risk factors for breast cancer in chinese women in ... · risk factors for breast cancer in chinese...

[CANCER RESEARCH 48, 1949-1953, April 1, 1988]

â€¢1Risk Factors for Breast Cancer in Chinese Women in ShanghaiJian-Min Yuan, Mimi C. Vu,2 Ronald K. Ross, Yu-Tang Gao, and Brian E. Henderson

Shanghai Cancer Institute, Shanghai, People's Republic of China [J-M. Y., Y-T. G.]; and the Department of Preventive Medicine, University of Southern California

School of Medicine, Los Angeles, California fM. C. Y., R. K. R., B. E. H.]

ABSTRACT

Five hundred thirty-four histologically confirmed incident cases of

breast cancer in Chinese women of Shanghai and an equal number of ageand sex-matched population controls were interviewed as part of an

epidemiolÃ³gica! study of breast cancer risk factors. Early age at menarchewas positively associated with breast cancer risk whereas early age atfirst full term pregnancy, high parity, and long duration of nursing wereeach negatively associated. We found high average body weight to be arisk factor, especially among women over age 60. Use of oral contraceptives after age 45 also was a risk factor, but use in general was not.Personal history of benign breast disease and history of breast cancer infirst degree female relatives both increased risk. Multivariate analysisshowed that each of these risk (or protective) factors was independentlyrelated to breast cancer. In addition to confirming most of the breastcancer risk factors of Western populations in a low risk developing Asiancountry, this study demonstrates a clear beneficial effect on breast cancerrisk of lactation in a population characterized by a long cumulativeduration of nursing in the majority of women. Finally, this study supportsseveral other recent reports of a residual and beneficial effect of parityon breast cancer risk after controlling for age at first full term pregnancy.

INTRODUCTION

The incidence of female breast cancer in Shanghai is amongthe lowest in the world, based on data reported in the recentvolume of Cancer Incidence in Five Continents (1). During theperiod 1973-1977, the average annual age-standardized incidence rate of breast cancer in Chinese women of Shanghai was19/100,000, about one-fifth the comparable rate in U. S. whitewomen. However, breast cancer rates in young women ofShanghai (those under age 55) have been steadily increasing inrecent years (Table 1). In an attempt to explain such increasesas well as to better define the risk factors for breast cancer inChinese women, we initiated a case-control study of breastcancer among female residents of the Shanghai urban area in1984. In this paper, we describe nondietary risk factors. Dietaryfactors will be reported in a separate paper.

METHODS

Cases were histologically confirmed incident cases of breast cancerdiagnosed between June 1, 1984 and May 31, 1985 among femaleresidents of Shanghai aged 20-69 years. Cases were identified throughthe Shanghai Cancer Registry, a population-based registry covering theentire Shanghai urban area. The registry records all cases of cancer thatare microscopically verified or mentioned on a death certificate. Fivehundred sixty-eight cases were identified by the registry as eligible forinclusion in the study. We were unable to locate 30 patients, one patienthad a mental disorder, and three others refused to be interviewed. Thus,94% (534/568) of all eligible patients were interviewed.

Received 9/10/87; revised 12/18/87; accepted 1/6/88.The costs of publication of this article were defrayed in part by the payment

of page charges. This article must therefore be hereby marked advertisement inaccordance with 18 U.S.C. Section 1734 solely to indicate this fact.

1The work was supported by a grant from the Chinese Ministry of PublicHealth, Public Health Service Grant K04 CA00884 from the U.S. NationalCancer Institute, and Grant SIG-2A from the American Cancer Society. Presentedat the Fifth Symposium on Epidemiology and Cancer Registries in the PacificBasin, November 16-21, 1986, Kauai, HI.

2To whom requests for reprints should be addressed, at the Department ofPreventive Medicine, University of Southern California School of Medicine, LosAngeles, CA 90033.

