods.
What outcome measures are being reported within the literature?.
Outcome measures varied both across and within study categories. Quality of life was the most consistent outcome measured across studies. This was assessed by a variety of tools, used alone or in combination, including the European Organisation For Research And Treatment Of Cancer (EORTC) Core Quality of Life Questionnaire QLQ-C30 (n = 11) [27,31,37,39,53,86,88,94,100,103,108], EORTC QLQ-CX24 (cervical cancer module) (n = 3) [27,31,100], EORTC QLQ-EN24 (endometrial cancer module) (n = 1) [100], EORTC QLQ-36 (n = 1) [111], EuroQol (EQ)-5D-3L (n = 1) [103], EQ-5D-5L (n = 1) [28], Cuestionario de Calidad de Vida QL-CA-AFex (CCV) (n = 1) [60], Functional Assessment of Cancer Therapy (FACT) -General subscale (n = 5) [25,36,54,57,68], and FACT-Cervix (n = 1) [63].
Both ENABLE [25] and the ongoing RadBone trial [28] assess feasibility considering recruitment rate, attrition, and study eligibility. The ENABLE study utilised the Patient Generated-Subjective Global Assessment (PG-SGA), bioelectrical impedance, and accelerometery to assess nutritional and physical activity outcomes. Additionally, they included the Physical Activity Questionnaire-Short form and Physical Activity Assessment Inventory to measure patient-reported physical activity and self-efficacy levels respectively. Whilst the PG-SGA is used as part of the tailored nutritional intervention in Prehab4Cancer, the secondary outcome measures in RadBone centre around longitudinal changes including incidence of radiotherapy related insufficiency fractures measured by Magnetic Resonance Imaging (MRI); bone mineral density measured by Dual-Energy X-ray Absorptiometry (DEXA); biochemical markers of bone turnover; and fracture risk using the FRAX® assessment tool [28]. Alongside the EQ-5D-5L, Grigoriadou et al. [28,33] are using the Patient-Reported Outcome Version of the Common Terminology Criteria for Adverse Events (PRO- CTCAE) and the Short Form Musculoskeletal Function Assessment to assess quality of life. Both Kaliamurthi et al. [27] and Andring et al. measured treatment related morbidity taking into consideration factors such as patient reported toxicity, hospital admissions and/or length of stay.
The distinct subgroups within the physical/exercise studies resulted in some shared outcomes. The studies evaluating prophylactic physiotherapy [34,39] both utilise patient-reported symptoms from the Gynecologic Cancer Lymphedema Questionnaire to identify risk and incidence of lower extremity lymphoedema. Pelvic floor strength was a primary outcome for the pelvic floor exercise studies, with Sacomori et al. [35] opting to measure pelvic floor strength using vaginal bidigital evaluation grading with the modified Oxford scale by a physical therapist and Jagdish et al. [38] using a perineometer. Both studies also used the International Consultation on Incontinence Questionnaire-Urinary Incontinence Short Form to assess urinary incontinence. The CTCAE was chosen by Tórtola-Navarro et al. [37] and Hauth et al. [36] to assess patient reported toxicity and adverse events. In the Tórtola-Navarro et al. [37] case study, the main outcome measure was feasibility of the programme determined by patient compliance but they were also interested in functional and exercise capacity changes using the Karnofsky index and both the Six Minute Walk Test and Five Times Sit to Stand Test.
In studies evaluating psychological interventions, common outcome measures included levels of psychological distress, anxiety and/or depression using tools such as: the Distress Thermometer (n = 1) [58]; Patient Reported Outcome Measurement Information System (PROMIS) Emotional-Distress Anxiety Short Form 4a (n = 1) [73]; the Hospital Anxiety and Depression Scale (n = 8) [43,46,53,58–60,68,72]; State-Trait Anxiety Inventory (n = 3) [56,62,67]; Six-item Spielberger State Anxiety Scale (n = 1) [43]; the Self-rating Anxiety Scale (n = 2) [63,65]; an 11-point anxiety numeric rating scale (n = 1) [71]; the Self-rating Depression scale (n = 1) [63]; the Beck Depression inventory (n = 1) [65]; and the Center for Epidemiological Studies Depression Scale (n = 1) [54]. Other outcomes included level of fatigue, assessed with the Chalder (n = 1) [61] Piper (n = 1) [63], or visual analogue (n = 1) [72] fatigue scales and pain levels using a numeric (n = 3) [61,62,71] or visual (n = 3) [43,56,72] rating scale. In addition to secondary outcomes of interest such as fatigue and pain levels, Texier and Meignant [72] are utilising a 10-item to perceived stress score to evaluate the impact of an educational physiotherapy yoga on perceived stress in cervical cancer patients undergoing brachytherapy. In the ongoing SISTER study, the primary outcome of interest is treatment completion rate measured by relative dose (expected vs actual dose received at six month follow-up) [73]. As a secondary measure, Oluloro et al. [73] are also evaluating the impact of the virtual support interventions on patient-reported social isolation using the Social Provisions Scale-24 and the PROMIS Short Form Social Isolation 4a.
