Recent Time Trends in Uterine Cancer VICTORIA PERSKY, MD, FAITH DAVIS, PHD, RICHARD BARRETT, PHD, ELIZABETH RUBY, MS, CAROLE SAILER, BA, AND PAUL LEVY, SCD Abstract: Recent trends in corpus uterine cancer incidence rates were explored using 1979-86 data from the Surveillance and End Results Program (SEER); recent trends in hospitalizations for corpus uterine cancer were explored using 1979-86 data from National Hospital Discharge Surveys (NHDS); and recent trends in exogenous hormone use were delineated using data from the 1980, 1981, and 1985 National Ambulatory Medical Care Surveys (NAMCS). Uterine cancer incidence rates using SEER data have continued to decline since 1979. An acceleration in the decline since 1983-84 is suggested in all women and in women with intact uteri ages 45-64.
Hospitalizations for uterine cancer have also declined since 1979, with a marked acceleration in the decline since 1983-84 for all women and for women ages 40-79 has increased 22 percent and use of unopposed exogenous estrogens in women of similar age has increased 7 percent, while use of exogenous progesterones have shown much more substantial increases of approximately 700 percent. Possible relationships between trends in exogenous hormone use and incidence rates of corpus uterine cancer are discussed. (Am J Public Health 1990;80:935-939.)
Introduction
are presented as a second source of data which, in part, reflect trends in cancer incidence. The NHDS encompasses a representative sample of patients discharged from short stay hospitals, exclusive of federal hospitals, in the 50 states and the District of Columbia. No distinction in NHDS is made between initial admissions and readmissions for corpus uterine cancer. Population estimates are determined by multiplying individual data by sampling weights. In the current report, corpus uterine cancer includes ICD-9 CM code 182.0-182.8.8 Hormone use was determined from the National Ambulatory Medical Care Survey (NAMCS) conducted in 1980, 1981, and 1985 with a multistage probability sample of patient visits to office-based physicians in the United States. Physicians were asked to record up to five drugs prescribed at the visit for a random sample of office visits occurring during a randomly selected week during the year.9 10 Physicians were asked to include both prescription and non-prescription drugs. All medicines containing either estrogens or progesterones were enumerated by year. Birth control pills were not included in these analyses. Medications containing both estrogen and testosterone, however, were included. In 1980, 1981 and 1985, they accounted for an estimated 3.2 percent, 1.0 percent, and 0 percent, respectively, of all estrogens prescribed by physicians for women ages 40-79 in those years. Population estimates were determined by multiplying individual data by sampling weights. Information on age-specific populations at risk was abstracted from census data. " Cancer rates from SEER and NHDS were then calculated by dividing the age-specific estimated numbers by the age-specific populations. In addition, the populations at risk (i.e., women with intact uteri) were establishing by estimating the cumulative age-specific proportions of women who had hysterectomies from hospital discharge data and excluding them from the denominator.'2 Cohort interpolation techniques were used to estimate the proportion of women with intact uteri at single years of age between 1979 and 1986; these figures were then combined to produce five-year rates. Age-adjusted uterine cancer rates from SEER were calculated both by standardization to the 1970 population with uterine cancer not otherwise specified (NOS) included in the data for purposes of comparability to other SEER publications, and by direct standardization to the 1980 population ages 40-79 without NOS included for purposes of comparability with NHDS data. Age-adjusted hospital admissions for uterine cancer rates from NHDS were
Incidence rates of cancer of the corpus uterus showed striking increases in the early 1970s following increases in use of postmenopausal estrogens. 1-3 Subsequently, incidence rates of corpus uterine cancer declined in the late 1970s following declines in use of estrogens. ' Since 1980, there has been an increase in use of progestins cycled with estrogens in an effort to combat the carcinogenic effect of unopposed estrogens while allowing for a protective effect of estrogens on osteoporosis.4 The effect of exogenous progesterones on trends in uterine cancer, however, has not been documented. The purpose of the current paper is to delineate more recent time trends in corpus uterine cancer incidence and hospitalization rates in the 1980s in relation to the increasing use of exogenous progestins. Methods
Age-specific and age-adjusted cancer incidence rates were obtained for the years 1979 through 1986 from the Surveillance Epidemiology and End Results (SEER) Program of the National Cancer Institute. The SEER Program identifies newly diagnosed cancer cases at 11 locations, including nine in the mainland United States plus Hawaii and Puerto Rico. These data, collected since 1973-75, cover approximately 10 percent of the total population of the United States and are considered fairly representative of the US population with respect to age, although Blacks and rural populations are underrepresented. Details of the SEER data collection have been published elsewhere.5 In the current report, corpus uterine cancer includes ICD-O topography codes 180.0-182.8.6 Corpus uterine cancer hospitalization rates between 1979 and 1986 were obtained from the National Hospital Discharge Surveys (NHDS) of the National Center for Health Statistics.7 Although hospitalization rates are not an exact measure of incidence rates, analyses of trends in the NHDS Address reprint requests to Victoria Persky, MD, Epidemiology Program, School of Public Health, University of Illinois at Chicago, Box 6998, Chicago, IL 60680. Dr. Davis, Ms. Ruby, and Dr. Levy are with that same program; Dr. Barrett is with the Sociology Department at the University; Ms. Sailer is with the Epidemiology Division of the Illinois Cancer Council. This paper, submitted to the Journal May 18, 1989, was revised and accepted for publication December 26, 1989. © 1990 American Journal of Public Health 0090-0036/90$1.50
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PERSKY, ET AL. calculated for ages 40-79 by direct standardization to the 1980 population. Age-specific and age-standardized rates were averaged over two-year intervals, to increase the stability of the estimates. For the NAMCS and NHDS data, standard errors of the age-specific rates were obtained by use of charts, tables, or formulas developed by the National Center for Health Statistics for these surveys. By appropriate algebraic manipulation of these age-specific standard errors, 95 percent confidence intervals were obtained for differences between successive two-year averages of the age-adjusted rates. For the SEER data, the variance among the eight age-adjusted single year rates was computed and this estimated variance was used to obtain 95 percent confidence intervals for differences between successive two-year averages of ageadjusted rates. Also, for the SEER data, linear regression methods were used to estimate the magnitude and statistical significance of the linear component of the time trend in the age-adjusted incidence rates.
