Spectrum of Breast Cancer in Asian WomenGaurav Agarwal, MS, DNB, PDC (Endocr Surg),1 P. V. Pradeep, MS, DNB, MRCS Ed,1

Vivek Aggarwal, MS,1 Cheng-Har Yip, MD FRCS (Glasg), FRCS Ed,2

Polly S. Y. Cheung, FRCS, FRACS, FACS3

1Department of Endocrine and Breast Surgery, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Raebareli Road,

Lucknow, 226014 Uttar Pradesh, India2Department of Surgery, University Malaya Medical Centre, Kuala Lumpur, Malaysia3Breast Care Center, Hong Kong Sanatorium and Hospital, Hong Kong, People�s Republic of China

Abstract

Introduction: Breast cancer is the leading cause of cancer-related deaths in Asia, and in recent

years is emerging as the commonest female malignancy in the developing Asian countries,

overtaking cancer of the uterine cervix. There have been no studies objectively comparing data

and facts relating to breast cancer in the developed, newly developed, and developing Asian

countries thus far.

Material and Methods: This multi-national collaborative study retrospectively compared the

demographic, clinical, pathological and outcomes data in breast cancer patients managed at

participating breast cancer centers in India, Malaysia and Hong Kong. Data, including those on the

availability of breast screening, treatment facilities and outcomes from other major cancer centers

and cancer registries of these countries and from other Asian countries were also reviewed.

Results: Despite an increasing trend, the incidence of breast cancer is lower, yet the cause-

specific mortality is significantly higher in developing Asian countries compared with developed

countries in Asia and the rest of the world. Patients are about one decade younger in developing

countries than their counterparts in developed nations. The proportions of young patients

(< 35 years) vary from about 10% in developed to up to 25% in developing Asian countries, which

carry a poorer prognosis. In the developing countries, the majority of breast cancer patients

continue to be diagnosed at a relatively late stage, and locally advanced cancers constitute over

50% of all patients managed. The stage-wise distribution of the disease is comparatively favorable

in developed Asian countries. Pathology of breast cancers in young Asian women and the clinical

picture are different from those of average patients managed elsewhere in the world. Owing to

lack of awareness, lack of funding, lack of infrastructure, and low priority in public health schemes,

breast cancer screening and early detection have not caught up in these under-privileged

societies.

Conclusions: The inadequacies of health care infrastructures and standards, sociocultural barri-

ers, economic realities, illiteracy, and the differences in the clinical and pathological attributes of

this disease in Asian women compared with the rest of the world together result in a different

spectrum of the disease. Better socioeconomic conditions, health awareness, and availability of

breast cancer screening in developed Asian countries seem to be the major causes of a favorable

clinical picture and outcomes in these countries.

Correspondence to: Gaurav Agarwal, MS, DNB, PDC (Endocr Surg),e-mail: gaurav@sgpgi.ac.in

� 2007 by the Societe Internationale de Chirurgie World J Surg (2007) 31: 1031–1040

Published Online: 26 March 2007 DOI: 10.1007/s00268-005-0585-9

B reast cancer is the commonest cancer among wo-

men worldwide, with the lowest incidence being

reported from far eastern and south eastern Asian

countries.1,2 In recent years, breast cancer has emerged

as the commonest female malignancy in the majority of

Asian countries,3 but remains the second commonest

female malignancy in some regions of developing Asian

countries, next to the cancer of uterine cervix.4 Although

the incidence of breast cancer is lower in Asian countries,

the cause-specific mortality in most Asian countries is

much higher as compared to western countries.2 Higher

proportions of breast cancer patients in developing Asian

countries are younger than patients in developed Asian

and western countries.5,6 Given the huge population in

the developing Asian nations, and the fact that up to 25%

of all breast cancer patients here are young, there are a

large number of young breast cancer patients in Asia.

Young age by itself is a known indicator of poor prognosis

in breast cancer patients.

