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BioMed Central
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BMC Public Health
Open Access
Research article
Inequalities in the incidence of cervical cancer in South East England
2001–2005: an investigation of population risk factors
Laura G Currin*, Ruth H Jack, Karen M Linklater, Vivian Mak, Henrik Møller
and Elizabeth A Davies
Address: King's College London, Thames Cancer Registry, 1st Floor, Capital House, Weston Street, London, SE1 3QD, UK
Email: Laura G Currin* - laura.g.currin@kcl.ac.uk; Ruth H Jack - ruth.jack@kcl.ac.uk; Karen M Linklater - karen.linklater@kcl.ac.uk;
Vivian Mak - vivian.mak@kcl.ac.uk; Henrik Møller - henrik.moller@kcl.ac.uk; Elizabeth A Davies - elizabeth.davies@kcl.ac.uk
* Corresponding author
Abstract
Background: The incidence of cervical cancer varies dramatically, both globally and within
individual countries. The age-standardised incidence of cervical cancer was compared across
primary care trusts (PCTs) in South East England, taking into account the prevalence of known
behavioural risk factors, screening coverage and the deprivation of the area.
Methods: Data on 2,231 cases diagnosed between 2001 and 2005 were extracted from the
Thames Cancer Registry, and data on risk factors and screening coverage were collated from
publicly available sources. Age-standardised incidence rates were calculated for each PCT using
cases of squamous cell carcinoma in the screening age group (25–64 years).
Results: The age-standardised incidence rate for cervical cancer in South East England was 6.7 per
100,000 population (European standard) but varied 3.1 fold between individual PCTs. Correlations
between the age-standardised incidence rate and smoking prevalence, teenage conception rates,
and deprivation were highly significant at the PCT level (p < 0.001). However, screening coverage
was not associated with the incidence of cervical cancer at the PCT level. Poisson regression
indicated that these variables were all highly correlated and could not determine the level of
independent contribution at a population level.
Conclusion: There is excess disease burden within South East England. Significant public health
gains can be made by reducing exposure to known risk factors at a population level.
Background
Cervical cancer represents a significant public health con-
cern. Worldwide, cervical cancer is the second most com-
mon malignancy among females [1]. Although the 5-year
survival rates for this cancer are relatively high, on average
women are diagnosed and die at a younger age than in
most other types of cancer. The total years of life lost due
to this illness are therefore substantial. Currently, cervical
cancer rates eighth in terms of cancer incidence in the
United Kingdom [2].
Within the United Kingdom, rates of cervical cancer are
highest in the Yorkshire and North West regions of Eng-
land, and Scotland; and lowest in the Eastern, South East
and London regions of England [2]. Within London, a
recent report highlighted the link between socio-eco-
Published: 20 February 2009
BMC Public Health 2009, 9:62 doi:10.1186/1471-2458-9-62
Received: 5 June 2008
Accepted: 20 February 2009
This article is available from: http://www.biomedcentral.com/1471-2458/9/62
© 2009 Currin et al; licensee BioMed Central Ltd.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
BMC Public Health 2009, 9:62 http://www.biomedcentral.com/1471-2458/9/62
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nomic deprivation and inequalities in cervical cancer inci-
dence and mortality [3]. Age-standardised incidence rates
per 100,000 European population were 9.6 in the most
deprived areas compared to 5.4 in the most affluent areas.
Age-standardised mortality rates were 4.2 and 1.7 per
100,000 for the most deprived and most affluent areas
respectively. This relationship between deprivation and
higher incidence of cervical cancer is consistently repli-
cated [4,5] even when controlling for access to medical
care [6].
The Cancer Reform Strategy published by the Department
of Health has recently prioritised the reduction of cancer
inequalities across England [7]. To target public health
interventions it is important to know why deprivation is
associated with increased rates of cervical cancer. For
example, is deprivation itself a predictor of cervical cancer,
or can the association be explained by a relationship
between deprivation and known aetiological risk factors?