groups 45-64, with 14-27 percent declines at those ages and with no particular trends apparent in the older and younger age groups (Figure 1). As seen in Table 2, admissions for uterine cancer in the NHDS declined approximately 1-2 percent per year between the years 1979-80 and 1983-84 and 6 percent per year between 1983-84 and 1985-86. Confidence intervals for the declines in rates between 1983-84 and 1985-86, but not from 1979-80 to 1983-84, excluded zero. Overall trends were similar among different age groups (Figure 2). As shown in Table 3, between 1980 and 1985 the total number of prescriptions for estrogens increased 22 percent from 11.3 to 13.8 per 100 persons ages 40-79. When women receiving both estrogen and progesterone were subtracted from the estimate, the prescriptions for unopposed estrogen use increased only 7 percent. Confidence intervals for both these increases included zero. During the same time period, however, total progesterone prescriptions increased from 0.6 to 4.9 per 100 persons (694%) and prescriptions for both estrogens and progesterones increased from 0.2 to 1.9 per 100 persons age 40-79 (946%). Confidence intervals for the increases in progesterone use excluded zero.
Results For the SEER data, there was a consistent decline each year in the age-adjusted incidence rate from 1979 through 1986 (p 0.0001). The average yearly decline in these rates from 1983 to 1986 (0.77/105) was higher than the decline from 1979 to 1982 (0.43/105). However, the differences between the two average declines was not statistically significant. As seen in Table 1, age-adjusted uterine cancer incidence rates in SEER declined approximately 1 percent per year between 1979-80 and 1983-84 and 2-3 percent per year between 1983-84 and 1985-86 for all women and for women with intact uteri. Confidence intervals for the declines in age-adjusted rates, however, for each time period included zero. Most of the decrease in uterine cancer rates occurred in the age
Discussion
-
The overall decline in uterine cancer rates since the mid-1970s'-3 has been attributed primarily to a decrease in the use of unopposed estrogens. This paper documents the continuation of this trend from two different data sources and also suggests that since 1983-84 there may have been an acceleration in this decline in uterine cancer concomitant with little change, or even a slight increase, in unopposed estrogen use. Data from SEER, but not NHDS, suggest that the declines in uterine cancer rates may be localized to age groups between 45-64 years. Exogenous hormones are
TABLE 1-Age-Specific and Age-Adjusted Corpus Uterine Cancer Incidence Rates' per 100,000 US Women, 1979-86, for All Women and for Women with Intact Uteri, Surveillance Epidemiology and End Results (SEER)
Women with Intact Uteri
All Women
Age (years) 25-29 30-34 35-39 40-44 45-49 50-54 55-59 60-64 65-69 70-74 75-79
Age-Adjb Declinec (95% Cl)d % Declinee
Age-Adjl
Declinec (95% Cl)d % Declinee
1979-80
1981-82
1983-84
1985-86
1979-80
1981-82
1983-84
1985-86
0.7 2.3 5.5 12.2 26.6 55.1 79.4
0.9 2.8 6.7 12.1 25.8 46.1 71.4 110.3 111.9 108.8 94.9 68.0
0.7 2.6 4.8 11.4 24.3 41.0 65.2 104.6 117.5 112.4 97.4 66.5
0.8 2.1 6.0 13.1 21.9 41.6 60.0 85.9 110.7 111.5 92.6 62.0
0.7 2.5 6.4 15.6 36.7 82.7 119.2
1.0 3.0 7.8 15.6 35.8 69.2 109.8 164.1 169.8 171.9 156.0 100.0
0.7 2.8 5.6 14.6 34.5 61.3 102.1 160.5 177.5 177.0 159.3 98.5
0.8 2.3 7.0 16.9 31.6 63.1 95.2 135.5 168.7 175.1 151.0 92.7
118.3 110.1 100.9 86.8 70.2
-1.6 (-8.2,5.0)
-2.2
(-8.7,4.5) -3.1 24.5
-0.7
(-3.1,1.7) -2.9
23.1 -0.7
(-3.2,1.7) -2.9
-2.6 (-10.7,5.5) -2.5
-4.5 (-11.1,2.1) -6.8
-2.2
23.8
173.3 168.0 160.0 143.9 102.6
-1.5 (-9.6,6.5) -1.5
-5.8 (-13.9,2.3) -5.9
21.6 -1.5
(-3.9,0.9) -6.5
a) Rates were averaged for the years 1979-80, 1981-82, 1983-84, and 1985-86. b) Age-adjusted for the ages 40-79 by the direct method to the 1980 population of women ages 40-79. c) Absolute decline in age-adjusted rates. d) 95% confidence limits for the decline in age-adjusted rates. e) Percentage decline in age-adjusted rates. f) Age-adjusted for all ages by the direct method to the 1970 population.