In most Asian societies, the majority of breast cancers

continue to be diagnosed at a relatively late stage. In

India, which represents a typical developing Asian

country with its multi-ethnic, multi-religious population

sharing similar peculiar economic, sociocultural chal-

lenges, health care facilities, and standards with the

majority of other developing Asian countries, locally ad-

vanced cancers constitute about 50% of the total.4 The

picture is, however, not so bleak in developed Asian

countries and regions such as Singapore, Hong Kong,

and Malaysia. Various factors such as lack of awareness,

unavailability of breast cancer screening and sociocul-

tural barriers of hesitation on the part of women to have

her breasts examined and seek treatment seem to result

in late stage at diagnosis in most Asian women. Besides

the poorer outcomes owing to late stage at diagnosis, and

relatively poorer breast cancer treatment opportunities

available to these patients, there seem to be other dif-

ferences in the clinical picture and pathology of breast

cancers in women in developing Asian countries, which

account for overall poorer outcomes. A lack of credible

and scientifically sound epidemiology data on breast

cancer from developing Asian countries makes it difficult

to understand the reasons for the different breast cancer

incidence, mortality, and outcomes in these countries

compared with developed countries in Asia and rest of

the world.

Asia, the largest and most populous continent in the

world, is a heterogeneous mix of nations that vary widely

in the cultural, social and economic structures, and in

geopolitical situations. All of these factors may have

some bearing on occurrence, progression, detection, and

management of breast cancer, and of most other malig-

nancies. The World Bank classifies India as a low in-

come, Malaysia as an upper-middle income, and Hong

Kong as a high income country7. These 3 countries are

very different in their socioeconomic as well as their

ethnic and cultural realities, and thus represent the

sociocultural and economic diversity of Asia. This survey

aimed at studying the overall picture of breast cancer

management in 3 Asian regions (Lucknow in India, Kuala

Lumpur in Malaysia, and Hong Kong, People�s Republic

of China) with an emphasis on the picture in young

women (< 35 years)

The objectives of this study were first, to study any

differences in incidence and mortality rates of breast

cancer, the spectrum of disease including age distribu-

tion, stages (TNM), tumor characteristics; and second, to

evaluate whether or not the comparative results from

participating centers and the available literature on these

issues point to any correlation of the differences with re-

gard to the social, cultural, and economic background,

and the availability of breast screening in various Asian

countries and regions.

MATERIALS AND METHODS

This collaborative and comparative multi-center retro-

spective study was carried out at 3 major Asian breast

cancer centers from India, Malaysia, and Hong Kong.

Demographic, clinical, pathological, and outcomes data

on breast cancer patients managed at the 3 participating

centers, namely, SGPGIMS, Lucknow, India; University

Malaya Medical Center, Kuala Lumpur, Malaysia; and

Hong Kong Sanatorium and Hospital, Hong Kong, were

collected and analyzed. Similar data, and data on the

availability of breast screening, treatment facilities, and

outcomes from other major cancer centers and cancer

registries of India, Hong Kong and Malaysia, as well as

from other Asian countries, were also reviewed. The

publications of the National Cancer Registry Program of

India, Indian Council of Medical Research—namely, the

2-year report on hospital-based cancer registries 1999–

2000, and the 2-year report of the population-based

cancer registries 1999–2000, assessing the burden and

care of cancer patients in India—were perused for this

purpose,8,9 with additional information on district-wise

distribution of breast cancers derived from the All India

Report 2001–2002 of the Development of an Atlas of

Cancer in India project of the National Cancer Registry

Program, ICMR and their website (http://www.cancerat-

lasindia.org/chapter6).3 The data for Malaysia and Hong

1032 Agarwal et al.: Breast Cancer in Asian Women

Kong were derived from the respective websites of

the National Cancer Registry of Malaysia (http://www.

crc.gov.my/ncr),10 and the Hong Kong Cancer Registry

(http://www.3.ha.org.hk/cancereg/stat.asp).11

A literature search was undertaken to unravel available

information on breast cancer demographics, detection,

treatment, and outcomes from various Asian countries in

the published scientific literature. Similar information was

also searched for on the internet, as well as other publi-

cations of cancer registries and organizations such as

the WHO, regional and national health agencies, institu-

tions and non-governmental organizations (NGOs), etc.

Appropriate similar publications and reports from other

geographic regions outside Asia, including those from the

International Agency for Research on Cancer (IARC),12

and its GLOBOCAN database,6 were used for the pur-

pose of comparing the incidence, clinical picture, pathol-

ogy, and outcomes of breast cancer between the Asian

and non-Asian regions and countries studied.

