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Identifying outcomes reported in exercise interventions in oesophagogastric cancer survivors: a systematic review

BMC Cancer volume 21, Article number: 586 (2021) Cite this article

Abstract

Background

Research investigating exercise interventions in oesophagogastric cancer survivors is sparse, and the outcomes are varied. The aim of this systematic review is to identify the domains and outcomes reported in exercise interventions in oesophagogastric cancer survivors to be included in a Delphi study, with a view to informing the development of a core outcome set (COS).

Methods

EMBASE, PubMed, CINHAL, Cochrane Library, SCOPUS, and PEDro were searched up to March 2020 using a predefined search strategy. The outcomes identified during data extraction were categorised using the core areas outlined in the OMERACT Filter 2.0.

Results

Fourteen domains and 63 outcomes were identified. The most frequently reported outcomes were in the domains of quality of life using the EORTC-QLQ-C30 questionnaire and the relevant disease-specific modules (100%), exercise capacity/fitness/physical function (100%), anthropometrics (83.33%), physical activity (66.67%), and biomarker analysis (50%).

Conclusion

This systematic review quantifies and describes the domains and outcomes examined in exercise interventions in oesophagogastric cancer survivors. Some inconsistency exists within the domains and outcomes used, and little attention was given to nutritional or economic endpoints. In order to develop a COS, a Delphi consensus process with key stakeholders is needed to identify the relevant domains and outcomes for inclusion.

Peer Review reports

Background

Oesophageal and gastric cancers account for nearly 9% of all cancers globally, with over 1.5 million new cases detected in 2018 [1]. Although survival rates are improving, surgical treatments for these cancers are associated with reduced physical functioning and poor health-related quality of life (QoL) [2,3,4]. Increasingly, exercise is being used in the management of oesophagogastric cancer, as emerging studies show that it plays a role in improving outcomes such as QoL and cardiorespiratory fitness [5, 6]. However, exercise prescription is complicated by the nutritional sequalae of the disease, including weight loss, sarcopenia, gut hormone alteration, malabsorption, and early satiety. This raises concerns that exercise training may create an excess energy deficit and contribute to further weight loss and worsening fatigue [7,8,9,10,11,12]. Therefore, interventions may need to include dietary support to ensure adequate fuel availability and replacement during and after exercise, and to manage debilitating nutritional symptoms [7, 13]. Consequently, in addition to commonly used outcomes such as QoL and exercise-related measures, it is argued that a range of other outcomes including both physical and nutritional endpoints may need to be considered in exercise interventions in oesophagogastric cancer, highlighting the value of a defined Core Outcome Set (COS) for this purpose.

A COS is defined as a standardised set of outcomes that should be measured and reported, as a minimum, in all clinical trials of a specific condition [14], thus leading to more useful trial results for data comparison and synthesis. COSs have already been developed for clinical effectiveness trials in oesophageal cancer resection surgery [15, 16], however, no COS exists for exercise interventions in oesophagogastric cancer survivors.

Little guidance exists around outcome reporting in exercise intervention trials generally, with only one relevant COS in patients with dementia under development [17]. The OMERACT Filter 2.0 [18], which was originally developed for interventions in rheumatology, provides a useful framework for identifying all key aspects, or “core areas” of a health condition, and is commonly used to aid COS development. In exercise oncology specifically, the American College of Sports Medicine Roundtable described a list of clinically relevant cancer-related health outcomes for which exercise may have therapeutic benefit, including anxiety, bone health, cardiotoxicity, chemotherapy-induced peripheral neuropathy, cognitive function, depressive symptoms, fatigue, health-related QoL, lymphoedema, pain, physical function, sleep, and treatment tolerance [7]. In addition, the 2015 Cancer and Aging Research Group NCI U13 Meeting provided recommendations for selecting outcomes for exercise intervention trials for older adults with cancer including decreased hospitalisations, reduced cancer treatment toxicity, disease prevention, disease-free survival or overall survival, and cost saving [19]. While these lists identify a considerable list of pertinent outcomes relevant to exercise interventions, there is an absence of standardisation and they lack specificity to the physical and nutritional concerns that are unique to oesophagogastric cancer survivorship.

The primary aim of this systematic review is to identify the outcomes reported in exercise interventions specifically in oesophagogastric cancer survivors to be included in a Delphi study, with a view to informing the development of a COS.

Methods

Search strategy

The search strategy was defined in consultation with a subject librarian. The strategy included a combination of disease terms (e.g. oesophageal cancer, oesophageal adenocarcinoma) and treatment terms (e.g. exercise therapy, physical training). Six electronic databases (EMBASE, PubMed, CINHAL, Cochrane Library, SCOPUS, and PEDro) were searched from inception to March 2020. The search strategy is available in Supporting Information 1.

