ORIGINAL ARTICLE

Attitudes and compliance of clinical management after genetictesting for hereditary breast and ovarian cancer among high-riskSouthern Chinese females with breast cancer history

Ava Kwong • Annie Tsz-Wai Chu • Christine Teen-Sum Wu •

Desiree Man-Sik Tse

� Springer Science+Business Media Dordrecht 2014

Abstract Western studies have shown that the uptake

rates of surveillance and prophylaxis may vary among

BRCA mutation carriers between ethnicities. The present

study is the first to investigate the behavioural impact and

subjective attitudes in Southern Chinese high-risk families

who had undergone BRCA1 and BRCA2 genetic testing up

to 2.5 years post-testing. Individuals who had such genetic

testing and have consented to participate in the prospective

database of Hong Kong Hereditary Breast Cancer Family

Registry were recruited and surveyed by a face-to-face or

telephone interview. Sociodemographic information,

genetic test results, pre- and post-testing surveillance,

medical regimes, and attitudes towards the choice of clin-

ical management were obtained by interviews and retrieval

of medical records using this prospective database. 69

females with breast cancer history were recruited into the

study. Twenty-nine female carriers (15 BRCA1 mutated

gene-carriers and 14 BRCA2 mutated gene-carriers) and 40

non-carriers of a BRCA 1/2 mutations were interviewed.

The uptake rate of high risk breast screening i.e. clinical

breast examination, mammography, and breast MRI is

significantly higher among female carriers (48.3 %) after

knowing genetic testing results than before (p \ 0.01). A

strong significant relationship between any increase or

decrease of ovarian ultrasound screening (OS) and genetic

status is found (p \ .001), with more females did OS and

with a higher frequency after knowing genetic testing

results among both carriers (22.7 % ? 86.4 %) and non-

carriers (37.5 % ? 50.0 %). Among carriers, very few

opted for prophylactic surgeries. The present cohort might

see prophylaxis as last resort and would use traditional

Chinese medicine in cancer risk management.

Keywords Southern Chinese � Hereditary breast and

ovarian cancer � Prophylaxis � Retrospective �Risk-reducing surgery

Introduction

Breast cancer (BC) is the most common cancer in women.

It is estimated that between 5 and 10 % of breast and

ovarian cancer patients are genetically-related, of which

majority is due to BRCA1/2 mutations [1]. Females who

carry a mutation of BRCA1 or BRCA2 gene have an ele-

vated lifetime risk of BC as high as 75 %. Their lifetime

risk of ovarian cancer (OC) can be increased to 50 % for

BRCA1 mutation carriers and 20 % for BRCA2 mutation

carriers. Moreover, the diagnosis is usually made at a much

younger age, often before menopause [2–5]. Among

affected patients who already had unilateral BC, risk of

contralateral BC is also high compared with women who

do not carry the mutated gene [6].

The identification of BRCA1 and BRCA 2 gene mutations

in 1994–1995 has enabled genetic testing of hereditary breast

and ovarian cancer (HBOC), and facilitated more precise risk

estimations in individuals from HBOC families. Genetic

counselling and testing of BRCA1 and BRCA2 mutation that

guides the choice of surveillance and prophylactic proce-

dures has become common and is considered standard of care

in most developed countries [7–10]. Although there are

increasing studies based on behavioural impact of genetic

A. Kwong (&) � A. T.-W. Chu � C. T.-S. Wu � D. M.-S. Tse

Division of Breast Surgery, Li Ka Shing Faculty of Medicine,

The University of Hong Kong, Hong Kong, China

e-mail: akwong@asiabreastregistry.com

A. Kwong � A. T.-W. Chu

The Hong Kong Hereditary Breast Cancer Family Registry,

Hong Kong, China

123

Familial Cancer

DOI 10.1007/s10689-014-9706-7

testing, most are performed in the West and to date there

are limited research performed in Asia. Based on studies on

management of BC it is likely that Asians take different

attitudes towards cancer diagnosis [11, 12]. The present

study focused on the behavioural impact of such genetic

testing among Chinese females.