RESULTS

The databases of participating centers provided valid

and complete information on 544 patients managed dur-

ing 1998–2004 at SGPGIMS, Lucknow, India; 2,009 pa-

tients managed at the UMMC Kuala Lumpur, Malaysia

during 1995–2004, and 901 patients managed at HKSH,

Hong Kong during 2003–2005. Published data from TMH,

Mumbai—another dedicated breast center in India—are

incorporated into the study for comparison of results.

Incidence, Demography and Mortality of BreastCancer in Asia

Breast cancer incidence in various Asian countries and

a comparison with other WHO regions, including USA

and France, are provided in Table 1. The numbers of new

breast cancers diagnosed in all 4 WHO regions is much

smaller than the numbers diagnosed in USA and France.2

Data from all urban and rural population-based cancer

registries (PBCR) in India suggest a rising incidence of

this disease in India. Yet, the age-adjusted rates reported

from various urban registries range from 24.8 to 33.4 per

100,000 of the population,3 which amount to about one-

third of the incidence reported from western countries

such as the USA (San Francisco, CA: non-Hispanic white

109.6 per 100,000) and Uruguay (Montevideo 114.9 per

100,000).12 The minimum age-adjusted rate reported

from the only rural population-based cancer registry in

India is even less at a mere 7.2 per 100,000,3 and is

somewhat similar to the incidence reported from other

developing countries such as the Gambia and Jiashan,

China.12 Breast cancer accounts for about one-quarter of

all cancers in Indian women, about half of all cancer-

related deaths. With the exception of Chennai, all urban

PBCRs in India report breast cancer to be the commonest

female malignancy over the years 2000–2001.3 This is a

different pattern from the earlier reports where cancer of

the uterine cervix was the commonest type of cancer,

even in urban centers. In the Chennai urban PBCR and

the Barshi rural PBCR, breast cancer remains the second

commonest female malignancy reported, with cancer of

the uterine cervix still remaining the number one cancer

problem.3,8,9

As per the National Cancer Registry of Malaysia, the

age-adjusted rate (incidence) of breast cancer in the year

2003 was 42.9 per 100,000 of the population.10 One in 20

Malaysian women is estimated to be affected by breast

cancer in her life time. However, the incidence of breast

cancer is reported to vary considerably among the 3

ethnic groups that constitute Malaysian society. The age-

adjusted rates in ethnic Chinese (59.7 per 100,000) and

Indians (55.8 per 100,000) are considerably higher than

Table 1.Number of new breast cancer patients diagnosed and deaths in various WHO regions2

WHO regions Number of new cases (thousands) Number of cancer deaths (thousands)

India, Nepal, Pakistan (SEARO D) 109 67Indonesia, Thailand, Singapore (SEARO B) 53.9 29China, Korea, Mongolia (WPRO B1) 102.1 57.5Cambodia, Myanmar (WPRO B2) 10.2 6.3Iran, Kuwait, Saudi Arabia, UAE (EMRO B) 10.2 5.1Egypt, Iraq, Yemen (EMRO D) 13.6 7USA (AMRO A) 226.5 53.3France, Germany (EURO A) 221.8 91.8

SEARO: South East Asian Regional Office; WPRO: Western Pacific Regional Office; EMRO: Eastern Mediterranean RegionalOffice; AMRO: Americas Regional Office; EURO: European Regional Office.

Agarwal et al.: Breast Cancer in Asian Women 1033

that in ethnic Malays (33.9 per 100,000).10 In Hong Kong,

2,059 new cases of breast cancer were registered in

2002. The crude rate was 59.0 and the age-adjusted rate

42.0 per 100,000 of the population. The relative fre-

quency of breast cancer amongst all malignancies in fe-

males was 20.8%, and its incidence doubled in the 1990s,

overtaking lung cancer as the number one cancer

affecting Hong Kong women. One in 23 women is ex-

pected to be affected in her life time. The mortality to

incidence ratio is 0.21.11

The breast cancer incidences in young women vary

widely amongst various Asian countries, with countries

like Pakistan having a high incidence and Japan a very

low incidence (Table 2).5,6 In the current study, 26% of

patients managed at SGPGIMS, Lucknow were younger

than 35 years of age, with the peak incidence in the age

group of 35–40 years. Data from TMH, Mumbai in India,

shows this proportion to be 11%.3 Of the 2,009 patients

managed between 1995 and 2004 at the UMMC, Kuala

Lumpur, Malaysia, 7.6% were younger than 35 years

age. The National Cancer Registry of Malaysia reports

13.4% of patients being younger than 40 years of age,

and a peak incidence in the age group of 50–59 years.10

Data from the Hong Kong Cancer Registry reports 11.6%

of patients to be younger than 40 years of age, and the

peak incidence of breast cancer in the age group of 50–

54 years.11 Data on the proportions of young patients in

various other countries and societies show that 7.4% of

American patients,13 29.3% of Taiwanese patients,

12.6% of patients in Singapore, and 8% of Australian

patients are under 40 years of age.14 These data indicate

that a higher proportion of breast cancer patients in

developing Asian countries are young, compared with

developed Asian countries and western countries.

