Breast Cancer Screening in Taiwan and China

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					Breast Disease 13 (2001) 41–48                                                                                         41
IOS Press




Breast Cancer Screening in Taiwan and China
                          a,*                       a          microcalcifications, along with mammography within a long
Chiun-Sheng Huang King-Jen Chang ,                             period, may provide more effective protection for Taiwanese
                   *
Chen-Yang Shenb,                                               and Chinese women against breast cancer.
a
  Department of Surgery, National Taiwan
University Hospital, Taipei, 100, Taiwan
                                                               BREAST CANCER IN CHINESE
Tel.: +886 2 23123456 ext 5080; Fax: +886                      POPULATIONS
2 2392 8856;E-mail:
cshuang@ha.mc.ntu.edu.tw                                          In contrast to incidence rates prevailing in
b
  Institute of Biomedical Sciences, Academia                   women in Western countries, the women in Tai-
Sinica, Taipei, 115, Taiwan                                    wan and China are considered to have the lowest
Tel.: +886 2 789 9036; Fax: +886 2 2782                        incidence of breast cancer in the world. The age-
3047; E-mail: bmcys@ccvax.sinica.edu.tw                        adjusted breast cancer incidence rate of 1996 in
                                                               Taiwanese women was 26.65/100,000 [1]. This
ABSTRACT: In contrast to incidence rates prevailing in         figure is comparable to that in women living in
women in Western countries, Chinese women in Taiwan and        urban areas in China. On the basis of a prospec-
China are considered to have the lowest incidence of breast    tive survey, in women in Shanghai, the largest
cancer in the world. However, in the past 20 years, breast     city on the east coast of China, the breast cancer
cancer incidence in Chinese women has seen a dramatic
increase of 50–100%, which strongly supports the need for
                                                               incidence was 26.5/100,000 from 1988 to 1992
breast cancer prevention and screening programs. It is also    [2,3], which is about only one-fourth to one-third
important to indicate that breast cancer in Chinese women is   the incidence in white women in Western popu-
characterized by younger age at tumor onset. More than         lations. Given the dominant contribution of es-
50% of the total breast cancer diagnosed annually is found     trogen to breast cancer development, the low in-
in premenopausal patients, creating the need to initiate
breast cancer screening programs in this popula-               cidence in Chinese women can be attributable to
tion. Initially, the breast cancer screening program de-       lower estrogen level. On average, Asian women
pended on breast self-examination. Since Chinese women         have 20% lower serum estradiol levels than
have relatively small breasts, it was assumed that breast      Western women [4], which could be related to
cancer was easier to detect by self-examination. However,
this strategy has failed. The dilemma of breast cancer
                                                               late menarche, early menopause, less common
screening can be summarized by the fact that Chinese have a    postmenopausal obesity, low fat or cholesterol
rapidly increasing incidence of premenopausal breast cancer,   intake from Eastern diets, or a combination of
while the overall incidence is still low. Therefore, since     these factors.
premenopausal women have denser breasts than postmeno-            In addition to environmental and dietary fac-
pausal women, and Chinese women have smaller breasts and
a higher percentage of dense breasts, increased mammogra-      tors, the low incidence of breast cancer in Chi-
phy screening frequency may be not the sole solution to        nese women also may be associated with differ-
increase detection in this age group. In our experience in     ent genetic background. For incidence, a high
Taiwan, the addition of breast ultrasound may be helpful.      frequency of high-activity alleles/genotypes of
Nearly all the nonpalpable cancers detected by mammogra-
phy in our women are due to microcalcifications, and ultra-
                                                               COMT, a gene involved in inactivation of the
sound is more sensitive in detecting nonpalpable cancers;      reactive metabolites of estrogen, has been identi-
Therefore, we suggest that a screening program, based on       fied in our population (e.g. >95% of women have
ultrasound to detect nonpalpable cancers not associated with   low-risk genotypes versus 72–87% in Western
                                                               women) [5]. This would contribute to markedly
*
 Corresponding authors: Chiun-Sheng Huang and Chen-            lower exposure of breast epithelium to tumori-
Yang Shen                                                      genic estrogen metabolites, which also might ex-

