Evaluating the global prevalence of HPV16 and HPV18 in cervical lesions and normal cytology

Introduction

Human Papillomavirus (HPV) infection is common in the anogenital tract, affecting both symptomatic and asymptomatic individuals regardless of sex. HPV is well-known for its connection to cervical cancer in women, but it also plays a significant role in other anogenital sites and contributes to conditions like recurrent juvenile respiratory papillomatosis and genital warts. Prevalence of HPV infection increases with the severity of cervical lesions, with nearly 100% of cervical cancer cases attributed to HPV. However, the actual prevalence may be underestimated due to limitations in detection methods and study designs.

Globally, HPV-16 and HPV-18, which can be prevented through vaccination, account for 70-80% of low-grade cervical lesions, while six other prevalent HPV types (31, 33, 35, 45, 52, and 58) collectively contribute to an additional 20% of cervical cancers worldwide. A systematic review was conducted to assess the global prevalence and type distribution of HPV in different cervical conditions, using PCR or HC2 methods to detect HPV DNA. The review provided estimates of HPV prevalence and type distribution globally and by geographic region, but caution should be exercised in interpreting the findings due to the limitations of the methods and study designs used.

Aim

The aim of this study is to investigate the global prevalence of HPV16 and HPV18 in cervical carcinoma, low-grade cervical lesions, high-grade cervical lesions, and normal cytology.

Significance of the Study

The significance of this study lies in its ability to provide crucial insights into the global prevalence HPV16 and HPV18 in various cervical conditions. By identifying the most prevalent HPV types and their association with cervical carcinoma, low-grade cervical lesions, high-grade cervical lesions, and normal cytology, the study informs public health planning, vaccination strategies, screening and diagnosis methods, and understanding regional variances.

Objectives

  1. Determine the global prevalence of HPV16 and HPV18 in cervical carcinoma, low-grade cervical lesions, high-grade cervical lesions, and normal cytology.

  2. Assess the distribution of HPV types, both globally and by geographical region, in cervical carcinoma, low-grade cervical lesions, high-grade cervical lesions, and normal cytology, based on the identified HPV DNA and genotyping techniques used in the studies.

Materials and Methods

A comprehensive systematic review was conducted to investigate the global prevalence HPV16 abd HPV18 in cervical carcinoma, low-grade cervical lesions, high-grade cervical lesions, and normal cytology. The review encompassed studies published from 1990 to the latest available data indicated in each respective section. The search strategy involved querying the PubMed database using the search terms ‘HPV’ AND ’cerv*’ without any language restrictions. Additionally, the reference lists of selected articles were scrutinized to identify further relevant studies.

Inclusion criteria for studies encompassed HPV DNA detection using polymerase chain reaction (PCR) or Hybrid Capture 2 (HC2) methods, a minimum of 20 cases for cervical carcinoma, 20 cases for low-grade cervical lesions, 20 cases for high-grade cervical lesions, and 100 cases for normal cytology. Furthermore, studies were required to provide a detailed description of the HPV DNA detection and genotyping techniques employed. The number of cases tested and the number of HPV-positive cases were pooled to estimate the global prevalence of HPV DNA and the distribution of HPV types, both globally and by geographical region. Binomial 95% confidence intervals were calculated to determine the precision of the estimated HPV prevalences. For a more comprehensive understanding of the methodology, please refer to the cited study.

Statistical analysis

The dataset was initially processed using Microsoft Excel 2019 v16.0, and subsequently subjected to statistical analysis using R software version 4.4.0 and RStudio version 2024.4.0.735, courtesy of the Posit team (2024). The following packages were employed: tidyverse, readxl, ggstatsplot, easystats, DT, leaflet, and leaflet.extras. Descriptive analysis was conducted to calculate summary statistics, including median, interquartile range (IQR), frequencies, and proportions of the variables. To compare the prevalence of HPV among participants across different continents, non-parametric tests were employed, specifically Wilcoxon’s rank sum test and Kruskal-Wallis test. Post hoc analysis was performed using Dunn’s test. To mitigate the risk of type I errors arising from multiple hypothesis testing, a correction for multiple comparisons was applied using Holm’s method, a sequential Bonferroni procedure that adjusts the significance level for each test in a step-down manner. This method ensures that the family-wise error rate (FWER) is controlled, thereby maintaining the overall significance level at 0.05. Specifically, the p-values were adjusted using Holm’s method, thereby controlling the FWER and preventing the inflation of type I errors. A geospatial map was generated using the leaflet package, providing a visual representation of the data. All statistical tests were two-sided, and p-values less than 0.05 were considered statistically significant, indicating a significant difference.

