Successes and Barriers of HPV Vaccination and Cervical Screening on Cervical Cancer Elimination

A special issue of Cancers (ISSN 2072-6694). This special issue belongs to the section "Cancer Epidemiology and Prevention".

Deadline for manuscript submissions: closed (30 September 2022) | Viewed by 24457

Special Issue Editor


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Guest Editor
Department of Epidemiology, School of Public Health, University of Alabama at Birmingham, Birmingham, AL, USA
Interests: HPV; cervical cancer; HPV-associated cancer; genetic and genomics; HIV and comorbidities; Kawasaki Disease; Infection and immune related diseases

Special Issue Information

Dear colleagues,

Cervical cancer is the fourth most common cancer in women, with over 570,000 new cases a year. The primary cause of cervical pre-cancer and cancer is infection with a high-risk or oncogenic human papillomavirus (HPV). Cervical cancer is a preventable disease, with several strategies for prevention and treatment, but it is mostly prevented through vaccination efforts and is curable if detected early at pre-cancer stages. In November 2020, WHO announced the “Global strategy to accelerate the elimination of cervical cancer as a public health problem”. It has suggested vaccinating 90 percent of girls against multiple strains of HPV by 15 years of age, screening 70 percent of women for cervical cancer at ages 35 and 45, and giving care to 90 percent of women with cervical pre-cancer lesions or cancer (90-70-90) targets to meet the cervical cancer elimination goal by 2030. However, there are global inequities with cervical cancer, which is a direct reflection of disparities in vaccination and screening in middle- and low-income countries. While some countries have already made great strides toward meeting these goals, others have many barriers and challenges.

The Special Issue will include a selection of high-quality articles that report and discuss the successes and barriers with cervical cancer prevention and screen-and-treat approaches in various settings and regions of the world. We expect that this unique effort will facilitate interaction and collaboration between stakeholders at national levels, including public health leaders, scientists, and political leaders in different countries with the common goal of eliminating cervical cancer.

Prof. Sadeep Shrestha
Guest Editor

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Keywords

  • cervical cancer
  • vaccination
  • HPV
  • screening
  • pre-cancer treatment
  • public health
  • human papillomavirus

Published Papers (10 papers)

