Risk Factors for Breast Cancer in Chinese

Risk Factors for Breast Cancer in Chinese

[CANCER RESEARCH 48, 1949-1953, April 1, 1988]
Risk Factors for Breast Cancer in Chinese Women in Shanghai
•1
Jian-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 age
and sex-matched population controls were interviewed as part of an
epidemiológica! study of breast cancer risk factors. Early age at menarche
was positively associated with breast cancer risk whereas early age at
first full term pregnancy, high parity, and long duration of nursing were
each negatively associated. We found high average body weight to be a
risk factor, especially among women over age 60. Use of oral contracep
tives 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 in
first degree female relatives both increased risk. Multivariate analysis
showed that each of these risk (or protective) factors was independently
related to breast cancer. In addition to confirming most of the breast
cancer risk factors of Western populations in a low risk developing Asian
country, this study demonstrates a clear beneficial effect on breast cancer
risk of lactation in a population characterized by a long cumulative
duration of nursing in the majority of women. Finally, this study supports
several other recent reports of a residual and beneficial effect of parity
on breast cancer risk after controlling for age at first full term pregnancy.
INTRODUCTION
The incidence of female breast cancer in Shanghai is among
the lowest in the world, based on data reported in the recent
volume of Cancer Incidence in Five Continents (1). During the
period 1973-1977, the average annual age-standardized inci
dence rate of breast cancer in Chinese women of Shanghai was
19/100,000, about one-fifth the comparable rate in U. S. white
women. However, breast cancer rates in young women of
Shanghai (those under age 55) have been steadily increasing in
recent years (Table 1). In an attempt to explain such increases
as well as to better define the risk factors for breast cancer in
Chinese women, we initiated a case-control study of breast
cancer among female residents of the Shanghai urban area in
1984. In this paper, we describe nondietary risk factors. Dietary
factors will be reported in a separate paper.
METHODS
Cases were histologically confirmed incident cases of breast cancer
diagnosed between June 1, 1984 and May 31, 1985 among female
residents of Shanghai aged 20-69 years. Cases were identified through
the Shanghai Cancer Registry, a population-based registry covering the
entire Shanghai urban area. The registry records all cases of cancer that
are microscopically verified or mentioned on a death certificate. Five
hundred sixty-eight cases were identified by the registry as eligible for
inclusion in the study. We were unable to locate 30 patients, one patient
had a mental disorder, and three others refused to be interviewed. Thus,
94% (534/568) of all eligible patients were interviewed.
Controls were chosen from the general populations of the Shanghai
urban area according to the following scheme: Shanghai is administra
tively divided into 1450 neighborhood committees, each of which was
assigned a unique number. We generated a list of 600 random numbers
within the range of 1 to 1450, which determined the neighborhood
committees from which the controls were selected, as cases entered
chronologically into the study. The matched control for the ith case
was selected from the neighborhood committee with an assigned num
ber identical to the ith entry of the random number listing. We next
randomly chose a household group from the approximately 20-30
household groups within each neighborhood committee. We identified
all women belonging to the selected household group who were in the
same 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. The
second control was asked to participate if the first control refused. In
all but seven instances, we interviewed the first control chosen.
All interviews were conducted in person by four trained interviewers
employing a structured questionnaire. The interview took approxi
mately an hour and requested information on certain demographic and
anthropométriecharacteristics, family history of cancer, lifetime occu
pational history including exposures to specific substances, smoking
and drinking habits, medical and medication history including use of
oral contraceptives and other hormones, exposure to x-rays, menstrual
and reproductive history, and the usual adult consumption of 64 food
groups.
All interviews were conducted in the period 1984-1985. The mean
time interval between diagnosis and interview of cases was 1.83 months,
and 88% of cases were interviewed within 3 months of diagnosis. The
mean time interval between interview of the index case and her matched
control was 3.05 months. Five-hundred and one (94%) of the 534 casecontrol pairs were interviewed within 6 months of each other.