Results

Dataset

Geospatial mapping of HPV infection studies

To access the study characteristics and findings, you can interact with the map by clicking on the coloured circles. Each circle represents a specific study and provides valuable information when clicked upon. This feature allows users to delve into the details of each study by exploring its unique findings and characteristics. In case you wish to explore data from other countries or revert to the initial map view, you can simply utilize the “reset view” option located below the zoom controls (+ and -). By clicking on this option, the map will return to its original state, enabling you to easily navigate and examine data from different countries.

This user-friendly functionality enhances the user experience by providing a convenient way to access and analyse study-specific information while maintaining the flexibility to explore data from various regions on the map.

World Map

Prevalence of HPV16 and HPV18 by continent in 2023

Among the continents, Oceania exhibits the highest median prevalence of HPV infection, with a median value of approximately 42.77%. In contrast, Africa demonstrates the lowest median prevalence of HPV16 and HPV18, with a median value of approximately 33.62%. The application of the Kruskal-Wallis test reveals a statistically significant difference in the prevalence of HPV infection across continents. This finding strongly suggests that the observed disparities in median values are unlikely to occur by random chance, emphasizing the presence of genuine variations in HPV prevalence among different continents.

Prevalence of HPV16 and HPV18 in normal cytology cases by continent in 2023

Among the continents, Oceania exhibits the highest median prevalence of HPV infection, with a median value of 8.30%. This prevalence is notably higher than what is observed in other continents. In contrast, Africa demonstrates the lowest median prevalence of HPV infection, recorded at 3.80%. When considering the error bars, which represent the 95% confidence intervals, the widest range is observed in the Americas and Europe. This indicates greater variability in the estimates of HPV prevalence within these continents compared to others, suggesting potential regional differences or inconsistencies in data collection.

Prevalence of HPV16 and HPV18 in LSIL cases by continent in 2023

The median prevalence of HPV in LSIL cases is highest in Europe and Oceania, with a median value of 27.10%. This prevalence surpasses that observed in other continents by a small margin. In contrast, Asia exhibits the lowest prevalence of HPV at 21.20%, followed by Africa at 24.90%. Utilizing the Kruskal-Wallis test, we establish a statistically significant difference in the prevalence of HPV infection across continents, indicating genuine variations among them. Further pairwise comparisons, considering adjusted p-values, unveil significant disparities in prevalence rates among continents. Notably, Europe and Oceania emerge as having significantly higher prevalence rates compared to other continents.

Prevalence of HPV16 and HPV18 in HSIL cases by continent in 2023

Oceania stands out among the continents with the highest median prevalence of HPV infection in HSIL cases, recording a median value of 59.10%. The Americas closely trail behind with a median prevalence of 56.90%. Africa exhibits the lowest median prevalence of HPV at 38.60%, followed by Asia at 42.10%. Utilizing the Kruskal-Wallis test, we establish a statistically significant difference in the prevalence of HPV infection across continents. Further pairwise comparisons, considering adjusted p-values, uncover significant disparities in prevalence rates among certain continents. Notably, the comparison between Africa and Oceania reveals a significant difference with an adjusted p-value, indicating substantial variations in HPV prevalence between these continents.

Prevalence of HPV16 and HPV18 in cervical cancer cases by continent in 2023

Oceania exhibits the highest median prevalence of HPV infection in cervical cancer cases, recording a median value of 76.60%, closely followed by Europe at 74.0%. This prevalence exceeds that observed in other continents. Conversely, Africa displays the lowest median prevalence among the examined continents, with a median value of 67.20%. These findings highlight significant variations in HPV prevalence across different continents, emphasizing the importance of comprehensive research to elucidate the contributing factors and establish effective strategies for prevention, screening, and treatment in each affected region.