In the aetiology of cervical cancer, the human papilloma
virus (HPV) is a necessary precursor for carcinogenesis
and is found in almost all cases of squamous cell carcino-
mas [8]. However, infection alone is insufficient to result
in cervical cancer as infection rates are approximately
1,000 times higher than the incidence of cervical cancer
and at least 90% of infections resolve spontaneously
[9,10]. Established co-factors for the development of cer-
vical cancer include multi-parity, age at first delivery,
tobacco use, and use of oral contraceptives [11-14].
Both HPV infection rates and the prevalence of co-factors
within a population are known to be influenced by socio-
economic variables. For example, in a recent study con-
ducted in the United States women living below the pov-
erty line had almost twice the rate of HPV compared to
those living above (23% versus 12%, p = .03) [15]. Part of
this relationship may be explained by different sexual
behaviour. Sexual contact determines exposure to HPV,
and early sexual intercourse has been identified as a risk
factor for the development of cervical cancer [16].
Epidemiological studies implicate cigarette smoking as an
independent risk factor for the development of cervical
cancer, with odds ratios ranging from 1.8 to 4.3 [17,18].
This effect appears to be limited to the squamous cell sub-
type of cervical cancer [17], although the exact biological
mechanism is still debated. Smoking is likely to lead to
cervical cancer through multiple pathways. There is evi-
dence of alteration of the tumour suppressor gene FHIT
[19], inhibition of normal cervical cell proliferation [20],
and local immune suppression resulting in persistent HPV
infection [21]. Smoking rates in a population are known
to be strongly predicted by socio-economic deprivation
[22]. Therefore, it is likely that the association between
cervical cancer and deprivation could be partially
explained by differential rates of smoking.
Socio-demographic features of a population may also
affect prevention efforts. Screening programmes are effec-
tive in reducing the incidence and mortality of cervical
cancer by detecting early cellular changes which could
lead to cervical cancer [23]. There is a 63% predicted
reduction in lifetime incidence in populations with an
effective screening program compared to unscreened pop-
ulations [24]. In England, the National Health Service
Cervical Screening Programme (NHSCSP) was estab-
lished in 1988 and the current target for screening cover-
age is 80% of all eligible females in the general practice
population (screened at variable, age-dependent, inter-
vals) [25,26]. However, screening utilisation is influenced
by socio-demographic variables. For example, women
from disadvantaged backgrounds are more likely to see
the screening procedure as aversive and feel less obliged to
attend than their more well off neighbours [27]. In the
UK, cervical screening coverage is consistently higher in
affluent areas, although this disparity is declining [28,29].
This study aimed to quantify the relationship between cer-
vical cancer incidence and aetiological risk factors and
screening coverage at a population level; and to investi-
gate whether deprivation itself predicts an additional risk
to the population studied. The specific objectives were:
1. To demonstrate geographical inequalities in the age-
standardised incidence of cervical cancer in the area of
South East England covered by the Thames Cancer Regis-
try (TCR) between 2001 and 2005.
2. To use Spearman's correlation coefficient to investigate
the association at a population level between incidence
and aetiological risk factors (i.e. sexual behaviour, smok-
ing); and incidence and screening coverage.
3. To use Poisson regression to determine if deprivation
remains an independent risk factor for the development
of cervical cancer when controlling for these variables.
Methods
In the United Kingdom cancer registries record the occur-
rence of cancer in their resident populations. During the
study period the Thames Cancer Registry (TCR) covered a
population of 12 million people living in the area includ-
ing London, Kent, Surrey and Sussex. In this area, cancer
registration is initiated by clinical and pathological infor-
mation received from hospitals and by information about
deaths provided by the National Health Service Central
Register through the Office for National Statistics. Trained
data collection officers collect further demographic infor-
mation, details on disease stage and treatment received in
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the six months following diagnosis from the medical
records of individual cases. Data are continuously added
to a central database and quality assured. To prevent dou-
ble counting, information about new tumours is cross-
checked against already registered cases.
Information on tumour stage is extracted from the medi-
cal records, however, since this information is often not
complete, TCR creates an in-house classification using all
available information to approximate stage at diagnosis.
