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Cervical cancer is the fourth most common cause of cancer death in women worldwide. Smoking is one of the risk factors for cervical cancer. Understanding the global distribution of the disease burden of cervical cancer attributable to smoking and related changes is of clear significance for the prevention and control of cervical cancer in key populations and for tobacco control. As far as we know, research on the burden of cervical cancer attributable to smoking is lacking.
We estimated the disease burden and mortality of cervical cancer attributable to smoking and related trends over time at the global, regional, and national levels.
Data were obtained from the Global Burden of Disease study website. Age-standardized rates were used to facilitate comparisons of mortality and disability-adjusted life years (DALYs) at different levels. The estimated annual percentage change (EAPC) was used to assess trends in the age-standardized mortality rate (ASMR) and the age-standardized DALY rate (ASDR). A Pearson correlation analysis was used to evaluate correlations between the sociodemographic index and the age-standardized rates.
In 2019, there were 30,136.65 (95% uncertainty interval [UI]: 14,945.09-49,639.87) cervical cancer–related deaths and 893,735.25 (95% UI 469,201.51-1,440,050.85) cervical cancer–related DALYs attributable to smoking. From 1990 to 2019, the global burden of cervical cancer attributable to smoking showed a decreasing trend around the world; the EAPCs for ASMR and ASDR were –2.11 (95% CI –2.16 to –2.06) and –2.22 (95% CI –2.26 to –2.18), respectively. In terms of age characteristics, in 2019, an upward trend was observed for age in the mortality of cervical cancer attributable to smoking. Analysis of the trend in DALYs with age revealed an initially increasing and then decreasing trend. From 1990 to 2019, the burden of disease in different age groups showed a downward trend. Among 204 countries, 180 countries showed downward trends, 10 countries showed upward trends, and the burden was stable in 14 countries. The Pearson correlation analysis revealed a significant negative correlation between sociodemographic index and the age-standardized rates of cervical cancer attributable to smoking (ρ=–0.228,
An increase over time in the absolute number of cervical cancer deaths and DALYs attributable to smoking and a decrease over time in the ASMR and ASDR for cervical cancer attributable to smoking were observed in the overall population, and differences in these variables were also observed between countries and regions. More attention should be paid to cervical cancer prevention and screening in women who smoke, especially in low- and middle-income countries.
Cervical cancer is the fourth most common cause of cancer death in women worldwide [
Among the above risk factors, we focus here on the influence of smoking. First, smoking is a known independent risk factor for cervical cancer. A meta-analysis of the results of 9 studies with a low risk of bias [
It is particularly important to pay attention to key groups of patients with cervical cancer [
The data used in this study were obtained from the 2019 GBD study, which provides a comprehensive and systematic assessment of the global burdens of 369 diseases, injuries, and impairments and 87 risk factors in 204 countries and territories during the 1990 to 2019 period. For this study, we extracted data on the burden of cervical cancer attributable to smoking, including mortality (calculated as the number of cervical cancer deaths × 100,000 / female population) [
In the current study, spatial division of the sample was achieved using 3 GBD division methods. The first method is based on the sociodemographic index (SDI), a comprehensive index used to measure the level of social development in a geographic area. The included countries and territories were divided by SDI into 5 superregions: low SDI, low-middle SDI, middle SDI, high-middle SDI, and high SDI. The second method involves dividing the world into 21 geographic regions according to epidemiological similarity and geographical proximity (eg, East Asia, Australasia, and Central Europe). The third method involves simple division by country and territory (for a total of 204 countries). Furthermore, the sample population of women aged 30 to 79 years was divided into 5-year age groups (eg, 30-34 years), and those aged 80 years and older were combined into one group, to yield 11 age groups.
