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Adherence to the World Cancer Research Fund/American Institute for Cancer Research recommendations for cancer prevention is associated with better health–related quality of life among long-term colorectal cancer survivors: results of the PROFILES registry

Adherence to the World Cancer Research Fund/American Institute for Cancer Research... Since colorectal cancer (CRC) survivors often suffer from long-term adverse health effects of the cancer and its treatment, having a negative impact on their health-related quality of life (HRQL), this study focuses on the association between adherence to WCRF/AICR recommendations and HRQL among CRC survivors. In a cross-sectional PROFILES registry study in 1096 CRC survivors (mean time since diagnosis 8.1 years), WCRF/AICR adherence scores (range 0–8, with a higher score for better adherence) were calculated, and HRQL was assessed using the EORTC QLQ-C30. Associations between adherence scores and HRQL scores were investigated using linear regression analyses. Additionally, associations with adherence to guidelines for body mass index (BMI) (normal weight, overweight and obese), physical activity (PA) (score 0/1) and diet (score < 3, 3– <4 and > 4) were evaluated separately. Mean adherence score was 4.81 ± 1.04. Higher WCRF/AICR scores were associated with better global health status (β 1.64; 95%CI 0.69/2.59), physical functioning (β 2.71; 95%CI 1.73/3.68), role functioning (β 2.87; 95%CI 1.53/4.21), cognitive functioning (β 1.25; 95%CI 0.19/2.32), social functioning (β 2.01; 95%CI 0.85/3.16) and fatigue (β − 2.81; 95%CI − 4.02/− 1.60). Adherence versus non-adherence PA was significantly associated with better physical, role, emotional and social functioning, global health status and less fatigue. Except for the association between being obese and physical functioning (β − 4.15; 95%CI − 47.16/− 1.15), no statistically significant associations with physical functioning were observed comparing adherence to non-adherence to BMI and dietary recommendations. Better adherence to the WCRF/AICR recommendations was positively associated with global health status, most functioning scales and less fatigue among CRC survivors. PA seemed to be the main contributor. . . . . . Keywords Colorectal cancer survivors Health-related quality of life WCRF guidelines Dietary guidelines Physical activity Body composition Introduction * Merel R. van Veen merelrvanveen@gmail.com In 2007, the World Cancer Research Fund/American Institute for Cancer Research (WCRF/AICR) launched the diet and 1 physical activity recommendations for cancer prevention [1]. Department of Research & Development, Netherlands Cancer survivors, defined as people who are living with a Comprehensive Cancer Organisation (IKNL), IKNL, P.O. Box 19079, 3501 DB Utrecht, The Netherlands diagnosis of cancer, including those who have recovered from the disease [1], or in other words those who finished treatment Division of Human Nutrition and Health, Wageningen University, P.O. Box 17, 6700 AA Wageningen, The Netherlands and are disease-free, are encouraged to follow these recom- mendations to reduce risk of recurrence and improve survival. CoRPS-Center of Research on Psychology in Somatic diseases, Department of Medical and Clinical Psychology, Tilburg University, Colorectal cancer (CRC) survivors often suffer from long- PO Box 90153, 5000 LE Tilburg, The Netherlands term adverse health effects of cancer and its treatment [2]. This Department of Epidemiology, GROW – School for Oncology and can have a negative impact on health-related quality of life Developmental Biology, Maastricht University, P.O. Box 616, 6200 (HRQL). Two systematic reviews showed that CRC survivors MD Maastricht, The Netherlands 4566 Support Care Cancer (2019) 27:4565–4574 had a lower physical functioning and more fatigue and psy- Data collection chological problems, including depression, anxiety and dis- tress than the general population [3, 4]. Because of the increas- CRC patients were invited for participation via a letter from ing numbers of CRC survivors, investigating possibilities to their (former) attending physician. The letter included a link to increase HRQL is very important. a secure website, a login name and a password, so that inter- Several studies showed an association between adherence ested patients could provide consent and complete question- to general non-cancer-specific dietary guidelines, such as the naires online. Those who preferred written communication Healthy Eating Index or the Mediterranean diet, and higher could return a postcard after which they received our paper- levels of HRQL in cancer survivors, including CRC survivors and-pencil informed consent form and questionnaire. Non- [5–7]. In addition, previous studies have demonstrated that respondents were sent a reminder letter and paper-and-pencil CRC survivors who met the public health exercise guidelines questionnaire within 2 months. Patients were reassured that reported better quality of life (QL) and fatigue scores than nonparticipation had no consequences for their follow-up care CRC survivors who did not meet these guidelines [8, 9]. or treatment. The NCR provided information on cancer diag- Although adherence to general dietary or exercise guidelines nosis and cancer treatment history, such as year of diagnosis, showed positive associations with HRQL, the association be- stage and localization of cancer and having a stoma. tween adherence to the cancer-specific WCRF/AICR recom- mendations on diet, physical activity and body weight/ Study population composition and HRQL have only been investigated in female cancer survivors in general [10], in breast cancer survivors The CRC study started in December 2010 and respon- [11] and in a small cross-sectional study (N =145) in CRC dents received subsequent HRQL questionnaires in survivors [12]. These studies showed that better adherence December 2011, December 2012 and January 2014. In to the WCRF/AICR recommendations was associated with August 2013, data on the adherence to WCRF/AICR rec- better HRQL [10–12]. However, due to the relatively small ommendations were collected once. A complete overview numbers in these studies, it was not possible to evaluate which of the selection of patients can be found on our website specific recommendations had the highest impact among CRC under ‘data & documentation’; https://www.dataarchive. survivors (diet, physical activity or body composition). The profilesregistry.nl/study_units/view/22. In the current aim of the present study was to investigate the association paper, we present data on the adherence to WCRF/AICR between adherence to the WCRF/AICR recommendations recommendations and data regarding HRQL of the subse- and HRQL for all recommendations together and for physical quent measurement in January 2014. Patients with unver- activity, body composition and diet separately in a large cohort ifiable addresses, with cognitive impairment, who died of CRC survivors. prior to the start of the study or were terminally ill, with stage 0/carcinoma in situ and those already included in our 2009 CRC study or another study (n = 169), were Subjects and methods excluded [14]. One thousand six hundred twenty-five par- ticipants were invited for the data collection in August Study design 2013, see Fig. 1. Between August 2013 and January 2014, 78 (4.8%) participants died or discontinued partic- This study was part of an ongoing longitudinal study investi- ipation, resulting in 1547 survivors who were invited for gating HRQL in CRC patients. All CRC patients stage I–IV, the questionnaire on HRQL in January 2014. Figure 1 diagnosed between January 2000 and June 2009 from the gives an overview of the number of non-responders and southern area of the Netherlands, were sampled via the excluded patients. Of the 1625 CRC survivors who were Netherlands Cancer Registry (NCR). The Patient Reported invited in August 2013, 1096 were included in the present Outcomes Following Initial Treatment and Long-term study (67.4% of invited participants in August 2013) Evaluation of Survivorship (PROFILES) registry was used (Fig. 1). to collect the data [13]. Ethical approval for the study was obtained from the Health-related quality of life local certified Medical Ethics Committee of the Maxima Medical Centre Veldhoven, the Netherlands (approval The validated European Organization for Research and number 0822). All participants gave informed consent. Treatment of Cancer–Quality of Life Questionnaire (EORTC Data from this longitudinal study are (partly) available QLQ)-C30 was used to assess HRQL and fatigue [15, 16]. For online for non-commercial scientific research, subject to CRC patients, previous research concludes that a healthy life- study question, privacy and confidentiality restrictions, style is mainly associated with functioning scales (i.e. physi- and registration (www.profilesregistry.nl). cal, emotional, social, cognitive and role functioning) and 4567 Support Care Cancer (2019) 27:4565–4574 Fig. 1 Flowchart of the study population fatigue [5, 17]. Therefore, only functioning scales, fatigue and were scored on a 4-point Likert scale ranging from ‘not at all’ global health status were included in the analysis. All items to ‘very much’, except for the items regarding global health 4568 Support Care Cancer (2019) 27:4565–4574 status which were scored from 1 (very poor) to 7 (excellent). month. Results were converted to time spent in light, All scores were linearly transformed to a scale ranging from 0 moderate and vigorous activities, which were then con- to 100 points [15, 18]. Higher scores on functioning scales verted to activity scores [23]. When this total activity represent better functioning, while a higher score on the fa- score was 5 or more, representing the number of activities tigue scale corresponds to more fatigue. of at least 30 min per week, persons were categorised as Changes in scores were considered clinically relevant if the adherent to the physical activity recommendation. If one mean difference was 5–14 points for physical functioning, 5– of the recommendations was met, participants received 1 11 points for social functioning, 3–9 points for cognitive func- point for that recommendation. tioning, 6–19 points for role functioning and 5–13 point for When a recommendation was not met, 0 or 0.5 points were fatigue [19]. For emotional functioning no cut-offs were de- allotted according to the available cut-off values. The total fined [19]. score had a range of 0–8; a higher score means better adher- ence to the recommendations [20]. Adherence to the WCRF/AICR recommendations Adherence to the eight WCRF/AICR recommendations was Analysis and statistical methods determined, six recommendations about healthy diet, one about body fatness and one about physical activity. The scor- Responders were compared to non-responders. The CRC sur- ing of adherence to the WCRF/AICR recommendations is vivors were categorised into three groups, based on tertiles of described extensively by Winkels et al. [20] and Romaguera WCRF/AICR adherence scores following the sample distribu- et al. [21]. tion. Chi-square (categorical variables) and one-way ANOVA With regard to a healthy diet, in 2007, the WCRF/AICR (continuous variables) were used to test for differences in published the following recommendations: ‘foods and baseline characteristics. drinks that promote weight gain: avoid high-calorie foods To assess the association between WCRF adherence scores and sugary drinks’, ‘plant-based foods: eat more grains, and HRQL, linear regression models were used both for the vegetables, fruit and beans’, ‘animal foods: limit red meat tertiles and for the continuous adherence scores. The follow- and avoid processed meat’, ‘alcoholic drinks: for cancer ing variables were tested whether they changed the regression prevention, don’t drink alcohol’, ‘preservation, processing coefficient by at least 10% [24]: gender, age, comorbidities, & preparation: eat less salt and avoid mouldy grains & smoking status, years since diagnosis, tumour localization, cereals’ and ‘dietary supplement use: for cancer preven- tumour stage, having a stoma, chemotherapy and radiothera- tion, don’trelyonsupplements’. To assess adherence to py; and for the analyses of the individual components diet, the recommendations concerning healthy diet, the Dutch physical activity and BMI. Gender (male/female), age (con- Healthy Diet-Food Frequency Questionnaire (DHD-FFQ) tinuous), comorbidities (no comorbidities, 1 comorbidity, >2 was used [22]. The original DHD-FFQ consists of 34 comorbidities) and smoking (current, former, never) changed items. To compensate for items that were missing in the the regression coefficient ≥ 10% and were included in the mul- DHD-FFQ but are incorporated in the WCRF/AICR rec- tivariable model. For the analyses of the individual compo- ommendations, additional questions on intake of meat, nents, diet and BMI changed by > 10% when physical activity processed meat and sugary beverages were added to the was added to the model, therefore physical activity was added questionnaire, from now on called WCRF/DHD-FFQ. to the multivariable model. Dummy variables were created for The WCRF/DHD-FFQ consists of 40 items on intakes of WCRF/AICR adherence score tertiles, smoking status and bread, fruit, vegetable, potatoes, milk, cheese, meat prod- comorbidities. ucts, fish, cookies, pastries, crisps, soup, fats and oils, take- Functioning scales, global health status and fatigue were away food, pizza, sugary drinks, alcoholic beverages and also examined separately in relation to each of the three com- discretionary salt. ponents of the adherence score (BMI (normal weight, over- Adherence to the recommendation regarding body fatness weight and obese), physical activity (score 0/1) and diet (low was determined based on body mass index (BMI) by calcu- adherence (score < 3 points), moderate adherence (score 3–< lating weight (kg)/height (m) . Weight and height were self- 4 points) and high adherence (> 4 points)). To evaluate the reported. BMI was categorised as normal weight (18.5 < BMI effect of the separate components of adherence scores on the 2 2 < 25 kg/m ), overweight (25 > BMI < 30 kg/m ) or obesity functioning scales, global health status and fatigue beyond the (BMI > 30 kg/m ). effects of the other components, the analysis of each compo- Physical activity was assessed using the Short nent was adjusted for the other components. Questionnaire to Assess Health-Enhancing Physical A p value < 0.05 was regarded as statistically significant. Activity (SQUASH) which contains questions about mul- All analyses were conducted using the Statistical Package for tiple activities referring to a normal week in the past Social Sciences (SPSS) version 23.0 (IBM). 4569 Support Care Cancer (2019) 27:4565–4574 Results respondents to the included respondents, non-respondents and excluded respondents did not differ from respondents (data General characteristics of the study population not shown). The mean total WCRF/AICR adherence score was 4.81 ± Respondents of our study were most often male, > 65 years 1.04 of a total of 8 points (range 1.33–8.00). old, had two or more comorbidities, were former smokers, had Higher WCRF/AICR adherence scores were more com- a mean time since diagnosis of 8.1 years, had a colon tumour, mon among women compared to men. The highest WCRF/ stage II, and did not receive chemotherapy or radiotherapy AICR adherence scores were found among survivors who (Table 1). When comparing the non-respondents and excluded never smoked, among older participants and among Table 1 Sociodemographic and clinical characteristics for the three tertiles of WCRF/AICR adherence scores (N =1096) Total population Tertile 1 WCRF Tertile 2 WCRF Tertile 3 WCRF adherence score adherence score adherence score < 4.42 points 4.42–5.33 points >5.33 points N (%) N (%) N (%) N (%) N 1096 (100%) 360 (33%) 365 (33%) 371 (34%) Gender* Male 635 (58%) 227 (63%) 229 (63%) 179 (48%) Female 461 (42%) 133 (37%) 136 (37%) 192 (52%) Missing 0 0 0 0 Age* Mean age (years +SD) 70.8 +9.2 69.7 + 9.5 70.9 + 9.1 71.7 +8.9 < 65 years 264 (24%) 102 (28%) 89 (24%) 73 (20%) > 65 years 832 (76%) 258 (72%) 276 (76%) 298 (80%) Missing 0 0 0 0 Comorbidities 0 261 (24%) 76 (21%) 85 (23%) 100 (27%) 1 306 (28%) 96 (27%) 102 (28%) 108 (29%) > 2 495 (45%) 183 (51%) 163 (45%) 149 (40%) Missing 34 (3%) 5 (1%) 15 (4%) 14 (4%) Smoking* Current 85 (8%) 33 (9%) 26 (7%) 26 (7%) Former 667 (61%) 237 (66%) 224 (61%) 206 (56%) Never 322 (29%) 83 (23%) 106 (29%) 133 (36%) Missing 22 (2%) 7 (2%) 9 (3%) 6 (2%) Years since diagnosis Mean time since diagnosis (SD) 8.1 +2.8 8.1 +2.8 8.2 + 2.8 7.9 +2.8 < 5 years 116 (11%) 39 (11%) 32 (9%) 45 (12%) > 5 years 980 (89%) 321 (89%) 333 (30%) 326 (88%) Missing 0 0 0 0 Tumour localization Colon 634 (58%) 204 (57%) 211 (58%) 219 (59%) Rectum 462 (42%) 156 (43%) 154 (42%) 152 (41%) Missing 0 0 0 0 Tumour stage Stage I 348 (32%) 111 (31%) 112 (31%) 125 (34%) Stage II 372 (34%) 108 (30%) 129 (35%) 135 (37%) Stage III 318 (29%) 119 (33%) 101 (28%) 98 (26%) Stage IV 26 (2%) 10 (3%) 12 (3%) 4 (1%) Missing 31 (3%) 12 (3%) 11 (3%) 8 (2%) Stoma Yes 168 (15%) 58 (16%) 46 (13%) 64 (17%) No 928 (85%) 302 (84%) 319 (87%) 307 (83%) Missing 0 0 0 0 Chemotherapy* Yes 329 (30%) 128 (36%) 113 (31%) 88 (24%) No 767 (70%) 232 (64%) 252 (69%) 283 (76%) Missing 0 0 0 0 Radiotherapy Yes 370 (34%) 125 (35%) 119 (33%) 126 (34%) No 726 (66%) 235 (65%) 246 (67%) 245 (66%) Missing 0 0 0 0 *p <0.05 4570 Support Care Cancer (2019) 27:4565–4574 participants who did not receive chemotherapy (Table 1). smoked (emotional functioning and global health status). For Years since diagnosis, tumour localization and stage, having years since diagnosis, tumour localization, tumour stage, hav- a stoma, comorbidities and receiving radiotherapy, were even- ing a stoma, receiving chemotherapy and radiotherapy, no ly distributed among the tertiles of WCRF/AICR adherence significant differences in HRQL was found (data not shown). scores. Thirty-four percent of respondents adhered to the BMI recommendation: ‘maintain body weight within the normal Health-Related Quality of Life range from age 21; BMI 18.5 <25 kg/m , 75% adhered to the physical activity recommendation: ‘be moderately physi- Survivors with the highest WCRF/AICR adherence scores cally active, equivalent to brisk walking, for at least 30 min (tertile 3; > 5.25 points) had the highest mean physical func- every day’ and the mean dietary adherence score was 