Breast cancer screening practices among Vietnamese women and factors associated with clinical breast examination uptake.

BACKGROUND: This study examined current breast cancer (BC) screening practices among Vietnamese women and the factors associated with the uptake of clinical breast examination (CBE).
METHODS: A total of 508 women aged 30-74 years in Hanoi completed a knowledge-attitude-practice (KAP) survey in 2019 including validated measures of breast cancer awareness (Breast-CAM) and health beliefs (Champion's Health Belief Model Scale). Descriptive statistics, χ2, and ANOVA tests were used to analyse KAP responses across groups with different sociodemographic characteristics. A logistic regression model assessed the associations of knowledge, beliefs, and sociodemographic characteristics with CBE uptake.
RESULTS: Only 18% of respondents were aware of BC signs, risk factors, and screening modalities although 63% had previously received BC screening. CBE was the most common screening modality with an uptake of 51%. A significantly higher proportion of urban residents compared with rural residents (32% vs 18%, Chi-square test, p = 0.04) received mammography. Unlike mammography, CBE uptake was not associated with sociodemographic characteristics (i.e., residence area/education level/occupation/household monthly income/possession of health insurance). CBE uptake was associated with BC knowledge (OR = 2.44, 95%CI: 1.37-4.32), perceived susceptibility to BC (OR = 1.15, 95%CI: 1.05-1.25), and perceived barriers to accessing CBE (OR = 0.88, 95%CI: 0.84-0.92).
CONCLUSION: The study points to the need for public health education and promotion interventions to address low levels of awareness about BC and to increase uptake of BC screening in Vietnam in advance of screening programme planning and implementation. It also suggests that screening programmes using CBE are promising given current engagement and the absence of socio-demographic disparities.

Introduction

Breast cancer (BC) is the most common cancer among Vietnamese women with 15,299 new cases in 2018 which accounted for 20.6% of all cancer cases in women [1]. This proportion is more than double that of the second most common cancer, colorectal (7,126 new cases, 9.6%) [1]. The estimated number of deaths due to BC was also the highest, at 6,103 deaths, which accounted for 13.9% of all cancer deaths [1]. Importantly, 64.7% of new BC cases were in women below the age 50 and 64.2% cases were diagnosed at late stage (stage III or IV) [2, 3]. Breast cancer in young women (aged < 40 years) tends to be more aggressive and diagnosed at later stages resulting in poorer survival rates compared to BC among older women [4, 5]. Although early detection through screening is critical in this context, Vietnam currently does not have a national BC screening programme.

Before implementing a screening programme, consideration needs to be given to the screening modality used, the feasibility of service delivery, the cost-effectiveness of the programme, and its acceptability to the targeted population. Mammography is very costly and prohibitively expensive in low-resource settings such as low-and middle-income countries (LMICs) [6, 7]. In contrast, clinical breast examination (CBE)–an alternative low-cost screening tool with downstaging effect–represents a realistic intervention in LMICs [8] and it has been shown to be cost-effective in Vietnam [9]. How acceptable such a programme would be is unclear though. This aspect is important to successful programme implementation. For example, a randomised controlled trial of CBE in the Philippines was terminated after the first screening round due to a low acceptance rate [10].

The Knowledge-Attitude-Practice (KAP) survey is a widely used method to improve understanding about health programme priorities and identify barriers to programme implementation [11, 12]. According to the World Health Organization (WHO), a KAP survey can identify knowledge gaps, beliefs, and behaviour patterns as well as the factors influencing these issues [11]. In KAP theory, the acquisition of knowledge, the generation of attitudes, and the formation of behaviours are three successive processes [13]. The KAP approach may draw upon relevant theories such as the health belief model (HBM) which points to the important influence of beliefs and perceptions in health harming and health promoting behaviours [14]. Therefore, the KAP approach and HMB were utilised in this study to assess the current screening practices of Vietnamese women and the factors associated with their uptake of CBE.

Methods

Study design, setting, and participants

We conducted a cross-sectional KAP household face-to-face interview survey at the community level in August 2019, in Hanoi which is the capital and the second most populous city in Vietnam.

The sample comprised (i) women aged 30–74 years who (ii) never had BC (self-reported), and (iii) consented to participate in the survey. Although BC screening programmes in Europe, the Americas, and Australia target women aged 40–74 years [15-18], this study chose the age range 30–74 years to reflect the younger age at which Vietnamese women, on average, are diagnosed with BC. In Vietnam, 64.7% of new BC cases in 2012 were below the age of 50 years old [2] and the age standardized incidence rate (ASR) increased from the age of 30 years old (i.e., 3.2, 20.7, and 54.5/100,000 women among the age group of 20–29, 30–39, and 40–49 years, respectively) [1].

