Elsevier

European Journal of Cancer

Volume 49, Issue 15, October 2013, Pages 3262-3273
European Journal of Cancer

Worldwide trends in cervical cancer incidence: Impact of screening against changes in disease risk factors

https://doi.org/10.1016/j.ejca.2013.04.024Get rights and content

Abstract

Background

Cervical cancer trends in a given country mainly depend on the existence of effective screening programmes and time changes in disease risk factors, notably exposure to human papillomavirus (HPV). Screening primarily influences variations by period of diagnosis, whereas changes in risk factors chiefly manifest themselves as variations in risk across successive birth cohorts of women.

Methods

We assessed trends in cervical cancer across 38 countries in five continents, age group 30–74 years, using age-standardised incidence rates (ASRs) and age-period-cohort (APC) models. Non-identifiability in APC models was circumvented by making assumptions based on a consistent relationship between age and cervical cancer incidence (i.e. approximately constant rates after age 45 years).

Findings

ASRs decreased in several countries, except in most of Eastern European populations, Thailand as well as Uganda, although the direction and magnitude of period and birth cohort effects varied substantially. Strong downward trends in cervical cancer risk by period were found in the highest-income countries, whereas no clear changes by period were found in lower-resourced settings. Successive generations of women born after 1940 or 1950 exhibited either an increase in risk of cervical cancer (in most European countries, Japan, China), no substantial changes (North America and Australia) or a decrease (Ecuador and India).

Interpretation

In countries where effective screening has been in place for a long time the consequences of underlying increases in cohort-specific risk were largely avoided. In the absence of screening, cohort-led increases or, stable, cervical cancer ASRs were observed. Our study underscores the importance of strengthening screening efforts and augmenting existing cancer control efforts with HPV vaccination, notably in those countries where unfavourable cohort effects are continuing or emerging.

Funding

Bill and Melinda Gates Foundation (BMGF).

Introduction

Invasive cervical cancer (ICC) is the third most common cancer in women worldwide, with an estimated 529,000 new cases in 2008. The burden of cervical cancer varies considerably worldwide, with more than 85% of the global burden occurring in low-to-medium-resource countries, where it is still in many instances the most common malignancy in women.1 Incidence and mortality rates of ICC have fallen over the past decades in a number of countries, mainly in high-resource countries following the introduction of screening programmes for cervical cancer.2, 3, 4, 5 However, stable or even rising trends have been observed in countries where screening activity is either lacking or suffers from low-quality and low-coverage.2, 4, 6

Persistent infection with oncogenic human papillomavirus (HPV) is considered a necessary cause of ICC.7 Other cofactors, such as high number of sexual partners, young age at first sexual intercourse,8 multiparity,9 oral contraceptive use,10 smoking11 and HIV infection,7 influence either the risk of acquisition of HPV infection or the progression to ICC. HPV infection could not be accurately detected in large epidemiological studies until the 1980s, and little is known on time trends of HPV prevalence in different populations.12, 13

The comparison of ICC trends in different countries offers, therefore, an opportunity to assess the impact of screening efforts set against background changes in ICC risk factors.2 For this purpose, we performed age-period-cohort (APC) analyses using incidence data from high-quality and longstanding population-based cancer registries from 38 countries to examine ICC patterns and trends across the major world regions.

Section snippets

Incidence data

New cases of ICC by age and calendar year of diagnosis were obtained from population-based cancer registries from the series Cancer Incidence in Five Continents (CI5) Volumes I to IX.14 Population data were obtained from the same sources. Registries were included in our study if there was availability of at least 15 consecutive years of data and they were included in the last volume of CI5. The last year of diagnosis available in Volume IX of CI5 was 2002, but more recent data accessible

ASRs of incident cervical cancer

Table 1 shows the incidence series available, by country, and the number of incident ICC cases, person-years and truncated ASRs for the period 1998–2002 and ages 30–74. Incidence rates varied approximately 10-fold across study populations, with the lowest ASR in 1998–2002 observed in Finland (ASR = 8 per 100,000) and the highest in Uganda (ASR = 104). Incidence rates in North America, Australia and Europe ranged between eight in Finland and 21 in Denmark and Norway. In Eastern Europe, ASRs were

Discussion

This descriptive analysis suggests that, despite general declines in ASRs globally, the risk of cervical cancer by calendar period of diagnosis and birth cohort varied substantially by country and world region in the last decades. Strong downward trends in ICC risk by period were observed in the highest-income countries in contrast to the mainly stable period curves seen elsewhere. Successive cohorts of women born in 1940–50 and thereafter exhibited either increases in ICC risk (e.g. in nearly

Contributors

S.V. and F.B. conceived and designed the study. J.L.T. provided cancer incidence estimates adapted from the Cancer Incidence in Five Continents database. S.V., M.P. and J.L.T. contributed to data collection and data analysis. S.V., F.B. and S.F. wrote the draft manuscript. All authors contributed to the interpretation of the data and approved the final manuscript.

Role of the funding source

The funders had no role in the design of the study; the collection, analysis and interpretation of the data; the decision to submit for publication; or the writing of the manuscript. The views expressed in this publication are those of the authors and not necessarily those of the funders.

Conflict of interest statement

None declared.

Acknowledgements

This work was supported by a grant from the Bill and Melinda Gates Foundation (BMGF), USA, (Grant Number OPP1053353).

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