Abstract
Background:
Endoscopic screening and adherence to a healthy lifestyle are major avenues for colorectal cancer (CRC) prevention. We investigated changes in lifestyles after endoscopic screening.
Methods:
We drew data from 76,303 pairs of time- and age-matched individuals who had and had not, respectively, reported first time endoscopic screening, in the three cohorts (Nurses’ Health Study I and II and the Health Professionals Follow-up Study). Detailed information was collected every 2–4 years on endoscopy screening, 12 lifestyle factors (including smoking, physical activity, regular use of aspirin/non-steroidal anti-inflammatory drugs, body weight, and 8 dietary factors), and adherence to a healthy lifestyle based on a score defined by 5 major lifestyle factors (smoking, alcohol, body weight, physical activity, and diet). We assessed changes in lifestyle from pre- to post-screening periods for the matched pairs. We also conducted subgroup analysis according to screening findings (negative, low- and high-risk polyps, and CRC).
Results:
Endoscopic screening was associated with higher prevalence of adherence to a healthy lifestyle (odds ratio [OR] = 1.09, 95% CI, 1.04, 1.16). The association strengthened with the severity of the screening findings, OR (95% CI) of 1.09 (1.03, 1.15) for negative screening, 1.19 (1.07, 1.33) for low-risk polyps, 1.42 (1.14, 1.77) for high-risk polyps, and 1.55 (1.17, 2.05) for CRC. The individual lifestyle factors and diet showed modest change.
Conclusion:
Endoscopic screening was associated with a modest improvement in healthy lifestyles, particularly in individuals with more severe endoscopic findings. Further efforts of integrating lifestyle medicine into the screening setting are needed, to better leverage the teachable moment in improving CRC prevention.
Keywords: Colorectal Cancer Screening, Lifestyle, Diet
Graphical Abstract
Background
Endoscopy screening and adherence to a healthy lifestyle have both been shown to decrease the incidence and mortality of colorectal cancer (CRC) (1, 2). Smoking, being overweight, physical inactivity, alcohol use, and low consumption of fiber are among the major modifiable risk factors causing early CRC death (3) and premature all-cause mortality in high-income countries (4). The aim of CRC screening is reducing CRC mortality without harms. It has been hypothesized that attending CRC screening might have unwanted effects such as an unhealthier lifestyle compared to the pre-screening period, known as the “health certificate” effect. This implies that screening attendees who are neoplasia-free may perceive that they are in good general health after screening, and thus more prone to engage in unhealthy behaviors (5–8). On the other hand, CRC screening has been proposed as a “teachable moment” for patients to adopt lifestyle modifications (9, 10).
European studies have investigated the effect of CRC screening on diet and lifestyle. However, the findings have been inconclusive (7, 8, 11–13). These studies are limited by a relatively small sample size, short follow-up, and lack of detailed diet and lifestyle information. Furthermore, these studies are mostly based on fecal occult blood test (FOBT) or sigmoidoscopy as the screening methods. Larger studies on colonoscopy screening with detailed lifestyle information are needed.
We examined the change in diet and lifestyle after endoscopic screening in the Nurses’ Health Study (NHS) I and II and the Health Professionals Follow-up Study (HPFS). In addition, we performed subgroup analysis according to screening findings.
Materials and Methods
Study population
The NHS I included 121,700 registered US female nurses aged 30 to 55 at enrollment in 1976. The NHS II included 116,429 registered US female nurses aged 25 to 42 years at enrollment in 1989. The HPFS enrolled 51,529 male health professionals, with 57% dentists, 8% pharmacists, 7% optometrists, 4% osteopath physicians, 4% podiatrists, and 20% veterinarians, aged 40 to 75 at study entry in 1986. More details have been described previously (14–16). Briefly, participants were mailed a biennial self-reported questionnaire that inquired detailed medical and lifestyle information, including history of endoscopic examinations and diagnosis of CRC and polyp. Diet was assessed by a validated food frequency questionnaire (FFQ) every four years. The validity of FFQs in assessing food and nutrient intake has been documented previously (17, 18). Based on the number of person-years in active follow-up divided by the total number of person-years in the cohorts the average follow-up rate has been greater than 90% in all three cohorts. Because detailed diet and lifestyle information was not available before 1986 and 1991 for NHS I/HPFS and NHS II, respectively, these years were used as the first possible inclusion years for the current study. Individuals who reported having had an endoscopy or a diagnosis of polyps or CRC or died before these years were excluded. A total of 76,303 participants were included in the current study who had reported first time endoscopic screening and had reported diet and lifestyle before the screening, among whom 28,208 were from NHS I, 34,518from NHS II and 13,577 from HPFS. For each of the 76,303 participants who had received endoscopic screening (cases), we identified a 1:1 age-matched control who had not yet undergone screening in the year when the case reported endoscopic screening within each of the three cohorts (sex was thus matched on as well).