Distribution of HPV prevalence among individuals with normal cytology in African countries

In the African countries sampled, the median value of HPV prevalence in normal cytology cases is approximately 3.8%, as depicted by the median line on the plot. Most countries exhibit a low prevalence rate, as evidenced by a notable cluster of data points positioned towards the lower end of the HPV prevalence scale. However, several countries, including Guinea, Kenya, Mozambique, Benin, and Tunisia, demonstrate higher prevalence rates. The extremely low Wilcoxon p-value (1.225e-10) associated with the distribution of HPV prevalence in normal cytology cases indicates a statistically significant finding. This strongly suggests that the observed distribution is not a result of random chance but rather indicates the presence of underlying factors or patterns that contribute to HPV prevalence rates across these countries.

Distribution of HPV prevalence among individuals with LSIL in African countries

In the African countries included in the sample, the median percentage of HPV prevalence in LSIL cases is approximately 24.90%. There is notable variation in HPV prevalence among these countries, with the majority of data points clustering around the median value. However, Senegal, displays significantly higher prevalence rates. The Wilcoxon p-value is remarkably low (p = 4.96e-11), indicating a statistically significant difference in HPV prevalence across the sampled countries. This finding highlights genuine disparities in HPV prevalence rates among these nations.

Distribution of HPV prevalence among individuals with HSIL in African countries

The median percentage of HPV prevalence in HSIL cases among the sampled African countries is approximately 38.60%. Ethiopia stands out with a significantly higher percentage of HPV prevalence in HSIL cases, reaching 63%, followed by Tanzania, Kenya, and Senegal. Conversely, Zimbabwe, Guinea, Nigeria, and South Africa exhibit the lowest HPV prevalence in HSIL cases. The majority of data points cluster around the median value, indicating that, for most countries included in the study, the HPV prevalence in HSIL cases aligns with the median percentage. However, it is crucial to acknowledge the variation in prevalence rates among countries and investigate the underlying factors contributing to the observed differences.

Distribution of HPV prevalence among individuals with cervical cancer in African countries

Among the sampled African countries, the median percentage of HPV prevalence in cervical cancer cases is approximately 67.20%. A broad range of HPV prevalence percentages is observed across these countries, with some recording values as low as 10% (e.g., Senegal) and others reaching as high as 98% (e.g., Sudan). While there is notable variability in HPV prevalence percentages, the majority of data points cluster around the median value of 67%, suggesting that, for most countries in this sample, the HPV prevalence in cervical cancer cases falls within this range.

Distribution of HPV prevalence among individuals with normal cytology in American countries

The median HPV prevalence in normal cytology cases among the surveyed countries is 4.50%. Cuba stands out among the countries depicted on the graph, displaying the highest HPV prevalence at 39%, followed by Honduras. The majority of countries included in the study exhibit an HPV prevalence below 10%, indicating a lower prevalence rate in normal cytology cases for these countries. These findings underscore the significance of ongoing monitoring and preventive measures to effectively manage HPV infections and mitigate the risk of progression to abnormal cytology and cervical cancer.

Distribution of HPV prevalence among individuals with LSIL in American countries

The data reveals a wide range of HPV prevalence in LSIL cases, with some countries exhibiting prevalence rates close to 5%, while Colombia shows an exceptionally high HPV prevalence of 80%. This substantial variability suggests variations in the incidence or detection of HPV-associated LSIL across different geographical areas. Certain countries stand out with particularly high HPV prevalence in LSIL cases. These findings may indicate unique epidemiological patterns, differences in healthcare practices, or variations in reporting mechanisms specific to those areas. The provided Wilcoxon rank statistic (630.00) and the associated p-value (≈ 1.63e-07) demonstrate a statistically significant difference in HPV prevalence between the countries being compared.

