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© The Author 2006. Published by Oxford University Press.
ARTICLE |
Functional Limitations in Elderly Female Cancer Survivors
Affiliations of authors: Health Research Center, Department of Family and Preventive Medicine, University of Utah School of Medicine, Salt Lake City, UT (CS); Division of Epidemiology and Community Health, University of Minnesota School of Public Health, Minneapolis, MN (DL, ARF); Division of Epidemiology, University of Pennsylvania School of Medicine, Philadelphia, PA (KHS); Division of Health Services Research and Policy, University of Minnesota School of Public Health, Minneapolis, MN (BAV); Department of Epidemiology, University of Iowa, Iowa City, IA (RBW)
Correspondence to: Carol Sweeney, PhD, Health Research Center, DFPM, 375 Chipeta Way, Suite A, University of Utah, Salt Lake City, UT 84108 (e-mail: csweeney{at}hrc.utah.edu).
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ABSTRACT |
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Background: The elderly population, including many who are long-term cancer survivors, is increasing. Aspects of quality of life in elderly cancer survivors are not well understood. Methods: Subjects were women who enrolled in a population-based cohort study in 1986. At follow-up in 1997, 25 719 women, at a median age of 72 years, reported on functional limitations. We used logistic regression to calculate prevalence odds ratios (ORs) and proportional hazards regression to calculate prevalence ratios (PRs) for associations between cancer survivor status and functional limitations, adjusting for baseline (precancer) characteristics including obesity, smoking, and diabetes. Results: Women who were cancer survivors for less than 2 years reported the most functional limitations, but long-term (5 or more years) cancer survivors remained more likely than cohort members who had not had cancer to report that they were unable to do heavy household work (42% of 1068 5-year survivors, versus 31% of 23 501 who never had cancer, multivariable OR = 1.47, 95% confidence interval [CI] = 1.27 to 1.69; PR = 1.22, 95% CI = 1.10 to 1.34), unable to walk a half mile (26% versus 19%, OR = 1.31, 95% CI = 1.1 to 1.54; PR = 1.16, 95% CI = 1.02 to 1.32), and unable to walk up and down stairs (9% versus 6%, OR = 1.34, 95% CI = 1.05 to 1.72; PR = 1.25, 95% CI = 1.00 to 1.56). The increased prevalence of functional limitations was apparent for 5-year survivors of breast cancer and also certain other cancers. Conclusions: Our findings support the need to target elderly cancer survivors for interventions to maintain or regain physical function.
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INTRODUCTION |
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Longer life expectancies, earlier detection of cancer by screening, and more successful treatment of cancer are contributing to the growth of the population of elderly long-term cancer survivors (1–3). The proportion of elderly people in the U.S. is growing—the group aged 75 years and older has increased from 3.1% of the population to 5.9% during the last 40 years (4). Within the elderly population, a substantial portion is affected by cancer (5). In 2001, an estimated 5.6% of women aged 60–69 years and 7.5% of women aged 70–79 years in the United States had been diagnosed with at least one invasive cancer (6). This translates to greater than 1 million women aged 60–69 years and greater than 2 million women aged 70 years and older in the U.S. population who are cancer survivors. Little is known about the long-term consequences of cancer in this older age group (7).
The ability of elderly individuals to perform activities such as housework, walking up and down stairs, or preparing meals is an important measure of the effects of health on function and the ability to live independently. Individuals who report functional limitations are at increased risk for health problems, for progression to disability, and, possibly, for earlier mortality (8–10). Studies have documented that cancer patients report deficits in physical function within 1 or 2 years after treatment. Some reports suggest that physical function of cancer survivors returns to normal over time (11), but existing studies considering function in long-term survivors have limitations. Several studies were based on single cross-sectional surveys (12–14), with no information on health before cancer diagnosis. The effects of cancer and its treatment on functional limitations may be of particular concern for the elderly because other age-related conditions, such as diabetes or high blood pressure, make them susceptible to a decline in physical function (15).