The study was approved by the institutional review board at the Brigham and Women’s Hospital and Harvard T.H. Chan School of Public Health.
Exposure assessment
On each biennial questionnaire, participants were asked if in the past two years they had undergone colonoscopy or sigmoidoscopy, and if yes, the reasons for these exams by predetermined answer options including family history of CRC and screening, defined as screening, and if any colorectal polyp or CRC had been diagnosed. For those who reported a diagnosis, we asked for permission to acquire their endoscopic and pathologic records. Investigators blinded to any exposure information reviewed all records and extracted clinicopathological data. The primary exposure of the current study was the first report of endoscopic use for CRC screening. We also assessed the exam findings (negative, low-risk polyps, high-risk polyps, and CRC). High-risk findings were as follows: 1) serrated polyps (including hyperplastic polyps and sessile serrated lesions) of ≥10mm or with dysplasia; 2) advanced adenomas (including ≥10mm adenomas of any histology, tubulovillous or villous adenomas, and adenomas with high-grade dysplasia). Low-risk polyps included all other polyp findings. If an individual had multiple findings of polyps and CRC, the individual was categorized with the most severe finding.
Outcome assessment
Our primary outcomes were based on self-reported lifestyle factors before and after the first endoscopic screening. For the unscreened individuals, the lifestyle data were collected from the same questionnaire cycles as the matched screened individuals for the pre- and post-screening periods. In the baseline and biennial follow-up questionnaires weight, smoking, physical activity, and regular use of aspirin/NSAID was reported. Smoking was dichotomized as current vs. noncurrent smoking. Physical activity was queried for a variety of leisure-time activities (e.g. walking, jogging, swimming, weight training etc.). Total physical activity was assessed by the total hours per week for moderate-to-vigorous intensity activity (including brisk walking) that requires the expenditure of at least 3 metabolic equivalents per hour (19). By the reported hours spend per week, physical activity was dichotomized into ≥7.5 MET-hours per week vs. < 7.5 MET-hours per week, which corresponds to weekly activity of at least 75 vigorous-intensity or 150 moderate-intensity minutes, as recommended by the Physical Activity Guidelines for Americans (20, 21). Details about assessment of aspirin/NASID use has been described previously (22–24). Briefly, the participants were asked if they took aspirin/NSAIDs regularly, and if so, the frequency and dose of use per week. Consistent with prior analysis (22–24), regular aspirin/NSAIDs use was dichotomized into ≥2 tablets per week vs. <2 tablets per week.
Every 4 years a validated FFQ was administered to measure diet and alcohol intake for processed meat (serving/day), red meat (serving/day), alcohol (g/day), fruit (serving/day), vegetables (serving/day), fiber (g/day), whole grain (g/day), and calcium (mg/day). To assess the overall change in lifestyle factors, we created a lifestyle score based on five major CRC risk lifestyle factors, including body mass index (kg/m2, BMI), smoking, alcohol consumption, physical activity, and diet. Each of the lifestyle factors was defined by a binary criterion, by which a participant received a score of one if they met the criterion and zero otherwise. In the score one point was given to each of the fulfilled lifestyle factors: a normal BMI between ≥ 18.5 and < 25.0 kg/m2 according to the World Health Organization, no current smoking, physical activity of ≥7.5 MET-hours per week, no or moderate alcohol drinking (≤1 drink/d for women, ≤2 drinks/d for men) (25), and having a healthy diet. Diet was assessed by adherence to the American Institute for Cancer Research/World Cancer Research Fund recommendations for cancer prevention (2) and the Dietary Guideline for Americans (25) that encompass the following components: processed meat of < 0.2 serving/day, red meat of < 0.5 serving/day, dietary fiber of ≥30 g/day, whole grain of ≥ 48 g/day or account for at least half of total grains. Individuals who met three or more of the four dietary criteria were considered to have a healthy diet. The overall lifestyle score ranged 0–5 with a higher score indicating a healthier lifestyle.