Study inclusion and exclusion criteria

Randomised and non-randomised clinical trials were included. As the purpose of this study was to identify the outcomes used in intervention trials, all study designs, including pilot and feasibility studies and published protocols were included. Studies that were not published in English and published abstracts were excluded. Studies that recruited adults (≥18 years of age) who had completed treatment with curative intent for oesophageal, oesophagogastric junction, or gastric cancer, and had been discharged from inpatient hospital care were included. Studies including aerobic and/or resistance exercise interventions to improve and/or maintain health-related physical fitness were included [20]. Studies were excluded if they used exercise modalities to improve and/or maintain skill-related physical fitness (e.g. Pilates, yoga) alone [20]. Exercise interventions could be delivered as a unimodality intervention or as part of a multimodal rehabilitation programme (e.g. exercise in conjunction with dietary counselling). Exercise interventions completed entirely during post-operative inpatient hospital stay were excluded. Studies were excluded if it was unclear as to what outcome(s) were measured.

Study selection

Two reviewers (LOC and ES) independently screened all titles, abstracts, and full texts. Any discrepancies were resolved by discussion with a third reviewer (EG).

Data extraction

Two researchers (LOC and ES) independently extracted relevant data using a data extraction template which was developed for the purposes of this review (Supporting Information 2). Data extracted included study characteristics, patient characteristics, intervention characteristics, and outcome characteristics. Any discrepancies were resolved through discussion.

The outcomes identified during data extraction were categorised using the predetermined core areas from the OMERACT Filter 2.0 (Fig. 1) [18]. The core areas are death, life impact, and pathophysiological manifestations, and although not considered a core area, it is strongly recommended that resource use/economic impact is also included. These core areas offer useful direction, as they ensure comprehensiveness across patient-centred outcomes.

Fig. 1
figure 1

OMERACT Filter 2.0 for outcome measurement in the setting of healthcare intervention studies. Reprinted from Journal of Clinical Epidemiology, 67, Boers, M., Kirwan, J. R., Wells, G., Beaton, D., Gossec, L., d’Agostino, M. A., Conaghan, P. G., Bingham, C. O., 3rd, Brooks, P., Landewé, R., March, L., Simon, L. S., Singh, J. A., Strand, V., & Tugwell, P., Developing Core Outcome Measurement Sets for Clinical Trials: OMERACT Filter 2.0, Pages 745–753 [12], Copyright (2014), with permission from Elsevier

Full size image

Quality assessment of outcome reporting was not examined, as the purpose of this review was purely to identify the list of reported outcomes to be included in a Delphi study, and not the quality of these outcomes, or the quality of the studies within which they were measured.

Results

Search results

Electronic searches identified 3564 references. After duplicate removal and title and abstract screening using Covidence systematic review management software (https://www.covidence.org/), 27 references were identified as relevant for full text review. Of these, seven studies met the inclusion criteria and were included in the systematic review. The Rehabilitation Strategies following Oesophageal Cancer (ReStOre) programme of work included one RCT [5] and one feasibility study with two papers reporting different outcomes [21, 22]. Twenty studies were excluded due to study design (n = 7), not being published in English (n = 5), study setting (n = 3), duplication (n = 2), interventions not using aerobic and/or resistance exercise modalities (n = 1), not oesophagogastric cancer patient populations (n = 1), and lack of clarity as to what outcome(s) were measured (n = 1). For the purpose of this review, the two papers from this one feasibility study were merged.

Study characteristics

The study characteristics of the six included studies are outlined in Table 1. The included studies comprise three randomised control trials (RCTs) [5, 6, 24], two single arm feasibility studies [21,22,23], and one protocol for an RCT [25]. All included studies were published between 2017 and 2020.

Table 1 Study characteristics/participant characteristics
Full size table

Participant characteristics

Four of the studies included participants who had oesophageal cancer only [6, 21, 22, 24, 25], one study included participants who had gastric cancer only [23], and one study included participants who had either oesophageal, oesophageal junction, or gastric cancers [5]. Surgery was used as a treatment technique in all studies. Mean/median time since surgery varied from immediately post-operation to 33.68 months (Table 1).

Intervention characteristics

Exercise is defined as physical activity that is planned, structured, and repetitive, with the purpose of improving or maintaining one or more components of health-related physical fitness [26]. This review examined interventions, which prescribed aerobic and/or resistance components of exercise, and these components are described in Table 1. Study participants were supervised by physiotherapists or exercise specialists, and/or were prescribed home-based programmes following pre-intervention training by physiotherapists or exercise specialists. Three of the six studies delivered the exercise interventions as part of a multidisciplinary rehabilitation programme, which included input from other multidisciplinary team members such as nurses and dietitians [5, 6, 21, 22] (Table 2).

Table 2 Intervention characteristics
Full size table

Study outcomes

A total of 14 domains and 63 outcomes that aligned with the OMERACT Filter 2.0 were identified [27] (Table 3).

Table 3 Study outcomes
Full size table

Mortality

Survivorship

One protocol paper planned to examine this domain through the Dutch National Cancer Registry and through medical records [25].

