IJE Advance Access originally published online on November 8, 2005
International Journal of Epidemiology 2006 35(1):151-158; doi:10.1093/ije/dyi226
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Article |
Weight change and risk of endometrial cancer
1 University of Wisconsin Comprehensive Cancer Center, Madison, Wisconsin, USA
2 Department of Population Health Sciences, University of Wisconsin, Madison, Wisconsin, USA
3 Fred Hutchinson Cancer Research Center, Seattle, Washington, USA
* Corresponding author. University of Wisconsin, 610 Walnut Street, WARF Room 701, Madison, WI 53726, USA. E-mail: trentham{at}wisc.edu
 |
Abstract |
|---|
 Top Abstract IntroductionMethodsResultsDiscussionConclusionsReferences |
|---|
Background Obesity is an established risk factor for endometrial cancer. Less well understood is the role of weight gain and weight change in determining risk.
Methods We analysed data from a population-based case–control study to evaluate the associations of body mass index (BMI), weight gain, and weight cycling with risk of endometrial cancer. Cases (n = 740) under age 80 with a new diagnosis of endometrial cancer were identified from Wisconsin's cancer registry. Controls (n = 2342) were randomly selected from driver's license lists and Medicare beneficiary files. Body size at three time points and other risk factor information were ascertained by interview in 1992–95.
Results Endometrial cases were more likely than controls to be nulliparous, have early ages at menarche and late ages at menopause, be diabetic, smoke cigarettes, and use post-menopausal hormones. After adjustment for these factors, increasing BMI was associated with increased risk (P-trend < 0.001); women in the top quartile of BMI (>29 kg/m2) had a 3-fold greater risk of endometrial cancer [95% confidence interval (95% CI) 2.4–4.2] compared with women in the lowest quartile (<23 kg/-m2). For each 5 kg weight gain, the odds ratio (OR) for endometrial cancer risk equalled 1.2 (95% CI 1.2–1.3). History of weight cycling modestly increased risk after adjustment for BMI and other factors (OR = 1.3; 95% CI 1.0–1.6). In addition, women who reported sustained weight loss had a reduced risk of endometrial cancer (OR = 0.7; 95% CI 0.6–0.9).
Conclusions These results suggest that weight gain and lack of weight stability are associated with risk of endometrial cancer.
Keywords Endometrial cancer, body weight, body mass index, weight gain, weight loss
Accepted 5 October 2005
|
Introduction |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionConclusionsReferences |
|---|
Research over the past 30 years has shown that obesity increases risk of endometrial cancer.1 Women with more adipose tissue tend to have increased levels of endogenous oestrogen, which is accompanied by increased proliferation of endometrial epithelial cells and subsequent higher risk of endometrial cancer.2 Obese women are also more likely to have increased levels of bioavailable oestrogen as a result of decreased sex hormone binding globulin (SHBG) levels.3 In addition, obese women are more likely to have anovulatory cycles and decreased levels of progesterone; this increases risk of endometrial cancer as a result of heightened endometrial cell division during anovulatory as compared with ovulatory cycles.2
While obesity is an established risk factor for endometrial cancer, the role of weight gain and weight cycling is not well understood. In order to further explore the associations between different aspects of weight and endometrial cancer risk, data from a population-based case–control study were examined.
|
Methods |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionConclusionsReferences |
|---|
This analysis was performed with data from a population-based case–control study conducted in Wisconsin in 1992–95.
Identification of cases
Cases were female Wisconsin residents, age 40–79 years, with a new diagnosis of invasive endometrial cancer during January 1, 1991 to December 31, 1994. Diagnostic reports, including information regarding cancer site, histology, extent of disease, and follow-up physician, were obtained from the Wisconsin Cancer Reporting System, a statewide tumour registry mandated by legal statute. The physician of record for each case received a written letter requesting permission to approach the subject. Cases with a listed telephone number and without a previous endometrial cancer diagnosis were eligible. Of the 856 women identified as eligible, 6 (0.7%) were not contacted owing to physician refusal, 50 (5.8%) were deceased, 53 (6.2%) refused, and 2 (0.2%) could not be located. A total of 745 case women were interviewed; 87% of those eligible. Owing to missing height and body weight data, five women were excluded from analysis. Endometrial cancer diagnoses were histologically confirmed for 98% of cases according to the tumour registry report.