Controls were chosen from the general populations of the Shanghaiurban area according to the following scheme: Shanghai is administratively divided into 1450 neighborhood committees, each of which wasassigned a unique number. We generated a list of 600 random numberswithin the range of 1 to 1450, which determined the neighborhoodcommittees from which the controls were selected, as cases enteredchronologically into the study. The matched control for the ith casewas selected from the neighborhood committee with an assigned number identical to the ith entry of the random number listing. We nextrandomly chose a household group from the approximately 20-30

household groups within each neighborhood committee. We identifiedall women belonging to the selected household group who were in thesame 5-year age group (20-24, 25-29, .. . 65-69) as the index case.We randomly chose and ranked two of these as potential controls. Thesecond control was asked to participate if the first control refused. Inall but seven instances, we interviewed the first control chosen.

All interviews were conducted in person by four trained interviewersemploying a structured questionnaire. The interview took approximately an hour and requested information on certain demographic andanthropomÃ©triecharacteristics, family history of cancer, lifetime occupational history including exposures to specific substances, smokingand drinking habits, medical and medication history including use oforal contraceptives and other hormones, exposure to x-rays, menstrualand reproductive history, and the usual adult consumption of 64 foodgroups.

All interviews were conducted in the period 1984-1985. The meantime interval between diagnosis and interview of cases was 1.83 months,and 88% of cases were interviewed within 3 months of diagnosis. Themean time interval between interview of the index case and her matchedcontrol was 3.05 months. Five-hundred and one (94%) of the 534 case-control pairs were interviewed within 6 months of each other.

We used standard matched pair methods (2) to analyze the interviewdata of the 534 completed pairs. Study variables were examined individually and then simultaneously for confounding and interaction effects. For each study variable, odds ratios (RR3 estimates) and their

corresponding P values and 95% CL were calculated. We used the exactbinomial test on individual dichotomous variables. The multivariateconditional logistic regression method was used on single variables withmore than two possible outcomes, as well as for multivariate analysis.All P values quoted are two-sided.

RESULTS

The majority (59%) of the cases were age 50 or older at thetime of diagnosis; the mean age was 50.76 years. The mean ageof the controls at the time of interview was 50.57 years. Asimilar number of cases (49%) and controls (51%) were born inShanghai. However, cases (60%) were more likely than controls(53%) to have lived primarily in a city environment before age15 (RR = 1.53, 95% CL = 1.13, 2.07 relative to a ruralenvironment). Also, cases were more educated with 11% havingattended university compared to 3% of controls (RR = 5.26,95% CL = 2.82, 9.81 relative to no formal education), eventhough cases and controls reported similar levels of familyincome at three requested time points during the previous 20years (1965, 1975, and 1982).

Table 2 presents data on menstrual and reproductive characteristics in cases versus controls. Age at menarche was inversely related to risk of breast cancer (P value for linear trend

3The abbreviations used are: RR, relative risk; CL, confidence limits; FTP,

full term pregnancy; OC, oral contraceptive.

1949

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RISK FACTORS FOR BREAST CANCER IN CHINESE WOMEN IN SHANGHAI

Table 1 Average annual age-specific incidence rates of femalebreast cancer in Shanghai

Rate/100,000

Agegroup0-1415-2425-3435-4445-5455-6465-7475+Age-standardized

(worldpopulation)rate1973-19760.00.35.727.740.957.664.652.817.61977-19800.00.36.130.047.155.053.961.218.01981-19840.00.26.243.448.759.768.459.720.9

Table 2 Menstrual and reproductive history of breast cancer cases and controls

Age at menarche(yr)18+17161514131

2 orearlierUsual

cycle length(day)24andunder25-3132

andoverNeverregularAge

at first FTP(yr)19andunder20-2425-2930

andoverNulliparousPostmenopausalNoYesAge

at menopause(yr)"44

andunder45-4950

and overCases2751891158610957373661131868182152646823430042135134Controls45659610584944521397981892230135334423330143140128RR.00.29.53.84.70.922.19.86.00.28.06.00.08.652.672.101.001.031.021.001.0995%