Tumours are categorised as 'local' (stage 1), 'extension
beyond organ of origin' (stage 2), 'regional lymph node
involvement' (stage 3) and 'metastasis' (stage 4). Tumours
with insufficient information are classified as having dis-
ease stage 'not known'.
The first objective of the study was, to describe inequali-
ties in South East England. Data were extracted from the
TCR database on 2,231 cases diagnosed with cervical can-
cer [ICD-10 category C53; [30]] between 2001 and 2005.
Descriptive statistics defined the sample by tumour type
and the stage of presentation. Cases were stratified into
five-year age bands to calculate age-specific incidence rates
for cervical cancer for the years 2001–2005. An age-stand-
ardised incidence rate was calculated for women living
within the entire catchment area using the European
standard population.
The geographic area covered by the TCR is diverse, includ-
ing urban, suburban and rural areas and areas of contrast-
ing affluence and deprivation. Thirty-one of the
constituent primary care trusts (PCTs) are within the Lon-
don Strategic Health Authority and eight within the South
East Coast Strategic Health Authority. To investigate ine-
qualities in the incidence of cervical cancer, the age-stand-
ardised incidence was calculated for each PCT. The age-
standardised incidence was calculated for women of all
ages, and then restricted to cases of squamous cell carcino-
mas within women aged 25–64 years to include only the
screened age group. Squamous cell cases were considered
specifically because this histological type is associated
with the risk conferred by smoking and also the most
likely to be detected by screening [17]. Calculation of
truncated age-standardised rates is described by Boyle and
Parkin [31]. Truncated incidence rates were used for all
between PCT comparisons, and a chi square test of heter-
ogeneity was used to establish the statistical significance
of the variation between PCTs.
The second objective of this study was to assess the rela-
tionship between age-standardised incidence and aetio-
logical risk factors or prevention efforts at the population
level. Although HPV infection rates are not routinely
measured, teenage conception rates can act as a proxy for
the early sexual contact which confers a behaviour risk for
cervical cancer [32]. One potential limitation of this
approach is the potential for teenage conception to be
confounded with other HPV co-factors such as tobacco
use or age at first delivery. However, teenage conception
rates are included as a health indicator by the Health Care
Commission [33] and therefore reliably measured and
reported at the PCT level. Teenage conception rates for the
PCTs covered by the TCR were obtained from the Office
for National Statistics (ONS) and then correlated with the
truncated age-standardised incidence rates by PCT. Spear-
man's correlation coefficient was used to test whether
these two factors were correlated.
National and regional figures for smoking prevalence are
regularly produced, yet figures for individual PCTs rely on
synthetic statistical estimation [34]. These synthetic esti-
mates were used to correlate PCT smoking prevalence
with the age-standardised incidence, using Spearman's
correlation coefficient.
Cervical screening coverage within PCTs was obtained
from the ONS [35]. Screening coverage was calculated by
considering the number of women screened divided by
the total eligible population within the target age range
(25 to 64) during the 2004/2005 financial year. ONS fig-
ures were used in preference to those reported by the
Quality and Outcomes Framework, as the latter are based
on remuneration figures for primary health care providers
and allow for some reductions in target population fig-
ures. Spearman's correlation coefficient was calculated to
assess the relationship between the age-standardised inci-
dence and screening coverage at the PCT level.
Cases were assigned into deprivation categories using
super-output areas, which are based on the postcode of
residence. The income domain of the Indices of Depriva-
tion 2004 was used to classify super-output areas into
deprivation quintiles in which 1 is the most affluent and
5 is the most deprived [36]. PCTs were ranked according
to the percentage of areas within their borders in the two
most deprived quintiles.
Finally, Poisson regression was used to model the inci-
dence of cervical cancer at the PCT level. The aim of this
analysis was to determine if deprivation predicted a risk
over and above that contributed by teenage conception,
smoking, and screening. All analyses were adjusted for age
and PCT.