Covariate assessment
In the baseline and biennial follow-up questionnaire, we assessed covariates that may influence lifestyles, including ethnicity, diagnoses of chronic diseases (including cardiovascular diseases (CVD), other cancers than CRC, and diabetes), physical exams within the last 2 years, and family history of CRC. Participants were defined as having a positive family history of CRC if at least one of their parents or siblings had been diagnosed with CRC.
Statistical analyses
Our main analysis was on the differences in changes in diet and lifestyle following the first report of endoscopic screening between the screened and matched unscreened. The data were organized in a longitudinal format and participants contributed with two observations with each representing a 2–4-year questionnaire cycle, one before and one at the first reported endoscopy screening. Multivariable-adjusted regressions for two clustered data (PROC GENMOD) were used to account for the two observations per individuals. We compared the dietary and lifestyle factors before and after endoscopic screening in screened and the matched unscreened and calculated the odds ratios (ORs) for categorical variables and mean differences for continuous variables, respectively, along with their 95% confidence intervals (CIs). In addition to the binary exposure for endoscopic screening, we also performed the analysis according to screening findings (negative, low- and high-risk polyps, and CRC). All analyses were adjusted for the following covariates: sex, ethnicity (Whites and non-Whites), diagnosis of chronic diseases (CVD, other cancer than CRC, or diabetes), physical exam in the past two years (yes or no), family history of CRC (yes or no), time of follow-up (continuous). We also performed stratified analyses according to age of screening (<60 years and ≥ 60 years), family history of CRC (yes or no) and time period of screening (1986–1996, 1997–2007 or 2008–2014). We tested the interaction between stratified variables age and family history of CRC and screening status using the Wald-test for the product term.
Missing data in a particular questionnaire cycle were imputed using the mean of the data from the proximate rounds before and after that missing cycle. For example, if physical activity was missing in the year 1990, we used the mean of physical activity reported in 1988 and 1992 to impute the physical activity in 1990. Our analysis was based on available-data method, under the assumption that missing is at random (26).
All the analyses were performed using SAS 9.4 (SAS Institute, Cary, NC, USA). All the statistical tests were two-sided and p-values <0.05 was considered statistically significant.
Results
During a median follow-up of 17 years, 76,303 participants reported to have their first time endoscopic screening, among whom 69,251 had negative screening and 7,052 had positive screening for any neoplastic findings; among the latter group, 5,344 had low-risk polyps, 1,457 had high-risk polyps, and 251 had CRC. Of the participants 94.1% were White, 18.6 % had family history of CRC and 90.2% reporting a physical examination within the last two years. We identified 76,303 unscreened individuals matched on, age, time of screening and cohort. The median age were 55 (50–63) and 82.2% were female.
The percentage of missingness ranged between 1–20% for the diet and lifestyle variables and were similar in the screened and unscreened groups, as well as in the pre- and post-screening periods (supplementary table 1).
Table 1 presents the multivariable-adjusted change in diet and lifestyle after screening. Table 2 shows the subgroup analysis according to the findings of screening. Table 3 shows the stratified analysis according to age and family history of CRC. Data for time period of screening and change in diet and lifestyle are presented in the Supplementary Table 2. We summarize below the major findings.
Table 1.