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Research

16 pages, 567 KiB  
Article
Results from Two HPV-Based Cervical Cancer Screening-Family Planning Integration Models in Malawi: A Cluster Randomized Trial
by Jennifer H. Tang, Fan Lee, Maganizo B. Chagomerana, Kachengwa Ghambi, Patani Mhango, Lizzie Msowoya, Tawonga Mkochi, Irene Magongwa, Eneli Mhango, Jacqueline Mbendera, Eunice Mwandira, Erik Schouten, Leah Gardner, Jennifer S. Smith, Luis Gadama and Lameck Chinula
Cancers 2023, 15(10), 2797; https://doi.org/10.3390/cancers15102797 - 17 May 2023
Cited by 1 | Viewed by 1406
Abstract
We conducted a cluster randomized trial of two models for integrating HPV self-collection into family-planning (FP) services at 16 health facilities in Malawi between March 2020–December 2021. Model 1 involved providing only clinic-based HPV self-collection, whereas Model 2 included both clinic-based and community-based [...] Read more.
We conducted a cluster randomized trial of two models for integrating HPV self-collection into family-planning (FP) services at 16 health facilities in Malawi between March 2020–December 2021. Model 1 involved providing only clinic-based HPV self-collection, whereas Model 2 included both clinic-based and community-based HPV self-collection. An endline household survey was performed in sampled villages and households between October-December 2021 in the catchment areas of the health facilities. We analyzed 7664 surveys from 400 villages. Participants from Model 2 areas were more likely to have ever undergone cervical cancer screening (CCS) than participants from Model 1 areas, after adjusting for district, facility location (urban versus rural), and facility size (hospital versus health center) (adjusted odds ratio = 1.73; 95% CI: 1.29, 2.33). Among participants who had ever undergone CCS, participants from Model 2 were more likely to report having undergone HPV self-collection than participants from Model 1 (50.5% versus 22.8%, p = 0.023). Participants from Model 2 were more likely to be using modern FP (adjusted odds ratio = 1.01; 95% CI: 1.41, 1.98) than Model 1 participants. The integration of FP and HPV self-collection in both the clinic and community increases CCS and modern FP uptake more than integration at the clinic-level alone. Full article
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15 pages, 1692 KiB  
Article
Cervical Cancer Screening and Associated Barriers among Women in India: A Generalized Structural Equation Modeling Approach
by Nilima Nilima, Kalaivani Mani, Siddharth Kaushik and Shesh Nath Rai
Cancers 2022, 14(13), 3076; https://doi.org/10.3390/cancers14133076 - 23 Jun 2022
Cited by 2 | Viewed by 2204
Abstract
Exploring the barriers and facilitators of cervical cancer screening (CCS) is essential to reduce the incidence and mortality, particularly in low and middle-income countries. The present study investigates the direct, indirect, and total effects of the barriers and facilitators on CCS in India [...] Read more.
Exploring the barriers and facilitators of cervical cancer screening (CCS) is essential to reduce the incidence and mortality, particularly in low and middle-income countries. The present study investigates the direct, indirect, and total effects of the barriers and facilitators on CCS in India through the generalized structural equation modeling using data from women files of the fourth round of the National Family Health Survey (NFHS-4). Generalized structural equation models were used to quantify the hypothetical pathway via fitting a series of regression equations. Age, body mass index, religion, years of schooling, awareness of sexually transmitted infection, contraception use, lifetime number of sex partners, number of children, and wealth index were shown to have significant direct effects on the CCS. Older women had 1.16 times the odds of getting screened for cervical cancer as compared to their younger counterpart. The odds of CCS among the women in richest wealth quintile is 2.50 times compared to the poorest. Those who are aware of STIs have 1.39 times the odds of getting screened for cervical cancer. Wealth index, years of schooling, and religion have a substantial indirect and total impact on the CCS. The findings will aid in policy formulations for enhancing the CCS in India. Full article
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8 pages, 688 KiB  
Article
Cervical Cancer Prevention in El Salvador: Gains to Date and Challenges for the Future
by Karla Alfaro, Montserrat Soler, Mauricio Maza, Mauricio Flores, Leticia López, Juan C. Rauda, Andrea Chacón, Patricia Erazo, Nora Villatoro, Eveline Mumenthaler, Rachel Masch, Gabriel Conzuelo, Juan C. Felix and Miriam Cremer
Cancers 2022, 14(11), 2776; https://doi.org/10.3390/cancers14112776 - 3 Jun 2022
Cited by 3 | Viewed by 2146
Abstract
Cervical cancer is preventable through vaccination, early detection, and the treatment of pre-cancerous lesions. However, global inequalities mean that the disease remains a leading cause of cancer death around the world, with over 80% of new cases and 90% of deaths occurring in [...] Read more.
