4. Discussion
Incidence of primary liver cancer is highest in Pakistani,
Bangladeshi, Black African and Chinese men and women in
England. Indian men and women have incidence rates that are
slightly higher than White groups, while Black Caribbean groups’
rates are similar to their White counterparts. Pakistani men and
0.4
0.6
0.8
1.0
1.5
2.0
3.0
4.0
5.0
6.0
7.0
Incidence rate ratio
Indian Pakistani Bangladeshi Black Black Chinese
Caribbean African
Fig. 2. Age-standardised incidence rate ratios for females diagnosed with primary
liver cancer, England, 2001–2007. White women used as baseline.
Table 2
Survival hazard ratios for male patients diagnosed with primary liver cancer, England, 2001–2007.
Model adjusting for
Age Age + deprivation Age, deprivation + co-morbidity
HR (95% CI) p HR (95% CI) p HR (95% CI) p
Ethnicity
White 1.00 1.00 1.00
Indian 0.97 (0.80,1.18) 0.765 0.95 (0.78,1.14) 0.567 0.95 (0.78,1.15) 0.577
Pakistani 0.86 (0.70,1.05) 0.147 0.82 (0.67,1.01) 0.063 0.82 (0.67,1.01) 0.063
Bangladeshi 0.95 (0.70,1.30) 0.764 0.91 (0.67,1.24) 0.542 0.91 (0.67,1.24) 0.543
Black Caribbean 0.87 (0.68,1.12) 0.288 0.84 (0.65,1.08) 0.178 0.84 (0.65,1.08) 0.170
Black African 0.95 (0.75,1.19) 0.646 0.91 (0.72,1.15) 0.438 0.91 (0.72,1.15) 0.433
Chinese 0.66 (0.51,0.86) 0.002 0.65 (0.50,0.85) 0.002 0.65 (0.50,0.85) 0.002
Other 0.85 (0.73,0.98) 0.023 0.83 (0.71,0.95) 0.009 0.83 (0.72,0.96) 0.011
Not known 1.40 (1.33,1.48) <0.001 1.41 (1.34,1.48) <0.001 1.52 (1.41,1.63) <0.001
x2 (8 df) 194.74 204.00 164.32
p-Value (heterogeneity) <0.0001 <0.0001 <0.0001
Deprivation quintile
1 (least deprived) 1.00 1.00
2 1.00 (0.93,1.07) 0.954 1.00 (0.93,1.07) 0.948
3 1.08 (1.00,1.16) 0.037 1.08 (1.00,1.16) 0.041
4 1.09 (1.02,1.17) 0.017 1.09 (1.01,1.17) 0.022
5 (most deprived) 1.14 (1.06,1.22) <0.001 1.13 (1.06,1.22) <0.001
x2 18.94 18.26
p-Trend <0.0001 <0.0001
Co-morbidity score
0 1.00
1 1.10 (1.04,1.17) 0.002
2+ 1.03 (0.97,1.08) 0.341
Not known 0.90 (0.82,0.99) 0.035
x2 (3 df) 17.04
p-Value (heterogeneity) 0.0007
36 R.H. Jack et al. / Cancer Epidemiology 37 (2013) 34–38women, Black African women, Chinese men, and men from the
‘Other’ ethnic group had better survival compared with their White
counterparts.
An earlier report that examined cancer incidence in major
ethnic groups in England found that primary liver cancer incidence
was around twice as high in Black men than White men [14]. In the
present study, Black Caribbean and Black African men had
incidence rate ratios of 1.2 and 3.3, respectively, highlighting
the differences between these two ethnic groups. Results were
more similar for Black women compared with White women, with
rate ratios of 1.3 in Black Caribbean women and 1.7 in Black African
women in the present study, and 1.7 for all Black women found
previously [14]. Previously much higher incidence rates have been
shown in Chinese groups in the US [7]. In California, incidence rates
were three times higher in Chinese men and women than in the
corresponding White groups [13], while the present study found
incidence rates were around four times higher in Chinese men and
twice as high in Chinese women.
The pattern of incidence in South Asians has previously been
less clear. A similar incidence of liver cancer has been found in the
US between a combined Indian and Pakistani group and USWhites
[21], and between British Indians and British Whites in Leicester
[27]. Combining South Asian groups in England, men and women
were found to have incidence rates around twice as a high as their
White counterparts [14]. Due to the poor survival of liver cancer
patients, mortality can be used as a proxy for incidence [4].
Examining liver cancer mortality in England and Wales found
higher standardised mortality ratios for first generation Indian,
Pakistani and Bangladeshi men and women than the general
population [28]. Bangladeshi men and women had the highest
mortality, followed by Pakistani, and then Indian groups.
However, when examining second generation South Asians, these
groups had lower mortality than the England and Wales
population. The difference between first and second generation
populations highlights the possible importance of early life
exposure to factors, such as hepatitis B [6,29]. Differences in
hepatitis B and C infection between ethnic groups have been
found within the UK [30,31].
