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Annals of Oncology 25: 1293–1311, 2014
doi:10.1093/annonc/mdu012
Published online 18 March 2014
Association between physical activity and mortality
among breast cancer and colorectal cancer survivors: a
systematic review and meta-analysis
D. Schmid* & M. F. Leitzmann
Department of Epidemiology and Preventive Medicine, University of Regensburg, Regensburg, Germany
Received 16 September 2013; revised 13 November 2013; accepted 3 December 2013
Background: Physical activity improves physical function during and after cancer treatment, but whether physical activ-
ity imparts survival benefit remains uncertain.
Design: Using prospective studies published through June 2013, we conducted a systematic review and random-
effects meta-analysis of pre- and post-diagnosis physical activity in relation to total and cancer mortality among breast or
colorectal cancer survivors.
Results: Sixteen studies of breast cancer survivors and seven studies of colorectal cancer survivors yielded 49095 total
cancer survivors, including 8129 total mortality cases and 4826 cancer mortality cases. Comparing the highest versus
lowest levels of pre-diagnosis physical activity among breast cancer survivors, the summary relative risks (RRs) of total
and breast cancer mortality were 0.77 [95% confidence interval (CI) = 0.69–0.88] and 0.77 (95% CI = 0.66–0.90, re-
spectively. For post-diagnosis physical activity, the summary RRs of total and breast cancer mortality were 0.52 (95%
*Correspondence to: Dr Daniela Schmid, Department of Epidemiology and Preventive
Medicine, University of Regensburg, Franz-Josef-Strauss-Allee 11, 93053 Regensburg,
Germany. Tel: +49-941-944-5245; Fax: +49-941-944-5202; E-mail: daniela.schmid@
klinik.uni-regensburg.de
© The Author 2014. Published by Oxford University Press on behalf of the European Society for Medical Oncology.
All rights reserved. For permissions, please email: journals.permissions@oup.com.
Annals of Oncology reviews
byguestonMay9,2015http://annonc.oxfordjournals.org/Downloadedfrom

CI = 0.42–0.64) and 0.72 (95% CI = 0.60–0.85), respectively. For pre-diagnosis physical activity among colorectal cancer
survivors, the summary RRs of total and colorectal cancer mortality were 0.74 (95% CI = 0.63–0.86) and 0.75 (95%
CI = 0.62–0.91), respectively. For post-diagnosis physical activity, the summary RRs of total and colorectal cancer mortal-
ity were 0.58 (95% CI = 0.48–0.70) and 0.61 (95% CI = 0.40–0.92), respectively. Each 10 metabolic equivalent task-hour/
week increase in post-diagnosis physical activity (equivalent to current recommendations of 150 min/week of at least
moderate intensity activity) was associated with 24% (95% CI = 11–36%) decreased total mortality risk among breast
cancer survivors and 28% (95% CI = 20–35%) decreased total mortality risk among colorectal cancer survivors. Breast or
colorectal cancer survivors who increased their physical activity by any level from pre- to post-diagnosis showed
decreased total mortality risk (RR = 0.61; 95% CI = 0.46–0.80) compared with those who did not change their physical
activity level or were inactive/insufficiently active before diagnosis.
Conclusion: Physical activity performed before or after cancer diagnosis is related to reduced mortality risk among
breast and colorectal cancer survivors.
Key words: cancer, meta-analysis, physical activity, survival
introduction
Breast cancer represents the number one cause of cancer incidence
and mortality in women, with 1.38 million new breast cancer
cases and 458 400 breast cancer deaths estimated to have occurred
in 2008 [1]. Colorectal cancer is the second most frequently diag-
nosed cancer in women and the third most frequently diagnosed
cancer in men, accounting for 1.23 million new colorectal cancer
cases and 608 700 colorectal cancer deaths in 2008.
The number of cancer survivors continues to increase due to
population aging, earlier diagnosis through improved screening,
and advances in modern cancer treatment [2]. The estimated
number of individuals with a history of cancer living in the
USA was 13.7 million in 2012 and is expected to increase to
nearly 18 million by 2022. The 5-year survival rate for breast
cancer patients among females improved from 75.1% between
1975 and 1977 to 90% between 2001 and 2007 [2]. Likewise, the
5-year colon cancer survival rate for men increased from 48.9%
between 1975 and 1977 to 66.1% between 2003 and 2009 [3].
For women, colon cancer survival increased from 50.6 to 65.7%
during that time.
Physical activity is an important determinant of beneficial
health conditions among cancer survivors [4], but whether
physical activity improves cancer survival remains inadequately
understood. Of cancer sites investigated thus far, breast cancer
and colorectal cancer have been the most extensively studied.
Specifically, 16 prospective studies examined physical activity in
relation to survival among individuals with a history of breast
cancer [5–20] and seven prospective studies investigated the
association between physical activity and survival among
individuals with colorectal cancer [21–27]. Most of those inves-
tigations reported an inverse association between physical activ-
ity and total or cancer mortality [5, 9–14, 16–23, 25–27],
although two studies reported a null relation [6, 15] and one
study found a positive association [8].
The aim of the current systematic review and meta-analysis
was to quantify the evidence from prospective studies of physical
activity in relation to total mortality and cancer mortality
among survivors of breast cancer or colorectal cancer. Our study
differs from two previous meta-analyses on this topic [28, 29] in
quantifying the effect size per increment of physical activity,
examining change in physical activity from pre- to post-diagno-
sis in relation to mortality among cancer survivors, and
performing meta-regression analyses to evaluate potential
sources of heterogeneity between studies.
materials and methods
literature search and inclusion criteria
Our meta-analysis was conducted according to the Preferred
Reporting Items of Systematic reviews and Meta-Analyses
(PRISMA) guidelines [30]. A comprehensive literature search
was carried out in PubMed from the earliest possible year to
June 2013 using the following search terms: (((((physical activ-
ity) OR motor activity) OR exercise)) AND ((((breast cancer)
OR colorectal cancer) OR colon cancer) OR rectal cancer))
AND ((((survival) OR survivor) OR mortality) OR recurrence).
In addition, we reviewed the bibliographic lists of retrieved arti-
cles for relevant studies. Studies were included if they met the
following criteria: they (1) were original human studies pub-
lished in English; (2) investigated the association between phys-
ical activity and risk of total mortality or cancer mortality
among breast cancer or colorectal cancer survivors; (3) provided
relative risk (RR) estimates and 95% confidence intervals (CIs)
or data to calculate them; (4) were at least matched or adjusted
for age. If datasets were found to overlap among publications,
we included the article with the largest sample size. Studies were
excluded if the exposure was physical activity combined with
another exposure. We also excluded studies that examined the
combination of cancer recurrence and cancer mortality.
data extraction
Both authors independently assessed the eligibility of studies
and any discrepancies were resolved by consensus. From each
article, the following information was extracted: first author’s
name, publication year, study geographic location, number of
study participants and cases, specific outcomes, measures of ex-
posure, adjustment factors, and RRs with corresponding 95%
CIs. If more than one risk estimate was reported in the same
article, we chose the most fully adjusted estimate. The effect size
and 95% CI were inverted when the most active group was used
as the reference group.
 | Schmid and Leitzmann Volume 25 | No. 7 | July 2014
reviews Annals of Oncology