This study received ethical approval (reference no: 319/2019/YTCC-HD3, dated 30 May 2019) from the Hanoi University of Public Health’s Institutional Review Board. All respondents received an information sheet about the study including information about its voluntary nature, objectives, target respondents, privacy, use of collected data, potential drawbacks, and benefits of participation. Interviewers also provided respondents with a verbal explanation about the study’s purpose and the interview procedure. Written informed consent was obtained from all respondents who agreed to participate.

Sample size and sampling methods

Sample size was calculated according to WHO guidance and using a formula that estimated a population proportion with specific absolute precision [19] (S1 Table in S1 File). The estimated proportion of women who had had BC screening in Vietnam was assumed to be 50% to generate the most conservative, or largest, sample size. A sample size of 500 was calculated using a 95% confidence interval, an absolute precision value of 0.1, a design effect of 2 (to account for cluster sampling) and a non-response rate of 10%.

Multistage sampling was used to sample survey respondents. In stage 1, one urban and one rural district in Hanoi were randomly selected; in stage 2, two communes per district were selected using Population Proportionate to Size (PPS) sampling; in stage 3, every nth household (from a chosen starting point) was approached (interval = 2); and in stage 4, one eligible respondent per household was interviewed. Age quota (S2 Table in S1 File) was applied (calculated based on the female age structure of Vietnam from Census 2009 [20]). If the eligible respondent was not at home or was not able to participate at the point of interview, interviewers would re-visit one time.

Survey tool

The Breast Module of the Cancer Awareness Measure (Breast-CAM, which can be accessed and downloaded freely at https://www.cancerresearchuk.org/health-professional/awareness-and-prevention/the-cancer-awareness-measures-cam) developed by Cancer Research UK, King’s College London, and University College London in 2009 [21] was used to assess respondents’ knowledge of BC. The Champion Health Belief Model Scale (CHBMS) was used to assess respondents’ beliefs about BC/BC screening [14].

Breast-CAM was used to assess women’s knowledge of the UK Breast Screening Programme. Currently, there is no BC screening programme in Vietnam. Therefore, Breast-CAM was modified to enquire about a respondent’s knowledge of BC screening modalities. The CHBMS does not have a CBE-specific version (only a breast self-examination-BSE (version 1993) and a mammography (version 1999)) [14, 22]. Unlike BSE, mammography and CBE are screening modalities that need to be provided by clinicians. Thus, we replaced the word ‘mammography’ with ‘clinical breast examination’ in all items except one item of the CHBMS version 1999. This modification changed the focus of the items to CBE and did not alter the meaning or purpose of the items. The item, ‘Having a mammogram exposes me to unnecessary radiation’ was excluded. Cronbach’s α for the CHBMS ranged from 0.75 to 0.88 in the original study [14] and from 0.69 to 0.78 in this study.

The instruments were translated into Vietnamese by the first author who is bilingual. Back translation was carried on by another researcher from Hanoi University of Public Health (HUPH). We compared and discussed the two versions and made some minor amendments. This revised Vietnamese version of the questionnaire was piloted by interviewing 10 volunteer respondents in Hanoi. The results of the pilot interviews were used to finalise the questionnaire used in the main data collection exercise.

Data collection

10 interviewers were recruited from HUPH’s 3rd and 4th year student cohorts who had experience of working as community survey interviewers. Two research assistants at HUPH acted as field supervisors and assisted the interviewers. The team received a 1-day-training course prior to data collection. The training included an introduction to the study objectives, how to select households and respondents, questionnaire briefing, and a practice session.

Data collection was carried out on weekends (17-18/8/2019 for the rural district and 23-26/8/2019 for the urban district). In each district, two supervised teams of five interviewers conducted the interviews simultaneously in two selected communes of the district. Data collection lasted longer in the urban area as the teams could interview women only early in the morning or late afternoon instead of throughout the whole day as was possible in the rural areas (because the proportion of urban dwelling women working as full-time employees was higher).

Variables and measurements

Main outcome: CBE screening practice/uptake

CBE screening uptake was a binary (yes or no) variable. A definition of CBE was provided alongside this question about CBE uptake to ensure that respondents had a common understanding of CBE and did not confuse it with BSE.

