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Inequalities in cancer screening, prevention and service engagement between UK ethnic minority groups

26 May 2022
16 min read
Volume 31 · Issue 10

Abstract

More people in the UK are living with cancer than ever before. With an increasingly ethnically diverse population, greater emphasis must be placed on understanding factors influencing cancer outcomes. This review seeks to explore UK-specific variations in engagement with cancer services in minority ethnic groups and describe successful interventions. The authors wish to highlight that, despite improvement to engagement and education strategies, inequalities still persist and work to improve cancer outcomes across our communities still needs to be prioritised. There are many reasons why cancer healthcare inequities exist for minority communities, reported on a spectrum ranging from cultural beliefs and awareness, through to racism. Strategies that successfully enhanced engagement included language support; culturally-sensitive reminders; community-based health workers and targeted outreach. Focusing on the diverse city of Leicester the authors describe how healthcare providers, researchers and community champions have worked collectively, delivering targeted community-based strategies to improve awareness and access to cancer services.

In the UK, the number of newly diagnosed cancers more than doubled between 1971 and 2017 from 143 602 to 306 000 (Office for National Statistics (ONS), 2011). With an increasingly ethnically diverse population, it is essential to consider factors that may interact with, and affect access to, screening and health services in the diagnosis and management of cancers across minority populations. These may reflect familial predispositions and socioeconomic and cultural variations (Bhopal et al, 2012; Özdemir and Dotto, 2017). Although cancer survival is improving, the EUROCAR-4 study demonstrated that UK cancer survival is lower than other European countries with comparable healthcare systems (Møller et al, 2009). Since 2012, UK breast cancer screening coverage has remained static and cervical cancer screening coverage has declined, both being well below the 80% coverage standard (Richards, 2019). It is also evident that there is scope for improvement in enhancing public awareness of cancer symptoms, particularly among lower socioeconomic and minority ethnic groups (Robb et al, 2009). Cancer is, and will remain, a public health priority, and it is vital that we understand the complexity and intersection of the cancer pathway within our communities, ensuring that equitable and targeted community-based interventions can be offered. This article will explore factors that affect screening uptake and routes to diagnosis in minority ethnic communities within the UK, and interventions to address these disparities, with a focus on Leicester as an example of a well-studied and diverse population.

Patterns of cancer incidence in UK minority ethnic communities

The 2011 Census showed that 13% of the total population were classified as ‘non-white’ ethnic groups, the largest groups being Indian, Pakistani, black African, black Caribbean, Bangladeshi and Chinese (ONS, 2011b). The UK has a centralised cancer registration system that can be linked to Hospital Episode Statistics (HES) self-assigned ethnicity data, enabling the study of variations in cancer incidence rates between ethnicities. The landmark Cancer Incidence and Survival by Major Ethnic Group, England, 2002-2006 report by the National Cancer Intelligence Network (NCIN) (2009), found that, generally, black and minority ethnic groups were at a lower overall risk of cancer than white groups for all malignancies combined. However, there are a number of specific cancers that have higher incidence rates in people of black or Asian ethnicity compared with white, such as prostate cancer (black), thyroid cancer, myeloma, and Hodgkin's lymphoma (black and Asian). (Delon et al, 2022). It is also important to recognise that black and Asian populations are not homogenous, and that incidence patterns vary widely within ethnic subsets and across generations (Table 1).