Although the incidence rates in Asian countries are less

than in western developed countries, the mortality rates

are disproportionately higher (Table 1).2 Breast cancer

thus remains the single largest cause of cancer deaths in

Asians, similar to the rest of the world. Globally, it ac-

counts for about 15% of all cancer deaths in women,

killing some 471.2 women per 100,000 of the population

annually.2

Breast Cancer Screening and Detectionin Asian Countries

An organized large-scale breast cancer screening

program is almost non-existent in India. The few breast

cancer screening programs available are largely targeted

at small communities, covering a minuscule proportion of

the Indian population, and rely on funds derived from

research grants or the screened individuals� own re-

sources. There is no government-funded or -aided mass

breast screening program available, and the experts also

advocate screening based on periodic breast examina-

tion by a physician and breast self examination.15 The

approach to breast cancer screening in Malaysia is more

or less identical to that in India, and population-based

breast cancer screening is not recommended due to

limited resources, and a lack of local statistics on mam-

mography and breast cancers.16

In Hong Kong, the first breast screening program was

set up in 1990 at Kwong Wah Hospital, with private

funding from a voluntary organization, the Tung Wah

Group. From its first pilot study of 3,829 asymptomatic

women, 2 cancers were detected per 1,000 women.

Since then, more well-women clinics have been set up

by voluntary organizations such as Tung Wah Eastern

Table 2.Number of new breast cancer patients diagnosed per 100,000 of the young populations in Asian countries5,6

10–14 years 15–19 years 20–24 years 25–29 years 30–34 years

Pakistan (1995–1997) – 1.2 6.3 14.0 48.4Israel (Jews) 0.1 0.2 2.1 9.7 33.3Singapore – – – 6.3 29.9Egypt – 0 1.4 8.5 29.9Bahrain – 0 0 0 27.7China (Beijing; 1993–1997) – 0.7 3 11 26.9Kuwait – 0 0 2.9 22.7Philippines (Manila) 0.1 0.5 1.9 8.2 22.1Jordan – 0 0.8 6.5 21.7Mali 0.5 1.9 2.9 8.5 21.7Oman – 1.9 2.9 8.5 21.7Korea (Seoul) – 0.3 1.5 6.1 17.3Japan (Nagasaki) – 0.4 1.8 3.1 16Thailand – 0.4 1.2 4.8 15.2Vietnam – 0.9 7.6 11.5 13.8

1034 Agarwal et al.: Breast Cancer in Asian Women

Hospital, the Family Planning Association and private

hospitals. The Hong Kong Government also set up 3

women�s health centers providing mammogram facilities

and breast screening advice with a fee charged for the

service. To date, the longest serving breast screening

program has served 46,637 women, with a cancer

detection rate of 5 per 1,000 women. However, the Hong

Kong government in its ‘‘Report on Cancer Prevention

and Screening’’ in December 2004, does not recommend

‘‘screening mammogram and breast self examination,’’

based on available local data, despite the admission that

Hong Kong has the highest incidence of breast cancer

among Asian countries (http://www.info.gov.hk/dh/dis-

eases/index.htm).

Clinical Picture of Breast Cancer in AsianWomen

Table 3 summarizes the stage-wise distribution of

breast cancer patients managed at the participating In-

dian, Malaysian, and Hong Kong centers of this study.

These data, together with those from other Asian coun-

tries, suggest that nearly all the patients are clinically

detected, and that almost none are screen-detected in

developing Asian countries. Local invasion occurs in up to

two-thirds and metastases in 6% to 25% of Indian and

Saudi patients.5,18 Significant proportions of patients

present with T2/T3 tumors, and even more strikingly, up

to one-third of all patients present with skin and/or chest

wall involvement (T4a–c). Inflammatory breast cancers

are seen more often in younger patients, putting them at

considerable risk.