3.48 + tioning scores (84.8 + 17.2 vs. 78.3 + 21.3) and role function- 0.87 of a total of 6 points (range 0.5–6.0). Fifty-eight percent ing scores (86.5 + 21.7 vs. 78.3 + 27.7) and the lowest mean adhered to the recommendation ‘foods and drinks that pro- scores on fatigue (16.6 + 19.7 vs. 24.7 +23.7),compared to mote weight gain: avoid sugary drinks’ with adherence = no survivors with the lowest WCRF/AICR adherence scores sugary drinks, 10% adhered to ‘plant-based foods: at least five (tertile 1; < 4.42 points; see Fig. 2). Although small, these portions/servings (at least 400 g) of a variety of non- starchy differences are considered clinically relevant [19]. vegetables of fruits every day’ with adherence = a mean fruit Multivariable linear regression models (Table 2)showed and vegetable intake > 400 g/day and dietary fibre > 17 g/day, that compared to the lowest tertile (< 4.42 points), the second 8% to ‘meat products: people who eat red meat to consume (4.42–5.25 points) and the third tertile (> 5.25 points) of the less than 500 g/week, very little, if any, to be processed’ with WCRF/AICR adherence score were significantly associated adherence = red/processed meat < 500 g/week of which proc- with higher scores on physical, role and social functioning essed meat < 3 g/day, 73% to ‘alcoholic drinks: If alcoholic and a lower level of fatigue. The highest tertile of the adher- drinks are consumed, limit consumption to no more than two ence score was significantly associated with higher scores on drinks a day for men, and one drink a day for women’,12% to emotional functioning, cognitive functioning and global ‘preservation, processing & preparation: Limit consumption health status compared to the lowest tertile. For an increase of processed foods with added salt to ensure an intake of <6 g in the continuous score of adherence to the WCRF/AICR (2.4 g sodium) a day’ and 75% to the recommendation on recommendations, significant associations were found for bet- ‘dietary supplement use: Dietary supplements are not recom- ter physical functioning, role functioning, cognitive function- mended for cancer prevention’. ing, social functioning and global health status and less Higher HRQL scores were seen among men (physical, fatigue. role, emotional functioning and global health status), for Multivariable linear regression models showed that adher- younger participants (< 65 years old) (physical and emotional ence to the physical activity recommendation was associated functioning), CRC survivors without comorbid conditions with better physical, role, emotional and social functioning, (for physical, role, emotional, cognitive, social functioning better global health status and less fatigue (Table 3). Being and global health status and fatigue) and those who never overweight was not significantly associated with different Fig. 2 HRQL scores by WCRF/AICR adherence scores (N = 1096). A single asterisk denotes small clinically relevant difference between tertile 1 and tertile 3 4571 Support Care Cancer (2019) 27:4565–4574 Table 2 The association between overall WCRF/AICR adherence score and HRQL and fatigue using multivariable linear regression (N = 1096) HRQL WCRF adherence scores Tertile 1 Tertile 2 Tertile 3 Continuous <4.42 points 4.42–5.25 points >5.25 points Physical functioning REF 3.88 (4.42, 6.33)* 6.94 (4.46, 9.42)* 2.71 (1.73, 3.68)* Role functioning REF 4.76 (1.40, 8.12)* 7.49 (4.09, 10.89)* 2.87 (1.53, 4.21)* Emotional functioning REF 2.35 (− 0.06, 4.75) 3.34 (0.90, 5.77)* 0.85 (− 0.11, 1.81) Cognitive functioning REF 1.90 (− 0.77, 4.57) 3.48 (0.78, 6.17)* 1.25 (0.19, 2.32)* Social functioning REF 3.56 (0.67, 6.44)* 6.12 (3.21, 9.04)* 2.01 (0.85, 3.16)* Global health status/QL REF 1.68 (− 0.70, 4.07) 4.33 (1.92, 6.74)* 1.64 (0.69, 2.59)* fatigue REF − 3.87 (− 6.90, − 0.84)* − 7.65 (− 10.72, − 4.59)* − 2.81 (− 4.02, − 1.60)* Results are expressed as β (95% confidence interval (CI)). All models were adjusted for age, gender, comorbidities and smoking. An increase in functioning scores and global health status indicates an improvement in HRQL. A decrease in fatigue scores indicates an improvement in fatigue *p <0.05 HRQL and fatigue scores compared to participants with a et al. who found that higher adherence to the total set of healthy weight. However, being obese was significantly asso- WCRF/AICR recommendations was associated with better ciated with lower physical functioning compared to healthy physical functioning and less fatigue in a small group (N = 145) of CRC survivors in the Netherlands [12]. weight respondents. Adherence to the dietary recommenda- tions was not associated with the different functioning scales, Of all recommendations, physical activity was most strongly global health status or fatigue. associated with most functioning scales: physical, role, emotion- al and social functioning; global health status and fatigue in our study. When investigating the crude model, diet was associated Discussion with physical functioning. However, when we adjusted for physical activity, as discussed in the BSubjects and Methods^ Higher adherence to the WCRF/AICR recommendations was section, the association was no longer significant. This indicates that physical activity indeed was the main component of the associated with better physical functioning, role functioning, social functioning and global health status and less fatigue WCRF/AICR associated with a better HRQL and not diet. For fatigue, there is ample evidence that physical activity among CRC survivors. Physical activity seemed to be the main has a positive influence [25]. This is also in line with the US component of the WCRF/AICR recommendations contributing to the observed associations. Being obese was associated with National Comprehensive Cancer Network guidelines for man- aging fatigue [26]. Two observational studies recommended worse physical functioning. Diet was not associated with the different functioning scales, global health status and fatigue. that CRC survivors should meet the public health exercise guideline (> 150 min of moderate to strenuous intensity exer- Previous studies showed an association between higher ad- herence to the non-cancer-specific Healthy Eating Index or the cise or > 60 min of strenuous intensity exercise per week), since CRC survivors who meet these standards had a higher Mediterranean diet and higher levels of HRQL in cancer sur- vivors, including CRC survivors [5–7]. Our study did not show quality of life than other survivors who did not meet these exercise guidelines [8, 14]. However, to be able to be physi- an association between the specific dietary recommendations of the WCRF/AICR and HRQL, however when looking at the cally active, a healthy diet and body weight are important. This is supported by our finding that being obese was nega- total adherence WCRF/AICR recommendations score, an as- tively associated with physical functioning. Therefore, it re- sociation between level of adherence and HRQL was found in CRC survivors similar to the association with the Healthy mains important to focus on the triad of physical activity, diet and body weight when targeting CRC survivors, as was also Eating Index or the Mediterranean diet [5–7]. Our study only found an inverse association between being obese and physical suggested by Blanchard et al. [27]. The differences found in functioning scales when compar- functioning. Our findings are in line with the results of Inoue- Choi who showed that higher adherence to the WCRF/AICR ing respondents with the highest WCRF/AICR adherence scores (> 5.25) to those with the lowest scores (< 4.42) are recommendations, especially to the physical activity recom- mendations, was significantly associated with higher physical subtle but nevertheless clinically meaningful, meaning that these differences are noticeable in daily clinical practice [19]. and mental component summary scores (SF-36) in a popula- tion of female cancer survivors with different cancer types [10]. The present study was the first study investigating the asso- ciations between adherence to the cancer-specific Our results are also in line with the results of Breedveld-Peters 4572 Support Care Cancer (2019) 27:4565–4574 WCRF/AICR recommendations and HRQL, in a large group of male and female CRC survivors. Major strengths of our study are the large sample size that made it possible to investigate the association between diet, physical activity and body fatness on HRQL separately, and the registry-based character of the study. However, there are also some limitations. First, selection bias may limit the generalizability of our findings. The present study covers CRC stage I–IV, with a mean time since diagnosis of 8.1 years. Patients with a worse prognosis or worse health might be less likely to participate in the study, might have more problems to complete the follow-up questionnaires or might have already died. Although our included participants were older and more often former smokers than the excluded partic- ipants, our study population may consist of more healthy CRC survivors possibly with different associations between a healthy lifestyle and HRQL. Absolute HRQL scores of our CRC sur- vivors should be interpreted cautiously and are not generaliz- able for the whole population of