Table 1. Variations in cancer incidence between UK black and minority ethnic groups
Site of cancer Patterns identified References
Gastrointestinal and hepatobiliary
  • 2 times higher incidence of oesophageal cancer in Bangladeshi women compared with white women
  • Black Caribbean men and women had higher incidences of gastric cancer compared with white counterparts
  • 6 times increased risk of oesophageal cancer in Bangladeshi women compared with Pakistani women
  • 4 times higher incidence rate of liver cancer in Chinese compared with whites
  • 2 times higher incidence rate of liver cancer in Bangladeshis compared with Indians
  • 3 times higher incidence rate of liver cancer in black Africans compared with black Caribbeans
  • Gallbladder cancer higher in all ethnic minority groups. Risk of gallbladder cancer 2 times higher in Bangladeshis compared with Indians, and higher incidence in black African group compared with black Caribbeans
Coupland et al, 2012; Ali et al, 2013
Genitourinary
  • Prostate cancer incidence significantly increased in black Caribbean and black Africans compared with whites
  • Prostate cancer incidence increased in Indian, Pakistani and mixed white and black Caribbean/African groups
Jack et al, 2007; Maruthappu et al, 2015
Head and neck and neurological
  • Bangladeshi females had higher incidence of oral, laryngeal and thyroid cancers compared with whites
  • Chinese males and females had higher incidence of nasopharyngeal cancers compared with whites
  • Blacks have higher incidence of meningioma and pituitary tumours compared with whites
  • Chinese have higher risk of thyroid cancer compared with whites
  • Thyroid cancer rates were significantly higher in Pakistani and Bangladeshi groups compared with whites, but not in Indians
Finlayson et al, 2014; Maile et al, 2016; Tataru et al, 2017
Lung
  • Bangladeshi men had highest incidence rates of lung cancer compared with all ethnic groups, which was not significantly different from white male incidence rates
Jack et al, 2011
Gynaecological and breast
  • All 6 non-white ethnic groups had lower rates of breast cancer compared with whites. Within the South Asian group, Bangladeshi women had lower rates than Indians and Pakistanis
  • For ovarian cancer, the South Asian and black groups had rates 60−65% that of white groups
  • Indian and Bangladeshi groups had lower rates compared with Pakistani groups. Black African incidence rates were higher than black Caribbean rates
  • There was no significant difference in ovarian cancer rates between Chinese and white groups
  • Cervical cancer rates in the South Asian group were 33% that of white groups, and black and Chinese groups had rates 70% of white groups
  • In endometrial cancer, there was little difference between the rates in South Asian and white groups. Within the South Asian group, Bangladeshis experienced rates 50% of that of Indian and Pakistani groups
  • Rates of endometrial cancer in black groups slightly higher than that of whites
  • Leicester has the highest rate of endometrial cancer in the UK. Asian women are more likely to be diagnosed at a younger age, with distinct genetic differences between tumours from South Asian and white women
Shirley et al, 2014; Polymeros et al, 2020
Haematological
  • For Hodgkin's lymphoma, the incidence rate was higher in the Pakistani group compared with whites. There were increased rates in South Asian males
  • Rates of mature B cell neoplasms were 20% higher in black groups compared with whites
  • The rate of diffuse large B cell lymphoma was 3 times higher in black African compared with black Caribbean groups
  • For plasma cell neoplasms (including myeloma), black subgroups had rates 2.5 times that of white groups
  • In mature T cell neoplasms, black groups had rates 3 times higher than white groups, with black Caribbeans having higher rates than black Africans
  • In subgroup analysis, rates of adult T-cell leukaemia/lymphoma were 40 times greater in black Caribbeans compared with whites
Shirley et al, 2013

In 2011, Leicester was recognised as the most ethnically diverse city in the UK, with 49% of the population being from a non-white background (ONS/NOMIS, 2011). These broad ethnic categorisations give a high level overview, but when framing health messages appropriate targeting is essential, taking into account both linguistic and cultural influences. Leicester's diverse population has historically been used to study relationships between ethnicity and cancer incidence. Studies investigating cancer incidence trends between 1990 and 2005 revealed Leicester's South Asians to have significantly lower rates of colorectal, lung, breast, prostate, kidney, stomach, bladder and oesophageal cancers, but a higher rate of head and neck and liver cancers (Smith et al, 2003; Ali et al, 2010). For colorectal cancer, however, there appeared to be an increasing incidence rate in younger age groups compared with their white counterparts (Smith et al, 2003; Norwood et al, 2009). It has also been shown that lung (Day et al, 2010) and breast (Stotter et al, 2014) cancer incidence rates in Leicester's British Indians have increased over time, bringing into question whether British South Asians should still be considered at low risk for these cancers.

A major determinant in improving outcomes is the prevention and early detection of cancer through the three UK national screening programme for breast, cervical and bowel cancers.

Screening barriers in ethnic communities

As UK NHS breast, cervical and bowel screening programmes have evolved from inception to routine service, barriers to engagement have been explored and reveal a dynamic change in response to changing cancer education and screening awareness, and the ethnographic, socioeconomic and geographical fluidity of the populations that they serve. Consequently, the type of interventions required to overcome these barriers must reflect this changing environment to help mitigate cancer health inequalities.