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42                     C.-S. Huang et al. / Breast Cancer Screening in Taiwan and China

plain the reduced risk of breast cancer seen in           gov/public/factrbk96/c10.htm). Asian society, in
Chinese women.                                            general, is conservative and Chinese women are
   In the past twenty years, breast cancer inci-          shy about discussing their breasts with their phy-
dence in Chinese women has increased dramati-             sicians; therefore, the earlier ages of breast can-
cally, with a total increase of 50–100%. Epide-           cer cannot simply be explained by earlier detec-
miological findings to explore risk factors sug-          tion due to public health policies for early
gest that breast cancer in Chinese women is re-           screening or younger women requesting asymp-
productive hormone dependent and is similar               tomatic screening. Instead, the evidences of ear-
with respect to hormonal-reproductive risk fac-           lier tumor onset may be contributed by two non-
tors to that in high-incidence areas [1,3]. There-        mutually exclusive possibilities. The first possi-
fore, given the similarity of patterns and the            bility suggests a cohort effect, which indicates
magnitude of association between major risk               that the contribution due to recent adaptation to
factors and breast cancer found in Chinese                Western life-style leading to higher estrogen ex-
women, the recent trend of earlier menarche and           posure may be relatively more pronounced
an increasing proportion of women with post-              among younger women. This possibility gains
menopausal obesity due to modern affluence will           support from a more dramatic increase of breast
provide a partial explanation for recent steep in-        cancer incidence in younger women, being
crease in breast cancer incidence. Furthermore,           87.1% and 85.4% in the age groups 35–44 and
given the important role of breast feeding to pre-        45–54, respectively (as compared to an increase
vent breast cancer, a dramatically decreasing             of 50% in all women) [3]. The second possibility
trend (from 90% breast feeding in the 60’s to             suggests that genetic predisposition may be more
30% in the 80’s in Taiwan) may be specifically            important in Taiwanese and Chinese breast can-
correlated to the increasing trend of breast can-         cers than in others. Unique p53 mutation pat-
cer. Interestingly, though the incidence is low,          tern/site [7] and novel regions of genomic dele-
breast cancer has remained one of the most                tion [6] have been found in breast cancers in
common cancers in women in Taiwan and China               these population, suggesting Chinese breast can-
and is among the leading causes of cancer mor-            cer may genetically differ from Western breast
tality [1,2]. Cervical cancer is the leading cancer       cancer. On the other hand, a few studies have
in women in these populations, but, consistently,         attempted to seek for germ-line mutation in high-
the incidence has begun to decrease recently in           penetrant genes, including BRCA1 and BRCA2,
Taiwan and in China. In the future, it is expected        in Chinese women or breast cancers [8,9], but no
that breast cancer will replace cervical cancer as        conclusive findings are available to examine the
the most common female cancer. These figures              contribution of these genes to early tumor onset.
strongly indicate that breast cancer is an issue of
particular public health and clinical importance.
   It is intriguing that Taiwanese and Chinese            BREAST CANCER SCREENING
breast cancer is characterized by younger age at          PROGRAM IN CHINESE POPULATIONS
tumor onset. More than 50% of total breast can-
cer diagnosed annually in Taiwan is composed of              In Taiwan, in order to combat the increasing
patients younger than 50 years of age, and this           threat of breast cancer, the Department of Health
proportion is higher than those observed in West-         has recently launched a 3-year breast cancer
ern populations [6]. Moreover, the incidence              screening campaign. During this period, a total of
ratio of younger (less than 50 years) versus older        1,000,000 women aged 35 years or older will
(50 years and older) breast cancer in Taiwan is           receive a physical examination by public health
0.25, more than two-fold that (0.09) in the United        nurses; in the event of suspicious findings, the
States (calculated based on the publication of the        examinee will be referred to a hospital for further
National Cancer Institute, USA, shown in the              examinations, including breast ultrasound and/or
following Internet address:http://www.nci.nih.            mammography. This is not the first action taken
                       C.-S. Huang et al. / Breast Cancer Screening in Taiwan and China                   43


by the Department of Health in Taiwan to combat           method for the early detection of breast cancer.