We used standard matched pair methods (2) to analyze the interview
data of the 534 completed pairs. Study variables were examined indi
vidually and then simultaneously for confounding and interaction ef
fects. For each study variable, odds ratios (RR3 estimates) and their
corresponding P values and 95% CL were calculated. We used the exact
binomial test on individual dichotomous variables. The multivariate
conditional logistic regression method was used on single variables with
more 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 the
time of diagnosis; the mean age was 50.76 years. The mean age
of the controls at the time of interview was 50.57 years. A
similar number of cases (49%) and controls (51%) were born in
Shanghai. However, cases (60%) were more likely than controls
(53%) to have lived primarily in a city environment before age
15 (RR = 1.53, 95% CL = 1.13, 2.07 relative to a rural
environment). Also, cases were more educated with 11% having
attended university compared to 3% of controls (RR = 5.26,
95% CL = 2.82, 9.81 relative to no formal education), even
though cases and controls reported similar levels of family
income at three requested time points during the previous 20
years (1965, 1975, and 1982).
Table 2 presents data on menstrual and reproductive char
acteristics in cases versus controls. Age at menarche was in
versely related to risk of breast cancer (P value for linear trend
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 in
accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
1The work was supported by a grant from the Chinese Ministry of Public
Health, Public Health Service Grant K04 CA00884 from the U.S. National
Cancer Institute, and Grant SIG-2A from the American Cancer Society. Presented
at the Fifth Symposium on Epidemiology and Cancer Registries in the Pacific
Basin, November 16-21, 1986, Kauai, HI.
2 To whom requests for reprints should be addressed, at the Department of
3The abbreviations used are: RR, relative risk; CL, confidence limits; FTP,
Preventive Medicine, University of Southern California School of Medicine, Los
full term pregnancy; OC, oral contraceptive.
Angeles, CA 90033.
1949
RISK FACTORS FOR BREAST CANCER IN CHINESE WOMEN IN SHANGHAI
Table 1 Average annual age-specific incidence rates of female
breast cancer in Shanghai
risk of breast cancer. The inverse association remained signifi
cant after adjustment had been made for age at first FTP and
Rate/100,000
duration of nursing (Table 3). Women with five or more FTPs
group0-1415-2425-3435-4445-5455-6465-7475+Age-standardized
Age
experienced a risk of breast cancer only 39% that in primiparous
women (95% CL = 0.19, 0.80). Increasing duration of nursing
was also significantly associated with decreasing risk of breast
cancer. The association remained significant after we controlled
for age at first FTP and number of FTPs (Table 3). Relative to
women whose total nursing time was under 3 years, long-term
nursing mothers (more than 9 years) exhibited a 63% reduction
(worldpopulation)
in risk of breast cancer (95% CL of RR = 0.14, 0.98). The
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
protective effect of long term nursing was independent of age
at diagnosis; there was no significant interaction between age
and the effect of total years of nursing (P = 0.53).
Table 2 Menstrual and reproductive history of breast cancer cases and controls
Risk of breast cancer was positively associated with high
CL0.71,
absolute body weight (Table 4). The RR for breast cancer in
Age
(yr)18+17161514131
at menarche
women weighing 60 kg or more relative to those weighing 45
kg or less was 2.41 (95% CL = 1.38, 4.22). There was no
2.370.88,
2.661.06,3.210.96, increase in risk of breast cancer among women weighing 4660 kg relative to those weighing 45 kg or less. There was a
3.011.11,3.321.16,4.151.08,3.190.93,
significant interaction between age and the effect of excess
earlierUsual
2 or
weight (P = 0.01). The elevation in risk for breast cancer among
women weighing over 60 kg showed a steady increase with age,
(day)24
cycle length
and was especially pronounced in women over age 60. Among
under25-3132
and
this group of older women, the RR for breast cancer in those
overNever
and
1.760.54,
weighing 61 kg or more relative to those weighing 50 kg or less
2.070.74,
regularAge
was 4.34 (95% CL = 1.41, 13.37). In contrast to average
(yr)19
at first FTP
absolute weight, high average relative weight (as measured by
under20-2425-2930
and
overNulliparousPostmenopausalNoYesAge
and
1.571.09,2.481.55,4.591.28,3.450.62,
Table 3 Distribution by number of FTP and duration of nursing among parous
cases and controls
Pairs in which either the case or the control was nulliparous were excluded
from the analysis. There were 429 pairs of parous women.
