Journal of Public Health Vol. 38, No. 2, pp. 330 334 doi:10.1093/pubmed/fdv038 Advance Access Publication March 31, 2015 The varying influence of socioeconomic deprivation on breast cancer screening uptake in Ruth H. Jack 1,2, Tony Robson 3, Elizabeth A. Davies 1,2 1 Knowledge and Intelligence Team, Public Health England, SE1 6LH, UK 2 Cancer Epidemiology and Population Health, King s College, SE1 9RT, UK 3 Quality Assurance Reference Centre, EC1A 7BE, UK Address correspondence to Ruth H. Jack, E-mail: ruth.jack@phe.gov.uk ABSTRACT Background We assessed the relationship between screening uptake and socioeconomic deprivation for women aged 50 52 invited to their first routine screening appointment between 2006 and 2009. Methods We examined uptake for overall and within six screening areas, using deprivation quintile, based on post code of residence. Results After adjustment for age, area and ethnicity, overall uptake decreased with increasing deprivation (adjusted odds ratio (OR) ¼ 0.95, P, 0.001). However, in two screening areas with lower uptake, women living in deprived areas had higher uptake than women from affluent areas. Conclusions These potential inequalities in early diagnosis across require further investigation. Keywords breast cancer, screening, socioeconomic deprivation Introduction In England, breast cancer screening uptake is a measure of the proportion of women attending for a National Health Service (NHS) screening appointment after being sent an invitation as part of the breast screening programme. Previous studies of different geographical areas within, southern and northern England have found lower uptake in areas of higher socioeconomic deprivation, 1 3 while a national survey found measures of individual wealth including car and home ownership were associated with ever having attended for a mammography. 4 is the largest and most diverse English city, and uptake of breast cancer screening by its population has remained lower than other regions. In 2011 12, the uptake of first invitation to the screening programme for women aged 50 70 years was 63% compared with an overall average of 73% for England. 5 Screening services in are organized into six geographical areas. The population of each differs in terms of deprivation, affluence and ethnic make-up, and local services have developed many specific initiatives to increase uptake in particular groups. Women living in the more deprived areas of are the largest group invited to breast cancer screening, and although they have a worse 5-year survival for breast cancer, the difference in survival between deprived and affluent women is less for screen-detected disease. 6 It is therefore important to ensure that there are no barriers to women attending breast cancer screening invitations. This study aimed to provide new information by examining the association between deprivation and uptake for women invited to their first call (a first invite to the routine national screening programme) appointment in, overall and for separate screening areas. Methods Data on women aged 50 52 who had a first call invitation between 31 March 2006 and 31 December 2009 were obtained by the former Thames Cancer Registry from the Quality Assurance Reference Centre (QARC). The QARC monitors the performance of the six geographical screening areas: (i) West of, (ii) North, (iii) Central and East, (iv) Barking, Havering Redbridge Ruth H. Jack, Epidemiologist/Research Associate Tony Robson, Information and Business Manager (QACo-ordinator) Elizabeth A. Davies, Reader in Cancer and Public Health 330 # Crown copyright 2015.
INFLUENCE OF SOCIOECONOMIC DEPRIVATION ON BREAST CANCER SCREENING 331 North Central and East West of Barking, Havering, Redbridge and Brentwood South West South East Deprivation group 1 Least deprived 2 3 4 5 Most deprived Fig. 1 Screening areas in and deprivation quintile, taken from the income domain of the Indices of Deprivation, 2007. Table 1 Number and percentage of women sent a breast cancer screening invitation in between 31 March 2006 and 31 December 2009, by deprivation quintile and screening area 1 (least deprived) 2 3 4 5 (most deprived) Total n (%) n (%) n (%) n (%) n (%) n (%) North 4216 (12) 4189 (12) 6670 (20) 9622 (28) 9226 (27) 33 923 (100) West of 3366 (12) 3227 (12) 6006 (22) 8000 (29) 6905 (25) 27 504 (100) Barking, Havering, Redbridge and Brentwood 2589 (16) 2864 (18) 3092 (19) 3900 (24) 3801 (23) 16 246 (100) Central and East 510 (2) 716 (3) 1578 (6) 5381 (21) 17 385 (68) 25 570 (100) South East 3468 (13) 3020 (11) 3817 (14) 7599 (28) 9148 (34) 27 052 (100) South West 6583 (23) 6250 (22) 5982 (21) 6159 (21) 3809 (13) 28 783 (100) Total 20 732 (13) 20 266 (13) 27 145 (17) 40 661 (26) 50 274 (32) 159 078 (100) and Brentwood, (v) South East and (vi) South West. The different patterns of deprivation and affluence of the population within each area, taken from the income domain of the Indices of Deprivation, 7 are shown in Fig. 1. Based on postcode of residence, each woman