936
AJPH August 1990, Vol. 80, No. 8
TRENDS IN UTERINE CANCER SER - Women with httct Utui
NHDS - Women wfth htoct Utri
250
jo 50-04
Age
55-8
*}44
DWogio
at
FIGURE 1-Age-Specific Uterine Cancer Incidence Rates by Year of Diagnosis: SEER-Women with Intact Uteri
FIGURE 2-Age-Specific Uterine Cancer Hospitalization Rates by Year of Hospitalization: NHDS-Women with Intact Uteri
thought to act at the promotional stage of uterine corpus carcinogenesis and to act within a short period of time: in the 1970s, trends in cancer rates followed trends in hormone use by only afew years' and case-control studiesl3 estimate latent periods of only three to six years. Thus it is possible that the decline since 1979 partly reflects a very recent increase in use of postmenopausal progestins. A protective effect of progestins is consistent with lower risks of uterine cancer observed in women on birth control pills containing both estrogens and progesterones,14-16 and with two recent studies in which post-menopausal women using estrogen-progesterone combinations were at somewhat lower risk of uterine cancer (OR = 0.6, CI = 0.2-1.4) and (OR = 0.9, CI = 0.4-2.0) than women not using hormones. '7-' Previous studies have also noted that adenomatous hyperplasia, thought to be a precursor to endometrial cancer, is reversed by the addition of progesterone.'9 Similarly, estrogen receptor activity is increased by estrogens and decreased by progesterones, lending biologic plausibility to a protective action of progesterone on estrogen-induced cancer.20 Another possible explanation for the declines in uterine cancer rates since 1979 is a protective effect of birth control
pills on cancer development, manifesting itself 10-20 years after exposure to contraceptives. Women currently ages 45-64 were ages 20-40 when oral contraceptives were first introduced. Older women were never exposed to oral contraceptives and were unlikely to have been exposed to postmenopausal progestins, which have been used only since 1970 and are used infrequently for women over age 65 years. In the current study, only 3-5 percent of progestins being prescribed for women in the years 1980, 1981, and 1985 were prescribed for women over 65 years of age. Hospital discharge data cannot accurately measure uterine cancer incidence rates because hospitalizations, rather than people, are enumerated, and the same person hospitalized repeatedly for the same illness may be counted more than once. Rates of hospitalization for cancer in NHDS are higher than cancer incidence rates in SEER.21 In the current study we found that hospitalization rates for uterine cancer based on NHDS were approximately twice the incidence rates for uterine cancer in SEER. Although much of the acceleration in the declines in hospitalizations seen since 1983-84 might be attributed to overall changes in hospitalizations secondary to the introduction of DRGs (diagnosis-
TABLE 2-Age-Specific and Age-Adjusted Hospital Admission Rates For Uterine Cancer (per 100,000) US Women, 1979-86, for all Women and for Women
with Intact Uteri, National Hospital Discharge Survey (NHDS) All Women
Age (years) 40-44 45-49 50-54 55-59
60-64 65-69 70-74 75-79
Age_adjb Declinec (95% CI)d % Decline"
Women with Intact Uteri
1979-80
1981-82
1983-84
1985-86
1979-80
1981-82
1983-84
1985-86
18.5 50.0 102.9 113.3 206.7 170.3 184.6 206.5 122.0
24.7 28.7 67.1 117.5 209.9 229.4 216.0 156.0 122.5
13.2 37.5 61.8 112.4 183.9 215.7 184.8 171.7 113.1
12.8 28.8 55.1 92.5 151.1 152.2 168.0 139.4
23.6 69.0 154.6 170.3 302.8 259.7 292.0 342.2 178.4
31.8 39.9 100.6 180.6 320.1 347.9 340.9 256.3 179.9
16.8 53.1 92.4 176.1 282.0 325.6 290.8 280.3 167.5
16.5 41.5 83.8 146.8 237.9 232.0 263.6 226.9 138.0
92.1
-8.8
-21.0
-10.8
-29.6
(-22.6,5.0)
(-30.4,-1.2)
(-31.9,10.3)
(-44.1,-1.5)
-7.3
-18.6
-6.1
-17.6
a) Rates were averaged for the years 1979-80, 1981-82, 1983-84, and 1985-86. b) Age-adjusted by the direct method to the 1980 population of US women ages 40-79 c) The decline in averaged age-adjusted rates were calculated for the time periods 1979-80 to 1983-84 and 1983-84 to 1985-86. d) 95% confidence intervals for the decline in averaged age-adjusted rates. e) The percentage decline in averaged age-adjusted rates were calculated for the time periods 1979-80 to 1983-84 and 1983-84 to 1985-86.
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PERSKY, ET AL. TABLE 3-Age-Adjusted Exogenous Hormones Use per 100 Persons by Year for Ages 40-79, Adjusted to 1980 Age Distribution, National Ambulatory Medical Care Survey (NAMCS)
Years Hormone All Estrogen
1980
1981
1985
11.29
11.23
13.81
Change 1980-85 (95% Cl)-
Percent Change 1980-85
2.52
+22%
(-1.48,6.51) Unopposed Estrogens
11.11
10.91
11.88
0.78
+7%
(-3.06,4.61) Estrogens and Progesterones All Progesterones
0.18
0.32
1.92
0.61
1.25
4.87
1.74 (0.78,2.70) 4.26 (2.96,5.55)
+946%
+694%
*95% confidence intervals for change in rate 1980-85.
related groups) preferentially affecting the elderly, the accelerations in the overall declines in incidence rates for corpus uterine cancer in SEER suggest that there may have been alterations in trends in incidence rates as well. The use of physician office visit prescriptions to estimate hormone use is subject to several potential errors. Although total use of progesterone can be approximated, use of progesterone simultaneously with estrogen cannot be precisely measured, since the NAMCS measures prescriptions at an individual visit, rather than total prescriptions. In addition, although every effort was made to eliminate birth control pills from the analysis, it is possible that some of the younger women may have been using birth control pills, rather than estrogen and progesterone, as noted. The restriction of the analyses to women ages 40-79 should minimize this error. The number of drug prescriptions may well be underestimated, since physicians were limited to a total of five drugs prescribed at each visit. A recent study using data from the National Disease and Therapeutic Index (NDTI) reported between 15 and 43 total oral estrogen mentions per 100 women ages 45-64 in 1985.4 They also noted a substantial increase in the percent of women prescribed both estrogens and progesterone. Use of both hormones account for 4 percent of all estrogen mentions in 1979 as compared to 28 percent in 1986. Unlike the NAMCS in the current study, the NDTI includes outpatient clinics, prescriptions written in hospitals, and telephone prescriptions. Since ascertainment of drug use in the NHDS, however, was similar in each year of the study, systematic underestimates of exogenous hormone use should not affect time trends. A detailed breakdown of specific estrogens used also revealed that a small percentage of women in 1980 and 1981 ingested hormones containing both estrogens and testosterone. A total of 3.2 percent of women using estrogens in 1980, 1.0 percent of women using estrogens in 1981, and 0 percent using estrogens in 1985 used medication also containing testosterone. These results are consistent with those of Hemminki, et al,4 who also noted that injected androgen/ estrogen preparations decreased from 7 percent in 1974 to 3 percent in 1986. We were not able to find any previous human studies which examined the effect of exogenous testosterone on endometrial hyperplasia. Studies in rabbits22 and in endometrial adenocarcinoma in vitro cell lines,23 however, indicate that testosterone has no effect on the development of hyperplasia or on tumor cell growth. Since only a small number of women in 1980 and 1981 were using testosterone, they were retained in the analysis. Finally, the numbers of women using progesterone in specific age strata were small, 938
precluding reports of age-specific rates. Despite the problems in estimating estrogen and progesterone use, consistency with other data and the magnitude of the increase between 1980 and 1985 support the possibility that the increase in use of progestins may be contributing to an acceleration in the decline in uterine cancer since 1984. ACKNOWLEDGMENTS The authors are deeply grateful to Hugo Koch, Health and Survey Statistician with the Division of Health Care Utilization, and to Lynn Ries, from Cancer Statistics Branch of the Surveillance and Epidemiology End Results (SEER), Division of Cancer Prevention and Control, National Cancer Institute for their patient help in analyzing the data from the National Ambulatory Care Survey and SEER. The authors also wish to express their appreciation of the personnel at the Hospital Care Statistics Branch of the Division of Health Care Statistics at the National Center of Health Statistics for their consultation in analyzing the data from the Hospital Discharge Survey. Our thanks also to Dr. John Lurain and Dr. Bill Haenszel for their insightful comments.
