Case-Control Study of Lifetime Physical Activity and Breast Cancer Risk
C. M. Friedenreich1,
H. E. Bryant1 and
K. S. Courneya2
1 Division of Epidemiology, Prevention and Screening, Alberta Cancer Board, Calgary, Alberta, Canada.
2 Faculty of Physical Education and Recreation, University of Alberta, Edmonton, Alberta, Canada.
 |
ABSTRACT
|
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A population-based case-control study of 1,233 incident breast cancer cases and 1,237 controls was conducted in Alberta, Canada, in 19951997 to examine the effect of lifetime physical activity patterns on breast cancer risk. No associations between physical activity and breast cancer were found for premenopausal women. For postmenopausal women in the highest quartile (
161 metabolic equivalent (MET)-hours/week per year) versus the lowest quartile (<104.8 MET-hours/week per year) of lifetime total physical activity, the adjusted odds ratio was 0.70 (95% confidence interval (CI): 0.52, 0.94). When the risks associated with each type of activity were examined for postmenopausal women, household and occupational activity conferred the largest risk reductions (odds ratio (OR) = 0.57, 95% CI: 0.41, 0.79 and OR = 0.59, 95% CI: 0.44, 0.81, respectively, for highest vs. lowest quartiles of activity), while recreational activity was not associated with any risk reductions. For postmenopausal women, the authors found stronger risk reductions for those who were also nonsmokers (OR = 0.64, 95% CI: 0.46, 0.88), non-alcohol-drinkers (OR = 0.39, 95% CI: 0.11, 0.77), or nulliparous (OR = 0.22, 95% CI: 0.07, 0.70) when they compared the highest with the lowest quartile of lifetime total physical activity. This study provides evidence that lifetime total activity reduces risk of postmenopausal breast cancer.
breast neoplasms; case-control studies; exercise; occupations; questionnaires
Abbreviations:
BMI, body mass index; CI, confidence interval; MET, metabolic equivalent; OR, odds ratio
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INTRODUCTION
|
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Evidence for an association between physical activity and breast cancer is accumulating rapidly; 23 of 35 studies (1
































35
) conducted thus far demonstrated a reduction in breast cancer risk for those women whose participation in occupational and/or recreational activities was the most active. The strength of the relation ranges from slight increases in risk found in two studies (3
, 5
) to no effect in 10 studies (6
, 10
, 11
, 14
, 18
, 22
, 24
, 27
, 31
, 34
) to 1070 percent decreases in the remaining 23 studies (1
, 2
, 4
, 7
9
, 12
, 13
, 15
17
, 19
21
, 23
, 25
, 26
, 28
30
, 32
, 33
, 35
). A dose-response relation was found in 15 (5
, 8
, 9
, 13
, 15
17
, 20
, 21
, 25
, 26
, 28
, 30
, 32
, 35
) of 23 studies (3
, 5
, 8
10
, 13


17
, 20
, 21
, 23







32
, 35
) that examined the trend. Given that the evidence for a protective effect of physical activity on breast cancer risk is either nonexistent or sometimes not very strong in these studies, reasons for the lack of consistency of effect need to be considered. Inconsistencies across these studies can be attributed to error in the measurement of physical activity, uncontrolled confounding, and incomplete assessment of effect modification, all of which influenced the majority of the studies conducted to date (36
). Indeed, the effect of physical activity on breast cancer risk appears to be more evident in those studies that had more complete, reliable assessments of physical activity; that controlled appropriately for possible confounders; and that examined the effects within subgroups of the study population. It is likely that physical activity influences breast cancer risk differentially for pre- and postmenopausal women; however, relatively few studies have examined the effects by menopausal status.
None of these previous studies examined the risk of breast cancer for all types of physical activity (e.g., occupational, household, and recreational) for entire lifetimes, assessing all parameters of physical activity (e.g., frequency, intensity, and duration). Furthermore, few of the previous studies have examined the relation between physical activity and breast cancer among subgroups of women for which different breast cancer risks may exist. Uncontrolled confounding by other risk factors also may have influenced the results of some previous studies. The association between physical activity and breast cancer risk is quite complex, reflecting the complicated and multiple biologic mechanisms that are likely operative. The present study was designed to address some of the unanswered questions regarding the type and dose of activity and the time periods in life when physical activity may be specifically associated with breast cancer risk.