RR
CL)7710074611173522011040241.000.61
(95%
CL)1.00°0.72
(95%
1.750.62,
Number
FTP12345+Duration
of
(yr)"44
at menopause
under45-4950
and
1.670.77,
(0.39,0.47
(0.45,0.67
(0.28,0.33(0.19,0.19(0.11,1.11
(0.38,0.59
1.56
and overCases2751891158610957373661131868182152646823430042135134Controls45659610584944521397981892230135334423330143140128RR.00.29.53.84.70.922.19.86.00.28.
(0.30,0.39(0.19,1.05(0.64,1.00*0.81
" Include only case-control pairs of age 50 and over.
nursing(mo)Never1-3637-7273-108109+Cases1161137855674726596138RRControls
of
test = 0.004). Women who began menstruation at age 12 or
younger had a RR of 2.19 (95% CL = 1.16, 4.15) relative to
those who began menstruation after age 17. Short menstrual
cycles were associated with an increased risk of breast cancer.
Women reporting usual cycle lengths of shorter than 25 days
had a 1.86 (95% CL = 1.08, 3.19)-fold increased risk of breast
cancer 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 been
no menstrual periods for at least 6 months prior to the time of
diagnosis/interview), and most of the subjects achieved meno
pause naturally (91% of cases and 93% of controls). Among
postmenopausal women, age at menopause was not signifi
cantly associated with breast cancer risk (P value for linear
trend test = 0.20). Excluding women who used oral contracep
tives after age 45 did not affect the results relating to age at
menopause.
Delayed age at first FTP and nulliparity were associated with
a significantly elevated risk of breast cancer. Compared to
parous 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 nulliparous
women was 2.10 (95% CL = 1.28, 3.45).
Increasing parity was significantly associated with decreasing
1950
(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
(0.53,0.35(0.16,0.37(0.14,1.16)1.21)1
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
(kg)45
Weight
CL0.61,
below46-5051-5556-6061
and
1.260.78,
1.610.56,
1.271.38,4.220.74,
aboveUnder
and
5050 age
below51-6061
and
aboveAge
and
1.580.82,
5.250.88,2.111.14,5.150.52,
50-5950
below51-606
and
aboveAge
1 and
over50
60 and
below51-6061
and
1.441.41,
and aboveCases88143164825710510314698724575619Controls90169149103231131027888
13.37
RISK FACTORS FOR BREAST CANCER IN CHINESE WOMEN IN SHANGHAI
the Quetelet's Index = weight/height2) was only weakly asso
ciated with breast cancer risk. Nonetheless, similar to the trend
observed with absolute weight, the association with high
Quetelet's Index was strongest among women age 60 or older.
A history of any OC use and the total duration of use were
similar between cases and controls (Table 5). However, there
was a significant excess of cases who used OCs during their
perimenopausal years. Thirteen cases and only four controls
used OCs after age 45 (RR = 4.00, 95% CL = 1.15, 16.59).
Furthermore, the mean duration of use after age 45 was longer
among case users relative to control users (3.5 versus 1.8 years).
Seven cases but no controls reported four or more years of OC
use after age 45.
A similar number of cases and controls (48% cases, 51 %
controls) reported an abortion, and the total number of abor
tions was comparable between the two groups (Table 5). Slightly
more cases than controls reported having had an abortion prior
to first FTP (nulliparous women who had had abortions were
included). 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 of
benign breast disease (RR = 4.56, 95% CL = 2.24, 9.58) (Table
6). Sixty-one % of such cases were diagnosed with the benign
condition more than 10 years prior to the diagnosis of breast
cancer; the mean interval was 12.8 years. Excluding those with
a recent history (10 years or less) had little effect on the strength
of the association (RR = 4.60).
Table 5 Use of oral contraceptives and abortion experience among cases and
controls
CL0.74,
Ever
OCNoYesDuration
used
1.510.69,
(yr)4
less5-910
or
1.530.49,
1.890.62,
3.171.15,
moreUsed
or
Eight cases (and five controls) reported a personal history of
other cancers and similar numbers of cases and controls re
ported a history of cancer among first degree relatives (RR =
1.12) (Table 6). However, 17 cases compared to only six con
trols reported a history of breast cancer among female first
degree relatives (RR = 2.83, 95% CL = 1.09, 7.32). Eleven
cases (and three controls) indicated their mother as the affected
family member; the remaining six cases indicated a sister as the
affected family member. Of the remaining two controls with a
positive 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 risk
of breast cancer and occupational exposure to chemicals, ciga
rette smoking, and alcohol consumption. Forty-two cases and
53 controls had ever smoked cigarettes (RR = 0.76, 95% CL =
0.49, 1.19). Only 12 cases and 14 controls had ever drunk
alcoholic beverages regularly (at least once a week).