Engagement with screening services is a critical component of cancer prevention and early detection strategies. Numerous studies have revealed that individuals from deprived areas or non-white backgrounds are less likely to engage with UK national cancer screening programmes, with consequent poorer health outcomes (Moss et al, 2012). There are potentially many reasons for this discrepancy, including: cancer knowledge and awareness, cultural determinants, cancer fear, perception of stigma, sociodemographics, age, the type of screening programme, general practice structure and ease of access, and the way in which screening information is presented (Webb et al, 2004; Moser et al, 2009; Robb et al, 2010; Ghanouni et al, 2017; Vrinten et al, 2019). To improve screening engagement, determinants of screening attendances in the context of each screening programme must be understood.

Breast screening

Breast screening uptake has been investigated in a number of communities across the UK. London-based studies have revealed large variation in screening uptake between different ethnic groups, even following adjustments for age, socioeconomic deprivation, and screening area, with black (Renshaw et al, 2010) and Bangladeshi (Jack et al, 2014) women at highest risk for screening non-attendance. Screening attendance in Scotland also revealed comparable trends following similar adjustments with higher non-attendance rates for Pakistani, other Asian and Indian women (Bansal et al, 2012). This pattern is repeated across geographic areas in the UK, with South Asian women significantly less likely to attend breast cancer screening. A study from Warwickshire also suggested that within this population, continued engagement with screening was lower in South Asian Muslim women (Szczepura et al, 2008; Price et al, 2010). This provides further evidence that although broad demographic definitions may be a useful way of identifying areas of priority, inequalities in screening attendance need to be addressed at a community level that recognise the needs of the local population.

Cervical screening

In England, the key factors associated with poorer cervical screening attendance have been identified as non-Caucasian ethnicity and deprivation (Webb et al, 2004; Bang et al, 2012; Massat et al, 2015). Poor knowledge of cervical cancer and associated risk factors are prevalent, which in turn impacts significantly on the perceived relevance of screening and consequent screening uptake. Poor screening attendance has been observed in women with sub-Saharan African (Ogbonna, 2017), Indian, Pakistani, Bangladeshi, Caribbean (Marlow et al, 2015a; 2015b) and Chinese (Conway et al, 2014) backgrounds.

Numerous studies have shown that specific cultural beliefs may play a role in decision making following a screening invitation (Marlow et al, 2019), compounded by a lack of recognition of specific screening terminology, low perceived risk due to sexual inactivity and the perception that a test is not required if asymptomatic (Marlow et al, 2015a; 2015b). Additionally, a study assessing attitudes of black women in London identified that African ethnicity, being younger, and being single, were associated with being overdue for screening (Ekechi et al, 2014). Screening uptake for cervical cancer is also affected by the age of the screen invitee. Screening non-attendance in women from ethnic minority groups specifically aged between 50 and 64 is often driven by a lack of screening awareness or a conscious decision not to attend (Marlow et al, 2017a; 2019). For London-based Somali women, further determinants of non-screening attendance were fatalistic attitudes expressed as ‘God's will’, and embarrassment associated with the presence of female genital mutilation (Abdullahi et al, 2009).

Bowel screening

The UK colorectal cancer screening pilot was undertaken in 1999, with a sub-study looking at potential barriers for ethnic populations commissioned in 2001, focusing on the large South Asian population at the pilot site (Szczepura et al, 2004). Overall uptake for faecal occult blood testing (FOBt) was relatively high, but was approximately half that of the white population in South Asians. Within the South Asian population, further disparities were observed, with lower uptake in Muslims compared with Hindus.

Lack of bowel screening awareness has been shown to be a barrier across all communities (Dharni et al, 2017). A study by Kobayashi (2016), revealed that in ‘never-screeners’, up to two-thirds of people had never read any of the screening literature, with this significantly more common in non-white participants. In South Asian groups, lack of engagement with literature was not just because of its presentation in English, but was similar for any written language, suggesting that verbal communications within faith communities may be a better way of delivering information (Palmer et al, 2015). For bowel screening, one of the main barriers to uptake in ethnic communities is centred around knowledge of screening and cancer (Robb et al, 2008a; Lo et al, 2015), with non-symptomatic South Asian groups having a more negative attitude towards bowel screening than those with African and Caribbean backgrounds (Taskila et al, 2009). Screening-related embarrassment and anxiety (Robb et al, 2008b), cancer fear, and culturally influenced health beliefs are also factors identified with poor bowel screening uptake (Austin et al, 2009).

