Background: Due to the increasing number of long-term (≥5 years post diagnosis) colorectal cancer survivors, long-term quality of life of these patients is highly relevant. Several studies have reported a positive association between physical activity and quality of life in colorectal cancer survivors, however, so far no systematic review has been published which focuses on long-term colorectal cancer survivors. Material and methods: A systematic review was conducted using the databases PubMed, Web of Science, PsychINFO, and CINAHL. Studies which investigated associations between physical activity and quality of life in long-term colorectal cancer survivors were included. Results and conclusion: Ten articles based on seven studies were identified. Long-term colorectal cancer survivors who were physically active reported better quality of life than long-term survivors who were not physically active. Both, moderate to vigorous physical activity and lower levels like light physical activity were associated with higher quality of life. Most studies assessed the association between physical activity and quality of life cross-sectionally but one prospective study which measured physical activity and quality of life at three different points in time also found associations between physical activity and quality of life. The association between physical activity and quality of life seemed to be stronger among women than among men. The findings of this systematic review support an association between physical activity and quality of life in long-term colorectal cancer survivors. However, the evidence is limited as most studies were based on cross-sectional and observational design. Keywords: Colorectal cancer, Quality of life, Physical activity, Exercise, Cancer survivor Background evidence from several studies [7–9] further suggests that In 2012, there were almost 1.4 million incident cases PA might have a positive effect on quality of life (QOL) in and roughly 700,000 deaths due to colorectal cancer CRC survivors. Studies have shown that patients who (CRC) worldwide . Colorectal cancer is the second were more physically active tended to report better QOL, most common cancer and the second leading cause of better functioning, less pain, insomnia, and fatigue [8, 9]. cancer-related deaths in Europe . However, a recent review article by Lynch et al. re- There is strong evidence that physical activity (PA), in ported inconsistent results of studies which investigated particular leisure-time PA, is associated with better overall the association between PA and QOL in short-term and [3–6] as well as CRC-specific [4, 5] survival in CRC pa- long-term (≥5 years post-diagnosis) CRC survivors. Al- tients. According to a recent meta-analysis based on 7422 though observational studies unanimously observed asso- CRC patients, PA after diagnosis was associated with a ciations between PA and QOL, the evidence is much 39% lower risk of CRC-specific mortality . Moreover, weaker from intervention studies. No systematic review to date has focused specifically on associations between PA and QOL in long-term CRC survivors. * Correspondence: firstname.lastname@example.org German Cancer Research Center (DKFZ), Divison of Clinical Epidemiology Due to recent improvements in early detection and treat- and Aging Research, Unit of Cancer Survivorship, Im Neuenheimer Feld 581, ment, the 5 year survival-rate of CRC has increased up to 69120 Heidelberg, Germany 66% [11, 12]. Thus, the QOL of long-term CRC survivors is Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Eyl et al. Health and Quality of Life Outcomes (2018) 16:112 Page 2 of 13 a highly relevant issue. Although a number of studies [13– were included. Furthermore, PA had to be the independ- 15] found that the overall QOL of CRC survivors was com- ent variable and QOL the outcome. All types of quanti- parable to the general population, they also reported that tative original studies, published in English or German, CRC survivors experience detriments in symptom-related were included. Conference abstracts, study protocols, QOL, even years after diagnosis. Studies [13, 16]further editorials, commentaries, qualitative studies, theses, re- suggest that detriments in QOL might be largest among views, and meta-analyses were not considered. There younger CRC survivors compared to cancer controls. Also, was no restriction regarding the publication date. the QOL of CRC survivors has been shown to change throughout the years after diagnosis. Jansen et al. found that Data extraction facets of QOL, such as physical functioning and pain wors- Titles and abstracts of all identified articles were screened ened over a 10-year follow-up period . Moreover, it has by the first reviewer (RE). Subsequently the full texts of been reported that CRC survivors experience different psy- the selected articles were checked for eligibility. The study chosocial and physical symptoms at various points in time characteristics of the eligible studies (e.g. first author, year, after diagnosis; for example shortly after treatment survivors journal, sample size, country, sex, age, tumor site, cancer reported more frequently symptoms such as neuropathy stage, cancer treatment, sampling, study design, comor- and sleep difficulty  whereas long-term CRC survivors bidities, inclusion and exclusion criteria, baseline response reported to have symptoms such as bowel problems, stress rate, timing/type of PA assessment, timing/type of QOL related to cancer, and depression . Due to these differ- assessment, confounders/adjustment, statistical methods, ences in psychosocial and physical symptoms between results) were independently extracted by two reviewers short-term and long-term survivors, we hypothesize that (RE and KX). Discrepancies were discussed and if they the overall effect of PA on QOL might vary. could not be solved, a third reviewer (VA) was involved. As PA may represent a promising intervention to im- prove QOL and alleviate the burden of living with can- Statistical significance and clinical relevance cer and since there has not been much