To assess the long-term influence of cancer and its treatment on physical function, we studied functional limitations reported at follow-up by elderly women in a population-based cohort study. We compared women who had a cancer diagnosis during the study period and were cancer survivors at follow-up with cohort members who had never been diagnosed with cancer. We were able to take into account information about health status at study entry, before any diagnosis of cancer.
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SUBJECTS AND METHODS |
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Study Cohort and Cancer Incidence Data
In 1986, a diet and health questionnaire was mailed to a population-based sample of female residents of Iowa, selected from drivers' license lists, who were aged 55–69 years. The primary aim of the study was to prospectively investigate risk factors for incident cancer among postmenopausal women, with particular interest in obesity and breast cancer. Information obtained through the baseline questionnaire included height, weight, waist and hip measurements, smoking status, education, and history of cancer and other chronic diseases. Respondents to this 1986 baseline questionnaire who were free of cancer (except skin) and were postmenopausal, a total of 37 233 women (43% response rate), formed the Iowa Women's Health Study (IWHS) cohort. The details of the methods of this cohort study and descriptions of cancer incidence and mortality in this study population have been reported (16–19); cancer incidence and mortality were found to be similar among participants and nonparticipants (19). All aspects of the study have received human subjects' research review and approval from institutional review boards at the University of Minnesota and the University of Iowa. The investigators and the institutional review boards judged that return of a questionnaire implied consent to take part in this research.
The IWHS cohort has been continuously followed for occurrence of incident cancer through linkage to the State Health Registry of Iowa, a Surveillance, Epidemiology, and End Results (SEER) program cancer registry. Data on stage at diagnosis (SEER stage categories of in situ, local, regional, or distant) and type of initial cancer treatment are also obtained from the registry; treatment information obtained by SEER registries is recognized to be reliable compared with that from other sources and is specific although not highly sensitive (20,21). Information on vital status of participants is obtained from electronic searches of death certificates in Iowa and the National Death Index. Several mailed follow-up questionnaires have been used to collect updated exposure and health status information.
Assessment of Functional Limitations
On follow-up questionnaires in 1989 and 1997, women were asked "which of these things are you healthy enough to do without help? a) heavy work around the house like shoveling snow or washing walls, windows, and floors? b) walk a half mile? c) go out to a movie, to church or a meeting, or to visit friends? d) walk up and down a flight of stairs? e) prepare most of your own meals?" Respondents marked "yes" or "no" after each of the five items. These are items from a scale developed by Rosow and Breslau (22) for assessment of functional health in elderly, community-dwelling individuals. Items from this scale have been used to assess functional limitations in large studies, including the Established Populations for Epidemiologic Studies of the Elderly (23) and the National Health Interview Survey. Self-report of these limitations by elderly study participants has good reproducibility (24,25).
Statistical Analysis
Respondents to the 1997 questionnaire who completed three or more of the functional limitation questions were included in the present analysis. Self-reported functional limitations from the 1997 questionnaire were treated as outcomes. Each woman was assigned to an exposure category according to her cancer survivor status on May 1, 1997, when data collection for the 1997 questionnaire began. The referent category was women who had never had cancer, i.e., women who did not report a history of any cancer other than skin cancer at baseline, and who had no diagnosis of cancer reported to the Iowa SEER registry up to April 30, 1997. Women who had an incident cancer diagnosis reported to the registry between baseline and April 30, 1997, were divided into three categories based on time since diagnosis. Cut points were 2 years after diagnosis, a time point associated with improvement in health, psychosocial, and functional status in some studies (13,26), and 5 years after diagnosis, a commonly used benchmark defining long-term survival (7,27). The first category included women who were diagnosed with cancer in May 1995 or later and thus were within 24 months of a cancer diagnosis at the time of the questionnaire. The second category included women who were diagnosed with cancer 2 or more but less than 5 years before the questionnaire. Women who had a cancer diagnosis after baseline but before May 1, 1992, had survived at least 5 years after diagnosis and were categorized as long-term cancer survivors. Women who had more than one incident cancer between 1986 and 1997 were excluded from analyses. Women who had a first diagnosis of cancer during the 1997 questionnaire data collection period were also excluded.
