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Prevalence and sociodemographic correlates of routine breast cancer screening practices among migrant-Australian women Michelle Lam,1 Cannas Kwok,2 Mi-Joung Lee1

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reast cancer is the most common cancer among women worldwide and in Australia, accounting for 25%1 and 2 28% of all female cancers, respectively. Given that health projections for 2020 anticipate the incidence of breast cancer among Australian women will continue to rise,2 early detection of breast cancer by regular screening is vital. In Australia, a populationbased mammographic screening program (BreastScreen) has been implemented for more than 20 years.3 However, immigrant women have consistently reported to have lower participation rates than Australianborn women. Given that immigrants account for more than one-quarter of Australia’s resident population (28.1%),4 it is imperative to investigate what factors have hindered their participation in breast cancer screening practices so that more targeted interventions can be developed and implemented. Epidemiological evidence indicates that a woman’s risk of developing breast cancer rises following migration from low-risk countries, such as those in Asia, to Western countries. A US study comparing Japanese migrants to their counterparts in Japan showed that breast cancer incidence was more than twice as high in Japanese-American women.5 Similar patterns were observed in Chinese women following migration to Australia.6 Considering the increase in incidence rates following migration, it is essential to promote breast cancer screening (BCS) practices among immigrant women in Western countries.

Abstract Objective: To evaluate breast cancer screening (BCS) practice and explore the relationship between sociodemographic factors and breast awareness (BA), clinical breast examination (CBE) and mammography in migrant-Australian women. Method: Secondary analysis was performed on the pooled sample (n=1,744) from five cross-sectional studies of BCS rates among immigrant-Australian women, and the associated sociodemographic factors. Results: Only 19% of women participated in routine BA, 27.4% of women in the target group of >40 year presented for an annual CBE, and 60.6% of women in the target group of 50–74 years received a biennial mammogram. Associated sociodemographic factors differed by modality except for length of Australian residency. In multivariable analysis, age, length of Australian residency, marital status, and employment status accounted for more than 50% of the variance in regular BA and CBE. Conclusion: These findings indicate suboptimal BCS rates persist among migrant-Australian women, and suggest the importance of certain sociodemographic factors in BCS practice. Implications for public health: Further education is required for BA and CBE practice in immigrant-Australian women, especially for those who have resided in Australia less than 12 years without a partner. Key words: immigrant-Australian women, breast cancer screening, mammograms, clinical breast examination, sociodemographic factors Breast self-exam (BSE), clinical breast examination (CBE) and mammography remain the primary means of early detection of breast cancer. Since 2009, the focus in Australia has shifted from BSE to being ‘breast aware’ (BA).7 This is due to a growing recognition that women did not perform BSE because of fear about not knowing the correct technique.8 Recent education campaigns have focused on ‘being breast aware’ as opposed to performing BSE. That is, women of all ages are encouraged to be familiar with the normal appearance and feel

of their breasts without a special technique. While asymptomatic women over 40 years of age are also recommended to attend a CBE annually, women aged from 50 to 74 are encouraged to have a mammogram biennially.7 Nevertheless, international studies among immigrant women consistently reveal that they are under-served groups. For example, local studies reported that only 22.1% of Chinese9 and 12.4% of KoreanAustralian women10 have been breast aware, and only 21.4% and 3.5% of Arabic 11 and African-Australian12 women had attended a

1. Discipline of Physiotherapy, Faculty of Health Sciences, The University of Sydney, New South Wales 2. School of Nursing and Midwifery, Western Sydney University, New South Wales Correspondence to: Dr Mi-Joung Lee, Discipline of Physiotherapy, Faculty of Health Sciences, The University of Sydney, PO Box 170, Lidcombe, NSW 1825; e-mail: [email protected] Submitted: February 2017; Revision requested: April 2017; Accepted: October 2017 The authors have stated they have no conflict of interest. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. Aust NZ J Public Health. 2017; Online; doi: 10.1111/1753-6405.12752

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CBE annually, respectively. Similarly, in the US, the prevalence of ever having a mammogram is lower among Arab-American women than American-born women by more than 22%.13 Consistently, only 27% to 57.5% of KoreanAmerican women reported having regular BSE and mammograms, respectively.14,15

between sociodemographic characteristics, acculturation level and BCS practices as recommended.