Distribution of HPV prevalence among individuals with HSIL in American countries

The median value of HPV prevalence in HSIL cases among the sampled countries is 56.90%. The spread of data points along the x-axis indicates variations in the percentage of HPV prevalence from country to country. There is a wide range of HPV prevalence in HSIL cases observed among the countries, with the lowest prevalence around 32% and the highest close to 73%. This significant variability suggests notable differences in HPV prevalence in HSIL cases across different countries in Latin America and the Caribbean.

Notably, some countries such as Chile, Canada, and Venezuela exhibit higher prevalence rates, which may be of particular interest for public health interventions. These countries could benefit from targeted strategies aimed at prevention, early detection, and treatment of HSIL cases associated with HPV. On the other hand, Cuba, Jamaica, and Nicaragua show a lower prevalence of HPV in HSIL cases. These findings highlight the importance of tailored approaches to address the varying HPV prevalence and associated risks in different countries within the region.

Distribution of HPV prevalence among individuals with cervical cancer in American countries

The median percentage of HPV prevalence in cervical cancer cases across the sampled countries is approximately 68.20%. There is a wide range of HPV prevalence percentages observed among the countries, with lower values noted in countries like Ecuador and Bolivia. On the other hand, higher HPV prevalence in cervical cancer cases is observed in countries such as Chile, Venezuela, Argentina, Canada, and the USA. The Wilcoxon rank sum test confirms that the differences in HPV prevalence among the sampled countries are statistically significant. This highlights the importance of understanding and addressing the varying HPV prevalence rates in cervical cancer cases in different countries, emphasizing the need for comprehensive prevention, screening, and treatment strategies to combat the burden of cervical cancer.

Distribution of HPV prevalence among individuals with normal cytology in Asian countries

In the listed countries, the prevalence of HPV in normal cytology cases displays significant variation, spanning from minimal occurrences (close to 0%) to higher rates reaching approximately 7%. It is worth noting that a group of countries, potentially sharing geographical proximity or similar healthcare practices, exhibits considerably elevated HPV prevalence rates. The statistical analysis conducted on the data utilizes the Wilcoxon rank test, resulting in a p-value of approximately 2.05e-09. This exceptionally low p-value indicates strong statistical evidence supporting the existence of significant disparities in HPV prevalence among the countries. This finding underscores the importance of understanding the underlying factors contributing to these variations and tailoring preventive and screening measures accordingly to effectively manage and reduce the burden of HPV infections.

Distribution of HPV prevalence among individuals with LSIL in Asian countries

The prevalence of HPV in cases of LSIL shows a wide range among the listed countries. The rates range from nearly 10% in Japan to approximately 80% in Myanmar, indicating substantial variability in the occurrence of HPV-associated LSIL across different geographical regions. The median HPV prevalence in LSIL cases across the sampled countries is reported as 21.20%. This suggests that while some countries exhibit notably high prevalence rates, the typical prevalence for this group of countries is around one-fifth of LSIL cases being HPV-associated. Certain countries demonstrate remarkably high HPV prevalence in LSIL cases. For instance, Myanmar exhibits a prevalence rate close to 80%, which significantly surpasses rates observed in most other countries within the dataset. This finding may indicate the necessity for targeted public health interventions in these outlier countries to address the heightened burden of HPV-associated LSIL.

Distribution of HPV prevalence among individuals with HSIL in Asian countries

The vertical line positioned at approximately 42.10% represents the median HPV prevalence in HSIL cases across the sampled countries. The data points are distributed across a wide range, with the majority of countries exhibiting HPV prevalence rates between 27% and 70% in HSIL cases. Notably, Israel, Iran, and India display higher prevalence rates compared to other countries in the dataset. On the other hand, Thailand, Turkey, and Kuwait show lower prevalence rates in HSIL cases. This variation in HPV prevalence highlights the differences in the burden of HPV-associated HSIL across different countries. Understanding the factors contributing to these variations can help in implementing targeted interventions, such as HPV vaccination programs and improved screening strategies, to effectively manage and reduce the impact of HSIL cases associated with HPV.