Non-screening programme cancer risk awareness

A lower awareness of cancer and cancer risk in UK ethnic populations also extends to other types of cancer that are not part of screening programmes. In the UK, African/Caribbean men have approximately three times higher prostate cancer incidence than that observed in men of European origin (Chinegwundoh et al, 2006). A study by Rajbabu et al (2007) showed that black men were unaware of their increased prostate cancer risk and had poor symptom knowledge, which could be improved by a simple educational intervention. In addition to lack of awareness, other barriers were present, such as the nature of, and embarrassment associated with, the digital rectal examination (DRE) (Seymour-Smith et al, 2016). Similarly, awareness and practice of self-examination for testicular cancer was also found to be lower in men of non-white ethnicity than for white men (Khadra and Oakeshott, 2002).

In Leicester, South Asian women's symptom knowledge for endometrial cancer (such as unscheduled vaginal bleeding) was better than for white women, but knowledge of risk factors was poorer. There was also an assumption that a negative cervical smear also meant they did not have endometrial cancer (Kumarakulasingam et al, 2018).

GP attendance

Presentation to primary care with cancer symptoms is often predated by a delay in the patient seeking help following the onset and development of initial symptoms (Scott et al, 2013). Early GP attendance is key, as increased use of the 2-week wait referral system through primary care is known to be associated with better cancer survival (Møller et al, 2015).

UK studies have shown that black and minority groups are more likely to delay presenting with symptoms, which consequently translates into diagnosis at a more advanced stage for some cancers (Jack et al, 2009; Macleod et al, 2009; Sadler et al, 2009). A survey of black and minority populations in England revealed lower rates of reporting for most cancer symptoms to their primary care team, with lower symptom recall and awareness in the African group (Robb et al, 2009; Waller et al, 2009). Barriers to health-seeking behaviours identified within these populations have included worry about what will be found, difficulty in accessing appointments and competing priorities (Waller et al, 2009). All of these behaviours have been further directly affected by the impact of the COVID-19 pandemic. For patients with breast cancer symptoms, South Asian women report more emotional barriers such as embarrassment than white women (Forbes et al, 2011). Barriers to health-seeking behaviours in primary care for cancer symptoms was assessed in a diverse London population of women. In women from black and minority backgrounds, factors reported included: use of alternative strategies such as prayer and alternative medicines to manage symptoms, avoidance of discussion around difficult symptoms, a language barrier, racism, and prioritising the needs of the family over their own health (Marlow et al, 2014). Similar findings have also been reported in a study including West African men (Ehiwe et al, 2012). Fear of cancer, including outcomes of death and recurrence, have also been identified (Marlow et al, 2014), with generational differences in attitudes to cancer described.

Elkan et al (2007) reported experiences of minority ethnic groups using cancer services provided by the NHS. Although some individuals experienced overt racism during their care, the authors drew particular attention to the fact that service provision may not exhibit racism through intent, but that this is the ultimate result precipitated by an institutionally inadequate response to linguistic, cultural or religious needs compounded by a lack of cultural competency. More recently, the National Cancer Patients Experience Survey in England revealed lower satisfaction in patients from ethnic minorities due to poorer understanding of, and less confidence in, healthcare professionals (Pinder et al, 2016), with non-white patients receiving less understandable explanations of treatment side effects compared with white patients (Trenchard et al, 2016).

Emergency presentations

Approximately 23% of cancers are diagnosed through the emergency route in England (NCIN, 2010; Bottle et al, 2012; Elliss-Brookes et al, 2012). Emergency presentation to hospital with a new diagnosis of cancer is often associated with advanced disease and physical frailty (Brewster et al, 2011, Shawihdi et al, 2011). Studies across multiple tumour sites have shown that emergency presentation is associated with poorer cancer outcome (Raine et al, 2010; Elliss-Brookes et al, 2012; Kane et al, 2017), with high excess 1-year cancer deaths in England compared with the European average, possibly reflecting later diagnosis (Thomson et al, 2009). Diagnosis at the point of emergency presentation may result from factors such as a delay in patients' presenting, delays at the level of primary or secondary care or, indeed, at any point in the diagnostic pathway (Swann et al, 2018). It is therefore important to understand how patient characteristics might influence late presentation and how we can help to identify patients at high risk.