Identification of controls
Community controls were enrolled based on random selection from population lists of Wisconsin drivers (women 40–64 years of age) and Medicare beneficiaries (women age 65–79). Controls were selected to yield an age distribution similar to that of the cases enrolled in a concurrent study of breast cancer,4 but otherwise controls were selected at random. Inclusion criteria required that all control subjects have a listed telephone number, have an intact uterus, and be free from endometrial cancer. Of 4362 women identified as potential controls, 88 (2.0%) were deceased, 521 (11.9%) refused, and 35 (0.8%) could not be located. Over 85% of controls (n = 3718) participated in the phone interview. Following the interview, 1304 controls with self-reported hysterectomy, 6 with unreliable interviews, and 66 with missing height and body weight values were excluded. Data on 2342 controls were available for analysis.
Data collection
Both cases and controls completed a 40 min structured telephone interview. The phone interview elicited information on each woman's height (recent and at age 20) and weight (recent, lowest and highest weight since age 20). Recorded weights excluded times during pregnancy, and the ‘recent’ time period corresponded to the year prior to the referent date, defined below. Women were asked if they had ever lost at least 20 lb then gained more than half of it back within the same year, how often this happened, and the age at which this last happened. Location of weight gain, specifically on the hips, stomach, or both, was queried for the recent time period.
Recent physical activity was evaluated at two levels, moderate and vigorous. Moderate activity was assessed by asking subjects how often they participated in ‘...moderate physical activities like recreational volleyball, softball, brisk walking or leisurely biking.’ Frequency of vigorous activity was determined by asking study subjects how often they participated in ‘vigorous physical activities, like running, basketball, lap swimming or gymnastics’. Moderate activities correspond approximately to metabolic equivalency scores (METs) of 4–6 and vigorous activities to METs of 7–12.5
The interview also covered the use of exogenous hormones, smoking status, alcohol consumption, selected dietary items, reproductive history, medical history, and demographic factors. Interviews were administered concurrently for both case and control participants. Questions regarding personal and family histories of cancer and cancer screening were asked toward the end of the interview to maintain blinding of interviewers to the disease status of participants.
Statistical analysis
Only events that occurred before the referent date were included in analyses. The referent date for cases was the date of cancer diagnosis. For controls, the referent date was assigned to correspond to the average diagnosis date among similarly aged cases (
1 year prior to interview). On average, 15.1 months elapsed between diagnosis and interview for cases.
Weight gain was determined by subtracting each participant's lowest weight since age 20 from their recent weight. Weight loss was calculated as a woman's highest weight (excluding pregnancy and breast-feeding periods) minus her recent weight. Weight cycling was defined as losing 
20 lb and then gaining more than half the weight back within the same year. Maximum adult weight difference was set as the difference between the lowest and highest adult weights reported by study participants. Quartile category cut-points were defined based on variable distributions among control participants.
Recent physical activity was defined as the level of activity 5 years before the referent date. The frequency of moderate and vigorous activity was dichotomized to reflect no activity and any activity. Dichotomous moderate and vigorous activity variables were cross-classified to represent no activity, only moderate activity, and any vigorous activity. The ‘any vigorous activity’ group included women who reported both vigorous and moderate activity or reported vigorous activity alone. Women were classified as post-menopausal if they reported natural menopause or bilateral oophorectomy before the referent date.
Odds ratios (ORs) and 95% confidence intervals (95% CIs) for endometrial cancer were produced using multivariate logistic regression models adjusted for potential confounders. All statistical models included age (continuous), age at menarche (4 categories), parity (4 categories), age at menopause (4 categories: premenopausal, <50, 50–55, 55+), smoking (never, former, current), post-menopausal hormone use (never, former, current), body mass index (BMI) quartile, recent physical activity (none, moderate only, any vigorous), and diabetes (absent, present). These variables were statistically significant (P < 0.05) in age-adjusted models. To obtain P-values for trend, we included select variables in regression models as continuous linear terms. Effect modification was evaluated by including cross-product interaction terms in logistic models with body size variables parameterized as continuous linear variables. The analyses described above were performed using SAS version 8.0 software (SAS Institute, Inc., Cary, NC).