Change in lifestyle factors from before first endoscopic screening to after first endoscopic screening compared to matched-unscreened in NHS1 1986–2014, NHS2 1989–2015 and HPFS 1986–2010
| Variables | Matched-unscreened | Screened | Odds ratio for categorical variables or mean differences for continues variables (95% CI) | ||
|---|---|---|---|---|---|
| pre-screening | post-screening | pre-screening | post-screening | ||
| Categorical variables, % | |||||
| Lifestyle score of five† ‡ | 6.2 | 7.5 | 6.9 | 9.1 | 1.09 (1.04, 1.16) |
| Lifestyle score of more than one† ‡ | 96.5 | 96.9 | 97.4 | 97.7 | 0.95 (0.88, 1.04) |
| Non-smoking * | 92.9 | 93.7 | 95.0 | 95.6 | 1.00 (0.97, 1.02) |
| Physical activity (≥7.5 MET-hours/week) * | 68.2 | 69.5 | 72.0 | 73.7 | 1.01 (0.99, 1.03) |
| Regular use of aspirin/NSAID (≥2 tabs/week) * | 43.4 | 46.1 | 44.0 | 46.3 | 0.97 (0.95, 0.99) |
| Continuous variables, median (q25, q75) | |||||
| Weight (kg) * | 72.6 (62.6, 83.9) | 72.6 (63.1, 83.9) | 71.2 (62.1, 81.7) | 71.7 (62.6, 82.6) | 0.0 (−0.1, 0.1) |
| Processed meat (servings/day)† | 0.1 (0.1, 0.3) | 0.1 (0.1, 0.3) | 0.1 (0.1, 0.2) | 0.1 (0.0, 0.2) | 0.0 (0.0, 0.0) |
| Red meat (servings/day)† | 0.5 (0.3, 0.9) | 0.5 (0.2, 0.8) | 0.5 (0.3, 0.8) | 0.44 (0.2, 0.8) | 0.0 (0.0, 0.0) |
| Alcohol (g/day)† | 2.0 (0.0, 8.7) | 2.1 (0.0, 9.4) | 2.5 (0.0, 9.5) | 2.5 (0.0, 10.6) | 0.1 (0.0, 0.2) |
| Fruit (servings/day)† | 1.42 (0.8, 2.3) | 1.5 (0.8, 2.4) | 1.5 (0.8, 2.4) | 1.6 (0.9, 2.4) | 0.0 (0.0, 0.0) |
| Vegetables (servings/day)† | 2.9 (1.9, 4.2) | 2.9 (1.9, 4.2) | 2.9 (1.9, 4.2) | 3.0 (2.0, 4.3) | 0.0 (0.0, 0.1) |
| Fiber (g/day)† | 19.6 (14.7, 25.7) | 20.4 (15.3, 26.7) | 20.0 (15.2, 25.9) | 21.0 (15.8, 27.3) | 0.3 (0.2, 0.4) |
| Wholegrain (g/day)† | 24.8 (13.5, 39.9) | 28.2 (15.9, 43.3) | 26.0 (14.4, 40.8) | 29.7 (17.5, 44.7) | 0.4 (0.1, 0.7) |
| Calcium (mg/day)† | 1127 (729, 1619) | 1211 (777, 1723) | 1189 (768, 1684) | 1302 (838, 1802) | 21.0 (13.6, 28.4) |
| Lifestyle score (point)† ‡ | 3.0 (2.0,4.0) | 3.0 (3.0,4.0) | 3.0 (3.0,4.0) | 3.0 (3.0,4.0) | 0.0 (0.0, 0.0) |
Abbreviations: NHS, the Nurses’ Health Study; HPFS Health Professional Follow-up Study; CRC colorectal cancer; CVD cardiovascular diseases; MET metabolic equivalent task; tabs tablets; kg kilogram; g gram; mg microgram; BMI body mass index; NSAID nonsteroidal anti-inflammatory drug.
Measured every 2 years. Model adjusted for: sex, diagnosis of chronic diseases (CVD, other cancer than CRC, diabetes), ethnicity (Whites and non-Whites), physical exam, family history of CRC, time of follow-up.
Measured every 4 years. Model adjusted for: sex, diagnosis of chronic diseases (CVD, other cancer than CRC, diabetes), ethnicity (Whites and non-Whites), physical exam, family history of CRC, time of follow-up.
Lifestyle score was measured every 4 years, one point was given for; non-smoking, BMI 18.5–24.9 kg/m2, Physical activity ≥7.5 MET-hours/week, alcohol of ≤ 14 g/day for women and ≤ 28 g/day for men and a diet score ≥3 points. In the diet score one point was given for; processed meat was ≤ 0.2 servings/day, red meat ≤ 0.5 servings/day, fiber ≥ 30 g/day, wholegrain ≥ 48 g/day or account for at least half of total grains.
Table 2.
Change in lifestyle factors comparing before first endoscopic screening to after first endoscopic screening compared to matched unscreened to findings at first endoscopic screening in NHS1 1986–2014, NHS2 1989–2015 and HPFS 1986–2010, odds ratio for categorical variables or mean of difference for continuous variables and 95% confidence interval.