Multiple studies have shown that age, sex and ethnicity may be associated with risk of a patient's first time admission for cancer being unplanned (Elliss-Brookes et al, 2012). Wide variation according to cancer type, deprivation score and place of residence have also been described (Bottle et al, 2012). In colorectal cancer, increased age, female sex, a non-white background, a more deprived socioeconomic background, and the presence of comorbidities have been associated with a higher rate of emergency presentation (Wallace et al, 2014). In contrast, one UK study reported that patients of white ethnicity were at greatest risk of diagnosis by emergency admission (Tsang et al, 2013).

UK studies focusing on exploring further data around emergency admissions across our ethnically diverse population, as well as other components of the cancer pathway such as screening, referral, cancer staging and treatment data, are required to understand how we can improve access to cancer care and improve the patient pathway.

Interventions to improve screening uptake and early presentation

This article has provided an overview of cancer healthcare inequalities and potential barriers for patients of non-white ethnicity in the UK. It is known that certain ethnic groups may be at increased risk of specific cancer types, that incidence of some cancers are increasing within specific ethnic populations, and that there are large gaps in providing equality of cancer education and service access. Much of this information has been available for many years, and it is essential to understand how the UK cancer healthcare community has responded to the challenge of improving equity of access for the UK's diverse populations. Studies that have been undertaken to improve awareness, understanding and access, and the impact on their targeted community, are described in Table 2.


Table 2. UK-specific interventions for improved screening uptake, cancer education and awareness
Cancer or screening population Intervention Target population Intervention success? Reference
Breast screening 2 hour training programme for GP reception staff to encourage screening in screening non-attendees London Borough of Newham: white, Indian, Pakistani, black, Bangladeshi, Chinese, other Yes. Significant improvement across all ethnicities, with largest attendance improvement in Indian women Atri et al, 1997
Breast screening Identification of ethnic language groups; GP endorsement letter; translation of literature; transport to screening centre; language support Cardiff GP practices serving Somali and South Asian populations Yes. Increase from 35.2% attendance to 50.7% attendance. Uptake was highest for Urdu and Gujarati speakers and lowest for Bengali and Somali speakers Bell et al, 1999
Breast screening Targeted outreach work through respected community organisations (phone calls, rebooking appointments, providing transport) Bangladeshi and white women in Tower Hamlets Primary Care Trust Yes: 44.5% attendance in 2005, 63.4% in 2009 Eilbert et al, 2009
Breast Screening Language and culture-sensitive telephone reminder calls Black and South Asian women Yes. Increase in uptake higher in South Asian women than black women Offman et al, 2014
Breast screening Randomised controlled trial of text message reminders at first breast screen London Borough of Hillingdon (47.8% of borough of non-white ethnicity) Significantly increased screening uptake with text message intervention Kerrison et al, 2015
Breast, cervical and bowel screening programmes Delivery of cancer prevention advice at screening appointments Census data used to select nationally representative sample Yes. Non-white ethnicity associated with increased willingness to receive lifestyle advice Stevens et al, 2019
Bowel screening Face-to-face health promotion; telephone health promotion Patients from culturally diverse London GP practices Telephone intervention significantly increased uptake in males and females; face-to-face significantly increased uptake in males only Shankleman et al, 2014
Cervical screening Face-to-face interview with multilingual interviewer asking preference to screening approach Indian, Pakistani, Bangladeshi, Caribbean, African and white British A strong recommendation for screening is preferred by ethnic minority women Marlow et al, 2017b
All cancers Determining the information needs of Asian and white British cancer patients and their families in Leicestershire Asian patients attending the oncology department at the Leicester Royal Infirmary Significantly more Asian patients would prefer information from their GP compared with their white counterparts, and would prefer to discuss information in their mother tongue Muthu Kumar et al, 2004
Prostate cancer (non-screening programme) Increasing prostate cancer awareness by provision of prostate health education GP surgeries, county/city councils, and community sources, with support from a Black Workers' Support Group and Black Managers' Forum to increase participation amongst ethnic minorities Men in the health education intervention group were more able to identify more symptoms of prostate cancer and identify risk factors Rajbabu et al, 2007
Interventions for cancer prevention Cancer Research UK Cancer Awareness Roadshow with trained cancer awareness nurse answering questions and giving tailored advice All community members in roadshows across the Midlands, north-west and north-east of England Black responders were significantly more likely to change health behaviours compared with all other ethnicities Smith et al, 2014
Enhancing cancer awareness Training workshops for community-based health workers to talk confidently about cancer signs and symptoms and risk factors Community-based health workers in areas with diverse populations (Sandwell, Birmingham and Solihull) Significant improvement in confidence for discussing signs and symptoms of cancer (increase from 32% to 96%) Grimmett et al, 2014
Endometrial cancer follow-up Patients offered patient-initiated follow-up (PIFU) following an early-stage endometrial cancer diagnosis. Involved open access to a clinical nurse specialist, instead of scheduled hospital appointments Leicester endometrial cancer patients South Asian women felt particularly reassured that they were able to speak to a Hindi/Gujarati-speaking clinical nurse specialist Kumarakulasingam et al, 2018