Cervical cancer is preventable through vaccination, early detection, and the treatment of pre-cancerous lesions. However, global inequalities mean that the disease remains a leading cause of cancer death around the world, with over 80% of new cases and 90% of deaths occurring in low- and middle-income countries (LMICs). In El Salvador, joint efforts between the Ministry of Health (MoH) and the non-profit organization Basic Health International (BHI) have been in place since 2008, with the goal of reducing the country’s disease burden. While the World Health Organization’s (WHO) call to action to eliminate cervical cancer provided worldwide momentum to implement new public health initiatives, the COVID-19 pandemic disrupted ongoing programs and jeopardized plans for the future. The purpose of this manuscript is to describe the progress that El Salvador has achieved in improving cervical cancer prevention, the impact of the pandemic on current strategies, and potential solutions that can help the country meet the WHO’s strategic targets by 2030 to accelerate the elimination of cervical cancer. Full article
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15 pages, 1290 KiB  
Article
Trends and Determinants in Uptake of Cervical Cancer Screening in Spain: An Analysis of National Surveys from 2017 and 2020
by Silvia Portero de la Cruz and Jesús Cebrino
Cancers 2022, 14(10), 2481; https://doi.org/10.3390/cancers14102481 - 18 May 2022
Cited by 1 | Viewed by 2414
Abstract
Cervical cancer rates have declined in industrialized nations as a result of cytology screening programs. However, there are still sizeable differences in screening adherence in Spain. This study aimed to identify the prevalence of cervical cancer screening among women in Spain, to analyze [...] Read more.
Cervical cancer rates have declined in industrialized nations as a result of cytology screening programs. However, there are still sizeable differences in screening adherence in Spain. This study aimed to identify the prevalence of cervical cancer screening among women in Spain, to analyze trends in that prevalence from 2017 and 2020 and to identify socio-demographic, health, and lifestyle factors related with adherence to this screening test. We conducted a cross-sectional study of 13,619 women aged 25–65 who participated in the 2017 Spanish National Health Survey and the 2020 European Health Survey for Spain. We used logistic regression to examine the relationship between socio-demographic, health and lifestyle factors and cervical cancer adherence. The prevalence of adherence was 73.18%. Additionally, there was a significant decrease in cervical cancer screening uptake from 2017 and 2020 among women aged 25–44 years (2017: 77.80%, 2020: 75.20%, p = 0.02), but an increase in the age group of 45–65 years (2017: 68.93%, 2020: 72.39%, p < 0.01) and in foreigners (2017: 64.29%, 2020: 72.29%, p < 0.01). Screening for cervical cancer is related with age, educational level, social class, insurance status, visits to the family doctor, alcohol consumption and free time physical exercise. Full article
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20 pages, 5118 KiB  
Article
Assessing the Acceptability of Home-Based HPV Self-Sampling: A Qualitative Study on Cervical Cancer Screening Conducted in Reunion Island Prior to the RESISTE Trial
by Dolorès Pourette, Amber Cripps, Margaux Guerrien, Caroline Desprès, Eric Opigez, Marc Bardou and Alexandre Dumont
Cancers 2022, 14(6), 1380; https://doi.org/10.3390/cancers14061380 - 8 Mar 2022
Cited by 7 | Viewed by 2369
Abstract
Cervical cancer incidence and mortality rates are 2 to 3 times higher in the overseas department of Reunion compared with mainland France. RESISTE’s cluster-randomized controlled trial aims to test the effectiveness of home-based self-sampling (HBSS) through a high-risk oncogenic papillomavirus test sent out [...] Read more.
Cervical cancer incidence and mortality rates are 2 to 3 times higher in the overseas department of Reunion compared with mainland France. RESISTE’s cluster-randomized controlled trial aims to test the effectiveness of home-based self-sampling (HBSS) through a high-risk oncogenic papillomavirus test sent out by post to women who have not been screened in the past 3 years, despite having been invited to do so through a reminder letter. Prior to the trial, qualitative research was carried out to understand screening barriers and assess anticipated acceptability. Semi-structured interviews were conducted with 35 women and 20 healthcare providers. Providers consider HBSS a viable method in reaching women who tend not to visit a doctor regularly, or who are reluctant to undergo a smear pap, as well as those who are geographically isolated. They considered, however, that women would require support, and that outreach was necessary to ensure more socially isolated women participate. The majority of the women surveyed were in favour of HBSS. However, two-thirds voiced concerns regarding the test’s efficiency and their ability to perform the test correctly, without harming themselves. Based on these findings, recommendations were formulated to reassure women on usage and quality, and to help reach socially isolated women. Full article
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11 pages, 411 KiB  
Article
An Intersectional Perspective on the Utilization of Cervical Cancer Screening among Migrants. A Cross-Sectional Analysis of Survey Data from Austria
by Patrick Brzoska, Diana Wahidie and Yüce Yilmaz-Aslan
Cancers 2021, 13(23), 6082; https://doi.org/10.3390/cancers13236082 - 2 Dec 2021
Cited by 4 | Viewed by 1859
Abstract
In most European countries, migrant women have lower rates of cervical cancer screening utilization than non-migrant women. While studies have illustrated that disparities can be partially explained by social determinants, they usually did not take into account the heterogeneity of the migrant population [...] Read more.