Previous studies have identified sociodemographic differences associated with BCS participation among immigrant women in Western countries.15-18 Compliance with screening recommendations has been reported to vary by marital status, education level, employment status and age, as well as acculturation level. Married and de facto Arab13,16 and Vietnamese15 women have consistently reported higher mammographic screening rates compared to their unmarried counterparts. Some previous studies found that BCS participants tend to be younger,18 educated9 and employed.19 However, a study of Chinese migrant-women in Australia9 found no significant correlation between either education or employment and mammographic screening. In the same study, older women also recorded higher rates of mammogram coverage. Conflicting evidence exists for the influence of education level on BCS uptake.

This was a secondary analysis based on data from five studies conducted between January 2009 and March 2015. Each involved self-administered questionnaires in separate Australian-migrant populations: African,12 Arabic,11 Korean,10 Indian25 and Chinese.26 Ethics approval was granted by the Human Ethics Committees of the University of Sydney (11311 on 13 November 2008) and Western Sydney University (H9759 on 26 March 2014).

Among other explanatory factors, critics attribute the heterogeneity in BCS participation to acculturation, the process in which an individual adopts the beliefs and practices of their host country.20 Length of stay in the host country17 and language proficiency16 are commonly used proxies for acculturation, and well-cited correlates for breast cancer screening practices among immigrant women in Western countries. A body of literature suggests that the longer the immigrant woman stays in the host country, the more likely they are to participate in mammographic screening. A similar pattern was observed for English proficiency.21,22 Limited English proficiency among migrants in Western countries has been consistently identified as a major barrier to BCS.14,23,24 Despite the ethnic heterogeneity of the Australian population, and the projection that breast cancer is likely to remain the most common female cancer,2 few studies have systematically examined BCS practice in Australian migrant populations. To fill the paucity of literature, this article endeavours to collectively: 1) examine the BCS status (breast awareness, clinical breast examination and mammograms) of migrant-Australian women; and 2) analyse the relationship

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Methods Design

Participants and recruitment A convenience sample of 1,791 migrant Australian women was recruited across five separate studies. Recruitment was through various ethnic associations, churches, community centres, women’s organisations and private clinics of those relevant ethnic communities in Sydney, the capital city of New South Wales, which is the state with the largest number of immigrants.5 The selection criteria included: 1) being 18 years of age and older; 2) having immigrated to Australia; 3) being self-identified from the relevant cultural groups; and 4) being able to read English or their relevant languages. Women with a history of breast cancer were excluded.

Data collection Data collection was performed by bilingual researchers who shared the culture and language of the participants from each community. With the assistance of community organisations, their female members were invited to participate in the study. Women who were willing to participate were given a study information sheet and questionnaire, with a choice of either English or their relevant language, and requested to return it to a sealed box located in the venue. Participants were made aware that participation was voluntary and that no personally identifiable information would be collected. Returning the questionnaire was taken as an indication of voluntary consent.

Instrument The Breast Cancer Screening Beliefs Questionnaire (BCSBQ) was designed as a culturally sensitive instrument to assess

women’s breast cancer beliefs and attitudes toward screening and was produced in versions of Arabic, Korean, Indian, African and Chinese languages. Reliability and validity of the questionnaire in each ethnic group were published elsewhere.10-12,25,26 The questionnaire obtained information on demographic variables such as age, length of stay in Australia, level of education, marital status and English proficiency. Information regarding women’s BCS practices was then obtained, including if they had heard of BA, CBE and mammographic screening and, if so, how often they participated in each modality.

Data analysis Secondary data analysis was performed on the combined five data sets using the Statistical Package for Social Sciences (IBM SPSS, version 22 for Windows). Descriptive statistics were used to characterise the sample and report BCS practices. Bivariate analysis was performed to evaluate associations between sociodemographic variables and three BCS modalities. For bivariate analysis, all variables were dichotomised. Age and length of stay were dichotomised using Receiver Operating Characteristic (ROC) analysis to identify optimal predictor cut-offs that indicate compliance with screening recommendations. Marital status was coded as “no partner” for single, divorced and widowed women, and “partner” for women in a married or de facto relationship. Level of education was coded as “secondary education or below” and “above secondary”, and English proficiency was coded “below average” and “average or above”. Employment was categorised into “unemployed”, which encompassed unemployed and retired women, and “employed”, which included those engaged in part-time and fulltime work. In line with Cancer Australia recommendations,7 BA was analysed among all women, while the data for CBE and mammogram compliance was only analysed for women over 40 years of age. Odds ratios (ORs) and 95% confidence intervals (CI) were calculated. Statistical significance was considered when p≤0.05 and/or OR>1.00. Multiple logistic regression models were used to fit the final model between sociodemographic variables and each of the screening modalities. Variables with p0.05) were progressively eliminated, starting with the least significant variable, until the remaining variables in the final model were all significant.