research in this All statistically significant results mentioned in this re- field, this review summarizes the current available evi- view refer to a p-value <0.05. If studies reported clinical dence investigating the association between PA and relevance using either the European Organization for QOL in long-term CRC survivors. Research and Treatment of Cancer QLQ-C30 question- naire (EORTC QLQ-C30) or the Short Form Health Sur- Materials and methods vey (SF-36), the reported clinical relevance was adopted. The literature search was carried out in August 2016 and For those studies using the EORTC QLQ-C30 and not was repeated in January 2017 to guarantee inclusion of all reporting clinical relevance, we determined clinical rele- relevant publications. The databases PubMed, Web of Sci- vance by using a medium clinical relevance, which is de- ence, PsychINFO and CINAHL were searched for relevant fined by Osoba et al.  as a mean difference of ≥10 articles. The exact combinations of search terms are listed score points. in the Additional file 1: Table S1. Cross-referencing was performed to identify additional articles which were not Combining the results of different QOL instruments identified by the database search. As the included studies used various QOL instruments with different notation for the embedded scales, results Inclusion criteria pertaining different QOL scales of different question- To be included in the review, studies had to assess QOL naires were combined as shown in Table 1. in CRC patients 5 and more years post-diagnosis and PA Two reviewers (RE and KX) checked the methodo- within the time span of diagnosis to QOL assessment. logical quality of each included article using items Results of studies which investigated short-term as well adapted from the checklist of Mols et al. , with a as long-term survivors were also eligible if specific re- more detailed emphasis on contents that are important sults for long-term survivors were provided. Studies to the specific study question of this review (Table 2). comprising survivors with a mean of ≥5 years since diag- The following quality criteria were considered: nosis were also included. We did not include studies examining PA/QOL among CRC survivors regardless of 1) Information bias: time since diagnosis, since testing for a moderating ef- a) Adequate assessment of exposure (i.e. valid PA fect of time was not our major interest. All types of CRC instrument, assessment of all PA aspects, and all kinds of PA were eligible. However, QOL had to objective measure rather than self-report) be assessed by more than one scale as it is a multidi- b) Adequate assessment of outcome (i.e. valid mensional concept. When studies investigated several QOL instrument, assessment of all relevant cancer types, only the specific results for CRC survivors QOL aspects) Eyl et al. Health and Quality of Life Outcomes (2018) 16:112 Page 3 of 13 Table 1 Combining the results of different QOL instruments Table 2 Quality assessment of included studies Questionnaire Scale First author year (ref.) Potential Limitations country Global QOL EORTC QLQ- Overall QOL/ global health C30  Blanchard 2004  - No validated PA questionnaire used USA SF-36  General health and global health - Possible response bias due to composite score self-reported PA EQ-5D  Overall health related quality of life - Sample size < 100 (HRQOL) - Cross-sectional study design Physical functioning EORTC QLQ- Physical functioning Blanchard 2008  - Possible response bias due to self-reported PA C30 USA - Only assessment of leisure-time PA SF-36 Physical functioning and physical health composite score - Cross-sectional study design FACT-C  Physical well-being Blanchard 2010  - Possible response bias due to self-reported PA USA PROMIS  Physical HRQOL - Only assessment of leisure-time PA Role functioning EORTC QLQ- Role functioning - Cross-sectional study design C30 Chambers 2012  - Possible response bias due to self-reported PA SF-36 Role physical Australia - Only assessment of leisure-time PA FACT-C Functional well-being Husson 2015  - Possible response bias due to self-reported PA Social functioning EORTC QLQ- Social functioning The Netherlands C30 Mols 2015  - Possible response bias due to self-reported PA SF-36 Social functioning The Netherlands - Cross-sectional study design FACT-C Social well-being Rodriguez 2015  - Possible response bias due to self-reported PA Emotional EORTC QLQ- Emotional functioning USA - Cross-sectional study design functioning C30 Thraen-Borowski 2013  - Possible response bias due to self-reported PA SF-36 Mental health USA - Only assessment of leisure-time PA FACT-C Emotional well-being - Cross-sectional study design Van Roekel 2015  - Possible response bias due to self-reported PA The Netherlands - Cross-sectional study design c) Adequate description of data (socio- demographic and medical data is described Van Roekel 2016  - Cross-sectional study design The Netherlands e.g. age, tumor stage at diagnosis etc.; the Articles based on same study population: American Cancer Society’s Study of process of data collection is described e.g. Cancer Survivors-II (SCS-II); Articles based on same study population: All interview or self-report) patients diagnosed between 2000 and 2009 and registered in the Patient 2) Selection bias: Reported Outcomes Following Initial treatment and Long term Evaluation of Survivorship (PROFILES registry); Articles based on same study population: a) Inclusion and/or exclusion criteria are Energy for life after ColoRectal cancer (EnCoRe) formulated b) Healthy (survivor) participation bias (i.e. information about non-participants at base- Results line, information about drop-outs at follow- Literature search up, attrition bias) The search identified 988 articles (Fig. 1). After remov- 3) Study design: ing the duplicates, 740 publications remained. After a) Description of timing of PA/QOL checking titles and abstracts for eligibility, 80 relevant assessment articles were identified. Thirty articles were excluded be- b) Adequate information regarding time since cause they were not original articles, and 