CL0.71,

2.370.88,2.661.06,3.210.96,

3.011.11,3.321.16,4.151.08,3.190.93,

1.760.54,2.070.74,

1.571.09,2.481.55,4.591.28,3.450.62,

1.750.62,

1.670.77,

1.56" Include only case-control pairs of age 50 and over.

test = 0.004). Women who began menstruation at age 12 oryounger had a RR of 2.19 (95% CL = 1.16, 4.15) relative tothose who began menstruation after age 17. Short menstrualcycles were associated with an increased risk of breast cancer.Women reporting usual cycle lengths of shorter than 25 dayshad a 1.86 (95% CL = 1.08, 3.19)-fold increased risk of breastcancer compared to those with cycle lengths of 25 to 31 days.A similar number of cases and controls were postmenopausal(a subject was classified as postmenopausal if there had beenno menstrual periods for at least 6 months prior to the time ofdiagnosis/interview), and most of the subjects achieved menopause naturally (91% of cases and 93% of controls). Amongpostmenopausal women, age at menopause was not significantly associated with breast cancer risk (P value for lineartrend test = 0.20). Excluding women who used oral contraceptives after age 45 did not affect the results relating to age atmenopause.

Delayed age at first FTP and nulliparity were associated witha significantly elevated risk of breast cancer. Compared toparous women whose first FTP occurred before the age of 20,those who had their first FTP after age 29 showed a RR of 2.67(95% CL = 1.55, 4.59). The comparable RR for nulliparouswomen was 2.10 (95% CL = 1.28, 3.45).

Increasing parity was significantly associated with decreasing

risk of breast cancer. The inverse association remained significant after adjustment had been made for age at first FTP andduration of nursing (Table 3). Women with five or more FTPsexperienced a risk of breast cancer only 39% that in primiparouswomen (95% CL = 0.19, 0.80). Increasing duration of nursingwas also significantly associated with decreasing risk of breastcancer. The association remained significant after we controlledfor age at first FTP and number of FTPs (Table 3). Relative towomen whose total nursing time was under 3 years, long-termnursing mothers (more than 9 years) exhibited a 63% reductionin risk of breast cancer (95% CL of RR = 0.14, 0.98). Theprotective effect of long term nursing was independent of ageat diagnosis; there was no significant interaction between ageand the effect of total years of nursing (P = 0.53).

Risk of breast cancer was positively associated with highabsolute body weight (Table 4). The RR for breast cancer inwomen weighing 60 kg or more relative to those weighing 45kg or less was 2.41 (95% CL = 1.38, 4.22). There was noincrease in risk of breast cancer among women weighing 46-60 kg relative to those weighing 45 kg or less. There was asignificant interaction between age and the effect of excessweight (P = 0.01). The elevation in risk for breast cancer amongwomen weighing over 60 kg showed a steady increase with age,and was especially pronounced in women over age 60. Amongthis group of older women, the RR for breast cancer in thoseweighing 61 kg or more relative to those weighing 50 kg or lesswas 4.34 (95% CL = 1.41, 13.37). In contrast to averageabsolute weight, high average relative weight (as measured by

Table 3 Distribution by number of FTP and duration of nursing among parouscases and controls

Pairs in which either the case or the control was nulliparous were excludedfrom the analysis. There were 429 pairs of parous women.

Number ofFTP12345+Duration

ofnursing(mo)Never1-3637-7273-108109+Cases1161137855674726596138RRControls

(95%CL)7710074611173522011040241.000.61

(0.39,0.47(0.28,0.33(0.19,0.19(0.11,1.11

(0.68,1.000.58

(0.40,0.20(0.10,0.19(0.08,0.96)0.79)0.60)0.34)1.79)0.84)0.41)0.48)Adjusted

RR(95%CL)1.00Â°0.72

(0.45,0.67(0.38,0.59(0.30,0.39(0.19,1.05(0.64,1.00*0.81

(0.53,0.35(0.16,0.37(0.14,1.16)1.21)1.16)0.80)1.72)1.25)0.79)0.98)

1RR adjusted for age at first FTP and duration of nursing.' RR adjusted for age at first FTP and number of FTP.