Results Of the 1,791 participants across the combined sample, 47 women (2.6%) were excluded from the analysis because they were Australianborn and/or had previously had breast cancer. A total of 1,744 women met the selection criteria and were included in the analysis. The detailed demographic characteristics of the participants are presented in Table 1. The mean age of the participants was 46.6 years (Standard deviation [SD] = 13.8). Of the 1,744 participants, 1,142 women (65.5%) were in the targeted >40 years for the recommended annual CBE, and 695 women (39.9%) were within the target age (50–74 years) for the current recommended biennial mammograms. More than half the women (53%) rated their English proficiency as good or very good, and nearly three-quarters (73.6%) reported being in a married or de facto relationship. The average amount of time the participants had lived in Australia was 12.6 years (SD=9.5). Descriptive analysis showed that, of the 1,744 women, 332 (19.0%) had participated in BA monthly, as recommended. Among the women in the target age group of >40 years, 313 women (27.4%) reported presenting an annual CBE, while 421 of women (60.6%) in the target age group of 50–74 years had attended for a biannual mammogram (Table 2). In bivariate analysis (Table 3), length of stay in Australia emerged as the most significant predictor of BA (≥12 years: OR 2.096; 95%CI 1.638–2.682; p=0.000), while employment status was the most predictive of not participating (OR 0.574; 95%CI 0.449–0.730; p=0.000). Women in a relationship (OR 1.346; 95%CI 1.012–1.791; p=0.041) and those aged over 48 years (OR 1.899; 95%CI 1.484–2.430; p=0.000) were considerably more likely to adhere to BA recommendations. English proficiency (p=0.473) and education level (p=0.163) were not statistically related to regular BA practice. With the exception of age, similar sociodemographic factors were associated

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with annual CBE attendance. Length of stay in Australia was again the most significant predictor of annual CBE (Table 4: OR 2.767; 95%CI 2.108–3.631; p=0.000); however, the ROC-curve for length of residence (≥15 years) was slightly longer compared to BA. Women with a current partner were more likely to have had a CBE in the past year (OR 1.716; 95%CI 1.210–2.434; p=0.002). Women who were currently employed were less likely to attend annual CBE (OR 0.643; 95%CI 0.495– 0.836; p=0.001). There was no appreciable difference in proportions for education level or English proficiency (Table 4). Different sociodemographic correlates were related to women’s biennial mammogram practice compared to BA and CBE practice (Table 4). Women who were more likely to present for biennial mammographic screening were aged ≥56 years (OR 1.453; 95%CI 1.067–1.978; p=0.018) and had lived in Australia for ≥14 years (OR 2.357; 95%CI 1.726–3.218; p=0.000). In addition, English-proficient women (OR 1.728; 95%CI 1.253–2.383; p=0.001) and women with a partner (OR 1.808; 95%CI 1.264–2.587; p=0.001) were more likely to participate in biennial mammogram. Level of education and employment status were not significantly related with biennial mammogram practice (p>0.05). In multivariable logistic regression analysis, age, length of stay and employment status were retained in the final model for BA, significantly accounting for 54% of the variance (p=0.000, OR=1.243). Length of stay, marital status and employment status explained 54% of the variance in annual CBE attendance (p=0.000, OR=0.628). Lastly, age, length of stay, marital status and English proficiency emerged as significant correlates

of mammogram receipt, accounting for 80.5% of the variance (p=0.000, OR=1.337).

