QJM Advance Access originally published online on June 12, 2007
QJM 2007 100(7):423-431; doi:10.1093/qjmed/hcm041
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Ethnic differences in cancer incidence and mortality: the Birmingham Factory Screening Project
From the University Department of Medicine, City Hospital, Birmingham, UK
Address correspondence to Dr D.A. Lane, University Department of Medicine, City Hospital, Dudley Road, Birmingham B18 7QH. email: deirdre.lane{at}swbh.nhs.uk
Received 18 October 2006 and in revised form 30 January 2007
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Summary |
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Background: There is little information on ethnic differences in the incidence of cancer and cancer mortality among adults in the UK, particularly concerning Afro-Caribbean people.
Aim: To examine differences in the incidence of malignant cancer and cancer mortality rates among White European, Afro-Caribbean, and South-Asian people, and to examine baseline demographic predictors of cancer mortality.
Design: Longitudinal cohort study.
Methods: We compared ethnic differences in the incidence of malignant cancer and cancer mortality over a mean (SD) follow-up of 19.9 (4.8) years, in relation to baseline demographic characteristics and blood pressure variables, in the 2713 participants (2090 White European men and women, 428 Afro-Caribbean men and women, and 195 South Asian men) enrolled in the Birmingham Factory Screening Project whose survival status on 31 December 2003 was known.
Results: White European women had a significantly higher incidence of cancer compared to Afro-Caribbean women (p = 0.019). In addition, South Asian men had a significantly lower incidence of cancer compared to White European men (p < 0.0001) and Afro-Caribbean men (p = 0.048). The incidence of cancer was similar in White European and Afro-Caribbean men (p = 1.00). Overall incidence densities of cancer and death from cancer were 0.6% and 0.3% per 100 person-years of observation, respectively. Age, ethnicity, and smoking status were independent predictors of both cancer incidence and cancer mortality.
Discussion: The incidence of, and death from, cancer are both lower in minority ethnic groups in the UK, than in their White European counterparts.
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Introduction |
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Cancer is the second leading cause of death in the UK, accounting for 27% of all deaths in 2001.1 Over the last 50 years in England and Wales, there has been a significant decline in mortality from cardiovascular and infectious diseases, but very little change in age-standardized cancer mortality rates. Lung, breast (female), colorectal and prostate cancer, the four most common cancers, accounted for more than half of the 225 000 new cases of malignant cancer registered in England in 2001,2 and just under half of the 128 000 deaths from cancer in the same year.2 In the West Midlands, the standardized registration ratios for all cancers (excluding non-melanoma skin cancer) were 2% higher in men and 1% lower in women than the age-specific incidence rates for England as a whole.2
There is a relative paucity of data on ethnic differences in cancer incidence3–6 and mortality from cancer7–13 among adults in the UK, particularly among Afro-Caribbeans.7–9,14 The most recent analysis of cancer mortality for all cancers by country of birth (a proxy for ethnicity) in England and Wales from 2001 to 2003,13 found that cancer mortality was higher for men and women born in Ireland or Scotland, and men born in West Africa, but lower for men and women born in Bangladesh, India, Pakistan, and East Africa, and for women born in the West Indies. Cancer mortality was similar to the whole population for people born in the Middle East, North Africa, for men born in the West Indies and for women born in West Africa. Most research on ethnic differences in cancer has highlighted the increased incidence of the relatively uncommon cancers of the liver, gallbladder, and hypopharynx among ethnic minority groups.3,5,6,9 However, based on the actual numbers of incident cases, the most common cancers among White-Europeans were also the most common cancers among people from ethnic minority groups, albeit with a lower incidence.5,12,13
Research from the US has demonstrated ethnic differences in cancer incidence and survival. Data from the Surveillance, Epidemiology and End Results (SEER) program of the National Cancer Institute reveal that survival is poorer among African-Americans compared to White Americans.15 Among other minority ethnic groups, cancer incidence and mortality rates are lower than in White and African-Americans for the four major cancers, and for all sites combined.16 However, the rates of stomach, liver and cervical cancers are higher in these groups compared to White Americans.16 Further, ethnic minorities in the US are more likely to be diagnosed with advanced stage disease than are White Americans.16
The aim of the present study was to examine differences in the incidence of malignant cancer and cancer mortality rates among White European, Afro-Caribbean, and South-Asian people, and to examine baseline demographic predictors of cancer mortality.
