Cervical cancer is an important global health problem in women. It is the fourth most common cancer in women worldwide with an age-standardised rate (ASR) of 14.2 per 100 000.1 Cervical screening and treatment of precancerous lesions have been shown to reduce the incidence and mortality of cervical cancer in many developed countries. This remarkable success has been achieved through organised screening programmes. Such programmes, however, are not routinely available in most developing countries.2 3

An organised cervical cancer screening programme was launched in Hong Kong in 2004 for 25- to 64-year-old women who were currently or previously had been sexually active.4 The programme does not proactively recruit eligible women who have never had a cervical smear. These women must seek cervical smear services by themselves from family health service clinics, well women clinics, general practitioners, or private gynaecologists for their first smear before they can be registered under the programme and become eligible for recall for subsequent smears. Of eligible women in Hong Kong, 30% have yet to have a cervical smear, despite the availability of the scheme for 11 years.5 The most common reasons cited were cost, lack of time, ignorance about cervical cancer and screening, lack of knowledge about how to access the screening service, and embarrassment.6 7 8 9 These reasons were particularly common for marginalised women.

‘Ripple Action’ is a collaborative project launched by several women professional bodies to serve the marginalised women in Hong Kong. Collaborating parties include doctors, nurses, lawyers, accountants, social workers, and various local women organisations. ‘WE Stand’ is a project launched by RainLily in collaboration with the Hong Kong Women Doctors Association to raise the awareness about sexual violence against foreign female workers and ethnic minority women. These two projects organise free cervical screening events for low-income women, new immigrants from Mainland China, and ethnic minority women. The objective of this study was to analyse the pattern of cervical smear abnormalities in these marginalised women.

The study group consisted of women who had a cervical smear taken in one of the 16 free cervical screening events held between March 2008 and November 2014. These women were recruited by various charitable non-governmental organisations (NGOs) and included low-income local Chinese women in receipt of assistance from NGOs, new immigrants from Mainland China who had lived in Hong Kong for less than 7 years, and ethnic minority women mainly from South Asia and South-East Asia. Demographic data, including age, self-reported ethnicity, date of last menstrual period, and history of cervical smear were recorded. Menstruating women and those with a hysterectomy or no sexual history were excluded from screening. Informed consent for cervical smear taking was obtained. Cervical smears were processed using the ThinPrep Pap Test liquid-based system in an accredited cytology laboratory and examined by accredited cytopathologists at a private hospital. All cervical smear reports were reviewed by specialist gynaecologists. Women with a normal cervical smear were called to collect the report in person from the referring NGO. Women with a cervical smear abnormality were individually counselled by a specialist gynaecologist. Women with atypical smears were referred to a family health service clinic for a follow-up smear. Women with epithelial lesions were referred to the gynaecology department in a public hospital.

The prevalence of cervical smear abnormalities in the study group was compared with a comparison group that comprised cervical smear reports selected from the database of a well women clinic in Hong Kong. The first 200 of every 1000 sequential smear reports taken in the four Februarys of the years 2011 to 2014 were selected. To ensure that these reports were from local Chinese population, reports bearing foreign names and those with the first alphabet of the identity card number being R (holders arrived Hong Kong from 2000 to 2011), M (holders arrived after 2011), or W (foreign workers) were excluded. Unsatisfactory smears and vault smears were also excluded. Statistical analysis of the difference in the prevalence of cervical smear abnormalities between the study and the comparison groups was performed with Chi squared test using the Statistical Package for the Social Sciences (Windows version 22.0; SPSS Inc, Chicago [IL], US). A P value of <0.05 was regarded as statistically significant. Binary logistic regression analysis was performed to predict the odds of having a cervical smear abnormality using the following variables: (1) age; (2) resident in Hong Kong for less than 7 years; (3) never had a cervical smear before; (4) ethnicity including local Chinese (reference group), new immigrant from Mainland China, South-East Asian (Indonesian, Filipino, and Thai) or South Asian (Indian, Pakistani, Sri Lankan, Nepalese, and Bangladeshi). The study was approved by the Joint Chinese University of Hong Kong–New Territories East Cluster Clinical Research Ethics Committee (CREC Ref. No.: 2015.426).