breast cancer. Between 1992 and 1997, a pro-              Therefore, mammography and breast ultrasound
gram was carried out to screen mothers, daugh-            were added to the screening modalities in Taiwan
ters, sisters, and grandmothers of breast cancer          when the high-risk group was screened for breast
patients identified at hospitals [10]. The partici-       cancer. Doubts about self-examination were
pants underwent annual screening using a combi-           supported by the results of a randomized trial of
nation of physical examination, mammography,              breast self-examination in Shanghai [12], in
and breast ultrasound. Female relatives of breast         which about 225,000 Chinese women were ran-
cancer patients were selected for screening be-           domized to either a self-examination instruction
cause of concern about cost-effectiveness. Al-            group or a control group. After 5 years of fol-
though mammographic mass screening for breast             low-up, the number of breast cancers detected in
cancer has proven to be effective in lowering             the two groups was equal, and the breast cancers
mortality in countries with a high incidence of           detected in the self-examination group were not
breast cancer [10], the application of mass               diagnosed at an earlier stage or at a smaller size
screening to a low incidence area such as Taiwan          than those in the control group. Cumulative
may not be worthwhile in terms of cost-                   breast cancer mortality rates during the 5 years
effectiveness. Screening high-risk women, there-          from entry into the trial also were almost identi-
fore, was considered a better approach. The re-           cal in the two groups. An interesting, yet not
sults showed that the mean sojourn time (duration         surprising, finding in this trial was that more be-
of the pre-clinical screen-detectable phase) in this      nign breast lesions were detected in the self-
high-risk group was shorter than that in females          examination group than in the control
from the general population. Annual screening             group. Benign breast tumors are better defined
of this high-risk group was estimated to result in        and easier to detect than malignant lesions, which
a significant 33% reduction in breast cancer              further explains why self-examination or exami-
mortality compared with a nonsignificant 20%              nation by physicians fails to detect many cancers
reduction using 2-yearly and 3-yearly screening           at an early stage. Although the follow-up period
regimes, respectively [10]. The cost-per-year of          was still short and the benefits of self-
lives saved by mass screening is estimated to be          examination have probably not yet emerged, the
15 times higher that involved in screening the            results justify consideration of other screening
high-risk group. Although screening of the high-          modalities.
risk group is cost effective, we must keep in mind           Two population-based breast cancer screenings
that it probably only covers 5% of the incidence          using mammography, with or without clinical
of breast cancer.                                         examination, were conducted in Singapore and
   As Taiwan is an area of low breast cancer in-          Hong Kong, with most of the participants being
cidence, the Department of Health’s policy for            Chinese women [13,14]. As in Taiwan, Singa-
breast cancer prevention has been breast self-            pore is experiencing an increasing incidence of
examination, which does not involve a large fi-           breast cancer. A randomized trial of screening
nancial outlay. The theory was that women                 using mammography without clinical examina-
might be able to detect subtle changes in their           tion in women aged 50–64 years was started in
own breasts that might be missed on clinical              1994 [13]. For every 1,000 women screened, 4.8
breast examination by doctors. Since Taiwanese            cancers were detected. The percentage of stage 0
women have relatively small breasts, it was as-           and stage 1 cancers was 64% in screened women,
sumed that self-examination would lead to earlier         compared to 26% in non-screened women.
detection of breast cancer. However, many                 When only invasive cancers were considered,
breast cancers were diagnosed in the late stage.          65% of cancers detected in screened women were
Although many factors contributed to this late            node-negative, compared with 47% in non-
discovery of cancer [11], many clinicians                 screened women. As this trial only screened
doubted that self-examination was an effective            women aged 50–64 years, it cannot give any in-
44                     C.-S. Huang et al. / Breast Cancer Screening in Taiwan and China

formation on whether, or how, younger women               women in this age group [21–23]. Most people
should be screened.                                       who are against annual screening for women in
    Clinical breast examination and mammogra-             their 40s believe that both the incidence and de-
phy were used in another mass screening pro-              tection rate of breast cancer in younger women is
gram in Hong Kong between 1993 and 1995 [14].             lower [24].
A total of 13,033 women aged 40–70 years were                Although the reasons for the discrepancy in
screened, and 8,504 women underwent mammog-               screening efficacy between different age groups
raphy. In all, 42 cancers were detected, 16 of            are not well understood, different tumor biology
which were nonpalpable. Four palpable cancers             and mammographic test characteristics in
were not detected by mammography. The cancer              younger women must be considered [25]. The
detection rate was 4.61/1,000 in the 40–49 year           doubling time for breast cancer in women under
age group and 6.46/1,000 in the over 50 year age          the age of 50 is 80 days, while that in women
group. When these two trials were compared,               aged 50 to 70 is 157 days [26]. The Swedish
mammography screening plus clinical examina-              two-county trial found that the tumor types
tion achieved a better detection rate than mam-           tended to be more aggressive in younger women
mography alone in women over the age of 50.               [27]. These screening results suggest that these
This finding is consistent with the concept that a        women are less likely to benefit. The lower
screening program using both mammography and              benefit from screening women aged 50 years or
clinical examination can achieve a higher sensi-          less, compared to those over 50 years, is due to a
tivity than either modality alone [15]. The lower         shorter sojourn time in the younger age group
detection rate in younger women raises the ques-          [28]. It has also been suggested that screening
tion whether the incidence in this age group is           every 2 or 3 years might be sufficient in women
lower (not the case in Taiwan, and probably not           aged 50 years or older, while annual screenings
in Hong Kong) or the sensitivity of mammogra-             might be required in women aged 40 to 49 years
phy in younger women is lower. Mammography                [27]. As a high incidence of interval cancers rep-
alone failed to detect 15% of breast cancers iden-        resents either rapid progression of breast tumors
tified by clinical examination, and the sensitivity       or poor sensitivity of the screening method, the
was lower in younger women [15]. Thus, com-               shorter sojourn time indicates a rapid progression
bined clinical examination and mammography is             of breast tumors in younger patients, which ne-
desirable.                                                cessitates a shorter screening interval or a more
                                                          sensitive screening modality. The ability of
                                                          mammography to detect breast cancer is affected
CONTROVERSY OF MAMMOGRAPHY                                by breast density [29,30], its sensitivity being
SCREENING IN YOUNG WOMEN                                  80% in women with fatty breasts and only 30%
                                                          in women with extremely dense breasts [29].