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Study population
Data from the Birmingham Factory Screening project, the Birmingham components of the INTERSALT study, and data from four churches in the West Midlands, were combined into a single database. Baseline data were collected over an 18-year period and participants were followed-up for a mean (SD) of 19.9 (4.8) years. Identical methods were used in all three studies, and have been reported in detail elsewhere.17–19 In summary, 2079 participants were recruited between 1979 and 1986 from 12 factories in Birmingham, engaged in light-to-moderate manufacturing or engineering industry, and none had any known toxicological hazard associated with cardiovascular or respiratory disease.17 INTERSALT was a collaborative study on the relationship between blood pressure and sodium and potassium intake in more than 50 population samples from 32 countries.18 All data (208 INTERSALT participants and 522 INTERSALT screenees) were collected between 1984 and 1986, following a standardized protocol with common field methods in all 52 centres and centralised training and certification of researchers. In addition, 92 participants were recruited from four churches in the West Midlands between 1996 and 1997. The local ethics committee review board approved all three studies, and all participants provided informed consent.
These 2901 participants formed the cohort for this study. Since there were few South-Asian women (n = 24), and few men (n = 19) and women (n = 5) from 'other' ethnic groups available for screening, their data were excluded from the present analyses. Accordingly, the effective sample population comprised 2853 participants.
Study design
The mean value of two blood pressure readings was used to classify participants as hypertensive (SBP 
140 mmHg and/or DBP 90 mmHg or taking anti-hypertensives at screening)20 or not. Information on cigarette smoking and alcohol consumption was elicited by completion of a general health questionnaire. For the purpose of this analysis, self-reported smoking status was dichotomized as non-current (never or past smoker) or current smoker. Alcohol consumption was recorded in units per week. Body mass index (BMI) was calculated as weight (kg) divided by height squared (m2). The ethnic origin of participants was assigned by the observer based on appearance and inquiry and not by country of birth, into one of the following three groups: White European, Afro-Caribbean, or South Asian.
Cancer incidence and survival status were determined by tracing participants through the Office for National Statistics (ONS). Of the 2853 participants, 140 (4.9%) could not be traced. Therefore, the present cohort consists of 2713 participants whose survival status on 31 December 2003 was known. Registrations for (and deaths from) cancer were coded according to the International Classification for Disease, Version 10 (ICD-10).21 Cancer registrations (n = 13) and deaths (n = 4) from benign neoplasms (D10–D36) and neoplasms of uncertain or unknown behaviour (D37–D48) were excluded from this analysis. The total number of person-years of observation was 51984.81 years and was calculated from the date the participant was enrolled into each screening survey until 31 December 2003, or to the time of death. The mean (SD) length of follow-up was 19.9 (4.8) years.
Statistical analyses
Statistical analyses used SPSS for Windows, version 11.0. All statistical tests were two-tailed; p values 
0.05 were considered statistically significant. White Europeans were used as the reference group in all analyses. One-way analysis of variance (with post hoc tests where appropriate) and 
2 tests were used to test for differences in the incidence of cancer between the three ethnic groups for men and women, respectively. Each of the baseline demographic and lifestyle variables was entered individually into a Cox regression model to predict the risk of death from cancer associated with each variable. To determine the independent predictors of cancer incidence and mortality from cancer, all variables were entered together into a Cox regression model.
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Demographic characteristics
The baseline demographic data for the 2713 participants in this cohort have been reported elsewhere:22 2090 (77.0%) White European men (n = 1475) and women (n = 615), 428 (15.8%) Afro-Caribbean men (n = 257) and women (n = 171), and 195 (7.2%) South Asian men. Mean (SD) ages at screening were 43.0 (11.9), 45.1 (12.5), and 34.6 (11.4) years, for White European, Afro-Caribbean, and South Asian men, respectively, and 42.1 (12.0) and 45.3 (14.1) for White-European and Afro-Caribbean women, respectively. Overall, Afro-Caribbean men (p = 0.029) and women (p = 0.003) were significantly older than White European men and women, while South-Asian men were significantly younger (p < 0.0001) than White European men and women.
