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. 2011 Feb 8;104(5):882–885. doi: 10.1038/sj.bjc.6606045

Physical activity and risk of colon adenoma: a meta-analysis

K Y Wolin 1,*, Y Yan 1, G A Colditz 1
PMCID: PMC3048199  PMID: 21304525

Abstract

Background:

Little evidence is available on the relation of physical activity with colon adenomas, a colon cancer precursor.

Methods:

We conducted a systematic literature review and meta-analysis of published studies (in English) through April 2010, examining physical activity or exercise and risk or prevalence of colon adenoma or polyp. Random effects models were used to estimate relative risks (RRs) and corresponding confidence intervals (CIs). A total of 20 studies were identified that examined the association and provided RRs and corresponding 95% CIs.

Results:

A significant inverse association between physical activity and colon adenomas was found with an overall RR of 0.84 (CI: 0.77–0.92). The association was similar in men (RR=0.81, CI: 0.67–0.98) and women (RR=0.87, CI: 0.74–1.02). The association appeared slightly stronger in large/advanced polyps (RR=0.70, CI: 0.56–0.88).

Conclusion:

This study confirms previous reports of a significant inverse association of physical activity and colon adenoma, and suggests that physical activity can have an important role in colon cancer prevention.

Keywords: physical activity, colon adenoma, colon polyp

Convincing evidence exists for a causal, inverse association between physical activity and risk of colon cancer (International Agency for Research on Cancer WHO, 2002; World Cancer Research Fund/American Institute for Cancer Research, 2007b; Wolin et al, 2009). This association is plausibly supported by several biological mechanisms, including decreased inflammation, decreased insulin-like growth factor levels, reduced hyperinsulinemia and modulated immune function (Wolin et al, 2009). Fewer data are available with respect to physical activity and colon adenomas, the precursor lesion detected and removed during sigmoidoscopy or colonoscopy. Although numerous studies have examined this association, no comprehensive meta-analysis is available. A limited meta-analysis by the World Cancer Research Fund included three studies, and estimated physical activity was associated with a statistically significant 15% reduction in colon polyp risk (World Cancer Research Fund/American Institute for Cancer Research, 2007a). Estimation of the risk reduction associated with the physical activity is important for public health because lifestyle is associated with a decreased risk of colon cancer, even among those who have undergone colon cancer screening (Wei et al, 2009). Furthermore, evidence on smoking has suggested that risk may vary for colon polyps versus colon cancer (Botteri et al, 2008). We therefore conducted a meta-analysis to estimate the summary relative risk (RR) of colon polyps associated with physical activity.

Materials and methods

We searched the literature using PubMed, CINAHL and Scopus for all studies on physical activity or exercise and colon polyps through April 2010. We employed the terms exercise and physical activity in combination with colon polyps using the terms colon polyp, colon adenoma, colorectal polyp, colorectal adenoma and adenomatous polyps. We also utilised a previous review of the data (Samad et al, 2005; Lee and Oguma, 2006; World Cancer Research Fund/American Institute for Cancer Research, 2007a) and manual searches of the reference lists of identified manuscripts. We included recurrent, incident and prevalent cases of colon polyps. We did not limit studies by type of physical activity or study sample demographics.

Our search yielded 89 potential articles. We excluded reviews, non-human studies, editorials/comments/letters to the editor, studies without colon polyps as an outcome, studies where physical activity was only included as a covariate (and thus no measure of association was presented), and where no metric for effect estimate precision (P-value, s.e., confidence interval (CI)) was provided. Combined with searches from the reference sections of manuscripts and previous reviews, this yielded 20 manuscripts. From each manuscript, we abstracted the sample size (including number of cases), gender, years of follow-up or type of control sample, case definition, physical activity domain, adenoma detection method, sample definition criteria and results. We also abstracted the variables that each study used in its most adjusted analysis. Data extraction was performed by a single investigator (KYW). Where studies included more than one type of physical activity without a summary measure, we included only leisure time physical activity, which is the major modifiable component of energy.