statistical analysis
We estimated pooled RRs comparing the highest versus lowest
categories of physical activity before and after diagnosis and
change in physical activity from pre- to post-diagnosis in rela-
tion to total or cancer mortality among breast and colorectal
cancer survivors using random-effects models [31]. We priori-
tized risk estimates of lifetime or long-term physical activity
measures over recent physical activity measures. We focused on
recreational physical activity because it represents the main
modifiable aspect of energy expenditure.
We calculated the Q-statistic to test for between-study hetero-
geneity and we used the I²-statistic to quantify the proportion of
the total variation due to heterogeneity [31]. Potential publica-
tion bias was assessed by visual inspection of funnel plots and
by using Egger’s regression test [32] and Begg’s rank correlation
test [33]. Sources of potential heterogeneity among studies were
explored using random-effects meta-regression.
We performed sensitivity analyses omitting one study at a
time from the initial meta-analysis. We addressed the potential
for reverse causation to the extent possible by conducting suba-
nalyses including only studies where post-diagnosis physical
activity was measured within 1–2 years of breast or colorectal
cancer diagnosis.
In an additional analysis, we investigated the association
between physical activity and total and cancer mortality among
subgroups of breast cancer survivors defined by levels of body
mass index (BMI), menopausal status, and estrogen receptor
(ER) status. We lacked corresponding data for colorectal cancer
survivors.
We also examined the relation of physical activity to total
mortality among breast and colorectal cancer survivors using
physical activity as a continuous variable. We pooled risk esti-
mates of physical activity in increments of 5, 10, or 15 metabolic
equivalent task (MET)-h/week using generalized least-squares
trend estimation as described by Orsini et al. [34]. All statistical
analyses were performed using the R-package ‘metafor’ [35] and
SAS version 9.2. P-values were two-sided and were considered
significant at α = 0.05.
results
literature search and description of the studies
Our literature search yielded 1297 publications in PubMed and
1 article identified by manual search (Figure 1). Based on the
screening of titles and abstracts, 32 articles remained for full
review. Of these, we excluded nine studies because they provided
information from overlapping studies or combined physical ac-
tivity with other exposures. A total of 16 studies on breast
cancer survival [5–20] and 7 studies on colorectal cancer survi-
vors [21–27] remained and were included in our meta-analysis.
The total number of individuals in the studies was 49095, in-
cluding 8129 cases of total mortality and 4826 cases of cancer
mortality. Most investigations focused on recreational physical
activity with the exception of 1 study that explored total physical
activity [25]. Physical activity was expressed as times per week,
hours per week, MET-hours per week, or energy expenditure in
calories per week. The number of adjustment factors ranged
from 2 to 16 (Table 1).
breast cancer survivors
pre- and post-diagnosis physical activity. Among breast cancer
survivors, high versus low pre-diagnosis physical activity was
associated with decreased risks of total mortality (RR = 0.77;
95% CI = 0.69–0.88) and breast cancer mortality (RR = 0.77;
95% CI = 0.66–0.90) (Figures 2 and 3). There was no statistically
significant heterogeneity among studies (total mortality:
I2
= 41%; Pheterogeneity = 0.08; breast cancer mortality: I2
= 30%;
Pheterogeneity = 0.16). High versus low post-diagnosis physical
activity was also related to decreased risk of total mortality
(RR = 0.52; 95% CI = 0.42–0.64) and breast cancer mortality
(RR = 0.72; 95% CI = 0.60–0.85). No heterogeneity among studies
was observed (total mortality: I2
= 34%; Pheterogeneity = 0.22;
breast cancer mortality: I2
= 0%; Pheterogeneity = 0.43). We found
no evidence of publication bias by visual inspection of the
funnel plot, Begg’s test (P = 0.33), and Egger’s test (P = 0.20).
Removal of one study at a time did not substantially alter the
results (supplementary Table S1, available at Annals of Oncology
online, for total mortality, supplementary Table S2, available at
Annals of Oncology online, for cancer mortality). A sensitivity
analysis investigating post-diagnosis physical activity measured
within 1–2 years of breast cancer diagnosis did not materially
change the findings (total mortality: RR = 0.57; 95% CI = 0.49–
0.67; breast cancer mortality: RR = 0.71; 95% CI = 0.58–0.86).
stratification by BMI, menopausal status, and tumor ER status.
The association between pre- or post-diagnosis physical activity
and total mortality among breast cancer survivors did not differ
according to BMI, menopausal status, or tumor ER status (all
Pheterogeneity > 0.05; Table 2). We noted a more pronounced
inverse association between the combination of pre- and post-
1297 articles identified in
PubMed
1 article identified from
reference lists
1298 articles identified
32 articles identified for full
review
23 articles included in the
meta-analysis
6 duplicate studies
3 combined exposures
1266 articles excluded that
were not related to physical
activity or total or recurrence
among cancer survivors
Figure 1. Flow diagram of the literature search strategy and study selection
for the meta-analysis.
Volume 25 | No. 7 | July 2014 doi:10.1093/annonc/mdu012 | 

Table 1. Characteristics of the 23 studies included in the meta-analysis
Author, year,
(country)
Cancer type,
stage
Outcome Study design, subjects/
cases, sex
Follow-up
duration
PA before/
after
diagnosis
Category and timing of PA
measurement
Main result: RR (95% CI) Adjustment factors
Rohan et al. [5],
1995
(Australia)
Breast cancer Cancer
mortality
Follow-up of a
population-based
case–control study,
411/112 women
2010 days Before >4000 versus 0 kcal/week of
interview-assessed
recreational PA during the
summer and winter
seasons 1 year before
diagnosis
0
>0 and ≤2000
>2000 ≤4000
>4000
1.0
1.42 (0.78–2.60)
0.73 (0.37–1.42)
0.98 (0.50–1.94)
Age, ER, and PR status, tumor
diameter, years of education,
history of benign breast disease,
age at menarche, age at first live
birth, height, Quetelet’s index,
energy intake, menopausal
status
Borugian et al.
[6], 2004
(Canada)
Breast cancer
stage: ductal
carcinoma
in situ, I, II,
II
Cancer
mortality
Prospective cohort
study, 602/112
women
Approx. 10
years
After >1 versus 0/week of self-
reported recreational PA
at baseline
None
A few times/year
A few times/
month
About once/week
More than once/
week
1.0
1.4 (0.7–2.6)
2.2 (1.2–4.0)
1.3 (0.7–2.3)
1.0 (0.6–1.6)
Total energy intake, age, stage at
diagnosis
Enger et al. [7],
2004 (USA)
Breast cancer
stage: in
situ,
localized,
regional,
distant
Cancer
mortality
Follow-up of a
population-based
case–control study,
717/251 women
10.4 years Before 3.8+ versus 0 h/week of
interview-assessed
recreational PA from first
menses to reference date
0
0.1-0.70
0.8-1.6
1.7-3.7
3.8+
1.00
0.86 (0.56–1.32)
0.59 (0.35–1.01)
0.87 (0.57–1.33)
1.30 (0.81–2.09)
Age, cancer stage, BMI
Abrahamson
et al. [8],
2006 (USA)
Breast cancer
stage: local,
distant,
regional
Total
mortality
Prospective cohort
study, 1230/285
women
8.5 years Before Quartiles (Q) 4 (43.1–98.0)
versus Q1 (1.6–16.6) of
relative units/week of
interview-assessed
recreational PA during the
three periods before
diagnosis
For BMI stratification:
high versus low recent PA
(median as the cut-point)
Q1 (1.6–16.6)
Q2 (16.7–29.4)
Q3 (29.5–43.0)
Q4 (43.1–98.0)
1.0
0.84 (0.60–1.18)
0.97 (0.70–1.35)
1.16 (0.84–1.60)
Income, cancer stage (age was not
included in the final model as it
was found not be a confounder)
Haydon et al.
[21], 2006
(USA)
Colorectal
cancer,
stage: I–IV
Total
mortality,
cancer
mortality
Prospective cohort
study, total
mortality: 526/208
men and women
cancer mortality:
526/181 men and
women
5.5 years Before >1 versus 0 times/week of
interview-assessed non-
occupational PA 6 months
before baseline
Total mortality:
0 times/week
>1 times/week
Cancer mortality:
0 times/week
>1 times/week
1.00
0.77 (0.58–1.03)
1.00
0.73 (0.54–1.00)
Sex, age, cancer stage
Meyerhardt
et al. [22],
2006,
Colon cancer,
stage: III
Total
mortality
Prospective cohort
study, 832/84 men
and women
After ≥27 versus <3 MET-h/week
of self-reported
recreational PA ∼6
<3
3–8.9
9–17.9
1.00
0.85 (0.49–1.49)
0.71 (0.36–1.41)
Sex, age, depth of invasion
through bowel wall, number of
positive lymph nodes, presence
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CALGB
(USA)
months after adjuvant
therapy
18–26.9
≥27
0.71 (0.32–1.59)
0.37 (0.16–0.82)
of clinical perforation at time of
surgery, presence of bowel
obstruction at time of surgery,
baseline CEA, tumor grade,
baseline performance status,
treatment arm, weight change
between ﬁrst and second
questionnaire, BMI at time of
second questionnaire, time
between study entry and
completion of second
questionnaire
Meyerhardt
et al. [23],
2006, NHS
(USA)
Colorectal
cancer,
stage: I–III
Total
mortality,
cancer
mortality
Prospective cohort
study,
total mortality: 573/
132 women
cancer mortality: 573/
80 women
9.6 years Before,
after
≥18 versus <3 MET-h/week
of self-reported
recreational PA 6 months
before diagnosis and 1–4
years after diagnosis
Total mortality:
pre-diagnosis:
<3
3–8.9
9.0–17.9
≥18
post-diagnosis:
<3
3–8.9
9.0–17.9
≥18
Cancer mortality:
pre-diagnosis:
<3
3–8.9
9.0–17.9
≥18
post-diagnosis:
<3
3–8.9
9.0–17.9
≥18
1.0
0.85 (0.52–1.37)
1.14 (0.69–1.87)
0.95 (0.57–1.59)
1.0
0.77 (0.48–1.23)
0.50 (0.28–0.90)
0.43 (0.25–0.74)
1.0
0.83 (0.45–1.53)
1.05 (0.56–1.99)
0.86 (0.44–1.67)
1.0
0.92 (0.50–1.69)
0.57 (0.56–1.20)
0.39 (0.18–0.82)
Age at diagnosis, BMI, change in
BMI before and after diagnosis,
cancer stage, cancer grade,
colon or rectal primary, year of
diagnosis, receipt of
chemotherapy, time from
diagnosis to PA measurement,
smoking status
Dal Maso et al.
[9], 2008
(Italy)
Breast cancer,
stage: I–IV
Total
mortality,
cancer
mortality
Follow-up of a
multicenter
hospital-based case–
control study,
total mortality:
1380/478 men and
women
cancer mortality:
1380/376
12.6 years Before ≥2 versus <2 h/week of
recent self-reported
recreational PA at baseline
Total mortality:
<2
≥2
Cancer mortality:
<2
≥2
1.0
0.82 (0.67–1.01)
1.0
0.85 (0.68–1.07)
Region of residence, age at
diagnosis, year at diagnosis,
TNM stage, ER/PR status
Continued
Volume25|No.7|July2014doi:10.1093/annonc/mdu012|
AnnalsofOncologyreviews