Cancer incidence
Primary cancer registrations by site (C00–C96 and D00–D09), for men and women in each of the ethnic groups, are shown in Table 1. Person-years of observation totalled 51 984.81, with a mean (SD) length of follow-up of 19.9 (4.8) years. By 31 December 2003, 300 (11.1%) people had been registered by the ONS with one or more diagnoses of cancer: 144 (48.0%) cases were terminal. The overall cancer incidence density was 0.6% per 100 person-years of observation. Among White European men, 14 had two registrations for cancer, and five had three. The corresponding figures for White European women were 12 and two, respectively. Only one Afro-Caribbean man had a second registration for cancer. No Afro-Caribbean women or South Asian men were registered with more than one cancer. There was a surprisingly low cumulative incidence of cancer, particularly among Afro-Caribbean women (6.4%) and South Asian men (3.1%) compared to White European men (11.8%) and women (13.3%). White European women had a significantly higher incidence of cancer compared to Afro-Caribbean women (2 = 5.46; p = 0.019), despite being significantly younger. In addition, South Asian men had a significantly lower incidence of cancer compared to White European men (p < 0.0001) and Afro-Caribbean men (p = 0.048). However, the incidence of cancer was similar between White European and Afro Caribbean men (p = 1.00).
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Overall, the four most common cancers in men were malignant neoplasm of the digestive organs (mainly colorectal cancer), lung and/or bronchus, skin, and prostate. Among women, the four most prevalent cancers were in situ neoplasms (mainly of the cervix uteri), breast, skin, and digestive organs. The small number of cancer registrations among Afro-Caribbean and South Asian men precluded formal analysis of ethnic differences in the type of cancer. Among Afro-Caribbean men, prostate cancer was the most common, followed by cancer of the digestive organs (Table 1). In South Asian men, there were only six registrations for cancer, three for lung cancer, two for cancer of the digestive organs and one for cancer of lymphoid, haematopoietic and related tissue. There were only 12 cancer registrations among Afro-Caribbean women, with the majority for cancer of the digestive system and breast.
Under multivariate analysis, age, ethnicity, and smoking status were independent predictors of cancer incidence (Table 4). Participants of White European origin and those who were older or smoked at enrolment were more likely to develop cancer during the follow-up period.
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Cancer mortality
By 31 December 2003, 450 participants had died: 168 (37.3%) from cancer. The overall incidence density of cancer mortality was 0.3% per 100 person years of observation. Table 2 presents the number of deaths by type of cancer, separately by sex and ethnicity. Overall, the majority of cancer deaths (n = 65; 38.7%) were of ill-defined, secondary and unspecified sites; 38 (22.6%) were due to cancer of the respiratory and intra-thoracic organs (C30-C39), mainly of the lung and bronchus (C34); and 34 (20.2%) deaths were due to cancer of the digestive organs (C15-C26). These three categories of cancer were also the most common causes of death when examining men and women separately and within each ethnic group. There were very few deaths from cancer among Afro-Caribbean men (n = 16) and women (n = 5) or South Asian men (n = 3).
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As shown in Table 3, age, ethnicity, BMI, smoking status, and hypertension were significant predictors of death from cancer. However, in multivariate analyses, the only significant predictors of mortality from cancer were age, ethnicity, BMI, and smoking status. White Europeans, older participants, those who smoked at screening, and those with a higher BMI, were more likely to die from cancer (Table 4).