In most European countries, migrant women have lower rates of cervical cancer screening utilization than non-migrant women. While studies have illustrated that disparities can be partially explained by social determinants, they usually did not take into account the heterogeneity of the migrant population in terms of cultural background or country of origin. Applying an intersectional approach and using 2019 data from a representative survey from Austria on 6228 women aged 20–69 years, the present study examines differences in the utilization of cervical cancer screening in the five largest migrant groups (i.e., individuals with a nationality from or born in a Yugoslav successor state, Turkey, Romania, Hungary, or Germany) residing in Austria. By means of a multivariable analysis, amongst others adjusted for socioeconomic and health-related determinants, it is illustrated that particularly Turkish migrant women have a lower utilization than the Austrian majority population (adjusted odds ratio (OR) = 0.60; 95% confidential interval (CI): 0.40–0.91), while no significant differences between the majority population and other groups of migrants became evident. The findings are indicative of the heterogeneity of migrants and likely result from different obstacles some groups of migrants encounter in the health system. This heterogeneity must be taken into account in order to support informed decision-making and to ensure adequate preventive care. Full article
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16 pages, 2248 KiB  
Article
Quantifying the Effects of Medical Examination and Possible Risk Factors against the Incidence of Cervical Cancer in a Low Human Papillomavirus Vaccination Coverage: An Ecological Study in Japan
by Yueming Yu, Ryota Matsuyama, Miwako Tsunematsu and Masayuki Kakehashi
Cancers 2021, 13(19), 4784; https://doi.org/10.3390/cancers13194784 - 24 Sep 2021
Viewed by 2678
Abstract
Cervical cancer (CC) is one of the most common gynecological malignancies in females, mainly caused by human papillomavirus (HPV). In countries with lower HPV vaccine coverage, such as Japan, medical examination may play a key role in decreasing CC incidence. This study aimed [...] Read more.
Cervical cancer (CC) is one of the most common gynecological malignancies in females, mainly caused by human papillomavirus (HPV). In countries with lower HPV vaccine coverage, such as Japan, medical examination may play a key role in decreasing CC incidence. This study aimed to quantify the effect of medical examination on cervical cancer (CC) incidence in Japan, considering the effects of possible risk factors. By collecting Japan’s Prefectural data on CC incidence (2013–2017), incidence of sexually transmitted diseases (STDs; Chlamydia, Herpes, Condyloma, and Gonorrhea; 1993–2012), screening and detailed examination rate against CC (2013–2016), smoking rate (2001–2013), economic status (disposable income and economic surplus; 2014–2015), and education status (2015), we analyzed associations among them using Pearson’s correlation coefficients. Additionally, assuming that the incidence of STDs reflects the frequency of risky sexual behavior at the co-infection point with HPV, we constructed generalized linear models to predict CC incidence, taking a 5–20-year time-lag between incidences of STDs and the CC incidence. Against CC incidence, Chlamydia in females and Gonorrhea in males with a 15-year time-lag showed positive associations, while Condyloma in both genders with a 15-year time-lag, screening rate, economic status, and smoking rate showed negative associations. An increase in screening test rate by 10% was estimated to decrease CC incidence by 9.6%. This means that screening tests decrease CC incidence effectively, but not drastically, suggesting the need for additional countermeasures for CC prevention. Full article
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16 pages, 2071 KiB  
Article
The Impact of the Human Papillomavirus Vaccine on High-Grade Cervical Lesions in Urban and Rural Areas: An Age–Period–Cohort Analysis
by Jaimie Z. Shing, Alicia Beeghly-Fadiel, Marie R. Griffin, Rachel S. Chang, Staci L. Sudenga, James C. Slaughter, Manideepthi Pemmaraju, Edward F. Mitchel and Pamela C. Hull
Cancers 2021, 13(16), 4215; https://doi.org/10.3390/cancers13164215 - 21 Aug 2021
Cited by 3 | Viewed by 2731
Abstract
Disparities in human papillomavirus (HPV) vaccination exist between urban (metropolitan statistical areas (MSAs)) and rural (non-MSAs) regions. To address whether the HPV vaccine’s impact differs by urbanicity, we examined trends in cervical intraepithelial neoplasia grades 2 or 3 and adenocarcinoma in situ (collectively, [...] Read more.