Table 1. Continued
Author, year,
(country)
Cancer type,
stage
cases, sex
Follow-up
duration
PA before/
after
diagnosis
measurement
Holick et al.
[10], 2008
(USA)
Breast cancer,
stage: local,
regional
Total
mortality,
cancer
mortality
Follow-up of three
population-based
case–control studies,
total mortality:
4482/412 men and
women
cancer mortality:
4482/109 men and
women
6 years After ≥21.0 versus <2.8 MET-h/
week of self-reported
recent recreational PA
after diagnosis
≥8.0 versus <8.0 MET-h/
week
Total mortality:
<2.8
2.8- 7.9
8.0-20.9
≥21.0
Cancer mortality:
<2.8
2.8-7.9
8.0- 20.9
≥21.0
1.0
0.58 (0.45–0.76)
0.53 (0.40–0.69)
0.44 (0.32–0.60)
1.0
0.65 (0.39–1.08)
0.59 (0.35–1.01)
0.51 (0.29–0.89)
Age at diagnosis, cancer stage at
diagnosis, state of residence at
diagnosis, interval between
diagnosis and PA assessment,
post-diagnosis BMI, post-
diagnosis menopausal status,
post-diagnosis HRT, total
energy intake in the year before
enrollment in the study,
education level at diagnosis,
family history of breast cancer
at diagnosis, initial treatment
modality
Irwin et al. [11],
2008 (USA)
Breast cancer,
stage: local,
regional
Total
mortality,
cancer
mortality
Prospective cohort
study,
164 women
cancer mortality:
933/115 women
6 years Before,
after
≥9 versus 0 MET-h/week of
interview-assessed
recreational PA 1 year
before diagnosis and 3
Total mortality:
pre-diagnosis:
0
0–8.9
≥9
post-diagnosis:
0
0–8.9
≥9
Cancer mortality:
pre-diagnosis:
0
0–8.9
≥9
post-diagnosis:
0
0–8.9
≥9
1.0
1.14 (0.75–1.74)
0.69 (0.45–1.06)
1.0
0.36 (0.17–0.73)
0.33 (0.15–0.73)
1.0
1.31 (0.80–1.85)
0.83 (0.49–1.38)
1.0
0.72 (0.28–1.85)
0.65 (0.23–1.87)
Age, race, cancer stage, initial
treatment, tamoxifen use (post-
diagnosis: additionally adjusted
for BMI, fruit/vegetable
servings per day)
Friedenreich
et al. [12],
2009
(Canada)
Breast cancer,
stage: 0–III
Total
mortality,
cancer
mortality
Prospective cohort
study,
total mortality:
1225/341 women
cancer mortality:
1225/225 women
8.3 years Before >19 versus ≤5 MET-h/week/
year of interview-assessed
lifetime recreational PA
before diagnosis
Total mortality:
≤5
>5≤10
>10≤19
>19
Cancer mortality:
≤5
>5≤10
1.0
0.66 (0.48–0.89)
0.71 (0.52–0.97)
0.73 (0.53–1.00)
1.0
0.68 (0.47–0.98)
Occupational activity, household
activity, age, tumor stage,
treatment, Scarff-Bloom-
Richardson grade, (total
mortality: additionally adjusted
for WHR, HRT use, oral
contraceptive use, weight gain
since age 20, total pack-years of
smoking for current and former
|SchmidandLeitzmannVolume25|No.7|July2014