Results
Tumour description
Table 1 illustrates the histological classification of inci-
dent cases of cervical cancer in the TCR in the years
between 2001 and 2005. Squamous cell carcinoma was
the most common presentation (63.9%; n = 1,425). Miss-
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ing data prevented determination of tumour stage in
34.5% (n = 770) of cases. However of the cases with suffi-
cient information, the majority (69.3%; n = 1,012) pre-
sented with localised disease (data not presented).
Age-specific incidence
Analysis of the age-specific incidence showed a marked
rise in cervical cancer incidence in the third and fourth
decade of life, followed by a relative plateau (Figure 1).
Age-standardised incidence
The age-standardised incidence rate for cervical cancer in
women living in South East England was 6.7 per 100,000
person years using the European standard population for
the years 2001–2005.
A test of heterogeneity demonstrated significant PCT vari-
ability in the truncated age-standardised incidence of
squamous cell cervical cancer in the potential screened
population (women age 25–64; χ2 (40) = 103.4; p <
0.0001). The highest incidence (11.6 per 100,000 person
years) was found in Lambeth PCT, and the eight PCTs
with the highest incidence were all found within London
rather than in suburban or rural environments. Surrey
PCT had the lowest incidence (3.7 per 100,000 person
years).
Deprivation
There was considerable variability in the underlying socio-
economic status of the PCT populations. For example, in
Surrey PCT only 8% of the super-output areas were in the
two most deprived quintiles, compared with Newham
PCT where all super-output areas were deprived. Figure 2
demonstrates that those PCTs with a higher proportion of
deprived areas also had a higher incidence of cervical can-
cer. Deprivation was highly correlated with the truncated
incidence of cervical cancer (Spearman r = 0.57; p <
0.001).
Risk and prevention
In addition to differences in socio-economic status, PCTs
also varied in terms of known risk factors (teenage con-
Table 1: Histological classification of cervical cancer diagnosed in
women in South East England, 2001–2005
Classification Count (%)
Squamous cell carcinoma 1,425 (63.9)
Adenocarcinoma 497 (22.3)
Unknown 251 (11.3)
Other specified histologies 58 (2.6)
Total 2,231 (100)
Age-specific incidence rates of cervical cancer in women in South East England, 2001–2005Figure 1
Age-specific incidence rates of cervical cancer in women in South East England, 2001–2005.
0
2
4
6
8
10
12
14
16
18
0 - 4 5-9 10-14 15-19 20-24 25-29 30-34 35-39 40-44 45-49 50-54 55-59 60-64 65-69 70-74 85-79 80-84 85+
Age
Inci denc e per 100,000 pers on y ears
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ception rates, smoking prevalence) and prevalence of pre-
ventative measures (cervical screening coverage).
The conception rates for women aged 15–17 varied over
four-fold. Richmond & Twickenham PCT had the lowest
rates of 23.6 per 1,000 population, compared to 95.2 per
1,000 in Lambeth PCT (Figure 3). There was a significant
correlation between teenage conception rates and the age-
adjusted incidence of squamous cell cervical cancer
(Spearman r = 0.65; p < 0.001).
Smoking prevalence in the TCR area varies from a low of
21% in Harrow PCT to a high of 38% in Islington PCT
(Figure 4). There was a significant positive correlation
between the age-standardised incidence of cervical cancer
and smoking prevalence at PCT level (Spearman r = 0.62;
p < 0.001).
PCT screening programmes had different levels of cover-
age. Screening of eligible women was lowest in Hammer-
smith & Fulham PCT (68.7%) and highest in Bexley PCT
(84.3%). Figure 5 illustrates the non-significant negative
correlation between age-standardised incidence and PCT
screening coverage (r = -0.09; p = 0.61).
Model of population risk
Table 2 presents the results from the Poisson regression
analyses. In the univariate analysis each individual popu-
lation variable significantly predicted the PCT incidence
of cervical cancer (adjusted for age). However, when the
four variables were considered together in the multivari-
ate analysis, the only predictor which remained independ-
ently significant was smoking prevalence (p < 0.05).