CRC survivors. Second, data in our study were self-reported by survivors, which might have led to underreporting (body weight) and overreporting (physi- cal activity, consumption of vegetable and fruits) due to social desirable answers [28–31]. Self-reporting of nutritional intake may lead to differential misclassification: obese participants might underreport their intake more than non-obese participants and elderly might be more eager to present themselves in a favourable way, giving a social desirable answer, hence their higher WCRF/AICR scores 32. Also non-differential misclas- sification might have occurred, probably leading to higher WCRF/AICR adherence scores. However, only one respondent had a total score of 8 points and the percentage survivors ad- hering to specific recommendations e.g., more plant-based foods, less red meat was often low, demonstrating how hard it is for CRC survivors and for the general public to adhere to the WCRF/AICR recommendations. Third, 75% of respondents reported to meet the guidelines for physical activity. This might be an overestimation, due to the nature of measuring physical activity: by means of a questionnaire (SQUASH) and not by the use of activity trackers. Fourth, the scoring of fatigue and other functioning scales by use of the EORTC QLQ-C30 may not be the best way to determine HRQL, especially fatigue, so many years after treatment. However, the EORTC QLQ-C30 is the most common questionnaire to determine HRQL in cancer sur- vivors. Hence, it makes it easy to compare our results to the work of others. Finally, due to the study design, with 6 months be- tween the questionnaire on adherence to the WCRF rec- ommendations and the questionnaire on HRQL in a co- hort with a mean time since diagnosis of 8.1 years, we cannot draw conclusions whether the association between HRQL and adherence to the WCRF/AICR recommenda- tions reflects a causal relation or reverse causation which means that survivors who have a better HRQL easier ad- here to the WCRF/AICR recommendations. Table 3 The association between HRQL and fatigue and physical activity, diet and BMI using multivariable linear regression (N = 1096) Physical functioning Role functioning Emotional functioning Cognitive functioning Social functioning Global health status/QL Fatigue Physical activity 0 REF REF REF REF REF REF REF 1 10.30 (8.01; 12.59)* 10.50 (7.31; 13.67)* 2.75 (0.45; 5.06)* 2.49 (− 0.07; 5.04) 6.20 (3.45; 8.95)* 6.27 (4.02; 8.53)* − 7.43 (− 10.32; − 4.54)* Diet 0– < 3 REF REF REF REF REF REF REF 3– <4 0.42 (− 1.98; 2.82) 1.55 (− 1.79; 4.89) 1.05 (− 1.38; 3.47) 1.52 (− 1.53; 3.83) 1.64 (− 1.25; 4.54) 1.96 (− 0.41; 4.33) − 2.87 (− 5.91; 0.16) >4 0.09 (− 2.45; 2.64) 0.38 (− 3.17; 3.92) 0.39 (− 2.18; 2.96) 1.71 (− 1.14; 4.55) 0.70 (− 2.37; 3.77) 0.26 (− 2.25; 2.78) − 3.12 (− 6.34; 0.10) BMI Normal weight REF REF REF REF REF REF REF Overweight − 0.24 (− 2.46; 1.98) 0.29 (− 2.80; 3.37) 0.97 (− 1.27; 3.20) − 0.58 (− 3.06; 1.90) 0.22 (− 2.45; 2.89) 1.74 (− 0.45; 3.93) − 0.49 (− 3.23; 2.32) Obese − 4.15 (− 7.16; 1.73 (− 5.91; 2.46) − 0.92 (− 3.95; 2.11) − 2.80 (− 6.15; 0.55) − 1.93 (− 5.54; 1.69) − 0.29 (− 3.25; 2.67) 2.81 (− 0.98; 6.60) − 1.15)* Results are expressed as β (95% confidence interval (CI)). All models were adjusted for age, gender, comorbidities and smoking. An increase in functioning scores and global health status indicates an improvement in HRQL. A decrease in fatigue scores indicates an improvement in fatigue *p <0.05 4573 Support Care Cancer (2019) 27:4565–4574 Informed consent Informed consent was obtained from all individual Conclusion participants included in the study. Higher adherence to the WCRF/AICR recommendations was Data We have control over all primary data, we agree to allow the associated with better physical, role, cognitive and social journal to review our data if requested. functioning, better global health status and less fatigue among Open Access This article is distributed under the terms of the Creative CRC survivors. Physical activity seemed to be the main con- Commons Attribution 4.0 International License (http:// tributor to higher scores on most functioning scales and global creativecommons.org/licenses/by/4.0/), which permits unrestricted use, health status and lower scores on fatigue in CRC survivors. distribution, and reproduction in any medium, provided you give appro- priate credit to the original author(s) and the source, provide a link to the Because CRC survivors with the highest adherence to the Creative Commons license, and indicate if changes were made. WCRF/AICR recommendations also report the highest HRQL, we recommend to investigate whether increasing the adherence in CRC survivors indeed results in better HRQL. However, previous research as well as the present study has shown that it is very difficult to motivate cancer survivors to positively References change their lifestyle [12, 20]. Even Lynch syndrome carriers, 1. World Cancer Research Fund and American Institute for Cancer with a very high inherited risk of developing CRC [33], from Research (2007) Food, nutrition, physical activity, and the preven- whom we hoped that they would be extremely motivated to tion of cancer: a global perspective. AICR, Washington DC change their lifestyle, were shown to adhere to those recom- 2. Miller KD, Siegel RL, Lin CC, Mariotto AB, Kramer JL, Rowland mendations only in a slightly better manner than CRC survi- JH, Stein KD, Alteri R, Jemal A (2016) Cancer treatment and sur- vors without Lynch syndrome. Adhering to the WCRF/AICR vivorship statistics, 2016. CA Cancer J Clin 66(4):271–289 3. Marventano S, Forjaz M, Grosso G, Mistretta A, Giorgianni G, recommendations can be challenging for CRC survivors. Thus, Platania A, Gangi S, Basile F, Biondi A (2013) Health related qual- trials aiming to increase adherence should not only focus on the ity of life in colorectal cancer patients: state of the art. BMC Surg effects better adherence has on cancer outcomes but also on 13(2):S15 tools to stimulate and motivate CRC survivors to follow the 4. Jansen L, Koch L, Brenner H, Arndt V (2010) Quality of life among recommendations to the best of their abilities. long-term (⩾ 5 years) colorectal cancer survivors–systematic re- view. Eur J Cancer 46(16):2879–2888 5. Schlesinger S, Walter J, Hampe J, von Schönfels W, Hinz S, Acknowledgements The authors thank the registration teams of the Küchler T, Jacobs G, Schafmayer C, Nöthlings U (2014) Netherlands Comprehensive Cancer Organisation for the collection of Lifestyle factors and health-related quality of life in colorectal can- data for the Netherlands Cancer Registry and members of the cer survivors. Cancer Causes Control 25(1):99–110 PROFILES registry for distribution and handling of the questionnaires. 6. Sánchez PH et al (2012) Adherence to the Mediterranean diet and We are very grateful for the participation of all patients and their doctors quality of life in the SUN Project. Eur J Clin Nutr 66(3):360–368 in the study. Special thanks go to Dr. M. van Bommel, who was willing to 7. Mosher CE, Sloane R, Morey MC, Snyder DC, Cohen HJ, Miller function as an independent advisor and to answer questions of patients. PE, Demark-Wahnefried W (2009) Associations between lifestyle We also want to thank the following hospitals for their cooperation: factors and quality of life among older long-term breast, prostate, Amphia hospital, Breda; Bernhoven Hospital, Uden; Catharina hospital, and colorectal cancer survivors. Cancer 115(17):4001–4009 Eindhoven; Elisabeth-TweeSteden hospital, Tilburg and Waalwijk; Elkerliek Hospital, Helmond; Jeroen Bosch hospital, ‘s Hertogenbosch; 8. Peddle CJ, Au H-J, Courneya KS (2008) Associations between Maxima Medical Centre, Eindhoven and Veldhoven; Sint Anna hospital, exercise, quality of life, and fatigue in colorectal cancer survivors. Geldrop; VieCury hospital, Venlo and Venray. Dis Colon Rectum 51(8):1242–1248 9. Courneya K et al (2003) A randomized trial of exercise and quality of life in colorectal cancer survivors. Eur J Cancer Care 12(4):347– Funding The present study was supported by a grant from the Alpe d’HuZes Foundation within the research programme ‘Leven met kanker’ of the Dutch Cancer Society (grant no. UM-2012-5653). In addition, the 10. Inoue-Choi M, Lazovich D, Prizment AE, Robien K (2013) present study was supported by a VENI grant (#451-10-041) from the Adherence to the World Cancer Research Fund/American Netherlands Organization for Scientific Research awarded to FM. MV is Institute for Cancer Research recommendations for cancer preven- supported by a grant from Alpe d’HuZes/Dutch Cancer Society, in the tion is associated with better health-related quality of life among project ‘A taskforce on nutrition and cancer’ (IKZ 2012-5426) and MJB elderly female cancer survivors. J Clin Oncol 31(14):1758–1766 is supported by a grant from Kankeronderzoekfonds Limburg as part of 11. Lei Y-Y, Ho SC, Cheng A, Kwok C, Lee CKI, Cheung KL, Lee R, Health Foundation Limburg (grant no. 00005739). Loong HHF, He YQ, Yeo W (2018) Adherence to the World Cancer Research Fund/American Institute for Cancer Research Guideline is associated with better health-related quality of life among Chinese Compliance with ethical standards patients with breast cancer. J Natl Compr Cancer Netw 16(3):275– Conflict of interest The authors declare that they have no conflict of 12. Breedveld-Peters, J.J., et al., Colorectal cancers survivors’ adher- interest. ence to lifestyle recommendations and cross-sectional associations with health-related quality of life. Br J Nutr, 2018: p. 1–10 Research involving human participants Ethical approval for the study 13. van de Poll-Franse LV et al (2011) The Patient Reported Outcomes was obtained from the local certified Medical Ethics Committee of the Following Initial treatment and Long term Evaluation of Maxima Medical Centre Veldhoven, the Netherlands (approval number 0822). Survivorship registry: scope, rationale and design of an 4574 Support Care Cancer (2019) 27:4565–4574 infrastructure for the study of physical and psychosocial outcomes 22. van Lee L et al (2012) The Dutch Healthy Diet index (DHD-index): an instrument to measure adherence to the Dutch Guidelines for a in cancer survivorship cohorts. Eur J Cancer 47(14):2188–2194 Healthy Diet. Nutr J 11(1):49 14. 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Adherence to the World Cancer Research Fund/American Institute for Cancer Research recommendations for cancer prevention is associated with better health–related quality of life among long-term colorectal cancer survivors: results of the PROFILES registry

