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American Journal of Epidemiology Advance Access originally published online on November 7, 2006
American Journal of Epidemiology 2007 165(3):262-270; doi:10.1093/aje/kwk010
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American Journal of Epidemiology Copyright © 2006 by the Johns Hopkins Bloomberg School of Public Health All rights reserved; printed in U.S.A.

ORIGINAL CONTRIBUTIONS

Racial/Ethnic Differences in Endometrial Cancer Risk: The Multiethnic Cohort Study

Veronica Wendy Setiawan1, Malcolm C. Pike1, Laurence N. Kolonel2, Abraham M. Nomura2, Marc T. Goodman2 and Brian E. Henderson1

1 Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA
2 Epidemiology Program, Cancer Research Center of Hawaii, University of Hawaii, Honolulu, HI

Reprint requests to Dr. V. Wendy Setiawan, Department of Preventive Medicine, University of Southern California, 1441 Eastlake Avenue, Room 4425, Los Angeles, CA 90033 (e-mail: vsetiawa{at}usc.edu).

Received for publication April 10, 2006. Accepted for publication June 20, 2006.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Few studies have examined differences in endometrial cancer risk among ethnic groups in the United States. The authors assessed the extent to which known risk factors for endometrial cancer explain the racial/ethnic differences in risk among 46,933 postmenopausal African-American, Native-Hawaiian, Japanese-American, Latina, and White women recruited to the prospective Multiethnic Cohort Study in 1993–1996. During a 7.3-year follow up period, 321 incident endometrial cancer cases were identified among these women. Data on known/suspected risk factors were obtained from baseline questionnaires, and comparisons of endometrial cancer incidence across racial/ethnic groups were estimated using log-linear proportional hazard models. Later age at menopause, unopposed estrogen therapy use, and obesity were associated with increased risk, while increasing parity and increasing duration of oral contraceptive use were associated with decreased risk. The relative risks for endometrial cancer (vs. Whites) were 0.76 (95% confidence interval (CI): 0.53, 1.08) for African Americans, 0.92 (95% CI: 0.58, 1.46) for Native Hawaiians, 0.61 (95% CI: 0.46, 0.83) for Japanese Americans, and 0.63 (95% CI: 0.46, 0.87) for Latinas. After adjustment for the risk factors, the relative risks were 0.68 (95% CI: 0.47, 0.98) for African Americans, 0.91 (95% CI: 0.56, 1.46) for Native Hawaiians, 0.74 (95% CI: 0.54, 1.01) for Japanese Americans, and 0.65 (95% CI: 0.47, 0.92) for Latinas. Results from this study show that the interethnic differences in endometrial cancer risk do not appear to be explained by differences in the distribution of known risk factors among women of different races/ethnicities.

cohort studies; endometrial neoplasms; ethnic groups; risk factors

Abbreviations: CI, confidence interval; RR, relative risk; SEER, Surveillance, Epidemiology, and End Results


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Cancer of the uterine corpus, of which 97 percent originates from the endometrium (1), is the fourth most common malignancy diagnosed among US females after breast, lung, and colorectal cancers (2). Use of estrogen-only therapy in postmenopausal women, obesity, late age at menopause, and early age at menarche are known risk factors for endometrial cancer, whereas use of combined oral contraceptives, increasing parity, and smoking are protective factors (1, 3). Diabetes and hypertension have also been associated with elevated endometrial cancer risk, but epidemiologic evidence for these risk factors is more limited (4).

The American Cancer Society estimates that 41,200 women will be diagnosed with endometrial cancer in 2006 (2). White women have higher incidence rates of endometrial cancer than any other ethnic group in the United States and, in particular, in 1998–2002 the rate in African Americans was only 74 percent that of Whites (5). In contrast, African Americans had a mortality rate from endometrial cancer that was 79 percent greater than the rate in Whites (5).