According to the GBD risk factor collaborators [
In the GBD study, population data from the report
The estimated annual percentage change (EAPC) was used to assess trends in the ASMR and ASDR. The natural logarithm of the ASR was fitted to the following regression line model: ln (ASR) = α + βx + ɛ, where x is the calendar year. EAPCs and 95% CIs were derived from the following regression model: y = 100 × (exp (β) − 1), where y is the EAPC [
The methods used to estimate disease burdens from indicators in the GBD have been described previously [
This study was approved by the Ethics Committee of Scientific Research and Clinical Trials of the First Affiliated Hospital of Zhengzhou University (NO. 2020-KY-167).
Detailed results on the global burden of mortality and disability-adjusted life-years due to cervical cancer attributable to smoking in 1990 and 2019 and temporal trends from 1990 to 2019 are provided in
Overall, a decreasing trend was observed in the global burden of cervical cancer attributable to smoking over the studied period. The ASMR decreased from 1.28 per 100,000 (95% UI 0.65-2.06) in 1990 to 0.69 per 100,000 (95% UI 0.35-1.14) in 2019, a decrease of 85.5%, with an EAPC of –2.11 (95% CI –2.16 to –2.06) during this period. The ASDR also decreased from 39.31 per 100,000 (95% UI 21.03-62.13) in 1990 to 20.75 per 100,000 (95% UI 10.85-33.51) in 2019, with an EAPC of –2.22 (95% CI –2.26 to –2.18).
The global burden of death due to cervical cancer attributable to smoking in 1990 and 2019 and temporal trends from 1990 to 2019.
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1990 | 2019 | Estimated annual percentage change from 1990 to 2019 (95% CI) | |||||||||
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Deaths, n (95% UIa) | Age-standardized mortality rate, n × 10-5 (95% UI) | Deaths, n (95% UI) | Age-standardized mortality rate, n × 10-5 (95% UI) |
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Global burden | 27,421.87 (13,984.40 to 6721.02) | 1.28 (0.65 to 2.06) | 30,136.65 (14,945.09 to 49,639.87) | 0.69 (0.35 to 1.14) | –2.11 (–2.16 to –2.06) | |||||||
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Low | 1830.31 (847.48 to 3193.99) | 1.43 (0.67 to 2.47) | 2665.07 (1196.19 to 4655.28) | 0.95 (0.44 to 1.64) | –1.52 (–1.59 to –1.44) | ||||||
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Low-middle | 3986.82 (2018.69 to 6721.02) | 1.28 (0.64 to 2.13) | 5040.14 (2422.69 to 8955.89) | 0.69 (0.34 to 1.25) | –2.25 (–2.32 to –2.08) | ||||||
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Middle | 6434.95 (3243.32 to 10,665.85) | 1.19 (0.58 to 1.98) | 7557.27 (3565.50 to 13,116.97) | 0.57 (0.27 to 1.00) | –2.69 (–2.81 to –2.57) | ||||||
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High-middle | 7475.99 (3799.58 to 12,052.88) | 1.27 (0.65 to 2.04) | 8453.26 (4173.18 to 13,819.28) | 0.79 (0.40 to 1.29) | –1.52 (–1.61 to –1.43) | ||||||
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High | 7669.50 (3471.33 to 12,062.72) | 1.43 (0.68 to 2.22) | 6390.02 (2793.35 to 10,482.46) | 0.75 (0.34 to 1.19) | –2.17 (–2.28 to –2.05) |
aUI: uncertainty interval.
The global burden of disability-adjusted life-years due to cervical cancer attributable to smoking in 1990 and 2019 and temporal trends from 1990 to 2019.