Individuals who carry the BRCA mutation will usually

be offered earlier and more intensive surveillance or/and

preventive measures. Clinical examination, mammogram/

ultrasound [13], and MRI screening are usually elected as a

modality to achieve early diagnosis of BC [14–16]; pelvic

examination, transvaginal ultrasound, and periodic

screening of tumor marker CA 125 [17, 18] for early

diagnosis of OC. Some individuals may be suitable to be

prescribed with chemoprevention drugs such as tamoxifen

or raloxifene for BC and oral contraceptive pills for OC

[19–24]. Others may opt for more radical and invasive

surgical prevention such as prophylactic mastectomy [25,

26] and salpingo-oophorectomy to remove the main

BRCA-targeted organs (breasts and ovaries) before the

diseases clinically develop [27–29]. In order to reduce the

risk of developing a second BC, women with previous

personal history of BC may consider prophylactic contra-

lateral mastectomy (PCM). PCM has been shown to lower

the incidence of unilateral BC [30–35] by up to 95 % in BC

patients with family history of BC [30]. This risk reduction,

adjusted for adjuvant chemotherapy and hormonal therapy

(i.e. treatment with Tamoxifen), in premenopausal and

post-menopausal women were 94.4 and 96 % respectively

[33]. Several studies have also shown that PCM was

associated with lower BC mortality [32]. Both prophylactic

mastectomy and salpingo-oophorectomy are irreversible

options. Despite the feasibility of breast reconstructions

after prophylactic mastectomy that could result in reduc-

tion of disfigurement, prophylaxis may still bear long-term

clinical, psychological, body-image, marital and procre-

ation implications.

Recent studies on Caucasians [36, 37] have shown that

risk assessment may change individuals’ perceptions and

estimation of their personal risk for breast and other can-

cers. It can also result in change of preference on preven-

tative and treatment options, and lead to the increase or

decrease of adherence to medical procedures and surveil-

lance management.

While research on the rippled behavioural effects fol-

lowing genetic testing has been receiving more attention in

the past decade [38–41], so are the uncertainties concerning

the depiction of changes of clinical management of indi-

viduals who have undergone genetic counselling and test-

ing for BRCA1/2 mutation. Going through genetic

counselling and hence understanding of personal and

family members’ risk may affect individuals’ health-con-

sciousness, anxiety related to subjective perception of

cancer risks, and either increase or decrease their engage-

ment in self-reassuring health behaviors. Genetic testing

may involve long-term behavioral implications that may

either encourage or hinder such health behaviours [40, 41].

Although genetic counselling and testing service for

HBOC risk is clinically available in limited number of

countries in Asia, the research output usually focussed on

the genetic sciences and the advancement of testing tech-

nology. The behavioural impact of BRCA1/2 mutation

testing, and more importantly its implications on an indi-

vidual’s awareness and election of preventive strategies

and related clinical management is still a novel research

area. China, in particular, lacks empirical data and infor-

mation in this area despite its clinical and theoretical

significance.

Past studies showed that Asians might share a different

clinical picture comparing with Caucasians in terms of BC

in general and HBOC [42–44]. In particular, various

studies have shown that individuals’ attitudes and accept-

ability toward preventive strategies for HBOC tend to vary

among different ethnic groups and results suggested that

the population’s perception of advantages and drawbacks

must be taken into careful consideration when establishing

medical recommendations or planning public health inter-

ventions [45].

Other than the conventional management options men-

tioned, the application of complementary and alternative

medicine/therapy (CAM) is increasingly popular among

cancer patients internationally. Traditional Chinese Medi-

cine (TCM) methods are gaining its popularity and fre-

quently applied as an adjunctive therapy for cancer

patients. The usage of TCM methods (for example Chinese

medicinal herbs, acupuncture and moxibustion, Chinese

remedial massage, cupping, Qigong) among Asian and

Chinese cancer patients are found to be particularly high

[46, 47], whereas nutritional supplements are used more

frequently by Caucasian patients [48, 49]. TCM methods

are usually used as a way of managing side effects of

conventional cancer treatment and boosting the immune

system.

As cancer genetic counseling and testing programs have

gradually become more widely available and affordable in

Asia, it is essential to examine their immediate and long-

term behavioural impact on high-risk individuals and

families before the design and implementation of clinical

and psychological service can be made possible.

The present study is one of the first in Hong Kong and

among Asia to study patients’ attitudes and compliance of

clinical and management service of a well-established local

high-risk BC clinic with a retrospective methodology,

complemented by a prospective database. The findings

from this study will provide information to help screen

particular patients/participants who may need further

A. Kwong et al.

123

counselling and reassurance in order to come up with

appropriate surgical options and decisions, and identify

potential risk factors. Results being generated from the

present study will formulate the foundations for future

prospective psychosocial research, prevention and inter-

vention strategies in hereditary oncology among Chinese

and Asians in the long run—which is still in its budding

stage.