The difference in endometrial cancer incidence between African Americans and Whites has been the subject of numerous reports (6–9), but fewer data are available on endometrial cancer rates among Latinas (8–10) and Asians (11). Although it is clear that racial/ethnic disparity in endometrial cancer incidence exists, the determinants of this variation are not clear. The objective of this analysis was to determine the extent to which known/suspected risk factors for endometrial cancer explain the racial/ethnic differences of this malignancy in a multiethnic cohort study of African-American, Native-Hawaiian, Japanese-American, Latina, and White women.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Study population
The Hawaii–Los Angeles Multiethnic Cohort Study is a prospective study designed to examine the association of diet, lifestyle, and genetic factors with the incidence of cancer and other chronic diseases. The details of the study design and baseline characteristics have been published (12). Briefly, the recruitment of the cohort began in 1993 and was completed in 1996. Potential participants were identified through driver's license files from the departments of motor vehicles, voter registration lists, and Health Care Financing Administration data files. The cohort consists of more than 215,000 men and women (aged 45–75 years at baseline) and comprises mainly five self-reported racial/ethnic populations: African Americans, Japanese Americans, Latinos, Native Hawaiians, and Whites living in Hawaii and California (mainly Los Angeles County). The response rates ranged from 20 percent in Latinos to 49 percent in Japanese Americans. Each participant completed a 26-page, self-administered, mailed questionnaire on diet, demographic factors, anthropometric measures, other lifestyle factors, history of prior medical conditions, family history of cancer and, for women, menstrual history, reproductive history, and exogenous hormone use. The institutional review boards at the University of Hawaii and at the University of Southern California approved the study protocol.

Inclusion and exclusion criteria
Women were excluded from the present analysis if they 1) reported a hysterectomy or a bilateral oophorectomy on the questionnaire (n = 30,073), 2) reported cancer of the breast, endometrium, or ovary on the questionnaire or if any of these cancers had been recorded by a cancer registry (described below) before the date the questionnaire was completed (n = 6,654), 3) were premenopausal at baseline (n = 13,753), or 4) had missing data on any of the following variables: body mass index, age at menarche, parity, oral contraceptive use, age at menopause, hormone therapy use, smoking status, first-degree family history of endometrial cancer, and self-reported diabetes or hypertension (n = 3,845). Women who reported taking antihypertensive medications were considered hypertensive. By use of the exclusion criteria, 12,120 African Americans, 4,233 Native Hawaiians, 12,611 Japanese Americans, 11,396 Latinas, and 12,260 Whites were excluded; after all exclusions, 46,933 postmenopausal women (16.5 percent African Americans, 6.6 percent Native Hawaiians, 30.7 percent Japanese Americans, 21.8 percent Latinas, and 24.4 percent Whites) were included in the analyses. The mean age at cohort entry was 61.6 years.

Follow-up and case identification
Follow-up began when participants completed the baseline questionnaire and continued to one of the following endpoints, whichever came first: 1) diagnosis of endometrial cancer, 2) diagnosis of breast or ovarian cancer, 3) death, or 4) end of follow-up (December 31, 2001). Incident endometrial cancer cases were identified by record linkage to the Hawaii Tumor Registry, the Cancer Surveillance Program for Los Angeles County, and the California State Cancer Registry. All tumor registries participate in the National Cancer Institute's Surveillance, Epidemiology, and End Results (SEER) Program of cancer registration. Cases of endometrial cancer included International Classification of Diseases for Oncology, Second Edition (ICD-O-2), code C54 (uterine corpus). Uterine sarcomas (n = 21) were not included as cases, but follow-up was censored for subjects with these tumors at the date of diagnosis. Deaths within the cohort were determined by annual linkage to state death certificate files in California and Hawaii and periodically to the National Death Index. Case ascertainment and death information were complete through December 31, 2001.