Main predictors: Knowledge of BC and attitude/belief

Questions were posed about three categories of knowledge: ‘BC symptoms’, ‘BC risk factors’, and ‘BC screening modalities’. Women who had knowledge in all three components were defined as ‘having knowledge’ or being knowledgeable about BC. Regarding each component, women who identified more than five non-lump symptoms (out of nine) or risk factors (out of 10) were defined as ‘having knowledge’ of BC symptoms and BC risk factors, respectively [21]; women who named at least one correct screening modality without any prompting (e.g., mammography, CBE, breast ultrasound) were defined as ‘having knowledge’ of BC screening modalities.

Attitudes/beliefs were assessed by using the modified CHBMS version 1999; 18 items were grouped into three subscales, perceived susceptibility (3 items), perceived benefits (5 items), and perceived barriers (10 items). Survey participants chose one of five responses to each item: Strongly disagree (1)–Disagree (2)–Not sure (3)–Agree (4)–Strongly agree (5) and the score (from one to five) to each item was summed to calculate a total score for each subscale.

Covariates

The selection of covariates was based on the results of a systematic review that identified factors associated with the uptake of BC screening in China [23]: ‘age’, ‘education level’ (completed at least primary education/completed secondary education/completed high school education/completed university degree), ‘occupation’ (full-time employee/self-employed/housewife/retired), ‘residence area’ (urban/rural), ‘possession of health insurance (HI)’, and ‘household’s monthly income’ (in six categories based on income quintile of general Vietnamese population in 2016 [24]).

Data analysis

Descriptive statistics (mean, standard deviation-SD, min/max values for continuous variables and percentages for discrete variables) were used to describe the sociodemographic characteristics of respondents, their knowledge of BC, their attitudes/beliefs towards BC/BC screening, and their screening practice or use. Knowledge and practice across groups with different sociodemographic characteristics were assessed using the Chi-square test while ANOVA assessed between-group differences regarding attitudes/beliefs. The factors that influenced CBE uptake were investigated using a logistic regression model. The various statistical procedures were conducted in STATA version 15.0.

Results

A total of 508 women completed the interviews (response rate of 95%). Only 21 out of 533 women refused to participate and four did not complete the interview. Respondents’ sociodemographic characteristics by area (urban vs rural) are presented in Table 1. Most respondents were married (92%); from the majority Kinh ethnic group (99%); and had no religion (96%). The average age of respondents was 46; 55% completed at least secondary education; 60% were self-employed; 71% had a household monthly income higher than 9,000,000 Vietnamese Dong (VND) (~$389); and 78% had HI.

Table 1

Sociodemographic characteristics by area (urban vs rural).

	Total	Urban	Rural	p-value
	n (%)	n (%)	n (%)
Total	508 (100.0)	256 (50.4)	252 (49.6)
Age, mean (sd)	46 (11)	47 (11)	46 (11)	NS
Education level
Completed at least primary education	107 (21.1)	22 (8.6)	85 (33.7)	<0.001
Completed secondary education	173 (34.1)	61 (23.9)	112 (44.4)
Completed high school education	110 (21.7)	81 (31.8)	29 (11.5)
Completed university degree	117 (23.1)	91 (35.7)	26 (10.3)
Occupation
Full-time employee	98 (19.3)	65 (25.4)	33 (13.1)	<0.001
Self-employed	303 (59.6)	122 (47.7)	181 (71.8)
Homemaker/housewife	66 (13.0)	33 (12.9)	33 (13.1)
Retired	41 (8.1)	36 (14.1)	5 (2.0)
Marital status
Single/Separated/Divorced/Widow	43 (8.5)	19 (7.4)	24 (9.5)	NS
Married	465 (91.5)	237 (92.6)	228 (90.5)
Household monthly income
< = 3,000,000 VND (~$129a)	34 (6.7)	2 (0.8)	32 (12.7)	<0.001
3,000,001–6,000,000 VND (~$130–259)	72 (14.2)	27 (10.6)	45 (17.9)
6,000,001–9,000,000 VND (~$260–389)	70 (13.8)	34 (13.3)	36 (14.3)
9,000,001–12,000,000 VND (~$390–519)	140 (27.6)	61 (23.9)	79 (31.3)
12,000,001–25,000,000 (~$519–1079)	129 (25.4)	85 (33.3)	44 (17.5)
>25,000,000 VND (~$1079)	42 (8.3)	36 (14.1)	6 (2.4)
Possessed health insurance	396 (78.0)	212 (82.8)	184 (73.0)	0.008
Ethnicity: Kinh	505 (99.4)	255 (99.6)	250 (99.2)	NS
Religion: No religion	489 (96.3)	242 (94.5)	247 (98.0)	NS

a Currency exchange rate in October 2020: 1 USD = 23,176 VND

NS: Not significant | VND: Vietnamese Dong (the currency of Vietnam) | $: United State Dollar (USD)