Table 4 Average weight of breast cancer cases and controls

Weight(kg)45

andbelow46-5051-5556-6061

andaboveUnder

age5050andbelow51-6061

andaboveAge

50-5950andbelow51-606

1 andaboveAge

60 andover50andbelow51-6061

and aboveCases88143164825710510314698724575619Controls9016914910323113102788801258704RR1.000.871.120.852.411.001.082.081.001.362.431.000.874.3495%

CL0.61,

1.260.78,1.610.56,1.271.38,4.220.74,

1.580.82,5.250.88,2.111.14,5.150.52,

1.441.41,13.37

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the Quetelet's Index = weight/height2) was only weakly asso

ciated with breast cancer risk. Nonetheless, similar to the trendobserved with absolute weight, the association with highQuetelet's Index was strongest among women age 60 or older.

A history of any OC use and the total duration of use weresimilar between cases and controls (Table 5). However, therewas a significant excess of cases who used OCs during theirperimenopausal years. Thirteen cases and only four controlsused OCs after age 45 (RR = 4.00, 95% CL = 1.15, 16.59).Furthermore, the mean duration of use after age 45 was longeramong case users relative to control users (3.5 versus 1.8 years).Seven cases but no controls reported four or more years of OCuse after age 45.

A similar number of cases and controls (48% cases, 51 %controls) reported an abortion, and the total number of abortions was comparable between the two groups (Table 5). Slightlymore cases than controls reported having had an abortion priorto first FTP (nulliparous women who had had abortions wereincluded). The excess was confined to women under age 40.Twelve cases versus five controls indicated such an experience(RR = 2.40, 95% CL = 0.84, 7.08).

Significantly more cases than controls reported a history ofbenign breast disease (RR = 4.56, 95% CL = 2.24, 9.58) (Table6). Sixty-one % of such cases were diagnosed with the benigncondition more than 10 years prior to the diagnosis of breastcancer; the mean interval was 12.8 years. Excluding those witha recent history (10 years or less) had little effect on the strengthof the association (RR = 4.60).

Table 5 Use of oral contraceptives and abortion experience among cases andcontrols

Ever usedOCNoYesDuration

(yr)4orless5-910

ormoreUsed

OC after age45NoYesEver

hadabortionNoYesTotal1234

or moreCases435996320165211327625814983188Controls43995622112530426227216482197RR1.001.061.030.971.401.004.001.000.890.850.960.891.0795%

CL0.74,

1.510.69,

1.530.49,1.890.62,3.171.15,

16.590.70,

1.150.64,

1.140.68,1.370.46,1.720.38,

3.00

Had abortion prior to first FTP 42 37 1.14 0.72,1.84Age at diagnosis (yr)

Under 40 12 5 2.40 0.84,7.0840 or over 30 32 0.93 0.54,1.58

Table 6 Personal and family history of benign breast disease and cancer

Cases Controls RR 95% CL

Personal history of benignbreast disease

No 493 525 1.00Yes 41 9 4.56 2.24,9.58

First degree relative hadcancer

No 420 429 1.00Yes 114 105 1.12 0.82,1.54

Female first degree relativehad breast cancer

No 517 528 1.00Yes 17 6 2.83 1.09,7.32

Eight cases (and five controls) reported a personal history ofother cancers and similar numbers of cases and controls reported a history of cancer among first degree relatives (RR =1.12) (Table 6). However, 17 cases compared to only six controls reported a history of breast cancer among female firstdegree relatives (RR = 2.83, 95% CL = 1.09, 7.32). Elevencases (and three controls) indicated their mother as the affectedfamily member; the remaining six cases indicated a sister as theaffected family member. Of the remaining two controls with apositive family history, one had a daughter with breast cancer,and one had a mother and a sister with breast cancer.