Life impact

Quality of life

QoL was reported or planned to be reported in all six studies. All studies chose to use The European Organization for Research and Treatment of Cancer QLQ-C30 (EORTC-QLQ-C30) to measure QoL [28]. This questionnaire has a modular design with a core questionnaire and disease-specific modules. The core questionnaire contains five scales measuring function (physical, social, role, cognitive, and emotional functioning), eight symptom scales (fatigue, nausea/vomiting, pain, dyspnoea, sleep disturbances, appetite loss, constipation, and diarrhoea), financial impact, and overall QoL. In addition to the core EORTC-QLQ-C30 questionnaire [28], Chang et al. [6] and the ReStOre feasibility study [21, 22] used the oesophageal-specific module (QLQ-OES18) [29]. Cho et al. [23] used the gastric-specific cancer module (QLQ-STO22) [30] and Van Vulpen et al. [25] planned to use the oesophagogastric-specific module (QLQ-OG25) [31]. The site-specific modules take into consideration any symptoms relating specifically to upper gastrointestinal symptoms, to include xerostomia, ageusia, dysphagia, choking, indigestion, and pain on eating or drinking.

Physical activity

Physical activity refers to “all movement including during leisure time, for transport to get to and from places, or as part of a person’s work” and relates to physical activity levels and activity behaviour [32]. Physical activity levels were measured or planned to be measured using accelerometers in three studies [5, 21, 22, 25]. In addition to the use of accelerometers, Van Vulpen and colleagues [25] planned to further examine activity levels using exercise logbooks and the Short Questionnaire to Assess Health-enhancing physical activity (SQUASH) [33]. One study [24] used a six-level scale to establish participants’ activity levels, where low figures indicate a sedentary and a high score an active lifestyle.

Sleep quality

Sleep disturbance was captured in the EORTC-QLQ-C30 [28]. Van Vulpen et al. [25] also planned to capture sleep quality through the Pittsburgh Sleep Quality Index [34].

Fatigue

Similarly, fatigue was captured in the EORTC-QLQ-C30 [28]. Van Vulpen et al. [25] planned to use an additional tool, the Multidimensional Fatigue Inventory, to record fatigue [35].

Anxiety and depression

Emotional functioning was assessed in the EORTC-QLQ-C30 [28]. In addition, Van Vulpen et al. [25] planned to use the Hospital Anxiety and Depression Scale (HADS) to measure depression and anxiety [36].

Pain

Pain was measured using the EORTC-QLQ-C30 [28]. Fagevik Olsén et al. [24] also used a 100-mm visual analogue scale to assess pain specifically in the neck, rib cage, and shoulders.

Diet

Appetite loss was explored in the EORTC-QLQ-C30 [28]. Van Vulpen et al. [25] planned to explore the impact of exercise interventions on malnutrition risk using the Patient-Generated Subjective Global Assessment Short Form [37], and dietary intake using a 3-day food diary.

Recurrence

One study planned to measure disease recurrence using data from the Dutch Cancer Registry and through medical records [25].

Resource use/economic impact

Resource use/economic impact

Financial impact was assessed in the EORTC-QLQ-C30 [28]. For a more comprehensive insight into the economic impact of oesophagogastric cancer, Van Vulpen et al. [25] proposed to measure and value productivity losses using the iMTA Productivity Cost Questionnaire [38].

Pathophysiological manifestations

Biomarker analysis

Two studies assessed outcomes through serologic analysis [6, 21]. One study examined the effect of exercise on inflammatory status and oxidative stress [21], while another examined albumin as a measure of nutritional status [6]. One other study planned to collect blood serum, plasma and cell pellet for future analyses of biomarkers [25].

Respiratory function

Fagevik Olsén et al. [23] assessed respiratory function by measuring forced vital capacity, forced expiratory volume in 1 s, and peak expiratory flow, using a spirometer.

Exercise capacity/fitness/physical function

Exercise capacity, fitness and/or physical function refer to an individual’s ability to undertake exercise and physical tasks of everyday living [39] and were measured or planned to be measured in all studies. Five studies measured or planned to measure exercise capacity using maximal cardiopulmonary exercise tests (CPETs) [5, 6, 21,22,23, 25]. In addition to CPETs, Chang et al. [6] and The ReStOre feasibility study [21, 22] measured functional capacity using the distance mobilised in the Six-Minute Walk Test [40].

Grip strength is often used as an indicator of overall muscle strength and was included as an outcome to be measured using a dynamometer in three studies [23,24,25].

Measures of lower extremity strength and physical capacity were captured using tools such as sit-to-stand tests [23, 24]. Cho et al. [23] used the 30 Second Sit to Stand Test [41], and Fagevik Olsén et al. [24] recorded the time needed to stand 10 times from a standard chair. As well as the Sit-to-Stand Test, Fagevik Olsén et al. [24] recorded the time needed to perform 10 heel raises without support.

Flexibility was assessed by Cho et al. [23] through the back-stretch exercise and a sit-and-reach exercise, and endurance was evaluated through the wall half squat test. Range of motion was assessed by Fagevik et al. [24] using a goniometer to measure the difference in chest expansion, thoracic flexion and extension, thoracic lateral flexion, active shoulder flexion and abduction.

The Disability Rating Index was employed by Fagevik Olsén et al. [24] to assess physical disability [42]. This questionnaire comprises 12 questions, which focus on basic activities of daily life, physical activities, and work-related/more vigorous activities.

Anthropometrics

Five studies monitored or planned to monitor participants’ body composition throughout the exercise interventions [5, 6, 21,22,23, 25].