   Although it is well documented that mass               After adjustment for age, menopausal status, use
screening using mammography lowers the mor-               of hormone replacement therapy, and body mass
tality of breast cancer among women over the age          index, the odds ratio for interval cancer in women
of 50, women aged 40 to 49 do not appear to               with extremely dense breasts compared with
benefit to the same extent. The reduction in              those with fatty breasts is about 6. In regard to
breast cancer mortality varied from 18% to 35%            age and breast density, more premenopausal than
for women who began screening between the                 postmenopausal women have dense breasts [29].
ages of 35 and 49 years [16–19]. Therefore,               The chance of having biopsy after mammography
mammographic screening is recommended every               examination is also different between young [40–
1–2 years for all women in their 40s [20], while          49] and old (50 and older) age groups. One study
the American College of Radiology, the Ameri-             noted that the probability of abnormal mammo-
can Cancer Society, and the American Medical              grams at first screening is the same in different
Association advise annual screening for all               age groups, but the positive predictive value of
                       C.-S. Huang et al. / Breast Cancer Screening in Taiwan and China                    45


screening mammography declines from about                 are more likely to be found with sonogra-
18% in women older than 60 to 4% in women                 phy. One study demonstrated that 0.3% of
aged 40 to 49 [31], resulting in more unnecessary         12,706 examinations performed by ultrasound, or
intervention procedures in women younger than             2.8% of 1,575 lesions detected, were cancers that
50 years.                                                 were detected by ultrasound but not by mammog-
                                                          raphy or physical examination [32]. The EGBCS
                                                          concludes that the high rates of false-positive
CURRENT BREAST CANCER SCREENING                           outcomes would lead to unnecessary further in-
POLICY IN TAIWAN: MAMMOGRAPHY                             vestigation. However, in this particular study,
AND ULTRASOUND                                            ultrasound was used to examine contralateral or
                                                          ipsilateral breasts of cancer patients for multifoci
   As mentioned above, in contrast to Western             lesions, in addition to primary cancer. The prob-
countries, breast cancer in Taiwan is character-          ability of finding another lesion is expected to be
ized by an earlier onset, with peak incidence at          low, and the intention of the examiner to biopsy
age 40–49, and more than 50% of breast cancers            the detected lesion in these high-risk patients will
arising in premenopausal women. Therefore, the            be high. Thus, the cancer detection rate was low
dilemma of breast cancer screening in Taiwan              and the false-negative rate high in this study. In
can be summarized by Taiwan having a rapidly              another prospective study, when breast ultra-
increasing incidence of breast cancer, especially         sound was used to screen 3,626 women with
in premenopausal women, while the incidence is            dense breasts and normal mammographic and
still low compared to Western countries. Since            physical examination findings, 11 (0.3%) were
premenopausal women have denser breasts than              found to have cancers [30]. These cancers, iden-
postmenopausal women, and Taiwanese women                 tified by ultrasound alone, did not differ in terms
have smaller breasts and a higher percentage of           of tumor size and stage from nonpalpable cancers
dense breasts, increasing the frequency of mam-           detected by mammography and were smaller and
mography screening may not be the sole solution           at a lower stage than palpable breast cancers. In
to increasing the detection rate in this age group.       women with dense breasts, overall cancer detec-
The addition of other screening modalities, such          tion increased by 17%, and the number of tumors
as breast ultrasound, may be helpful, as breast           detected only by imaging increased by 37%.
ultrasound can detect some breast cancers in              These results support the idea that ultrasound is
dense breasts that are missed by mammography              very helpful in detecting nonpalpable cancers
[30,32].                                                  missed by mammography of dense breasts, more
   A consensus statement by the European Group            frequent in premenopausal women.