Materials and methods

Female index patients, with BC and/or OC and their family

members, who were referred from 12 government and pri-

vate-based hospitals and private practitioners, to The Cancer

Genetic Service by the Hong Kong Hereditary and High Risk

BC Programme between June 2007 to January 2010 for

genetic counseling and testing (both positive and negative)

from the Registry’s (www.asiabreastregistry.com) database

were randomly contacted. As reported in a previous study by

our research team [50], all study participants underwent

standard and thorough pre-and post- genetic counselling by a

trained genetic counsellor and a breast surgeon with training

in cancer genetics and clinical psychology at our high-risk

clinic. Mutation detection was performed using full gene

sequencing and multiplex ligation-dependent probe ampli-

fications (MLPA). A standard epidemiological question-

naire, including family history, gyneacological history, and

cancer history was administered. Clinical and medical

information of all individuals, including choice of manage-

ment, were prospectively collected and recorded in the

database collection under The Hong Kong Hereditary BC

Family Registry (The Registry).

Participants

Participants were identified from the clinical patient data-

base of The Registry. Eligible participants included cancer

affected females over age 18 years, who received pre-

testing genetic counselling, molecular testing for BRCA1/2

and post-test counselling between 2007 and 2009.

A retrospective approach was adopted in this study. It

employed a follow-up survey to verify participants’

adherence to the surveillance and management guidelines

offered since the receipt of his/her BRCA 1/2 genetic

testing results in a retrospective format. Participants were

contacted and invited to take part in the study via telephone

interviews or face-to-face interviews during their periodic

medical assessment at the High Risk Breast Clinic of Tung

Wah Hospital. A questionnaire and medical information

from participants’ medical record were traced with consent

in order to compare that with participants’ recollection.

The design of the study and the questionnaire were

submitted and approved by board of ethics and determined

to induce no physical and psychological harm to

participants.

Measures

A self-designed questionnaire was used to obtain demo-

graphic information on marital status, education, occupa-

tion and employment status. An extensive review of

participants’ medical history, cancer history, genetic status,

surveillance and prevention strategies, usage of CAM, and

reasons for doing/not doing so before and up to 2.5 years

after undergoing genetic counseling or/and testing were

included. One trained research assistant assisted partici-

pants to complete the questionnaire either via telephone or

during their medical follow up at the study site.

Results

A total of 69 women with BC history who underwent genetic

counselling and testing at the Registry completed the ques-

tionnaire via telephone interviews or face-to-face interview

during their periodic follow-up at the clinic. The mean age of

the final sample was 46 years (range 27–70 years). The

demographic composition and clinical characteristics of the

study population are summarized in Table 1. Table 2 dif-

ferentiates the demographical and clinical differences

between mutation carriers and non-carriers.

Source of referrals and means to access to the genetic

services

Majority of the present cohort is index patients of a family,

while 13 % is family members of affected index patients. All

participants had cancer before and they are usually referred by

their clinicians and a minority is self-referred via our Pro-

gramme’s public awareness campaign. The majority (85.5 %)

of the current cohort decided to undergo genetic counseling

after initial telephone contacts with our trained nurses to

obtain some background information. 10.1 % of the partici-

pants said that they decided to contact the clinic and attend the

genetic counseling session and eventually underwent the

testing due to the suggestions of their family members (they

are the family members of the affected index patients, who did

or did not have a cancer diagnosis themselves). Only 4.3 %

said that it was entirely their personal decision.

Impact of genetic counselling and testing on screening

behaviours

Participants were being asked a range of questions based

on their personal recall (with the confirmation from a

Attitudes and compliance of clinical management

123

prospective medical database) of their cancer prevention

and surveillance habit before and after going through

genetic counseling and knowing their genetic testing

results (GT). Their uptake of breast screening, ovarian

screening, prophylactic surgeries/procedures, and adop-

tion of alternative medicines were documented and

compared. Any positive or negative changes in fre-

quencies of surveillance were analyzed. Increase in fre-

quency of surveillance (irrespective of intensity of

increase) was coded and analyzed as a positive change in

frequency of uptake rate. Same logic applied to decrease

of frequency. Further analyses were applied for in-depth

investigation.