Reliability substudy
To evaluate the reliability of the questionnaire, we reinterviewed a sequential sample of control subjects. After an average of 3.4 months (range = 2–6 months), 188 controls (71%) completed a second interview. The intraclass correlation coefficient (ICC) and 95% lower confidence limits (LCLs) were estimated to evaluate the reproducibility of body-size questionnaire items.6 Among women interviewed a second time, reproducibility of the interview was high. The ICC for recent weight was 0.93 (LCL 0.91). The ICCs for height, BMI, and highest adult weight were each >0.9. The ICC for lowest adult weight was 0.85 (LCL 0.81).
|
Results |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionConclusionsReferences |
|---|
Cases and controls were, on average, similarly aged (62.9 and 63.3 years, respectively). Endometrial cases were more likely than controls to use post-menopausal hormone therapy, currently smoke, be nulliparous, have younger ages at menarche and older ages at menopause, and to be diabetic. Recent moderate and vigorous physical activity was inversely associated with endometrial cancer risk (Table 1). Menstrual cycle irregularity, alcohol intake, and education were not strongly associated with risk of endometrial cancer (data not shown).
|
Although height was not significantly associated with risk, weight and BMI were strongly related to increased endometrial cancer risk (Table 2). Compared with the leanest quartile, the adjusted OR for the fourth quartile of weight was 3.44 (95% CI 2.63–4.51 for
77.2 vs 
58.9 kg). Similarly, women in the highest quartile of BMI had a 3-fold increased risk of endometrial cancer as compared with women in the lowest quartile category (OR = 3.20; 95% CI 2.42–4.24 for >29.1 vs <22.6 kg/m2).
|
Weight gain since the lowest adult weight was associated with increased endometrial cancer risk; for each 5 kg weight gain, risk of endometrial cancer increased by 21% (95% CI 1.15–1.27). When categorized by approximate quartile cut-points, women with fourth quartile weight gain (
21 kg) had 2.56 times the risk of endometrial cancer (95% CI 1.73–3.78) compared with women who gained 0–7 kg (Table 3). Lowest weight (r = 0.53) was not as highly correlated with recent weight as was highest weight (r = 0.86); most women appeared to gain weight throughout life, so that the time since lowest weight tended to be greater than the time since highest weight. Women who reported sustained weight loss, defined as at least 5 years at a weight that is less than their highest weight since age 20 (excluding weight during pregnancy), had a reduced risk (OR = 0.72; 95% CI 0.55–0.93) of endometrial cancer. We did not observe an association between magnitude of weight loss and endometrial cancer risk (P-trend = 0.4).
|
Adjusting for BMI attenuated the association between a history of weight cycling and risk (Table 3). Before adjusting for BMI, women who reported a history of losing at least 20 lb then gaining at least half back within a year had 1.72 times the risk of endometrial cancer (95% CI 1.37–2.15). Adjustment for BMI attenuated the increased risk to 27% (95% CI 1.00–1.61).
Location of any extra body weight, before and after adjustment for BMI, was not associated with risk of endometrial cancer (Table 3). Before adjustment for BMI, women who reported that they did not tend to carry extra weight had a 39% decreased risk of endometrial cancer (OR = 0.61; 95% CI 0.42–0.88) as compared with women who carried extra weight below the waist, such as on the hips. Adjustment for BMI removed this association.
We calculated the difference between highest and lowest adult weights to consider the relative timing of these weights. Women who reported that their highest adult weight occurred before their lowest weight (i.e. those who lost weight) did not have a statistically significant change in endometrial cancer risk. However, women who reported that their highest weight occurred subsequent to their lowest weight (i.e. those who gained weight) were at increased risk of endometrial cancer (Figure 1). We observed a U-shaped curve for endometrial cancer risk by maximum adult weight difference (P for the quadratic term <0.0001). The OR of endometrial cancer risk for women who gained 30 kg equalled 2.44 (95% CI: 1.59–3.75) compared with women who gained 5–10 kg.