Discussion
Main findings
The age-standardised incidence rate for cervical cancer in
South East England is 6.7 per 100,000 European standard
population. When restricting the analysis to squamous
cell carcinoma, which is the histological type most likely
to be influenced by smoking prevalence and screening,
there were significant inequalities in incidence within the
area. There was a 3.1 fold difference between primary care
trusts (PCTs) with the highest and lowest incidence. Age-
standardised incidence rates of cervical cancer were signif-
icantly correlated with deprivation, teenage conception
rates, and smoking prevalence. Attempts to model the
independent contribution of these risk factors at a popu-
lation level suggested that all these variables are highly
Deprivation (red line) and age-standardised incidence of squamous cell cervical cancer (bars) in women aged 25–64 by PCT in South East England, 2001–2005Figure 2
Deprivation (red line) and age-standardised incidence of squamous cell cervical cancer (bars) in women aged
25–64 by PCT in South East England, 2001–2005.
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correlated with one another, and this potential confound-
ing limits the conclusions about the contribution of spe-
cific risk factors at the population level.
When looking at population studies of cervical cancer,
deprived areas are known to have an increased incidence
of cervical cancer [3-5,15]. This relationship remains even
when controlling for availability and access to medical
services [5], suggesting that these populations have differ-
ential exposure to risk factors important in the develop-
ment and progression of the disease. These risk factors are
potentially modifiable at the population level using pub-
lic health interventions. For example, differences in sexual
behaviour can influence the development of cervical can-
cer due to the transmission of HPV, and this variable sex-
ual behaviour has been used to explain the vast
inequalities between countries [37] and within popula-
tions [38]. Randomised trials have shown that popula-
tion-based interventions can reduce risky sexual
behaviour [39]; however the subsequent reduction in
incidence of sexually transmitted infections has not been
established [40].
Although smoking prevalence has been declining, areas of
lower socio-economic status have a disproportionate
number of active smokers. Smoking is known to be an
independent risk factor for cervical cancer [18], with the
exact biological mechanism yet to be determined. Smok-
ing cessation has been the target of a major public health
campaign in the UK, and the National Institute for Clini-
cal Health and Excellence has produced recommenda-
tions for effective interventions [41]. By targeting these
interventions in deprived areas with high smoking inci-
dence one benefit could be the reduction of inequalities in
the incidence of cervical cancer.
In this study, the lack of correlation between population
screening and incidence of cervical cancer could be due to
relatively uniform levels of screening in all PCTs studied,
with the lowest levels above 68% of eligible females.
While this homogeneity may mask a significant associa-
tion between screening and incidence, it does highlight
that a number of PCTs are below the Department of
Health target of 80% screening coverage. Improvements
in screening coverage at the population level could result
in further reductions in the incidence and mortality of this
Teenage conception (red line) and age-standardised incidence of squamous cell cervical cancer (bars) in women aged 25–64 by PCT in South East England, 2001–2005Figure 3
Teenage conception (red line) and age-standardised incidence of squamous cell cervical cancer (bars) in
women aged 25–64 by PCT in South East England, 2001–2005.
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disease [23]. Creative approaches may be needed to
increase participation in those groups who will benefit
most from screening, including lower socio-economic
groups and those who smoke. Arguments have also been
made for changes in the delivery of screening programmes
to improve the yield of positive results and reduce the rate
of false positives [7,23]. The emphasis on screening
should continue despite advances in HPV vaccination
programmes. HPV vaccination of girls aged 12 to 13 years
began in the UK in September 2008 [42]. However, the
time lag between infection and carcinogenesis means the
vaccination programme will not result in a decline in cer-
vical cancer incidence at a population level for at least a
decade, underlining the importance of continued screen-
ing.
Limitations
This study makes use of one of the largest population-
based cancer registries in Europe to investigate inequali-
ties in cancer incidence in a geographically defined area.
Publicly available data were used to investigate known
risk factors, including smoking and social deprivation.
However, reliance on existing datasets limits the flexibility
and range of analysis to variables that are currently avail-
able at the PCT level.