Knowledge of breast cancer

61% of respondents were knowledgeable about BC symptoms (i.e., they identified ≥ 5 non-lump symptoms). The top three commonly reported symptoms were ‘lump in breast’ (85%), ‘discharge from nipple’ (79%), and ‘pain in breast/armpit’ (77%). The three least commonly known symptoms were ‘puckering/dimpling of breast skin’ (42%), ‘nipple rash’ (42%), and ‘redness of breast skin’ (43%) (S1 Fig in S1 File). Only 40% of respondents had knowledge of BC risk factors. The most commonly known risk factors were ‘past history of BC’ (83%) and ‘having a close relative with BC’ (59%). The least commonly known risk factors were ‘having late menopause’ (21%) and ‘starting periods early’ (17%) (S2 Fig in S1 File). Half of respondents (49%) had knowledge of BC screening modalities. The most commonly known screening modality was CBE (63%), followed by breast ultrasound (52%), and mammography (23%) (S3 Fig in S1 File).

Only 18% of respondents had knowledge of all three domains (symptoms, risk factors, and screening modalities) (Table 2). Overall, a higher level of knowledge about BC was associated with living in an urban area, a higher education level, retirement status, and a higher household monthly income (Chi-square tests, all tests p<0.05). There was no significant association between knowledge of BC and age.

Table 2

Knowledge of breast cancer by sociodemographic characteristics.

Characteristics (n = 508)	Overall knowledge of BCa		p-value
	n	%
Total	91	17.9
Residence area
Urban	62	24.2	<0.001
Rural	29	11.5
Education level
Completed at least primary education	13	12.1	0.002
Completed secondary education	21	12.1
Completed high school education	26	23.6
Completed university degree and above	31	26.5
Occupation
Full-time employee	25	25.5	<0.001
Self-employed	41	13.5
Homemaker/housewife	10	15.2
Retired	15	36.6
Household monthly income
< = 3,000,000 VND (~$129b)	6	17.6	0.004
3,000,001–6,000,000 VND (~$130–259)	7	9.7
6,000,001–9,000,000 VND (~$260–389)	7	10.0
9,000,001–12,000,000 VND (~$390–519)	25	17.9
12,000,001–25,000,000 (~$519–1079)	33	25.6
>25,000,000 VND (~$1079)	13	31.0
Age group
30–39	30	17.2	NS
40–49	26	16.8
50–59	16	15.0
60–74	19	26.4

a Knowledge of BC: Have knowledge in all of the following three domains ‘symptoms’, ‘risk factors’, and ‘screening modalities’

b Currency exchange rate in October 2020: 1 USD = 23,176 VND

BC: Breast cancer | NS: Not significant | VND: Vietnamese Dong | $: United State Dollar (USD)

Attitude/belief towards BC/BC screening

Table 3 shows subscale scores for the CHBMS by sociodemographic characteristics. Younger respondents had a significantly higher perceived susceptibility score regarding BC (ANOVA test, p<0.001) whereas older respondents had a significantly higher perceived benefits score for CBE (ANOVA test, p<0.001). Respondents who lived in a rural area, were self-employed (including homemaker/housewife), had a lower education level, and had a lower household monthly income were more likely to have significantly higher scores regarding perceived barriers to accessing and using CBE (ANOVA test, all tests p<0.001). Age was not associated with the perceived barriers subscale score.

Table 3

Mean CHBMS subscale scores by sociodemographic characteristics.