|
Modifiers of weight gain and BMI
We did not observe effect modification of weight gain or BMI associations with endometrial cancer risk by age, smoking, parity, age at menarche, menopausal status, age at menopause, or physical activity. The cross-product interaction term for weight gain by post-menopausal hormone use was statistically significant; however, analyses stratified by 15 kg weight gain produced similar effect estimates and overlapping CIs for never, former, and current post-menopausal hormone users. We additionally evaluated the OR for endometrial cancer risk by BMI among never, former, and current post-menopausal hormone users but were unable to distinguish a clear pattern of effect (data not shown).
|
Discussion |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionConclusionsReferences |
|---|
More than 25 reports published over the past two decades have confirmed the association we observed of greater BMI and increased endometrial cancer risk, primarily among post-menopausal women, but the relation is also evident to a lesser degree among premenopausal women.1 We were also able to examine many other characteristics of body size and endometrial cancer.
We observed a significant increase in endometrial cancer risk with increasing weight gained since age 20 in multivariable adjusted models. Our results generally agreed with those in previously published studies. Of 10 prior investigations, 6 reported that weight gain was an important predictor of risk,7–12 while others did not identify an association between weight gain and endometrial cancer risk.13–16 However, past studies have varied greatly in their adjustment for recent BMI and other confounders.12 We found that this adjustment was essential for the identification of relevant weight periods.
We found that women with a history of weight cycling had an increased risk of endometrial cancer after adjustment for recent weight. To our knowledge, only two other studies have evaluated the risk of endometrial cancer associated with weight cycling.9,14 Our results generally agreed with those reported by Swanson et al., where frequent weight cycling (defined as losing and then regaining 20 lb at least 5 times) nearly tripled endometrial cancer risk (95% CI 1.7–5.0) in initial models. However, following adjustment for current weight, this association was attenuated (RR = 1.6; 95% CI 0.8–2.9).9 Conversely, French et al.14 reported no association for endometrial cancer risk by weight cycling or any weight change category among women living in Iowa.
Previous research has proposed that the distribution of body fat has implications for hormonal profiles and subsequent endometrial cancer risk.17 Android obesity, or body fat located primarily on the upper body (stomach, chest), has been associated with increased estradiol and testosterone levels and decreased SHBG compared with gynoid type obesity, or body fat distributed mainly on the lower body (hips, thighs, buttocks).8,18 The waist-to-hip ratio (WHR) and waist-to-thigh ratio (WTR) are commonly used measures of the relative degree of upper body weight.2 Studies that examined WHR and/or WTR have reported that women with upper body fat had a 2–15-fold increase in endometrial cancer risk.9,19–21 We were not able to replicate these elevated risk estimates by asking women to describe whether they tended to carry extra weight on their hips or stomach.
Weight at early ages (approximately age 18–20) has not been statistically important after adjustment for recent weight in a majority of studies.2,7,9,10,13,16,22 Two studies observed a positive association between endometrial cancer risk associated with body mass at ages 10–2515,23 and a third reported a decreased risk of endometrial cancer associated with low body mass (<20 kg/m2) at age 20 but did not adjust for recent BMI.12 While we did not explicitly ask for weight at age 18 or 20, the majority of women in our study reported that their lowest adult weight occurred at age 20. Recent BMI probably confounds associations of other body size characteristics and endometrial cancer risk; adjustment for this factor is critical to identifying whether early body weight and/or weight distribution exert independent effects.
As we reported previously, BMI modified the risk of endometrial cancer associated with post-menopausal hormone use.24 Relatively lean women (<25 kg/m2) who used oestrogen alone had the greatest risk of endometrial cancer (RR = 1.20, 95% CI 1.14–1.27 per year of use; P = 0.004).24 This finding was consistent with the additive effect of body weight and either exogenous oestrogen therapy25 or endogenous oestrone26 suggested by Potischman et al. and La Vecchia et al. In our study, BMI also modified the association between diabetes and endometrial cancer risk (P-interaction = 0.04).27 A diagnosis of diabetes was associated with endometrial cancer risk among women with BMI > 31.9 kg/m2 but not <29.1 kg/m2.27
In this analysis, the association between weight gain and endometrial cancer risk was not modified by age, smoking, parity, age at menarche, menopausal status, age at menopause, or physical activity. We observed a borderline significant interaction between BMI and weight gain (P = 0.06). We are aware of only one other study that has looked at the association of weight gain and endometrial cancer risk stratified by recent BMI. Although Levi et al. did not observe an association between weight gain and endometrial cancer risk overall (RR = 1.0; 95% CI 0.6–1.5 for third tertile gain compared with weight loss, unadjusted for BMI), there was a suggestion of reduced cancer risk associated with upper tertiles of weight gain among women with BMI 25 kg/m2.13 Additionally, the authors' use of BMI at diagnosis may have reflected weight change associated with preclinical disease.