32 were ex- diagnosis cluded because they did not include long-term CRC c) Adequate sample size and power survivors. Two studies [22, 23] assessed QOL on only d) Prospective study design rather than cross- one scale and were therefore excluded. One study  sectional did not report any results regarding the association of 4) Correction of outcome measures for confounding PA and QOL. One study  did not report separate re- (e.g. age, sex, comorbidities) sults for CRC survivors and four studies [26–29] were excluded for several other reasons. In the end, ten arti- This systematic review was guided by the criteria, set cles based on seven studies were included in this system- out by the PRISMA guidelines . atic review. Two articles of Blanchard et al. [30, 31] were Eyl et al. Health and Quality of Life Outcomes (2018) 16:112 Page 4 of 13 Fig. 1 Literature search process. QOL: quality of life; PA: physical activity; CRC: colorectal cancer based on the same study population (American Cancer QOL assessment ranged from 68.4  to 81.5  Society’s Study of Cancer Survivors-II, SCS-II). Also the years. Two studies were restricted to long-term survi- data for the two articles of van Roekel et al. [32, 33] vors only [36, 37]. All the other studies [9, 30–35, 38] were taken from an identical study population (Energy did not provide specific results for long-term CRC sur- for life after ColoRectal cancer, EnCoRe). Further, all vivors, but comprised survivors with a mean of ≥5years CRC patients diagnosed between 2000 and 2009 as reg- since diagnosis at the time of QOL assessment. Four istered in the PROFILES cancer registry were selected studies [30–35] included CRC survivors from 2 years for the articles of Mols et al.  and Husson et al. . post-diagnosis, one prospective study included par- In case of multiple articles per study, each study only ticipants from five months post-diagnosis, but the re- counted once but results from all articles are shown in sults for the association between PA and QOL was the tables. based on PA and QOL data collected 5 years post-diagnosis. Mols et al. includedsurvivors from Study characteristics 1 year up to 11 years post-diagnosis. Participants’ characteristics The majority of the studies [9, 30, 32, 33, 35]pro- Four studies were conducted in the US [30, 31, 35–37], vided information regarding treatment, such as propor- two [9, 32–34] in the Netherlands and one in Australia tions of patients undergoing surgery, chemotherapy and  (Table 3). Sample sizes ranged from 86 to radiation. Three studies included patients with metasta- 1918 . All of the included studies investigated fe- ses [9, 30, 31, 34, 35], three studies [32, 33, 36, 38]ex- male and male survivors, but most reported a slightly cluded patients with metastases and one study did higher proportion of males. The mean age at time of not report cancer stage. Four studies [35–38]solely Eyl et al. Health and Quality of Life Outcomes (2018) 16:112 Page 5 of 13 Table 3 Study characteristics First author Study design Sample Age at survey Time since Cancer Cancer PA QOL Meeting ACS year (ref.) size diagnosis treatment stage instrument instrument PA guideline country Blanchard Cross-sectional, 86 Mean(SD) ≥2 years 33.7% Surgery I-IV Adherence SF-36 69.8% 2004  population-based 69.22(12.5) ≥5 years 30.2% Radiation to ACS PA USA ≥10 years Chemotherapy guideline 36.0% Blanchard Cross-sectional, 1918 Mean(SD) ≥2 years 33.4% Surgery I-IV GLTEQ SF-36 35% 2008  population-based 70.2(11.0) ≥5 years 35.3% Radiation USA ≥10 years Chemotherapy 31.3% Hormone therapy Immuno therapy BMT Blanchard Cross-sectional, 668 Mean(SD) ≥2 years 26.8% In treatment I-IV GLTEQ SF-36 HW 20.0% 2010  population-based 70.2(11.1) ≥5 years 40.5% (not further OW 30.0% USA ≥10 years specified) OB 24.4% 32.0% Chambers Cross-sectional & 632 Mean ≥5 years Surgery I-III AAS FACT-C – 2012  longitudinal, 69.02 Mean(SD) Chemotherapy SWLS Australia population-based 5(6.1) Husson Cross-sectional & 1739 Mean(SD) ≥2 years Radiation I-IV EPIC EORTC 82% 2015  longitudinal, 68.4(9.4) Mean(SD) Chemotherapy QLQ-C30 The population-based 5.1(2.8) Netherlands Mols 2015 Cross-sectional, 1648 Mean(SD) 1–11 years Surgery I-IV EPIC EORTC Chemotherapy:  population-based Chemotherapy: Mean(SD) Radiation QLQ-C30 93% The 66.7(9.8) Chemotherapy: CIPN20 No Netherlands No 5.6(2.8) Chemotherapy: chemotherapy: No 89% 70.6(9.0) chemotherapy: 6.1(2.8) Rodriguez Cross-sectional, 593 Mean 73.8 Only ≥5 years Number of I-III GLTEQ PROMIS – 2015  population-based Mean treatments EQ-5D USA 6.2 Thraen- Cross-sectional, 832 Mean(SD) Only ≥5 years–– CHAMPS SF-36 52% Borowski population-based 81.5(5.8) Mean(SD) 2013  8.2(1.7) USA Van Roekel Cross-sectional, 151 Mean(SD) 2–10 years Surgery I-III SQUASH EORTC 71% 2015  mono-centric 69.8(8.7) Mean(SD) Radiation QLQ-C30 The 5.7(1.8) Chemotherapy WHODAS Netherlands II CIS HADS Van Roekel Cross-sectional, 145 Mean(SD) 2–10 years Surgery I-III MMOXX1 EORTC – 2016  mono-centric 70.0(8.7) Mean(SD) Radiation QLQ-C30 The 5.7(1.9) Chemotherapy WHODAS Netherlands II CIS HADS Ref. Reference, PA physical activity, QOL quality of life, ACS PA guideline American Cancer Society physical activity recommendations of at least 150 min of MVPA per week, SF-36 The Short Form Health Survey, BMT Bone marrow transplantation, GLTEQ Godin Leisure-Time Exercise Questionnaire, HW healty weight, OW over weight, OB obese, AAS The Active Australian Survey, FACT-C Functional Assessment of Cancer Therapy-General (FACT-G) plus CRC-specific measurements, SWLS Satisfaction With Life Scale, EPIC European Prospective Investigation into Cancer Physical Activity Questionnaire, EORTC QLQ-C30 European Organization for Research and Treatment of Cancer QLQ-C30 questionnaire, CIPN20 European Organization for Research and Treatment of Cancer QLQ-CIPN20 Chemotherapy- induced peripheral neuropathy questionnaire PROMIS Patient-Reported Outcomes Measurement Information System, EQ-5D EuroQol Five-Dimension Questionnaire, CHAMPS The Community Healthy Activities Model Program for Seniors, SQUASH The Short Questionnaire to Assess Health-enhancing