The conditional logistic regression method was employed to
examine the simultaneous effect of all significant risk factors
identified by the univariate analysis. When the individual risk
factors were introduced into the regression model in the order
shown in Table 7, the additional effect of each of the risk factors
was statistically significant. Similar results were obtained when
we included childhood residence (rural, town, city) and highest
level of formal education in the regression model prior to the
stepwise procedure. Unadjusted and adjusted regression coef
ficients for each of the risk (or protective) factors are presented
in Table 7. Adjusted and unadjusted regression coefficients
were similar for all factors except the three highly correlated
reproductive factors: age at first FTP, number of FTPs, and
duration of nursing. As expected, inclusion of these three cor
related variables in a regression model weakened somewhat the
association of each of these variables with the disease. None of
the associations reported above showed any appreciable change
when dietary findings were taken into consideration.
DISCUSSION
45NoYesEver
OC after age
This represents the first large population-based case-control
study of breast cancer to be conducted in the People's Republic
of China. The study demonstrates a high degree of reproduciabortionNoYesTotal1234
had
bility of most established menstrual and reproductive breast
1.150.64,
cancer risk factors of Western populations in a low risk devel
oping country. Henderson et al. (3) have interpreted these risk
1.140.68,
1.370.46,
factors under a unifying hypothesis that endogenous levels of
1.720.38,
biologically available estrogen, and perhaps prolactin, play a
or moreCases435996320165211327625814983188Controls43995622112530426227216482197RR1.001.061.030.971.401.004.001.000.890.850.960.891.0795%
3.00
critical role in the genesis of breast cancer.
Had abortion prior to first FTP
42
37
1.14 0.72,1.84
Onset of menstruation is shown to relate to risk over a wide
16.590.70,
Age at diagnosis (yr)
Under 40
40 or over
12
30
5
32
2.40
0.93
0.84,7.08
0.54,1.58
Table 6 Personal and family history of benign breast disease and cancer
Cases
Controls
RR
95% CL
Personal history of benign
breast disease
No
Yes
493
41
525
9
1.00
4.56
2.24,9.58
First degree relative had
cancer
No
Yes
420
114
429
105
1.00
1.12
0.82,1.54
Female first degree relative
had breast cancer
No
Yes
517
17
528
6
1.00
2.83
1.09,7.32
Table 7 Unadjusted and adjusted regression coefficients for various risk
(or protective) factors of breast cancer
0"-0.0780.6200.012-0.168-0.0811.8421.0681.429
P*)(0.052)(0.043)(0.194)(0.004)
.;-0.1050.5660.072-0.229-0.1901.3860.9341.5161.041Adjusted
FactorAge
(yr)Usual
at menarche
25daysAge
cycle length under
(yr)Number
at first FTP
FTPDuration
of
(yr)Used of nursing
4561+OC after age
weightHad
kg average
diseaseFemale
benign breast
relativehad
first degree
breast cancerUnadjusted
" Parameters estimated from conditional logistic regression model which in
cluded childhood residence, highest level of formal education, and all factors in
the table.
* Two-sided P value associated with adjusted /3/SE(adjusted ß),where
SK(adjusted >¡)
= standard error of adjusted 0.
1951
RISK FACTORS FOR BREAST CANCER IN CHINESE WOMEN IN SHANGHAI
age range; risk increases almost monotonically with single
decrements in age at menarche. Nulliparous women are at high
risk and early age at first FTP is a protective factor for breast
cancer in this population. The frequent observation (4, 5) that
risk in women with a very late first pregnancy actually exceeds
that in nulliparous women also is confirmed in this study.