>10≤19
>19
0.65 (0.45–0.94)
0.54 (0.36–0.79)
smokers; for cancer mortality:
additionally for PR status,
WHR, HRT use)
Meyerhardt
et al. [24],
2009 (USA)
Colorectal
cancer,
stage: I–III
Total
mortality,
cancer
mortality
Prospective cohort
study,
258 men
cancer mortality:
661/88 men
8.6 years After >27 versus ≤ 3 MET-h/week
of self-reported
recreational PA 4 months
to 4 years after diagnosis
Total mortality:
≤3
3.1–9
9.1–18
18.1–27
>27
Cancer mortality:
≤3
3.1–9
9.1–18
18.1–27
>27
1.0
1.0 (0.68–1.48)
1.12 (0.74–1.70)
0.74 (0.46–1.20)
0.59 (0.41–0.86)
1.0
1.06 (0.55–2.08)
1.30 (0.65–2.59)
0.76 (0.33–1.77)
0.47 (0.24–0.92)
Age at diagnosis, cancer stage,
cancer grade, colon or rectal
primary, year of diagnosis, BMI,
time from diagnosis to PA
measurement, change in BMI
before and after diagnosis,
smoking status
West-Wright
et al. [13],
2009 (USA)
Breast cancer,
stage:
localized,
non-
localized
Total
mortality,
cancer
mortality
Prospective cohort
study,
total mortality:
3539/460 women
cancer mortality:
3539/221 women
38.5
months
Before >3 h versus >0.5 h/week/y of
recent PA (combined
moderate and strenuous
PA) 3 years before study
entry
Total mortality:
>0.5
>0.5-≤3
>3
Cancer mortality:
>0.5
>0.5-≤3
>3
1.0
0.83 (0.65–1.07)
0.73 (0.55–0.96)
1.0
0.65 (0.45–0.93)
0.53 (0.35–0.80)
Age, race, BMI, total energy
intake, number of comorbid
conditions, ER status
Emaus et al.
[14], 2010
(Denmark)
Breast cancer,
stage: I–IV
Total
mortality,
cancer
mortality
Prospective cohort
study,
total mortality:
1364/429 women
cancer mortality:
1364/355 women
8.2 years Before Hard versus sedentary self-
in the year preceding a
screening mammogram
regular versus sedentary
recent recreational PA
Total mortality:
Sedentary
Moderate
Hard
Cancer mortality:
Sedentary
Moderate
Hard
1.0
0.88 (0.70–1.11)
0.74 (0.51–1.08)
1.0
0.92 (0.71–1.19)
0.75 (0.49–1.15)
Age at diagnosis, pre-diagnostic
observation time, tumor stage,
region of residence, calendar
year before and after 1995, BMI
Hellmann et al.
[15], 2010
(Denmark)
Breast cancer,
stage: local,
regional,
metastatic
Total
mortality,
cancer
mortality
Prospective cohort
study,
323 women
cancer mortality:
420/178 women
7.8 years Before >4 versus 0 h/week self-
before diagnosis
Total mortality:
Inactive
2–4 h/week
>4 h/week
Cancer mortality:
Inactive
2–4 h/week
>4 h/week
1.00
1.07 (0.77–1.49)
1.00 (0.69–1.45)
1.00
0.83 (0.55–1.27)
1.01 (0.62–1.63)
Alcohol intake, smoking, BMI,
HRT, age, cancer stage,
menopausal status, parity,
education, adjuvant treatment
Keegan et al.
[16], 2010
(USA )
Breast cancer Total
mortality
Prospective cohort
study, 3833/605
women
7.8 years Before >46.0 versus ≤6.7 MET-h/
week of self-reported
recreational PA three years
Total mortality:
Q1: ≤6.7
Q2: 6.8–16.3
1.00
0.86 (0.76–1.11)
Study center, age of diagnosis,
race/ethnicity, number of
affected nodes, BMI, time since
Continued
Volume25|No.7|July2014doi:10.1093/annonc/mdu012|

Table 1. Continued
Author, year,
(country)
Cancer type,
stage
cases, sex
Follow-up
duration
PA before/
after
diagnosis
measurement
before diagnosis
for BMI stratification: 17.7
versus 0 MET-h/week
Q3: 16.4–26.1
Q4: 26.2–46.0
Q5 > 46.0
0.84 (0.46–1.10)
0.88 (0.68–1.14)
0.93 (0.72–1.21)
last full pregnancy, ER status,
PR status, tumor grade, tumor
size, tumor type
Baade et al.
[25], 2011
(Australia)
Colorectal
cancer,
stage: I–III
Total
mortality,
cancer
mortality
Prospective cohort
study,
total mortality:
1825/462 men and
women
cancer mortality:
1825/345
4.9 years After Sufficiently active total PA
versus sedentary 5 months
after diagnosis
Total mortality:
Sedentary
Insufficiently
active
Sufficiently active
Cancer mortality:
Sedentary
Insufficiently
active
Sufficiently active
1.00
0.72 (0.57–0.91)
0.75 (0.60–0.94)
1.00
0.90 (0.69–1.17)
0.88 (0.68–1.15)
Sex, age, BMI, smoking status,
marital status, education level,
private health insurance, site,
stage of disease, treatment,
comorbidities
Irwin et al. [17],
2011 (USA)
Breast cancer Total
mortality,
cancer
mortality
Prospective cohort
study,
total mortality:
4643/350 women
cancer mortality:
4643/194 women
3.3 years Before,
after
9+ versus 0 MET-h/week of
self-reported recreational
MVPA at baseline (pre-
diagnosis PA) and 3 or 6
For BMI stratification: >0
versus 0 MET-h/week
Total mortality:
pre-diagnosis:
0
1–3.0
3.1–8.9
9+
post-diagnosis:
0
1–3.0
9+
Cancer mortality:
pre-diagnosis:
0
1–3.0
3.1–8.9
9+
post-diagnosis:
0
1–3.0
3.1–8.9
9+
1.00
0.81 (0.56–1.16)
0.67 (0.50–0.91)
0.61 (0.47–0.81)
1.00
0.72 (0.48–1.07)
0.54 (0.38–0.79)
1.00
0.83 (0.51–1.37)
0.82 (0.55–1.22)
0.71 (0.49–1.03)
1.00
0.30 (0.09–0.99)
0.77 (0.43–1.38)
0.61 (0.35–0.99)
Age, ethnicity, study arm, previous
HRT, BMI, diabetes, alcohol,
smoking, intakes of total
energy, percent energy from fat,
and servings of fruits and
vegetables (post-diagnosis:
additionally adjusted for stage,
ER, PR, grade, HER2, time from
diagnosis to PA assessment)
Cleveland et al.
[18], 2012
(USA)
Breast cancer Total
mortality,
cancer
mortality
Prospective cohort
study,
total mortality:
1451/192 women
66.7
months
Before ≥ 9 versus 0 MET-h/week of
interview-assessed lifetime
recreational PA before
diagnosis
Total mortality:
0
>0 to <9
≥9
1.00
0.59 (0.42–0.82)
0.57 (0.39–0.83)
Age at diagnosis, BMI,
menopausal status
|SchmidandLeitzmannVolume25|No.7|July2014

cancer mortality:
1225/120 women
Cancer mortality:
0
1.00
>0 to <9
≥9
0.61 (0.40–0.92)
0.66 (0.42–1.06)
Beasley et al.
[19], 2012
(USA, China)
Breast cancer Total
mortality,
cancer
mortality
Four prospective
cohort studies,
total mortality:
11 315/1468 women;
Cancer mortality:
11 282/971 women
Not
provided
After 36.5 versus 0 MET-h/week of
recreational PA 18–48
months after diagnosis
for BMI and menopausal
status stratiﬁcation: ≥10.0
versus<10.0 MET-h/week
Total mortality:
0 MET-h/week
3.7 MET-h/week
10.0 MET-h/
week
18.7 MET-h/
week
36.5 MET-h/
week
1.00
0.90 (0.77–1.04)
0.77 (0.66–0.90)
0.71 (0.60–0.84)
0.60 (0.51–0.72)
Age at diagnosis, race, menopausal
status, TNM stage, hormone
receptor status, treatment, post-
diagnosis BMI, smoking status
Kuiper et al.
[26], 2012
(USA)
Colorectal
cancer,
stage:
localized,
regional
Total
mortality,
cancer
mortality
Multicenter
prospective
cohort study,
total mortality:
1339/265 women
cancer mortality:
1339/171 women
11.9 years Before,
after
≥18 versus 0 MET-
h/week of self-report-
assessed recreational PA
∼5.6 years before
diagnosis and 1.5 years
after diagnosis
Total mortality:
Pre-diagnosis:
0
>0–2.9
3.0–8.9
9.0–17.9
≥18.0
post-diagnosis:
0
>0–2.9
3.0–8.9
9.0–17.9
≥18.0
Cancer mortality:
pre-diagnosis:
0
>0–2.9
3.0–8.9
9.0–17.9
≥18.0
post-diagnosis:
0
>0–2.9
3.0–8.9
9.0–17.9
≥18.0
1
0.93 (0.61–1.43)
1.01 (0.71–1.43)
0.77 (0.52–1.12)
0.63 (0.42–0.96)
1
0.71 (0.40–1.30)
0.42 (0.23–0.77)
0.57 (0.31–1.07)
0.41 (0.21–0.81)
1.00
0.98 (0.58–1.66)
1.01 (0.65–1.57)
0.74 (0.46–1.20)
0.68 (0.41–1.13)
1.00
0.49 (0.21–1.14)
0.30 (0.12–0.73)
0.53 (0.22–1.25)
0.29 (0.11–0.77)
Age at diagnosis, study arm, BMI
(post-diagnosis, pre-diagnosis),
tumor stage, ethnicity,
education, alcohol, smoking,
and HRT (post-diagnosis:
additionally adjusted for time
from diagnosis to
measurement)
Campbell et al.
[27], 2013
(USA)
Colorectal
cancer,
stage:
Total
mortality,
Prospective cohort
study,
total mortality:
6.8 years Before,
after
≥8.75 versus
<3.5 MET-h/week of
recreational PA
Total mortality:
pre-diagnosis:
<3.5 1.00
Age at diagnosis, smoking status,
BMI, red meat intake, cancer
Continued
Volume25|No.7|July2014doi:10.1093/annonc/mdu012|