Half of the young patients managed at SGPGIMS,

Lucknow, India, had Stage III disease. Similarly, in earlier

reports, 50%–60% of Malaysian women had stage III or

IV disease,19 compared with only 14% of young American

women presenting at Stage III.20 The stage-wise distri-

bution of patients is worse in the case of younger pa-

tients, as revealed in Table 4, which provides a stage-

wise comparison of young breast cancer patients man-

aged at some centers in India, USA, and Singa-

pore.18,20,21 The proportion of Stage III patients in

Singapore is reported to be 22%,21 which is closer to the

American rather than the Asian figures. At the University

of Malaya Medical Centre, Kuala Lumpur, Malaysia, of

the 2,009 breast cancer patients managed, 152 were

under the age of 35 years. In this group of young women,

69% were at Stages 1 and 2, while 31% were at Stages 3

and 4, which is marginally higher than the 27% of patients

Table 4.Stage-wise comparison of young breast cancer patients managed at centers in Asia and the USA

SGPGIMS, Lucknow,India (%)

RCC, Trivandrum,India17 (%)

Changi,Singapore20 (%)

New York,USA19 (%)

Tx 3 6 – –T1 9 12 30 54T2 24 47 59 36T3 32 27 11 10T4 32 9 – –LN + 67 60 53 51

SGPGIMS: Sanjay Gandhi Postgraduate Institute of Medical Sciences; RCC: Regional Cancer Center; Tx to T4: tumor stages(TNM-AJCC classification); LN+: metastatic lymph nodes.

Table 3.Stage-wise distribution of patients at 3 Asian centers

Stage(TNM-AJCC classification)

SGPGIMS, Lucknow,India

(n = 544, 1998–2004; %)

UMMC, KualaLumpur, Malaysia (n = 2,009,

1995–2004; %)

HKSH, Hong Kong(n = 901,

2003–2005; %)

0 1 3 13I 4 23 34II 34 47 43III 51 16 9IV 9 11 1

SGPGIMS: Sanjay Gandhi Postgraduate Institute of Medical Sciences; UMMC: University Malaya Medical Center; HKSH: HongKong Sanatorium and Hospital.

Agarwal et al.: Breast Cancer in Asian Women 1035

of all age groups with Stages 3 and 4 disease. Similarly,

of the young patients managed at the Breast Cancer

Center of HKSH, Hong Kong, the majority were managed

at Stages 0 to 2, with Stages 3–4 disease comprising less

than 10% of all patients. Both the Malaysian and Hong

Kong centers recorded a trend toward larger tumor size,

more lymph nodal metastases, and poorer histological

grade and hormone receptor status.

Pathology

Data on the pathology of breast cancer in Asian women

revealed a pattern of a higher proportion of patients with

high tumor grade (grade 3 of the Bloom and Richardson

grading system), and hormone receptor-negative tumors.

About 60% of SGPGIMS breast cancer patients had

grade 3 tumors, 66% had axillary lymph nodal metasta-

ses, and 58% are estrogen (ER) and progesterone (PR)

receptor-negative. Data from Mumbai, India, showed a

slightly better ER- and PR-negative rates of 47%.4 Data

from the University of Malaya Medical Center Registry

showed that in all patients, 11.4% patients had Grade 1,

52.5% had Grade 2 while 36.1% had Grade 3 cancers.

56.4% were ER-positive. In Hong Kong, of all the invasive

cancers, 83.6% were ductal and 3.8% lobular. Grade 3

tumors were present in 48.3%. Lymph vascular invasion

was present in 30.7%. Estrogen receptor was positive in

76.6%. The data on HER-2neu immunoreactivity in Asian

patients are scarce, but the available information hints at

low rates of positive HER-2neu status. Seventeen of 100

recent breast cancer patients managed at SGPGIMS

Lucknow were found to over-express HER-2neu (immu-

nohistochemical evaluation). HER-2 over expression was

present in 22.6% of patients managed at the Breast Care

Center, HKSH, Hong Kong. In the young Malaysian pa-

tients (less than 35 years old) from the UMMC data, the

median tumor size was 4.0 cm with a mean of 5.1 cm.