invited to the programme was assigned to a socioeconomic deprivation quintile calculated across the whole of England using this measure. Self-assigned ethnicity was recorded by the screening programme when a woman attended for screening using the 16 ethnic groups from the England and Wales 2001 Census. These were White British, White Irish, White Other, Mixed White and Black Caribbean, Mixed White and Black African, Mixed White and Asian, Mixed Other, Indian, Pakistani, Bangladeshi, Asian Other, Black Caribbean, Black African, Black Other, Chinese and Any Other. However, if a woman never attended a screening appointment, or chose not to describe her ethnic group when she attended, this information was missing. Where this was the case, multiple imputation was used to estimate her ethnicity from the 16 groups above. Variables included in the imputation were age at invitation, screening area, ward of residence, socioeconomic deprivation and whether the woman attended the screening appointment being analysed. Some ethnicity information was available for women who did not attend the first call invitation included here as they were screened on a later occasion. Logistic regression was used to assess screening uptake in the socioeconomic deprivation quintiles, both unadjusted and adjusted for age at invitation, screening area and ethnicity. The analysis was repeated for the six different screening areas, adjusted for age and ethnicity. Results for each socioeconomic group were back transformed to calculate adjusted proportions. A linear trend was calculated to assess the association firstly for all of, and then within the different
332 JOURNAL OF PUBLIC HEALTH screening areas, to investigate whether the same trend was evident. During the study period, regional cancer registries had support to collect and analyse cancer data under Section 251 of the NHS 2006 Act. The NHS Cancer Screening Programme had a confidentiality protocol covering the collection, processing and release of data. These approvals were reviewed annually by the National Information and Governance Board. This study used an anonymized dataset, and separate ethical approval was not required. (a) OR = 0.89 2 (b) 1 (Least deprived) 2 3 4 5 (Most deprived) OR = 0.95 2 1 (Least deprived) 2 3 4 5 (Most deprived) Fig. 2 Breast cancer screening uptake in by deprivation quintile, odds ratio (OR) and P-value for trend. (a) Unadjusted and (b) Adjusted for age at invitation, screening area and ethnicity.
INFLUENCE OF SOCIOECONOMIC DEPRIVATION ON BREAST CANCER SCREENING 333 OR = 0.94 OR = 1.03 P = 0.005 OR = 0.95 P = 0.001 OR = 1.03 P = 0.046 OR = 0.85 OR = 0.96 2 1 2 3 4 5 1 2 3 4 5 1 2 3 4 5 1 2 3 4 5 1 2 3 4 5 1 2 3 4 5 North West of 1= Least deprived, 5= Most deprived Barking, Havering, Redbridge and Brentwood Central and East South East South West Fig. 3 Breast cancer screening uptake by deprivation quintile in different screening areas of, odds ratio (OR) and P-value for trend, adjusted for age at invitation and ethnicity. 1, least deprived; 5, most deprived. Results Data on 159 078 women invited for their first call breast screening appointment were included. The number and percentage of these women by deprivation quintile are shown in Table 1. Women resident in the Central and East screening area were most likely to live in the most deprived quintile (68%), compared with 13 34% in the other screening areas. Ethnicity information was available for 95 284 () women. Overall, 96 452 (61%) women attended within 6 months of their invitation, but this percentage decreased from 66 and 67% in the two most affluent socioeconomic quintiles to 56% in the most deprived quintile (trend OR ¼ 0.89, P, 0.001). This association was attenuated after adjusting for age at invitation, screening area and ethnicity, but remained statistically significant (OR ¼ 0.95, P, 0.001) (Fig. 2). Overall attendance in the different screening areas ranged from 55% in Central and East and 56% in the West of areas, to 71% in Barking, Havering, Redbridge and Brentwood. When data for the different screening areas were analysed separately (Fig. 3), increasing deprivation was associated with lower screening uptake in South East (OR ¼ 0.85, P, 0.001), South West (OR ¼ 0.96, P, 0.001), North (OR ¼ 0.94, P, 0.001) and Barking, Havering, Redbridge and Brentwood (OR ¼ 0.95, P, 0.001). However, in the West of (OR ¼ 1.03, P ¼ 0.005) and Central and East (OR ¼ 1.03, P ¼ 0.046) screening areas, uptake increased with increasing deprivation. Only in Barking, Havering, Redbridge and Brentwood was screening uptake among the most deprived quintile above. Discussion This study found that while the screening uptake for overall replicates the established finding of lower rates in more deprived areas, this association does not apply in the same way within each of the six screening areas. The uptake of women from the most deprived group reaches the national target of only in one screening area, which also has the highest overall uptake in. Although there is little recent published research on interventions to increase attendance specifically in women from deprived areas, there may be lessons from the practice of services and the experience of women in this area. The unexpected association between increasing deprivation and uptake in two of the other screening areas could represent the success of initiatives reaching deprived women and/or lack of uptake by more affluent women. Although these two areas have the lowest overall uptake rates, one has reported developing tailored interventions to reach women from a diverse mix of ethnic groups. 8 Interventions included rebooking appointments, providing transport to appointments,