physical activity, WHODAS World Health Organization Disability Assessment Schedule, CIS Checklist Individual Strength, HADS Hospital Anxiety and Depression Scale, a b MMOXX1 Triaxial MOX activity monitor, Time since diagnosis at time point of QOL assessment; Articles based on same study population: American Cancer Society’s Study of Cancer Survivors-II (SCS-II); Articles based on same study population: All patients diagnosed between 2000 and 2009 and registered in the Patient Reported Outcomes Following Initial treatment and Long term Evaluation of Survivorship (PROFILES registry); Articles based on same study population: Energy for life after ColoRectal cancer (EnCoRe) Eyl et al. Health and Quality of Life Outcomes (2018) 16:112 Page 6 of 13 included survivors with a primary diagnosis of CRC, articles [9, 32–34, 37]. In four of these articles light PA the other studies did not give information about inclu- (LPA) was defined as <3 MET–h/wk, whereas moderate sion of survivors with other cancer diagnoses. Four arti- to vigorous PA (MVPA) was defined as an intensity of cles [31–33, 36] reported the inclusion of patients with ≥3 MET–h/wk [9, 32, 34, 37]. One article  defined cancer recurrence. PA as >1.5 MET–h/day and did not further differentiate Regarding cancer site, all studies included patients between LPA and MVPA. with colon as well as rectal cancers. Five studies [9, 32– 34, 36–38] included solely patients with CRC, whilst two QOL assessment studies [30, 31, 35] also included patients with other Quality of life was assessed only at one point in time in cancer types. However, the results regarding the associ- most of the studies [9, 30–33, 35–37]. Only the two longi- ation between PA and QOL as well as all figures shown tudinal studies [34, 38] assessed QOL at different inter- in Table 3 are CRC-specific, only response rates are re- vals. Chambers et al.  assessed QOL five months ported for all cancer types together [30, 31, 35]. post-diagnosis and 5 years after diagnosis. Husson et al.  assessed QOL in yearly intervals over a three year Study design period, starting with a baseline average time since diagno- All included studies were observational in design. Recruit- sis of 5.1 years. The QOL questionnaires most commonly ment methods varied across studies, six [9, 30, 31, 34–38] used were the EORTC QLQ-C30 [9, 32–34] and the used population-based recruitment, and one [32, 33] SF-36 [30, 31, 35, 37]. Information was collected by mail was completed in a single institution. Two of the articles in six studies [9, 30–32, 34–37], by telephone in five stud- [34, 38] were prospective, longitudinal designs assessing ies [30, 31, 35–38], and in person in one study . One PA and/or QOL at multiple points in time, while the study [32, 33] assessed only some of the EORTC remaining eight were cross-sectional [9, 30–33, 35–37]. QLQ-C30 subscales and additionally used the Hospital Anxiety and Depression Scale (HADS), the Checklist Indi- Response rate and follow-up rate vidual Strength (CIS), and the World Health Organization The response rates in the aforementioned cross-sectional Disability Assessment Schedule (WHODAS) question- studies ranged from 33% (notCRC-specific) to naire to assess QOL in CRC survivors. 83% . Husson et al.  reported a participation of 73% at baseline, 83% for the first and 82% for the second follow-up. In the study of Chambers et al.  Analysis, statistical methods, and clinical relevance 56% of the survivors participated in the follow-up, how- All studies compared CRC survivors who were active ever no information was given regarding baseline with those who were less active or not active. Most participation. of the studies compared survivors who met the ACS PA recommendations to those survivors who did not Assessment and categorization of PA [9, 30, 31, 34, 35, 37]. Two studies compared different Apart from one article  which measured PA pro- amounts of activity to a non-active reference group of spectively at three points in time, all other studies [9, CRC survivors [36, 38]. Some studies compared survivors´ 30–33, 35–38] assessed PA only once. One study  QOL according to higher and lower levels of LPA [32, 37] measured PA by using the Triaxial MOX activity moni- and/or MVPA [32, 34, 36, 37]. One study additionally tor (MMOXX1). The MMOXX1 is able to objectively compared lower with higher amounts of non-exercise measure sedentary, standing and PA time. Apart from (e.g. gardening) and planned exercise (PA that is planned, Blanchard et al.  who only reported the adherence or structured and repetitive e.g. jogging) . non-adherence to the American Cancer Society (ACS) All studies examined possible confounding factors PA recommendations , all other studies [9, 30–32, including age, sex, and comorbidities by some sort of 34–37] used validated PA instruments relying on multivariable regression modeling or analysis of (co)vari- self-report. The questionnaire most frequently applied ance. Six studies adjusted for body mass index (BMI) was the Godin Leisure-Time Exercise Questionnaire and only three for smoking. Three studies performed (GLTEQ) . Several studies [9, 30, 31, 34, 35, 37] used stratified analyses by age, sex, comorbidities, treatment, the PA guideline of the ACS  to differentiate be- and BMI for the association between PA and QOL. tween active and non-active survivors. The ACS recom- Two studies [9, 34] reported clinical relevance for the mends at least 150 min of moderate intensity exercise EORTC QLQ-C30. One study reported an overall clin- each week or 75 min of vigorous intensity activity each ical relevance for the SF-36 of 5–10 score points mean week or an equivalent combination of both . To fur- difference . For some studies [30, 31, 35, 38]the ther quantify the intensity of the PA, metabolic equiva- clinical relevance was not reported and could not be lent hours per week (MET–h/wk)  were used in five derived from the available information. Moreover two Eyl et al. Health and Quality of Life Outcomes (2018) 16:112 Page 7 of 13 studies used standard deviations to determine clinical studies which investigated global