About 52% were ER-positive. Only 5.6% had Grade 1

(Bloom and Richardson) tumors, while 55.1% of patients

had Grade 2 and 39.3% Grade 3 tumors. On the whole,

women < 35 years age presented with larger tumors and

at a later stage. They were also more likely to be ER-

negative and with a higher grade of cancer compared

with the overall average.

DISCUSSION

Comparisons among various regions of the world show

a 3-tier distribution of the magnitude of the breast cancer

problem. The number of new cases and age-standard-

ized incidence rates of breast cancer are low in Asia,

intermediate in South America and eastern Europe, and

high in North America and western Europe.2 China,

Korea, Thailand and Japan—all Asian countries—are

amongst the countries with the lowest incidence of breast

carcinoma. Besides the geographic differences, breast

cancer incidence seems directly proportionate to the level

of industrial development of a country, although there are

numerous exceptions to this rule. The age-adjusted rate

is 37.4 per 100,000 for the global female population, but

the rate in developed countries (67.8 per 100,000) is

nearly 3 times that in the developing countries (23.8 per

100,000).6 Japan with its high level of industrial devel-

opment yet moderate breast cancer incidence and Uru-

guay with only a moderate level of development yet high

breast cancer incidence provide contradictions to this

rule.

There seem to be many plausible reasons for differ-

ences in breast cancer incidence. The low average life

expectancy of women in developing Asian countries has

a bearing on the incidence of breast cancer, which has a

known correlation with increasing age. However, even the

age-adjusted incidence rates of this disease are lower in

Asia. Probable explanations for this are: shorter life span

of estrogen exposure in Asian women, late menarche

related to under-nutrition, and early menopause. In the

majority of Asian societies, bearing many children, having

the first child at an early age, and feeding children for long

periods are the norm. All of these are factors known to

protect against breast cancer.22 In a study on breast

cancer risk factors among Asian–American ethnic

groups, 68.5% of Chinese, 75.5% of Japanese, and

72.1% of Asian women as a whole were below the age of

30 at the time of their first delivery.23 Asian diets in gen-

eral have less fat and higher fiber content, and many of its

ingredients contain soy proteins, which have been sug-

gested, albeit with questionable validity, to have some

protective effect against breast cancer.24,25 Furthermore,

the usage of oral contraceptive pills and hormone

replacement therapies, known risk-enhancing factors, is

rather low in Asians. The putative protection afforded by

these factors in Asians is strengthened by increased

incidence rates of breast cancer in urban Asian societies

that are fast adopting the western life-style and food

habits, and that second generation immigrant Asians in

the USA are found to have a similar breast cancer risk to

other American women.26

Lack of breast cancer awareness, inaccessible health

care and screening, unaffordable treatment, competing

health care needs such as communicable diseases,

1036 Agarwal et al.: Breast Cancer in Asian Women

some of which get higher priority than neoplastic dis-

eases, sociocultural barriers (Purdah, unwillingness to

expose oneself due to sociocultural compulsions) and

reliance on low-cost traditional/alternative medicines are

a few of the risk factors unique to Asian and Indian wo-

men that culminate in poorer outcomes for breast cancer

in these societies. Women in developing Asian countries

are ill-aware of breast cancer. As a result, many of them

ignore an evident breast problem or lump, resulting in a

delay in diagnosis, which is reflected in the outcome. It is

not uncommon for women to be aware of a breast lump

for many years before seeking medical attention. Many

such patients seem to have an attitude of denial of this

fact, postponing seeking medical attention until an overt

secondary change of the disease such as skin edema or

ulceration (Fig. 1), or symptomatic metastatic disease. At

SGPGIMS, Lucknow, India, about 55% of patients pre-

senting with locally advanced breast cancer were well

aware of the presence of a possibly life-threatening

cancerous breast lump, yet sought treatment only when

the disease had progressed to that stage.

Most Asian countries, barring a few relatively developed

ones, do not have an organized breast cancer screening

program serving the entire or a substantial part of the

population, owing to the high costs involved and the low

yield of such programs. The social and cultural beliefs also

make women hesitate to subject themselves to screening

breast examinations and imaging. Breast self-examination

is an alternative in countries with limited resources, though

with its known limitations.27 Teaching breast self-exami-

nation does help in improving awareness about breast

health issues as a whole, and about breast cancer in

particular. Many studies have shown that periodic physical

examination by a physician as a screening modality is at

least as effective in reducing breast cancer mortality.