 |
MATERIALS AND METHODS
|
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We conducted a population-based case-control study in Alberta, Canada, between August 1995 and August 1997. This study received ethics committee approval, and all study subjects provided written informed consent before the interview was conducted. Incident, histologically confirmed in situ and invasive cases of breast cancer were identified directly from the Alberta Cancer Registry, a population-based cancer registry that has an estimated 95 percent case ascertainment rate (37
). Cases were eligible for the study if they were Alberta residents, no older than age 80 years, English speaking, and able to complete an interview. A total of 1,764 cases were identified as potentially eligible; of these women, 182 were ineligible because of the following reasons: physician refusal (n = 32), language barrier (n = 38), having moved from a telephone number or having a disconnected telephone (n = 22), unavailability during the study period (n = 84), or death (n = 6). Of the remaining 1,582 eligible women, 1,239 (78.3 percent) completed an in-person interview, 341 refused, and 2 had incomplete interviews.
Female controls were identified through random digit dialing by using the Waksberg method (38
). Controls were frequency matched to cases on age (±5 years) and place of residence (urban/rural) and were free of any cancer diagnosis excluding nonmelanoma skin cancer. The telephone recruiters identified 2,265 women as potentially eligible, and 1,581 women (69.8 percent) agreed to receive a study package. However, 68 women could not be interviewed (they were not eligible (n = 40), had moved or had a disconnected telephone (n = 19), or were not available (n = 9)). Interviews were completed with 1,241 of the 1,513 (82.0 percent) eligible and available women who received the study package. The overall response rate for the controls was 56.5 percent (1,241/2,197). The final data set for analysis included 1,233 cases and 1,237 controls, since the data for 6 cases and 4 controls had to be excluded because of too many missing values. The final data set included 130 in situ cases and 2,340 invasive cases. No in situ cases were excluded, because there was no a priori reason to believe that physical activity would influence the risk of developing in situ cancer differently from invasive cancer. This assumption was tested in the data analysis by excluding in situ cases from the final models and comparing the results for the invasive cases with only the total case group.
 |
Data collection
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In-person interviews were conducted after permission to contact the patients was obtained from the cases' physicians. Respondents reported their menstrual and reproductive histories, hormone use history, mammography history, personal history of breast disease, breast biopsies and cancer, family history of cancer, lifetime physical activity patterns, dietary intake during the reference year, alcohol consumption, smoking habits, demographic characteristics, and past anthropometric measurements. For cases, all data obtained were current as of the date of diagnosis, and controls were assigned a comparable date. Diet during the reference year was assessed by using the National Cancer Institute's Block food frequency questionnaire (39
). Current height, weight, and waist and hip circumferences were measured by the interviewers at the end of the interview by using standardized methods.
Two recall calendars, one focusing on educational and occupational activities and the other on major life events, were mailed to the participants before the interview. These calendars, designed specifically for this study, were pilot tested with the questionnaire and were used as memory aids to improve respondent recall of lifetime physical activity. The interviewers used cognitive interviewing methods (40
, 41
) to assist the respondents in answering the questions. Several quality control measures of the interviewers' methods were incorporated into the study design.
Lifetime physical activity was estimated by using a questionnaire developed and tested for reliability in a pilot study that preceded the case-control study (42
). This questionnaire assessed occupational, household, and recreational activity separately throughout a respondent's lifetime. Recall and memory-probing aids were used, including a recall calendar and lists of examples of activities. The frequency and duration of these activities were assessed by recording the number of years, months per year, weeks per month, days per week, and hours per day that each activity was performed. The intensity of the activity was estimated by the participant as sedentary (used for occupational activities only), light, moderate, or heavy (i.e., self-reported intensity). Definitions were provided for each intensity level by type of activity, with examples for study participants. In addition to self-reported intensities, a specific metabolic equivalent (MET) value was assigned to each reported activity on the basis of the description of the activity. The MET values used were abstracted from the Compendium of Physical Activities (43
). A MET is defined as the ratio of the associated metabolic rate for a specific activity as compared with the resting metabolic rate (44
). A MET is the average seated resting energy cost for an adult and is set at 3.5 ml/kg per minute of oxygen. The variables estimated in this analysis were the average MET-hours/week per year spent in occupational, household, and recreational activity over the respondent's lifetime (refer to the Appendix). Total lifetime physical activity was estimated as the sum of occupational, household, and recreational activity.