For nutritional studies, incidence and severity of gastrointestinal toxicities were generally measured by versions of the CTCAE (n = 11) [82,83,86,88,91,93,96,99,100,103,112] and the Radiation Therapy Oncology Group (RTOG) criteria (n = 4) [84,95,99,105]. Additionally, some studies included the Bristol stool chart to monitor change in consistency or incidence of watery stools (n = 5) [80,81,85,86,88] and monitored the administration of intestinal regulators and/or anti-diarrhoeal agents during interventions (n = 7) [81,82,84,88,90,93,97]. A subset of studies (n = 4) [85,86,105,112] monitored faecal calprotectin levels as an indicator of intestinal inflammation whereas others monitored inflammation using markers such as c-reactive protein (n = 2) [80,105]. Body mass loss (n = 2) [100,110], body mass change (n = 4) [82,84,97,112] and change in body composition (n = 2) [95,103] were also frequently used to evaluate the impact of nutritional interventions. Like the ENABLE study, Aredes et al. [103] used the PG-SGA to assess nutritional status. However, they also utilised computed tomography (CT) images to evaluate changes body composition including skeletal muscle quantity and quality. Similarly, in an ongoing trial evaluating an immunonutrition intervention for individuals with nutritional risk, prevalence of malnutrition and sarcopenia are being assessed using a modified Global Leadership Initiative on Malnutrition criteria and the Skeletal Muscle Index respectively [108]. Other outcome measures for this study focus on survival including dose-limiting toxicity-free survival, two-year overall survival, and two-year progression free survival [108].
Discussion
This scoping review identified 56 studies, spanning 66 years, evaluating unimodal or multimodal prehabilitation interventions for patients with gynaecological malignancies treated with radiotherapy. It is not entirely unexpected that cervical cancer was the most highly represented gynaecological cancer type across studies considering it is the 8th most common cancer globally [116] and is more often treated with techniques such as brachytherapy than other tumour sites. Our findings indicate there are fewer studies focusing on multimodal prehabilitation programmes. Although, it is encouraging that ongoing trials like RadBone [28] are able to utilise established prehabilitation services and integrate them into a package tailored to radiotherapy patients. Despite many studies evaluating unimodal interventions, there is a clear imbalance between the categories, with physical exercise interventions being comparatively underrepresented.
The heterogeneity of studies in respect to intervention components, initiation, duration, delivery, outcome measures and the tools used to assess these, complicates future work in the form of a systematic review or meta-analysis to build on our findings. As the scope of this review is very broad, including a wide range of records from various countries spanning six decades, some variation was anticipated. Similar issues were identified by Saggu et al. [14] in their scoping review of prehabilitation interventions for gynaecological cancer patients receiving surgery. This is further compounded by inconsistent and incomplete reporting of interventions. Study heterogeneity and ambiguous reporting are frequently cited limitations of systematic reviews and meta-analyses in similar populations [1,15,117–120]. Promisingly, tools such as the TIDieR checklist are being used in more recent studies which has improved the completeness of reporting and replicability of interventions [25]. This is particularly important when considering the rationale of a complex intervention. Despite many authors expressing the need for an intervention to address the burden patients experience, few provided clear theory or rationale underpinning design and delivery. Prehabilitation is understudied in this population therefore comprehensive and transparent reporting is essential to facilitate future intervention development and inform changes in practice [121].
The total number of outcomes measured across studies and tools used to assess these was extensive, and incomplete reporting further impeded data charting. Despite the variation in outcome measures, there were a small number of validated instruments favoured by researchers. The EORTC QLQ-C30 is designed to measure health-related quality of life specifically in individuals with cancer [122]. The frequent use of this instrument is not surprising due to its length of circulation and availability in multiple languages. However, only a small proportion of studies used it alongside the recommended disease or symptom-specific modules. Similarly, the CTCAE provides an internationally recognised standard criteria for the reporting of adverse events in cancer therapy and clinical trials. Although more recently it has been acknowledged that additional use of PRO-CTCAE can provide greater insight into patient’s perception of toxicities which is beneficial to establishing tolerability of an intervention [123]. Several patient-reported outcome measures were also used across studies which highlights growing recognition of the importance of patient experience when developing and evaluating interventions [124]. The agreement of a core outcome set (COS) that are consistently measured by widely-accepted, validated tools will facilitate greater comparison between studies to inform future decisions regarding prehabilitation and this has also been recently acknowledged in surgical populations [125]. A project to agree standardised outcome measures for prehabilitation in cancer is currently being undertaken as part of the Core Outcome Measures in Effectiveness Trials (COMET) initiative [126]. However, it is important that consideration is given to how outcomes of interest and measures of efficacy may vary between different treatment populations [127].
