Cancer Causes and Control, 4, 355 - 360

Incidence trends for cancers of the breast, ovary, and corpus uteri in urban Shanghai, 1972-89

F a n Jin, X i a o - O u Shu, Susan S. Devesa , Wei Z h e n g , Wil l iam J. Blot, and Y u - T a n g G a o

(Received 8 February 1993; accepted in revised form 3 May 1993)

Incidence data from the Shanghai (People's Republic of China) Cancer Registry were used to assess the tem- poral trends of three major female cancers during I972-89. Rates for cancers of the breast, corpus uteri and, to a lesser extent, ovary rose over the study period. The increases in breast and ovarian cancer were most pro- nounced among women under age 50, whereas those for corpus uteri cancer were restricted generally to those aged 55 to 69 years. When considered by cohort year of birth, risk of breast and ovarian cancers rose among women born since 1925 and 1935, respectively, but little evidence of cohort effect was apparent for corpus uteri cancer. Potential explanations for these patterns are explored.

Key words: Breast cancer, corpus uteri cancer, endometrial cancer, incidence, ovary cancer, People's Republic of China, Shanghai, trends.

I n t r o d u c t i o n

Cancers of the breast, corpus uteri, and ovary share marked similarities in geographic distribution. Inci- dence rates of these cancers are high in most industrial- ized countries (except Japan), intermediate in eastern and southern Europe, and low in Asia, Africa, and central and tropical South America? These geographic differences have been attributed more to environmen- tal factors, including reproductive patterns, estrogen use, and dietary intake, than to genetic factors. 2-4

During the past several decades, incidence rates for breast cancer and, to a lesser extent, corpus uteri and ovarian cancers, have been increasing in some low-risk populations, including Chinese women living in the United States, Hong Kong, and SingaporeY Whether native Chinese also have experienced increases is of particular interest because this population not only accounts for one-fourth the global population, but also

has been undergoing dramatic economic and lifestyle changes during the last two decades.

Using data from the Shanghai Cancer Registry, we examined the incidence trends for breast, corpus uteri, and ovarian cancers during 1972-89 in Shanghai, People's Republic of China. The major findings are presented in this paper.

Mater ia ls and m e t h o d s

The Shanghai Cancer Registry is a population-based cancer registry covering an urban area with a recent population of 6.8 million people. Although the bound- aries of Shanghai and the registry coverage have changed over the years, this analysis is restricted to the 10 districts for which data are available for the entire time period. All hospitals in Shanghai are required to

Drs fin and Gao are with the Shanghai Cancer Institute, Department of Epidemiology , Shanghai, People "s Republic of China. Dr Shu is with the National Institute of Child Health and Human Development, Bethesda, MD, USA. Drs Devesa, Zheng, and Blot are with the National Cancer Institute, Bethesda MD, USA. Address correspondence to Dr Devesa, National Cancer Institute, Division of Cancer Etiology, Epidemiology and Biostatistics Program, EPN 415, Bethesda, MD 20892, USA.

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1:. Jin et al

report all newly diagnosed cancer cases to the Shanghai m 100 Cancer Registry using a standardized form? The infor- rr

Ill mation collected includes name, date of birth, sex, >. address, occupation, cancer site, and date and basis of cancer diagnosis. Patients with newly diagnosed cancer O of breast (ICD-99 code 174), corpus uteri (ICD-9 code wa: 182) and ovary (ICD-9 code 183) during 1972-89 were a. o 10 included in this study, o °

o To minimize random variation, cases were com- o m , .

bined over several years. All rates were age-adjusted n- using the standard World population in five-year age a.w groups. Population estimates were based on periodic ua censuses (1973, 1979, 1982, 1985, 1990), with age- and sex-specific intercensal estimates derived by linear 10 interpolation for intervening years. Annual percent changes in incidence were estimated by means of a lin- ear regression of the logarithm of the respective rates 100 on calendar year, weighted by the number of cases.

Results

A total of 13,261 breast cancers, 2,007 corpus uteri can- cers, and 3,228 ovarian cancers were diagnosed among female residents in urban Shanghai during 1972-89, accounting for 12.5 percent, 1.9 percent, and 3.0 per- cent of cancers among women during this time period, respectively. During 1972-89, there was a dramatic increase of almost 40 percent in the age-adjusted inci- dence rates of breast cancer, for an annual increase of 2.3 percent (Table 1). Breast cancer incidence rose from 18.3/100,000 in 1972-74, ranking third among all female cancers, to 25.1/100,000 in 1987-89, becoming the most common female cancer. The incidence of cor- pus uteri cancer rose 30 percent, or almost two percent per year, during this period. In contrast, increases in

Table 1. Age-adjusted incidence rates a of breast, ovary, and corpus uteri cancer in urban Shanghai, 1972-74 to 1987-89

Time period Breast Ovary Corpus uteri

(yr) No. Rate No. Rate No. Rate

1972-74 1,760 18.3 456 4.8 241 2.5 1975-77 1,676 16.9 400 4.0 254 2.4 1978-80 1,966 18.7 553 5.3 326 2.9 1981-83 2,167 19.8 546 4.7 343 2.9 1984-86 2,544 20.8 587 4.6 404 3.1 1987-89 3,148 25.1 686 5.2 439 3.2 Percent

change 37.6 9.5 29.6 APC b 2.3 c 0.7 1.8 °

a Per 100,000 person-years, age-adjusted dard population.

b Annual percent change. c p~< 0.01.