A late menopause had no apparent effect on breast cancer
risk in Shanghainese women. As observed by others studying
Western populations (6, 7), there is an age-dependent relation
ship between unadjusted body weight and breast cancer risk in
Chinese women. The effect of high body weight is most appar
ent in the older age groups. This increase in breast cancer risk
with increased body weight, especially among postmenopausal
women, might be explicable by the associated increased levels
of endogenous estrogens derived from peripheral conversion of
adrenal androgens (3).
Our study also confirms the importance of a personal history
of benign breast disease and a family history of breast cancer
in a first degree relative as breast cancer risk factors in a low
risk Asian population. The relative increase in risk associated
with each of these conditions is at least as high as that seen in
high risk countries (8, 9).
Two recent articles have reported a beneficial effect of lacta
tion on risk of breast cancer in premenopausal Western women
(10, 11). Our study confirms this negative association in
Chinese women, independent of age or menopausa! status. The
large cumulative number of nursing months by a high propor
tion of mothers in our population allows for more precise
estimates of the effects of lactation on breast cancer risk than
those obtained from most previous epidemiológica! studies.
Henderson et al. (12) recently reviewed the epidemiológica! and
experimental evidence which suggests that the cumulative num
ber of ovulatory cycles is directly related to breast cancer risk.
Based on this hypothesis, a beneficial effect of long duration of
nursing, as observed in the current study, comes as no surprise,
as nursing results in a substantial delay in reestablishment of
ovulation following a completed pregnancy.
It is useful to compare the observed risk estimates associated
with lactation to those expected using the published statistical
model of breast cancer incidence of Pike et al. (5). This model
has 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 rate
at 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 FTP
and age at menopause: the model assumes that "breast tissue
aging" starts at menarche, moves regularly at rate/) = 1 to first
FTP when there is a one-time increase in d(t). After first FTP,
d(t) slows to rate f¡=0.7 until age 40 when it experiences a
linear decrease to 0.1 at menopause, after which the rate stays
constant 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 typical
anovulatory monthly cycle induced by lactation, breast tissue
aging is comparable to that of a postmenopausal woman. The
median age (reported age +0.5) at menarche, at first FTP, and
at menopause of our population controls are 14.6, 22.7, and
48.3 years, respectively. Substituting these values in the Pike et
al. model, we obtained a predicted RR of 0.70 for a Shan
ghainese woman of age 52 (median age of our case series), who
has nursed for 5 years, relative to her counterpart who has
never nursed. The RR actually observed in our study was 0.67.
Most previous epidemiológica! studies have demonstrated a
protective 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 residual
protective effect of an increasing number of births (14-17). In
Shanghainese women, each subsequent full term pregnancy
after the first was associated with an approximately 15% further
reduction in breast cancer risk after controlling for age at FTP
and other menstrual and reproductive factors.
Several other factors evaluated in this study are of interest in
comparison to findings from previous epidemiológica! studies
in higher risk populations. Whereas OC use during the middle
reproductive years has no apparent effect on breast cancer risk,
five studies have reported on use during the perimenopausal
period and all find some increase in risk relative to nonusers
(18-22). Henderson et al. (12) have argued that this effect is
explicable on the basis of greater hormonal exposure to breast
tissue when on OCs than would have "normally" occurred
during this period of frequent anovulatory cycles. We observe
a substantial influence of OC use during the perimenopausal
period on breast cancer risk in Shanghai, consistent with this
hypothesis.
Epidemiológica! studies have been inconsistent in their find
ings relating abortion to breast cancer risk. However, two
studies concentrating on breast cancer risk following a first
trimester abortion before a full term pregnancy in young women
all found an increase in risk (23-24). Self-reported abortion
appears to be unrelated to risk overall in this low risk popula
tion, but our results are consistent with an elevation in risk in
young women following an abortion prior to a full term preg
nancy.
Significant associations between alcohol consumption and
breast cancer have recently been reported, with relative risk
estimates of approximately 1.5-2.0 (25-30). No biological
mechanism has been proposed to explain this association. We
do not observe an association between alcohol consumption
and breast cancer risk in the present study; however, only a few
cases and controls had ever drunk alcoholic beverages at least
once a week. It has been suggested that cigarette smoking might
protect against breast cancer although results from previous
epidemiological studies have been inconsistent (28, 31). No
association is apparent in Shanghai.
ACKNOWLEDGMENTS
We thank Kazuko Arakawa for her assistance in data analysis.
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