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Obesity and Risk of Cancer in Postmenopausal Korean Women

Yun-Mi Song, Joohon Sung, Mina Ha

From the Department of Family Medicine, Samsung Medical Center; Center for Clinical Research, Samsung Biomedical Research Institute, SungKyunKwan University School of Medicine; Department of Epidemiology, School of Public Health, Seoul National University; Department of Cancer Epidemiology and Cancer Prevention, National Cancer Center, Seoul; and Department of Preventive Medicine, Dankook University College of Medicine, Cheonan, South Korea

Corresponding author: Mina Ha, MD, MPH, PhD, Department of Preventive Medicine, Dankook University College of Medicine, Cheonan, Chungnam, South Korea, 330-714; e-mail: minaha{at}dku.edu

	ABSTRACT

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Purpose To evaluate an association between obesity, measured by body mass index (BMI; kg/m²), and risk of cancer at individual and all sites in postmenopausal women.

Methods A cohort of 170,481 postmenopausal Korean women who were age 40 to 64 years at baseline measurement of BMI was observed prospectively from 1994 to 2003 for cancer incidence. Multivariable adjusted proportional hazard models were used for evaluating the association.

Results Women with a BMI of 30 kg/m² or higher had a 23% higher risk of cancer than women with a BMI between 21.0 and 22.9 kg/m² (hazard ratio = 1.23; 95% CI, 1.08 to 1.41). According to the increase in BMI level, significant positive trends existed in cancers of colon, breast, corpus uteri, and kidney with hazard ratios of 1.05 (95% CI, 1.02 to 1.08), 1.07 (95% CI, 1.05 to 1.10), 1.13 (95% CI, 1.07 to 1.20), and 1.08 (95% CI, 1.02 to 1.15), respectively, for the increase of BMI by 1 kg/m². When the analysis was limited to never-smokers, women with a BMI of 25 kg/m² or higher showed a significantly increased risk of cancers of the colon, breast, corpus uteri, and kidney and leukemia compared with the normal BMI (18.5 to 22.9 kg/m²) group.

Conclusion Although variations exist between the individual cancer sites, obesity was associated with an overall increased risk of cancer in postmenopausal Korean women. To reduce the risk of cancer, active strategies to prevent obesity should be implemented in postmenopausal women.

	INTRODUCTION

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The prevalence of obesity is increasing around the world, and the obesity-related disease burden is one of the most important health issues, even in the Asian countries where the mean body mass index (BMI) and the prevalence of obesity were once lower than those in Western countries.^1-6 The Korean National Health and Nutrition Survey showed an increase in prevalence of obesity (BMI > 25 kg/m²) among the adult male and female population from 26% and 26.5% in 1998 to 33.5% and 29.3% in 2001,^7,8 which was in parallel with an increase in mortality from diabetes from 6.8% to 24.3% among 100,000 persons between 1985 and 2004.⁹ There has been evidence of an association between excess body weight and an increased risk of cancers.^10-14 However, most previous studies on this issue have been conducted mainly on the Western population, and there have been only a few studies in the Asian population, who might have a different lifestyle, genetic background, and disease prevalence.¹⁵ Furthermore, studies in Asian women are more scarce, with limited data for cancers at individual sites.^15,16 We evaluated the association between BMI, a measurement of body fatness, and cancer in all sites and individual sites in a cohort of postmenopausal Korean women.

	METHODS

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Study Population
Study participants were postmenopausal women age between 40 and 64 years. They were public servants or unemployed dependants who underwent a health examination provided by the Korea Medical Insurance Corporation, one of the major institutions of the Korean National Health Insurance System. Ninety-five percent of public servants and 52% of all the invited female dependents age 40 to 64 years underwent the health examination between 1993 and 1994. Among these female examinees, we identified postmenopausal women age 40 to 64 years based on self-report of natural menopause (142,821 women, 83.8% of all postmenopausal women) and hormonal replacement therapy (6,144 women, 3.6%). Women older than 55 years at baseline examination (21,516 women, 12.6%) were also considered to be postmenopausal, which was based on the facts that the median age at menopause among Korean women is 50 years and that 95% of Korean women were shown to have undergone menopause before 55 years of age in a nationwide Korean study.¹⁷

Among the 173,542 postmenopausal women, those who died (n = 419) or were diagnosed with a cancer (n = 2,534) before the beginning of the study and whose BMI was unknown or was in the lower or upper 0.01% range (n = 108) were excluded. Finally, a total of 170,481 women were included in the study. Cancer diagnosis before the beginning of study was identified based on self-report and the data of the Korea Central Cancer Registry (KCCR) and Serious Diseases Registry (SDR). The Internal Review Board of Samsung Medical Center (Seoul, South Korea) approved this study.