When attempting to explain inequalities in cervical cancer
incidence it is important to consider all the known aetio-
logical risk factors. The most important risk factor in the
development of cervical cancer is infection with human
papilloma virus (HPV) [8,37,43]. However, when analys-
ing cervical cancer rates at a population level there are sev-
eral difficulties quantifying concurrent or previous HPV
infection. First, HPV infection is widespread and infection
rates range from 4–40% in sexually active women with
normal cervical cytology, yet most HPV infections resolve
without leading to detectable lesions [9,44,45]. Second,
HPV infection rates are not routinely collected from repre-
sentative populations. Although infection with another
sexually transmitted infection such as genital warts could
be a useful proxy measure, this data is not available at the
PCT level. This is an avenue for further research.
Synthetic estimates of smoking prevalence are not as
robust as actual surveillance of the behaviour of the pop-
ulation of interest. Measures were in place to ensure con-
sistency and reliability in these estimates [34], but the
Smoking prevalence (red line) and age-standardised incidence of squamous cell cervical cancer (bars) in women aged 25–64 by PCT in South East England, 2001–2005Figure 4
Smoking prevalence (red line) and age-standardised incidence of squamous cell cervical cancer (bars) in
women aged 25–64 by PCT in South East England, 2001–2005.
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methodology might introduce a degree of confounding
when considered in the context of other population char-
acteristics. Synthetic estimates are calculated from the
demographic and social characteristics of the area and
they may therefore prove unreliable for inclusion in mod-
els of risk which also include these variables [46].
Screening participation rates at the population level are
unlikely to represent adequately the variability in screen-
ing behaviours which may influence the development of
cervical cancer. Optimal screening periods are variable by
age [25,47], and this study does not take into account this
factor in analysis, nor does it consider that many of the
women screened may still be at an increased risk due to
longer periods between screening.
Conclusion
There are inequalities in the incidence of cervical cancer in
South East England, and higher rates are clearly associated
with deprivation. Public health campaigns could decrease
the disease burden of cervical cancer by focusing on
known aetiological risk factors. However, these risks clus-
ter together and it is difficult to determine the individual
contribution of each variable at a population level. The
proximity of areas of high and low incidence demonstrate
that population risk factors for cervical cancer can vary
dramatically within a region. In the future other data, such
as that on sexually transmitted infections, needs to be
reported at a level of detail which is not currently availa-
ble. Using better information on which individuals within
a population have increased risk of cervical cancer, screen-
Screening coverage (red line) and age-standardised incidence of squamous cell cervical cancer (bars) in women aged 25–64 by PCT in South East England, 2001–2005Figure 5
Screening coverage (red line) and age-standardised incidence of squamous cell cervical cancer (bars) in
women aged 25–64 by PCT in South East England, 2001–2005.
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Table 2: Predictors of the incidence of squamous cell cervical
cancer at PCT level in South East England, 2001–2005
Univariate analysis* IRR z p95% CI
Deprivation 1.01 3.5 <0.001 1.00 – 1.01
Teenage conception 1.01 4.8 <0.001 1.01 – 1.02
Smoking prevalence 1.04 4.5 <0.001 1.02 – 1.06
Screening coverage 0.97 -2.6 0.008 0.95 – 0.99
Multivariate analysis†IRR z P95% CI
Deprivation 1.00 0.28 0.78 1.00 – 1.00
Teenage conception 1.01 1.76 0.08 1.00 – 1.01
Smoking prevalence 1.02 2.06 0.04 1.00 – 1.02
Screening coverage 1.00 -0.42 0.67 0.97 – 1.00
* adjusted for age and PCT
† adjusted for age, PCT, deprivation, smoking, teenage conception,
and screening coverage
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ing programmes and preventative efforts could be targeted
more effectively.
Competing interests
The authors declare that they have no competing interests.
Authors' contributions
LGC conceived the project, analysed data analysis and
drafted the manuscript; RHJ, KML, and VM assisted with
data analysis and interpretation; HM and EAD assisted
with data interpretation and critically revised the manu-
script. All authors contributed to the study design and
approved the final manuscript.
Acknowledgements
We would like to thank the London Quality Assurance Reference Centre
for comments on an earlier draft.
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