Limitations of our study should be considered when interpreting the results. Our study relied on self-reported height, weight, and weight history information. Despite prevalent concerns regarding the accuracy of self-reported weight, we derive confidence from others' reports of high correlation between reported and actual weights for current weight (coefficient = 0.98), 4 year recall (coefficient = 0.94), and 28 year recall.28 Casey et al. also reported high correspondence between actual and recalled weight at ages 18 (coefficient = 0.87) to 40 (coefficient = 0.95) among 50 year old women.29 The high correlation (coefficients 0.85) between repeated interviews in our study provides additional reassurance regarding the reliability of our data. Further, the high response rates of cases and controls make substantial selection bias unlikely.
The study interview addressed participants' maximum and minimum lifetime weights, and the earliest ages at which they occurred. Bias may have been introduced to our calculation of ‘time since highest weight’ if women initially lost the excess weight and regained it more recently. However, such misclassification would probably attenuate our effect estimates by overestimating the duration of weight loss. In our study population, the reduced risk of endometrial cancer among women who reported that their highest weight occurred at least 5 years before their recent weight may be a conservative estimate of the protective effect of sustained weight loss.
The observed increase in endometrial risk among women with higher BMI and weight gain is consistent with the unopposed oestrogen hypothesis.30,31 Ovarian production of oestrogens ceases after menopause and adipose tissue may become the primary source of endogenous oestrogen.2,31 Women with greater body weight are also more likely to have decreased levels of SHBG, further increasing levels of bioavailable oestrogen.2,30 Exposure to oestrogens unopposed by progesterone results in proliferation of epithelial tissue in the endometrium. Heightened cellular proliferation provides greater opportunity for somatic mutations and replication errors to occur.30
Oestrogen-stimulated proliferative activity in the endometrium is mediated by insulin-like growth factor-1 (IGF-1).31 IGF-1 production is inhibited by IGFBP-1, the predominant IGF-binding protein in the endometrium. With greater body mass, especially intra-abdominal fat that may accompany adult weight gain, insulin resistance can result.31 Insulin resistance decreases IGFBP-1 levels; conversely, progesterone stimulates IGFBP-1 synthesis.31 Insulin sensitivity typically improves and levels of IGFBP-1 and SHBG increase with weight loss and physical activity.31
Among premenopausal women, obesity is not associated with increases in bioavailable oestrogen but can cause chronic anovulation.31 Anovulatory cycles are strongly associated with reductions in progesterone synthesis.31 Progesterone deficiency has been proposed as the primary mechanism for increased endometrial cancer risk among premenopausal women.30,31
|
Conclusions |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionConclusionsReferences |
|---|
Our results suggest that the maintenance of leaner body mass and persistent weight loss may reduce endometrial cancer risk.
|
Acknowledgments |
|---|
A preliminary version of this report was presented at the Society for Epidemiologic Research, Boston, MA, and is supported in part by grants from the National Cancer Institute (CA47147) and the American Cancer Society (PDT-446). The authors wish to thank Patrick Remington, Henry Anderson, Laura Stephenson, the staff of the Wisconsin Women's Health Study, and all study participants.