The clinical picture of breast cancer is more favorable in

Malaysia and Hong Kong. Population-based mammo-

graphic screening is not recommended in Malaysia due to

limited resources and lack of infrastructure, expertise,

and local standards for mammography.16 Because of

this, ductal carcinoma in situ is rare, comprising only 2.7%

of the total number of cancers seen. Screening by clinical

breast examination is opportunistic, i.e., when a woman

sees a doctor, a clinical breast examination is encour-

aged. Women are also taught breast self-examination by

nurses when they attend the community maternal and

child health clinics. The emphasis currently is on creating

‘‘breast-awareness’’ among the public, utilizing the media

as the main source of information. With this approach, it

is hoped that women will present earlier to their doctor

with breast lumps.

Among 901 consecutive cancer patients at the HKSH

breast care centre, Hong Kong from September 2003 to

November 2005, the mode of presentation of breast

cancer was mostly by incidental discovery by the patient

(81.4%), the remaining were discovered by regular breast

screening, which included monthly breast self-examina-

tion, annual clinical examination by a doctor, screening

mammogram, and additional screening ultrasound when

the breast density was high. The introduction of breast

cancer screening programs in Hong Kong has resulted in

a major change in the disease pattern of breast cancer. In

the pre-screening era in the 1980s in Hong Kong, stage 0

cancer was limited to the diagnosis of Paget�s disease

only in < 2% of cases, around 40% to 50% were at stages

3 and 4 at first diagnosis, which was quite different from

the data just quoted from a local breast centre in the

years 2003–2005.28 Yet, owing to the lack of appropriate

resources, and unsure of the overall cost-effectiveness of

the mammographic screening, the Hong Kong govern-

ment still does not recommend this as a routine screening

procedure for the masses.17

The impact of breast cancer awareness and cost-effec-

tive screening on the outcome of this disease is well

understood by health policy planners in the majority of

Asian countries. In countries like India, such efforts are

coming mostly from non-governmental and volun-

tary organizations. The community initiatives of the

SGPGI Breast Health Program (http://www.sgpgibreast-

health.org) in creating awareness, teaching breast self-

examination to women, providing periodic screening

physical examination, and investigative work-up including

Figure 1. Clinical picture of breast cancer inAsian women: the good, a T2N0 tumor managedwith breast conservation surgery and sentinellymph node biopsy; the bad, an inflammatorybreast carcinoma (T4dN1M0); the ugly, fungatingbreast cancer with chest wall fixity (T4cN2M0).

Agarwal et al.: Breast Cancer in Asian Women 1037

breast screening only for the high-risk individuals over the

past decade or so in and around Lucknow, India, have re-

sulted in somewhat better acceptance of breast cancer

screening by educated urban women in the region. A minor

shift to earlier stages at diagnosis has also resulted

simultaneously, as has better acceptance of contemporary

breast cancer treatment strategies such as breast con-

servation, sentinel lymph node studies, breast recon-

struction, and comprehensive multi-modal treatment

protocols, which are all provided by SGPGIMS, Lucknow,

at a subsidized cost and on a ‘‘no professional fee’’ basis.

Similar benefits, albeit reaching a minuscule proportion of

the huge Indian population, have resulted from the efforts

and initiatives of other institutions, agencies, and non-

governmental organizations such as the Cancer Patients

Aid Society, Mumbai (http://www.cpaaindia.org).

It is, however, disturbing to see many women ignoring

their disease until they have large fungating tumors with

sepsis (Fig. 1). High proportions of women have axillary

node-positive disease. Striking features reflecting tumors

that have been ignored for a long time are large tumor

size, skin ulceration or fungation in up to 10%, and

more than 3 metastatic lymph nodes in the majority

(4, SGPGIMS Lucknow data).

Even basic clinical data on breast cancer from Asian

countries are scarce, which is a reflection of either a total

lack of or ineffective cancer registries in this region. If

available, the quality of data is often questioned, with the

majority of data coming from hospital-based registries in

large cities, rather than from community studies and reg-

istries. The multi-modal comprehensive breast cancer

treatment is out of reach of the average woman in a

developing Asian country. The cost of chemotherapy or

surgery at government-run hospitals is at times more than

the average monthly income of Asian households. Treat-

ment at more convenient private and corporate hospitals,

which are many times more costly, though do not always

offer better quality treatment and services, is reserved for

the few in the upper echelon of society who can afford it.4

The high quality contemporary surgical and adjuvant

treatments are available and affordable for only a minority

of the population. Besides, most Asian societies are male-

dominated, where women occupy a relatively inferior so-

cial position. The health care and nutritional needs of

women are thus often ignored, and the scarce finances

reserved for the men-folk of the family.