There was no association, positive or negative, between riskof breast cancer and occupational exposure to chemicals, cigarette smoking, and alcohol consumption. Forty-two cases and53 controls had ever smoked cigarettes (RR = 0.76, 95% CL =0.49, 1.19). Only 12 cases and 14 controls had ever drunkalcoholic beverages regularly (at least once a week).

The conditional logistic regression method was employed toexamine the simultaneous effect of all significant risk factorsidentified by the univariate analysis. When the individual riskfactors were introduced into the regression model in the ordershown in Table 7, the additional effect of each of the risk factorswas statistically significant. Similar results were obtained whenwe included childhood residence (rural, town, city) and highestlevel of formal education in the regression model prior to thestepwise procedure. Unadjusted and adjusted regression coefficients for each of the risk (or protective) factors are presentedin Table 7. Adjusted and unadjusted regression coefficientswere similar for all factors except the three highly correlatedreproductive factors: age at first FTP, number of FTPs, andduration of nursing. As expected, inclusion of these three correlated variables in a regression model weakened somewhat theassociation of each of these variables with the disease. None ofthe associations reported above showed any appreciable changewhen dietary findings were taken into consideration.

DISCUSSION

This represents the first large population-based case-controlstudy of breast cancer to be conducted in the People's Republic

of China. The study demonstrates a high degree of reproduci-bility of most established menstrual and reproductive breastcancer risk factors of Western populations in a low risk developing country. Henderson et al. (3) have interpreted these riskfactors under a unifying hypothesis that endogenous levels ofbiologically available estrogen, and perhaps prolactin, play acritical role in the genesis of breast cancer.

Onset of menstruation is shown to relate to risk over a wide

Table 7 Unadjusted and adjusted regression coefficients for various risk(or protective) factors of breast cancer

FactorAge

at menarche(yr)Usualcycle length under25daysAge

at first FTP(yr)NumberofFTPDurationof nursing(yr)Used

OC after age4561+kg averageweightHadbenign breastdiseaseFemale

first degreerelativehadbreast cancerUnadjusted

.;-0.1050.5660.072-0.229-0.1901.3860.9341.5161.041Adjusted0"-0.0780.6200.012-0.168-0.0811.8421.0681.4291.101(Two-sidedP*)(0.052)(0.043)(0.194)(0.004)(0.062)(0.008)(0.000)(0.000)(0.036)

" Parameters estimated from conditional logistic regression model which in

cluded childhood residence, highest level of formal education, and all factors inthe table.

* Two-sided P value associated with adjusted /3/SE(adjusted ÃŸ),whereSK(adjusted >Â¡)= standard error of adjusted 0.

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age range; risk increases almost monotonically with singledecrements in age at menarche. Nulliparous women are at highrisk and early age at first FTP is a protective factor for breastcancer in this population. The frequent observation (4, 5) thatrisk in women with a very late first pregnancy actually exceedsthat in nulliparous women also is confirmed in this study.

A late menopause had no apparent effect on breast cancerrisk in Shanghainese women. As observed by others studyingWestern populations (6, 7), there is an age-dependent relationship between unadjusted body weight and breast cancer risk inChinese women. The effect of high body weight is most apparent in the older age groups. This increase in breast cancer riskwith increased body weight, especially among postmenopausalwomen, might be explicable by the associated increased levelsof endogenous estrogens derived from peripheral conversion ofadrenal androgens (3).

Our study also confirms the importance of a personal historyof benign breast disease and a family history of breast cancerin a first degree relative as breast cancer risk factors in a lowrisk Asian population. The relative increase in risk associatedwith each of these conditions is at least as high as that seen inhigh risk countries (8, 9).

Two recent articles have reported a beneficial effect of lactation on risk of breast cancer in premenopausal Western women(10, 11). Our study confirms this negative association inChinese women, independent of age or menopausa! status. Thelarge cumulative number of nursing months by a high proportion of mothers in our population allows for more preciseestimates of the effects of lactation on breast cancer risk thanthose obtained from most previous epidemiolÃ³gica! studies.Henderson et al. (12) recently reviewed the epidemiolÃ³gica! andexperimental evidence which suggests that the cumulative number of ovulatory cycles is directly related to breast cancer risk.Based on this hypothesis, a beneficial effect of long duration ofnursing, as observed in the current study, comes as no surprise,as nursing results in a substantial delay in reestablishment ofovulation following a completed pregnancy.