Prevalence odds ratios (ORs) and their 95% confidence intervals (CIs) for the cross-sectional associations between cancer survivor status and report of each functional limitation in 1997 were calculated using unconditional logistic regression models. We also created a scale of the number of functional limitations reported, consistent with the intended use of these questionnaire items as a combined scale (22). Values could range from zero (no reported limitations) to five (limitations reported for all of the activities). The association between cancer survivor status and the number of functional limitations was evaluated using an ordinal logistic regression [proportional-odds (28)] model. The odds ratio from the ordinal logistic model represents the relative odds of being in each higher category on the scale compared with any lower category or the odds ratio for reporting one additional limitation. Odds ratios for outcomes with high prevalence, such as these functional limitations in the elderly, will be farther from the null than risk ratios or prevalence ratios. Prevalence odds ratios are a valid measure for prevalence data (29,30), and for this study odds ratios were presented for the primary analysis because odd ratios could be estimated for both the individual item responses and the ordinal scale outcome. We also calculated prevalence ratios (PRs) for the individual limitations, using a proportional hazards model with equal time at risk for all subjects (30). We conducted subgroup analyses, further dividing cancer survivors into categories according to cancer site, stage at diagnosis, and type of treatment. Likelihood ratio tests (two-sided) were used to assess evidence of heterogeneity of the odds ratios among subgroups. P<.05 was considered statistically significant.
Exposures such as cigarette smoking and high body mass index (BMI, weight in kg divided by height in m2) are risk factors for cancer and are independent predictors of functional limitations (31). Therefore these exposures are potential confounders of the association between cancer survivor status and functional limitations. Similarly, chronic medical conditions, such as diabetes and high blood pressure, affect risk of some cancers and are also related to functional limitations (15). We addressed potential confounding by exposure to cancer risk factors or history of chronic disease as reported at baseline by adding variables representing the following baseline characteristics to the regression models: age, treated as a continuous variable; prevalent high blood pressure, heart disease, or diabetes at baseline, history of fracture, current (at baseline) or former cigarette smoking, and participation in moderate or vigorous physical activity at least two times per week, with indicator variables representing yes/no for each of these exposures; and pack-years of smoking, quartiles of BMI, quartiles of waist-to-hip ratio, educational attainment, and self-assessed general health at baseline (excellent, good, fair, or poor), with ordered categories of each of these exposures entered in the model as continuous variables. The same set of adjustment variables was used for all analyses.
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RESULTS |
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Response to the Follow-up Questionnaire
Characteristics of the cohort members at baseline and of respondents and nonrespondents to the 1997 follow-up questionnaire are shown in Table 1. Of the 33 313 eligible IWHS cohort members who were deemed to be alive in 1997, 26 283 returned the follow-up questionnaire (78.9%). Women who were 5-year cancer survivors were somewhat more likely to respond (84.2%) than women who were free of cancer (78.7%), women within 2 years of a cancer diagnosis (75.6%), or those who had survived at least 2 years but less than 5 years (81.3%). Other factors associated with response to the 1997 follow-up questionnaire were younger age, no diabetes, lower waist-to-hip ratio, more education, and better general health as reported at baseline; the associations between these predictors and participation were similar among cancer survivors and women with no cancer. Respondents had a median age of 72 years. After exclusions (n = 150 respondents with missing responses for two or more functional limitations questions, n = 212 respondents who were diagnosed with cancer during the 1997 questionnaire data collection period, and n = 202 women who had two or more cancer diagnoses during follow-up), the study population for this analysis included 25 719 women, 23 501 without cancer and 2218 cancer survivors, including 1068 who had survived 5 or more years after a cancer diagnosis.