On average, cohort participants were followed for 7.3 years. A total of 321 incident cancer cases of endometrial cancer were identified during the follow-up period. The stage of endometrial cancer was defined according to the SEER staging system: localized, advanced (regional and distant), and unknown. Tumor grade was classified into four categories: low (grade 1, well differentiated), medium (grade 2, moderately differentiated), high (grade 3 or higher, poorly differentiated to undifferentiated), and unknown. Tumor histology was classified in accordance with the International Classification of Diseases for Oncology, Second Edition. Tumor subtype was categorized into less aggressive (endometrioid adenocarcinoma and mucinous adenocarcinoma) and more aggressive (squamous carcinoma, clear cell adenocarcinoma, serous adenocarcinoma, undifferentiated carcinoma, transitional cell carcinoma, and mullerian/mesodermal mixed tumors) (13).

Statistical analysis
The differences in the distributions of stage, grade, and histology comparing Whites with other racial/ethnic groups were tested using {chi}2 tests.

To identify which factors differed among racial/ethnic groups and which therefore might account for racial/ethnic differences in endometrial cancer risk, we first assessed racial/ethnic-specific distributions of several known/potential risk factors: body mass index, age at natural menopause, age at menarche, parity, duration of oral contraceptive use, type and duration of hormone therapy use, self-reported diabetes, hypertension, smoking status, and family history of endometrial cancer. Current hormone therapy use at baseline continues for most of the women for at least some further period until censoring time, so that the true duration of hormone therapy use is underestimated. We adjusted for time on the study to correct for this underestimation using methods previously described (14).

Hazard ratios for endometrial cancer incidence associated with the above risk factors, which are referred to here as "relative risks," were estimated using log-linear proportional hazard models stratified by age at recruitment (in 1-year age groups) and year of recruitment (single years). The underlying time variable in the analysis was time from the date of enrollment to the date of endometrial cancer diagnosis, death, or censoring. In the results adjusted for race/ethnicity, race/ethnicity was used as a stratification variable, and the relative risks associated with the exposure variables were assumed to be the same across all five ethnic groups.

To evaluate the association between race/ethnicity and endometrial cancer risk, we compared the incidence rates in each racial/ethnic group with that of White women. The relative risks for endometrial cancer incidence associated with race/ethnicity were estimated with and without adjustment for the known/potential risk factors listed above. Additional factors, such as education and screening behaviors, were considered because they might explain racial/ethnic differences in risk and/or stage at diagnosis. We used the number of years since the last Papanicolaou smear and mammogram as proxies for screening behavior. We performed separate analyses for localized and advanced cases and for less aggressive and more aggressive histology. All p values are two sided. Statistical analyses were performed in SAS, version 8.2 (SAS Institute, Inc., Cary, North Carolina), software and in STATA, version 8 (StataCorp LP, College Station, Texas), software.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Table 1 shows the relative risks of endometrial cancer, as well as the age-adjusted incidence rates. Compared with Whites, endometrial cancer rates were 24 percent lower in African Americans, 8 percent lower in Native Hawaiians, 39 percent lower in Japanese Americans, and 37 percent lower in Latinas. Among the 22 percent (n = 71) of women with advanced disease, the incidence rate was 80 percent higher among African Americans, 63 percent higher in Native Hawaiians, and 16 percent higher in Latinas than among Whites. Japanese Americans had the lowest incidence of advanced cancer, with an incidence rate 37 percent lower than that of Whites.


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  		TABLE 1. Incidence rates and risk of endometrial cancer among postmenopausal women recruited to the Hawaii–Los Angeles Multiethnic Cohort Study in 1993–1996

 
There were clear racial/ethnic differences in stage, grade, and histologic subtype between Whites and African Americans (table 1). African Americans had much higher proportions of advanced tumors (38.2 percent vs. 15.4 percent, p = 0.001), high-grade tumors (32.7 percent vs. 19.2 percent, p < 0.001), and more aggressive histology (30.9 percent vs. 8.7 percent, p < 0.001) than did White women. Latinas also had higher proportions of advanced tumors (27.9 percent vs. 15.4 percent, p = 0.041), high-grade tumors (29.5 percent vs. 19.2 percent, p = 0.027), and more aggressive histology (26.2 percent vs. 8.7 percent, p = 0.002) compared with Whites. The tumor characteristics in Whites, Japanese Americans, and Native Hawaiians were similar; that is, most cases were diagnosed at localized stage, were low grade, and were of less aggressive histologic type.