Height and weight were reported in the ReStOre feasibility study, the ReStOre RCT, and by Cho et al. [5, 21,22,23]. Body mass index (BMI) was recorded by Chang et al. [6] and the ReStOre feasibility study [21, 22]. Van Vulpen et al. [25] also planned to record height, weight, and BMI.

In addition, Cho et al. [23] measured the circumference of the abdomen, waist, upper arm, lower arm, hips, thigh, and calf. The ReStOre feasibility study and the ReStOre RCT [5, 21, 22] recorded waist and midarm circumference measurements, and van Vulpen et al. [25] planned to measure waist and hip circumference.

The ReStOre RCT and the ReStOre feasibility study [5, 21, 22] both examined body composition using bioimpedance analysis, which estimated fat mass, fat mass percentage, fat-free mass, fat mass index, fat-free mass index, and skeletal muscle mass. Similarly, Cho et al. [23] calculated percent body fat using the 7-site Jackson Pollock skinfold equation [43]. They also recorded subcutaneous fat thickness of chest/pectoral, midaxillary, abdominal, suprailiac, subscapular, triceps, and thigh muscles. Furthermore, they recorded values for muscle and fat volumes by obtaining muscle computed tomography (CT) cross-sectional areas of whole muscular components and fatty CT cross-sectional areas of visceral and subcutaneous fat at the levels of T11–12, L2–3, L3–4, and L4–5.

Discussion

This review is the first stage in the development of a COS, and as such is an important information source. From this systematic review, we have identified a potential list of outcomes to be included in a Delphi study, which is the next step in developing a COS. The six studies eligible for inclusion have all been published since 2017, illustrating that this area of research is still in its infancy. This presents a timely opportunity to develop a COS.

Fourteen domains and 63 outcomes were reported in the included studies. All studies reported outcomes in the domains of QoL and exercise capacity/fitness/physical function. Less consistently reported outcomes were anthropometrics, physical activity, and blood analysis. One trial protocol planned to explore diet and nutrition as its own outcome [25]. This may be an important outcome for inclusion, as distressing bowel symptoms related to food intake, such as urgency, flatus, and diarrhoea, are commonly reported in this population [44, 45]. In a study of 100 bowel cancer survivors, 10% of participants identified physical activity as a precipitator of distressing bowel symptoms and 73% of participants restricted leisure activities in deference to the bowel symptoms they experienced [46]. Thus, it can be hypothesised that the symptoms experienced by oesophagogastric cancer survivors may have a negative impact on exercise participation, and therefore, these symptoms may require monitoring. Furthermore, reduced nutrient intake is associated with sarcopenia, which is reported in 26 to 75% of oesophageal cancer patients [47]. The European Working Group on Sarcopenia in Older People 2 (EWGSOP2) uses low muscle strength as the primary parameter of sarcopenia. A sarcopenia diagnosis is then confirmed by detection of low muscle quantity and quality using dual-energy X-ray absorptiometry (DXA), bioelectrical impedance analysis (BIA), magnetic resonance imaging (MRI), or computed tomography (CT) [48]. Only three studies in this review assessed muscle strength [23,24,25], and four studies measured low muscle quantity and quality using BIA or CT [5, 21,22,23]. These outcomes may be important measures in the identification, and consequent management, of sarcopenia, and may warrant inclusion when designing exercise interventions for oesophagogastric cancer survivors.

Research examining the cost-effectiveness of exercise interventions in some cancer populations, such as breast and colon, is emerging [49, 50], yet little is known about the economic impact of these exercise interventions in oesophagogastric cancer survivors. Although one trial protocol did plan to include the economic impact of oesophagogastric cancer on the individual [25], no study estimated the economic impact on society. This is considered important, as rising health care costs present challenges, even in wealthy societies [18, 19, 51].

In order to enhance the quality of health care to make better decisions about interventions, a COS should contain the outcomes which are most important to the stakeholders [52]. Stakeholders should comprise those who will use the COS in research, healthcare professionals with experience of patients with oesophagogastric cancer, oesophagogastric cancer survivors and/or their representatives in order to reach agreement on the outcomes to be included [53]. By including these stakeholders in the COS development process and in defining the endpoints for future studies, an interdisciplinary and collaborative approach is ensured allowing for a broad variety of relevant outcomes to be assessed. The stakeholders should also inform how and when these outcomes should be measured. The next step in this COS development process involves a Delphi consensus process with these key stakeholders [54].

Limitations

This review has some limitations. Only studies published in English were included in this review and studies in other languages may have been inadvertently excluded. Few eligible studies were identified (n = 6) and one included study is a protocol, but the findings are still important in directing the next phase of this research. There was heterogeneity between included studies due to different patient characteristics and intervention characteristics. Most of the patients in this review had a diagnosis of oesophageal cancer and underwent open surgical treatment. However, some patients with gastric cancer were treated using minimally invasive surgical procedures which may result in a different rehabilitation journey. Furthermore, some participants received chemotherapy and/or radiotherapy in addition to surgery, and time since surgery differed between studies. It could be argued that these factors may have impacted the researchers’ justification of outcome choice, but the next phase of COS development will determine the salience of these outcomes. This study provides a starting point.