Breast screening habit

Patients were being asked about the frequency of breast

screening before and after they got their genetic test results.

In the present study and following discussion, breast

screening (BS) is defined as clinical breast examination

(CBE) provided by clinicians, along with mammography.

Pearson Chi Square results showed that there is no sig-

nificant relationship (p [ .05) between change of fre-

quency of BS and genetic status, although both carriers and

non-carriers had a greater uptake rate of BS after knowing

genetic results and Fig. 1 suggests that an effect may be

present.

An important finding is that Pearson Chi Square statistic

revealed a significant relationship between high risk breast

screening habit (HRBS) i.e. (any increase of decrease of

CBE, mammography and Breast MRI) and genetic status,

X2 (2, N = 69) = 9.8, p \ .01. Among carriers, more

females (13.8 % ? 48.3 %) chose HRBS post-GT, also

with a higher frequency (see Fig. 2). The findings among

non-carriers was exactly the opposite, less females

(10 % ? 7.5 %) chose HRBS post-GT, and for those who

continued to do HRBS, they did it less frequently.

Table 1 Demographic composition and clinical characteristics of

study population

All participants (n = 69)

n %

BRCA status

BRCA1 15 21.7

BRCA2 14 20.3

Negative 40 58.0

Age (year)

Mean ± SD 46 ± 10

Median (range) 46 (27–70)

Educational level

Primary 11 15.9

Secondary 42 60.9

Tertiary or above 16 23.2

Marital status

Single 22 31.9

Married 42 60.9

Divorced 5 7.2

Age first diagnosed with breast cancer (year)

Mean ± SD 41 ± 11

Median (range) 40 (18–68)

Table 2 Demographical differences and clinical differences between

mutation carriers and non-carriers

Mutation carrier

(n = 29)

Non-carrier

(n = 40)

n % n %

BRCA status

BRCA1 15 51.7 Non carrier (n = 40)

BRCA2 14 48.3

Age (year)

Mean ± SD 46 ± 12 45 ± 10

Median (range) 46 (27–70) 46(28–65)

Educational level

Primary 5 17.2 6 15.0

Secondary 17 58.6 26 62.5

Tertiary or above 7 24.1 9 22.5

Marital status

Single 8 27.6 14 35.0

Married 21 72.4 21 52.5

Divorced 0 0.0 5 12.5

Age first diagnosed with breast cancer (year)

Mean ± SD 41 ± 11 41 ± 10

Median (range) 38 (24–68) 41.0 (18–62)

0.0%

10.0%

20.0%

30.0%

40.0%

50.0%

60.0%

70.0%

80.0%

90.0%

100.0%

Before GT After GT

Non-carrier

Carrier

Fig. 1 Effect of GT on CBE and MMG uptake (carriers and

noncarriers)

A. Kwong et al.

123

Ovarian screening habit

Patients were being asked about the frequency of ovarian

ultrasound screening (OS) before and after they went through

genetic counseling and testing. In the present study and

following discussion, OS was being defined as transvaginal

or abdominal ultrasound. After excluding those who under-

went bilateral salpingo-oophorectomy, the Pearson Chi

Square statistic revealed a strong significant relationship

between any increase or decrease of OS and genetic status, X2

(1, N = 57) = 15.9, p \ .001, with more people did OS and

with a higher frequency (Fig. 3) after knowing GT results

among both carriers (22.7 % ? 86.4 %) and non-carriers

(37.5 % ? 50.0 %).

Prophylactic surgeries

One important finding of the present study is that PCM or

prophylactic bilateral salpingo-oophorectomy (PBSO) was

unpopular among the present cohort. After excluding those

who already underwent bilateral mastectomy or bilateral

salpingo-oophorectomy before undergoing genetic coun-

seling and testing, only 14.3 % of carriers opted for PCM

while 2.8 % non carriers chose such method. 18.2 % eli-

gible carriers opted for PBSO while no non-carriers chose

that. And among those who underwent prophylaxis, only

one single participant opted for PCM as well as PBSO.

Chinese and alternative medicine

Other than adhering to standard screening and prophylaxis,

a considerable proportion of this sample is found to be

using alternative medicine (for example TCM, Chinese

herbal supplements) as complementary options for cancer

prevention and health enhancement. A substantial number

of those being tested positive included TCM as their rou-

tine treatment post-GT (66.7 %). Interestingly, 56.2 % of

those being tested negative also used TCM as health

enhancement post-GT.