	Perceived susceptibilitya	P-value	Perceived benefitsb	p-value	Perceived barriersc	p-value
	mean (sd)		mean (sd)		mean (sd)
Total	9.3 (2.3)		19.7 (2.1)		23.7 (4.8)
Residence area
Urban	9.2 (2.2)	NS	19.6 (2.1)	NS	22.5 (4.3)	<0.001
Rural	9.4 (2.4)		19.7 (2.1)		24.9 (5.0)
Occupation
Full-time employee	9.7 (1.9)	NS	19.2 (2.2)	NS	22.0 (4.3)	<0.001
Self-employed	9.4 (2.4)		19.7 (2.1)		24.3 (4.9)
Homemaker/housewife	8.9 (2.4)		20.0 (1.8)		24.2 (3.9)
Retired	8.8 (2.2)		20.2 (2.0)		22.6 (5.5)
Education level
Completed at least primary education	9.4 (2.7)	NS	19.6 (2.2)	<0.001	26.2 (5.2)	<0.001
Completed secondary education	9.2 (2.3)		20.0 (1.9)		24.1 (4.7)
Completed high school education	9.4 (2.2)		20.0 (1.8)		22.6 (4.2)
Completed university degree and above	9.4 (2.1)		19.0 (2.3)		21.8 (4.1)
Household monthly income
< = 3,000,000 VND (~$129d)	8.8 (2.7)	NS	19.6 (2.5)	NS	27.6 (4.6)	<0.001
3,000,001–6,000,000 VND (~$130–259)	9.3 (2.4)		19.8 (1.9)		25.1 (5.5)
6,000,001–9,000,000 VND (~$260–389)	9.5 (2.2)		19.5 (2.0)		24.3 (4.5)
9,000,001–12,000,000 VND (~$390–519)	9.4 (2.3)		20.0 (1.7)		23.9 (4.4)
12,000,001–25,000,000 (~$519–1079)	9.6 (2.2)		19.5 (2.3)		22.4 (4.2)
>25,000,000 VND (~$1079)	9.3 (2.1)		19.3 (2.2)		21.3 (4.2)
Age group (in years)
<40	9.7 (2.0)	<0.001	19.2 (2.3)	<0.001	22.8 (4.5)	NS
40–49	9.5 (2.4)		19.8 (1.8)		24.3 (4.9)
50–59	9.0 (2.3)		19.8 (2.1)		24.5 (4.7)
60+	8.5 (2.5)		20.3 (1.8)		23.4 (5.4)

a Perceived susceptibility scale has min = 3, max = 15

b Perceived benefits scale has min = 5, max = 25

c Perceived barriers scale has min = 10, max = 50

d Currency exchange rate in October 2020: 1 USD = 23,176 VND

CHBMS: Champion Health Belief Model Scale | NS: Not significant | sd: standard deviation | VND: Vietnamese Dong (the currency of Vietnam) | $: United State Dollar (USD)

CBE screening practice/uptake

63% of respondents had experienced some mode of BC screening (Fig 1); 51% of this proportion reported that they had received CBE, followed by breast ultrasound (48%), mammography (25%) and MRI (6%). Area of residence was not associated with uptake except in the case of mammography—32% of respondents in urban area compared to 18% of rural dwellers had had a mammogram (Chi-square test, p = 0.04).

Fig 1

Respondents who had been screened for breast cancer (any modality) by area.

Factors associated with CBE uptake

Table 4 shows the results of a logistic regression model that assessed the association between a range of factors and CBE uptake. Sociodemographic characteristics (i.e., residence area, education level, occupation, household monthly income, and possession of HI) and a respondent’s perceived benefits of getting CBE were not associated with the uptake of CBE. Women who had knowledge of BC were 2.4 times more likely to avail of CBE (OR = 2.44, 95% CI: 1.37–4.32). Each point higher in the perceived susceptibility score significantly increased the odds of CBE uptake 1.15 times (OR = 1.15, 95% CI: 1.05–1.25) whilst each point higher in the perceived barriers score significantly decreased the odds of CBE uptake 0.88 times (OR = 0.88, 95% CI: 0.84–0.92).

Table 4

Which factors are associated with the uptake of clinical breast examination?