334 JOURNAL OF PUBLIC HEALTH sending talking invitations for women with low literacy and improving the efficiency and effectiveness of the screening service itself, by setting up a dedicated call centre and providing customer service training for all staff. The high turnover of population in generally, and in some boroughs particularly, 9 means that invitations could be sent to women who are no longer residents, and lowering the uptake rates. One limitation of this study is the lack of information on the uptake of private screening programmes that could mean more affluent women are not responding to their NHS invitations. This would lead to inequalities being under-reported and is suggested by similar rates of screen-detected disease in the two least deprived quintiles within NHS cancer registration data records. 6 Asecond limitation is that a large proportion of women () did not have a record of their self-defined ethnicity information available for analysis. While multiple imputation was used to estimate their ethnic group, it would be preferable if more complete and directly obtained data could be captured to improve future investigations of access to services. Analysing women whose first invitation in the same period was a routine recall (after a previous attendance for a routine screening programme mammography) showed similar results, with lower uptake in more affluent areas in the West of and Central and East screening areas (data not shown). This suggests that there are continuing inequalities in access to screening services that could impact on population cancer outcomes. Conclusion The overall uptake of breast screening is lower in women living in more deprived areas of, but this association does not apply in the same way to all screening areas. Further investigation and regular audit of local practice is needed to understand why women are not attending, both to inform service development and decrease inequalities in early diagnosis. Authors contribution R.H.J., T.R. and E.A.D. designed the study; T.R. acquired and advised on the data; R.H.J. analysed the data and wrote the first draft; E.A.D. revised and completed the manuscript. All authors interpreted the data, commented on the manuscript and had final approval of the version to be published. Acknowledgements We thank Steve Dixon, former Head of Quality Assurance for the Quality Assurance Centre, for his help in securing the data and funding for this study. Funding This study was funded by the Quality Assurance Centre and the former Thames Cancer Registry in King s College. The work was carried out by the Thames Cancer Registry which received funding from the Department of Health. The views expressed in the publication are those of the authors and not necessarily those of the Department of Health. The study was completed with the support of the Knowledge and Intelligence Team, Public Health England. References 1 Sutton S, Bickler G, Sancho-Aldridge J et al. Prospective study of predictors of attendance for breast screening in inner. J Epidemiol Commun Health 1994;48:65 73. 2 Banks E, Beral V, Cameron R et al. Comparison of various characteristics of women who do and do not attend for breast cancer screening. Breast Cancer Res 2002;4:R1. 3 Maheswaran R, Pearson T, Jordan H et al. Socioeconomic deprivation, travel distance, location of service, and uptake of breast cancer screening in North Derbyshire, UK. J Epidemiol Commun Health 2006;60:208 12. 4 Moser K, Patnick J, Beral V. Inequalities in reported use of breast and cervical screening in Great Britain: analysis of cross sectional survey data. BMJ 2009;338:b2025. 5 Health and Social Care Information Centre. Breast Screening Programme, England - 2011 12. 2013. http://www.hscic.gov.uk/ catalogue/pub10339 (13 December 2014, date last accessed). 6 Davies EA, Renshaw C, Dixon S et al. Socioeconomic and ethnic inequalities in screen-detected breast cancer in. J Public Health 2013;35:607 15. 7 Noble M, McLennan D, Wilkinson K et al. The English Indices of Deprivation 2007. : Department for Communities and Local Government, 2008. 8 Eilbert KW, Carroll K, Peach J et al. Approaches to improving breast screening uptake: evidence and experience from Tower Hamlets. Br J Cancer 2009;101:S64 7. 9 Hollis J. Focus on - Population and Migration. : Greater Authority, 2010.