The tumor grade increased with stage (table 2). African Americans had higher grade tumors than did Whites (medium or high grade: 72.4 percent vs. 42.9 percent in localized tumors and 100 percent vs. 81.3 percent in advanced tumors). Within localized tumors, the distributions of histologic subtypes were similar; within advanced tumors, Whites had 18.8 percent of tumors with more aggressive histology compared with 61.9 percent in African Americans (p = 0.009) and 41.7 percent in Latinas (p = 0.085). Even among advanced stage and high-grade tumors, African Americans and Latinas had higher proportions of tumors with more aggressive histology than did Whites (data not shown).


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  		TABLE 2. Relations between tumor grade and histology with stage at diagnosis among postmenopausal women recruited to the Hawaii–Los Angeles Multiethnic Cohort Study in 1993–1996

 
The distributions of risk factors for endometrial cancer by racial/ethnic group are shown in table 3. African Americans had the highest body mass index, followed by Native Hawaiians, Latinas, Whites, and Japanese Americans. The risk of endometrial cancer was increased substantially (relative risk (RR) = 3.14, 95 percent confidence interval (CI): 2.33, 4.22) in obese women (body mass index: ≥30 kg/m2) relative to women with a body mass index of less than 25 kg/m2. The association between endometrial cancer and overweight, defined as a body mass index between 25 and less than 30 kg/m2, was less striking (RR = 1.28, 95 percent CI: 0.96, 1.71).


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  		TABLE 3. Distributions of risk factors* and their associated relative risks for endometrial cancer among postmenopausal women recruited to the Hawaii–Los Angeles Multiethnic Cohort Study in 1993–1996

 
Native Hawaiians reached menarche at an earlier age than did the women in other ethnic groups. Compared with women who had an early age at menarche (≤12 years of age), women who had menarche at 13–14 years and 15 years or later had 14 percent and 15 percent reductions in endometrial cancer risk, respectively. The test for trend, however, was not statistically significant (ptrend = 0.239).

Age at natural menopause was later in Japanese Americans. Older age at menopause was associated with a significantly greater risk of endometrial cancer (ptrend = 0.002). Compared with women whose menopause occurred before the age of 45 years, those whose menstruation stopped between the ages of 50 and 54 years had a 67 percent elevated risk of endometrial cancer, and women with menopause after the age of 55 years experienced a 79 percent elevated risk.

There were major ethnic differences in parity. The proportion of women who were nulliparous was highest in Whites. Among parous women, Latinas and Native Hawaiians had the most children, followed by African Americans, Whites, and Japanese Americans. We observed a 14 percent reduction in risk of endometrial cancer among women with one or two children compared with nulliparous women. Further reduction in risk was observed with increasing parity: a 38 percent decreased risk in women with three or four children and a 42 percent decreased risk in women with five or more children (ptrend = 0.001).

Whites and Japanese Americans used postmenopausal hormone therapy to a much greater extent than did the other ethnic groups. Current estrogen-only therapy use was associated with an increased risk of endometrial cancer, and risk was estimated to increase 36 percent per 5 years of use (95 percent CI: 1.22, 1.53). Past estrogen-only therapy use was also associated with an increase in risk (per 5 years of use: RR = 1.67, 95 percent CI: 1.40, 1.98). There was a modest increase in risk associated with current estrogen-progestin therapy use, but it was not statistically significant (RR = 1.09, 95 percent CI: 0.97, 1.24). Past progestin therapy use appeared to be associated with a decreased risk, but very few women reported using this type of hormone.

Whites and African Americans were more likely to have used oral contraceptives than were Japanese Americans, Native Hawaiians, or Latinas. History of oral contraceptive use was associated with a reduced risk of endometrial cancer. Risk decreased with increasing years of use (ptrend = 0.034).

A larger proportion of Whites, African Americans, and Native Hawaiians were either former or current smokers than in the other ethnic groups. There was no clear association between smoking and risk of endometrial cancer.