REFERENCES 1. Marrett LD, Meigs JW, Flannery JT: Trends in the incidence of cancer of the corpus uteri in Connecticut, 1964-1979, in relation to consumption of exogenous estrogens. Am J Epidemiol 1982; 116:57-67. 2. Jick H, Walker AM, Rothman KL: The epidemic of endometrial cancer. Am J Public Health 1980; 70:264-267. 3. Fwertz M, Jensen OM: Trends in the incidence of cancer of the corpus uterus in Denmark 1943-1980. Am J Epidemiol 1984; 119:725-732. 4. Hemminki E, Kennedy DL, Baum C, McKinlay SM: Prescribing of noncontraceptive estrogens and progestins in the United States, 1974-86. Am J Public Health 1988; 78:1479-1481. 5. Young JL, Percy CL, Asire AJ: Surveillance, Epidemiology, and End Results: Incidence and Mortality Data, 1973-77. National Cancer Institute Monograph 57, NIH Pub No. 81-2330. Bethesda, MD: NCI, 1981. 6. ICD-O International Classification of Diseases for Oncology. Geneva: World Health Organization, 1976. 7. National Center for Health Statistics, W.R. Simmons: Development of the Design of the NCHS Hospital Discharge Survey. Vital and Health Statistics. Series 2, No. 39 PHS Pub. No. 1000, Public Health Service. Washington, DC; Govt Printing Office, 1970. 8. The International Classification of Diseases 9th Revision. Clinical Modification ICD 9. CM Volume 1. Ann Arbor, MI: Edwards Brothers, 1978. 9. National Center for Health Statistics: National Ambulatory Medical Care Survey: Background and Methodology, United States, Vital and Health Statistics. Series 2 No. 61 DHEW Pub (HRA) 74-1335. Health Resources Administration. Washington, DC: Govt Printing Office, March 1974. 10. National Center for Health Statistics, Koch H: The collection and processing of drug information, National Ambulatory Medical Care Survey, United States, 1980. Vital and Health Statistics, Series 2 No. 90 DHHS Pub No. (PHS) 82-1364. Public Health Service. Washington, DC: Govt Printing Office, March 1982. 11. US Department of Commerce Bureau of Census: Estimates of the Population of the United States, by Age, Sex, and Race: 1980 to 1986. Current Population Reports. Series P-25, No. 1000. 12. US Department of Health and Human Services: Hysterectomies in the United States, 1965-84. Data from the National Health Survey, Series 13, No. 92. DHHS Pub. No. (PHS) 88-1753. Washington, DC: Govt Printing Office, 1987.
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TRENDS IN UTERINE CANCER 13. Hulka BS, Fowler WC, Kaufman DG, Grimson RC, Greenberg BG, Hogue CJR, Berger GS, Pulliam CC: Estrogen and endometrial cancer: Cases and two control groups from North Carolina. Am J Obstet Gynecol 1980; 137:92-101. 14. Centers for Disease Control: Steroid Hormone Study: Oral contraceptive use and the risk of endometrial cancer. JAMA 1983; 249:1600-1604. 15. Hulka BS, Chamless LE, Kaufman DG, Fowler WC, Greenberg BG: Protection against endometrial carcinoma by combination-product oral contraceptives. JAMA 1982; 247:475-477. 16. Kaufman DW, Shapiro S, Slone D, Rosenberg L, Miettinen OS, Stolley PD, Knapp RC, Leavitt T, Watring WG, Rosenshein NB, Lewis JL, Schottenfeld D, Engle RL: Decreased risk of endometrial cancer among oral-contraceptive users. N Engl J Med 1980; 303:1045-1047. 17. Persson IR, Adami HO, Eklund G, Johansson EDB, Lindberg BS, Lindgren A: The risk of endometrial neoplasia and treatment with estrogens and estrogen-progestogen combinations. Acta Obstet Gynecol Scand 1986; 65:211-217.
I
18. Persson I, Adami HO, Bergkvist L, Lindgren A, Pettersson B, Hoover R, Schairer C: Risk of endometrial cancer after treatment with oestrogens alone or in conjunction with progestogens: Results of a prospective study. Br Med J 1989; 278:147-151. 19. Whitehead MI, Townsend PT, Pryse-Davies J, Ryder TA, King RJB: Effects of estrogens and progestins on the biochemistry and morphology of the postmenopausal endometrium. N Engl J Med 1981; 305:1599-1605. 20. Hsueh AJW, Peck EJ Jr, Clark JH: Control of uterine estrogen receptor levels by progesterone. Endocrinology 1976; 98:438-444. 21. Centers for Disease Control, Epidemiology and Surveillance Branch, Division of Chronic Disease Control: Hospital discharge rates for four major cancers-United States, 1970-1986 MMWR 1988; 37(38) 585-588. 22. Meissner WA, Sommers SC: Endometrial changes after prolonged progesterone and testosterone administration to rabbits. Cancer Res 1966; 26:474-478. 23. Centola GM: Inhibition of endometrial carcinoma cell cultures by a synthetic androgen. Cancer Res 1985; 45:6264-6267.