Conclusion

The variation and potential gaps in outcomes reported in exercise interventions for oesophagogastric cancer survivors warrants the development of a COS, and this systematic review forms the first phase of its development. By ensuring that all interventions and reported outcomes are comprehensive in their approach, a COS would improve the quality of future research and influence oesophagogastric cancer survivorship.

Availability of data and materials

All data generated and analysed during this study are included in this published article and its supplementary information files. Supplementary information files can be requested from the corresponding author (EG).

Abbreviations

BMI:

Body mass index

Borg Scale:

Borg Scale of Relative Perceived Exertion

COMET:

Core Outcome Measures in Effectiveness Trials

COS:

Core outcome set

CPET:

Cardiopulmonary exercise test

CT:

Computed tomography

EORTC-QLQ-C30:

The European Organization for Research and Treatment of Cancer QLQ-C30

EORTC-QLQ-OES18:

The European Organization for Research and Treatment of Cancer oesophageal-specific module

EORTC-QLQ-OG25:

The European Organization for Research and Treatment of Cancer oesophagogastric-specific module

EORTC-QLQ-STO22:

The European Organization for Research and Treatment of Cancer gastric-specific module

EWGSOP2:

The European Working Group on Sarcopenia in Older People 2

HRR:

Heart rate reserve

Mins:

Minutes

N/A:

Not applicable

QoL:

Quality of life

ReStOre:

The Rehabilitation Strategies following Oesophageal Cancer

RCT:

Randomised control trial

Reps:

Repetitions

RM:

Repetition Maximum

SQUASH:

Short Questionnaire to Assess Health-enhancing physical activity

References

  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424. https://doi.org/10.3322/caac.21492.

    Article  PubMed  Google Scholar 

  2. Scarpa M, Valente S, Alfieri R, Cagol M, Diamantis G, Ancona E, et al. Systematic review of health-related quality of life after esophagectomy for esophageal cancer. World J Gastroenterol. 2011;17(42):4660–74. https://doi.org/10.3748/wjg.v17.i42.4660.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Barbour AP, Lagergren P, Hughes R, Alderson D, Barham CP, Blazeby JM. Health-related quality of life among patients with adenocarcinoma of the gastro-oesophageal junction treated by gastrectomy or oesophagectomy. Br J Surg. 2008;95(1):80–4. https://doi.org/10.1002/bjs.5912.

    Article  CAS  PubMed  Google Scholar 

  4. Gannon JA, Guinan EM, Doyle SL, Beddy P, Reynolds JV, Hussey J. Reduced fitness and physical functioning are long-term sequelae after curative treatment for esophageal cancer: a matched control study. Dis Esophagus. 2017;30(8):1–7. https://doi.org/10.1093/dote/dox018.

    Article  CAS  PubMed  Google Scholar 

  5. O'Neill LM, Guinan E, Doyle SL, Bennett AE, Murphy C, Elliott JA, et al. The RESTORE randomized controlled trial: impact of a multidisciplinary rehabilitative program on cardiorespiratory fitness in esophagogastric cancer survivorship. Ann Surg. 2018;268(5):747–55. https://doi.org/10.1097/SLA.0000000000002895.

    Article  PubMed  Google Scholar 

  6. Chang YL, Tsai YF, Hsu CL, Chao YK, Hsu CC, Lin KC. The effectiveness of a nurse-led exercise and health education informatics program on exercise capacity and quality of life among cancer survivors after esophagectomy: a randomized controlled trial. Int J Nurs Stud. 2020;101:103418. https://doi.org/10.1016/j.ijnurstu.2019.103418.

    Article  PubMed  Google Scholar 

  7. Campbell KL, Winters-Stone KM, Wiskemann J, May AM, Schwartz AL, Courneya KS, et al. Exercise guidelines for cancer survivors: consensus statement from international multidisciplinary roundtable. Med Sci Sports Exerc. 2019;51(11):2375–90. https://doi.org/10.1249/MSS.0000000000002116.

    Article  PubMed  Google Scholar 

  8. Ryan AM, Healy LA, Power DG, Rowley SP, Reynolds JV. Short-term nutritional implications of total gastrectomy for malignancy, and the impact of parenteral nutritional support. Clin Nutr. 2007;26(6):718–27. https://doi.org/10.1016/j.clnu.2007.08.013.

    Article  PubMed  Google Scholar 

  9. Martin L, Jia C, Rouvelas I, Lagergren P. Risk factors for malnutrition after oesophageal and cardia cancer surgery. Br J Surg. 2008;95(11):1362–8. https://doi.org/10.1002/bjs.6374.

    Article  CAS  PubMed  Google Scholar 

  10. Martin L, Lagergren P. Long-term weight change after oesophageal cancer surgery. Br J Surg. 2009;96(11):1308–14. https://doi.org/10.1002/bjs.6723.

    Article  CAS  PubMed  Google Scholar 

  11. Elliott JA, Docherty NG, Eckhardt HG, Doyle SL, Guinan EM, Ravi N, et al. Weight loss, satiety, and the postprandial gut hormone response after esophagectomy: a prospective study. Ann Surg. 2017;266(1):82–90. https://doi.org/10.1097/SLA.0000000000001918.