| Variables | Negative endoscopy | Positive endoscopy (low-risk and high-risk polyps and CRC) | Low-risk polyps | High-risk polyps | CRC |
|---|---|---|---|---|---|
| Categorical variables | |||||
| Lifestyle score of five† ‡ | 1.09 (1.03, 1.15) | 1.19 (1.07, 1.33) | 1.19 (1.07, 1.33) | 1.42 (1.14, 1.77) | 1.55 (1.17, 2.05) |
| Lifestyle score of more than one† ‡ | 0.95 (0.87, 1,03) | 0.90 (0.76, 1.06) | 0.90 (0.96, 1.06) | 0.80 (0.58, 1.12) | 0.76 (0.50, 1.15) |
| Non-smoking* | 0.99 (0.96, 1.01) | 0.97 (0.92, 1.03) | 0.97 (0.92, 1.03) | 0.95 (0.85, 1.05) | 0.93 (0.82, 1.07) |
| Physical activity (≥7.5 MET-hours/week)* | 1.01 (0.99, 1.03) | 1.02 (0.98, 1.07) | 1.02 (0.98, 1.07) | 1.04 (0.96, 1.07) | 1.05 (0.95, 1.17) |
| Regular use of aspirin/NSAID (≥2 tabs/week)* | 0.97 (0.94, 0.99) | 0.94 (0.89, 0.99) | 0.94 (0.89, 0.99) | 0.88 (0.80, 0.98) | 0.85 (0.75, 0.97) |
| Continuous variables, median (q25, q75) | |||||
| Weight (kg)* | 0.0 (−0.2, 0.1) | 0.3 (0.1, 0.4) | 0.4 (0.2, 0.6) | 0.0 (−0.3, 0.2) | −0.8 (−1.7, 0.0) |
| Processed meat (servings/day)† | 0.0 (0.0, 0.0) | 0.0 (0.0, 0.1) | 0.0 (0.0, 0.0) | 0.0 (0.0, 0.0) | 0.0 (0.0, 0.0) |
| Red meat (servings/day)† | 0.0 (0.0, 0.1) | 0.0 (0.0, 0.0) | 0.0 (0.0, 0.0) | 0.0 (0.0, 0.0) | 0.0 (−0.1, 0.1) |
| Alcohol (g/day)† | 0.1 (0.0, 0.2) | 0.1 (−0.2, 0.3) | 0.2 (−0.1, 0.4) | −0.1 (−0.7, 0.4) | −1.4 (−3.0, 0.3) |
| Fruit (servings/day)† | 0.0 (0.0, 0.0) | 0.0 (0.0, 0.0) | 0.0 (0.0, 0.0) | 0.0 (−0.1, 0.1) | −0.2 (−0.3, 0.0) |
| Vegetables (servings/day)† | 0.0 (0.0, 0.0) | 0.0 (0.0, 0.1) | 0.0 (0.0, 0.1) | 0.0 (−0.1, 0.1) | −0.2 (−0.5, 0.1) |
| Fiber (g/day)† | 0.3 (0.2, 0.3) | 0.3 (0.0, 0.5) | 0.3 (0.0, 0.5) | 0.5 (−0.1, 1.0) | −0.7 (−1.8, 0.5) |
| Wholegrain (g/day)† | 0.4 (0.1, 0.7) | 0.2 (−0.4, 0.8) | 0.0 (−0.7, 0.7) | 0.9 (−0.4, 2.1) | 0.2 (−3.3, 3.6) |
| Calcium (mg/day)† | 20 (13, 28) | 27 (9, 43) | 25 (6, 44) | 45 (7, 82) | −43 (−113, 27) |
| Lifestyle score (point)† ‡ | 0.0 (0.0, 0.0) | 0.0 (0.0, 0.1) | 0.0 (0.0, 0.1) | 0.0 (0.0, 0.1) | 0.2 (0.0, 0.3) |
Abbreviations: NHS, the Nurses’ Health Study; HPFS Health Professional Follow-up Study; CRC colorectal cancer; CVD cardiovascular diseases; MET metabolic equivalent task; tabs tablets; kg kilogram; g gram; mg microgram; BMI body mass index; NSAID nonsteroidal anti-inflammatory drug.
Measured every 2 years. Model adjusted for: sex, diagnosis of chronic diseases (CVD, other cancer than CRC, diabetes), ethnicity (Whites and non-Whites), physical exam, family history of CRC, time of follow-up.
Measured every 4 years. Model adjusted for: sex, diagnosis of chronic diseases (CVD, other cancer than CRC, diabetes), ethnicity (Whites and non-Whites), physical exam, family history of CRC, time of follow-up.
Lifestyle score was measured every 4 years, one point was given for; non-smoking, BMI 18.5–24.9 kg/m2, Physical activity ≥7.5 MET-hours/week, alcohol of ≤ 14 g/day for women and ≤ 28 g/day for men and a diet score ≥3 points. In the diet score one point was given for; processed meat was ≤ 0.2 servings/day, red meat ≤ 0.5 servings/day, fiber ≥ 30 g/day, wholegrain ≥ 48 g/day or account for at least half of total grains.