KEY MESSAGES
|
|
References |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionConclusionsReferences |
|---|
1 Vainio H, Bianchini F. Weight Control and Physical Activity. Lyon, France: IARC Press, 2002.
2 Hill HA, Austin H. Nutrition and endometrial cancer. Cancer Causes Control 1996;7:19–32.[CrossRef][ISI][Medline]
3 Purdie DM, Green AC. Epidemiology of endometrial cancer. Best Pract Res Clin Obstet Gynaecol 2001;15:341–54.[CrossRef][Medline]
4 Trentham-Dietz A, Newcomb PA, Egan KM et al. Weight change and risk of postmenopausal breast cancer (United States). Cancer Causes Control 2000;11:533–42.[CrossRef][ISI][Medline]
5 Ainsworth BE, Haskell WL, Leon AS et al. Compendium of physical activities: classification of energy costs of human physical activities. Med Sci Sports Exerc 1993;25:71–80.[ISI][Medline]
6 Armstrong BK, White E, Saracci R. Principles of Exposure Measurement in Epidemiology. Monographs in Epidemiology and Biostatistics. New York: Oxford University Press, 1995, pp. 78–114.
7 Le Marchand L, Wilkens LR, Mi MP. Early-age body size, adult weight gain and endometrial cancer risk. Int J Cancer 1991;48:807–11.[ISI][Medline]
8 Shu XO, Brinton LA, Zheng W et al. Relation of obesity and body fat distribution to endometrial cancer in Shanghai, China. Cancer Res 1992;52:3865–70.
9 Swanson CA, Potischman N, Wilbanks GD et al. Relation of endometrial cancer risk to past and contemporary body size and body fat distribution. Cancer Epidemiol Biomarkers Prev 1993;2:321–27.[Abstract]
10 Olson SH, Trevisan M, Marshall JR et al. Body mass index, weight gain, and risk of endometrial cancer. Nutr Cancer 1995;23:141–49.[ISI][Medline]
11 Ballard-Barbash R, Swanson CA. Body weight: estimation of risk for breast and endometrial cancers. Am J Clin Nutr 1996;63 (3 Suppl.):437S–41S.
12 Schouten LJ, Goldbohm RA, van den Brandt PA. Anthropometry, physical activity, and endometrial cancer risk: results from the Netherlands Cohort Study. J Natl Cancer Inst 2004;96:1635–38.
13 Levi F, La Vecchia C, Negri E, Parazzini F, Franceschi S. Body mass at different ages and subsequent endometrial cancer risk. Int J Cancer 1992;50:567–71.[ISI][Medline]
14 French SA, Folsom AR, Jeffery RW, Zheng W, Mink PJ, Baxter JE. Weight variability and incident disease in older women: the Iowa Women's Health Study. Int J Obes Relat Metab Disord 1997;21:217–23.[CrossRef][ISI][Medline]
15 Terry P, Baron JA, Weiderpass E, Yuen J, Lichtenstein P, Nyren O. Lifestyle and endometrial cancer risk: a cohort study from the Swedish Twin Registry. Int J Cancer 1999;82:38–42.[CrossRef][ISI][Medline]
16 Weiderpass E, Persson I, Adami HO, Magnusson C, Lindgren A, Baron JA. Body size in different periods of life, diabetes mellitus, hypertension, and risk of postmenopausal endometrial cancer (Sweden). Cancer Causes Control 2000;11:185–92.[CrossRef][ISI][Medline]
17 Popiela A, Gabrys MS, Panszczyk M. Environmental factors and risk for endometrial cancer development. Eur J Gynaecol Oncol 2003;24:209–13.[ISI][Medline]
18 Kirschner MA, Samojlik E, Drejka M, Szmal E, Schneider G, Ertel N. Androgen-estrogen metabolism in women with upper body versus lower body obesity. J Clin Endocrinol Metab 1990;70:473–79.[Abstract]
19 Lapidus L, Helgesson O, Merck C, Bjorntorp P. Adipose tissue distribution and female carcinomas. A 12-year follow-up of participants in the population study of women in Gothenburg, Sweden. Int J Obes 1988;12:361–68.[ISI][Medline]
20 Elliott EA, Matanoski GM, Rosenshein NB, Grumbine FC, Diamond EL. Body fat patterning in women with endometrial cancer. Gynecol Oncol 1990;39:253–58.[CrossRef][ISI][Medline]
21 Schapira DV, Kumar NB, Lyman GH, Cavanagh D, Roberts WS, LaPolla J. Upper-body fat distribution and endometrial cancer risk. JAMA 1991;266:1808–11.[Abstract]
22 Henderson BE, Casagrande JT, Pike MC, Mack T, Rosario I, Duke A. The epidemiology of endometrial cancer in young women. Br J Cancer 1983;47:749–56.[ISI][Medline]
23 Blitzer PH, Blitzer EC, Rimm AA. Association between teen-age obesity and cancer in 56,111 women: all cancers and endometrial carcinoma. Prev Med 1976;5:20–31.[CrossRef][ISI][Medline]
24 Newcomb PA, Trentham-Dietz A. Patterns of postmenopausal progestin use with estrogen in relation to endometrial cancer (United States). Cancer Causes Control 2003;14:195–201.[CrossRef][ISI][Medline]
25 La Vecchia C, Franceschi S, Gallus G et al. Oestrogens and obesity as risk factors for endometrial cancer in Italy. Int J Epidemiol 1982;11:120–26.