Characteristics (n = 504)	Ever had CBE	Adjusted Odds ratio a	95% CI
	Mean (sd)
Perceived susceptibility of getting BC	9.7 (2.2)	1.15 *	[1.05–1.25]
(min = 3, max = 15)
Perceived benefits of getting CBE	19.8 (2.0)	1.03	[0.94–1.13]
(min = 5, max = 25)
Perceived barriers of getting CBE	22.5 (4.5)	0.88 **	[0.84–0.92]
(min = 10, max = 50)
	Ever had CBE	Adjusted Odds ratio a	95% CI
	n (%)
Overall knowledge of BC
Noref	195 (46.8)	1.00
Yes	65 (71.4)	2.44 *	[1.37–4.32]
Residence area
Urbanref	141 (55.1)	1.00
Rural	119 (47.2)	1.22	[0.78–1.92]
Age groups
<40ref	96 (55.2)	1.00	[1.00–1.00]
40–49	79 (51.0)	1.14	[0.69–1.89]
50–59	58 (54.2)	1.36	[0.74–2.47]
60+	27 (37.5)	0.47	[0.21–1.01]
Education level
Completed at least primary educationref	37 (34.6)	1.00
Completed secondary education	88 (50.9)	1.61	[0.90–2.88]
Completed high school education	62 (56.4)	1.71	[0.84–3.49]
Completed university degree	72 (61.5)	2.01	[0.88–4.60]
Occupation
Full-time employeeref	61 (62.2)	1.00
Self-employed	145 (47.9)	0.92	[0.50–1.70]
Homemaker/housewife	29 (43.9)	0.83	[0.37–1.82]
Retired	25 (61.0)	1.70	[0.65–4.43]
Household monthly income
< = 3,000,000 VND (~$129b)ref	10 (29.4)	1.00
3,000,001–6,000,000 VND (~$130–259)	35 (48.6)	1.41	[0.54–3.69]
6,000,001–9,000,000 VND (~$260–389)	32 (45.7)	1.06	[0.39–2.82]
9,000,001–12,000,000 VND (~$390–519)	81 (57.9)	1.49	[0.60–3.65]
12,000,001–25,000,000 (~$519–1079)	71 (55.0)	0.90	[0.35–2.35]
>25,000,000 VND (~$1079)	24 (57.1)	0.86	[0.28–2.63]
Possession of health insurance
Noref	46 (41.1)	1.00
Yes	214 (54.0)	1.12	[0.68–1.82]

BC: Breast cancer | CBE: Clinical breast examination | CI: confidence interval | sd: standard deviation | VND: Vietnamese Dong (the currency of Vietnam) | $: United State Dollar (USD)

ref: reference group

a Odds ratios were adjusted for knowledge of BC, perceived susceptibility, perceived benefits, perceived barriers, residence area, age group, education level, occupation, household monthly income, and possession of health insurance.

b Currency exchange rate in October 2020: 1 USD = 23,176 VND

* p < 0.05,

** p < 0.001

Discussion

The results of the analysis indicate a low level of overall BC knowledge (18%). Yet, 63% of respondents reported participating in at least one type of BC screening modality. Among all types of BC screening modalities, CBE had the highest uptake—two times higher than mammography. CBE uptake was not associated with sociodemographic characteristics in contrast to mammography. This finding together with the results of other research [8] indicates the potential for CBE to be used to extend access to essential cancer services in an equitable way.

Regarding CBE uptake, this study reported a higher percentage compared with previous studies among women in general aged 20–60 years conducted in 2015 and 2017 (51% vs 32%) [25, 26]. The higher CBE uptake proportion in our study may be related to the influence of previous pilot CBE screening programmes in Hanoi (which was the study site for 4/5 pilots [27]) or may reflect a trend towards increased knowledge. Studies in other specific Vietnamese populations such as ethnic minorities and female teachers in primary schools [28, 29] have reported wider variation in CBE uptake, from 17% to 63%. Regarding mammography uptake, both current and previous studies reported a significantly lower uptake proportion compared to CBE [25, 29, 30].

The study also highlights the strong association between BC knowledge and uptake of CBE. Although previous studies of the association between knowledge and CBE specifically are limited, the link between knowledge and BC screening uptake in general is well established [23, 28, 31, 32]. Our results regarding the other factors that were associated with CBE uptake i.e., perceived susceptibility and perceived barriers, highlight the importance of ensuring that a BC screening programme is targeted towards populations that have received BC awareness raising and, so, are informed about and have a good understanding of BC in order to help to maximise the potential of the screening programme.

The study underscores that the current level of BC knowledge (across all three categories: ‘symptoms’, ‘risk factors’, and ‘screening modalities’ among Vietnamese women aged 30–74 years in Hanoi is extremely low (18%). The use of self-developed questionnaires and various definitions of ‘good/bad knowledge’ in all previous KAP studies in relation to BC in Vietnam (five in English and 12 in Vietnamese, published between 2009 and 2019) makes it difficult to undertake meaningful comparisons between the results of these studies and the study that is presented in this paper and, in addition, hinders an assessment of cancer awareness and knowledge in Vietnam including trends over time. Future research should use standardised instruments in order to generate reliable, comparative, and actionable findings to inform public health and cancer preventive service planning decisions.