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Springer Journals
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Copyright © 2019 by The Author(s)
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Medicine & Public Health; Oncology; Nursing; Nursing Research; Pain Medicine; Rehabilitation Medicine
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0941-4355
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1433-7339
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10.1007/s00520-019-04735-y
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Abstract

Since colorectal cancer (CRC) survivors often suffer from long-term adverse health effects of the cancer and its treatment, having a negative impact on their health-related quality of life (HRQL), this study focuses on the association between adherence to WCRF/AICR recommendations and HRQL among CRC survivors. In a cross-sectional PROFILES registry study in 1096 CRC survivors (mean time since diagnosis 8.1 years), WCRF/AICR adherence scores (range 0–8, with a higher score for better adherence) were calculated, and HRQL was assessed using the EORTC QLQ-C30. Associations between adherence scores and HRQL scores were investigated using linear regression analyses. Additionally, associations with adherence to guidelines for body mass index (BMI) (normal weight, overweight and obese), physical activity (PA) (score 0/1) and diet (score < 3, 3– <4 and > 4) were evaluated separately. Mean adherence score was 4.81 ± 1.04. Higher WCRF/AICR scores were associated with better global health status (β 1.64; 95%CI 0.69/2.59), physical functioning (β 2.71; 95%CI 1.73/3.68), role functioning (β 2.87; 95%CI 1.53/4.21), cognitive functioning (β 1.25; 95%CI 0.19/2.32), social functioning (β 2.01; 95%CI 0.85/3.16) and fatigue (β − 2.81; 95%CI − 4.02/− 1.60). Adherence versus non-adherence PA was significantly associated with better physical, role, emotional and social functioning, global health status and less fatigue. Except for the association between being obese and physical functioning (β − 4.15; 95%CI − 47.16/− 1.15), no statistically significant associations with physical functioning were observed comparing adherence to non-adherence to BMI and dietary recommendations. Better adherence to the WCRF/AICR recommendations was positively associated with global health status, most functioning scales and less fatigue among CRC survivors. PA seemed to be the main contributor. . . . . . Keywords Colorectal cancer survivors Health-related quality of life WCRF guidelines Dietary guidelines Physical activity Body composition Introduction * Merel R. van Veen merelrvanveen@gmail.com In 2007, the World Cancer Research Fund/American Institute for Cancer Research (WCRF/AICR) launched the diet and 1 physical activity recommendations for cancer prevention [1]. Department of Research & Development, Netherlands Cancer survivors, defined as people who are living with a Comprehensive Cancer Organisation (IKNL), IKNL, P.O. Box 19079, 3501 DB Utrecht, The Netherlands diagnosis of cancer, including those who have recovered from the disease [1], or in other words those who finished treatment Division of Human Nutrition and Health, Wageningen University, P.O. Box 17, 6700 AA Wageningen, The Netherlands and are disease-free, are encouraged to follow these recom- mendations to reduce risk of recurrence and improve survival. CoRPS-Center of Research on Psychology in Somatic diseases, Department of Medical and Clinical Psychology, Tilburg University, Colorectal cancer (CRC) survivors often suffer from long- PO Box 90153, 5000 LE Tilburg, The Netherlands term adverse health effects of cancer and its treatment [2]. This Department of Epidemiology, GROW – School for Oncology and can have a negative impact on health-related quality of life Developmental Biology, Maastricht University, P.O. Box 616, 6200 (HRQL). Two systematic reviews showed that CRC survivors MD Maastricht, The Netherlands 4566 Support Care Cancer (2019) 27:4565–4574 had a lower physical functioning and more fatigue and psy- Data collection chological problems, including depression, anxiety and dis- tress than the general population [3, 4]. Because of the increas- CRC patients were invited for participation via a letter from ing numbers of CRC survivors, investigating possibilities to their (former) attending physician. The letter included a link to increase HRQL is very important. a secure website, a login name and a password, so that inter- Several studies showed an association between adherence ested patients could provide consent and complete question- to general non-cancer-specific dietary guidelines, such as the naires online. Those who preferred written communication Healthy Eating Index or the Mediterranean diet, and higher could return a postcard after which they received our paper- levels of HRQL in cancer survivors, including CRC survivors and-pencil informed consent form and questionnaire. Non- [5–7]. In addition, previous studies have demonstrated that respondents were sent a reminder letter and paper-and-pencil CRC survivors who met the public health exercise guidelines questionnaire within 2 months. Patients were reassured that reported better quality of life (QL) and fatigue scores than nonparticipation had no consequences for their follow-up care CRC survivors who did not meet these guidelines [8, 9]. or treatment. The NCR provided information on cancer diag- Although adherence to general dietary or exercise guidelines nosis and cancer treatment history, such as year of diagnosis, showed positive associations with HRQL, the association be- stage and localization of cancer and having a stoma. tween adherence to the cancer-specific WCRF/AICR recom- mendations on diet, physical activity and body weight/ Study population composition and HRQL have only been investigated in female cancer survivors in general [10], in breast cancer survivors The CRC study started in December 2010 and respon- [11] and in a small cross-sectional study (N =145) in CRC dents received subsequent HRQL questionnaires in survivors [12]. These studies showed that better adherence December 2011, December 2012 and January 2014. In to the WCRF/AICR recommendations was associated with August 2013, data on the adherence to WCRF/AICR rec- better HRQL [10–12]. However, due to the relatively small ommendations were collected once. A complete overview numbers in these studies, it was not possible to evaluate which of the selection of patients can be found on our website specific recommendations had the highest impact among CRC under ‘data & documentation’; https://www.dataarchive. survivors (diet, physical activity or body composition). The profilesregistry.nl/study_units/view/22. In the current aim of the present study was to investigate the association paper, we present data on the adherence to WCRF/AICR between adherence to the WCRF/AICR recommendations recommendations and data regarding HRQL of the subse- and HRQL for all recommendations together and for physical quent measurement in January 2014. Patients with unver- activity, body composition and diet separately in a large cohort ifiable addresses, with cognitive impairment, who died of CRC survivors. prior to the start of the study or were terminally ill, with stage 0/carcinoma in situ and those already included in our 2009 CRC study or another study (n = 169), were Subjects and methods excluded [14]. One thousand six hundred twenty-five par- ticipants were invited for the data collection in August Study design 2013, see Fig. 1. Between August 2013 and January 2014, 78 (4.8%) participants died or discontinued partic- This study was part of an ongoing longitudinal study investi- ipation, resulting in 1547 survivors who were invited for gating HRQL in CRC patients. All CRC patients stage I–IV, the questionnaire on HRQL in January 2014. Figure 1 diagnosed between January 2000 and June 2009 from the gives an overview of the number of non-responders