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1990 | 2019 | Estimated annual percentage change from 1990 to 2019 (95% CI) | ||||||||
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DALYsa, n (95% UIb) | Age-standardized DALY rate, n × 10-5 (95% UI) | DALYs, n (95% UI) | Age-standardized DALY rate, n × 10-5 (95% UI) |
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Global burden | 863,494.73 (464,325.44 to 1,365,563.86) | 39.31 (21.03 to 62.13) | 893,735.25 (469,201.51 to 1,440,050.85) | 20.75 (10.85 to 33.51) | –2.22 (–2.26 to –2.18) | ||||||
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Low | 61,306.72 (26,248.83 to 107,671.43) | 43.51 (19.69 to 76.28) | 85,793.88 (34,342.57 to 153,086.77) | 27.53 (11.86 to 48.17) | –1.68 (–1.76 to –1.69) | |||||
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Low-middle | 127,334.6 (64,663.76 to 208,130.21) | 37.08 (18.61 to 61.43) | 150,971.38 (71,542.69 to 275,063.88) | 19.69 (9.37 to 35.44) | –2.32 (–2.44 to –2.19) | |||||
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Middle | 197,494.21 (103,798.33 to 328,143.85) | 33.63 (17.30 to 55.60) | 216,363.48 (107,107.20 to 372,743.62) | 15.65 (7.73 to 26.95) | –2.75 (–2.85 to –2.66) | |||||
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High-middle | 242,456.35 (131,242.40 to 377,394.25) | 41.44 (22.49 to 64.40) | 260,369.48 (137,295.16 to 409,749.35) | 25.66 (13.93 to 40.26) | –1.58 (–1.66 to –1.49) | |||||
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High | 234,111.80 (117,412.53 to 360,250.81) | 46.78 (24.10 to 70.67) | 179,289.26 (85,852.04 to 285,069.42) | 23.88 (12.15 to 36.84) | –2.27 (–2.38 to –2.16) |
aDALY: disability-adjusted life-year.
bUI: uncertainty interval.
Analysis of the 5 superregions divided by SDI revealed that the absolute number of cervical cancer deaths attributable to smoking ranged from 2665.07 (95% UI 1196.19-4655.28) in the low-SDI region to 8453.26 (95% UI 4173.18-13,819.28) in the high-middle–SDI region. The lowest and highest absolute numbers of DALYs were 85,793.88 (95% UI 34,342.57-153,086.77) in the low-SDI region and 260,369.48 (95% UI 137,295.16-409,749.35) in the high-middle–SDI region, respectively.
The highest ASMR and ASDR values were 0.95 per 100,000 (95% UI 0.44-1.64) and 27.53 per 100,000 (95% UI 11.86-48.17), respectively, in the low-SDI region, and the lowest ASMR and ASDR values were 0.6 per 100,000 (95% UI 0.35-1.14) and 15.65 per 100,000 (95% UI 7.73-26.95), respectively, in the middle-SDI region.
Downward trends in the ASMR and ASDR were observed in all 5 SDI superregions from 1990 to 2019. The largest declines were observed in the middle-SDI region, with EAPCs of –2.69 (95% CI –2.81 to –2.57) and –2.75 (95% CI –2.85 to –2.66) for the ASMR and ASDR, respectively. The smallest declines in the ASMR and ASDR were observed in the low-SDI and high-middle–SDI regions, respectively, with EAPCs of –1.51 (95% CI –1.59 to –1.44) and –1.58 (95% CI –1.66 to –1.49).
Among the 21 geographic regions, the largest absolute numbers of cervical cancer–related deaths and DALYs attributable to smoking in 2019 were observed in East Asia, and the smallest absolute numbers were observed in Oceania. In the same year, the highest ASMR was 2.84 per 100,000 (95% CI 1.33-5.01), and the highest ASDR was 95.03 per 100,000 (95% CI 52.82-142.33), observed in Oceania and southern Latin America, respectively, whereas the lowest ASMR was 0.23 per 100,000 (95% CI 0.09-0.43), and the lowest ASDR was 6.71 per 100,000 (95% CI 3.05-11.69), observed in North Africa and the Middle East, respectively.