Table 3.
Change in lifestyle factors comparing before first endoscopic screening to after first endoscopic screening compared to matched unscreened, stratified separately by family history of CRC (no, yes) and age at screening, <60 year, ≥ 60 years in NHS1 1986–2014, NHS2 1989–2015 and HPFS 1986–2010 odds ratio for categorical variables or mean of difference for continuous variables and 95% confidence interval and p-value for heterogeneity.
| Family history of CRC | Age group | |||||
|---|---|---|---|---|---|---|
| No | Yes | p ╬ | < 60 years | ≥ 60 years | p ╬ | |
| Categorical variables | ||||||
| Lifestyle score of five† ‡ | 1.08 (1.02, 1.14) | 1.16 (1.06, 1.27) | .11 | 1.14 (1.07, 1.21) | 1.03 (0.96, 1.10) | .01 |
| Lifestyle score of more than one† ‡ | 0.94 (0.87, 1.02) | 1.02 (0.89, 1.17) | .24 | 0.90 (0.82, 0.99) | 1.04 (0.94, 1.15) | .01 |
| Non-smoking* | 0.99 (0.96, 1.02) | 1.02 (0.98, 1.07) | .14 | 0.99 (0.96, 1.02) | 1.00 (0.97, 1.04) | .65 |
| Physical activity (≥7.5 MET-hours/week)* | 1.01 (0.99, 1.04) | 0.99 (0.96, 1.03) | .18 | 1.02 (1.00 ,1.05) | 0.99 (0.97, 1.02) | .03 |
| Regular use of aspirin/NSAID (≥2 tabs/week)* | 0.98 (0.95, 1.00) | 0.94 (0.91, 0.98) | .07 | 0.98 (0.95, 1.00) | 0.97 (0.94, 0.99) | .52 |
| Continuous variables, median (q25, q75) | ||||||
| Weight (kg)* | −0.1 (−0.2, 0.1) | 0.3 (0.1, 0.5) | <.001 | 0.4 (0.2, 0.5) | −0.6 (−0.8, −0.4) | <.001 |
| Processed meat (servings/day)† | 0.0 (0.0, 0.0) | 0.0 (0.0, 0.0) | <.001 | 0.0 (0.0, 0.0) | 0.0 (0.0, 0.0) | <.001 |
| Red meat (servings/day)† | 0.0 (0.0, 0.0) | 0.0 (0.0, 0.0) | .10 | 0.0 (0.0, 0.0) | 0.0 (0.0, 0.0) | .01 |
| Alcohol (g/day)† | 0.1 (0.0, 0.2) | 0.0 (−0.2, 0.1) | .12 | 0.3 (0.2, 0.4) | −0.3 (−0.4, −0.1) | <.001 |
| Fruit (servings/day)† | 0.0 (−0.1, 0.0) | 0.0 (0.0, 0.0) | <.001 | 0.1 (0.1, 0.1) | −0.1 (−0.1, −0.1) | <.001 |
| Vegetables (servings/day)† | 0.0 (0.0, 0.0) | 0.1 (0.0, 0.1) | .36 | 0.1 (0.1, 0.1) | −0.1 (−0.1, −0.1) | <.001 |
| Fiber (g/day)† | 0.3 (0.2, 0.4) | 0.2 (0.0, 0.3) | .26 | 0.6 (0.5, 0.7) | −0.3 (−0.4, −0.2) | <.001 |
| Wholegrain (g/day)† | 0.3 (0.1, 0.6) | 0.6 (0.1, 1.0) | .31 | 0.6 (0.3, 0.9) | 0.1 (−0.2, 0.5) | .02 |
| Calcium (mg/day)† | 20 (12, 27) | 27 (15, 39) | .26 | 33 (25, 42) | 1 (−8, 11) | <.001 |
| Lifestyle score (point)† ‡ | 0.0 (0.0, 0.0) | 0.0 (0.0, 0.0) | .96 | 0.0 (0.0, 0.0) | 0.0 (0.0, 0.0) | <.001 |
Abbreviations: NHS, the Nurses’ Health Study; HPFS Health Professional Follow-up Study; CRC colorectal cancer; CVD cardiovascular diseases; MET metabolic equivalent task; tabs tablets; kg kilogram; g gram; mg microgram; BMI body mass index; NSAID nonsteroidal anti-inflammatory drug.