Discussion To our knowledge, this study is the first of its kind to report BCS practice according to

Table 1: Sociodemographic characteristics of participants (N = 1,744). Variable Years of age Length of stay in Australia (years) Ethnicity African Arabic Indian Korean Chinese Marital status Single Married/de facto Divorced/separated Widowed Missing Education None or primary school Secondary school Technical (TAFE) or other college Tertiary or above Missing Employment status Full Time Part Time Unemployed Retired Missing English proficiency Not at all Little Average Good Very good

Mean 46.6 12.6 N

SD 13.8 9.5 %

264 251 242 249 738

15.1 14.4 13.9 14.3 42.3

264 1,281 121 75 3

15.1 73.5 6.9 4.3

118 408 374 843 1

6.8 23.4 21.4 48.3

498 408 589 242 7

28.6 23.4 33.8 13.9

130 286 40 457 468

7.5 16.4 23.1 26.2 26.8

Table 2: Breast cancer screening practices of all participants and target age group. Screening practice Breast awareness Ever heard of it Ever performed Performed as recommended (monthly) Clinical breast examinationa Ever heard of it Ever performed Performed as recommended (annually) Mammogramb Ever heard of it Ever performed Performed as recommended (biannually)

All participants N (%) 1,472/1,744 (84.4) 1,120/1,744 (64.2) 332/1,744 (19.0)

Target age group† N (%)

1,228/1,744 915/1,744 401/1,744

(70.4) (52.5) (23.0)

836/1142 694/1142 313/1142

(73.2) (60.8) (27.4)

1,334/1,744 832/1,744 610/1,744

(76.5) (47.7) (35.0)

609/695 522/695 421/695

(87.4) (75.1) (60.6)

a: Clinical breast examination: 40 years or older b: Mammogram: between 50 and 74 years


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Cancer Australia recommendations7 for a large sample, without disaggregating ethnic groups. Our results indicate that migrantAustralian women are not partaking in BCS, particularly regarding breast awareness and attending CBE in accordance with guidelines, with only 19.0% and 27.4% of the participants being breast aware and attending CBE annually, respectively. Our observations are consistent with those made among immigrant groups in the US,14 Canada27 and the UK.28 This is alarming, as epidemiological studies suggest that the peak age for breast cancer among women from cultural backgrounds such as Arabic, African and Asian (40–49 years)29 is much younger than for Caucasian women (65–69 years).30 While mammogram is targeted at women over the age of 50, being breast aware and CBE are the key screening practices for younger women to detect breast cancer early. In terms of mammographic participation, our study did reveal some promising results, with 60.6% of the participants having attended a mammogram biannually as recommended. This is slightly higher than the national figure of 55% among Australian-born women and 50% among non-English-speaking background women, respectively.3 However, in interpreting these results, it is important to note that the sample represented an acculturated group of women. More than three-quarters (76.1%) of the participants rated their English proficiency as average or higher than average, and almost threequarters of the women were college or

tertiary graduates (60.7%). Considering that English proficiency appears to be a predictor for mammography participation, sampling bias may have accounted for such favourable findings. Therefore, further research with a larger sample of immigrant women with lower English proficiency is warranted. Our study revealed important sociodemographic characteristics associated with three BCS modalities in a large, ethnically diverse migrant-Australian sample. The positive influence of marital status on BCS is well articulated in the literature. Our findings of superior BA participation, as well as CBE and mammogram attendance among married and de facto women, mirror those reported for migrants in Denmark19 and the US.18,20 A possible explanation may lie in the important role of a spouse in mediating attitudes towards BCS.31 Along with household size, marital status is posited to reflect social support.16 A review of immigrant women and their cancer screening behaviours found that women are more inclined to seek BCS when it is socially sanctioned by a spouse, family member or friend and with membership with community groups.32 This is in line with studies that consistently demonstrate that significant others play a vital role in women’s healthseeking behaviours. Unmarried women should therefore constitute a target group for BCS practices promotion. Our finding that employed women are significantly less likely to report BA and CBE attendance contradicts studies in which

Table 3: Demographic factors associated with monthly breast awareness. Variable Age (years) (n=1,719) < 48a ≥ 48a Length of stay (years) (n=1,719) < 12a > 12a Marital Status (n=1,717) No partner Current partner Education (n=1,718) Secondary and below Above secondary Employment Status (n=1,715) Unemployed Employed English proficiency (n=1,719) Below average Average or above

No

Yes N (%)

OR (95% CI)

p-value

732 (42.6) 655 (38.1)