Office of Minority Health Resource Center: A Nationwide Service I
A nationwide service of the Office of Minority Health (OMH) within the federal government is the OMH Resource Center, a comprehensive information and referral service designed to assist health professionals in locating hard-to-find information. There is no charge for the service. The computerized database contains a directory of current resources, information and other materials on health issues relevant to Asians/Pacific Islanders, Blacks, Hispanics, and Native Americans in the United States. The Database-Access to the database can be activated by calling OMH-RC where a knowledgeable information specialist can conduct searches of the database while you are on the telephone. The Resource Center database is organized into three types of reference information: a) organizations providing minority health-related services, community-based programs, and federally funded projects; b) information and materials by ethnic group, priority disease, or geographic area; and c) volunteer technical assistance experts. Organizations-The database includes organizations prominent in minority health, such as coalition groups, community-based organizations, reference centers, national voluntary health-related groups; government and private agencies; disease support groups; clinical services; foundations; social service organizations; educational organizations, university research centers, etc. Materials-The materials collection includes references on published and unpublished materials; federal reports; landmark studies; statistical reports; sources of foreign language materials; pamphlets; handbooks; training manuals; curricula; bibliographies; select listings by racial/ethnic groups; project reports; monographs; audiovisuals, videotapes, and audiocassettes; etc. Technical Assistance-Technicals assistance is available through a unique service called the Resource Persons Network (RPN), a cadre of 2,000 health experts who have volunteered to offer their technical expertise to community and health organizations. To reach these individuals, you need only call the Resource Center, where an information specialist will assist you in locating potential contacts. The Resource Center functions solely as a a facilitator in this type of technical assistance. Publications-The Resource Center produces and disseminates publications highlighting the minority health disparity issue, and is the distribution point for select free publications on minority health issues from federal agencies. Single copies are provided to individual requestors; bulk copies are handled as special orders by writing the OMH-RC Information Services Coordinator and specifying the number of copies desired and their intended use. These requests are handled by a separate bulk distribution center. For further information about the Resource Center, contact: Kym Collins-Lee, Office of Minority Health Resource Center (OMH-RC), P.O. Box 37337, Washington DC 20013-7227. Tel: 1-800/444/6472. Comments or inquiries for the Office of Minority Health should be directed to Annette M. Nieves, OMH, Room 118-F, HHH Building, 200 Independence Avenue, SW, Washington, DC 20201. Tel: 202/245-0020.
AJPH August 1990, Vol. 80, No. 8
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Hospitalizations for uterine cancer have also declined since 1979, with a marked acceleration in the decline since 1983-84 for all women and for women ages 40-79 has increased 22 percent and use of unopposed exogenous estrogens in women of similar age has increased 7 percent, while use of exogenous progesterones have shown much more substantial increases of approximately 700 percent. Possible relationships between trends in exogenous hormone use and incidence rates of corpus uterine cancer are discussed. (Am J Public Health 1990;80:935-939.)
Introduction
are presented as a second source of data which, in part, reflect trends in cancer incidence. The NHDS encompasses a representative sample of patients discharged from short stay hospitals, exclusive of federal hospitals, in the 50 states and the District of Columbia. No distinction in NHDS is made between initial admissions and readmissions for corpus uterine cancer. Population estimates are determined by multiplying individual data by sampling weights. In the current report, corpus uterine cancer includes ICD-9 CM code 182.0-182.8.8 Hormone use was determined from the National Ambulatory Medical Care Survey (NAMCS) conducted in 1980, 1981, and 1985 with a multistage probability sample of patient visits to office-based physicians in the United States. Physicians were asked to record up to five drugs prescribed at the visit for a random sample of office visits occurring during a randomly selected week during the year.9 10 Physicians were asked to include both prescription and non-prescription drugs. All medicines containing either estrogens or progesterones were enumerated by year. Birth control pills were not included in these analyses. Medications containing both estrogen and testosterone, however, were included. In 1980, 1981 and 1985, they accounted for an estimated 3.2 percent, 1.0 percent, and 0 percent, respectively, of all estrogens prescribed by physicians for women ages 40-79 in those years. Population estimates were determined by multiplying individual data by sampling weights. Information on age-specific populations at risk was abstracted from census data. " Cancer rates from SEER and NHDS were then calculated by dividing the age-specific estimated numbers by the age-specific populations. In addition, the populations at risk (i.e., women with intact uteri) were establishing by estimating the cumulative age-specific proportions of women who had hysterectomies from hospital discharge data and excluding them from the denominator.'2 Cohort interpolation techniques were used to estimate the proportion of women with intact uteri at single years of age between 1979 and 1986; these figures were then combined to produce five-year rates. Age-adjusted uterine cancer rates from SEER were calculated both by standardization to the 1970 population with uterine cancer not otherwise specified (NOS) included in the data for purposes of comparability to other SEER publications, and by direct standardization to the 1980 population ages 40-79 without NOS included for purposes of comparability with NHDS data. Age-adjusted hospital admissions for uterine cancer rates from NHDS were
Incidence rates of cancer of the corpus uterus showed striking increases in the early 1970s following increases in use of postmenopausal estrogens. 1-3 Subsequently, incidence rates of corpus uterine cancer declined in the late 1970s following declines in use of estrogens. ' Since 1980, there has been an increase in use of progestins cycled with estrogens in an effort to combat the carcinogenic effect of unopposed estrogens while allowing for a protective effect of estrogens on osteoporosis.4 The effect of exogenous progesterones on trends in uterine cancer, however, has not been documented. The purpose of the current paper is to delineate more recent time trends in corpus uterine cancer incidence and hospitalization rates in the 1980s in relation to the increasing use of exogenous progestins. Methods
Age-specific and age-adjusted cancer incidence rates were obtained for the years 1979 through 1986 from the Surveillance Epidemiology and End Results (SEER) Program of the National Cancer Institute. The SEER Program identifies newly diagnosed cancer cases at 11 locations, including nine in the mainland United States plus Hawaii and Puerto Rico. These data, collected since 1973-75, cover approximately 10 percent of the total population of the United States and are considered fairly representative of the US population with respect to age, although Blacks and rural populations are underrepresented. Details of the SEER data collection have been published elsewhere.5 In the current report, corpus uterine cancer includes ICD-O topography codes 180.0-182.8.6 Corpus uterine cancer hospitalization rates between 1979 and 1986 were obtained from the National Hospital Discharge Surveys (NHDS) of the National Center for Health Statistics.7 Although hospitalization rates are not an exact measure of incidence rates, analyses of trends in the NHDS Address reprint requests to Victoria Persky, MD, Epidemiology Program, School of Public Health, University of Illinois at Chicago, Box 6998, Chicago, IL 60680. Dr. Davis, Ms. Ruby, and Dr. Levy are with that same program; Dr. Barrett is with the Sociology Department at the University; Ms. Sailer is with the Epidemiology Division of the Illinois Cancer Council. This paper, submitted to the Journal May 18, 1989, was revised and accepted for publication December 26, 1989. © 1990 American Journal of Public Health 0090-0036/90$1.50
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PERSKY, ET AL. calculated for ages 40-79 by direct standardization to the 1980 population. Age-specific and age-standardized rates were averaged over two-year intervals, to increase the stability of the estimates. For the NAMCS and NHDS data, standard errors of the age-specific rates were obtained by use of charts, tables, or formulas developed by the National Center for Health Statistics for these surveys. By appropriate algebraic manipulation of these age-specific standard errors, 95 percent confidence intervals were obtained for differences between successive two-year averages of the age-adjusted rates. For the SEER data, the variance among the eight age-adjusted single year rates was computed and this estimated variance was used to obtain 95 percent confidence intervals for differences between successive two-year averages of ageadjusted rates. Also, for the SEER data, linear regression methods were used to estimate the magnitude and statistical significance of the linear component of the time trend in the age-adjusted incidence rates.