Previous meta-analyses have suggested that results for adenomatous polyps need to be presented separately from hyperplastic or malignant polyps. (Botteri et al, 2008) Although we did not restrict our analysis to studies where data was limited to adenomatous polyps, we did consider those results separately. Specifically, we excluded results for hyperplastic polyps where feasible. We also identified studies considered to be the ‘best approach’ using criteria similar to those used in a previous meta-analysis (Botteri et al, 2008), namely, studies that met all of the following: (1) limited the outcome to only adenomatous polyps; (2) all individuals received a full colonoscopy; and (3) the study population excluded anyone with inherited colorectal cancer syndromes, inflammatory bowel disease, a history of colon polyps or cancer, or a previous colon resection.

Data analysis

Meta-analysis of random effects was used to allow for the heterogeneity of results across studies. (Mosteller and Colditz, 1996) Data were processed in SAS, and the analyses were performed using R-package ‘meta’ (SAS Institute Inc., Cary, NC, USA). A summary forest plot was generated in Stata (StataCorp LP, College Station, TX, USA). As most studies reported RRs or odds ratios (ORs) and their associated 95 percent CIs, we used these data as summary statistics for each study. First, we derived the s.e. of log (RR or OR) using the 95 percent CI, with the expression: (log (upper limit) – log (lower limit))/2*1.96. These s.es were used as weights for summary effect estimates in the meta-analysis. We visually examined publication bias using Funnel plots, and employed the rank correlation method to formally test for bias. (Begg and Mazumdar, 1994) Where studies reported results separately for men and women, we included both estimates when reporting the overall association. To evaluate the potential effects of limiting results to only adenomatous polyps, we conducted exploratory analysis in the subset of those studies. We also included results separately for large/advanced adenoma, if the data were presented as such in the original manuscript. We also conducted exploratory analyses limited to those studies defined as the ‘best approach’. To test sub-analysis differences (large vs all adenomas; best approach vs all studies), we partitioned ‘total heterogeneity’ into between-group and within-group heterogeneity, and used the ‘between-group’ heterogeneity index as the test statistic against χ2 distribution with 1 degree of freedom. (Cooper and Hedges, 1994).

Results

We identified 20 studies of physical activity and colon adenomas (Table 1). (Kono et al, 1991, 1999; Little et al, 1993; Shinchi et al, 1994; Giovannucci et al, 1995, 1996; Sandler et al, 1995; Neugut et al, 1996; Enger et al, 1997; Lubin et al, 1997; Kahn et al, 1998; Boutron-Ruault et al, 2001; Colbert et al, 2002; Lieberman et al, 2003; Tiemersma et al, 2003; Hauret et al, 2004; Wallace et al, 2005; Larsen et al, 2006; Rosenberg et al, 2006; Hermann et al, 2009) Most collected physical activity information via questionnaire, with nine studies only collecting information on leisure activity. Studies often did not specify or query the reasons participants underwent colonoscopy or sigmoidoscopy, thus, cases included are both symptomatic and screening. Only two studies (Colbert et al, 2002; Wallace et al, 2005) included procedures for the study, both were in studies of polyp recurrence. All but two studies (Kahn et al, 1998; Rosenberg et al, 2006) reported results for adenomas separately from all polyps or limited results to adenomas. A total of 10 studies (Shinchi et al, 1994; Giovannucci et al, 1995, 1996; Lubin et al, 1997; Kono et al, 1999; Boutron-Ruault et al, 2001; Colbert et al, 2002; Lieberman et al, 2003; Wallace et al, 2005; Larsen et al, 2006) reported results separately for large or advanced adenomas.

Table 1. Studies include in meta-analysis of physical activity and colon polyps.