123 (7.2) 209 (12.1)

1 1.899 (1.484-2.430)

0.000

766 (44.6) 621 (36.1)

123 (7.2) 209 (12.1)

1 2.096 (1.638-2.682)

0.000

381 (22.2) 1004 (58.5)

73 (4.3) 259 (15.1)

1 1.346 (1.012-1.791)

0.041

405 (23.6) 981 (57.1)

110 (6.4) 222 (12.9)

1 0.833 ( 0.645-1.076)

0.163

624 (36.4) 760 (44.3)

195 (11.4) 136 (7.9)

1 0.574 (0.449-0.730)

0.000

325 (18.9) 1062 (61.8)

84 (4.9) 248 (14.4)

1 0.904 (0.685-1.192)

0.473

a: Cut-offs calculated using ROC curve. OR = odds ratio; CI = confidence interval

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positive associations between employment status and screening compliance were found.19 It also challenges the theory that employed women are better positioned to access health information, and are thus more aware and inclined to practice BCS. An explanation for our findings may exist in health negligence due to competing priorities in women’s lives such as work and family commitments. Shirazi and colleagues report that Afghan women in Northern California acknowledge their family’s needs above their own, citing a lack of time as a significant barrier to BCS.33 Literature regarding education level and screening rates is varied, and our results showed no correlation between education and any of BCS. While some have found that highly educated women are more likely to possess the skills necessary to negotiate health services and access BCS,9 others document an inverted U-shaped association between education and participation in screening.19 This may be explained by the critical approach to screening exhibited by educated women. It is important to note that our sample represented a welleducated group of women, with the majority of participants being college or tertiary graduates (69.7%). Had fewer well-educated women been included in the study, the results may have been broader than those that were found. However, it is also worth noting Australia’s skilled migration schema, in which migrant candidates are granted points for higher education attainment. This offers a possible explanation for the high education levels within our sample. Consistent with previous studies,20 our study found that older women are significantly more likely to practice BA and to attend mammogram. This may be a result of agespecific health information, free biennial mammograms or invitations offered to women over 50 years of age. Older women are also more likely to be retired, so work commitments and time would be less of a barrier for BCS.9 As mentioned earlier, immigrant women tend to be diagnosed with breast cancer at a younger age, therefore future education efforts should emphasise the importance of BA and CBE as a diagnostic tool for younger women who are not yet eligible for free mammographic screening. Historically, acculturation surrogates such as length of residency in the adopted country and English proficiency have been consistently cited as predictors for BCS


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Breast cancer screening among migrant-Australian women

practice among immigrant women.22 Our findings partially support this claim. Length of stay in Australia appears as the strongest predictor of BA participation and CBE attendance, and is significantly associated with mammographic attendance. This is consistent with patterns observed among Hispanic-American31 and Chinese-New Zealand34 migrant women, and endorses the theory that BCS ratios increase in tandem with length of time in the adopted country.23,31 This may be a function of increased exposure to health information, additional opportunities for health education24 and development of skills to negotiate the health system.35 Clearly, additional efforts should be directed at educating and promoting BCS awareness among new arrival immigrants. In terms of English proficiency, a significant association was only found in mammographic attendance, and not with BA and CBE. This is consistent with studies among Korean women in the US21 and Vietnamese women in Canada,36 which demonstrate a strong association between English proficiency and mammogram attendance. In such populations, English proficiency poses difficulties when navigating mammographic screening services, particularly when

making appointments or communicating with technicians. It is not uncommon that immigrants prefer to consult a family doctor who shares a similar culture and language. In this case, language would not be a barrier for attending a CBE, and factors other than demographic issues may be responsible for hindering screening participation. We must consider that acculturation is a multidimensional process that reflects assimilation with the adopted culture, its attitudes and beliefs, including those related to cancer screening.22 Operationalising acculturation with sociodemographic factors may not be sufficient, as it neglects the influence of culturally mediated beliefs on health-seeking behaviours. BA may be affected by conservative beliefs held by women from minority cultures that render touching of the body taboo.32,37 A body of literature also shows that culturally mediated cancer beliefs such as fatalism are strong correlates of immigrant women’s cancer screening practices.21,32 These beliefs may persist regardless of education and English proficiency. In multivariate modelling, mammogram attendance was strongly predicted by four sociodemographic characteristics. In fact,

95% of women who were English proficient, older than 56 years of age, had a partner and had lived in Australia for more than 17 years were mammogram recipients. These results indicate that current mammography promotion programs should be revised, and additional interventions should be developed to target those who fall outside this subgroup. Health promotion interventions for early diagnosis of breast cancer should be expanded to include navigational assistance to support young, recent migrants and those without a partner in negotiating the health system.