Measured every 2 years. Model adjusted for: sex, diagnosis of chronic diseases (CVD, other cancer than CRC, diabetes), ethnicity (Whites and non-Whites), physical exam, time of follow-up.
Measured every 4 years. Model adjusted for: sex, diagnosis of chronic diseases (CVD, other cancer than CRC, diabetes), ethnicity (Whites and non-Whites), physical exam, time of follow-up.
Lifestyle score was measured every 4 years, one point was given for; non-smoking, BMI 18.5–24.9 kg/m2, Physical activity ≥7.5 MET-hours/week, alcohol of ≤ 14 g/day for women and ≤ 28 g/day for men and a diet score ≥3 points. In the diet score one point was given for; processed meat was ≤ 0.2 servings/day, red meat ≤ 0.5 servings/day, fiber ≥ 30 g/day, wholegrain ≥ 48 g/day or account for at least half of total grains.
p-value for heterogeneity.
An increase in adhering to a lifestyle score of 5 after screening was observed with an OR of 1.09 (95% CI, 1.04, 1.16). The association strengthened with the severity of the screening findings, with the OR (95% CI) of 1.09 (1.03, 1.15) for negative screening, 1.19 (1.07, 1.33) for positive screening, 1.19 (1.07, 1.33) for low-risk polyps, 1.42 (1.14, 1.77) for high-risk polyps, and 1.55 (1.17, 2.05) for CRC. For the stratified analysis on age, a significant heterogeneity was observed. Age < 60 OR 1.14 (95% CI, 1.07, 1.21), age ≥60 OR 1.03 (95% CI, 0.96, 1.10), (P for heterogeneity, 0.01).
We observed the weight change varied according to the severity of the screening findings. A decreased prevalence of having a regular use of aspirin/NSAID after screening was observed where the association strengthened with the severity of screening findings.
No clinically significant changes in dietary factors or alcohol were observed.
The results for change in lifestyle according to time periods of screening were largely similar to the main results (Supplementary table 2).
Discussion
The current study represents a comprehensive analysis of changes in 12 dietary and lifestyle risk factors for CRC after endoscopic screening. We found that after screening, there was a modest improvement in adherences to a healthier lifestyle but no clinically significant changes in the individual factors. The changes in lifestyle factors tended to be larger for individuals with more severe findings at screening.
The modest improvement in lifestyles observed in the screening group indicate the potential effect of the teachable moment in CRC screening (9, 10) without any explicit intervention. Given the established role of unhealthy lifestyle in risk of CRC (2), integrating lifestyle modification with screening represents the most effective approach to CRC prevention (27). For the largest improvement in lifestyle and diet change this should be done with support and advice by trained personnel grounded in behavioral science (9, 28). Indeed, we have shown that adherences to a healthy lifestyle is associated with the benefit of endoscopic screening (29) and risk reduction of CRC for endoscopic screened and unscreened (27).
Studies investigating how diet and lifestyle change after CRC screening are limited and results remain mixed. Most previous studies have been conducted in European countries, using FOBT or sigmoidoscopy as the screening method and compared to a non-screened control group (7, 8, 11–13). A FOBT-based CRC screening study from the U.K found an increase in physical activity for screened participants (13). The Norwegian Colorectal Cancer Prevention (NORCCAP) study using sigmoidoscopy screening found an unfavorable change in physical activity after screening at three and eleven years follow-up (7, 8). Only at three-year follow-up, an increase in smoking and weight and a decrease in fruit and vegetable consumption were observed after screening (7). In the Bowel Cancer Screening in Norway - a pilot study, no changes in lifestyle were observed at one-year follow-up (12). A Finnish study did not find any lifestyle change after FOBT screening at two-year follow-up (11).
The changes in lifestyle factors observed in our study tended to be larger for individuals with more severe findings at screening. No prior studies have yet investigated this. Individuals with clinically significant findings could benefit more from lifestyle modifications than the general population in decreasing the risk of CRC (30, 31) and should maybe be the one to focus on (30).