Author and Year Gender Number of study subjects Number of Cases Relative Risk Lower Confidence Interval Upper Confidence Interval Type of Physical Activity Case definition Non-case/ comparison definition
Kono et al, 1991 Both 1148 80 0.44 0.22 0.87 Leisure Adenoma None
Little et al, 1993 Both 300 147 0.46 0.17 1.29 Leisure Adenoma FOBT negative
Shinchi et al, 1994 Both 1712 228 1.2 0.8 2 Leisure Adenoma None
Giovannucci et al, 1995 Men 12 879 455 0.79 0.57 1.09 Leisure Distal Adenoma No polyp
Sandler, 1995 Men 234 86 0.92 0.36 2.31 Leisure Adenoma Hyperplastic/none
Sandler, 1995 Women 350 114 0.64 0.35 1.19 Leisure Adenoma Hyperplastic/none
Giovannucci et al, 1996 Women 13 057 330 0.58 0.4 0.86 Leisure Distal Adenoma None
Neugut, 1996 Men 400 225 0.6 0.4 1 Total Adenoma None
Neugut, 1996 Women 411 283 1.3 0.7 2.3 Total Adenoma None
Enger et al, 1997 Both 920 460 1 0.7 1.5 Total Adenoma No polyp
Lubin et al, 1997 Both 392 196 0.6 0.3 0.9 Total Large/advanced Adenoma Hyperplastic/None
Kahn et al, 1998 Men 72 868 7504 0.83 0.76 0.91 Total All polyps None
Kahn et al, 1998 Women 81 356 5111 0.9 0.78 1.03 Total All polyps None
Kono et al, 1999 Both 415 189 0.6 0.3 1.3 Leisure Adenoma Normal
Boutron-Ruault et al, 2001 Both 581 154 1.3 0.7 2.5 Total Small adenoma None
Boutron-Ruault et al, 2001 Both 635 208 0.8 0.4 1.5 Total Large/advanced adenoma None
Colbert et al, 2002 Both 1839 733 1.2 0.9 1.6 Total Adenoma or cancer None
Lieberman et al, 2003 Both 2082 312 0.94 0.86 1.02 Total Large/advanced adenoma None
Tiemersma et al, 2003 Women 471 196 1.05 0.72 1.54 Not specified Adenoma None
Tiemersma et al, 2003 Men 398 237 0.69 0.43 1.1 Not specified Adenoma None
Hauret et al, 2004 Both 405 177 0.63 0.34 1.17 Total Adenoma Hyperplastic/None
Wallace et al, 2005 Men 787 539 0.35 0.17 0.72 Total Large/advanced adenoma None
Wallace et al, 2005 Women 787 205 1.21 0.36 4.03 Total Large/advanced adenoma None
Larsen et al, 2006 Both 3696 426 0.96 0.74 1.25 Total Low risk adenoma None
Larsen et al, 2006 Both 3376 106 0.56 0.34 0.92 Total Large/advanced adenoma or cancer None
Rosenberg et al, 2006 Women 45 400 1390 0.72 0.57 0.91 Leisure All polyps None
Hermann et al, 2009 Both 4510 527 1.02 0.74 1.42 Total Adenoma None
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Abbreviation: FOBT=Fecal occult blood test.

We found significant heterogeneity in the results (P<0.01) and thus, focus our report on the random effects analysis (Figure 1). Overall, there was a significant inverse association between physical activity and colon polyps (fixed effect RR=0.87, 95% CI: 0.83–0.91; random effects RR=0.84, 95% CI: 0.77–0.92) when comparing the most to least active individuals in each study. The summary RR was significant and similar in men (RR=0.81, 95% CI: 0.67–0.98) and women (RR=0.87, 95% CI: 0.74–1.02).

Figure 1.