for Breast Cancer Screening (EGBCS) is, how-                  One retrospective study in Japan reported the
ever, against the use of ultrasound in population         use of breast ultrasound in a non-randomized
screening at any age due to the high rates of both        mass screening [36]. In one group of 15,935
false-positive and false-negative results associ-         women, only physical examination was per-
ated with mass screening using breast ultrasound          formed, and 5 breast cancers were detected. In
[33]. Many of the false-negative results are due          another group of 18,539 women, ultrasound plus
to difficulty in microcalcification detection using       physical examination was performed, and 22
breast ultrasound, although we found that it is not       cancers were detected. Sixteen of these 22
impossible to detect microcalcification, not nec-         women had early breast cancer and 13 (59.1%) of
essarily associated with mass, in nonpalpable             the 22 cancers were not palpable. Of the 22
breast lesions using this method [34]. Others             women, 50% were younger than 50 years. Al-
have reported that they could use ultrasound to           though the overall cancer detection rate was low,
localize microcalcifications detected by mam-             which might be due to the low incidence of breast
mography [35]. Since mammography is not usu-              cancer in Japan or the low sensitivity of the
ally requested in younger women, calcifications           screening modalities, breast ultrasound is useful
46                      C.-S. Huang et al. / Breast Cancer Screening in Taiwan and China

in mass screening for the detection of early breast        the sensitivity. The mean time for performing a
cancers, many of which will be in women under              bilateral ultrasound screening is about 4 minutes
the age of 50 and will be missed by physical ex-           (range 1.5–9.75 minutes), which is not too time-
amination. One criterion for evaluating screening          consuming for mass screening. Two additional
efficacy is that more than 50% of screen-detected          advantages of breast ultrasound are that no radia-
cancers should be smaller than 15 mm [37], and             tion is involved and no pain is felt during exami-
breast ultrasound should be able to do this.               nation. Although the radiation risk from mam-
   If the main limitation of ultrasound in mass            mography screening is probably not too high to
screening is the difficulty in detecting DCIS asso-        prohibit women under the age of 50 from benefit-
ciated with microcalcifications, the significance of       ing from screening, ultrasound involves no radia-
DCIS needs to be clearly understood. Although              tion, allowing more frequent screening in a short
many pathological and molecular biological stud-           interval. In addition, in contrast to mammogra-
ies suggest that many cases of DCIS will progress          phy, since ultrasound examination does not in-
to invasive carcinoma if undetected or untreated           volve pain, compliance will be better, especially in
[38,39], it is estimated that only 30-50% of DCIS          Chinese women with smaller and denser breasts.
will progress to invasive cancer, with the remain-            In Taiwan, a randomized mass screening has
der regressing or remaining indolent [40,41]. In           been proposed recently to investigate the role of
addition, it is not documented whether all invasive        breast ultrasound in breast cancer screening. The
carcinomas arise from in situ cancers. In the first        results should be able to define whether breast ul-
mammography screening conducted on 1,000                   trasound is useful in reducing breast cancer mor-
women aged 40 to 49 and first screened by mam-             tality in women aged 40–49.
mography, 1.5 cases were DCIS and 1.5 cases in-
vasive cancer, compared with 2 DCIS and 7 inva-
sive cancer for every 1,000 women aged 50 to 69            SUMMARY
[31]. In the Sickles series, in which most of the
patients were Caucasians, microcalcifications sug-            As the incidence and mortality of breast cancer
gesting malignancy constituted 42% of nonpalpa-            has increased in Chinese women, there is a need to
ble breast cancers [42]. In our series, nearly all the     initiate a more effective breast cancer screening
nonpalpable cancers detected by mammography in             program. Unlike Western countries, a higher pro-
Taiwanese women were due to the presence of                portion of premenopausal breast cancer is found in
microcalcifications. Ultrasound is probably more           our population, and Chinese women have denser
sensitive than mammography in detecting nonpal-            breasts. To solve this particular problem, we be-
pable cancers; however, it fails to detect microcal-       lieve that increasing only the frequency of mam-
cifications. Mammography is the best tool to de-           mography screening may not be the ideal solu-
tect DCIS associated with microcalcifications,             tion. However, it is possible that the addition of
which probably will not progress rapidly to inva-          breast ultrasound will be helpful. A randomized
sive cancer; therefore, it can be performed over a         screening trial has been proposed recently in Tai-
longer interval, with ultrasound being added to            wan to address the role of breast ultrasound in
detect nonpalpable cancers not associated with             breast cancer screening. The results should be
microcalcifications.                                       able to determine whether it will be useful in re-
   Although the sensitivity and specificity of             ducing breast cancer mortality in women aged 40–
breast ultrasound is highly operator- and machine-         49.
dependent, and screening the whole breast is time
consuming, the examiner will gain experience in
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