and southern area of the Netherlands, were sampled via the excluded patients. Of the 1625 CRC survivors who were Netherlands Cancer Registry (NCR). The Patient Reported invited in August 2013, 1096 were included in the present Outcomes Following Initial Treatment and Long-term study (67.4% of invited participants in August 2013) Evaluation of Survivorship (PROFILES) registry was used (Fig. 1). to collect the data [13]. Ethical approval for the study was obtained from the Health-related quality of life local certified Medical Ethics Committee of the Maxima Medical Centre Veldhoven, the Netherlands (approval The validated European Organization for Research and number 0822). All participants gave informed consent. Treatment of Cancer–Quality of Life Questionnaire (EORTC Data from this longitudinal study are (partly) available QLQ)-C30 was used to assess HRQL and fatigue [15, 16]. For online for non-commercial scientific research, subject to CRC patients, previous research concludes that a healthy life- study question, privacy and confidentiality restrictions, style is mainly associated with functioning scales (i.e. physi- and registration (www.profilesregistry.nl). cal, emotional, social, cognitive and role functioning) and 4567 Support Care Cancer (2019) 27:4565–4574 Fig. 1 Flowchart of the study population fatigue [5, 17]. Therefore, only functioning scales, fatigue and were scored on a 4-point Likert scale ranging from ‘not at all’ global health status were included in the analysis. All items to ‘very much’, except for the items regarding global health 4568 Support Care Cancer (2019) 27:4565–4574 status which were scored from 1 (very poor) to 7 (excellent). month. Results were converted to time spent in light, All scores were linearly transformed to a scale ranging from 0 moderate and vigorous activities, which were then con- to 100 points [15, 18]. Higher scores on functioning scales verted to activity scores [23]. When this total activity represent better functioning, while a higher score on the fa- score was 5 or more, representing the number of activities tigue scale corresponds to more fatigue. of at least 30 min per week, persons were categorised as Changes in scores were considered clinically relevant if the adherent to the physical activity recommendation. If one mean difference was 5–14 points for physical functioning, 5– of the recommendations was met, participants received 1 11 points for social functioning, 3–9 points for cognitive func- point for that recommendation. tioning, 6–19 points for role functioning and 5–13 point for When a recommendation was not met, 0 or 0.5 points were fatigue [19]. For emotional functioning no cut-offs were de- allotted according to the available cut-off values. The total fined [19]. score had a range of 0–8; a higher score means better adher- ence to the recommendations [20]. Adherence to the WCRF/AICR recommendations Adherence to the eight WCRF/AICR recommendations was Analysis and statistical methods determined, six recommendations about healthy diet, one about body fatness and one about physical activity. The scor- Responders were compared to non-responders. The CRC sur- ing of adherence to the WCRF/AICR recommendations is vivors were categorised into three groups, based on tertiles of described extensively by Winkels et al. [20] and Romaguera WCRF/AICR adherence scores following the sample distribu- et al. [21]. tion. Chi-square (categorical variables) and one-way ANOVA With regard to a healthy diet, in 2007, the WCRF/AICR (continuous variables) were used to test for differences in published the following recommendations: ‘foods and baseline characteristics. drinks that promote weight gain: avoid high-calorie foods To assess the association between WCRF adherence scores and sugary drinks’, ‘plant-based foods: eat more grains, and HRQL, linear regression models were used both for the vegetables, fruit and beans’, ‘animal foods: limit red meat tertiles and for the continuous adherence scores. The follow- and avoid processed meat’, ‘alcoholic drinks: for cancer ing variables were tested whether they changed the regression prevention, don’t drink alcohol’, ‘preservation, processing coefficient by at least 10% [24]: gender, age, comorbidities, & preparation: eat less salt and avoid mouldy grains & smoking status, years since diagnosis, tumour localization, cereals’ and ‘dietary supplement use: for cancer preven- tumour stage, having a stoma, chemotherapy and radiothera- tion, don’trelyonsupplements’. To assess adherence to py; and for the analyses of the individual components diet, the recommendations concerning healthy diet, the Dutch physical activity and BMI. Gender (male/female), age (con- Healthy Diet-Food Frequency Questionnaire (DHD-FFQ) tinuous), comorbidities (no comorbidities, 1 comorbidity, >2 was used [22]. The original DHD-FFQ consists of 34 comorbidities) and smoking (current, former, never) changed items. To compensate for items that were missing in the the regression coefficient ≥ 10% and were included in the mul- DHD-FFQ but are incorporated in the WCRF/AICR rec- tivariable model. For the analyses of the individual compo- ommendations, additional questions on intake of meat, nents, diet and BMI changed by > 10% when physical activity processed meat and sugary beverages were added to the was added to the model, therefore physical activity was added questionnaire, from now on called WCRF/DHD-FFQ. to the multivariable model. Dummy variables were created for The WCRF/DHD-FFQ consists of 40 items on intakes of WCRF/AICR adherence score tertiles, smoking status and bread, fruit, vegetable, potatoes, milk, cheese, meat prod- comorbidities. ucts, fish, cookies, pastries, crisps, soup, fats and oils, take- Functioning scales, global health status and fatigue were away food, pizza, sugary drinks, alcoholic beverages and also examined separately in relation to each of the three com- discretionary salt. ponents of the adherence score (BMI (normal weight, over- Adherence to the recommendation regarding body fatness weight and obese), physical activity (score 0/1) and diet (low was determined based on body mass index (BMI) by calcu- adherence (score < 3 points), moderate adherence (score 3–< lating weight (kg)/height (m) . Weight and height were self- 4 points) and high adherence (> 4 points)). To evaluate the reported. BMI was categorised as normal weight (18.5 < BMI effect of the separate components of adherence scores on the 2 2 < 25 kg/m ), overweight (25 > BMI < 30 kg/m ) or obesity functioning scales, global health status and fatigue beyond the (BMI > 30 kg/m ). effects of the other components, the analysis of each compo- Physical activity was assessed using the Short nent was adjusted for the other components. Questionnaire to Assess Health-Enhancing Physical A p value < 0.05 was regarded as statistically significant. Activity (SQUASH) which contains questions about mul- All analyses were conducted using the Statistical Package for tiple activities referring to a normal week in the past Social Sciences (SPSS) version 23.0 (IBM). 4569 Support Care Cancer (2019) 27:4565–4574 Results respondents to the included respondents, non-respondents and excluded respondents did not differ from respondents (data General characteristics of the study population not shown). The mean total WCRF/AICR adherence score was 4.81 ± Respondents of our study were most often male, > 65 years 1.04 of a total of 8 points (range 1.33–8.00). old, had two or more comorbidities, were former smokers, had Higher WCRF/AICR adherence scores were more com- a mean time since diagnosis of 8.1 years, had a colon tumour, mon among women compared to men. The highest WCRF/ stage II, and did not receive chemotherapy or radiotherapy AICR adherence scores were found among survivors who (Table 1). When comparing the non-respondents and excluded never smoked, among older participants and among Table 1 Sociodemographic and clinical characteristics for the three tertiles of WCRF/AICR adherence scores (N =1096) Total population Tertile 1 WCRF Tertile 2 WCRF Tertile 3 WCRF adherence score adherence score adherence score < 4.42 points 4.42–5.33 points >5.33 points N (%) N (%) N (%) N (%) N 1096 (100%) 360 (33%) 365 (33%) 371 (34%) Gender* Male 635 (58%) 227 (63%) 229 (63%) 179 (48%) Female 461 (42%) 133 (37%) 136 (37%) 192 (52%) Missing 0 0 0 0 Age* Mean age (years +SD) 70.8 +9.2 69.7 + 9.5 70.9 + 9.1 71.7 +8.9 < 65 years 264 (24%) 102 (28%) 89 (24%) 73 (20%) > 65 years 832 (76%) 258 (72%) 276 (76%) 298 (80%) Missing 0 0 0 0 Comorbidities 0 261 (24%) 76 (21%) 85 (23%) 100 (27%) 1 306 (28%) 96 (27%) 102 (28%) 108 (29%) > 2 495 (45%) 183 (51%) 163 (45%) 149 (40%) Missing 34 (3%) 5 (1%) 15 (4%) 14 (4%) Smoking* Current 85 (8%) 33 (9%) 26 (7%) 26 (7%) Former 667 (61%) 237 (66%) 224 (61%) 206 (56%) Never 322 (29%) 83 (23%) 106 (29%) 133 (36%) Missing 22 (2%) 7 (2%) 9 (3%) 6 (2%) Years since diagnosis Mean time since diagnosis (SD) 8.1 +2.8 8.1 +2.8 8.2 + 2.8 7.9 +2.8 < 5 years 116 (11%) 39 (11%) 32 (9%) 45 (12%) > 5 years 980 (89%) 321 (89%) 333 (30%) 326 (88%) Missing 0 0 0 0 Tumour localization Colon 634 (58%) 204 (57%) 211 (58%) 219 (59%) Rectum 462 (42%) 156 (43%) 154 (42%) 152 (41%) Missing 0 0 0 0 Tumour stage Stage I 348 (32%) 111 (31%) 112 (31%) 125 (34%) Stage II 