    Article  PubMed  Google Scholar 

  12. Heneghan HM, Zaborowski A, Fanning M, McHugh A, Doyle S, Moore J, et al. Prospective study of malabsorption and malnutrition after esophageal and gastric cancer surgery. Ann Surg. 2015;262(5):803–7; discussion 7-8. https://doi.org/10.1097/SLA.0000000000001445.

    Article  PubMed  Google Scholar 

  13. O'Neill L, Gannon J, Guinan E, Reynolds JV, Hussey J. Multidisciplinary rehabilitation across the esophageal cancer journey. J Thorac Dis. 2017;9(12):E1140–e2. https://doi.org/10.21037/jtd.2017.11.72.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Williamson PR, Altman DG, Bagley H, Barnes KL, Blazeby JM, Brookes ST, et al. The COMET handbook: version 1.0. Trials. 2017;18(Suppl 3):280.

    Article  Google Scholar 

  15. Blazeby JM, Macefield R, Blencowe NS, Jacobs M, McNair AG, Sprangers M, et al. Core information set for oesophageal cancer surgery. Br J Surg. 2015;102(8):936–43. https://doi.org/10.1002/bjs.9840.

    Article  CAS  PubMed  Google Scholar 

  16. Avery KNL, Chalmers KA, Brookes ST, Blencowe NS, Coulman K, Whale K, et al. Development of a core outcome set for clinical effectiveness trials in esophageal cancer resection surgery. Ann Surg. 2018;267(4):700–10. https://doi.org/10.1097/SLA.0000000000002204.

    Article  PubMed  Google Scholar 

  17. Gonçalves AC, Cruz J, Marques A, Demain S, Samuel D. Evaluating physical activity in dementia: a systematic review of outcomes to inform the development of a core outcome set. Age Ageing. 2018;47(1):34–41. https://doi.org/10.1093/ageing/afx135.

    Article  PubMed  Google Scholar 

  18. Boers M, Kirwan JR, Wells G, Beaton D, Gossec L, d'Agostino MA, et al. Developing core outcome measurement sets for clinical trials: OMERACT filter 2.0. J Clin Epidemiol. 2014;67(7):745–53. https://doi.org/10.1016/j.jclinepi.2013.11.013.

    Article  PubMed  Google Scholar 

  19. Kilari D, Soto-Perez-de-Celis E, Mohile SG, Alibhai SM, Presley CJ, Wildes TM, et al. Designing exercise clinical trials for older adults with cancer: recommendations from 2015 cancer and aging research group NCI U13 meeting. J Geriatr Oncol. 2016;7(4):293–304. https://doi.org/10.1016/j.jgo.2016.04.007.

    Article  PubMed  PubMed Central  Google Scholar 

  20. American College of Sports Medicine. ACSM’s guidelines for exercise testing and prescription. 10th ed. Philadelphia: Wolters Kluwer; 2018.

    Google Scholar 

  21. Guinan EM, Doyle SL, O'Neill L, Dunne MR, Foley EK, O'Sullivan J, et al. Effects of a multimodal rehabilitation programme on inflammation and oxidative stress in oesophageal cancer survivors: the ReStOre feasibility study. Support Care Cancer. 2017;25(3):749–56. https://doi.org/10.1007/s00520-016-3455-0.

    Article  PubMed  Google Scholar 

  22. O’Neill L, Guinan E, Doyle SL, Elliott JA, O’Sullivan J, Reynolds JV, et al. Rehabilitation strategies following esophageal cancer (the ReStOre trial): a feasibility study. 2017.

    Google Scholar 

  23. Cho I, Son Y, Song S, Bae YJ, Kim YN, Kim HI, et al. Feasibility and effects of a postoperative recovery exercise program developed specifically for gastric cancer patients (PREP-GC) undergoing minimally invasive gastrectomy. J Gastric Cancer. 2018;18(2):118–33. https://doi.org/10.5230/jgc.2018.18.e12.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Fagevik Olsén M, Kjellby Wendt G, Hammerlid E, Smedh U. Effects of a training intervention for enhancing recovery after Ivor-Lewis esophagus surgery: a randomized controlled trial. Scand J Surg. 2017;106(2):116–25. https://doi.org/10.1177/1457496916655499.

    Article  PubMed  Google Scholar 

  25. van Vulpen JK, Siersema PD, van Hillegersberg R, Nieuwenhuijzen GAP, Kouwenhoven EA, Groenendijk RPR, et al. Physical exeRcise following esophageal cancer treatment (PERFECT) study: design of a randomized controlled trial. BMC Cancer. 2017;17(1):552. https://doi.org/10.1186/s12885-017-3542-8.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Caspersen CJ, Powell KE, Christenson GM. Physical activity, exercise, and physical fitness: definitions and distinctions for health-related research. Public Health Rep. 1985;100(2):126–31.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. van Tol RR, van Zwietering E, Kleijnen J, Melenhorst J, Stassen LPS, Dirksen CD, et al. Towards a core outcome set for hemorrhoidal disease-a systematic review of outcomes reported in literature. Int J Color Dis. 2018;33(7):849–56. https://doi.org/10.1007/s00384-018-3046-2.