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Discussion |
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This study demonstrates a low cumulative incidence of malignant cancer and low mortality rate from cancer in the two main ethnic minority groups in the UK (compared to White Europeans) over an average 20-year follow-up period. The incidence of cancer was significantly lower among Afro-Caribbean women and South Asian men compared to White Europeans, with a similar incidence of cancer in Afro-Caribbean and White European men. These findings are similar to previous UK studies that have examined the incidence of cancer3–6,13 and cancer mortality among ethnic minorities.7–11,13
Three of the most common cancers for men (colorectal, lung, and prostate) and two of the most common cancers among women (breast and colorectal) in the present cohort, mirror the most commonly reported cancers nationally.2 However, skin cancer had the highest incidence but the lowest mortality in the present study. Lung cancer and cancer of the digestive organs were the second and third most common cause of death from cancer, reflecting the poor survival rate from these cancers seen nationally.2 Unfortunately, the majority of deaths from cancer in this cohort were classified as ill-defined, secondary and unspecified sites, which is one the major problems associated with using data from death certificates. Although the incidence of cancer among ethnic minorities in the present study was low, the most common cancers among these groups mirror the most common cancers in White Europeans, consistent with the recent review findings of Wild and colleagues.13
An earlier study reported that the incidence of cancer among ethnic minorities in the UK was similar to those seen in their country of origin.4 However, a more recent survey has demonstrated a higher rate of cancer in South Asian migrants to the UK compared to those in the Indian subcontinent.6 This may be a reflection of exposure to the major risk factors for certain types of cancer and changing lifestyles among second and subsequent generations. For example, recent figures reveal that in England, Bangladeshi men have the highest prevalence of cigarette smoking (44%), followed by White Irish (39%) and Black Caribbean men (35%), with Pakistani and Indian men having a similar prevalence of cigarette smoking (26% and 23%, respectively), to the general population (27%).2 Similarly, in women the prevalence of smoking is highest among White Irish and Black Caribbean women (33% and 25%, respectively). Although few South-Asian women smoke, more than one quarter of Bangladeshi women chew tobacco. Therefore, the incidence of, and mortality rate from, lung cancer may increase in ethnic minority groups due to the changes in smoking behaviour, and shift towards that of the general population.
Further, a recent review23 found lower rates of lung cancer among South Asian men compared to non-South-Asian men, but with an increasing incidence of lung cancer among the former. Smoking rates are higher among British South Asians aged 30–49 years than in those aged 50–74.23 The incidence of lung cancer is much lower than in the rest of the population, but among South Asians, it is the most common cancer for men and the second most common among women.12,13
In research from animal and epidemiological studies, being obese or overweight increases the risk of certain types of cancer, including breast (in post-menopausal women), colon, endometrial, gallbladder, kidney, liver, oesophagus, ovarian, pancreas, and prostate.24–27 Physical inactivity and a poor diet may also contribute to certain types of cancer, although the data supporting such a viewpoint is limited. Diets with high fruit and vegetable intake, and low in meat, animal fat and/or calories have been associated with a risk reduction in several of the most common forms of cancer.28–30
It is not possible to discuss all the major determinants of cancer risk in detail here, as survival from cancer varies not only by the type of cancer but also by a number of factors including age, sex and socio-economic status. In the present study, age, ethnicity, and smoking status were significant independent predictors of both cancer incidence and mortality from cancer, with White Europeans, older participants, and those who smoked being at increased risk of developing and/or dying from cancer. Further, participants who had a higher BMI were at increased risk of death from cancer. Ethnic differences in survival from cancer may simply be a reflection of socio-economic differences.13 In England and Wales, cancer survival is dependent on socio-economic status. In the most recent analysis of cancer survival in England and Wales,31 although cancer survival improved during the 1990s for most cancers examined, survival was significantly lower among people from lower socio-economic status groups than in more affluent groups, indicating that the deprivation gap in survival between the rich and the poor has widened for patients diagnosed with cancer in the late 1990s, compared with those diagnosed in the late 1980s.31
There are important differences in cancer incidence and mortality by country of birth. However, country of birth is becoming an increasingly unreliable measure of ethnicity. Future research should establish patterns of cancer mortality among offspring of migrants. A longitudinal study of 1% of the population of England and Wales followed from 1971 to 1989 revealed that a longer duration of residence in the UK was associated with increased mortality from cancer among South Asians,32 but no effect of length of UK residence was seen in migrants from the Caribbean in terms of death from cancer.14