Several socio-demographic factors were associated with knowledge of BC. Women who lived in an urban area, who had a higher education level and higher household monthly income, and who were retired were more likely to have better knowledge about BC. This pattern of results is consistent with similar studies, globally [23, 25, 33–35] and point to the need for BC awareness raising programmes that are targeted towards, and tailored to, particular groups in the population of Vietnamese women.

Regarding factors that were associated with beliefs towards BC/CBE, the influence of age (group) on the sub-scales of the CHBMS is notable. Indeed, the age of a woman had a negative association with her perceived susceptibility to BC, but it had a positive association with the benefits that she perceived came from CBE screening, whilst age did not appear to exert any influence on her perception of the barriers to availing of CBE. Arguably, this particular mixture or combination of beliefs is likely to lead women to engage in screening behaviour, particularly if they participate in BC knowledge and awareness raising programmes [36]. The much younger age at which BC is diagnosed in Vietnam compared to HICs [2, 7, 37] may explain why younger respondents were more alert to the likelihood of a BC diagnosis despite the fact that BC risk increases with age [38]. The finding that socio-demographic factors such as living in a rural area, being self-employed/a housewife, having lower education and household income were significantly associated with the perception that there were barriers to CBE screening points again to the need for a targeted public health/cancer education programme.

The study has several strengths. For example, it is the first study in Vietnam to use standardised and validated instruments (i.e., Breast-CAM and CHBMS) to assess BC knowledge, attitudes, and beliefs among Vietnamese women. As such, it facilitates comparisons with studies from other countries and provides reliable data for the planning of BC interventions and related policy in Vietnam. More specifically, the study provides novel and valuable insights about the factors that influence the uptake of CBE which will contribute to the implementation of future screening programmes. The study’s limitations include uncertainty about the extent to which the results may be generalized to the whole country and, so, further research is required. We could not explore the influence of ethnicity in relation to CBE uptake as 99% of respondents were from the majority Kinh ethnic group. There is a need for further research to investigate KAP and uptake among ethnic minorities in Vietnam (there are 53 ethnic minorities and they account for 15% of the population [39]).

Conclusions

Only 18% of Vietnamese women aged 30–74 years old had knowledge of BC symptoms, risk factors, and screening modalities though around 63% had had previous experience of BC screening. CBE was the most common screening modality (51% of screened women). Mammography tends to be located in the larger medical centres and it is unsurprising, perhaps, that the uptake in urban areas was almost double the proportion that was reported by respondents in rural areas. Unlike mammography, CBE uptake was not associated with sociodemographic characteristics. CBE uptake predictors were knowledge of BC, perceived susceptibility to BC, and perceived barriers to using CBE. Public health education or promotion interventions are essential preceding the implementation of a BC screening programme in Vietnam. Current engagement and the absence of socio-demographic disparities indicate that a CBE programme is likely to produce positive outcomes for Vietnamese women, their families, and wider society.

Minimal dataset.

(XLS)

Click here for additional data file.

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(PDF)

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22 Feb 2022

Breast cancer screening practices among Vietnamese women and factors associated with clinical breast examination uptake

PLOS ONE

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Reviewer #1: Yes

Reviewer #2: Partly

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

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Reviewer #1: Yes

Reviewer #2: No

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Reviewer #1: Yes

Reviewer #2: Yes

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5. Review Comments to the Author

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Reviewer #1: The subject matter of this manuscript is a global public health issue and very critical for all countries. The authors have presented the results in an intelligible fashion in mostly simple and clear language. The sample size is large and seem representative for the Vitanamese women of reproductive age. The results are well analyzed and presented clearly and the statistical analysis are robust. The discussion section is also presented concisely and the conclusions are drawn based on the results presented.

I do have a few suggestions that I think will make the manuscript even more meaningful to all readers.

1. Please, provide more elaboration on the ethical review and approval process in addition to the approval number and the statement that participants gave consent prior to be being included in the study. What kind of consent was given? Written or verbal and how was participants informed and convinced to participate and to consent?

2. Please, provide some explanation on the inclusion and exclusion criteria for the study besides the age limitation.

3. In the results presentation, you used statements such as " approximately, less than, about around two-thirds". Please, be straight forward and use the exact percentages instead of the probable phrases before the percentages in parenthesis.

4. Please, be consistent with the use of either Vietnam women or Vietnamese women instead of using them interchangeably. However, I could be wrong as both could be acceptable in Vietnam. Please, advise.

5. There are a few vocabulary issues and a careful edit will resolve them, please.

6. In the discussion section, please, provide more relevant studies in the literature related to your study and do the relevant comparisons.