    Article  Google Scholar 

  28. Aaronson NK, Ahmedzai S, Bergman B, Bullinger M, Cull A, Duez NJ, et al. The European Organization for Research and Treatment of Cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology. J Natl Cancer Inst. 1993;85(5):365–76. https://doi.org/10.1093/jnci/85.5.365.

    Article  CAS  PubMed  Google Scholar 

  29. Blazeby JM, Conroy T, Hammerlid E, Fayers P, Sezer O, Koller M, et al. Clinical and psychometric validation of an EORTC questionnaire module, the EORTC QLQ-OES18, to assess quality of life in patients with oesophageal cancer. Eur J Cancer. 2003;39(10):1384–94. https://doi.org/10.1016/S0959-8049(03)00270-3.

    Article  CAS  PubMed  Google Scholar 

  30. Blazeby JM, Conroy T, Bottomley A, Vickery C, Arraras J, Sezer O, et al. Clinical and psychometric validation of a questionnaire module, the EORTC QLQ-STO 22, to assess quality of life in patients with gastric cancer. Eur J Cancer. 2004;40(15):2260–8. https://doi.org/10.1016/j.ejca.2004.05.023.

    Article  CAS  PubMed  Google Scholar 

  31. Lagergren P, Fayers P, Conroy T, Stein HJ, Sezer O, Hardwick R, et al. Clinical and psychometric validation of a questionnaire module, the EORTC QLQ-OG25, to assess health-related quality of life in patients with cancer of the oesophagus, the oesophago-gastric junction and the stomach. Eur J Cancer. 2007;43(14):2066–73. https://doi.org/10.1016/j.ejca.2007.07.005.

    Article  PubMed  Google Scholar 

  32. World Health Organization. Physical activity. 2020. Available from: https://www.who.int/news-room/fact-sheets/detail/physical-activity.

    Google Scholar 

  33. Wendel-Vos GC, Schuit AJ, Saris WH, Kromhout D. Reproducibility and relative validity of the short questionnaire to assess health-enhancing physical activity. J Clin Epidemiol. 2003;56(12):1163–9. https://doi.org/10.1016/S0895-4356(03)00220-8.

    Article  PubMed  Google Scholar 

  34. Buysse DJ, Reynolds CF 3rd, Monk TH, Berman SR, Kupfer DJ. The Pittsburgh sleep quality index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989;28(2):193–213. https://doi.org/10.1016/0165-1781(89)90047-4.

    Article  CAS  PubMed  Google Scholar 

  35. Smets EM, Garssen B, Bonke B, De Haes JC. The multidimensional fatigue inventory (MFI) psychometric qualities of an instrument to assess fatigue. J Psychosom Res. 1995;39(3):315–25. https://doi.org/10.1016/0022-3999(94)00125-O.

    Article  CAS  PubMed  Google Scholar 

  36. Zigmond AS, Snaith RP. The hospital anxiety and depression scale. Acta Psychiatr Scand. 1983;67(6):361–70. https://doi.org/10.1111/j.1600-0447.1983.tb09716.x.

    Article  CAS  Google Scholar 

  37. Gabrielson DK, Scaffidi D, Leung E, Stoyanoff L, Robinson J, Nisenbaum R, et al. Use of an abridged scored patient-generated subjective global assessment (abPG-SGA) as a nutritional screening tool for cancer patients in an outpatient setting. Nutr Cancer. 2013;65(2):234–9. https://doi.org/10.1080/01635581.2013.755554.

    Article  PubMed  Google Scholar 

  38. Bouwmans C, Krol M, Severens H, Koopmanschap M, Brouwer W, Hakkaart-van RL. The iMTA productivity cost questionnaire: a standardized instrument for measuring and valuing health-related productivity losses. Value Health. 2015;18(6):753–8. https://doi.org/10.1016/j.jval.2015.05.009.

    Article  PubMed  Google Scholar 

  39. Cooper R, Kuh D, Cooper C, Gale CR, Lawlor DA, Matthews F, et al. Objective measures of physical capability and subsequent health: a systematic review. Age Ageing. 2011;40(1):14–23. https://doi.org/10.1093/ageing/afq117.

    Article  PubMed  Google Scholar 

  40. ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories. ATS statement: guidelines for the six-minute walk test. Am J Respir Crit Care Med. 2002;166(1):111–7.

    Article  Google Scholar 

  41. Jones CJ, Rikli RE, Beam WC. A 30-s chair-stand test as a measure of lower body strength in community-residing older adults. Res Q Exerc Sport. 1999;70(2):113–9. https://doi.org/10.1080/02701367.1999.10608028.

    Article  CAS  PubMed  Google Scholar 

  42. Salén BA, Spangfort EV, Nygren AL, Nordemar R. The disability rating index: an instrument for the assessment of disability in clinical settings. J Clin Epidemiol. 1994;47(12):1423–35. https://doi.org/10.1016/0895-4356(94)90086-8.

    Article  PubMed  Google Scholar 

  43. Jackson AS, Pollock ML, Gettman LR. Intertester reliability of selected skinfold and circumference measurements and percent fat estimates. Restor Q. 1978;49(4):546–51.