Downward trends in the cervical cancer burden attributable to smoking were observed in most geographic regions from 1990 to 2019. The largest decrease was observed in Central Latin America, with an EAPC of –4.52 (95% CI –4.73 to –4.30) for the ASMR, and in tropical Latin America, with an EAPC of –4.38 (95% CI –4.58 to –4.17) for the ASDR. In contrast, an upward trend was observed in Eastern Europe, with EAPCs of 0.76 (95% CI 0.45-1.07) and 1.2 (95% CI 0.85-1.55) for the ASMR and ASDR, respectively.
In 2019, the highest ASMR of cervical cancer attributable to smoking across all 204 included countries and territories was 483.2 times the lowest ASMR; the highest value of 24.16 per 100,000 (95% CI 13.27-38.83) was observed in Kiribati, and the lowest value of 0.05 per 100,000 (95% CI 0.02-0.11) was observed in Egypt. Kiribati and Egypt also had the highest and lowest ASDRs, at 734.33 per 100,000 (95% CI 385.97-1,184.35) and 1.17 per 100,000 (95% CI 0.39-2.57), respectively.
A downward trend in the ASMR of cervical cancer attributable to smoking was observed in most countries over time (ie, the EAPC was less than zero and the upper limit of the 95% CI was less than zero), with the strongest trends observed in Mexico, Thailand, Singapore, the Maldives, and Denmark. In contrast, upward trends in the ASMR (ie, the EAPC was greater than zero and the lower limit of the 95% CI was greater than zero) were observed in 10 countries over time (listed in descending order according to the EAPC value): Lesotho, the Russian Federation, Bulgaria, Afghanistan, Albania, Uzbekistan, Italy, Kyrgyzstan, Bosnia and Herzegovina, and Guinea-Bissau. In addition, 16 countries showed stable ASMR over time (the 95% CI included zero). Similarly, downward trends in the ASDR were observed in most countries over time. However, upward trends were observed in Lesotho, the Russian Federation, Bulgaria, Afghanistan, Albania, Uzbekistan, Italy, Kyrgyzstan, Bosnia and Herzegovina, and the Democratic People’s Republic of Korea, while ASDR was stable in 14 countries.
The global distribution of ASMRs of cervical cancer attributable to smoking in 2019. ASMR: age-standardized mortality rate.
The global distribution of ASDRs of cervical cancer attributable to smoking in 2019. ASDR: age-standardized disability-adjusted life-year rate.
EAPCs in the ASMR of cervical cancer attributable to smoking by country from 1990 to 2019. EAPC: estimated annual percentage change; ASMR: age-standardized mortality rate.
EAPCs in the ASDR of cervical cancer attributable to smoking by country from 1990 to 2019. EAPC: estimated annual percentage change; ASDR: age-standardized disability-adjusted life-year rate.
In 2019, an upward trend was observed in the mortality of cervical cancer attributable to smoking with age. The highest mortality rate was observed in the population older than 80 years, except for a low value in the group aged 75 to 79 years (
Figures S3 and S4 in
Figures S5 and S6 in
Our study estimated time trends in the burden of cervical cancer attributable to smoking from 1990 to 2019 at the global, regional, and national levels. In terms of spatial distribution, the worldwide distribution of this burden in 2019 was quite different in each country and region. In terms of time trends, 10 countries showed increasing trends from 1990 to 2019 and 14 countries were stable. These countries were distributed in Europe, Central Asia, and South Africa; other countries and regions showed decreasing trends.