Governments of developing Asian countries spend a

minuscule proportion of their GDP on health care, and

only a fraction of this small budget is allocated to neo-

plastic diseases. There are important medical problems

that need more urgent attention and financial support, like

epidemics of communicable diseases, malnutrition, infant

mortality, vaccination programs, and natural calamities.

The infrastructure for managing neoplastic diseases is

even less developed. For example, in India, there are

fewer than 100 surgical oncology centers to cater for the

population of more than one billion. The numbers of

radiotherapy units are far less than the WHO recom-

mendations of a minimum of 0.4 units per million of the

population. There is little emphasis on neoplastic dis-

eases in the undergraduate medical education curricu-

lum, and no country-specific guidelines or protocols that

take into account the local health care infrastructure and

health economics are available. As a result, even those

patients who do seek medical attention for a breast lump

often do not get sufficient and timely advice and appro-

priate multi-modal treatment, other than that at special-

ized centers of excellence.

Only a minority of patients benefit from less invasive

surgical techniques and other contemporary management

strategies. Even at the few centers offering breast

conservational surgery, breast conservation rates are low

due to the late presentation and low acceptance of breast

conservation surgery.29 Reports from other developing

Asian countries indicate similarly poor breast conservation

rates and the unavailability of comprehensive treatment

opportunities to breast cancer patients. In comparison,

comprehensive multi-modal therapy is available to the

majority of patients in Hong Kong. Of the Malaysian

patients managed at the University Malaya Medical Cen-

ter, some 27% underwent breast conservational surgery.

An even smaller proportion of patients can be offered

the benefits of sentinel lymph node studies as the

majority present with clinically palpable axillary lymph

nodes. In India, only 3 centers offer sentinel lymph node

studies, using a combination of radio-pharmaceutical and

blue dye, on a consistent basis. In a validation study, 70

consecutive sentinel lymph node procedures at SGPG-

IMS, Lucknow, using in-house prepared low-cost Tc-

antimony colloid and blue dye, have resulted in achieving

a negative predictive value of sentinel lymph node pro-

cedures in ruling out axillary metastases of 95.65%; the

positive predictive value was 100% and overall accuracy

97%, while the cost incurred was only 2% of that of the

commercially available dyes.30 Such innovations may

perhaps be useful for other developing countries where

costs are a major deterrent.

In conclusion, the overall picture of breast cancer is

strikingly variable among Asian countries, and among

regions and ethnic groups within individual countries.

Although the incidence is comparatively lower in east and

southeastern Asia, breast cancer has emerged as the

1038 Agarwal et al.: Breast Cancer in Asian Women

largest cancer problem in Asian women, and the largest

cause of cancer-related deaths. It remains the second

commonest malignancy in women in the rural areas of

developing Asian countries. A high proportion of Asian

breast cancer patients are young. Poor awareness, a lack

of breast cancer screening programs, limited health care

facilities, sociocultural barriers, and faith in low-cost tra-

ditional alternative medicine systems are responsible for

the delayed presentation and advanced stage at diag-

nosis in the majority of patients in developing Asian

countries. The availability of screening programs has

instigated a change toward earlier staging of breast

cancer in most urban Asian societies, but the benefits do

not yet seem to have reached the rural areas and under-

developed regions.

Owing to the limitations of the quality of data and

information available on these issues, the authors do not

make any claims that this study is an epidemiologically

and scientifically perfect account of breast cancer in

various regions and countries in Asia. However, the

information provided should be seen as an attempt to

bridge the divide.

ACKNOWLEDGEMENTS

Gaurav Agarwal wishes to thank Dr A. Nandakumar,

DyDG-ICMR and Officer In-Charge NCRP, for providing

the detailed reports of the National Cancer Registry

Program; the Faculty and Residents of the Departments

of Endocrine and Breast Surgery, and Radiotherapy for

the upkeep of data; and the organizers of the Breast

Surgery International Symposium on ‘‘Breast Cancer in

Developing Countries’’ at the International Surgical

Week, 2006, Durban, South Africa.

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