Table 1. Continued
Author, year,
(country)
Cancer type,
stage
cases, sex
Follow-up
duration
PA before/
after
diagnosis
measurement
localized,
regional
cancer
mortality
2293/846 men and
women
cancer mortality:
2293/379 men and
women
assessed 7 years before
diagnosis and 1.7 and 2.3
3.5–8.74
≥8.75
post-diagnosis:
<3.5
3.5–8.74
≥8.75
Cancer mortality:
pre-diagnosis:
<3.5
3.5–8.74
≥8.75
post-diagnosis:
<3.5
3.5–8.74
≥8.75
0.69 (0.55 –0.85)
0.72 (0.58 –0.89)
1.00
0.78 (0.60 –1.00)
0.58 (0.47 –0.71)
1.00
0.68 (0.49–0.95)
0.78 (0.57–1.08)
1.00
1.00 (0.64–1.56)
0.87 (0.61 –1.24)
stage, leisure-time spent sitting,
education
Schmidt et al.
[20], 2013
(Germany)
Breast cancer,
stage: I–IIIa
Total
mortality,
cancer
mortality
Prospective cohort
study,
total mortality:
3393/367 women
cancer mortality:
3393/243 women
5.6 years Before ≥42 versus 0 MET-
h/week of recent recreational
PA assessed at ≥50 years of
age until diagnosis
For BMI stratiﬁcation: any
versus no PA
Total mortality:
0
>0 to <12
12 to <24
24 to <42
≥42
1.00
0.67 (0.50–0.90)
0.76 (0.55–1.04)
0.77 (0.56–1.07)
0.66 (0.47–0.92)
Tumor size, nodal status, tumor
grade, ER/PR status,
radiotherapy, screen-detected
tumor, HT use at diagnosis, age
at diagnosis, BMI pre-diagnosis,
smoking status and pack-years,
pre-existing angina pectoris (for
total mortality: additionally
adjusted for pre-existing
hypertension, previous stroke,
and insulin therapy)
RR, relative risk; CI, conﬁdence interval; PA, physical activity; MVPA, moderate to vigorous physical activity; MET, metabolic equivalent of task; BMI, body mass index; WHR, waist to hip ratio; HRT,
hormone replacement therapy; CEA, carcinoembryonic antigen; ER, estrogen receptor; PR, progesterone receptor.
|SchmidandLeitzmannVolume25|No.7|July2014

diagnosis physical activity and breast cancer mortality among
post-menopausal women (RR = 0.71; 95% CI = 0.62–0.82) than
pre-menopausal women (RR = 0.96; 95% CI = 0.74–1.23)
(Pdifference = 0.04).
dose–response relation between physical activity and total
mortality and cancer mortality. Each 5, 10, or 15 MET-h/week
increase in pre-diagnosis physical activity was related to a 7%
(95% CI = 2–12%), 13% (95% CI = 4–21%), and 19% (95%
CI = 6–30%) reduction in risk of total mortality among breast
cancer survivors, respectively (Table 3). Each 5, 10, or 15 MET-
h/week increase in post-diagnosis physical activity was
associated with a 13% (95% CI = 6–20%), 24% (95% CI = 11–
36%), and 34% (95% CI = 16–38%) decreased risk of total
mortality, respectively. The risk estimates for increments of 5,
10, or 15 MET-h/week in pre-diagnosis physical activity in
relation to cancer mortality among breast cancer survivors were
similar to those seen for total mortality (Table 3). Each 5, 10, or
15 MET-h/week increase in post-diagnosis physical activity
revealed a 6% (95% CI = 3–8%), 11% (95% CI = 6–15%), and
0.25 0.50 1.00 2.00 4.00
Relative risk (log scale)
Baade et al., 2011 (men and women)
Meyerhardt et al., 2009 (men)
Campbell et al., 2013 (women and men)
Meyerhardt et al., 2006, NHS (women)
Kuiper et al., 2012 (women)
Meyerhardt et al., 2006, CALGB (men and women)
Meyerhardt et al., 2006, NHS (women)
Haydon et al., 2006 (men and women)
Beasley et al., 2012 (women)
Irwin et al., 2011 (women)
Holick et al., 2008 (women)
Abrahamson et al., 2006 (women)
Hellmann et al., 2010 (women)
Keegan et al., 2010 (women)
Dal Maso et al., 2008 (women)
Emaus et al., 2010 (women)
West−Wright et al., 2009 (women)
Friedenreich et al., 2009 (women)
Schmidt et al., 2013 (women)
Cleveland et al., 2012 (women) 0.57 [0.39, 0.83]
0.61 [0.47, 0.81]
0.66 [0.47, 0.92]
0.69 [0.45, 1.06]
0.73 [0.53, 1.00]
0.73 [0.55, 0.96]
0.74 [0.51, 1.08]
0.82 [0.67, 1.01]
0.93 [0.72, 1.21]
1.00 [0.69, 1.45]
1.16 [0.84, 1.60]
0.33 [0.15, 0.73]
0.44 [0.32, 0.60]
0.54 [0.38, 0.79]
0.60 [0.51, 0.72]
0.63 [0.42, 0.96]
0.72 [0.58, 0.89]
0.77 [0.58, 1.03]
0.95 [0.57, 1.59]
0.37 [0.16, 0.82]
0.41 [0.21, 0.81]
0.43 [0.25, 0.74]
0.58 [0.47, 0.71]
0.59 [0.41, 0.86]
0.75 [0.60, 0.94]
Authors, year (Gender) Relative risk [95% CI]
Breast cancer (pre−diagnosis PA)
Breast cancer (post−diagnosis PA)
Colorectal cancer (pre−diagnosis PA)
Colorectal cancer (post−diagnosis PA)
0.77 [0.69, 0.88]Random effects model
Figure 2. Forest plot of the relation between physical activity (PA) and total mortality stratiﬁed by cancer site.
Volume 25 | No. 7 | July 2014 doi:10.1093/annonc/mdu012 | 