Nutritional interventions in this population currently aim to address malnutrition and/or minimise GI toxicities. Despite advances in radiotherapy resulting in reduced morbidity and mortality, pelvic radiotherapy patients still experience acute and chronic GI toxicities which can impact quality of life and treatment tolerability [1]. Interruptions in treatment due toxicities and increase in overall treatment time impacts radiotherapy efficacy [1,128]. Therefore, nutritional support for gynaecological patients receiving radiotherapy is an important element of prehabilitation. Minimising the impact of radiation-induced dysbiosis and intestinal injury through the introduction of pre- and probiotics was a recurring concept in the literature, yet it is acknowledged more evidence is required to gauge the effectiveness of these interventions [1]. Additionally, malnutrition may occur due to changes in gastrointestinal absorption and digestive functioning. Nutritional interventions such as dietary changes are a proactive approach to addressing GI toxicity and improving nutritional status. However, the observed variation across studies highlights that there is not yet a clear approach for these interventions. Globally, differences in radiotherapy techniques, resources and cultural differences, including dietary preferences, may account for some of the observed variation in nutritional interventions.
The physical exercise interventions discussed in this review differ from those frequently used in prehabilitation for cancer surgery. Both the studies evaluating prophylactic physiotherapy for lymphoedema [34,39] and pelvic floor strengthening [35,38] exercises, highlight how prehabilitation can be adapted to address the unique challenges of a target population. There are several factors which may explain the comparative lack of studies evaluating physical exercise interventions. Prior to radiotherapy, patients have a CT scan to develop a highly conformal plan for treatment delivery. As such, subsequent changes in body mass are avoided as they can alter the planned dose to the target volumes and organs at risk [129]. Acute side effects such as vaginal mucositis, nausea; faecal and urinary urgency; and fatigue can present during radiotherapy treatment [1,2] which may influence patients’ desire and ability to exercise. Moreover, travelling to a radiotherapy department multiple times a week for several weeks restricts patients time to participate in additional activities, frequently cited as one of the major barriers to exercise [130]. In their case study, Tórtola-Navarro et al. [37] were able to deliver a highly tailored physical activity programme with consideration for factors such as delivery of chemotherapy which impacts patients’ general wellbeing and energy levels. In the pilot randomised controlled trial ENABLE [25], healthcare professionals worked with participants to develop a home-based physical activity programme with patient-centred nutritional and activity goals, yet some patients still expressed challenges engaging with the programme whilst navigating the side-effects of treatment.
It is well-established that gynaecological cancer and its subsequent treatment has a profound impact on psychological well-being [3,6,8]. The risk of traumatisation during brachytherapy further strengthens the need for psychological support in prehabilitation for these patients [6,7]. Studies have shown that gynaecological cancer survivors have unmet informational needs exacerbating existing psychological distress including increased anxiety and feelings of embarrassment [131–134]. Tailored information, provided in a timely manner, including involvement from both healthcare professionals and peers with lived experience can contribute to engagement, patient satisfaction and feelings of preparedness [135]. It is promising that a several studies identified this as an issue and incorporated elements of patient education, in diverse formats, to address this. The psychological interventions in this review ranged from brief interventions for relaxation during brachytherapy to more complex psychoeducational interventions addressing psychosexual concerns and providing social support. The multifactorial nature of psychological distress in gynaecological cancer patients necessitates a multifaceted approach, providing patients with relevant support at an appropriate time to minimise the impact of treatment-related burden.