groups 45-64, with 14-27 percent declines at those ages and with no particular trends apparent in the older and younger age groups (Figure 1). As seen in Table 2, admissions for uterine cancer in the NHDS declined approximately 1-2 percent per year between the years 1979-80 and 1983-84 and 6 percent per year between 1983-84 and 1985-86. Confidence intervals for the declines in rates between 1983-84 and 1985-86, but not from 1979-80 to 1983-84, excluded zero. Overall trends were similar among different age groups (Figure 2). As shown in Table 3, between 1980 and 1985 the total number of prescriptions for estrogens increased 22 percent from 11.3 to 13.8 per 100 persons ages 40-79. When women receiving both estrogen and progesterone were subtracted from the estimate, the prescriptions for unopposed estrogen use increased only 7 percent. Confidence intervals for both these increases included zero. During the same time period, however, total progesterone prescriptions increased from 0.6 to 4.9 per 100 persons (694%) and prescriptions for both estrogens and progesterones increased from 0.2 to 1.9 per 100 persons age 40-79 (946%). Confidence intervals for the increases in progesterone use excluded zero.
Results For the SEER data, there was a consistent decline each year in the age-adjusted incidence rate from 1979 through 1986 (p 0.0001). The average yearly decline in these rates from 1983 to 1986 (0.77/105) was higher than the decline from 1979 to 1982 (0.43/105). However, the differences between the two average declines was not statistically significant. As seen in Table 1, age-adjusted uterine cancer incidence rates in SEER declined approximately 1 percent per year between 1979-80 and 1983-84 and 2-3 percent per year between 1983-84 and 1985-86 for all women and for women with intact uteri. Confidence intervals for the declines in age-adjusted rates, however, for each time period included zero. Most of the decrease in uterine cancer rates occurred in the age
Discussion
-
The overall decline in uterine cancer rates since the mid-1970s'-3 has been attributed primarily to a decrease in the use of unopposed estrogens. This paper documents the continuation of this trend from two different data sources and also suggests that since 1983-84 there may have been an acceleration in this decline in uterine cancer concomitant with little change, or even a slight increase, in unopposed estrogen use. Data from SEER, but not NHDS, suggest that the declines in uterine cancer rates may be localized to age groups between 45-64 years. Exogenous hormones are
TABLE 1-Age-Specific and Age-Adjusted Corpus Uterine Cancer Incidence Rates' per 100,000 US Women, 1979-86, for All Women and for Women with Intact Uteri, Surveillance Epidemiology and End Results (SEER)
Women with Intact Uteri
All Women
Age (years) 25-29 30-34 35-39 40-44 45-49 50-54 55-59 60-64 65-69 70-74 75-79
Age-Adjb Declinec (95% Cl)d % Declinee
Age-Adjl
Declinec (95% Cl)d % Declinee
1979-80
1981-82
1983-84
1985-86
1979-80
1981-82
1983-84
1985-86
0.7 2.3 5.5 12.2 26.6 55.1 79.4
0.9 2.8 6.7 12.1 25.8 46.1 71.4 110.3 111.9 108.8 94.9 68.0
0.7 2.6 4.8 11.4 24.3 41.0 65.2 104.6 117.5 112.4 97.4 66.5
0.8 2.1 6.0 13.1 21.9 41.6 60.0 85.9 110.7 111.5 92.6 62.0
0.7 2.5 6.4 15.6 36.7 82.7 119.2
1.0 3.0 7.8 15.6 35.8 69.2 109.8 164.1 169.8 171.9 156.0 100.0
0.7 2.8 5.6 14.6 34.5 61.3 102.1 160.5 177.5 177.0 159.3 98.5
0.8 2.3 7.0 16.9 31.6 63.1 95.2 135.5 168.7 175.1 151.0 92.7
118.3 110.1 100.9 86.8 70.2
-1.6 (-8.2,5.0)
-2.2
(-8.7,4.5) -3.1 24.5
-0.7
(-3.1,1.7) -2.9
23.1 -0.7
(-3.2,1.7) -2.9
-2.6 (-10.7,5.5) -2.5
-4.5 (-11.1,2.1) -6.8
-2.2
23.8
173.3 168.0 160.0 143.9 102.6
-1.5 (-9.6,6.5) -1.5
-5.8 (-13.9,2.3) -5.9
21.6 -1.5
(-3.9,0.9) -6.5
a) Rates were averaged for the years 1979-80, 1981-82, 1983-84, and 1985-86. b) Age-adjusted for the ages 40-79 by the direct method to the 1980 population of women ages 40-79. c) Absolute decline in age-adjusted rates. d) 95% confidence limits for the decline in age-adjusted rates. e) Percentage decline in age-adjusted rates. f) Age-adjusted for all ages by the direct method to the 1970 population.