Figure 1

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Meta-analysis of physical activity and colon adenoma. Study physical activity level comparisons are as follows: Kono et al, 1991: ⩾120 vs 0 min per week; Little et al, 1993: ⩾30 min vs none; Shinchi et al, 1994: daily vs none; Giovannucci et al, 1995: highest vs lowest quintile; Sandler, 1995: highest vs lowest quartile; Giovannucci et al, 1996: highest vs lowest quintile; Neugut et al, 1996: any vs none; Lubin et al, 1997: >5.5 h per day vs <4 h per day; Enger et al, 1997: highest vs lowest quartile; Kahn et al, 1998: high vs low; Kono et al, 1999: ⩾36 MET h per wk vs <4 MET h per wk; Boutron-Ruault et al, 2001: high vs low; Colbert et al, 2002: high vs low quartile; Lieberman et al, 2003: per 5 unit change in physical activity index; Tiemersma et al, 2003: not specified; Hauret et al, 2004: >40 MET h per wk vs <17.1 MET h per wk; Wallace et al, 2005: high vs low tertile; Larsen et al, 2006: high vs low quartile; Rosenberg et al, 2006: ⩾40 MET h per wk vs none; Hermann et al, 2009: active vs inactive. ES=effect size; MET=metabolic equivalent.

There was a tendency for the effect of physical activity to be restricted to large or advanced adenomas and not low grade ones. Similarly, physical activity was associated with large (>1 cm) (RR=0.63, 95% CI: 0.36–1.10), but not with small adenomas in a sample of US male health professionals (Giovannucci et al, 1995). In a cohort of US female nurses, a significant overall risk reduction (RR=0.58, 95% CI: 0.40–0.86) was reported, which was also stronger for larger than smaller adenomas (Giovannucci et al, 1996). Our meta-analysis found the effect was stronger, though not significantly so (P=0.16), for large or advanced (RR=0.70, 95% CI: 0.56–0.88) adenomas than for the overall effect. In analyses limited to the 18 studies where results for adenomatous polyps were separated from all polyps (i.e., hyperplastic, malignant polyps), the meta-analysis estimate for the association between physical activity and risk of polyps was largely unchanged (RR=0.83, 95% CI: 0.73–0.93). In analysis limited to the six studies (Kono et al, 1991; Sandler et al, 1995; Colbert et al, 2002; Lieberman et al, 2003; Tiemersma et al, 2003; Hauret et al, 2004) defined as the ‘best approach,’ the effect estimate was similar to that for all studies (RR=0.87, 95% CI: 0.73–1.05), though not statistically significant.

Discussion

Previous, though limited, reviews have indicated physical activity is associated with a significant reduction in colon polyp risk. (World Cancer Research Fund/American Institute for Cancer Research, 2007a) Our comprehensive meta-analysis supports this conclusion, showing a significant 16% risk reduction when comparing the most to the least active. Risk reductions were similar for men and women, and held when limited to studies designated as the best approach. We found the association was notably stronger when analyses were limited to advanced or large polyps, with a risk reduction of 35%.

These results support the previously documented role of physical activity in colon cancer prevention (International Agency for Research on Cancer WHO, 2002; World Cancer Research Fund/American Institute for Cancer Research, 2007a and 2007b; Wolin et al, 2009). Earlier reports that failed to find an association between physical activity and colon polyps had suggested that physical activity may be more important in the adenoma to carcinoma sequence than in adenoma development (Colbert et al, 2002). Our meta-analysis, combined with the above-mentioned data demonstrating physical activity's role in colon cancer prevention, suggests that physical activity has a role across the carcinogenic process. Several mechanisms have been proposed for such effects, including enhanced immune function, decreased inflammation, reduced insulin levels and insulin resistance, and higher vitamin D levels (Wolin et al, 2009). Hyperinsulinemia has also been directly related to colon polyp risk (Wei et al, 2006).

This comprehensive meta-analysis provides support for an inverse association between physical activity and colon polyps, and also for the role of physical activity in colon cancer carcinogenesis. Physical activity may reduce the risk of colon polyps by 15% and may provide a substantially larger reduction in risk of large and advanced polyps.

Acknowledgments

GAC is supported by an American Cancer Society Clinical Research Professorship. KYW, GAC and YY are supported by CA091842.

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