Women were classified as postmenopausal if they stated that they were postmenopausal (n = 641) or reported that they had stopped menstruating for over a year by the reference date and their age was 50 years or more (n = 201). Those women who had had a hysterectomy were considered postmenopausal if the hysterectomy had occurred after menopause (n = 40), if they had had a bilateral oophorectomy before menopause (n = 240), if they had had symptoms of menopause after hysterectomy (n = 278), or if their current age was 55 years or more (n = 61). When this method was used, we found that 1,533 women were postmenopausal and 937 were premenopausal. We also used a stricter definition of menopausal status in which we included only those women whose age at menopause and hence their menopausal status were clearly known at the time of the interview. When we used that definition, there were 195 women of uncertain menopausal status who were excluded and 868 premenopausal women and 1,407 postmenopausal women. All analyses were completed for this restricted sample and were compared with the full data set. Since there were no substantive differences in the results obtained, the full data set was included to maximize study power.
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Statistical analysis
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Descriptive statistics were prepared to characterize the study population and to examine case-control differences. Variables were categorized into quantiles according to the distribution of the variables among the controls. Odds ratios for breast cancer were estimated by using unconditional logistic regression, and a full assessment of confounding and effect modification was conducted. Variables considered as confounders were age; body mass index (BMI) (weight/height2); waist-hip ratio; marital status; educational level; ethnicity; family history of breast cancer; whether menstruation had ever ceased for reasons besides pregnancy; irregular menstrual cycles; ever and duration of oral contraceptive use; parity and gravidity; ever breastfeeding; ever, type, and duration of hormone replacement therapy; history of benign breast disease; previous benign breast biopsy; ever alcohol consumption; ever and current cigarette smoking; total pack-years of smoking; total caloric intake; and daily dietary fat intake. Final models were adjusted for waist-hip ratio (in quartiles), educational level (in quintiles), ever use of hormone replacement therapy, history of benign breast disease, first-degree family history of breast cancer, current cigarette smoking, and ever alcohol consumption. Models of each type of activity were adjusted for the other types of activity. Possible effect modification by menopausal status, family history of breast cancer, parity, current cigarette smoking, ever alcohol consumption, and ever use of hormone replacement therapy was also examined, since these factors either have been identified previously as possible effect modifiers in other research studies (8
, 15
, 33
) or have been suggested as possible effect modifiers (36
). Tests for linear trend were performed for all models of categorized data by including the continuous, rather than the categorized, variable for each of the variables being modeled.
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RESULTS
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The cases and controls had similar sociodemographic and anthropometric characteristics as well as medical and reproductive histories (table 1). Compared with controls, cases were somewhat less educated, were less likely to have breastfed their children and to use exogenous hormones, and were more likely to have had a diagnosis of benign breast disease or a family history of breast cancer and to be ever regular and current cigarette smokers. Cases also had a higher waist-hip ratio and a higher total caloric intake. The average level of physical activity reported by cases and controls over their lifetimes was also very similar. The median activity level for cases and controls was approximately 120 MET-hours/week per year. This level of activity is equivalent to 17 MET-hours/day or 12 hours of 1.4 MET of activity per day.
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TABLE 1. Sociodemographic and anthropometric characteristics, and medical and reproductive histories, of cases and controls (n = 2,470) studied to assess the relation between lifetime physical activity and breast cancer risk, Alberta, Canada, 19951997
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Since menopausal status was an important effect modifier in these data, and because our study included women no older than age 80 years at diagnosis, all of the analyses presented in this paper were stratified on menopausal status. The multivariable-adjusted risk associated with lifetime total physical activity for the highest versus lowest quartile of activity among premenopausal women was 1.07 (95 percent confidence interval (CI): 0.72, 1.61) (table 2); for postmenopausal women, it was 0.70 (95 percent CI: 0.52, 0.94). Evidence for a trend in decreasing risk with increasing activity was found for postmenopausal women only. Some evidence for possible confounding was found in these data, since the multivariable-adjusted risks were more pronounced than the age-adjusted risks. No substantial differences were found in these risk estimates when the in situ cases were excluded. For example, the highest quartile risk estimate for premenopausal women was 1.10 (95 percent CI: 0.75, 1.61) and for postmenopausal women was 0.72 (95 percent CI: 0.53, 0.97) (data not shown). Hence, all subsequent analyses were performed by including both in situ and invasive cases.