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TRENDS IN UTERINE CANCER SER - Women with httct Utui
NHDS - Women wfth htoct Utri
250
jo 50-04
Age
55-8
*}44
DWogio
at
FIGURE 1-Age-Specific Uterine Cancer Incidence Rates by Year of Diagnosis: SEER-Women with Intact Uteri
FIGURE 2-Age-Specific Uterine Cancer Hospitalization Rates by Year of Hospitalization: NHDS-Women with Intact Uteri
thought to act at the promotional stage of uterine corpus carcinogenesis and to act within a short period of time: in the 1970s, trends in cancer rates followed trends in hormone use by only afew years' and case-control studiesl3 estimate latent periods of only three to six years. Thus it is possible that the decline since 1979 partly reflects a very recent increase in use of postmenopausal progestins. A protective effect of progestins is consistent with lower risks of uterine cancer observed in women on birth control pills containing both estrogens and progesterones,14-16 and with two recent studies in which post-menopausal women using estrogen-progesterone combinations were at somewhat lower risk of uterine cancer (OR = 0.6, CI = 0.2-1.4) and (OR = 0.9, CI = 0.4-2.0) than women not using hormones. '7-' Previous studies have also noted that adenomatous hyperplasia, thought to be a precursor to endometrial cancer, is reversed by the addition of progesterone.'9 Similarly, estrogen receptor activity is increased by estrogens and decreased by progesterones, lending biologic plausibility to a protective action of progesterone on estrogen-induced cancer.20 Another possible explanation for the declines in uterine cancer rates since 1979 is a protective effect of birth control
pills on cancer development, manifesting itself 10-20 years after exposure to contraceptives. Women currently ages 45-64 were ages 20-40 when oral contraceptives were first introduced. Older women were never exposed to oral contraceptives and were unlikely to have been exposed to postmenopausal progestins, which have been used only since 1970 and are used infrequently for women over age 65 years. In the current study, only 3-5 percent of progestins being prescribed for women in the years 1980, 1981, and 1985 were prescribed for women over 65 years of age. Hospital discharge data cannot accurately measure uterine cancer incidence rates because hospitalizations, rather than people, are enumerated, and the same person hospitalized repeatedly for the same illness may be counted more than once. Rates of hospitalization for cancer in NHDS are higher than cancer incidence rates in SEER.21 In the current study we found that hospitalization rates for uterine cancer based on NHDS were approximately twice the incidence rates for uterine cancer in SEER. Although much of the acceleration in the declines in hospitalizations seen since 1983-84 might be attributed to overall changes in hospitalizations secondary to the introduction of DRGs (diagnosis-
TABLE 2-Age-Specific and Age-Adjusted Hospital Admission Rates For Uterine Cancer (per 100,000) US Women, 1979-86, for all Women and for Women
with Intact Uteri, National Hospital Discharge Survey (NHDS) All Women
Age (years) 40-44 45-49 50-54 55-59
60-64 65-69 70-74 75-79
Age_adjb Declinec (95% CI)d % Decline"
Women with Intact Uteri
1979-80
1981-82
1983-84
1985-86
1979-80
1981-82
1983-84
1985-86
18.5 50.0 102.9 113.3 206.7 170.3 184.6 206.5 122.0
24.7 28.7 67.1 117.5 209.9 229.4 216.0 156.0 122.5
13.2 37.5 61.8 112.4 183.9 215.7 184.8 171.7 113.1
12.8 28.8 55.1 92.5 151.1 152.2 168.0 139.4
23.6 69.0 154.6 170.3 302.8 259.7 292.0 342.2 178.4
31.8 39.9 100.6 180.6 320.1 347.9 340.9 256.3 179.9
16.8 53.1 92.4 176.1 282.0 325.6 290.8 280.3 167.5
16.5 41.5 83.8 146.8 237.9 232.0 263.6 226.9 138.0
92.1
-8.8
-21.0
-10.8
-29.6
(-22.6,5.0)
(-30.4,-1.2)
(-31.9,10.3)
(-44.1,-1.5)
-7.3
-18.6
-6.1
-17.6
a) Rates were averaged for the years 1979-80, 1981-82, 1983-84, and 1985-86. b) Age-adjusted by the direct method to the 1980 population of US women ages 40-79 c) The decline in averaged age-adjusted rates were calculated for the time periods 1979-80 to 1983-84 and 1983-84 to 1985-86. d) 95% confidence intervals for the decline in averaged age-adjusted rates. e) The percentage decline in averaged age-adjusted rates were calculated for the time periods 1979-80 to 1983-84 and 1983-84 to 1985-86.
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PERSKY, ET AL. TABLE 3-Age-Adjusted Exogenous Hormones Use per 100 Persons by Year for Ages 40-79, Adjusted to 1980 Age Distribution, National Ambulatory Medical Care Survey (NAMCS)
Years Hormone All Estrogen
1980
1981
1985
11.29
11.23
13.81
Change 1980-85 (95% Cl)-
Percent Change 1980-85
2.52
+22%
(-1.48,6.51) Unopposed Estrogens
11.11
10.91
11.88
0.78
+7%
(-3.06,4.61) Estrogens and Progesterones All Progesterones
0.18
0.32
1.92
0.61
1.25
4.87
1.74 (0.78,2.70) 4.26 (2.96,5.55)
+946%
+694%
*95% confidence intervals for change in rate 1980-85.
related groups) preferentially affecting the elderly, the accelerations in the overall declines in incidence rates for corpus uterine cancer in SEER suggest that there may have been alterations in trends in incidence rates as well. The use of physician office visit prescriptions to estimate hormone use is subject to several potential errors. Although total use of progesterone can be approximated, use of progesterone simultaneously with estrogen cannot be precisely measured, since the NAMCS measures prescriptions at an individual visit, rather than total prescriptions. In addition, although every effort was made to eliminate birth control pills from the analysis, it is possible that some of the younger women may have been using birth control pills, rather than estrogen and progesterone, as noted. The restriction of the analyses to women ages 40-79 should minimize this error. The number of drug prescriptions may well be underestimated, since physicians were limited to a total of five drugs prescribed at each visit. A recent study using data from the National Disease and Therapeutic Index (NDTI) reported between 15 and 43 total oral estrogen mentions per 100 women ages 45-64 in 1985.4 They also noted a substantial increase in the percent of women prescribed both estrogens and progesterone. Use of both hormones account for 4 percent of all estrogen mentions in 1979 as compared to 28 percent in 1986. Unlike the NAMCS in the current study, the NDTI includes outpatient clinics, prescriptions written in hospitals, and telephone prescriptions. Since ascertainment of drug use in the NHDS, however, was similar in each year of the study, systematic underestimates of exogenous hormone use should not affect time trends. A detailed breakdown of specific estrogens used also revealed that a small percentage of women in 1980 and 1981 ingested hormones containing both estrogens and testosterone. A total of 3.2 percent of women using estrogens in 1980, 1.0 percent of women using estrogens in 1981, and 0 percent using estrogens in 1985 used medication also containing testosterone. These results are consistent with those of Hemminki, et al,4 who also noted that injected androgen/ estrogen preparations decreased from 7 percent in 1974 to 3 percent in 1986. We were not able to find any previous human studies which examined the effect of exogenous testosterone on endometrial hyperplasia. Studies in rabbits22 and in endometrial adenocarcinoma in vitro cell lines,23 however, indicate that testosterone has no effect on the development of hyperplasia or on tumor cell growth. Since only a small number of women in 1980 and 1981 were using testosterone, they were retained in the analysis. Finally, the numbers of women using progesterone in specific age strata were small, 938
precluding reports of age-specific rates. Despite the problems in estimating estrogen and progesterone use, consistency with other data and the magnitude of the increase between 1980 and 1985 support the possibility that the increase in use of progestins may be contributing to an acceleration in the decline in uterine cancer since 1984. ACKNOWLEDGMENTS The authors are deeply grateful to Hugo Koch, Health and Survey Statistician with the Division of Health Care Utilization, and to Lynn Ries, from Cancer Statistics Branch of the Surveillance and Epidemiology End Results (SEER), Division of Cancer Prevention and Control, National Cancer Institute for their patient help in analyzing the data from the National Ambulatory Care Survey and SEER. The authors also wish to express their appreciation of the personnel at the Hospital Care Statistics Branch of the Division of Health Care Statistics at the National Center of Health Statistics for their consultation in analyzing the data from the Hospital Discharge Survey. Our thanks also to Dr. John Lurain and Dr. Bill Haenszel for their insightful comments.