    CAS  Google Scholar 

  44. Graham L, Wikman A. Toward improved survivorship: supportive care needs of esophageal cancer patients, a literature review. Dis Esophagus. 2016;29(8):1081–9. https://doi.org/10.1111/dote.12424.

    Article  CAS  PubMed  Google Scholar 

  45. Verschuur EM, Steyerberg EW, Kuipers EJ, Essink-Bot ML, Tran KT, Van Der Gaast A, et al. Experiences and expectations of patients after oesophageal cancer surgery: an explorative study. Eur J Cancer Care (Engl). 2006;15(4):324–32. https://doi.org/10.1111/j.1365-2354.2006.00659.x.

    Article  CAS  Google Scholar 

  46. Yin L, Fan L, Tan R, Yang G, Jiang F, Zhang C, et al. Bowel symptoms and self-care strategies of survivors in the process of restoration after low anterior resection of rectal cancer. BMC Surg. 2018;18(1):35. https://doi.org/10.1186/s12893-018-0368-5.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Elliott JA, Doyle SL, Murphy CF, King S, Guinan EM, Beddy P, et al. Sarcopenia: prevalence, and impact on operative and oncologic outcomes in the multimodal management of locally advanced esophageal cancer. Ann Surg. 2017;266(5):822–30. https://doi.org/10.1097/SLA.0000000000002398.

    Article  PubMed  Google Scholar 

  48. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48(4):601. https://doi.org/10.1093/ageing/afz046.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Gordon LG, DiSipio T, Battistutta D, Yates P, Bashford J, Pyke C, et al. Cost-effectiveness of a pragmatic exercise intervention for women with breast cancer: results from a randomized controlled trial. Psychooncology. 2017;26(5):649–55. https://doi.org/10.1002/pon.4201.

    Article  PubMed  Google Scholar 

  50. May AM, Bosch MJ, Velthuis MJ, van der Wall E, Steins Bisschop CN, Los M, et al. 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. 2017;7(3):e012187. https://doi.org/10.1136/bmjopen-2016-012187.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Ramsey S, Willke R, Briggs A, Brown R, Buxton M, Chawla A, et al. Good research practices for cost-effectiveness analysis alongside clinical trials: the ISPOR RCT-CEA task force report. Value Health. 2005;8(5):521–33. https://doi.org/10.1111/j.1524-4733.2005.00045.x.

    Article  PubMed  Google Scholar 

  52. Clarke M, Williamson PR. Core outcome sets and systematic reviews. Syst Rev. 2016;5(1):11. https://doi.org/10.1186/s13643-016-0188-6.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Kirkham JJ, Davis K, Altman DG, Blazeby JM, Clarke M, Tunis S, et al. Core outcome set-STAndards for development: the COS-STAD recommendations. PLoS Med. 2017;14(11):e1002447. https://doi.org/10.1371/journal.pmed.1002447.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Williamson PR, Altman DG, Blazeby JM, Clarke M, Devane D, Gargon E, et al. Developing core outcome sets for clinical trials: issues to consider. Trials. 2012;13(1):132. https://doi.org/10.1186/1745-6215-13-132.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We would like to thank Mr. David Mockler, medical librarian at Trinity College Dublin, for developing the search strategy for this systematic review.

Funding

Louise O’Connor is supported through funding from Health Research Board Ireland grant DIFA-FA-2018-009. The funding body had no role in the design of the study; in the collection, analysis and interpretation of data; or in writing the manuscript.

Author information

Authors and Affiliations

  1. Discipline of Physiotherapy, School of Medicine, Trinity College Dublin, Dublin, Ireland

    Louise O’Connor, Emily Smyth, Linda O’Neill & Juliette Hussey

  2. Discipline of Clinical Medicine, Trinity College Dublin, Dublin, Ireland

    Annemarie E. Bennett

  3. School of Nursing & Midwifery, Trinity College Dublin, Dublin, Ireland

    Valerie Smith

  4. Department of Survery St James’s Hospital and Trinity Translational Medicine Institute, Trinity College Dublin, Dublin, Ireland

    John V. Reynolds

  5. School of Medicine, Trinity College Dublin, Dublin, Ireland

    Emer Guinan

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  1. Louise O’Connor
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  5. Linda O’Neill
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  6. John V. Reynolds
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  8. Emer Guinan
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Contributions

LOC and LON developed and applied the search strategy. LOC and ES carried out data extraction and data analysis. LOC and EG wrote the initial and final drafts of the manuscript, and ES, LON, AB, VS, JR, and JH made contributions to the revision of the manuscript. ES, LON, AB, VS, JR and JH read and approved the final manuscript. The author(s) read and approved the final manuscript.

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Correspondence to Emer Guinan.

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Competing interests

Dr. Emer Guinan currently serves as an associate editor of the BMC Cancer Journal.

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Supplementary Information

Additional file 1: Supporting Information 1.

Search Strategy. Supporting Information 2. Data Extraction.

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O’Connor, L., Smyth, E., Bennett, A.E. et al. Identifying outcomes reported in exercise interventions in oesophagogastric cancer survivors: a systematic review. BMC Cancer 21, 586 (2021). https://doi.org/10.1186/s12885-021-08290-w

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BMC Cancer

ISSN: 1471-2407

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