QOL. Differences in relevance [9, 33]. global QOL between physically active versus non-active survivors were clinically relevant in two [34, 37] of the Study findings regarding the association between PA and five studies. Three out of four studies reported a positive QOL association between PA and physical functioning, of According to the included studies, 35–80% of the CRC these two [34, 37] associations were of clinical relevance. survivors met the ACS PA recommendations (Table 3). Two studies [30, 35] did not report any results on phys- Tables 4 and 5 and the Additional file 2: Table S2 and ical functioning. In contrast, results for role and social Additional file 3: Table S3 show the study specific results functioning were more heterogeneous and less often sta- regarding the association between PA and QOL according tistically significant. to type of analysis and type of QOL instrument. Since the included studies used various QOL questionnaires, which Different levels of PA and linear association of PA and differ in included scales, not all studies contributed to the QOL results on every outcome and are thus not considered Table 5 shows the results from studies examining the as- when summarizing the respective findings. sociation between multiple levels of PA and QOL. Higher QOL was associated with both, lower and higher levels of Physically active vs. not active PA intensity but the association between PA and QOL Five of the six studies which compared active with depended on the specific QOL dimension. For instance, non-active CRC survivors, found positive associations survivors who had higher levels of LPA reported signifi- between PA and QOL (Table 4). Regarding specific sub- cantly and clinically relevant higher physical functioning scales, homogenous results were found for global QOL, than survivors who had lower LPA levels [32, 37], but no which was positively associated with PA in all of the five association was found between global QOL, social Table 4 Association of PA and QOL - Active vs. non-active Statistical significance (p <0.05) and clinical relevance a,b,c +/−: significant positive/negative clinical relevance association ns: not statistically significant .: not reported Study C30 QL PF RF EF SF CF d b b b b b Husson 2015  Meeting vs. not meeting ACS PA guideline, Interindividual + + + + + + Meeting vs. not meeting ACS PA guideline, Intraindividual ++ + ns ns ns c c c c c c Mols 2015  Meeting vs. not meeting ACS PA guideline + + + + + + Study SF-36 PF RP BP SF MH RE VT GH GCS PCS MCS Blanchard 2004  Meeting vs. not meeting ACS PA guideline . . . . . . . . + .. Blanchard 2008  Meeting vs. not meeting ACS PA guideline . . . . . . . . + .. a a a a a Thraen-Borowski 2013  Meeting vs. not meeting ACS PA guideline + + ++ ns ns + + .. . Study FACT-C/ SWLS PWB SWB EWB FWB CCS SWLS Chambers 2012  Sedentary - Ref. ns ns ns ns ns ns Insufficiently active (1–149 min/wk) Sufficiently active (≥150 min/wk) ns ns ns ns ns ns Study PROMIS/ EQ-5D Physical HRQOL Mental HRQOL Overall HRQOL c c Rodriguez 2015  PA min/wk + (≤60, 61–149, ns + (≤60, 61–149, No PA - Ref. 150–249) 150–249) ≤60, 61–149, 150–249, 250+ PA physical activity, QOL quality of life, C30 (European Organization for Research and Treatment of Cancer QLQ-C30 questionnaire) QL global quality of life, PF physical functioning, RF role functioning, EF emotional functioning, SF social functioning, CF cognitive functioning, ACS PA guideline American Cancer Society physical activity recommendations of at least 150 min of MVPA per week, SF-36 (The Short Form Health Survey) PF physical functioning, RP role limitations due to physical health problems, BP bodily pain, SF social functioning, MH general mental health, RE role limitations due to emotional problems, VT vitality, GH general health perceptions, GCS global health composite score, PCS physical composite score, MCS mental composite score, FACT-C (Functional Assessment of Cancer Therapy - Colorectal Cancer) PWB physical well-being, SWB social well-being, EWB emotional well-being, FWB functional well-being, CCS colorectal cancer scale, SWLS (Satisfaction with Life Scale), Ref. Reference, min/wk minutes per week, PROMIS (Patient-Reported Outcomes Measurement Information System), EQ-5D a b c (EuroQol Five-Dimension Questionnaire), clinical relevance reported by authors; clinical relevance calculated by RE; clinical relevance: no values, no cut-off for d e calculation available; interindividual: patients average amount of PA/ average level PA of total group; intraindividual: patients PA level at one time point/ patients average PA level Eyl et al. Health and Quality of Life Outcomes (2018) 16:112 Page 8 of 13 Table 5 Association of PA and QOL - Different levels of PA and linear association Statistical significance (p <0.05) and clinical relevance a,b,c Different levels of PA +/−: significant positive/negative clinical relevance association ns: not statistically significant .: not reported Study C30 QL PF RF EF SF CF b b Van Roekel 2015  >LPA (Q4 = ≥23.0 h/wk) vs. ns + + .ns . <LPA (Q1 = ≤2.0 h/wk) >LPA (Q3 = 10.0-22.0 h/wk) vs. .. . . . . <LPA (Q1 = ≤2.0 h/wk) >MVPA (Q4 = ≥15.5 h/wk) vs. ns + ns . ns . <MVPA (Q1 = ≤4.3 h/wk) b b >MVPA (Q3 = 8.7-15.0 h/wk) vs. ns . + .