16% (95% CI = 9–22%) reduction in risk of cancer mortality
among breast cancer survivors, respectively.
colorectal cancer survivors
pre- and post-diagnosis physical activity. Colorectal cancer
survivors with high versus low levels of pre-diagnosis physical
activity showed decreased risks of total mortality (RR = 0.74; 95%
CI = 0.63–0.86) and colorectal cancer mortality (RR = 0.75; 95%,
CI = 0.62–0.91; Figures 2 and 3). No heterogeneity among studies
was observed (total mortality: I² = 0%; Pheterogeneity = 0.66; cancer
mortality: I2
= 0%; Pheterogeneity = 0.94). High versus low post-
diagnosis physical activity showed strong risk reductions for both
total mortality (RR = 0.58; 95% CI = 0.48–0.70) and colorectal
cancer mortality (RR = 0.61; 95% CI = 0.40–0.92). For total
mortality, no signiﬁcant heterogeneity among studies was
observed (I2
= 40%; Pheterogeneity = 0.16), whereas there was some
evidence of heterogeneity among studies for colorectal cancer
mortality (I2
= 69%; Pheterogeneity = 0.03). After removal of the
0.25 0.50 1.00 2.00 4.00
Baade et al., 2011 (men and women)
Meyerhardt et al., 2009 (men)
Meyerhardt et al., 2006 (women)
Haydon et al., 2006 (men and women)
Borugian et al., 2004 (women)
Beasley et al., 2012 (women)
Holick et al., 2008 (women)
Hellmann et al., 2010 (women)
Rohan et al., 1995 (women)
Dal Maso et al., 2008 (women)
Schmidt et al., 2013 (women)
Enger et al., 2004 (women)
Emaus et al., 2010 (women)
Cleveland et al., 2012 (women)
Friedenreich et al., 2009 (women)
West−Wright et al., 2009 (women) 0.53 [0.35, 0.80]
0.54 [0.36, 0.79]
0.66 [0.42, 1.06]
0.71 [0.49, 1.03]
0.75 [0.49, 1.15]
0.78 [0.45, 1.34]
0.80 [0.53, 1.21]
0.83 [0.49, 1.38]
0.85 [0.68, 1.07]
0.98 [0.50, 1.94]
1.01 [0.62, 1.63]
0.51 [0.29, 0.89]
0.61 [0.35, 0.99]
0.65 [0.23, 1.87]
0.73 [0.59, 0.91]
1.00 [0.60, 1.60]
0.68 [0.41, 1.13]
0.73 [0.54, 1.00]
0.78 [0.57, 1.08]
0.86 [0.44, 1.67]
0.29 [0.11, 0.77]
0.39 [0.18, 0.82]
0.47 [0.24, 0.92]
0.87 [0.61, 1.24]
0.88 [0.68, 1.15]
Breast cancer (pre−diagnosis PA)
Breast cancer (post−diagnosis PA)
Colorectal cancer (pre−diagnosis PA)
Colorectal cancer (post−diagnosis PA)
Figure 3. Forest plot of the relation between physical activity (PA) and cancer mortality stratiﬁed by cancer site.
 | Schmid and Leitzmann Volume 25 | No. 7 | July 2014

Kuiper et al. study [26] (lowest risk estimate) from this analysis,
the heterogeneity was no longer statistically significant
(Pheterogeneity = 0.08). The funnel plot, Egger’s test (P = 0.48),
and Begg’s test (P = 0.11) indicated no evidence for publication
bias for total mortality. For the post-diagnosis physical activity
and colorectal cancer mortality relation, visual inspection of the
funnel plot revealed asymmetry and Egger’s and Begg’s tests
were both statistically significant (Egger’s test: P = 0.001; Begg’s
test: P = 0.02). Omission of one study at a time did not
materially alter the results (S1 for total mortality, S2 for cancer
mortality). Examining only studies that measured post-
diagnosis physical activity within 1–2 years after colorectal
cancer diagnosis did not appreciably alter the findings (total
mortality: RR = 0.53; 95% CI = 0.42–0.67; cancer mortality:
RR = 0.51; 95% CI = 0.26–1.03).
Dose–response relation between physical activity and total
mortality and cancer mortality. Each 5, 10, or 15 MET-h/week
increase in pre-diagnosis physical activity was related to a 7%
(95% CI = 1–13%), 14% (95% CI = 1–25%), and 20% (95%
CI = 2–35%) reduction in risk of total mortality among
colorectal cancer survivors, respectively (Table 3). By
comparison, each 5, 10, or 15 MET-h/week increase in post-
diagnosis physical activity was associated with a 15% (95%
CI = 10–19%), 28% (95% CI = 20–35%), and 38% (95%
CI = 28–47%) lower risk of total mortality, respectively. The
dose-response analyses of pre- and post-diagnosis physical
activity in relation to cancer mortality revealed results similar
to those seen for total mortality, although relations of
pre-diagnosis physical activity to colorectal cancer mortality
were statistically non-significant (Table 3).
Table 2. Relation of physical activity to total mortality and cancer mortality among breast cancer survivors, stratified by BMI, menopausal status and
ER status
Stratification criterion Total mortality Cancer mortality
Number of
datasets included
RR [95% CI]
(high versus low PA)
I2
(%) *P-value Number of
datasets included
RR [95% CI]
I2
(%) *P-value
Pre-diagnosis PA
BMI
<25 kg/m² 6 0.70 [0.55, 0.89] 52 3 0.77 [0.58, 1.04] 0
≥25 kg/m² 6 0.77 [0.64, 0.92] 0 0.54 3 0.65 [0.37, 1.16] 65 0.53
Menopausal status
Pre-menopausal 3 0.67 [0.36, 1.25] 33 4 1.03 [0.71, 1.48] 15
Post-menopausal 3 0.75 [0.54, 1.05] 44 0.80 3 0.68 [0.47, 0.99] 0 0.10
Tumor ER status
ER positive 2 0.72 [0.56, 0.92] 0 1 0.46 [0.26, 0.80] -
ER negative 2 0.62 [0.20, 1.91] 83 0.85 1 0.33 [0.13, 0.83] - -
Post-diagnosis PA
BMI
<25 kg/m² 3 0.64 [0.48, 0.86] 27 2 0.73 [0.61, 0.87] 0
≥25 kg/m² 3 0.60 [0.39, 0.93] 53 0.99 2 0.74 [0.66, 0.84] 0 0.85
Menopausal status
Pre-menopausal 1 0.84 [0.68, 1.03] - 2 0.94 [0.60, 1.49] 43
Post-menopausal 1 0.70 [0.62, 0.79] - - 2 0.71 [0.61, 0.83] 0 0.18
Tumor ER status
ER positive 3 0.46 [0.23, 0.92] 89 1 0.79 [0.67, 0.93] -
ER negative 3 0.73 [0.59, 0.89] 0 0.28 1 0.66 [0.52, 0.84] - -
Pre- and post-diagnosis PA
combined
BMI
<25 kg/m² 9 0.68 [0.58, 0.81] 42 5 0.74 [0.64, 0.86] 0
≥25 kg/m² 9 0.74 [0.65, 0.84] 0 0.57 5 0.70 [0.57, 0.87] 28 0.92
Menopausal status
Pre-menopausal 4 0.82 [0.68, 0.98] 0 6 0.96 [0.74, 1.23] 25
Post-menopausal 4 0.72 [0.63, 0.81] 6 0.21 5 0.71 [0.62, 0.82] 0 0.04
Tumor ER status
ER positive 5 0.60 [0.45, 0.81] 75 2 0.64 [0.39, 1.08] 70
ER negative 5 0.74 [0.53, 1.03] 39 0.42 2 0.54 [0.29, 1.00] 51 0.68
RR, relative risk; CI, confidence interval; PA, physical activity; BMI, body mass index; ER, estrogen receptor.
*The P-values for difference across strata were obtained using meta-regression comparing the model including the stratification variable as explanatory
variable with the null model not including any explanatory variables.
Volume 25 | No. 7 | July 2014 doi:10.1093/annonc/mdu012 | 