There were 1194 participants across the 16 free cervical screening events. Five women were excluded from cervical smear screening because of previous hysterectomy or current menstruation. Thus, the study group consisted of 1189 marginalised women, including 324 low-income local Chinese women who were receiving assistance from NGOs, 540 new immigrants from Mainland China who were residents in Hong Kong for less than 7 years, and 325 ethnic minority women mainly from South Asia and South-East Asia. The characteristics of the study group, including the self-reported ethnicity, history of cervical smear, and prevalence of cervical smear abnormalities are shown in Table 1. Among the 838 women with information available about a history of cervical smear, 357 (42.6%) had never had a cervical smear. Compared with the local Chinese in the study group, there were significantly more ethnic minority women and new immigrants from Mainland China who had never had a cervical smear (61.2% vs 45.4% vs 25.0%; P<0.001), and their prevalence of cervical smear abnormalities was also significantly higher (20.0% vs 12.8% vs 9.0%; P<0.001) [Table 1].

There were 163 women with cervical smear abnormalities in the study group, including 129 (79%) atypical cells of unknown significance (ACUS), 21 (13%) low-grade squamous intraepithelial lesion (LSIL), and 13 (8%) high-grade squamous intraepithelial lesion (HSIL). Compared with the 1141 local Chinese women in the comparison group, the study group had a significantly higher proportion of women who had never had a cervical smear (42.6% vs 0%; P<0.001), and a significantly higher prevalence of cervical smear abnormalities (13.7% vs 1.4%; P<0.001), including ACUS (10.8% vs 0.5%; P<0.001), LSIL (1.8% vs 0.8%; P=0.036), and HSIL (1.1% vs 0.1%; P=0.002) [Table 2]. Binary logistic regression analysis showed that the strongest predictors for abnormal cervical smear were being South Asian (odds ratio [OR]=11.859; 95% confidence interval [CI], 4.635-30.341), South-East Asian (OR=6.484; 95% CI, 3.192-13.171), or a new immigrant from Mainland China (OR=6.253; 95% CI, 2.463-15.877) [Table 3].

We also compared the prevalence of cervical smear abnormalities in the study group with another data set that consisted of 509 439 cervical cytology tests first recorded among registered women in the Cervical Screening Information System (CSIS) from the Cervical Screening Programme of the Department of Health from 2004 to 2014.10 Similar to the previous findings, the study group once again had a significantly higher prevalence of cervical smear abnormalities (13.7% vs 6.3%; P<0.001), including ACUS (10.8% vs 4.0%; P<0.001) and HSIL (1.1% vs 0.4%; P=0.005) although the prevalence of LSIL was not significantly different (1.8% vs 1.9%; P=0.833) [Table 4].

We attempted to contact those women with an abnormal cervical smear to ensure compliance with subsequent gynaecological assessment and treatment after the events and were successful in 58 (36%) instances. Among the 47 women with ACUS, 30 (64%) attended for subsequent assessment, three underwent colposcopy and one had loop excision. Of the six women with LSIL, five attended subsequent assessment of whom four underwent colposcopy and none required loop excision. All five women with HSIL attended subsequent colposcopic assessment and four had loop excision.