Prehabilitation interventions are generally considered to be those delivered between diagnosis and the beginning of acute treatment [136]. This review included studies that introduce interventions both before and during the delivery of radiotherapy, with some spanning the pre-, intra- and post-treatment periods. Prehabilitation is an evolving concept and consideration must be given to each population’s unique needs [127]. As acknowledged by Flores et al. [22], the timing of intervention delivery is influenced by the nature of radiotherapy including its role within multimodal cancer care and delayed development of acute side effects. Therefore, including interventions implemented during radiotherapy is key to understanding prehabilitation in the context of radiotherapy, particularly if multiphasic prehabilitation becomes more prevalent in the future. In the multiphasic framework, prehabilitation is viewed as a health optimising strategy initiated at multiple time points after diagnosis [127]. Prehabilitation interventions are tailored to current and anticipated experiences throughout multimodal cancer care to minimise adverse effects and reduce treatment delay [127]. Prehabilitation for a gynaecological cancer patient prior to surgery may include aerobic exercise, resistance training, psychological support and pre-operative carbohydrate loading [137]. This patient may then go on to receive prehabilitation tailored for adjuvant radiotherapy such as prophylactic complex physiotherapy, nutritional interventions to reduce GI toxicity, pelvic floor strengthening, and psychosexual support including radiotherapy-specific education. If the patient is then scheduled for brachytherapy, they will receive further targeted interventions. As prehabilitation for non-surgical therapies continues to develop, we must examine the boundaries between prehabilitation and rehabilitation. If the end of prehabilitation continues to be defined by the beginning of treatment, there may be a gap for interventions during the treatment period that align with the principles of prehabilitation and go beyond standard supportive care.
The strengths of this scoping review lie in its comprehensive and inclusive approach to exploring a relatively understudied area. By including studies evaluating unimodal interventions, this review provides a holistic summary of the evidence base and offers invaluable insight into the components, timing and rationale of prehabilitation interventions in this population. Additionally, the broad inclusion criteria ensures that this review captures a wide range of evidence, including emerging research and recent innovations. This inclusive methodology strengthens the relevance and applicability of these findings to inform future research.
There are only a handful of studies evaluating multimodal prehabilitation in this population and these are limited to smaller studies and feasibility trials with limited published results. Whilst such studies provide valuable insight, larger randomised controlled trials are required in the future to strengthen the evidence base for prehabilitation in individuals with gynaecological malignancies undergoing radiotherapy. Future studies should prioritise complete and transparent reporting of interventions and adoption of a COS informed by multiple-stakeholders to be reported as a minimum across all cancer prehabilitation trials. This will reduce ambiguity and observed heterogeneity in the literature and facilitate data synthesis to establish efficacy and inform changes in practice and policy. Physical exercise interventions remain relatively unexplored and mixed-methods approaches, as was used in ENABLE [29], can provide valuable insight as to how we can adapt interventions to overcome perceived barriers to exercise in prehabilitation for patients undergoing (chemo)radiotherapy. Involving individuals with lived experience in the intervention development process, such as in the HAPPY [56], SISTER [71] and PeNTAGOn [66] trials, is an important element for ongoing research to ensure patients’ needs are being addressed in a way that is acceptable to them.
Limitations
Despite an extensive literature search, it is possible that some studies may have been missed particularly as the term “prehabilitation” is not consistently used across the literature and only English language studies could be included due to limited resources. However, a significant amount of time was spent developing the search strategies and inclusion criteria, including extensive search terms, broad publication date ranges and information sources, to maximise the inclusion of relevant studies. It is outside the scope of this review to comment on the effectiveness of interventions and, as a risk of bias for studies was not performed, the results of this review are limited in terms of informing clinical guidance or policy. Nonetheless, this review captures the current landscape of prehabilitation in this population and highlights the gaps in current research.
Conclusion
This review highlights the diverse research relating to prehabilitation for gynaecological cancer patients undergoing radiotherapy. Interventions to reduce functional impairment and address adverse patient experiences are not necessarily a new concept but there is growing consideration for the complexities of managing treatment and disease-related burden, with increased involvement of those with lived experiences during study development. Studies evaluating unimodal interventions are more prevalent and there remains gaps in knowledge and literature that need to be addressed. Physical exercise interventions are still relatively unexplored in this patient population and consideration must be given to the barriers to physical activity experienced by this patient group. The physical and psychological impacts of cancer diagnosis and treatment are closely entwined; therefore, further development of multimodal prehabilitation interventions to cohesively address these is an important area for future research. Larger, randomised controlled trials will be useful for establishing efficacy of prehabilitation for gynaecological cancer patients undergoing radiotherapy although researchers must recognise that a nuanced approach is required. Complete and transparent reporting of interventions, along with greater consistency in outcome measures, will allow for a more cohesive approach to prehabilitation for this patient population and facilitate change in both practice and policy.
Supporting information
S1 Table. Search strategies for all databases (February 2024).
https://doi.org/10.1371/journal.pone.0319518.s002
(DOCX)
S2 Table. Search strategies for all databases (October 2024).
https://doi.org/10.1371/journal.pone.0319518.s003
(DOCX)
Acknowledgments
The authors would like to thank Eva Thackery and the research librarians at Lancashire Teaching Hospitals for their assistance informing the search strategy and peer review.
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