The differences in results between our study and the previous studies might be due to the screening setting. Our study was based on an opportunistic and self-initiated screening where the previous studies were based on national organized screening, causing differences in the study population (32). Another difference was the measure of diet and lifestyle. We used a validated FFQ where most other studies have used short lifestyle questionnaires that were often not validated. The previous studies are based on small randomized controlled studies of screening comparing lifestyle of screened individuals to a control group not invited to screening. Thus, the interventional setting makes it difficult to disentangle the effect of interventions from that of screening itself. In contrast, our study is observational and may better capture the changes in real-life settings. Furthermore, our study population was based on health professionals where the previous studies were based on the general population.
Our study has some strengths, including the prospective design, large sample size, long-term follow-up, comprehensive collection of diet and lifestyle factors. Moreover, diagnostic documentation for screening findings enabled us to investigate if differences in diet and lifestyle were dependent on the screening findings. In addition, change was compared to a matched unscreened group there by adjusting for the general secular trend in diet and lifestyles, such as an increase in body fatness over the past few decades. Furthermore the unscreened consisted of never screened and not screened yet, decreasing any selection bias due to higher health consciousness related to screening (33).
Several limitations of our study need to be noted as well. First, as an observational study, we cannot rule out the influence of residual confounding and other lifetime events or participation in other screening programs that might cause change in lifestyle, not adjusted for. However, we adjusted for physical examination within the last two years and diagnoses of other diseases and the matched design help minimize the likelihood of uncontrolled confounding. Second, the screening, diet, and lifestyle factors were all self-reported and are subject to measurement error. However, the validity of these self-reported measures has been established in our previous validation studies (17, 18). Third, we did not have information on other CRC-screening methods, such as FOBT and our results can only be generalized to individuals attending endoscopic screening. Fourth, our study was based on a selected population of health professionals and the findings may not be generalizable to the general American population. Prior evidence indicates that individuals with lower socioeconomic status might be more prone to the health certificate effect of CRC screening (34).
In conclusion, we found an overall modest improvement in lifestyle factors after endoscopic screening for CRC, where change tended to be greater with more severe endoscopic findings. Given the importance of lifestyle factors for CRC prevention, integrating patient support for lifestyle modification, may substantially improve the benefit of CRC screening.
Supplementary Material
What You Need to Know.
Background:
Endoscopic screening and adherence to a healthy lifestyle are two major approaches for colorectal cancer prevention. It remains unclear whether and how individuals may change their lifestyles after endoscopic screening.
Findings:
In this first time American study we observed a modest change to a healthier lifestyle after endoscopic screening. Larger changes were found for individuals with more severe screening findings.
Implications for patient care:
Given the importance of lifestyle for colorectal cancer prevention, integrating patient education in lifestyle modification may improve the benefit of colorectal cancer screening.
Acknowledgement:
We would like to thank the participants and staff of the Nurses’ Health Study and Health Professionals Follow-up Study for their valuable contributions as well as the following state cancer registries for their help: AL, AZ, AR, CA, CO, CT, DE, FL, GA, ID, IL, IN, IA, KY, LA, ME, MD, MA, MI, NE, NH, NJ, NY, NC, ND, OH, OK, OR, PA, RI, SC, TN, TX, VA, WA, WY. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Grand Suppoert:
This work was supported by the US National Intitules of Health (NIH) (UM1 CA186107, P01 CA87969, U01 CA176726, U01 CA167552; R00 CA215314 to MS, K24 DK098311, R01 CA137178, R01 CA202704 to ATC; P01 CA55075, R01 CA151993, R35 CA197735 to SO; R03 CA197879, R21 CA222940 to KW; P01 CA55075, R01 CA151993, R35 CA197735 to SO; R21 CA230873 to KW and SO ); the American Institute for Cancer Research (to KW); the American Cancer Society (MRSG-17-220-01 – NEC to MS); the South-Eastern Norway Reginal Health Authority (project number: 20190770 to MDK).
The funders had no role in the design and conduct of the study.
Abbreviations:
- BMI
body mass index
- CI
confidence intervals
- CRC
colorectal cancer
- CVD
cardiovascular diseases FFQ, food frequency questionnaire
- FOBT
fecal occult blood test
- HPFS
Health professionals Follow-up study
- MET
metabolic equivalent of task
- NHS
Nurses’ Health Study
- NORCCAP
The Norwegian Colorectal Cancer Prevention
- NSAIDs
aspirin/non-steroidal anti-inflammatory drugs
- OR
odds ratio
Footnotes
Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Disclosures: ATC previously served as a consultant for Bayer Healthcare and Pfizer for work unrelated to the topic of this manuscript. All remaining authors have declared no conflicts of interest.
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