Correlations between demographic factors and findings

Basic demographic factors such as age, marital status, and

educational levels have been analyzed with the uptake of

surveillance, prophylactic surgeries, CAM respectively. No

significant correlations and differences could be identified

in this cohort.

Discussion

The main findings of the present study showed that carriers

tended to adhere to high-risk breast and ovarian screening

as the major preventive measures for heightened risks of

BC and OC. Very few opted for prophylactic surgeries

such as PCM and PBSO. In terms of elimination of cancer

risks radically, the success of the personalized risk-man-

agement program does depend on the uptake of these

surgeries. In the present cohort, such surgeries appeared to

be unpopular.

First of all, despite being the most effective procedures,

PCM and PBSO are radical procedures which entail

physical and psychological impact. And whether a patient

opts for such radical procedure depends on her subjective

cancer risk assessment and tolerance of such cancer risks.

Another reason is that Chinese may opt for other non-

invasive methods to manage cancer risks e.g. TCM or

change of diet. While western medicine is still considered

to be the first-line option, a considerable amount of carriers

(and also non-carriers) would implement TCM simulta-

neously as a complementary method either for cancer

prevention or enhancing their general health. Even in

modern cities like Hong Kong, many individuals still value

traditional Chinese medical philosophy and treatment like

herbology, Yin/Yang concept and qigong. They may view

prophylaxis as last resort, and that also explains low uptake

rate of prophylactic surgeries among carriers.

As population- or community-based ovarian screening is

currently not offered by government in Hong Kong, it is

worth noting of the relatively high uptake of ovarian

screening even among non-carriers. In general, locals in

0.0%

5.0%

10.0%

15.0%

20.0%

25.0%

30.0%

35.0%

40.0%

45.0%

Less frequent More frequent

Non-carrierCarrier

Fig. 2 Effect of GT on HRBS uptakes (carriers and noncarriers)

0.0%

10.0%

20.0%

30.0%

40.0%

50.0%

60.0%

70.0%

80.0%

More frequent

Non-carrier

Carrier

Fig. 3 Effect of GT on OS uptake (carriers and noncarriers)

Attitudes and compliance of clinical management

123

Hong Kong need to either arrange their own checkup

through public sectors (usually with a considerably long

waiting time) or private sectors which can cost from US

$100–$250.

One postulation is that prior personal and family’s

cancer experience may have an effect on the enhancement

of awareness and level of health-consciousness among the

present cohort, including the non -carriers. And, the

information the research team provided in the genetic

counselling session did highlight the importance of general

ovarian checkup for any females (irrespective of cancer

history).

Despite the current findings, we should not omit the fact

that public awareness of Hereditary Breast and Ovarian

Cancer Syndromes may have increased in Hong Kong

especially after annual educational campaigns by the

Registry and also by world-wide promotion and impact

such as The Angelina Jolie’s effects. In the past 2 years,

the research team’s clinics have observed an increasing

trend of HRBS and PBSO among carriers as cancer risk

management. It is very important to perform prospective

and longitudinal research in order to examine the attitudes,

risk perceptions and decisional considerations among the

high risk group as their lives and the community’s under-

standing of the syndromes will evolve and improve.

Limitations and future direction

The present study’s major limitation is inherent to its ret-

rospective design. Bias and distorted memories on the part

of the participants are not uncommon in retrospective

studies. We have taken note of this possible limitation and

therefore other than solely relied on participants’ report on

their surveillance reports, formal medical record on a

prospective database have also been obtained with consent

to ensure accuracy of information.

Due to its retrospective nature, the results of the present

study cannot and should not be used to deduce causal

relationships whenever available. However, the results can

serve as useful groundwork in designing further studies in

the area. Our team is currently working on a large-scale

prospective study to investigate on the understanding of

psychological impact and attitude-change towards clinical

management of different sub-groups of this population.

Acknowledgments The authors thank Dr. Ellen Li charitable

Foundation and Kerry Group Kuok Foundation Limited for their

continual support of the work of the Hong Kong Hereditary and High

Risk Breast and Ovarian Cancer Programme and Hong Kong

Hereditary Breast Cancer Family Registry; the team at the Depart-

ment of Molecular Pathology, Hong Kong Sanatorium and Hospital

for contributing to the laboratory work.

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