It is useful to compare the observed risk estimates associatedwith lactation to those expected using the published statisticalmodel of breast cancer incidence of Pike et al. (5). This modelhas the form I(t) = a[d(t)]4S where I(t) is the probability of

being diagnosed with breast cancer at age t (the incidence rateat age t) and d(t) is the "relevant age" of the breast tissue. d(t)

incorporates the effects of age at menarche, age at first FTPand age at menopause: the model assumes that "breast tissueaging" starts at menarche, moves regularly at rate/) = 1 to firstFTP when there is a one-time increase in d(t). After first FTP,d(t) slows to rate fÂ¡=0.7 until age 40 when it experiences alinear decrease to 0.1 at menopause, after which the rate staysconstant at 0.1. Using a model developed by Risch et al. (13),we can calculate that 1 year of lactation results, on the average,in 8.1 months of anovulation. We can estimate that in a typicalanovulatory monthly cycle induced by lactation, breast tissueaging is comparable to that of a postmenopausal woman. Themedian age (reported age +0.5) at menarche, at first FTP, andat menopause of our population controls are 14.6, 22.7, and48.3 years, respectively. Substituting these values in the Pike etal. model, we obtained a predicted RR of 0.70 for a Shanghainese woman of age 52 (median age of our case series), whohas nursed for 5 years, relative to her counterpart who hasnever nursed. The RR actually observed in our study was 0.67.

Most previous epidemiolÃ³gica! studies have demonstrated aprotective effect on breast cancer risk of an early first FTP (8).This observation is confirmed in the current study. Recently,

several studies in other populations have observed a residualprotective effect of an increasing number of births (14-17). InShanghainese women, each subsequent full term pregnancyafter the first was associated with an approximately 15% furtherreduction in breast cancer risk after controlling for age at FTPand other menstrual and reproductive factors.

Several other factors evaluated in this study are of interest incomparison to findings from previous epidemiolÃ³gica! studiesin higher risk populations. Whereas OC use during the middlereproductive years has no apparent effect on breast cancer risk,five studies have reported on use during the perimenopausalperiod and all find some increase in risk relative to nonusers(18-22). Henderson et al. (12) have argued that this effect isexplicable on the basis of greater hormonal exposure to breasttissue when on OCs than would have "normally" occurred

during this period of frequent anovulatory cycles. We observea substantial influence of OC use during the perimenopausalperiod on breast cancer risk in Shanghai, consistent with thishypothesis.

EpidemiolÃ³gica! studies have been inconsistent in their findings relating abortion to breast cancer risk. However, twostudies concentrating on breast cancer risk following a firsttrimester abortion before a full term pregnancy in young womenall found an increase in risk (23-24). Self-reported abortionappears to be unrelated to risk overall in this low risk population, but our results are consistent with an elevation in risk inyoung women following an abortion prior to a full term pregnancy.

Significant associations between alcohol consumption andbreast cancer have recently been reported, with relative riskestimates of approximately 1.5-2.0 (25-30). No biologicalmechanism has been proposed to explain this association. Wedo not observe an association between alcohol consumptionand breast cancer risk in the present study; however, only a fewcases and controls had ever drunk alcoholic beverages at leastonce a week. It has been suggested that cigarette smoking mightprotect against breast cancer although results from previousepidemiological studies have been inconsistent (28, 31). Noassociation is apparent in Shanghai.

ACKNOWLEDGMENTS

We thank Kazuko Arakawa for her assistance in data analysis.

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1988;48:1949-1953. Cancer Res Jian-Min Yuan, Mimi C. Yu, Ronald K. Ross, et al. Risk Factors for Breast Cancer in Chinese Women in Shanghai

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