356 Cancer Causes and Control. Vol 4. 1993

using the World stan-

I 10

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Figure 1. Age-specific, cancer incidence rates in urban Shanghai, 1972-77 and 1984-89: breast, ovary, and corpus uteri. 12], breast 1972-77; 18, breast 1984-89; A, ovary 1972-77; &, ovary 1984-89; ©, corpus uteri 1972-74; 0, cor- pus uteri, 1984-89.

Trends for female cancers in Shanghai

Table 2. Percent changes in age-specific cancer incidence rales in urban Shanghai from 1972-77 to 1984-89

Age group Breast Ovary Corpus uteri

(yrs) Min. a % Change Min. a % Change Min." % Change

25-29 42 - 4 . 4 21 41.4 - - - - 30-34 82 48.5 21 55.4 m _ 35-39 207 82.1 31 61.8 17 -19 .6 40-44 398 104.3 68 45.1 27 11.8 45-49 534 35.1 ~ 98 - 6 . 5 64 8.9 50-54 529 11.4 122 2.1 126 3.7 55-59 474 7.4 129 - 6 . 9 84 60.0 60-64 399 2.9 98 6.5 50 74.3 65-69 311 17.1 64 33.3 40 33.7 70-74 228 13.5 54 26.3 25 10.7 75-79 113 37.6 24 36.8 13 33.4 80-84 51 43.0 12 22.5 - - - - 85+ 23 0.4 . . . .

a Minimum number of cases on which the site- and age-specific rates were based. - - minimum number = 5 or fewer cases.

age-adjusted, ovarian-cancer incidence rates were less marked.

Although increases in breast cancer appeared in vir- tually all age groups, the largest proportional changes occurred in young women (Figure 1 and Table 2). Rates among women aged 35 to 44 years increased from 82 to 104 percent from the mid-1970s to the late 1980s. Increases among women aged 50 to 74 years were minimal, whereas rates rose about 40 percent among women aged 75 to 84. Ovarian cancer increases also tended to be more marked at younger and older ages, and rates were virtually unchanged at ages 45 to 64 years. In contrast, the rises in corpus uteri cancer were restricted to women aged 55 years and older, par- ticularly at ages 55 to 69. The three cancers shared some similarities in the age-specific incidence curves, being rare among young women and increasing rapidly in late reproductive life. Differences, however, occurred after menopause, with rates plateauing for both breast and ovarian cancers, and declining for corpus uteri can- cer. The age of the peak or plateau increased over time for both ovarian and corpus uteri cancers, and was older for ovarian than for corpus uteri cancer.

When the age-specific trends were plotted according to cohort year of birth, breast cancer risks appeared to rise somewhat among women born around the turn of the century, then were fairly similar among women born from the early 1900s through about 1925, and have increased substantially among women born thereafter (Figure 2). Similar to the patterns for breast cancer, some increases in ovarian cancer risk among women born recently are suggested, in contrast to little change among women born during the earlier years. Increases in corpus uteri rates among recent birth cohorts were not apparent (not shown).

Discussion

This study revealed that incidence rates for cancers of the breast and ovary increased rapidly among young women during the last two decades in urban Shanghai, with the most striking increases for corpus uteri cancer among women aged 55 to 69 years.

These striking secular changes are unlikely to be due to changes in case ascertainment. Improvement in diag- nosis for these three cancers in Shanghai over the 18- year study period is not thought to be marked, especially since mammography is not used widely in Shanghai and the vast majority of breast cancers still are detected by physical examination. The increases also are unlikely to be explained by improvements in cancer reporting, since they persisted over 18 years, were at different speeds for the three cancers, and were distributed unevenly among women in different age groups. In fact, the operation of the Shanghai Cancer Registry has improved over the years, changing to a computerized system from a manual one, which allowed the identification and consolidation of dupli- cate records and more efficient identification of non- residents. When the registry converted from ICD-8 to ICD-9, all the original case cards were recoded. Coupled with more recent and accurate population estimates, our current rates are more likely to reflect the historical cancer experience in Shanghai than data available in the past.