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TABLE 2. Odds ratios for lifetime total physical activity of cases and controls (n = 2,470), by menopausal status, Alberta, Canada, 19951997
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The next analyses examined the influence of each type of activity while controlling for all other types of activity in the same multivariable model (table 3). Strong risk reductions were found for both occupational and household activity but not for recreational activity. For postmenopausal women, the risk for the highest quartile of occupational activity was 0.59 (95 percent CI: 0.44, 0.81), and for household activity it was 0.57 (95 percent CI: 0.41, 0.79). Evidence for a statistically significant trend of decreasing risk with increasing levels of physical activity was observed for both lifetime occupational and household activities.
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TABLE 3. Odds ratios for lifetime occupational, household, and recreational activity of cases and controls (n = 2,470), by menopausal status, Alberta, Canada, 19951997
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The breast cancer risks associated with lifetime total and each type of physical activity were also examined within other subgroups of the population to assess any possible effect modification. Reductions in breast cancer risk were also found for women who had not consumed alcohol in their lifetimes (table 4). Risk reductions were observed within each stratum of menopausal status, but, because of the small sample sizes among premenopausal women, there was a lack of precision around those point estimates. Postmenopausal women in the highest quartile of lifetime total physical activity who were nondrinkers had an adjusted risk of 0.29 (95 percent CI: 0.11, 0.77).
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TABLE 4. Odds ratios for lifetime total physical activity of cases and controls (n = 2,470), by alcohol consumption and menopausal status, Alberta, Canada, 19951997
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Risk reductions were observed for postmenopausal women who were not current cigarette smokers; women in the highest activity quartile had a risk of 0.64 (95 percent CI: 0.46, 0.88) (table 5). In contrast, no association between higher physical activity and breast cancer risk was observed for premenopausal women who were nonsmokers.
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TABLE 5. Odds ratios for lifetime total physical activity of cases and controls (n = 2,470), by current cigarette smoker and menopausal status, Alberta, Canada, 19951997
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There were no differences in the risks of breast cancer for these measures of physical activity among subgroups of the women stratified by first-degree family history of breast cancer and by ever use of hormone replacement therapy (data not shown). There was a greater risk decrease among postmenopausal, nulliparous women for total lifetime activity (odds ratio (OR) = 0.22, 95 percent CI: 0.07, 0.70) (table 6). When the risk was examined specifically by number of livebirths (none,
2, >2), there was no trend in decreasing risk with increasing number of livebirths (data not shown), but decreased risks were found for nulligravid women (data not shown).
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TABLE 6. Odds ratios for lifetime total physical activity of cases and controls (n = 2,470), by parity and menopausal status, Alberta, Canada, 19951997
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Breast cancer risk associated with physical activity was also examined within tertiles of BMI (<25,
25<30,
30) (table 7). No evidence was found of a benefit of physical activity for premenopausal women regardless of BMI, and there was no evidence that BMI modified the relation of physical activity with breast cancer risk.
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TABLE 7. Odds ratios for lifetime total physical activity of cases and controls (n = 2,470), by body mass index tertile and menopausal status, Alberta, Canada, 19951997
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DISCUSSION
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To our knowledge, this is the first study to examine breast cancer risk associated with all types of physical activity and total lifetime activity. We found that total lifetime activity was associated with a 30 percent reduction in breast cancer risk for postmenopausal women and that this risk decrease was attributable to occupational and household activity. No comparable risk decreases were observed for the premenopausal women in this study. We also observed greater risk reductions within particular subgroups of the population, including postmenopausal women who were nondrinkers, nonsmokers, or nulliparous. Before discussing these results, we will address limitations of this investigation.
Although this was a large population-based case-control study that included population controls, a possible selection bias was introduced because of the low response rate among controls. To address the issue of selection bias, we compared the controls with a sample of female Albertans aged 25 years or more (n = 6,146) who were included in the 19961997 National Population Health Survey conducted by Statistics Canada (45
). In that survey, respondents were asked about the frequency and duration of their current recreational activities. Controls sampled in this study were found to have current recreational activity levels comparable to those persons sampled within the Alberta component of the National Population Health Survey. Smoking prevalence rates, ever consumption of alcohol, and hormone replacement therapy use were also compared. Smoking prevalence rates were somewhat lower among our control population than the general Alberta population, but alcohol consumption and hormone use were very comparable. We considered the controls representative of the base population of Albertan women from which the cases were sampled.