Disparities in human papillomavirus (HPV) vaccination exist between urban (metropolitan statistical areas (MSAs)) and rural (non-MSAs) regions. To address whether the HPV vaccine’s impact differs by urbanicity, we examined trends in cervical intraepithelial neoplasia grades 2 or 3 and adenocarcinoma in situ (collectively, CIN2+) incidence in MSAs and non-MSAs among Tennessee Medicaid (TennCare)-enrolled women aged 18–39 years and among the subset screened for cervical cancer in Tennessee, United States. Using TennCare claims data, we identified annual age-group-specific (18–20, 21–24, 25–29, 30–34, and 35–39 years) CIN2+ incidence (2008–2018). Joinpoint regression was used to identify trends over time. Age–period–cohort Poisson regression models were used to evaluate age, period, and cohort effects. All analyses were stratified by urbanicity (MSA versus non-MSA). From 2008–2018, 11,243 incident CIN2+ events (7956 in MSAs; 3287 in non-MSAs) were identified among TennCare-enrolled women aged 18–39 years. CIN2+ incident trends (2008–2018) were similar between women in MSAs and non-MSAs, with largest declines among ages 18–20 (MSA average annual percent change (AAPC): −30.4, 95% confidence interval (95%CI): −35.4, −25.0; non-MSA AAPC: −30.9, 95%CI: −36.8, −24.5) and 21–24 years (MSA AAPC: −14.8, 95%CI: −18.1, −11.3; non-MSA AAPC: −15.1, 95%CI: −17.9, −12.2). Significant declines for ages 18–20 years began in 2008 in MSAs compared to 2010 in non-MSAs. Trends were largely driven by age and cohort effects. These patterns were consistent among screened women. Despite evidence of HPV vaccine impact on reducing CIN2+ incidence regardless of urbanicity, significant declines in CIN2+ incidence were delayed in non-MSAs versus MSAs. Full article
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13 pages, 620 KiB  
Article
Sociodemographic Correlates of Human Papillomavirus Vaccine Uptake: Opportunistic and Catch-Up Vaccination in Norway
by Li Dong, Mari Nygård and Bo T. Hansen
Cancers 2021, 13(14), 3483; https://doi.org/10.3390/cancers13143483 - 12 Jul 2021
Cited by 11 | Viewed by 2499
Abstract
Achieving equity in human papillomavirus (HPV) vaccination has high priority. In this nationwide registry-based study, we aimed to investigate sociodemographic correlates of HPV vaccine uptake among women who were vaccinated opportunistically at their own initiative and cost during October 2006–June 2018, and among [...] Read more.
Achieving equity in human papillomavirus (HPV) vaccination has high priority. In this nationwide registry-based study, we aimed to investigate sociodemographic correlates of HPV vaccine uptake among women who were vaccinated opportunistically at their own initiative and cost during October 2006–June 2018, and among women who were vaccinated free-of-charge in a catch-up vaccination program during November 2016–June 2018. For 840,328 female residents born in Norway between 1975 and 1996, we retrieved HPV vaccination and sociodemographic data from national registries. We used separate models to analyze the sociodemographic correlates of the initiation and completion of HPV vaccination in opportunistic and catch-up vaccination settings. Overall initiation rate for opportunistic HPV vaccination was 2.2%. Uptake increased consistently with birth year, maternal education level, and household income. Having two immigrant parents or a mother working in a lower prestige occupation was strongly associated with low opportunistic vaccination uptake. Similar but weaker inequities were observed in catch-up HPV vaccination. Initiation rate during the first 20 months of the catch-up program was 46.2%. Completion rate was 72.1% and 73.0% for opportunistic or catch-up vaccination, respectively, with small inequities. In conclusion, HPV vaccine uptake was strongly associated with sociodemographic background both in opportunistic and catch-up vaccination settings, with particularly low uptake associated with having two immigrant parents and low household income. Full article
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11 pages, 3473 KiB  
Article
Colposcopic Impression Has a Key Role in the Estimation of the Risk of HSIL/CIN3
by Marta del Pino, Martina Aida Angeles, Cristina Martí, Carla Henere, Meritxell Munmany, Lorena Marimon, Adela Saco, Natalia Rakislova, Jaume Ordi and Aureli Torné
Cancers 2021, 13(6), 1224; https://doi.org/10.3390/cancers13061224 - 11 Mar 2021
Cited by 8 | Viewed by 2156
Abstract
Recently published guidelines stratify the risk of high-grade squamous intraepithelial lesion/grade 3 cervical intraepithelial neoplasia (HSIL/CIN3) based on hrHPV detection and Pap smear results. However, colposcopic impression could also provide valuable information for risk estimation. We aimed to analyze the value of adding [...] Read more.
Recently published guidelines stratify the risk of high-grade squamous intraepithelial lesion/grade 3 cervical intraepithelial neoplasia (HSIL/CIN3) based on hrHPV detection and Pap smear results. However, colposcopic impression could also provide valuable information for risk estimation. We aimed to analyze the value of adding colposcopic impression to screening tests for the diagnosis of HSIL/CIN3 in 302 women referred for colposcopy due to an abnormal Pap smear. All women underwent hrHPV detection and genotyping (HPV 16/18 vs. non-16/18 hrHPV), Pap smear, and colposcopy with at least one biopsy. HSIL Pap smear, HPV 16/18, and grade 2 colposcopy findings increased the risk of HSIL/CIN3 in the univariate analysis but only colposcopy retained significance in the multivariate model. At least 30% of the women with grade 2 colposcopy findings had HSIL/CIN3, independent of the screening test results. Among women with an HSIL Pap smear and grade 2 colposcopy findings, 53.3% had HSIL/CIN3 independently of the hrHPV genotype. Contrarily, the prevalence of HSIL/CIN3 in women with <HSIL Pap smear, non-HPV 16/18 infection, and normal colposcopy or with grade 1 findings was 2.9% and 8.1%, respectively. In conclusion, colposcopy impression provides essential information to identify women at risk of HSIL/CIN3. Full article
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