BMI and Covariates
The weights and heights were measured using standardized stadiometers and scales during a health examination with the women in light clothing. Otherwise, no specific guidelines were used. BMI was calculated as the weight in kilograms divided by the height in meters squared and was categorized into the following seven groups: less than 18.5, 18.5 to 20.9, 21.0 to 22.9, 23.0 to 24.9, 25.0 to 26.9, 27.0 to 29.9, and 30 kg/m². A BMI of 30 kg/m² and 18.5 kg/m² comprised of the highest 3.76% and lowest 2.55%, respectively, of the whole range of BMI distribution in the study population.

Information on the health-related behavior and menopausal status at baseline were obtained from a self-administered questionnaire during a health examination. The smoking status was classified into two groups (never-smoker or ever-smoker). Current smokers (4.9%) and former smokers (2.7%) were combined into ever-smoker group because their proportions were low. Two categories were used for physical exercise (performing regular exercise or not) because more detailed information was not available. Two categories were used for alcohol consumption (nondrinker or drinker) because prevalence of alcohol drinking was low. Socioeconomic status was classified into four groups based on the quartile distribution of the monthly salary level of the women public servants or the salary level of public servants who support the unemployed female dependants.

Cancer Incidence
We identified women who were diagnosed with cancer between October 1, 1994 and December 31, 2003 through data linkage with death report data from the Korean National Statistical Office, KCCR of the Korea National Cancer Center, and SDR of the Korea National Health Insurance Corporation using a personal identification number. KCCR is a hospital-based cancer registration system that began in 1978. The percentage of registered hospitals participating in KCCR was 74%, 79%, and 79% in 1995, 1999, and 2002, respectively.¹⁸ To increase the completeness of finding cancer patients, we used the data of SDR, a nationwide registry identifying persons with serious diseases such as cancer to provide them with greater benefit of medical expenses.

The end point of the follow-up was the date of the first diagnosis of cancer, the date of death for those who died of noncancer causes, or December 31, 2003, whichever came first. For the cancer patients who were ascertained from SDR or death report data, information on the date of the first diagnosis was obtained from the medical claim data of the Korea National Health Insurance Corporation. For the 54 cancer patients identified from death report data, date of the first cancer diagnosis was imputed by using average survival time of individual cancer.¹⁹ Average survival time was estimated for 5-year intervals of age based on the data of cancer patients from the study population for whom information on both the date of cancer diagnosis and the date of death was available.

Statistical Analyses
The age-adjusted incidence per 100,000 person-years was calculated in each BMI group using the 5-year age distribution of the whole Korean female population in 1994 as a standard population. The hazard ratio and 95% CI of cancer in each BMI group compared with referent BMI level (21.0 to 22.9 kg/m²) were estimated using the Cox proportional hazards regression model after testing the proportionality assumption, with an adjustment for age (years), height (centimeters), alcohol consumption (yes or no), smoking (ever or never), physical exercise (yes or no), and pay level (quartile) at baseline. Trends of cancer risk for the increase in BMI were tested using BMI level as a continuous scale with a unit of 1 kg/m² in the corresponding models.

To examine the effect of preclinical cancers that may cause weight loss and thus bias the association between BMI and cancer, we repeated the analysis after excluding the cancer patients occurring within the first 5 years of follow-up. To eliminate the probable effect of smoking on the association, additional analysis was performed being limited to never-smokers. In this analysis, we evaluated the risk of cancer associated with being overweight (BMI, 23.0 to 24.9 kg/m²) or obese (BMI 25 kg/m²), with the BMI level between 18.5 and 22.9 kg/m² as a referent group.³ All of the analyses were carried out using the SAS statistical package (SAS Institute, Cary, NC), and a P < .05 was considered significant.

	RESULTS

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We observed 170,481 women for an average of 8.75 years (standard deviation [SD] = 1.15 years), resulting in a total of 1,491,465 person-years (Table 1). During the follow-up, 7,333 cancer patients were ascertained, 6,782 (92.5%) from KCCR, 280 (3.8%) from SDR, and 271 (3.7%) from death report data.