Misclassification of exposure was a possibility in this study since respondents were asked to report detailed lifetime physical activity patterns. The effect of misclassification of physical activity would have been to decrease the ability of the study to demonstrate an effect of physical activity on breast cancer risk (nondifferential misclassification bias). Hence, the risk estimates that we observed may have underestimated the true effect of physical activity on breast cancer.
Despite these limitations, we were able to detect a decreased risk of breast cancer for postmenopausal women who were the most physically active during their lifetimes regarding all activities combined and for occupational and household activity. This study's results support the majority of previous investigations (1
, 2
, 4
, 7
9
, 12
, 13
, 15
17
, 19
21
, 23
, 25
, 26
, 28
30
, 32
, 33
, 35
) that found decreased risks with increased levels of physical activity. The one previous study (33
) that stratified persons into quartiles of combined occupational and recreational activities found the largest risk reductions when information on both types of activity was combined. We know of no other study that has yet combined information on the frequency, duration, and intensity of all types of activity into one total activity variable. The Verloop et al. (33
) study suggests that total activity may be the most etiologically relevant variable to assess.
Some interesting subgroup effects were noted in this investigation, suggesting that physical activity may have a greater effect for women who are postmenopausal, nulliparous, alcohol abstainers, and nonsmokers. Some studies have found larger risk reductions for premenopausal women (7
, 8
, 16
, 20
, 25
, 28
) or postmenopausal women (21
, 26
), while others have observed no differences in the level of risk reductions by menopausal status or by age (19
, 23
, 24
, 27
, 32
). Bernstein et al. (15
), in their study of women no older than age 40 years, and Carpenter et al. (30
), in their investigation of women aged 5564 years, observed strong risk reductions for both of these age groups. In contrast, Rockhill et al. observed risk reductions only in the older (12
) but not younger cohort (10
) of nurses from the Nurses' Health Studies. Although there is no consistency regarding when in life physical activity influences breast cancer risk, it would be biologically plausible that physical activity might exert more influence after menopause in controlling postmenopausal obesity, which is an established risk factor for breast cancer.
The data on the influence of parity and physical activity on breast cancer risk are also inconsistent. Some studies have found greater risk reductions for parous (13
, 15
, 17
) or nulliparous (25
, 33
) women, while others have found no difference across strata of parity (20
). In this investigation, we found that physical activity had a stronger protective effect for women who were either nulliparous or nulligravid.
In some studies, greater risk reductions for active women were observed for those women whose BMI was low (8
, 25
, 33
), while other studies observed these risk decreases more clearly for women whose BMI was high (20
, 35
). Still other studies found no effect modification of physical activity and breast cancer by BMI (9
, 10
, 15
, 21
, 24
, 27
). Weight gain over adulthood did not influence risk for the premenopausal women participating in Nurses' Health Study II (10
), a result that is not surprising given that premenopausal obesity is not a risk factor for breast cancer (46
). In contrast, in the case-control studies by Carpenter et al. (30
) and Shoff et al. (35
) that included postmenopausal women, effect modification by weight gain over lifetime was observed. When women maintained their weight throughout adulthood, breast cancer risk was substantially reduced for those who consistently exercised at high levels throughout their lifetimes (30
, 35
).
Verloop et al. (33
) also found that women with no prior history of benign breast disease and women with a family history of breast cancer who were the most physically active experienced larger risk decreases than the women in the other strata of those variables. Our study and others that examined effect modification by family history of breast cancer (10
, 27
) and benign breast disease (10
) did not find any influence of these factors.
No known previous investigations have reported any effect modification by alcohol consumption or smoking status, as we found. Before any conclusions can be drawn about the possible influence of smoking and of alcohol consumption on the relation between physical activity and breast cancer, confirmation of these results in other studies is needed. The smoking subgroup effects may be attributable to the lower smoking prevalence rates among the control group in this study as compared with the Alberta female population (16.5 vs. 23.2 percent) (45
). In our study, 70.1 percent of the controls reported that they had ever consumed alcohol for at least 6 months during their lifetimes, whereas, in the Alberta sample, 72.5 percent of women reported regular or occasional current alcohol consumption.
Four main hypotheses exist for the underlying biologic mechanisms that may be operative regarding the association between physical activity and breast cancer (47
). These mechanisms are related to endogenous estrogen exposure, adiposity, insulin-like growth factors, and immune function. The first hypothesis suggests that physical activity may reduce lifetime exposure to sex hormones by delaying menarche, by inducing an earlier age at menopause, and by increasing anovulation, all of which are associated with lower cumulative exposure to endogenous estradiol (47
, 48
). In this study, we attempted to investigate whether early age at menarche, irregular menstrual cycles, and interruptions in menstrual cycles, besides those occurring during pregnancy and lactation, were associated with physical activity. No clear associations between any of these menstrual risk factors and physical activity were found; however, the sample sizes for some of these analyses were quite small, which may have precluded detection of any associations.