Cervical cancer is an important health issue for women in Hong Kong. It is the eighth most common cancer in the local female population.11 Over the past three decades, the ASR of cervical cancer has declined from 25 per 100 000 in 1983 to 8.7 per 100 000 in 2013.11 The figure remains higher than that of other high-income countries such as Finland (ASR=4.3 per 100 000).1 After the organised cervical screening programme was launched, the ever-screened rate increased from 37% in 2003 to 64% 2008,12 and remained approximately 70% until 2014.5 As this programme does not proactively recruit eligible women, 30% remain never-screened.5 Studies show that these women tend to be immigrants or have a lower socio-economic status with lower family income.6 7 8 9 13 In Hong Kong, 20% of women belonged to these groups. In 2012, there were 1.02 million people living below the poverty line in Hong Kong; 250 000 were adult women and comprised 7.3% of our female population.14 15 In 2011, there were 171 322 mainlanders who had been resident in Hong Kong for less than 7 years; 80 237 were women aged 25 to 54 years, comprising 2.3% of our female population.15 16 Immigrants from other ethnic groups constituted 10.2% of our female population in 2011; 7% were South-East Asian domestic helpers from Philippines, Indonesia, and Thailand, and the remaining 3% were South Asians from India, Pakistan, and Nepal.15 Studies show that immigrants often develop cervical cancer at rates more akin to their country of origin.13 Since these countries have a high prevalence of cervical cancer with ASR ranging from 16 to 22 per 100 000,1 it is not surprising that our study group had a significantly higher prevalence of cervical smear abnormalities than the comparison group (13.7% vs 1.4%). This also explains the 6- to 11-fold higher risk of cervical smear abnormalities in South Asian, South-East Asian, and new immigrants from Mainland China. More importantly, almost half (42.6%) of these women had never had a cervical smear. This was particularly true for ethnic minority women (61.2%) and new immigrants from Mainland China (45.4%). This shows that there are inequalities in our community in the access to cervical screening, similar to most metropolitan cities worldwide.17 18 The resultant under-screening of high-risk women and over-screening of low-risk women are clearly demonstrated by the significant difference in prevalence of cervical smear abnormalities between our study group and comparison group. To ensure that cervical screening services reach these marginalised women, it is imperative to understand the barriers to screening.

Cost is a common barrier for low-income women and immigrants with economic hardship.6 7 8 13 Of the female mainlanders who had been resident in Hong Kong for less than 7 years, 7.6% were in receipt of social assistance.16 Foreign domestic helpers earn only HK$4210 a month. The charge for a cervical smear provided by the public health sector is HK$100 and may be unaffordable by some women. Even if the screening service is free, other costs related to attending screening, such as transportation and taking time-off work, are deterrents.13 These barriers can be surmounted by community outreach that refers to the efforts made beyond the walls of the health care facility to reach target populations.19 The first step of outreach is to identify the target populations and this can be facilitated by collaboration with NGOs.13 19 Provision of a free service in mobile screening units outside working hours is also effective.19 Studies also show that the availability of female service providers helps reduce embarrassment about cervical cancer screening, and thus reluctance to attend, among Chinese and other ethnic groups.6 7 8 13 19 Utilising these strategies, we organised free screening events during weekends by women doctors, and we have successfully attracted almost 1200 marginalised women to participate.

Another important barrier to screening is ignorance about cervical cancer prevention and lack of awareness of screening service access,6 7 8 9 13 19 consequent to low health literacy.13 20 Health literacy refers to how easy it is for an individual to obtain, process, and understand health information and services to make appropriate health decisions.13 Low health literacy means that a person is unable to understand the health information available, access health services effectively, and make informed health decisions.20 In other words, health literacy is dependent not only on the education level and literacy of the individual, but also on how well health information is delivered and how accessible the health service is to the individual. Efforts to improve health literacy will help reduce health inequalities.20 For women with a low education level or low literacy, rewriting pamphlets in simple language or employing non-written forms of communication such as radio and television programmes are recommended.13 19 In Hong Kong, television programmes designed to promote cervical cancer screening are available, but they are broadcast in the local Cantonese dialect.21 As 68.3% of ethnic minority adults do not understand Chinese language and 36% of the new female immigrants from Mainland China do not speak Cantonese,22 23 they will not benefit from these programmes. It is worthwhile to translate these educational materials into different languages. In our recent free cervical cancer screening events, health talks on cervical cancer prevention were given with simultaneous translation into languages spoken by the participants, aiming to empower them to become peer health educators in their families and circle of friends, so that the health literacy in their community could be improved.

It is now known that cervical cancer is caused by human papillomavirus (HPV). Vaccination against HPV for 9- to 13-year-old girls combined with regular screening for precancerous lesions in women aged over 30 years followed by adequate treatment are now the key preventive approaches against cervical cancer.24 We have launched a free HPV vaccination programme for 9- to 18-year-old girls in this marginalised population. Since 2013, 176 girls from low-income families and 24 girls from ethnic minority groups have been vaccinated. It is hoped that our free cervical smear programme and free HPV vaccination programme will help reduce the incidence of cervical cancer in these marginalised women.