372 (34%) 108 (30%) 129 (35%) 135 (37%) Stage III 318 (29%) 119 (33%) 101 (28%) 98 (26%) Stage IV 26 (2%) 10 (3%) 12 (3%) 4 (1%) Missing 31 (3%) 12 (3%) 11 (3%) 8 (2%) Stoma Yes 168 (15%) 58 (16%) 46 (13%) 64 (17%) No 928 (85%) 302 (84%) 319 (87%) 307 (83%) Missing 0 0 0 0 Chemotherapy* Yes 329 (30%) 128 (36%) 113 (31%) 88 (24%) No 767 (70%) 232 (64%) 252 (69%) 283 (76%) Missing 0 0 0 0 Radiotherapy Yes 370 (34%) 125 (35%) 119 (33%) 126 (34%) No 726 (66%) 235 (65%) 246 (67%) 245 (66%) Missing 0 0 0 0 *p <0.05 4570 Support Care Cancer (2019) 27:4565–4574 participants who did not receive chemotherapy (Table 1). smoked (emotional functioning and global health status). For Years since diagnosis, tumour localization and stage, having years since diagnosis, tumour localization, tumour stage, hav- a stoma, comorbidities and receiving radiotherapy, were even- ing a stoma, receiving chemotherapy and radiotherapy, no ly distributed among the tertiles of WCRF/AICR adherence significant differences in HRQL was found (data not shown). scores. Thirty-four percent of respondents adhered to the BMI recommendation: ‘maintain body weight within the normal Health-Related Quality of Life range from age 21; BMI 18.5 <25 kg/m , 75% adhered to the physical activity recommendation: ‘be moderately physi- Survivors with the highest WCRF/AICR adherence scores cally active, equivalent to brisk walking, for at least 30 min (tertile 3; > 5.25 points) had the highest mean physical func- every day’ and the mean dietary adherence score was 3.48 + tioning scores (84.8 + 17.2 vs. 78.3 + 21.3) and role function- 0.87 of a total of 6 points (range 0.5–6.0). Fifty-eight percent ing scores (86.5 + 21.7 vs. 78.3 + 27.7) and the lowest mean adhered to the recommendation ‘foods and drinks that pro- scores on fatigue (16.6 + 19.7 vs. 24.7 +23.7),compared to mote weight gain: avoid sugary drinks’ with adherence = no survivors with the lowest WCRF/AICR adherence scores sugary drinks, 10% adhered to ‘plant-based foods: at least five (tertile 1; < 4.42 points; see Fig. 2). Although small, these portions/servings (at least 400 g) of a variety of non- starchy differences are considered clinically relevant [19]. vegetables of fruits every day’ with adherence = a mean fruit Multivariable linear regression models (Table 2)showed and vegetable intake > 400 g/day and dietary fibre > 17 g/day, that compared to the lowest tertile (< 4.42 points), the second 8% to ‘meat products: people who eat red meat to consume (4.42–5.25 points) and the third tertile (> 5.25 points) of the less than 500 g/week, very little, if any, to be processed’ with WCRF/AICR adherence score were significantly associated adherence = red/processed meat < 500 g/week of which proc- with higher scores on physical, role and social functioning essed meat < 3 g/day, 73% to ‘alcoholic drinks: If alcoholic and a lower level of fatigue. The highest tertile of the adher- drinks are consumed, limit consumption to no more than two ence score was significantly associated with higher scores on drinks a day for men, and one drink a day for women’,12% to emotional functioning, cognitive functioning and global ‘preservation, processing & preparation: Limit consumption health status compared to the lowest tertile. For an increase of processed foods with added salt to ensure an intake of <6 g in the continuous score of adherence to the WCRF/AICR (2.4 g sodium) a day’ and 75% to the recommendation on recommendations, significant associations were found for bet- ‘dietary supplement use: Dietary supplements are not recom- ter physical functioning, role functioning, cognitive function- mended for cancer prevention’. ing, social functioning and global health status and less Higher HRQL scores were seen among men (physical, fatigue. role, emotional functioning and global health status), for Multivariable linear regression models showed that adher- younger participants (< 65 years old) (physical and emotional ence to the physical activity recommendation was associated functioning), CRC survivors without comorbid conditions with better physical, role, emotional and social functioning, (for physical, role, emotional, cognitive, social functioning better global health status and less fatigue (Table 3). Being and global health status and fatigue) and those who never overweight was not significantly associated with different Fig. 2 HRQL scores by WCRF/AICR adherence scores (N = 1096). A single asterisk denotes small clinically relevant difference between tertile 1 and tertile 3 4571 Support Care Cancer (2019) 27:4565–4574 Table 2 The association between overall WCRF/AICR adherence score and HRQL and fatigue using multivariable linear regression (N = 1096) HRQL WCRF adherence scores Tertile 1 Tertile 2 Tertile 3 Continuous <4.42 points 4.42–5.25 points >5.25 points Physical functioning REF 3.88 (4.42, 6.33)* 6.94 (4.46, 9.42)* 2.71 (1.73, 3.68)* Role functioning REF 4.76 (1.40, 8.12)* 7.49 (4.09, 10.89)* 2.87 (1.53, 4.21)* Emotional functioning REF 2.35 (− 0.06, 4.75) 3.34 (0.90, 5.77)* 0.85 (− 0.11, 1.81) Cognitive functioning REF 1.90 (− 0.77, 4.57) 3.48 (0.78, 6.17)* 1.25 (0.19, 2.32)* Social functioning REF 3.56 (0.67, 6.44)* 6.12 (3.21, 9.04)* 2.01 (0.85, 3.16)* Global health status/QL REF 1.68 (− 0.70, 4.07) 4.33 (1.92, 6.74)* 1.64 (0.69, 2.59)* fatigue REF − 3.87 (− 6.90, − 0.84)* − 7.65 (− 10.72, − 4.59)* − 2.81 (− 4.02, − 1.60)* Results are expressed as β (95% confidence interval (CI)). All models were adjusted for age, gender, comorbidities and smoking. An increase in functioning scores and global health status indicates an improvement in HRQL. A decrease in fatigue scores indicates an improvement in fatigue *p <0.05 HRQL and fatigue scores compared to participants with a et al. who found that higher adherence to the total set of healthy weight. However, being obese was significantly asso- WCRF/AICR recommendations was associated with better ciated with lower physical functioning compared to healthy physical functioning and less fatigue in a small group (N = 145) of CRC survivors in the Netherlands [12]. weight respondents. Adherence to the dietary recommenda- tions was not associated with the different functioning scales, Of all recommendations, physical activity was most strongly global health status or fatigue. associated with most functioning scales: physical, role, emotion- al and social functioning; global health status and fatigue in our study. When investigating the crude model, diet was associated Discussion with physical functioning. However, when we adjusted for physical activity, as discussed in the BSubjects and Methods^ Higher adherence to the WCRF/AICR recommendations was section, the association was no longer significant. This indicates that physical activity indeed was the main component of the associated with better physical functioning, role functioning, social functioning and global health status and less fatigue WCRF/AICR associated with a better HRQL and not diet. For fatigue, there is ample evidence that physical activity among CRC survivors. Physical activity seemed to be the main has a positive influence [25]. This is also in line with the US component of the WCRF/AICR recommendations contributing to the observed associations. Being obese was associated with National Comprehensive Cancer Network guidelines for man- aging fatigue [26]. Two observational studies recommended worse physical functioning. Diet was not associated with the different functioning scales, global health status and fatigue. that CRC survivors should meet the public health exercise guideline (> 150 min of moderate to strenuous intensity exer- Previous studies showed an association between higher ad- herence to the non-cancer-specific Healthy Eating Index or the cise or > 60 min of strenuous intensity exercise per week), since CRC survivors who meet these standards had a higher Mediterranean diet and higher levels of HRQL in cancer sur- vivors, including CRC survivors [5–7]. Our study did not show quality of life than other survivors who did not meet these exercise guidelines [8, 14]. However, to be able to be physi- an association between the specific dietary recommendations of the WCRF/AICR and HRQL, however when looking at the cally active, a healthy diet and body weight are important. This is supported by our finding that being obese was nega- total adherence WCRF/AICR recommendations score, an as- tively associated with physical functioning. Therefore, it re- sociation between level of adherence and HRQL was found in CRC survivors similar to the association with the Healthy mains important to focus on the triad of physical activity, diet and body weight when targeting CRC survivors, as was also Eating Index or the Mediterranean diet [5–7]. Our study only found an inverse association between being obese and physical suggested by Blanchard et al. [27]. The differences found in functioning scales when compar- functioning. Our findings are in line with the results of Inoue- Choi who showed that higher adherence to the WCRF/AICR ing respondents with the highest WCRF/AICR adherence scores (> 5.25) to those with the lowest scores (< 4.42) are recommendations, especially to the physical activity recom- mendations, was significantly associated with higher physical subtle but nevertheless