+ . <MVPA (Q1 = ≤4.3 h/wk) Study SF-36 PF RP BP SF MH RE VT GH GCS PCS MCS Thraen-Borowski >MVPA (Q4 = ≥11.3 h/wk) vs. . ... . . . . . + ns 2013  <MVPA (Q1 = 0.0 h/wk) >LPA (Q4 = ≥13.0 h/wk) vs. . ... . . . . . ns ns <LPA (Q1 = ≤1.5 h/wk) b b >LPA (Q4 = ≥9.0 h/wk) vs. . ... . . . . . + + <LPA (Q1 = 0.0 h/wk) f b >Planned exercise (Q4 = ≥9.5 h/wk) vs. . ... . . . . . + ns <Planned exercise (Q1 = 0.0 h/wk) >Non-exercise (Q4 = ≥16.5 h/wk) vs. . ... . . . . . + ns <Non-exercise (Q1 = ≤1.6 h/wk) Study WHODAS/ CIS/ HADS DIS FA DIST Van Roekel 2015  >LPA (Q4 = ≥23.0 h/wk) vs. – ns ns <LPA (Q1 = ≤2.0 h/wk) >LPA (Q3 = 10.0-22.0 h/wk) vs. ns – ns <LPA (Q1 = ≤2.0 h/wk) >MVPA (Q4 = ≥15.5 h/wk) vs. ns ns ns <MVPA (Q1 = ≤4.3 h/wk) c c c >MVPA (Q3 = 8.7-15.0 h/wk) vs. – – – <MVPA (Q1 = ≤4.3 h/wk) Study PROMIS/ EQ-5D Physical HRQOL Mental HRQOL Overall HRQOL Rodriguez 2015  MVPA min/wk. ns ns + (61–149, 150 No MVPA - Ref. +) ≤60, 61–149, 150+ ns (≤ 60) Linear association PA and QOL (continuous results) Study C30 QL PF RF EF SF CF Hussonn 2015  Continuous: Additional hour of MVPA/wk., Interindividual++ + + + + Continuous: Additional hour of MVPA/wk., Intraindividual ns + ns ns ns + Van Roekel 2016  Single-variable model, PA ns + ns . ns . Partition model, PA ns + ns . ns . Substituting 1 h/day of sedentary time with PA ns + ns . ns . Substituting 1 h/day of standing time with PA ns ns ns . ns . Study WHODAS/ CIS/ HADS DIS FA ANX DEP j c Van Roekel 2016  Single-variable model PA – ns ns ns Eyl et al. Health and Quality of Life Outcomes (2018) 16:112 Page 9 of 13 Table 5 Association of PA and QOL - Different levels of PA and linear association (Continued) Statistical significance (p <0.05) and clinical relevance a,b,c Different levels of PA +/−: significant positive/negative clinical relevance association ns: not statistically significant .: not reported Study C30 QL PF RF EF SF CF Partition model PA ns ns ns ns Substituting 1 h/day of sedentary time with PA ns ns ns ns Substituting 1 h/day of standing time with PA ns ns ns ns PA physical activity, QOL quality of life, C30 (European Organization for Research and Treatment of Cancer QLQ-C30 questionnaire), QL global quality of life, PF physical functioning, RF role functioning, EF emotional functioning, SF social functioning, CF cognitive functioning; > more; < less, LPA light physical activity (<3 MET), Q Quartile, h/wk hours per week, MVPA moderate to vigorous physical activity (≥3 MET), SF-36 (The Short Form Health Survey) PF physical functioning, RP role limitations due to physical health problems, BP bodily pain, SF social functioning, MH general mental health, RE role limitations due to emotional problems, VT vitality, GH general health perceptions, GCS global health composite score, PCS physical composite score, MCS mental composite score, WHODAS (World Health Organization Disability Assessment Schedule II) DIS disability, CIS (Checklist Individual Strength) FA fatigue, HADS (Hospital Anxiety and Depression Scale), DIST distress, ANX anxiety, DEP depression, PROMIS (Patient-Reported Outcomes Measurement Information System), EQ-5D (EuroQol Five-Dimensions a b c Questionnaire), Ref. Reference, clinical relevance reported by authors; clinical relevance calculated by RE; clinical relevance: no values, no cut-off for calculation d e f g available; participants reported LPA and MVPA; participants reported only LPA; intentional exercise e.g. jogging; non-intentional exercise e.g. gardening; h i interindividual: patients average amount of PA/ average level PA of total group; intraindividual: patients PA level at one time point/ patients average PA level; j k PA was entered separately in a single confounder-adjusted model, without adjustment for any of the other activities (sedentary, standing); all activity categories (sedentary, standing, PA) were entered simultaneously in a single confounder-adjusted model, to estimate independent associations of each activity category functioning, and LPA , respectively. Positive associa- with PA. In both investigations no significant associa- tions between MVPA and physical functioning were found tions were found in men. in two [32, 37]ofthree [32, 36, 37] studies. Survivors who Van Roekel et al. [32, 33] reported heterogeneous re- reported higher MVPA levels reported significantly and sults for the association between LPA/PA and QOL clinically relevant higher physical functioning compared stratified by number of comorbidities. Survivors with ≥2 to survivors who had lower MVPA levels [32, 37]. comorbidities who reported higher levels of LPA re- When assessing PA as a continuous variable, signifi- ported significantly and clinically relevant higher phys- cant positive associations of MVPA with higher global ical and role functioning and significantly less disability QOL, physical, emotional, social, and cognitive function- than survivors with lower levels of LPA. No associations ing were found . Van Roekel et al. reported signifi- were observed between higher levels of LPA and global cant positive associations between PA time (hour/day) QOL, social functioning, fatigue, and distress. No associ- and physical functioning and disability, however, no as- ations were reported for LPA levels and any QOL scales sociations were found for global QOL, role and social for survivors with <2 comorbidities . In contrast, functioning, fatigue, anxiety, and depression . when using sedentary time or standing time as a proxy measures of (lack of) PA, none of the QOL scales were Further subgroup analyses and changes in the associated with PA in neither survivors with <2 nor sur- association of PA and QOL over time vivors ≥2 comorbidities . Only the study by van Roekel et al. provided results Heterogeneous results were also reported regarding stratified for age  and sex [32, 33] (Additional file 2: the association between PA and QOL with respect to Table S2). The association between PA and QOL did not BMI. According to van Roekel et al.  non-obese sur- differ between younger and older survivors. However, vivors who were physically active reported higher global the association between LPA/PA and QOL seemed to be QOL, lower depression and anxiety than less active stronger among women than among men. Women who non-obese survivors. No association between PA and had higher LPA levels reported significantly and clinic- QOL was found among obese survivors. In contrast, in ally relevant higher physical, role, and social functioning the study of Blanchard et al.  no associations be- and significantly less disability compared to women who tween PA and QOL were found according to BMI. had lower LPA levels. The association of PA with global Survivors without chemotherapy treatment who were QOL, fatigue, and distress was not statistically signifi- physically active scored significantly lower on the sen- cant. When substituting one hour of sedentary time with sory, motor, and autonomic scale of the European PA, PA was clinically and significantly associated