Table 1 shows the distribution of characteristics of participants according to BMI level. Women at both ends of BMI distribution were more likely to be older, to drink alcohol, and to have lower pay level and were less likely to be engaged in regular exercise. Smoking was most prevalent among women in the lowest BMI group.

Table 2 demonstrates an association between BMI and cancers at all and individual sites. The risk of cancers at all sites combined increased with increasing BMI level, and the women with the highest BMI had a 23% higher risk compared with the referent BMI (21.0 to 22.9 kg/m²) group after adjusting for covariates. There were significant trends of increase in the risk of cancers at colon, breast, corpus uteri, and kidney with increasing BMI level, which persisted even after excluding the earlier 5-year cancer events.

View larger version (10K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 1. Relative risks and 95% CIs for cancers at all and individual sites associated with a body mass index (BMI) of (A) 23.0 to 24.9 kg/m2 or (B) 25 kg/m2 or higher among 141,299 never-smoking postmenopausal Korean women age 40 to 64 years (1994 to 2003). The relative risk was estimated using the Cox proportional hazards model with BMI between 18.5 and 22.9 kg/m2 as a reference category, adjusted for age, height, alcohol consumption, smoking status, physical exercise, and pay level.

	DISCUSSION

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The direction and strength of association with BMI varied by individual sites of cancer, and a positive association was found only for cancers at the colon, breast, corpus uteri, and kidney, which suggests that obesity influences cancer risk through different mechanisms according to the specific cancer sites or types.

There has been previous evidence that increased endogenous sex hormones increase the risk of hormone-related cancers such as breast and endometrial cancer in obese women.^21-23 Increase in the risk of breast and endometrial cancers in postmenopausal obese women was consistently observed in previous studies of Western as well as Asian populations.^15,20 We reconfirmed that finding in this study of a Korean population.

Ovarian cancer is also likely to have a sex hormone etiology given the risk factors related with reproduction,²⁴ and positive association with obesity was seen in many studies.^12,14,20 However, the association tended to be weaker in postmenopausal women than in premenopausal women.²⁵ In a study of British women, there was a positive trend for the risk of ovarian cancer with increasing BMI, but this finding was not repeated in postmenopausal women.²⁰ Similar to the British study, a positive association between BMI and the risk of ovarian cancer was not definitely shown in this postmenopausal Korean population. The association between obesity and ovarian cancer needs more investigation.

In this study of Korean women, colon cancer was positively associated with obesity, which is consistent with the findings of many studies^10,11,26 including a recent meta-analysis of 30 prospective studies.²⁷ However, the finding in our study seems to be in contrast to the results of previous other studies showing a positive association in premenopausal women but no specific association in postmenopausal women.^20,28-30 A probable explanation for the difference in findings between our study and other studies is that the association between obesity and colon cancer in postmenopausal women could be influenced by the exogenous estrogen exposure. A large European prospective study reported that abdominal adiposity or BMI was positively associated with the risk of colorectal cancers only in never users of postmenopausal hormones, but not in postmenopausal hormone users.³¹ Given the small number of exogenous estrogen users (7%) included, the findings of the present study seem compatible with those of European women with no exposure to postmenopausal hormones. However, another report indicating that a positive association between BMI and colon cancer was not altered by estrogen exposure among postmenopausal women²³ raises the possibility that the finding of this study has reflected a true association. Therefore, more studies are necessary to clarify this issue.

Several previous studies have demonstrated a positive association between being overweight or obese and leukemia,^14,20,32,33 but not all studies have found this association.¹⁴ Although statistical significance was lost when earlier events were excluded, the finding of increased risk of leukemia at the highest BMI level ( 30 kg/m²) in the present study seems to support a role of obesity as a risk factor of leukemia. Moreover, an analysis limited to never-smokers showed that the higher BMI group ( 25 kg/m²) had a significantly increased risk of leukemia compared with the normal BMI group (18.5 to 24.9 kg/m²). The increased risk of leukemia at the lowest BMI level (< 18.5 kg/m²) seems hardly reliable and needs further investigation because the estimation was based on only a small number of patients (n = 4).