The present study found that Pakistani men and women, and
Chinese men had better survival than their White counterparts.
This is similar to Goggins and Wong’s [21] study that reported
Indian/Pakistani and Chinese groups had better survival than the
White group, although these results only reached statistical
significance in the larger Chinese group. Studies in the US have
examined survival in patients with hepatocellular carcinoma and
intrahepatic cholangiocarcinoma separately and found that Black
patients generally had worse survival than other groups [17–20].
Conversely, in the present study, Black African women had better
survival than White women, and there was no statistically
significant difference between the Black Caribbean and White
groups. Stage of disease at diagnosis may be responsible for
variation in survival among ethnic group. Some ethnic groups are
intensively monitored for HBV and HCV infection resulting in
earlier diagnosis and thus perhaps affecting their survival.
Unfortunately, this information is not currently available in the
National Cancer Data Repository, though future work examining
survival should assess the impact of stage of disease where
possible.
The long period of time covered by this study, and the fact that
all cancer registrations in England are included, have meant that
more detailed ethnic groups have been analysed. However, around
a quarter of patients did not have any ethnicity information
available. If these patients were from a particular ethnic group, this
may have biased the results. For example, if those without
ethnicity information were actually White, the incidence rate
ratios for the other ethnic groups would be decreased. This
Table 3
Survival hazard ratios for female patients diagnosed with primary liver cancer, England, 2001–2007.
Model adjusting for
Age Age + deprivation Age, deprivation + co-morbidity
HR (95% CI) p HR (95% CI) p HR (95% CI) p
Ethnicity
White 1.00 1.00 1.00
Indian 1.05 (0.80,1.38) 0.745 1.02 (0.77,1.34) 0.908 1.02 (0.77, 1.34) 0.911
Pakistani 0.76 (0.57,1.02) 0.068 0.74 (0.55,0.99) 0.041 0.73 (0.54, 0.98) 0.036
Bangladeshi 1.26 (0.77,2.07) 0.359 1.21 (0.74,1.99) 0.450 1.20 (0.73, 1.97) 0.475
Black Caribbean 0.92 (0.67,1.26) 0.601 0.88 (0.64,1.21) 0.432 0.87 (0.63, 1.20) 0.392
Black African 0.61 (0.38,0.96) 0.035 0.58 (0.37,0.93) 0.024 0.59 (0.37, 0.94) 0.025
Chinese 1.21 (0.74,1.98) 0.449 1.20 (0.73,1.97) 0.468 1.18 (0.72, 1.93) 0.510
Other 0.93 (0.74,1.17) 0.532 0.92 (0.73,1.16) 0.476 0.92 (0.73, 1.16) 0.492
Not known 1.34 (1.25,1.43) <0.001 1.34 (1.26,1.43) <0.001 1.39 (1.28, 1.52) <0.001
x2 (8 df) 88.28 91.45 68.26
p-Value (heterogeneity) <0.0001 <0.0001 <0.0001
Deprivation quintile
1 (least deprived) 1.00 1.00
2 1.09 (1.00,1.20) 0.058 1.09 (0.99,1.20) 0.064
3 1.16 (1.06,1.27) 0.002 1.16 (1.06,1.27) 0.002
4 1.20 (1.10,1.31) <0.001 1.20 (1.10,1.31) <0.001
5 (most deprived) 1.18 (1.08,1.29) <0.001 1.18 (1.08,1.29) <0.001
x2 16.50 16.08
p-Trend <0.0001 <0.0001
Co-morbidity score
0 1.00
1 1.09 (1.02,1.18) 0.017
2+ 1.04 (0.97,1.12) 0.311
Not known 0.97 (0.86,1.08) 0.559
x2 (3 df) 6.72
p-Value (heterogeneity) 0.0812
R.H. Jack et al. / Cancer Epidemiology 37 (2013) 34–38 37extreme assumption would misclassify some patients from other
ethnic groups. Using this reclassification as a sensitivity analysis,
the incidence rate ratios for Pakistani, Bangladeshi, Black African
and Chinese men, and Pakistani and Bangladeshi women were still
statistically significantly high (data not shown).
The availability of population estimates for different age and
ethnic groups meant that the assumption that the population
was unchanged since the 2001 Census was not needed. The
differences between the estimated data and the original Census
data are small in the older age groups, and so the results were
not materially affected by using either population dataset.
This study has found variations in the incidence and survival of
primary liver cancer between ethnic groups. Both clinicians and
the communities affected should be aware of the higher risks in
particular ethnic groups. These differences are possibly due to
higher prevalence of established risk factors such as chronic
hepatitis B and C viral infection in some, but not all ethnic groups.
Due to the low seroprevalence of hepatitis B in the UK, country of
birth, age at migration and length of stay in England are likely to be
important factors in this disease, and future research should
examine these where possible.
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