In Leicester, a number of the approaches shown in Table 2 have been taken forward, in order to improve equity of access and education across the community. Leicester City Clinical Commissioning Group (CCG) has engaged with community faith leaders to promote the importance of screening; introduced breast checking and breast screening videos for social media in Gujarati; made videos available in a variety of languages (Bengali, Gujarati, Hindi, Polish, Punjabi and Urdu) explaining how to take faecal immunochemical test (FIT) samples; made the Leicester Good Health Guide available in Gujarati, Hindi, Polish and Urdu; used community venues in areas with diverse populations and high footfall to hold cancer-related events and distribute information; and collaborated with an Asian language radio station for multilingual cancer health messaging.

Just before the onset of COVID-19, Leicester City CCG launched the Cancer Champions initiative to recruit individuals from across different communities to train and learn more about cancer, allowing them to take that information back into their respective communities. This was focused on supporting work helping to educate communities on prevention, screening, and living with and beyond a cancer diagnosis. Further work with the Centre for Ethnic Health Research (CEHR), at the University of Leicester, has also proved vital to improve engagement with local minority communities through events such as ‘Play Domino, Talk Prostate’ (CEHR, 2018) aimed specifically at the African-Caribbean community, and the Big Health Connect, led by local community champions supported by the CEHR with information provided by local health and community services. The importance of engaging ethnic minority communities with the concept of cancer research has also been brought into these community events by the Hope Clinical Trials Centre, with engagement ideas led by the Patient and Carer's Advisory Group, offering information in lay language and translation into Gujarati.

Conclusions

Despite cancer inequalities in minority ethnic communities being well described over many years within the UK, many of these inequalities still persist. It should be a priority of the cancer health and research communities to continue to source innovative ways in which they can ensure equity of access to information, education and cancer services. In order to design these strategies, it is imperative that they involve the communities which they serve, to produce services and interventions that are truly impactful. An exemplar of the way in which researchers can meaningfully interact with diverse minority communities was published by the CEHR with a focus on diabetes research (Prinjha et al, 2020). Having teams of relevant healthcare providers, including nurses, researchers and community experts working collectively, will ensure convergence of appropriate skillsets, linguistic, and cultural competencies, ensuring that cancer health messages are framed and delivered in a culturally appropriate manner for maximum impact.

KEY POINTS

  • Improving equity of access for cancer services is key for improved outcomes
  • Although there is increasing research into drivers of cancer inequalities in minority ethnic groups, this is the first article to summarise UK-only studies to enhance relevance for a UK readership
  • Strategies that have been shown to be successful for improved service engagement include language support, culturally-sensitive reminders, community based health workers, and targeted outreach
  • Working in partnership with our local communities needs to be central to future engagement strategies

CPD reflective questions

  • What strategies does your local cancer centre/clinical commissioning group have in place to reach out to differing communities?
  • There are often pockets of innovative engagement strategies across multiple institutions. Do you try to link them together and share ideas and best practice?
  • Do you support community champions to take cancer messaging back into the community?