The burden of cervical cancer related to smoking in the whole population showed an increase in the absolute number of cases and a decrease over time for the ASMR and ASDR, as well as differences in different countries and regions. This may be related, first, to the distribution characteristics of female smokers and female smoking rates around the world. Global smoking prevalence among women aged 15 years or older declined by 37.7% in 2019 compared with 1990, but population growth led to an increase in the total number of female smokers. There were 146 million current female smokers aged 30 years or older in 2019. At the same time, the prevalence of smoking among women aged 15 years or older varied greatly in different countries and regions, with the age-standardized prevalence of smoking tobacco use ranging from 0.696% in Eritrea to 42.3% in Greenland [
Second, the implementation of tobacco control measures may also have affected the spatial distribution characteristics and temporal trends of the burden of cervical cancer attributable to smoking. In 2005, the World Health Organization (WHO) Framework Convention on Tobacco Control (FCTC) entered into force [
Tobacco control is one of the most important cancer prevention behaviors. However, for smokers, a focus on cancer screening has the greatest potential benefit because it allows the timely detection of disease and early intervention [
According to our study, the distribution of and trends in the burden of cervical cancer attributable to smoking also differed in different age groups. Mortality due to cervical cancer related to smoking increases with age, which may be related to longer exposure to smoking [
The results of this study show that the level of socioeconomic development is correlated with the burden of cervical cancer attributable to smoking and trends in this burden. First, countries or regions with different economic development levels have different levels of burden of cervical cancer attributable to smoking. In 2019, this burden was mainly concentrated in low- and middle-SDI countries in southern Africa, South America, and Asia. This is consistent with the global distribution of the overall burden of cervical cancer; 86% of the global burden of cervical cancer is in Africa, Latin America and the Caribbean, and Asia [
This study has some limitations. First, the availability of certain data on the disease burden of cervical cancer attributable to smoking in low-income countries is poor, while the GBD study relied heavily on existing epidemiological studies to estimate global disease prevalence. However, all national data calculation standards were consistent, so data quality was guaranteed. Second, the GBD study did not present data on the disease burden of cervical cancer from second-hand smoke (ie, household or occupational exposure), which is an important mode of tobacco exposure in women. If this risk factor were taken into account, the disease burden of cervical cancer due to tobacco would be higher than the current estimate, and the trend might also be different. Third, we only estimated the burden of cervical cancer attributable to smoking, but the combined effects of smoking and other risk factors may increase or complicate the burden of cervical cancer.
The distribution of the disease burden of cervical cancer attributable to smoking and trends in this burden differ in different countries and regions of the world. More attention should be paid to cervical cancer prevention and screening in women who smoke, especially in low- and middle-income countries.
The global burden and mortality of cervical cancer attributable to smoking in 1990 and 2019 and temporal trends from 1990 to 2019 (Geographic Regions).
Age-specific rates of global cervical cancer deaths attributable to smoking in 2019.
Age-specific rates of global cervical cancer DALYs attributable to smoking in 2019. DALY: disability-adjusted life-year.
EAPCs in ASMR of cervical cancer attributable to smoking by age group from 1990 to 2019. EAPC: estimated annual percentage change; ASMR: age-standardized mortality rate.
EAPCs in ASDR of cervical cancer attributable to smoking by age group from 1990 to 2019. EAPC: estimated annual percentage change; ASDR: age-standardized disability-adjusted life-year rate.
The correlations between the SDI index and EAPCs of the ASMR. ASMR: age-standardized mortality rate; EAPC: estimated annual percentage change.
The correlations between the SDI index and EAPCs of the ASDR. ASDR: age-standardized disability-adjusted life-year rate; EAPC: estimated annual percentage change.
age-standardized disability-adjusted life-year rate
age-standardized mortality rate
age-standardized rate
disability-adjusted life-year
estimated annual percentage change
Framework Convention on Tobacco Control
Global Burden of Disease
sociodemographic index
uncertainty interval
World Health Organization
This work was supported by grants from the Medical Science and Technology Research Plan Joint Construction Project of Henan Province (LHGJ20190223).
The datasets generated and analyzed during this study are available in the Global Burden of Disease (GBD) study 2019 data repository (https://ghdx.healthdata.org/gbd-results-tool).
All authors contributed to the study conception and design. Data curation was performed by FR and KL. RY and YX rechecked the data. Statistical analysis and data visualization were performed by RY and ZT. The original draft of the manuscript was written by RY. Review and editing of the manuscript were performed by FR and ZT.
None declared.