with Organization for Research and Treatment of Cancer higher physical functioning and lower disability in QLQ-CIPN20 Chemotherapy-induced peripheral neur- women. However, PA was not associated with global opathy questionnaire (CIPN 20), compared to non-active QOL, role and social functioning, fatigue, anxiety, and survivors . The association between PA and QOL depression when substituting one hour of sedentary time among CRC survivors with chemotherapy treatment did Eyl et al. Health and Quality of Life Outcomes (2018) 16:112 Page 10 of 13 not substantially differ, only no significant associations examined possible confounding factors like age, sex, and were found for PA and the autonomic scale. In both, comorbidities and used validated QOL and PA question- survivors with and without chemotherapy treatment, as- naires, most of the included studies have some short- sociations between PA and the motor scale were of clin- comings which might limit their contributions to ical relevance. existing evidence. Only one study assessed PA and QOL at various points Nine of ten included articles assessed the association in time among the same patients . In CRC survivors between PA and QOL using a cross-sectional design. For who were physically active over a three years period, role these studies we cannot assume causality, only an associ- and social functioning improved whereas role and social ation between PA and QOL at one point in time. More- functioning declined in non-active survivors. No associa- over, only few studies reported results stratified by tions were found between persistent PA and global QOL, important covariates such as age, sex, or treatment. Al- physical, emotional, and cognitive functioning . though the focus of this review article was on long-term CRC survivors, only two studies [36, 37] were identified Discussion that solely included long-term CRC survivors. All other Key findings studies included short and long-term survivors with a The results from this systematic review demonstrate that mean of 5 or more years since diagnosis. Thus, results of long-term CRC survivors who were more physically active the review are in parts not only based on long-term sur- generally reported higher QOL than non-active survivors. vivors. Since we did not include CRC survivors irre- Moreover, different PA levels such as LPA and MVPA spective of time since diagnosis, but rather focused on seemed to be associated with QOL in long-term CRC sur- long-term survivors, testing for a moderating time since vivors. The association between PA and QOL associations treatment was not possible. seemed to be stronger among women than among men. Given the older age of long-term CRC survivors and the However, no general conclusion can be drawn, since only higher number of comorbid chronic conditions, it may be few studies performed specific subgroup analyses. reasonable to assume that the magnitude of the effect of To our knowledge, three review articles [10, 42, 43] PA on QOL would be smaller, relative to short-term survi- have been published on the associations between PA and vors.However,inthe majority of theincludedstudiesthis QOL in CRC survivors. However, the articles [10, 42, 43] effect appears to remain statistically significant. published so far were based on studies which mainly A further limitation of the current studies is that the ma- included short-term CRC survivors and no systematic jority used self-reported PA measures. Only one study  review has specifically focused on long-term CRC sur- used an activity monitor to assess PA. In this context, infor- vivors. The results which were found in this review art- mation bias such as reporting bias might occur in studies icle are quite homogenous. Eight of the ten included relying on self-reported PA levels or by only assessing leis- articles found associations between PA and QOL, ure time PA, but not work-related PA. Furthermore, there whereas the results of the previous reviews are more in- were differences in the measurement tools used to assess consistent. In line with our findings, Lynch et al.  QOL which may also introduce some information bias. who included short-term and long-term survivors, also Some studies [9, 32–34, 38] used cancer-specific QOL reported associations between PA and QOL in observa- questionnaires andother studies[30, 31, 35–37]usedgen- tional studies. Otto et al. reportedthatthe associ- eral QOL instruments. Therefore the differences in the ation between PA and QOL was stable over time but QOL assessment might limit the comparability of the re- only focused on short-term survivors. In contrast, the sults. In addition, many QOL instruments specifically de- review article and meta-analysis of Cramer et al.  signed for cancer patients under active treatment, such as which included only short-term survivors did not find the EORTC QLQ-C30 and the FACT-G, with their supple- an association between PA and HRQOL. The inconsist- mentary condition-specific or symptom-specific modules, ent findings between our review and the previous are not entirely appropriate or sufficient for assessing the review articles might be explained in parts by the differ- experience of disease free cancer survivors. ent study population characteristics. The most obvious Furthermore, the sensitivity of QOL instruments and difference is the varying time since diagnosis. Due to scales to detect subtle differences in QOL may have had the heterogeneous findings, it remains unclear whether an impact on the results. For example, two of the included the overall effect of PA on QOL differs for short-term articles [31, 38] did not find any association between PA and long-term CRC patients. and QOL. An explanation for the non-significant results in the article of Chambers et al.  might be the use of Limitations specific questionnaires (FACT-C, SWLS), which might Even though the majority of the studies, included in this not be sufficiently sensitive. The other article not review had large sample sizes, were population based, finding significant associations is based on the same study Eyl et al. Health and Quality