Diabetes and hypertension were much more frequent among African Americans, Native Hawaiians, and Latinas than among Japanese Americans or Whites. We found no significant association between history of these diseases and risk of endometrial cancer.

The prevalence of family history of endometrial cancer was low in this cohort, ranging from 0.6 percent in African Americans to 2.1 percent in Latinas. No clear association between family history and risk of endometrial cancer was observed.

The risks of endometrial cancer in each ethnic group relative to Whites are shown in table 4. Whites had the highest endometrial cancer risk for all stages combined; the relative risks among African Americans, Native Hawaiians, Japanese Americans, and Latinas were all lower than one. After risk factor adjustment, the relative risks among African Americans and Latinas were statistically significantly lower than one. Japanese Americans had the lowest observed risk (RR = 0.61); the relative risk was attenuated after multivariate adjustment (RR = 0.74), and this was not quite statistically significant. Native Hawaiians had a risk close to that of Whites. The risk patterns for localized cancer were similar to those for all cancer. Whites had by far the highest risk of localized cancer. Further adjustments for education and years since the most recent Papanicolaou smear and mammogram examination did not alter the observed patterns (data not shown).


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  		TABLE 4. Relative risks of endometrial cancer among postmenopausal women recruited to the Hawaii–Los Angeles Multiethnic Cohort Study in 1993–1996

 
African Americans had higher risks of developing advanced disease and cancer with more aggressive histology than did Whites. The relative risk for advanced endometrial cancer among African Americans was 1.80 and, adjusted for risk factors, it was 1.57. The relative risk of more aggressive cancer among African Americans was 2.96, and their relative risk adjusted for risk factors was 2.63. Native Hawaiians also had a higher risk of advanced cancer than did Whites, but there were very few advanced cases in this racial/ethnic group (n = 5). Latinas had slightly greater risk of advanced cancer than did Whites, but they had a much higher risk of developing cancer with more aggressive histology than Whites did. The risk of developing advanced cancer and more aggressive cancer was lower in Japanese Americans than in Whites.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
In this prospective multiethnic study, we show that racial/ethnic differences in the prevalence of risk factors do not account for the observed racial/ethnic disparities in endometrial cancer incidence. We found that the risk of endometrial cancer in Whites far exceeded that in African Americans, Native Hawaiians, Japanese Americans, and Latinas. African Americans, however, had the highest risk of developing advanced cancer, and African Americans and Latinas had the highest risk of developing tumors with aggressive histology.

Compared with other racial/ethnic groups, White women had the highest incidence of endometrial cancer. This lower endometrial cancer incidence in non-White women than in Whites in our cohort reflects the pattern reported by the SEER Program for women in the same age and ethnic group (5). The risk of endometrial cancer among African Americans in the cohort was 24 percent lower than that of White women. African Americans in our study have a greater number of children, but they also are much heavier compared with Whites. Adjustment for these risk factors did not explain the observed lower risk among African Americans. We excluded women who reported a hysterectomy on the questionnaire, but the frequency of hysterectomy during the follow-up period is unknown. Women who underwent hysterectomy after baseline should have been censored at the time of the procedure. In all age groups, the prevalence of hysterectomy is higher among African Americans than among White women (15); if during our follow-up the rate of hysterectomy is higher in African Americans than in Whites, then the estimated relative risk comparing these two groups may have been biased away from the null.

Although African Americans had a reduced incidence of endometrial cancer compared with White women, they were more likely to be diagnosed at a later stage, a finding consistent with many studies (6, 7, 9, 13, 16, 17). Differences in screening behavior may partly contribute to the difference in endometrial cancer stage at diagnosis (13, 16, 17). In order to reduce potential confounding due to screening behavior when assessing ethnic differences in endometrial cancer risk by stage at diagnosis, we adjusted for screening behavior (Papanicolaou smear and mammogram) in our analyses; this further adjustment, however, did not alter our results. In agreement with other studies (6, 7, 9, 13, 16, 17), African Americans in our cohort had higher grade and more aggressive tumors compared with Whites. Even within the same stage at diagnosis, differences in grade and histology between African Americans and Whites remained, suggesting a biologic basis. Further research is needed to explain the biologic factors that predispose African Americans to develop more aggressive tumors.