26 Potischman N, Gail MH, Troisi R, Wacholder S, Hoover RN. Measurement error does not explain the persistence of a body mass index association with endometrial cancer after adjustment for endogenous hormones. Epidemiology 1999;10:76–79.[ISI][Medline]
27 Shoff SM, Newcomb PA. Diabetes, body size, and risk of endometrial cancer. Am J Epidemiol 1998;148:234–40.
28 Stevens J, Keil JE, Waid LR, Gazes PC. Accuracy of current, 4-year, and 28-year self-reported body weight in an elderly population. Am J Epidemiol 1990;132:1156–63.
29 Casey VA, Dwyer JT, Berkey CS, Coleman KA, Gardner J, Valadian I. Long-term memory of body weight and past weight satisfaction: a longitudinal follow-up study. Am J Clin Nutr 1991;53:1493–98.
30 Akhmedkhanov A, Zeleniuch-Jacquotte A, Toniolo P. Role of exogenous and endogenous hormones in endometrial cancer: review of the evidence and research perspectives. Ann N Y Acad Sci 2001;943:296–315.
31 Kaaks R, Lukanova A, Kurzer MS. Obesity, endogenous hormones, and endometrial cancer risk: a synthetic review. Cancer Epidemiol Biomarkers Prev 2002;11:1531–43.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  J. S. Kwon and K. H. Lu Cost-Effectiveness Analysis of Endometrial Cancer Prevention Strategies for Obese Women Obstet. Gynecol., July 1, 2008; 112(1): 56 - 63. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Rapp, J. Klenk, H. Ulmer, H. Concin, G. Diem, W. Oberaigner, and J. Schroeder Weight change and cancer risk in a cohort of more than 65 000 adults in Austria Ann. Onc., April 1, 2008; 19(4): 641 - 648. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. C. Rodriguez, B.J. Rimel, W. Watkin, J. M. Turbov, C. Barry, H. Du, G. L. Maxwell, and J.M. Cline Progestin Treatment Induces Apoptosis and Modulates Transforming Growth Factor-{beta} in the Uterine Endometrium Cancer Epidemiol. Biomarkers Prev., March 1, 2008; 17(3): 578 - 584. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Lane Obesity and gynaecological cancer Menopause Int, March 1, 2008; 14(1): 33 - 37. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. L. McCullough, A. V. Patel, R. Patel, C. Rodriguez, H. S. Feigelson, E. V. Bandera, T. Gansler, M. J. Thun, and E. E. Calle Body Mass and Endometrial Cancer Risk by Hormone Replacement Therapy and Cancer Subtype Cancer Epidemiol. Biomarkers Prev., January 1, 2008; 17(1): 73 - 79. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S.-C. Chang, J. V. Lacey Jr., L. A. Brinton, P. Hartge, K. Adams, T. Mouw, L. Carroll, A. Hollenbeck, A. Schatzkin, and M. F. Leitzmann Lifetime Weight History and Endometrial Cancer Risk by Type of Menopausal Hormone Use in the NIH-AARP Diet and Health Study Cancer Epidemiol. Biomarkers Prev., April 1, 2007; 16(4): 723 - 730. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. M Webb Commentary: Weight gain, weight loss, and endometrial cancer Int. J. Epidemiol., February 1, 2006; 35(1): 166 - 168. [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||