of Life Outcomes (2018) 16:112 Page 11 of 13 population as another included article  which found different PA levels such as LPA and MVPA seemed to associations between PA and QOL. However, the article of be associated with QOL in long-term CRC survivors, Blanchard et al. which did not report significant results therefore it might be beneficial for long-term CRC survi- , did not present the results for the general associa- vors to be physically active. Further prospective studies tions of PA with QOL again, but only reported the associ- and randomized controlled trials are needed to further ation between PA and QOL stratified by BMI. Therefore evaluate and confirm the causality of the association be- BMI might have been a confounding factor. tween PA and QOL specifically in long-term CRC survi- Due to the heterogeneity of the study methods and re- vors, in order to provide more solid evidence for sults, no meta-analysis could be performed. individual PA recommendations. As a result of early detection and treatment, more and more CRC patients are becoming long-term survivors Additional files . Therefore, there is a need to maintain or improve the QOL of these patients. Previous studies suggest that Additional file 1: Table S1. Search terms. (DOCX 13 kb) counselling CRC survivors to engage in regular PA is Additional file 2: Table S2. Association of PA and QOL – Subgroup analyses. (DOCX 43 kb) warranted to improve the prognosis of those patients. Additional file 3: Table S3. Association of PA and QOL - Symptom The results of this review further support a positive as- scales. (DOCX 18 kb) sociation between PA and QOL, however most included studies have some limitations regarding the study design, Abbreviations thus results should be interpreted with caution. ACS: American Cancer Society; BMI: Body mass index; CIPN20: European To overcome the aforementioned limitations and to Organization for Research and Treatment of Cancer QLQ-CIPN20 Chemotherapy-induced peripheral neuropathy questionnaire; CIS: Checklist provide more evidence regarding the causality of a poten- Individual Strength; CRC: Colorectal cancer; EORTC QLQ-C30: European tial beneficial effect of PA on QOL, there is an urgent Organization for Research and Treatment of Cancer QLQ-C30 questionnaire; need for more prospective studies assessing PA and QOL EQ-5D: EuroQol Five-Dimension Questionnaire; FACT-C: Functional Assessment of Cancer Therapy - Colorectal Cancer; GLTEQ: Godin Leisure- at multiple points in time, preferably by using a random- Time Exercise Questionnaire; HADS: Hospital Anxiety and Depression Scale; ized controlled trial design (e.g. ). Also future studies HRQOL: Overall health related quality of life; LPA: Light physical activity; should more often incorporate a prospective and validated MET–h/wk: Metabolic equivalent hours per week; MMOXX1: Triaxial MOX activity monitor; MVPA: Moderate to vigorous physical activity; PA: Physical assessment of PA, for example by including objective ac- activity; PROMIS: Patient-Reported Outcomes Measurement Information tivity monitoring, in order to learn more about the System; QOL: Quality of life; SF-36: The Short Form Health Survey; dose-response relationship of PA and QOL. More atten- SWLS: Satisfaction With Life Scale; WHODAS: World Health Organization Disability Assessment Schedule tion should be given to potential effect modification by age, gender, type of treatment, stage, and other clinically Acknowledgements relevant patients´ characteristics. As health-related QOL This work was supported by a grant from the German Federal Ministry of represents a multi-dimensional concept, studies should Education and Research (grant No 01ER1505A), KX was supported by a grant from the Chinese Scholarship Council. use validated and reliable QOL instruments for which clinically important differences have been established and Funding which cover both cancer-specific and general QOL mea- This work was supported by a grant from the German Federal Ministry of Education and Research (grant No 01ER1505A). sures regarding psychological as well as physical aspects. In order to differentiate potential specific effects of PA on Availability of data and materials QOL in CRC survivors from general effects of PA, add- Data sharing is not applicable to this article as no datasets were generated itional studies comparing CRC survivors with an or analyzed during the current study. age-matched sample from the general population as con- Authors' contributions trols might be warranted. RE: Conception of manuscript, data collection, data interpretation, writing of Future studies including the aforementioned sugges- the manuscript; KX: Data collection, Data interpretation, and approval of the tions may help to identify survivors who will benefit manuscript; VA, LK: Conception, revision, and approval of the manuscript; HB: Revision, and approval of the manuscript. All authors read and approved the most from PA intervention and to identify the point in final manuscript time and the level of PA that may be beneficial to CRC survivors. Therefore, we may potentially be able to pro- Ethics approval and consent to participate Not applicable. vide more specific and adequate recommendations re- garding PA in CRC patients. Competing interests The authors declare that they have no competing interests. Conclusions Despite the limitations of the existing evidence, the re- Publisher’sNote sults of our systematic review indicate that overall, PA is Springer Nature remains neutral with regard to jurisdictional claims in associated with better QOL in CRC survivors. Moreover, published maps and institutional affiliations. Eyl et al. Health and Quality of Life Outcomes (2018) 16:112 Page 12 of 13 Author details 18. Jansen L, Koch L, Brenner H, Arndt V. Quality of life among long-term (>/=5 years) German Cancer Research Center (DKFZ), Division of Clinical Epidemiology colorectal cancer survivors–systematic review. Eur J Cancer. 2010;46:2879–88. and Aging Research, Im Neuenheimer Feld 581, 69120 Heidelberg, Germany. 19. 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