7. Please, add a section on strengths and limitations and add the statement on your use of standardized instrument compared to personally developed instruments as a strength. Then provide a weakness if there a challenge you encountered.

Overall, the study is important and will provide a critical resource for health promotion and disease prevention officers in addition to adding knowledge to existing literature.

Reviewer #2: Given the absence of a copy editor, it would serve the authors well to have the manuscript proof-read and edited to improve conciseness.

Abstract:

Was the instrument cross culturally adapted, translated, back translated? Please elaborate.

Was IRB approval obtained, were patients consented. Based on answers to questions, it appears they did. But might be better to state this in methods: In this IRB-approved study, consented patients responded to a 300-item scale cross culturally adapted from the …”

When you say, “18% of V. Women had knowledge’” what does that mean – this percentage discussed with someone, heard about breast cancer, …

Introduction:

Excellent first paragraph with high yield information. It might help to mention that in the absence of a population-based screening program, early detection (of which awareness is key) is essential.

Second paragraph:

The second sentence is inaccurate and should be removed. In fact, mammography is highly useful in this age group. It does have reduced sensitivity in dense breast women, which is more common in Vietnamese and young women for a variety of reasons. However, it is still effective. Also, there are multiple reasons to list to describe why mammography is not a good option in LMICs.

Unlike first paragraph, where authors provided specific data to support their research, the second paragraph lacks data and speaks generally. I would prefer more information here. I think a lot of this paragraph is unnecessary and could be more concise to present data without increasing word count.

Methods:

Paragraph 1:

Please state why you chose neighborhoods in Hanoi and what you did when someone wasn't home (did you return, leave your number). What days and times of days did you visit? (if you visited during weekday, then maybe women at home were more likely new mothers or unemployed, or…). It helps reader understand bias that might be present/how generalizable the results are.

I think the ethical statement should be at front of paragraph, but this is more stylistic.

Was the instrument translated, back translated, who translated? Were the interviewers trained, what experience did they have?

Results:

It would help to see the instrument. I’m not sure what a “non-lump symptom” is or what the authors considered risk factors.

Pain is a late symptom. In fact, studies have shown that pain alone as a symptom is unlikely to be related to breast cancer. Is this what you want women, particularly young women, to learn. Part of raising awareness is to limit overburdening the healthcare system and teaching “pain” as a breast cancer symptom could have opposite effect.

Breast cancer knowledge is presented as a scale. Did they check the relationship between the items?

Discussion:

Please use first paragraph to state the most important finding of the study and what implication this has on the Vietnamese population (as it pertains to breast cancer)

Authors do a good job of stating their results and stating (usually) how this relates to Vietnamese population, but then fail to drive home the “so what”. Also, the discussion lacks conciseness and synthesis of the results. I would avoid showing data here unless it helps convey a point you make in the paragraph.

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Reviewer #1: No

Reviewer #2: No

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1 Apr 2022

Please find details in attached file 'Response to reviewers'

Submitted filename: Response to reviewers.docx

Click here for additional data file.

22 Apr 2022

26 Apr 2022

Please find details in attached file 'Response to reviewers'.

Submitted filename: Response to reviewers.docx

Click here for additional data file.

18 May 2022

Breast cancer screening practices among Vietnamese women and factors associated with clinical breast examination uptake

PONE-D-21-17006R2

Dear,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

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Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: All comments have been addressed

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2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

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Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: I have thoroughly reviewed the manuscript again comparing this version to the original and first revised versions and have concluded that the authors have done a great job of improving the manuscript greatly. All the concerns I had and the almost all the minor issues have been addressed.

Reviewer #2: The authors addressed all my comments and the paper reads substantially better. They now provide substantial details necessary to replicate their work. Their work is important and will be interesting to the PLOS readership. There remain a couple of typos (For example):

1. In methods, first section line 87 should say "on average" because all Vietnamese women aren't diagnosed with breast cancer at an earlier age that European women, it's just that the average age at presentation is younger.

2. Line 92 "This study" rather than "The study"

3. first paragraph of discussion, last sentence should specify what "this screening" means - is it CBE or mammography. It may mean that a couple of commas are needed around in contrast to mammography. Also, do the authors mean "socially acceptable method for screening" (Rather than potential screening method) since their data shows that many women of all demographic received CBE despite few having awareness?

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Reviewer #1: No

Reviewer #2: No

20 May 2022

PONE-D-21-17006R2

Breast cancer screening practices among Vietnamese women and factors associated with clinical breast examination uptake

Dear Dr. Ngan:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

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