It is felt generally that endogenous hormones play an important role in the development of cancers of the breast, corpus uteri, and o v a r y . 4J°'11 Early menarche, late menopause, and nulliparity have been linked con- sistently to the risk of all three cancers in many popu- lations, 3,4,12 including in Shanghai. 1~-~5 Thus, the upward

Cancer Causes and Control. Vol 4, 1993 3 5 7

F. fin et al

O9 t'r"

>-

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0 0 o 0 0 ,p-

rr" UJ 13. LLI I-- < fie

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1 I I I 1 1885 1905 1925 1845 1965 1885

COHORT YEAR OF BIRTH

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I I I 1905 1925 1945 1965

COHORT YEAR OF BIRTH

Figure 2. Age-specific cancer incidence trends in urban Shanghai by cohort year of birth: breast and ovary. D, 75-84; B, 65-74; ©, 55-64; 0, 45-54; A, 35-44; A, 25-34.

trends may be related to changes in the distribution of menstrual and reproductive factors among successive birth cohorts in urban Shanghai, 16 including a decreas- ing number of livebirths among women of repro- ductive age during the last two decades. In addition, increasing age at first livebirth, an important risk factor for breast cancer, may contribute to the rising inci- dence of this malignancyJ 7 Changes in the prevalence of other hormonally related factors, in particular obes- ity, also may account, in part, for the upward trends of endometrial cancer and postmenopausal breast cancer; documentation of changes in the prevalence of obesity among Shanghai women is not available at this time, however.

In the early 1970s, there was a striking increase of corpus uteri cancer in the United States and other west- ern countries, followed by a decline in the late 1970s) 8-21 Women aged 45 to 64 years experienced both the largest increase and decline. This trend has been attributed to the widespread use of unopposed estro- gen replacement therapy in the late 1960s and early 1970s, followed by a dramatic reduction in exposure during the late 1970s in these countries. Estrogen use among peri- and postmenopausal women in urban Shanghai remains low, 15 but its increased use over the last two decades may contribute to the increases in cor- pus uteri cancer seen among women aged 55 to 64. Since estrogen use is related only weakly to the risk of breast or ovarian cancer, 22-23 the low prevalence of estrogen use in Shanghai may have limited its impact on the incidence of these cancers among women of peri- and postmenopausal ages.

Oral contraceptive (OC) use has been shown to be a

358 Cancer Causes and Control. Vol 4. 1993

strong protector against cancers of the corpus uteri and ovary? ,4,24 However, its use, particularly before a first- term pregnancy, appears linked to an elevated risk of breast cancer among young women. 25 Thus, increased use of OCs could amplify risk of breast cancer but off- set the risk of corpus uteri and ovarian cancers among young females in Shanghai who are changing their reproductive patterns. Indeed, breast cancer among women aged 35 to 44 increased rapidly in the late 1970s, shortly after the introduction of OCs. By 1984-85, about 12 percent of reproductive-age women had ever used OCs? 6 Use is more common among parous than nulliparous Shanghai women, perhaps contributing to the larger increases in breast cancer at older childbearing ages (35 to 44 years) instead of younger ages (25 to 34 years).

Dietary and nutritional factors, especially fat intake, have been suggested to influence risk for corpus uteri cancer and perhaps breast and ovarian cancers as well. 27-3° Lactose intake from dairy products has been linked to the risk of ovarian cancer. 31 In Shanghai, the per capita consumption of pork, poultry, eggs, and milk products in 1982 was two to three times that in 1956, 32 and studies there have associated these foods with risk of endometria133 and ovarian 34 cancers. There is also some evidence suggesting that dietary fat might be related to the risk of breast cancer in Shanghai." Thus, the increasing intake of dietary fat, particularly fat from foods of animal origin, may contribute to the rising trends of these cancers. In the analytic studies, however, the dietary fat effect did not vary with age? TM

Therefore, the increases in ovarian and breast cancers at younger and older ages, in contrast to those of corpus

Trends for female cancers in Shanghai

uteri cancer at the middle ages, are unlikely to be explained solely by dietary changes, and suggest the interplay of several factors.

In summary, incidence rates for cancers of the breast, corpus uteri, and to a lesser extent, ovary have been increasing over the past two decades in urban Shanghai. These increases are likely to be due to changes in menstrual and reproductive patterns, diet- ary intake, and use of hormonal products. The age ~pe- cific trends suggest some similarities in the changing risks for breast and ovarian cancers, in contrast to those for corpus uteri cancer. Further analytic studies will be needed to confirm these observations and to provide strategies for primary prevention of these cancers.

Acknowledgements--We thank Mss Shu-Zen Zhou, Rong-Fang Tiao, Ai-Qing Chen, Ru-Rong Fang, and Mr Yi-Ling Jiang of the Shanghai Cancer Registry for their assistance in data collection and management; and Dr Yong-Bing Xiang and Ms Lu Sun of the Shanghai Cancer Institute, and Ms Ruth Parsons and Mr Gray Williams of IMS Inc, for their assistance in data pre- paration and computing.

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