potential modifying factors
We performed subanalyses to examine whether the relations of
pre- and post-diagnosis physical activity to total mortality
among survivors of breast or colorectal cancers were potentially
modified by the type of physical activity assessment, number of
study participants, number of cases, study geographic location,
and adjustments for tumor stage, cancer treatment, smoking,
and adiposity.
The relation of pre-diagnosis physical activity to total mor-
tality among breast cancer survivors did not differ according to
potential effect modifying variables (Table 4). The inverse asso-
ciation between post-diagnosis physical activity and total mor-
tality among breast cancer survivors appeared to be slightly
more pronounced in studies with interview-based (RR = 0.42;
95% CI = 0.32–0.57) than self-reported physical activity assess-
ments (RR = 0.59; 95% CI = 0.50–0.69), although the formal test
for heterogeneity was only borderline statistically significant
(Pdifference = 0.05).
The association between pre-diagnosis physical activity
and total mortality among colorectal cancer survivors was
not affected by potential effect modifying variables (Table 5).
The association between post-diagnosis physical activity and
total mortality among colorectal cancer survivors differed by
study geographic region (Pdifference = 0.02), with summary
RRs of 0.55 (95% CI = 0.50–0.69) and 0.75 (95% CI = 0.60,
0.94) for studies conducted in North America and Australia,
respectively. However, that effect modification was based on
only five studies from North America and one study from
Australia.
change in physical activity from pre- to
post-diagnosis
We pooled the data from three studies that provided risk esti-
mates for the relations of change in physical activity from
pre-to post-diagnosis to mortality in survivors of breast
cancer [11, 17] and colorectal cancer [22]. Compared with
survivors of breast or colorectal cancer who did not change
their physical activity level from pre- to post-diagnosis or
were inactive/insufficiently active before diagnosis, those who
increased their physical activity level showed a statistically
significant decreased risk of total mortality (RR = 0.61; 95%
CI = 0.46–0.80) and a suggestive decreased risk of cancer
mortality (RR = 0.71; 95% CI = 0.45–1.12; Figure 4). In con-
trast, individuals who decreased their physical activity level
from pre- to post-diagnosis displayed statistically non-signifi-
cant increased risks of total mortality (RR = 1.72; 95%
CI = 0.76–3.87) and cancer mortality (RR = 1.28; 95%
CI = 0.87–1.90) when compared with those who did not
change their physical activity level or were inactive/insuffi-
ciently active before diagnosis.
discussion
Our meta-analysis showed that engaging in the approximate
equivalent of 150 min of at least moderate physical activity per
week after cancer diagnosis was associated with a 24% reduced
risk of total mortality among breast cancer survivors. Among
colorectal cancer survivors, a similar dose of post-diagnosis
Table 3. Dose–response relation of physical activity to total mortality and cancer mortality among breast and colorectal survivors for an increase of 5,
10, or 15 MET-h/week of physical activity
Breast cancer survivors Colorectal cancer survivors
Number of datasets
included
RR [95% CI] of
total mortality
Number of datasets
included
RR [95% CI] of
total mortality
Total mortality
Pre-diagnosis PA
Increase of 5 MET-h/week 6 0.93 [0.89, 0.98] 3 0.93 [0.87, 0.99]
Post-diagnosis PA
Cancer mortality
Pre-diagnosis PA
Post-diagnosis PA
RR, relative risk; CI, confidence interval; PA, physical activity; MET, metabolic equivalent of task.
 | Schmid and Leitzmann Volume 25 | No. 7 | July 2014

physical activity was related to a 28% decreased risk of total
mortality. A comparable amount of physical activity performed
pre-diagnosis was related to a 13% reduced total mortality risk
among breast cancer survivors and a 14% decreased total mor-
tality risk among colorectal cancer survivors. In addition, we
found that an increase in physical activity from pre- to post-
Table 4. Relation of physical activity to total mortality among survivors of breast cancer, stratified by selected characteristics
Stratification criterion Number of
datasets included
RR [95% CI] (high
versus low PA)
I2
(%) *P- value
Pre-diagnosis physical activity
Type of physical activity assessment
Self-report 5 0.78 [0.66, 0.94] 40
Interview 6 0.76 [0.63, 0.92] 53 0.87
Number of study participants
<2000 study participants 7 0.81 [0.68, 0.95] 44
≥2000 study participants 4 0.73 [0.60, 0.88] 42 0.44
Number of cases
<350 cases 5 0.81 [0.63, 1.05] 61
≥350 cases 6 0.76 [0.67, 0.86] 19 0.53
Study geographic region
Europe 4 0.80 [0.69, 0.92] 0
North America 7 0.76 [0.63, 0.91] 57 0.76
Number of adjustment factors
>8 adjustment factors 5 0.77 [0.64, 0.93] 46
≤8 adjustment factors 6 0.78 [0.65, 0.93] 48 0.90
Adjustment for tumor stage
Adjusted for tumor stage 7 0.81 [0.71, 0.93] 31
Not adjusted for tumor stage 4 0.71 [0.56, 0.90] 53 0.32
Adjustment for cancer treatment
Adjusted for cancer treatment 4 0.75 [0.63, 0.90] 0
Not adjusted for cancer treatment 7 0.78 [0.66, 0.93] 57 0.82
Adjustment for smoking
Adjusted for smoking 4 0.72 [0.59, 0.88] 32
Not adjusted for smoking 7 0.81 [0.69, 0.94] 43 0.39
Adjustment for adiposity
Adjusted for adiposity 8 0.74 [0.65, 0.84] 27
Not adjusted for adiposity 3 0.88 [0.67, 1.15] 56 0.18
Post-diagnosis physical activity
Self-report 2 0.59 [0.50, 0.69] 0
Interview 2 0.42 [0.32, 0.57] 0 0.05
<2000 study participants 1 0.33 [0.15, 0.73] –
≥2000 study participants 3 0.54 [0.44, 0.66] 35 0.26
Number of cases
<350 cases 2 0.48 [0.32, 0.72] 17
≥350 cases 2 0.53 [0.39, 0.71] 65 0.70
Not adjusted for cancer treatment 1 0.54 [0.37, 0.79] – 0.80
Adjusted for smoking 1 0.60 [0.50, 0.72] –
RR, relative risk; CI, confidence interval; PA, physical activity
*The P-values for difference across strata were obtained using meta-regression comparing the model including the stratification variable as an
explanatory variable with the null model not including any explanatory variables.
Volume 25 | No. 7 | July 2014 doi:10.1093/annonc/mdu012 | 

diagnosis was associated with reduced risk of total mortality.
The apparent protection from total mortality afforded by
physical activity was observed in analyses with and without
adjustments for tumor stage, cancer treatment, smoking, and
adiposity, and it was evident in both large and small studies, in
studies using self-reported and interview-based physical activity
assessments, and in studies from different countries. Among
breast cancer survivors, the benefit of physical activity was
evident for both lean and overweight women, for pre- and post-
menopausal women, and for ER positive and negative tumors.
These findings strongly support current physical activity
guidelines for cancer survivors, which endorse 150 min of mod-
erate activity per week [36].
Numerous biologic mechanisms potentially explain the
observed apparent protective effect of physical activity on total
and cancer mortality among cancer survivors. For example, inter-
vention studies in breast cancer survivors show that exercise
lowers C-reactive protein and blood pressure [37], facilitates
weight loss [38], decreases insulin and insulin-like growth factors
[39], and improves immune function [40], physiologic processes
that plausibly mediate the inverse physical activity and mortality
relation in cancer survivors. In addition, physical activity lowers
Table 5. Relation of physical activity to total mortality among survivors of colorectal cancer, stratified by selected characteristics
Stratification criterion Number of
datasets included
RR [95% CI]
I2
(%) *P -value
Pre-diagnosis physical activity
Self-report 3 0.73 [0.61, 0.87] 0
Interview 1 0.77 [0.58, 1.03] – 0.74
≥2000 study participants 1 0.72 [0.58, 0.89] – 0.74
Number of cases
<350 cases 3 0.76 [0.61, 0.94] 0
≥350 cases 1 0.72 [0.58, 0.89] – 0.74
Adjusted for cancer treatment 1 0.95 [0.57, 1.59] –
Not adjusted for smoking 1 0.77 [0.58, 1.03] – 0.74
Post-diagnosis physical activity
≥2000 study participants 1 0.58 [0.47, 0.71] – 0.87
Number of cases
<350 cases 4 0.49 [0.38, 0.64] 0
≥350 cases 2 0.66 [0.51, 0.84] 64 0.11
Study geographic region
North America 5 0.55 [0.46, 0.64] 0
Australia 1 0.75 [0.60, 0.94] – 0.02
>8 of adjustment factors 5 0.55 [0.41, 0.74] 49
≤8 of adjustment factors 1 0.58 [0.47, 0.71] – 0.87
RR, relative risk; CI, confidence interval; PA, physical activity.
*The P-values for difference across strata were obtained using meta-regression comparing the model including the stratification variable as an
explanatory variable with the null model not including any explanatory variables.
 | Schmid and Leitzmann Volume 25 | No. 7 | July 2014