The risk of kidney cancer was increased with increasing BMI level in most previous studies of Western population,^14,21,35 and hormonal or metabolic factors have been proposed as a probable biologic mechanism by which obesity influences renal cell carcinogenesis.^36,37 Although a Japanese study¹⁵ and a Chinese study³⁸ could not demonstrate a significant association, both of these studies might have had insufficient power because of the small number of kidney cancer patients included. A Korean study examining this issue in men including 105 kidney cancer patients reported a positive association, with a 3.85-fold increase in the risk in the highest BMI group ( 30 kg/m²) compared with men with a BMI between 18.5 and 22.9 kg/m².²⁶ In our study, there was a positive trend in the risk of kidney cancer with increasing BMI level, and the women in the highest BMI group showed a 2.61-fold higher risk compared with women with a BMI between 21.0 and 22.9 kg/m². The positive association between obesity and the risk of kidney cancer in both of the Korean studies strongly supports the role of obesity as a risk factor of kidney cancer in the Asian population as well.

An inverse association between BMI and lung cancer has been frequently observed. However, controversies exist regarding whether the association is true. Some studies reported that the inverse association between lung cancer and BMI was caused by the effect of smoking,^39-42 whereas prior chronic respiratory disease being associated with leanness seemed to be able to explain the increased risk of lung cancer in the low BMI group in other studies.^43-45 There was evidence of an inverse association between BMI and lung cancer in this study too, and the association persisted even after the exclusion of earlier events. However, the inverse association completely disappeared when we restricted the analysis to nonsmoking women. This provides strong evidence for the effect of smoking on the association between BMI and lung cancer, negating the true association between leanness and lung cancer risk.

The strengths of this study were a large number of participants and an adequate number of cancer events, which allowed an evaluation of the association between a wide range of BMI levels and all cancer as well as cancers of individual sites in postmenopausal women.

There were some limitations in this study. The waist circumference, which might be a better index of adiposity in relation to cancer, was not measured. Menopausal status was assessed based on self-report of natural menopause and hormonal replacement therapy or on age criteria instead of hormonal measurement, which might have caused biased result for cancers having different association with BMI by menopausal status. In addition, inclusion of women with a history of hormone replacement therapy might have caused biased results for cancers at several sites such as breast, ovary, endometrium, and colon for which increased or decreased association with hormonal replacement therapy has been suggested.^46,47 However, in the analyses limited to the subgroup of women reporting natural menopause but no use of hormone replacement therapy, the associations between BMI and those cancers did not materially change (data not shown). In addition, the covariate of socioeconomic status was assessed based only on the salary level, which might not accurately reflect true socioeconomic position.

Although we tried to assess cancer incidence as completely as possible by using KCCR as well as SDR and death data, incompleteness of outcome assessment might be possible given the incomplete (74% to 79%) participation of hospitals in the KCCR. However, it is less likely for the outcome assessment to be performed differentially according to the BMI level and to cause significantly biased results. We could not evaluate the heterogeneous association with BMI between cancers occurring at similar sites but with different histology or function. Categorization of various cancers that could have different pathophysiology into one group might have obscured significant associations in individual cancer level. The results of this study, which are limited to postmenopausal Korean women age 40 to 64 years, should be generalized carefully in premenopausal women, younger or older women, men, or other ethnic populations.

In conclusion, although variations exist between the individual cancer sites, obesity was associated with an overall increased risk of cancer in postmenopausal Korean women, which is consistent with the findings from studies in the Western population. Given the increasing prevalence of obesity in postmenopausal women, active strategies to prevent obesity should be implemented in postmenopausal women to reduce the risk of cancer, especially colon, breast, corpus uteri, and kidney cancer.

	AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

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The author(s) indicated no potential conflicts of interest.

	AUTHOR CONTRIBUTIONS

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Conception and design: Yun-Mi Song, Joohon Sung, Mina Ha

Collection and assembly of data: Yun-Mi Song, Joohon Sung

Data analysis and interpretation: Yun-Mi Song, Joohon Sung, Mina Ha

Manuscript writing: Yun-Mi Song, Mina Ha

Final approval of manuscript: Yun-Mi Song, Joohon Sung, Mina Ha

	NOTES

 
Supported by Samsung Biomedical Research Institute Grant No. SBRI C-A5-115-1, National Cancer Center Grant No. 0610552-2, and the Ministry of Health and Welfare, Korea Grant No. 01-PJ1-PG1-01CH10-0007.

The sponsors of the study had no role in study design, data collection, data analysis, data interpretation, or writing of the article.

Authors’ disclosures of potential conflicts of interest and author contributions are found at the end of this article.

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Submitted December 12, 2007; accepted April 3, 2008.

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