Japanese Americans had lower endometrial cancer rates compared with Whites, irrespective of stage at diagnosis. Similar to our findings, those of Liao et al. (11) found that the incidence of endometrial cancer among US-born Japanese was two-thirds the rate of Whites. The rate in US-born Japanese, however, was twice that of Japanese born in Japan. In our cohort, only four Japanese-American cases (5 percent) were born in Japan. Thus, we were unable to calculate rates for the US-born and the Japan-born Japanese separately. Liao et al. (11) suggested that a plausible explanation for the different rates in US-born and Japan-born Japanese could lie in the different prevalences of obesity and use of hormone therapy. In the Multiethnic Cohort Study, Japanese Americans were much leaner than Whites were, but they used hormone therapy to the same extent as White women, and they also had a later age at menopause and were less likely to use oral contraceptives. Adjustment for these risk factors did not affect the observed difference in endometrial cancer rates between Japanese Americans and Whites. The reasons for this are unclear, but one factor that could contribute to this disparity is the dietary differences between these two ethnic groups. Previous studies have suggested that soy products may be protective against endometrial cancer (18–22) and, in the Multiethnic Cohort Study, the consumption of tofu is highest among Japanese-American women (12).

Previous studies have reported that, among most Latino populations, endometrial cancer occurrence is lower than that in Whites (8–10). We observed that endometrial cancer risk in Latinas is 37 percent lower than that of the Whites, and this difference is not explained by their greater number of children or their later age at menarche. The reasons for their low endometrial cancer rates are not completely clear but may have a dietary basis (12). Some studies have suggested that high fiber intake may protect against endometrial cancer (18). In the Multiethnic Cohort Study and other studies, intakes of dietary fiber and of legumes, an important food source of fiber, are much higher among Latinos than among Whites (8, 12). Interestingly, we recently observed that higher intake of dietary fiber is associated with lower circulating estrogen levels among postmenopausal Latinas (23). Subsequent studies focusing on fiber and soy food intakes should help to clarify their roles in endometrial cancer risk.

We observed that, relative to Whites, Latinas were more likely to present with advanced stage at diagnosis. The later stage at diagnosis among Latinas is probably related to access to early diagnosis, although biologic factors that predispose them to develop more aggressive tumors are also possible since, within the same stage, they were more likely to have tumors with aggressive histology than were White women. Studies on the difference in stage at diagnosis or histology between Latinas and Whites are scarce (9, 10). Further studies are needed to confirm our observations.

The observed risk of endometrial cancer among Native Hawaiians was slightly lower than that of the Whites, but there were very few Native Hawaiian cases, so further follow-up of the cohort is needed to draw meaningful conclusions about this ethnic group.

Our study has several strengths and limitations. The strengths of this study include its prospective design, the exclusion of women with cancer and hysterectomy at baseline, and the ability to take into account most known and suspected endometrial cancer risk factors. One limitation of this study is the lack of updated hysterectomy and risk factor information during the follow-up period. No updated hysterectomy information precluded us from censoring those who were no longer at risk during the follow-up period. Another potential limitation is a possibility of differential loss to follow-up across ethnicity. However, since the outmigration rates in the adult population are low in California and Hawaii, this possibility seems unlikely (12).

In summary, we provide some of the first results comparing endometrial cancer risk among different racial/ethnic groups in relation to various risk factors. We showed that the interracial differences in endometrial cancer risk do not appear to be explained by differences in the distribution of known risk factors among women of different races/ethnicities. This justifies additional studies to search for other environmental and genetic risk factors for endometrial cancer.


   ACKNOWLEDGMENTS
 
This work was supported by grant CA54281 from the National Cancer Institute. V. W. S. is supported by grant CA116543 from the National Cancer Institute.

The authors thank Dr. Lynne Wilkens, Dr. Kristine Monroe, Peggy Wan, and Hank Huang for their assistance with data management and analysis.

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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