clinically meaningful, meaning that these differences are noticeable in daily clinical practice [19]. and mental component summary scores (SF-36) in a popula- tion of female cancer survivors with different cancer types [10]. The present study was the first study investigating the asso- ciations between adherence to the cancer-specific Our results are also in line with the results of Breedveld-Peters 4572 Support Care Cancer (2019) 27:4565–4574 WCRF/AICR recommendations and HRQL, in a large group of male and female CRC survivors. Major strengths of our study are the large sample size that made it possible to investigate the association between diet, physical activity and body fatness on HRQL separately, and the registry-based character of the study. However, there are also some limitations. First, selection bias may limit the generalizability of our findings. The present study covers CRC stage I–IV, with a mean time since diagnosis of 8.1 years. Patients with a worse prognosis or worse health might be less likely to participate in the study, might have more problems to complete the follow-up questionnaires or might have already died. Although our included participants were older and more often former smokers than the excluded partic- ipants, our study population may consist of more healthy CRC survivors possibly with different associations between a healthy lifestyle and HRQL. Absolute HRQL scores of our CRC sur- vivors should be interpreted cautiously and are not generaliz- able for the whole population of CRC survivors. Second, data in our study were self-reported by survivors, which might have led to underreporting (body weight) and overreporting (physi- cal activity, consumption of vegetable and fruits) due to social desirable answers [28–31]. Self-reporting of nutritional intake may lead to differential misclassification: obese participants might underreport their intake more than non-obese participants and elderly might be more eager to present themselves in a favourable way, giving a social desirable answer, hence their higher WCRF/AICR scores 32. Also non-differential misclas- sification might have occurred, probably leading to higher WCRF/AICR adherence scores. However, only one respondent had a total score of 8 points and the percentage survivors ad- hering to specific recommendations e.g., more plant-based foods, less red meat was often low, demonstrating how hard it is for CRC survivors and for the general public to adhere to the WCRF/AICR recommendations. Third, 75% of respondents reported to meet the guidelines for physical activity. This might be an overestimation, due to the nature of measuring physical activity: by means of a questionnaire (SQUASH) and not by the use of activity trackers. Fourth, the scoring of fatigue and other functioning scales by use of the EORTC QLQ-C30 may not be the best way to determine HRQL, especially fatigue, so many years after treatment. However, the EORTC QLQ-C30 is the most common questionnaire to determine HRQL in cancer sur- vivors. Hence, it makes it easy to compare our results to the work of others. Finally, due to the study design, with 6 months be- tween the questionnaire on adherence to the WCRF rec- ommendations and the questionnaire on HRQL in a co- hort with a mean time since diagnosis of 8.1 years, we cannot draw conclusions whether the association between HRQL and adherence to the WCRF/AICR recommenda- tions reflects a causal relation or reverse causation which means that survivors who have a better HRQL easier ad- here to the WCRF/AICR recommendations. Table 3 The association between HRQL and fatigue and physical activity, diet and BMI using multivariable linear regression (N = 1096) Physical functioning Role functioning Emotional functioning Cognitive functioning Social functioning Global health status/QL Fatigue Physical activity 0 REF REF REF REF REF REF REF 1 10.30 (8.01; 12.59)* 10.50 (7.31; 13.67)* 2.75 (0.45; 5.06)* 2.49 (− 0.07; 5.04) 6.20 (3.45; 8.95)* 6.27 (4.02; 8.53)* − 7.43 (− 10.32; − 4.54)* Diet 0– < 3 REF REF REF REF REF REF REF 3– <4 0.42 (− 1.98; 2.82) 1.55 (− 1.79; 4.89) 1.05 (− 1.38; 3.47) 1.52 (− 1.53; 3.83) 1.64 (− 1.25; 4.54) 1.96 (− 0.41; 4.33) − 2.87 (− 5.91; 0.16) >4 0.09 (− 2.45; 2.64) 0.38 (− 3.17; 3.92) 0.39 (− 2.18; 2.96) 1.71 (− 1.14; 4.55) 0.70 (− 2.37; 3.77) 0.26 (− 2.25; 2.78) − 3.12 (− 6.34; 0.10) BMI Normal weight REF REF REF REF REF REF REF Overweight − 0.24 (− 2.46; 1.98) 0.29 (− 2.80; 3.37) 0.97 (− 1.27; 3.20) − 0.58 (− 3.06; 1.90) 0.22 (− 2.45; 2.89) 1.74 (− 0.45; 3.93) − 0.49 (− 3.23; 2.32) Obese − 4.15 (− 7.16; 1.73 (− 5.91; 2.46) − 0.92 (− 3.95; 2.11) − 2.80 (− 6.15; 0.55) − 1.93 (− 5.54; 1.69) − 0.29 (− 3.25; 2.67) 2.81 (− 0.98; 6.60) − 1.15)* Results are expressed as β (95% confidence interval (CI)). All models were adjusted for age, gender, comorbidities and smoking. An increase in functioning scores and global health status indicates an improvement in HRQL. A decrease in fatigue scores indicates an improvement in fatigue *p <0.05 4573 Support Care Cancer (2019) 27:4565–4574 Informed consent Informed consent was obtained from all individual Conclusion participants included in the study. Higher adherence to the WCRF/AICR recommendations was Data We have control over all primary data, we agree to allow the associated with better physical, role, cognitive and social journal to review our data if requested. functioning, better global health status and less fatigue among Open Access This article is distributed under the terms of the Creative CRC survivors. Physical activity seemed to be the main con- Commons Attribution 4.0 International License (http:// tributor to higher scores on most functioning scales and global creativecommons.org/licenses/by/4.0/), which permits unrestricted use, health status and lower scores on fatigue in CRC survivors. distribution, and reproduction in any medium, provided you give appro- priate credit to the original author(s) and the source, provide a link to the Because CRC survivors with the highest adherence to the Creative Commons license, and indicate if changes were made. WCRF/AICR recommendations also report the highest HRQL, we recommend to investigate whether increasing the adherence in CRC survivors indeed results in better HRQL. However, previous research as well as the present study has shown that it is very difficult to motivate cancer survivors to positively References change their lifestyle [12, 20]. Even Lynch syndrome carriers, 1. World Cancer Research Fund and American Institute for Cancer with a very high inherited risk of developing CRC [33], from Research (2007) Food, nutrition, physical activity, and the preven- whom we hoped that they would be extremely motivated to tion of cancer: a global perspective. AICR, Washington DC change their lifestyle, were shown to adhere to those recom- 2. Miller KD, Siegel RL, Lin CC, Mariotto AB, Kramer JL, Rowland mendations only in a slightly better manner than CRC survi- JH, Stein KD, Alteri R, Jemal A (2016) Cancer treatment and sur- vors without Lynch syndrome. Adhering to the WCRF/AICR vivorship statistics, 2016. CA Cancer J Clin 66(4):271–289 3. Marventano S, Forjaz M, Grosso G, Mistretta A, Giorgianni G, recommendations can be challenging for CRC survivors. Thus, Platania A, Gangi S, Basile F, Biondi A (2013) Health related qual- trials aiming to increase adherence should not only focus on the ity of life in colorectal cancer patients: state of the art. BMC Surg effects better adherence has on cancer outcomes but also on 13(2):S15 tools to stimulate and motivate CRC survivors to follow the 4. Jansen L, Koch L, Brenner H, Arndt V (2010) Quality of life among recommendations to the best of their abilities. long-term (⩾ 5 years) colorectal cancer survivors–systematic re- view. Eur J Cancer 46(16):2879–2888 5. Schlesinger S, Walter J, Hampe J, von Schönfels W, Hinz S, Acknowledgements The authors thank the registration teams of the Küchler T, Jacobs G, Schafmayer C, Nöthlings U (2014) Netherlands Comprehensive Cancer Organisation for the collection of Lifestyle factors and health-related quality of life in colorectal can- data for the Netherlands Cancer Registry and members of the cer survivors. Cancer Causes Control 25(1):99–110 PROFILES registry for distribution and handling of the questionnaires. 6. Sánchez PH et al (2012) Adherence to the Mediterranean diet and We are very grateful for the participation of all patients and their doctors quality of life in the SUN Project. Eur J Clin Nutr 66(3):360–368 in the study. Special thanks go to Dr. M. van Bommel, who was willing to 7. Mosher CE, Sloane R, Morey MC, Snyder DC, Cohen HJ, Miller function as an independent advisor and to answer questions of patients. PE, Demark-Wahnefried W (2009) Associations between lifestyle We also want to thank the following hospitals for their cooperation: factors and quality of life among older long-term breast, prostate, Amphia hospital, Breda; Bernhoven Hospital, Uden; Catharina hospital, and colorectal cancer survivors. Cancer 115(17):4001–4009 Eindhoven; Elisabeth-TweeSteden hospital, Tilburg and Waalwijk; Elkerliek Hospital, Helmond; Jeroen Bosch hospital, ‘s Hertogenbosch; 8. 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Published: Mar 29, 2019

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