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Prevalence of Functional Limitations
Sixty-three percent of respondents to the 1997 follow-up questionnaire reported no functional limitations. Proportions with any limitations by subject characteristics were calculated (Table 1). We estimated odds ratios of negative responses to the individual functional limitation items for cancer survivors compared with women who had never had cancer (Table 2). The reported prevalence of functional limitations among subjects who had never had cancer was very low (2.1%) for each of two activities: going out (to church, a movie, or to visit friends) and preparing meals. The limitation reported most often by the women without cancer was for doing heavy work around the house (31.1%). Survivors of less than 2 years after cancer diagnosis were statistically significantly more likely to report each of the five functional limitations than women who had never had cancer. For three of the functions assessed, women who were 2- to less than 5-year survivors were also statistically significantly more likely than women with no cancer to report limitations, but for all five questions the odds ratios were closer to the null than those for the women with a more recent cancer diagnosis. Prevalence of limitations in ability to go out and in ability to prepare meals for cancer survivors of 5 years or longer were similar to those in women with no cancer. However, for the three functions requiring mobility or strength, i.e., ability to do heavy work (OR = 1.47, 95% CI = 1.27 to 1.69; PR = 1.22, 95% CI = 1.10 to 1.34), to walk a half mile (OR = 1.31, 95% CI = 1.11 to 1.55; PR = 1.16, 95% CI = 1.02 to 1.32), or to walk up and down stairs (OR = 1.34, 95% CI = 1.05 to 1.72; PR = 1.25, 95% CI = 1.00 to 1.56), 5-year cancer survivors were statistically significantly more likely to report limitations than women who had never had cancer.
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Odds ratios for the association between cancer survivor status and functional limitations from the models adjusted for age and baseline general health, BMI, waist-to-hip ratio, smoking, education, physical activity, diabetes, heart disease, high blood pressure, and fracture (as shown in Table 2) were somewhat closer to the null than estimates adjusted for age only. For example, for reporting a limitation in walking a half mile, age-adjusted odds ratios were 1.54 (95% CI = 1.28 to 1.84) for 2-to <5-year cancer survivors and 1.39 (95% CI = 1.20 to 1.60) for 5 or more-year survivors. Each of the model variables representing baseline characteristics, e.g., BMI, smoking, and physical activity, was statistically significantly (all P<.01) associated with functional limitations, with the exception of education, which became statistically nonsignificant in the multivariable model.
Functional limitations were first assessed in the IWHS cohort in the 1989 follow-up questionnaire. We considered the influence of preexisting limitations on the associations between cancer survivor status and functional limitations by excluding subjects who were diagnosed with cancer before 1990 and those who reported limitations in 1989. The odds ratios of reporting functional limitations for cancer survivors of less than 5 years from these analyses (Table 2) were essentially the same as those for the full cohort. Exclusion of subjects diagnosed with cancer before 1990 reduced the number of 5-year cancer survivors in the analysis by more than 50%; odds ratios after the exclusion were above 1.0 for each limitation but had wide confidence intervals.
We also evaluated the number of functional limitations reported by each woman. Cancer survivors were more likely than women without cancer to report one additional functional limitation, based on the ordinal logistic multivariable regression model (for <2-year survivors, OR = 1.90, 95% CI = 1.59 to 2.28; for 2- to <5-year survivors, OR = 1.47, 95% CI = 1.25 to 1.72; and for 5-year survivors, OR = 1.43, 95% CI = 1.26 to 1.62).
Functional Limitations by Cancer Site and Type of Treatment
We further examined the number of functional limitations among 5-year cancer survivors by cancer site (Fig. 1). The most common cancer diagnoses for the 5-year survivors were breast (n = 482), colon (n = 130), endometrium (n = 121), rectum and anus (n = 47), and melanoma and other skin (n = 46). Five-year breast cancer survivors reported statistically significantly more functional limitations than women who had not had cancer (OR = 1.37, 95% CI = 1.14 to 1.65). For 5-year survivors of cancers of the colon, endometrium, rectum and anus, and melanoma, the odds ratios for functional limitations were slightly above 1.0, but there was no statistical evidence of a difference from cancer-free women. For each of the other specific cancer sites, there were fewer than 30 participants who were 5-year survivors, but even given these small numbers, statistically significantly elevated odds ratios for functional limitations were detected for 5-year survivors of hematopoietic cancers, kidney and other urinary cancers, lung and bronchus, other genital sites, and lymphoma. In a test for differences in odds ratios across all categories of cancer sites (Fig. 1), differences in functional limitations by site did not reach statistical significance (
2 = 26.37, 17 df, P = .07).