Limitations Generalisation of these results needs to be made with caution. Although the convenience sample was drawn from various community organisations and across only five ethnic groups, these groups are the largest non-English background immigrant populations in the major cities of Australia.4,38 In addition, our study was conducted only in Sydney, but migrant people – especially those from non-English-speaking backgrounds – are more likely to live in major urban areas than people born in Australia and people from English-speaking countries such as New

Table 4: Demographic factors associated with participation in cbe and mammograms as recommended an women within target age. Variable

No N (%)

Annual CBE (n = 1142) Yes OR (95% CI)

No

p-value

Biennial Mammogram (n = 695) Yes OR (95% CI) N (%)

p-value

Age (years)

< 53a > 53a

391 (34.2) 438 (38.4)

152 (13.3) 161 (14.1)

1 0.946 (0.729-1.227)

0.673

< 56a > 56a

127 (18.3) 147 (21.1)

157 (22.6) 264 (38.0)

1 1.453 (1.067-1.978)

0.018

486 (42.6) 343 (30.0)

106 (9.3) 207 (18.1)

1 2.767 (2.108-3.631)

0.000

< 14a > 14a

153 (22.0) 121 (17.4)

147 (21.2) 274 (39.4)

1 2.357 (1.726- 3.218)

0.000

194 (17.0 635 (55.6)

47 (4.1) 266 (23.3)

1 1.716 (1.210-2.434)

0.002

80 (11.5) 194 (27.9)

78 (11.2) 343 (49.4)

1 1.808 (1.264-2.587)

0.001

305 (26.7) 524 (45.9)

114 (10.0) 199 (17.4)

1 1.016 (0.776-1.331)

0.908

128 (18.4) 146 (21.0)

177 (25.5) 244 (35.1)

1 1.209 (0.890-1.642)

0.225

376 (32.9) 453 (39.7)

176 (15.4) 137 (12.0)

1 0.643 (0.495 -0.836)

0.001

141 (20.3) 133 (19.1)

205 (29.5) 216 (31.1)

1 1.117 (0.824-1.514)

0.476

238 (20.8) 591 (51.8)

88 (7.7) 225 (19.7)

1 1.030 (0.771-1.374)

0.843

111 (16.0) 163 (23.5)

119 (17.1) 302 (43.5)

1 1.728 (1.253-2.383)

0.001

Length of stay (years)

< 15a > 15a Marital status

No partner Current Partner Education

Secondary and below Above secondary Employment status

Unemployed Employed English proficiency

Below average Average or above a: Cut-offs calculated using ROC curve OR = odds ratio; CI = confidence interval

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References

Zealand and the UK.38 Our sample was more homogenous and acculturated than we had anticipated, with women predominantly being married, educated, English-proficient and long-term Australian residents. While a more varied and representative sample would allow associations between sociodemographic gradients and BCS to be more apparent, the increased skills and education focus within Australia’s migration scheme suggests our sample may be representative of the country’s current migrant population. Reliance on self-reported measures and use of translated questionnaires may have also confounded our results.

Conclusion Breast cancer is the most common female cancer in Australia, yet our findings indicate that the screening participation rates in BCS practices among immigrant women are not favourable. Our results suggest that sociodemographic variables are influential in participation in all screening modalities. Continued effort is needed to further elucidate the influence of sociodemographic characteristics on screening behaviours in this vulnerable population.

Implications for public health Breast cancer screening promotion efforts should be focused on specific subgroups of immigrant women to allow further understanding of the barriers to participation in breast cancer screening practices. Specific focus should be in promoting early detection of breast cancer for immigrant women who are younger than 50 years old and newly arrived in Australia, and those without a partner. Those immigrant women should be educated on the importance of regular BA, and CBE in particular, as they are not yet eligible for free mammographic screening and tend to be diagnosed with breast cancer at a younger age.

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