endogenous estrogen levels among healthy postmenopausal
women [41] and an etiologic pathway involving decreased levels
of endogenous estrogens among physically active women may
also be operative after breast cancer diagnosis. This may partly
explain the pronounced inverse relations of physical activity to
breast cancer mortality in post-menopausal women seen in our
meta-analysis.
Our ﬁndings showed that physical activity performed before
cancer diagnosis was related to reduced risks of both total and
cancer mortality. One possible explanation for the reduced risk
of mortality observed for pre-diagnosis physical activity is that
individuals who are physically active before being diagnosed
with cancer are predisposed to biologically less aggressive
tumors [22]. Moreover, pre-diagnosis physical activity may
beneﬁcially affect the treatment process because it leads to
improved functional capacity to tolerate and complete surgery
and adjuvant treatment [27].
Individuals who are physically active before diagnosis remain
physically active during the post-diagnosis period [42] as shown
by positive correlations between pre-diagnosis physical activity
0.25 0.50 1.00 2.00 4.00
Meyerhardt et al., 2006 (women) 0.51 [0.30, 0.85]
0.55 [0.22, 1.38]
0.67 [0.46, 0.96]
1.06 [0.73, 1.54]
1.23 [0.79, 1.91]
3.95 [ 1.45, 6.17]
0.48 [0.24, 0.97]
0.82 [0.29, 2.34]
0.91 [0.51, 1.64]
1.06 [0.59, 1.88]
1.32 [0.74, 2.34]
3.69 [0.88, 15.92]
Increase in PA from pre− to post−diagnosis (total mortality)
Decrease in PA from pre− to post−diagnosis (total mortality)
Increase in PA from pre− to post−diagnosis (cancer mortality)
Decrease in PA from pre− to post−diagnosis (cancer mortality)
Figure 4. Forest plot of the relations of change in physical activity (PA) from pre- to post-diagnosis to total mortality and cancer mortality.
Volume 25 | No. 7 | July 2014 doi:10.1093/annonc/mdu012 | 

and post-diagnosis physical activity among colorectal cancer
survivors (correlation coefficient: 0.4) [24] and breast cancer
survivors (correlation coefficient: 0.5) [20]. One study of breast
cancer survivors [43] that was not included in the current meta-
analysis because the study population overlapped with that
from a more recent study [19] reported that adjustment for pre-
diagnosis physical activity did not change the association
between post-diagnosis physical activity and breast cancer mor-
tality. Likewise, two studies among colorectal cancer survivors
[22, 24] adjusted for pre-diagnosis physical activity, which did
not affect the relation of post-diagnosis physical activity to colo-
rectal cancer mortality. One of those studies [22] also reported
that adjustment for pre-diagnosis physical activity did not alter
the association between post-diagnosis physical activity and
total mortality [22]. This suggests that the decreased risk of
mortality seen with post-diagnosis physical activity among
breast and colorectal cancer survivors is independent of pre-
diagnosis physical activity levels. However, none of the other
studies included in the meta-analysis herein mutually adjusted
for pre- and post-diagnosis physical activity. Thus, the inverse
relation of post-diagnosis physical activity to mortality we
observed among cancer survivors could also partly reflect the
influence of increased pre-diagnosis physical activity.
For some cancers, predominantly those with high survival
rates, the leading causes of death are often distinct from those
related to the primary cancer because with advancing age, the
risk for comorbidities increases [2, 44, 45]. Thus, enhanced
engagement in physical activity after diagnosis among cancer
survivors may exert a beneficial effect on biologic pathways
involved in the development of comorbidities, even though such
conditions may not strongly affect cancer recurrence and cancer
mortality [22].
Although individuals reduce their exercise participation
during cancer therapy [23, 42], patients report that their physic-
al function and quality of life are almost identical to the general
population 1 year after surgery [46]. After treatment, cancer
patients may be more motivated to change their behavior and to
adopt a healthy lifestyle. We found that increasing physical ac-
tivity engagement from pre- to post-diagnosis was associated
with reduced mortality risk among cancer survivors, which
emphasizes the importance of physical activity participation
after cancer treatment.
We are aware of two previous meta-analyses of the associa-
tions between physical activity and mortality among survivors
of breast cancer [28] and colorectal cancer [29]. The previous
meta-analysis of physical activity and breast cancer survival [28]
was based on six studies and did not find a statistically signifi-
cant relationship between pre-diagnosis physical activity and
breast cancer mortality but was able to report reduced risks of
total and breast cancer mortality for post-diagnosis physical ac-
tivity. Our meta-analysis included 12 additional studies [5, 6, 9,
12–20] on physical activity and breast cancer survival with
33 684 additional breast cancer cases. Moreover, we included
one article [19] that provided the most updated data from the
Nurses’ Health Study (NHS) and the Life After Cancer
Epidemiological (LACE) Study. The previous meta-analysis of
physical activity and colorectal cancer survival reported inverse
relations of both pre- and post-diagnosis physical activity to total
and colorectal cancer mortality [29]. Our finding of an inverse
association between post-diagnosis physical activity and colorec-
tal cancer mortality should be interpreted with caution because
we found evidence for publication bias regarding that relation.
The primary strength of our meta-analysis is its comprehen-
siveness which included three issues not dealt with in previous
meta-analyses [28, 29]: (1) quantification of the amount of
physical activity needed for protection against mortality among
cancer survivors; (2) examination of change in physical activity
from pre- to post-diagnosis in relation to mortality among
cancer survivors; (3) performance of meta-regression to evaluate
potential sources of heterogeneity among studies. Further
strengths of our meta-analysis are that it focused on well-
designed prospective studies and that it was characterized by a
large sample size, yielding valid and precise summary RRs for
physical activity.
One potential limitation of our meta-analysis is that the asso-
ciations reported in individual studies may have been hampered
by reverse causality which could have occurred if cancer patients
had been less physically active due to symptoms of the disease at
the time of physical activity assessment. However, studies that
excluded cancer patients shortly before or after cancer diagnosis
in sensitivity analyses reported that results were not materially
altered by that procedure [11, 22, 24]. In addition, we performed
separate meta-analyses that were restricted to studies with post-
diagnosis physical activity measured within 1–2 years of breast
or colorectal cancer diagnosis. We observed no change in the
results, indicating that our findings are not likely due to the
effects of reverse causation. An additional shortcoming of our
study is variability in the range of physical activity levels
reported in the individual studies. We found no meaningful het-
erogeneity among studies regarding the associations between
pre- and post-diagnosis physical activity and total mortality
among breast and colorectal cancer survivors. Although the
studies included in our meta-analysis adjusted for numerous
confounding variables, we cannot rule out potential residual
confounding or confounding by unmeasured factors, such as
adherence to therapy. However, because the summary risk esti-
mates for physical activity in our meta-analysis did not appre-
ciably differ among studies that adjusted for cancer therapy,
tumor stage, and adiposity, and those that did not, we assume
that such confounding would not be substantial.
An additional potential limitation of our study is measure-
ment error associated with self-reported or interview-based
physical activity assessments. However, because the physical ac-
tivity data were gathered before the occurrence of death, any
random measurement error in physical activity assessment
would tend to underestimate the association between physical
activity and mortality.
In summary, we found that engaging in physical activity before
or after cancer diagnosis was associated with statistically signifi-
cant decreased risks of total and cancer mortality among breast
and colorectal cancer survivors. We also observed that an increase
in physical activity from pre- to post-diagnosis was associated
with reduced risk of cancer mortality. Future studies should
examine how physical activity participation could best be incor-
porated into daily routines after cancer treatment. In the mean-
time, physicians should consider counseling cancer survivors to
adopt a physically active lifestyle, taking into account the medical
and physical condition of their cancer patients.
 | Schmid and Leitzmann Volume 25 | No. 7 | July 2014

disclosure
The authors have declared no conflicts of interest.
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