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As noted above, the largest group of 5-year survivors in the IWHS cohort were women who had had breast cancer. For this group, we examined the association between functional limitations and cancer survivor status by stage at diagnosis and by the type of treatment that was received as the first course of therapy. Odds ratios for reporting one more functional limitation by 5-year breast cancer survivors, compared with women with no cancer diagnosis, by stage at diagnosis, were highest for women with regional or distant disease (Table 3) but were also increased at a level that approached statistical significance in women with in situ and local disease. The number of limitations reported at follow-up by breast cancer survivors did not differ by stage at diagnosis (P = .18). Two frequent types of initial therapy for breast cancer for women in the cohort were a combination of a partial mastectomy procedure (such as a lumpectomy) with radiation therapy and total or modified radical mastectomy without radiation (Table 3). Women who had received a partial mastectomy and radiation reported similar numbers of functional limitations as women who had never had cancer, whereas women who had received the more extensive surgery reported statistically significantly more limitations. The difference in the number of functional limitations between these two treatment groups was not sufficient to provide evidence of heterogeneity of the association (P = .31). The association between cancer survivor status and functional limitations differed little between 5-year breast cancer survivors who were treated with chemotherapy and those who were not nor between women treated with hormonal therapy and those who were not.
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DISCUSSION |
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TopNotesAbstractIntroductionSubjects and methodsResultsDiscussionReferences |
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In a population-based cohort of postmenopausal women who were followed into their elderly years, we found that women who had a cancer diagnosis during the study period reported more functional limitations at follow-up than women who had not had cancer. Participants who were less than 2-year cancer survivors had a higher prevalence of limitations than women who were survivors of 2 or more years. This improvement over time is probably explained by a combination of two factors. First, selection of individuals with cancer who had fewer limitations would take place over time; that is, individuals who had less severe disease at diagnosis and who were not affected by early recurrence would be more likely to survive and would be available to respond to the questionnaire. Second, recovery from effects of the disease and its treatment would take place over time. Our data are consistent with those of other studies (11,12,27,32) that have reported an improved quality of life with time since cancer diagnosis.
We treated survivors of 5 or more years after cancer diagnosis as a category of interest for this analysis because this is the time period most often used to define long-term survivors for cancer survivorship research (7). Five-year cancer survival is also used as a clinical benchmark of recovery, and, for some cancers, risk of recurrence after 5 years is low. In our study, the majority of women who had survived 5 or more years after a cancer diagnosis reported no functional limitations. Five-year cancer survivors were similar to women who had never had cancer in frequency of reporting limitations for two of the activities, able to go out and able to prepare meals. In contrast to smaller studies of long-term cancer survivors that found no difference from control subjects (32,33), in our large study population we detected physical function deficits for 5-year cancer survivors compared with women without cancer. These differences were not attributable to baseline differences in other risk factors or health conditions such as obesity, smoking, or diabetes. Specifically, long-term cancer survivors reported more limitations for three activities that assess strength and mobility: ability to do heavy housework, to walk a half mile, and to go up and down stairs.
Women affected by the most common cancer in this cohort, breast cancer, reported an excess of functional limitations, as did women who had had cancers of each of several other sites. When we considered subgroups of 5-year breast cancer survivors, the association between cancer survivor status and functional limitations was not statistically different by tumor stage or type of initial treatment. Although the cohort was large, the number of 5-year cancer survivors available for analysis limited our statistical power to detect heterogeneity of association by cancer site or by type of treatment. Regardless, the data did not point toward an association that was specific to one cancer site or stage at diagnosis. It is possible that long-term effects of treatment, e.g., the cognitive effects of chemotherapy or lymphedema following breast cancer surgery contribute to the functional limitations. However, the lack of specificity of the association as to cancer site or stage leads to the possible interpretation that the excess of functional limitations develops through a mechanism that is common to more than one cancer site, such as fatigue, depression, or physical inactivity following cancer treatment.