In the US, explanations for ethnic differences in the incidence of, and mortality from, cancer have been proposed. There may be ethnic differences in exposure to elements that increase the risk of certain cancers (e.g. hepatitis C for liver cancer), access to regular cancer screening services, and appropriate high-quality treatment15 and differences in responses to treatment. Low socio-economic status, lack of health insurance and low literacy, which may be more prevalent among ethnic minorities, can also delay diagnosis and reduce access to, and efficiency of therapies.13,33–36 Some studies have demonstrated that given similar cancer treatments and medical care, ethnic differences are eliminated.37
The low incidence of malignant cancer among minority ethnic groups in the UK compared to White Europeans may be due to lack of awareness of symptoms of certain cancers, failure to perform self-checks for breast/testicular cancer, and cultural differences in healthcare-seeking behaviour. However, a recent UK study examining the uptake of healthcare services by children and young people from minority ethnic groups revealed that ethnic minorities received a poorer quality of healthcare compared to the Caucasian population,37 despite the fact that South Asians accessed GP services more often than Caucasian children.37 In contrast, data from the ‘National Survey of NHS Patients: Cancer’, examining sociodemographic factors and delays in the diagnosis of six cancers (colorectal, lung, ovarian, prostate, breast, and non-Hodgkin's lymphoma), revealed that although Black and South Asian women experienced longer delays than White women for breast cancer diagnosis, there were no significant differences for total delays between minority ethnic groups and for other types of cancer.38
Limitations
This study has a number of limitations, many of which have been discussed previously,19,22 but is one of the largest datasets of cancer mortality amongst minority ethnic groups in the UK. In the present analyses, there were relatively few diagnoses of, and deaths, from cancer among minority ethnic groups, preventing statistical analysis of ethnic differences in the incidence of different types of cancer and by age group. In addition, we have no details on the stage of cancer at diagnosis or treatment details. Analyses were not adjusted for socio-economic status and co-morbidity, as this information was not available. There are also inherent problems associated with mortality analyses based on death certificate information. Firstly, there is considerable variation in the accuracy and detail of recording information on the cause of death; in the present cohort, the majority of the deaths from cancer were coded without specification of site. Secondly, information is only available for deaths that occurred in the UK. Deaths occurring outside of the UK may vary by ethnic group.39 For example, it may be possible that people return to their country of origin to seek medical care and/or to die.12 In addition, the paucity of deaths among the South Asian men and Afro-Caribbean women in the present study means that the numbers are too small for accurate interpretation of the results. Finally, almost 5% of the cohort could not be traced by the ONS. It is possible that more people from minority ethnic groups could not be traced.
The results from this study cannot be generalized to all ethnic minority groups in the UK, as this sample was drawn mainly from factory workers in the West Midlands and as such may represent the effect of socio-economic status on cancer. However, many studies examining the incidence of various diseases have been conducted on cohorts sampled from one particular socio-economic group (e.g. the Whitehall II cohort). There may also be a bias in selection, participation, and follow-up in our sample, although the same may be true for other cohort studies.
Bhopal and Rankin12 highlight the lack of attention given to cancer awareness and prevention in ethnic minorities, probably due to the misperception that cancer is not a major problem for ethnic minority groups. The reason for this misperception is that rates of cancer are compared to those of White Europeans, rather than focusing on the actual number of incident cases within each ethnic group.12 It is important to identify which cancers are most prevalent within each ethnic group, to allow appropriately targeted cancer awareness information, screening and prevention strategies. Changing lifestyles and improved awareness among ethnic minorities suggest that the pattern of incident cancer and mortality may begin to resemble that of the general population.
Conclusions
The cumulative incidence of cancer and cancer mortality rates among Afro-Caribbean men and (particularly) women, and South Asian men compared to White European men and women, was surprisingly low. It would be interesting to examine the incidence of cancer among UK-born people from minority ethnic groups, to determine whether they reflect the incidence rates evident among White Europeans in the UK and ethnic minorities in the USA.
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The authors wish to thank the management and workforce of the following companies for their help in this project: The Birmingham Box Co Ltd, Birmingham Metal Finishers, Blue Circle Cement, Brockhouse District Steel, RG Brown, Cooperative Society Laundry, Delta Wire Ltd, GKN Screws and Fasteners Ltd, Lucas Electrical, Stevens and Bullivant Ltd, Sturmey-Archer (Raleigh) Ltd, and Tonge and Wills Ltd. In addition, we would also like to thank the following clinical staff for their commitment and efforts in recruiting and screening participants: Dr J.K. Cruickshank, Mrs M. Beevers, R. Haynes, and R. Hornby. Finally, the authors would also like to thank Solvay and Boehringer Ingleheim pharmaceutical companies for their educational non-promotional grants towards this project.
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