The second hypothesis is that physical activity reduces postmenopausal body weight, controls weight gain over the lifetime, and decreases abdominal adiposity, all of which have been associated with breast cancer risk (46
, 49
51
). In the full data set of our study, we found that BMI and weight gain since age 20 years were not related to breast cancer risk, while a nearly 50 percent increased risk (OR = 1.47, 95 percent CI: 1.18, 1.84) was found for women in the highest quartile of waist-hip ratio (
0.82 vs. <0.74). When the analyses were stratified by menopausal status, there was a slightly elevated risk of breast cancer among the postmenopausal women in the highest quartile of weight gain over lifetime (OR = 1.29, 95 percent CI: 0.98, 1.71). No similar risk increases were observed for BMI or for the premenopausal women for any of the variables considered. On the other hand, waist-hip ratio was particularly strongly associated with breast cancer risk for the postmenopausal women (OR = 1.62, 95 percent CI: 1.22, 2.14).
The third hypothesis is that physical activity might lower plasma concentrations of insulin-like growth factor-I, possibly mediated via a negative energy balance (47
, 52
). A positive association between plasma levels of insulin-like growth factor-I and risk of breast cancer in premenopausal women has been observed in the Nurses' Health Study (53
). To our knowledge, no epidemiologic studies have yet examined the joint effects of physical activity and insulin-like growth factors.
The final hypothesis is that moderate physical activity enhances the immune system by increasing the number of natural killer cells, circulating lymphocytes, granulocytes, monocytes, and macrophages, whereas vigorous physical activity may decrease immune function (47
, 54
). Currently, the possible role of the immune system in breast cancer carcinogenesis has not been demonstrated in any epidemiologic studies; hence, this mechanism is still speculative and in need of more investigation.
In summary, this study confirms previous research suggesting that physical activity reduces the risk of breast cancer. The risk reduction is particularly notable for occupational and household activity, for postmenopausal women, and for nondrinkers and nonsmokers. We addressed deficiencies in physical activity assessments of previous investigations by designing and using a questionnaire that measured lifetime physical activity patterns, including all types and parameters of activity. Furthermore, we measured and assessed a wide range of possible confounders and effect modifiers of the association between physical activity and breast cancer, thereby overcoming some of the other limitations of previous research. Numerous questions remain regarding the etiologic role of physical activity and breast cancer that need to be addressed in studies that examine more specifically the underlying hypothesized biologic mechanisms.
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APPENDIX
|
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Estimation of Physical Activity Variables
The physical activity variables were estimated first by type of activity and were then summed over all activities to obtain total lifetime physical activity.
 |
ACKNOWLEDGMENTS
|
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This study was funded by grants from the Canadian Breast Cancer Research Initiative
and the Alberta Cancer Board Research Initiative Program
. Dr. C. M. Friedenreich was supported by a National Health Research Scholar Award from Health Canada
. Dr. K. S. Courneya's research program is supported by the National Cancer Institute of Canada
with funds from the Canadian Cancer Society
through the CCS/NCIC Sociobehavioral Cancer Research Network.
The authors acknowledge the contribution of Kathleen Douglas-England for study coordination; Zeva Mah, Laura Godard, Mila Belic, and Doreen Mandziuk for assistance with the research project; Valerie Hudson for data cleaning; Victoria Stagg for data processing and Xuechao Chen for data analysis; Lisa Alexander, Selena Chow, Pearl Cooke, Shelley Cooper, Linda Davison, Marilyn Dickson, Carrie Lavis, Doreen Mandziuk, Hijin Park, Jodi Parrotta, and Nicole Slot for interviewing the study participants; and Dr. Colleen Maxwell for providing data analysis of the National Population Health Survey data.
 |
NOTES
|
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Reprint requests to Dr. C. M. Friedenreich, Division of Epidemiology, Prevention and Screening, Alberta Cancer Board, 1331-29 Street NW, Calgary, Alberta, Canada T2N 4N2 (chrisf{at}cancerboard.ab.ca).
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Received for publication June 22, 2000.
Accepted for publication December 20, 2000.