Physical activity and functional limitations are inter-related in the elderly. Prospective studies show that elderly participants who do not engage in physical activity are at increased risk of functional decline (31,34–36). This phenomenon may explain some of the excess of functional limitations in long-term cancer survivors that we observed in this study, because there is evidence that women decrease their physical activity during cancer treatment and that activity may not be restored to prediagnosis levels after treatment (37–39). Reported effects of cancer treatment include persistent fatigue (40–43), psychologic effects (26,44), and, for breast cancer, lymphedema (45,46). These side effects have been linked to reduced physical activity (44,47), which, for the elderly, places them at risk for a decline in physical function (48).
Strengths of the present study are that cancer survivors were followed for more than 5 years, and that it included a reference population of women with no cancer. We were able to adjust for a number of baseline predictors of functional limitations. In our analysis, estimated odds ratios moved slightly toward the null in adjusted compared with unadjusted models. Although prediagnosis characteristics of cancer survivors such as BMI and smoking acted as confounders for analysis of postcancer quality of life, strong and statistically significant associations persisted after adjustment for baseline characteristics. The associations appeared to be independent of prediagnosis characteristics.
A potential limitation of our study is that functional limitations were not assessed at baseline. However, when we restricted analyses to individuals who were initially free of limitations, the odds ratios were similar to those obtained from the full cohort. Thus, in this dataset, functional limitations present before cancer diagnosis did not appear to act as confounders. Adjusting for functional limitations present before a cancer diagnosis reduced our statistical power, because excluding subjects with a cancer diagnosis before the first assessment of functional limitations in 1989 eliminated more than half of the 5-year survivors. However, given that there was no evidence of confounding, we conclude that the results for the full cohort without this restriction should be considered valid estimates of the odds ratios.
Another limitation of the study is that physical activity was not assessed on the follow-up questionnaires. Physical activity was assessed at baseline; lack of physical activity was related to functional limitations at follow-up but was not a confounder or effect modifier of the association between cancer survivor status and functional limitations. Although other studies have shown that individuals with cancer often have reduced physical activity compared with prediagnosis activity levels, effects of cancer survivor status on physical activity cannot be described in this cohort.
No information on disease recurrence was available for women in this study, and some of the excess of limitations in cancer survivors may be explained by recurrence of cancer. However, for some cancers, the risk of recurrence after 5 years is low. In the example of breast cancer, which has high incidence but low mortality (Table 1) in this elderly cohort, it is unlikely that many 5-year survivors were experiencing recurrences when they responded to the questionnaire, yet the odds ratio for functional limitations was statistically significantly elevated among these women. This implies that other factors play a role in the increased prevalence of functional limitations.
Nonresponse to follow-up questionnaires is always a methodologic concern in cohort studies. Although participation in the Iowa Women's Health Study 1997 follow-up was good for a mailed questionnaire in a population-based group, almost 80% overall, there were differences between respondents and nonrespondents. Respondents tended to be those who had reported better health at baseline. Therefore, the prevalence of functional limitations among respondents may underestimate the true prevalence in the cohort. For the purposes of the comparisons in the present analysis, however, the data would be biased only if the predictors of nonresponse among cancer survivors were very different from those of women without cancer, which was not the case.
In summary, we have compared elderly women who are cancer survivors with their peers who have not had cancer with respect to self-reported functional limitations. Consistent with most previous studies on this topic, we found that women's abilities to perform normal activities were most affected during the period 2 years after diagnosis. However, long-term cancer survivors also showed modest, but statistically significant, differences in prevalence of functional limitations compared with women without cancer. Five or more years after a cancer diagnosis, survivors had 30–50% increased odds of reporting an inability to do activities requiring mobility and strength. The increased prevalence of limitations in long-term survivors was not linked to one cancer site or stage at diagnosis, but rather seemed to be a general phenomenon. These findings support the need for interventions to prevent and reverse functional decline (44,48) among elderly long-term cancer survivors.
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NOTES |
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Supported by National Cancer Institute award R01 CA39742 (to A. R. Folsom).
The authors thank Ching-Ping Hong for data management support. The funding agency had no role in the study design, data collection, analysis, or interpretation of the results.
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Manuscript received August 19, 2005; revised February 7, 2006; accepted February 24, 2006.
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J Natl Cancer Inst 2006 98: 506-507.
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