Our study was a retrospective analysis of data obtained from our free cervical cancer screening campaign. Limited by the nature of the campaign, important information such as occupation, education level, household income, and reasons for not attending screening was not obtained. Some data on the history of cervical smear were missed due to a language barrier. Moreover, self-reported smear history may not be reliable in this group of women with low health literacy.

The comparison group may not be ideal as it may represent an ultra-low-risk population, as reflected by the low prevalence of cervical smear abnormalities in these women who had regular cervical smears. Nonetheless, this is the only accessible data set from which to obtain the necessary raw data for analysis. Moreover, limited by the scarcity of data available on the smear reports from the Well Women Clinic, the only means to avoid including women with a similar background to those in the study group was by excluding reports bearing foreign names and those with the first alphabet of the identity card number being R, M, or W. When we compared the prevalence of cervical smear abnormalities in the study group with the CSIS data,10 which may be more representative of the general population, the findings remained similar and the prevalence of cervical smear abnormalities remained 2-fold higher (Table 4).

It would be more informative to have data about HPV DNA testing on all abnormal smears, but unfortunately the test was not covered by the charitable fund. The picture would also be more complete if the colposcopic or histological diagnosis of those women with abnormal cervical smears was available. Such information could not be obtained without the individual’s consent. We did attempt to contact these women to ensure compliance with subsequent gynaecological assessment and treatment after the event, but were successful in only 36% of cases as they came from a very mobile population. It is encouraging that most contactable women with LSIL or HSIL did attend subsequent assessment, and almost all with HSIL received treatment. It is hoped that by identifying and treating precancerous lesions, our campaign may help reduce the incidence of cervical cancer in these marginalised women.

The prevalence of cervical smear abnormality in marginalised women is at least double that of the general population and almost half had never had a cervical smear. South Asian, South-East Asian, and new immigrants from Mainland China had a 6- to 11-fold increased risk of cervical smear abnormalities compared with local Chinese population. The Government should play a proactive role in developing a more comprehensive cervical cancer screening programme in Hong Kong and ensuring adequate coverage for marginalised women by developing community outreach programmes through collaboration with community NGOs.

We thank the following organisations for collaboration in the ‘Ripple Action’ and ‘WE Stand’ projects (in alphabetical order): Association of Women Accountants (Hong Kong) Ltd, GoodNews Communication International, Hepatitis Free Generation, Hong Kong Ap Lei Chau Women’s Association, Hong Kong Employment Development Service, Hong Kong Federation of Women, Hong Kong Federation of Women Lawyers, Hong Kong Island Women’s Association, Hong Kong Nurses General Union, Hong Kong Outlying Islands Women’s Association, Hong Kong Playground Association, Hong Kong Sheng Kung Hui Lady MacLehose Centre, Hong Kong Sheng Kung Hui Welfare Council Limited, Hong Kong Women Doctors Association, International Social Service Hong Kong Branch, Kowloon Women’s Organisations Federation, Narcotics Division of Security Bureau, Po Tat Women’s Association, RainLily Association Concerning Sexual Violence Against Women, Social Welfare Department, The Neighbourhood Advice-Action Council, Village Volunteers of Hong Kong Sanatorium and Hospital, Yang Memorial Methodist Social Service Family Education and Support Centre, and Yuen Long Town Hall Support Service Centre for Ethnic Minorities.

We thank Dr Ellen Li Charitable Foundation for funding all the cervical smears in the ‘Ripple Action’ and ‘WE Stand’ projects. We thank Zonta Club of Kowloon for sponsoring all the HPV vaccines. We thank Dr KL Mak for retrieving cervical smear data for the comparison group; Prof DS Sahota for statistical support; Prof TKH Chung, Prof SSC Ho, and Prof TC Li for editorial assistance; and Prof HYS Ngan, the advisor of the ‘Ripple Action’ and ‘WE Stand’ free cervical screening projects.

All the cervical smears taken in the “Ripple Action” and “WE Stand” projects were funded by Dr Ellen Li Charitable Foundation. All the HPV vaccines were sponsored by Zonta Club of Kowloon. All authors have disclosed no conflicts of interest.

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