REFERENCES 1. Marrett LD, Meigs JW, Flannery JT: Trends in the incidence of cancer of the corpus uteri in Connecticut, 1964-1979, in relation to consumption of exogenous estrogens. Am J Epidemiol 1982; 116:57-67. 2. Jick H, Walker AM, Rothman KL: The epidemic of endometrial cancer. Am J Public Health 1980; 70:264-267. 3. Fwertz M, Jensen OM: Trends in the incidence of cancer of the corpus uterus in Denmark 1943-1980. Am J Epidemiol 1984; 119:725-732. 4. Hemminki E, Kennedy DL, Baum C, McKinlay SM: Prescribing of noncontraceptive estrogens and progestins in the United States, 1974-86. Am J Public Health 1988; 78:1479-1481. 5. Young JL, Percy CL, Asire AJ: Surveillance, Epidemiology, and End Results: Incidence and Mortality Data, 1973-77. National Cancer Institute Monograph 57, NIH Pub No. 81-2330. Bethesda, MD: NCI, 1981. 6. ICD-O International Classification of Diseases for Oncology. Geneva: World Health Organization, 1976. 7. National Center for Health Statistics, W.R. Simmons: Development of the Design of the NCHS Hospital Discharge Survey. Vital and Health Statistics. Series 2, No. 39 PHS Pub. No. 1000, Public Health Service. Washington, DC; Govt Printing Office, 1970. 8. The International Classification of Diseases 9th Revision. Clinical Modification ICD 9. CM Volume 1. Ann Arbor, MI: Edwards Brothers, 1978. 9. National Center for Health Statistics: National Ambulatory Medical Care Survey: Background and Methodology, United States, Vital and Health Statistics. Series 2 No. 61 DHEW Pub (HRA) 74-1335. Health Resources Administration. Washington, DC: Govt Printing Office, March 1974. 10. National Center for Health Statistics, Koch H: The collection and processing of drug information, National Ambulatory Medical Care Survey, United States, 1980. Vital and Health Statistics, Series 2 No. 90 DHHS Pub No. (PHS) 82-1364. Public Health Service. Washington, DC: Govt Printing Office, March 1982. 11. US Department of Commerce Bureau of Census: Estimates of the Population of the United States, by Age, Sex, and Race: 1980 to 1986. Current Population Reports. Series P-25, No. 1000. 12. US Department of Health and Human Services: Hysterectomies in the United States, 1965-84. Data from the National Health Survey, Series 13, No. 92. DHHS Pub. No. (PHS) 88-1753. Washington, DC: Govt Printing Office, 1987.
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TRENDS IN UTERINE CANCER 13. Hulka BS, Fowler WC, Kaufman DG, Grimson RC, Greenberg BG, Hogue CJR, Berger GS, Pulliam CC: Estrogen and endometrial cancer: Cases and two control groups from North Carolina. Am J Obstet Gynecol 1980; 137:92-101. 14. Centers for Disease Control: Steroid Hormone Study: Oral contraceptive use and the risk of endometrial cancer. JAMA 1983; 249:1600-1604. 15. Hulka BS, Chamless LE, Kaufman DG, Fowler WC, Greenberg BG: Protection against endometrial carcinoma by combination-product oral contraceptives. JAMA 1982; 247:475-477. 16. Kaufman DW, Shapiro S, Slone D, Rosenberg L, Miettinen OS, Stolley PD, Knapp RC, Leavitt T, Watring WG, Rosenshein NB, Lewis JL, Schottenfeld D, Engle RL: Decreased risk of endometrial cancer among oral-contraceptive users. N Engl J Med 1980; 303:1045-1047. 17. Persson IR, Adami HO, Eklund G, Johansson EDB, Lindberg BS, Lindgren A: The risk of endometrial neoplasia and treatment with estrogens and estrogen-progestogen combinations. Acta Obstet Gynecol Scand 1986; 65:211-217.
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18. Persson I, Adami HO, Bergkvist L, Lindgren A, Pettersson B, Hoover R, Schairer C: Risk of endometrial cancer after treatment with oestrogens alone or in conjunction with progestogens: Results of a prospective study. Br Med J 1989; 278:147-151. 19. Whitehead MI, Townsend PT, Pryse-Davies J, Ryder TA, King RJB: Effects of estrogens and progestins on the biochemistry and morphology of the postmenopausal endometrium. N Engl J Med 1981; 305:1599-1605. 20. Hsueh AJW, Peck EJ Jr, Clark JH: Control of uterine estrogen receptor levels by progesterone. Endocrinology 1976; 98:438-444. 21. Centers for Disease Control, Epidemiology and Surveillance Branch, Division of Chronic Disease Control: Hospital discharge rates for four major cancers-United States, 1970-1986 MMWR 1988; 37(38) 585-588. 22. Meissner WA, Sommers SC: Endometrial changes after prolonged progesterone and testosterone administration to rabbits. Cancer Res 1966; 26:474-478. 23. Centola GM: Inhibition of endometrial carcinoma cell cultures by a synthetic androgen. Cancer Res 1985; 45:6264-6267.
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