Distribution of HPV prevalence among individuals with cervical cancer in Asian countries

The median HPV prevalence in ICC (invasive cervical cancer) cases is reported as 68.90%. Jordan, Malaysia, Syria, Pakistan, and Indonesia show a high prevalence of HPV in ICC cases, while Mongolia, Japan, Philippines, and Iran exhibit a low prevalence. The data points predominantly cluster towards the lower end of the HPV prevalence scale, with a majority of the countries displaying prevalence rates below 70%. However, as the prevalence increases, there is noticeable variability in the numerical value of cervical cancer cases among countries, suggesting potential differences in the burden of cervical cancer in countries with higher HPV prevalence.

Several countries demonstrate exceptionally high HPV prevalence rates exceeding 80%. These countries highlight a concerning pattern where a substantial proportion of cervical cancer cases in these regions are associated with HPV infection. This finding underscores the need for targeted medical interventions, such as HPV vaccination programs and improved screening and treatment strategies, or further exploration into the underlying factors contributing to these elevated prevalence rates. Addressing the high burden of HPV-associated cervical cancer cases in these countries is crucial for reducing the impact of the disease and improving women’s health outcomes.

Distribution of HPV prevalence among individuals with normal cytology in European countries

There is a wide range of HPV prevalence in normal cytology cases among the countries presented. Some countries have very low prevalence rates, close to 0%, while others have rates that are significantly higher, approaching 18%. This suggests that there are substantial differences in HPV prevalence across these countries, which could be due to various factors such as differences in vaccination rates, screening practices, or sexual health education. The median line shows that the median HPV prevalence in normal cytology cases among the sampled countries is around 3.8%. This median value provides a central tendency measure of the HPV prevalence across the countries, indicating that half of the countries have a prevalence below this value and half above.

Distribution of HPV prevalence among individuals with LSIL in European countries

The median HPV prevalence in LSIL cases across the observed countries is 27.10%. The Wilcoxon rank sum test suggests that there is a statistically significant difference in HPV prevalence between the countries being compared. The distribution of HPV prevalence in LSIL cases is skewed towards the lower end, with some countries having a prevalence below the median, and a few countries with exceptionally high prevalence rates.

Distribution of HPV prevalence among individuals with HSIL in European countries

There is a wide variation in HPV prevalence in HSIL cases across different European countries. The prevalence ranges from below 20% to nearly 80%, indicating significant disparities in HPV infection rates associated with high-grade lesions. Some countries such as Ireland, Switzerland, Netherlands, and Slovenia exhibit a high prevalence of HPV in HSIL cases, while others like Croatia and Norway demonstrate a comparatively lower prevalence. The median HPV prevalence in HSIL cases among the countries represented is marked by the blue dashed line, which appears to be at approximately 54.50%. This suggests that half of the countries have an HPV prevalence in HSIL cases below this value and half above.

Distribution of HPV prevalence among individuals with cervical cancer in European countries

The countries at the top of the plot, such as Hungary, Luxembourg, and Finland, show a high percentage of HPV prevalence in cervical cancer cases. This suggests that HPV is a significant factor in cervical cancer in these countries. The blue dashed line indicates the median value of HPV prevalence among the countries listed. The median appears to be around 74%, which means that half of the countries have an HPV prevalence in cervical cancer cases that is above this value and half below.

Distribution of HPV prevalence among individuals with normal cytology in Oceania countries

There is a wide range of HPV prevalence in normal cytology cases across the Pacific region. Australia shows the highest prevalence rate, which is significantly higher than the other countries listed. The median HPV prevalence rate in normal cytology cases among the countries listed is 8.30%. This indicates that half of the countries have a prevalence rate below this value and the other half above it.

Distribution of HPV prevalence among individuals with LSIL in Oceania countries

The HPV prevalence in LSIL cases is relatively consistent across the Pacific Island countries and territories, with a median value of approximately 27.10%. The interquartile range (IQR) is very narrow, indicating that the majority of the countries have a prevalence rate close to the median, suggesting low variability in HPV prevalence among these countries in LSIL cases. These findings suggest a consistent pattern of HPV prevalence in LSIL cases across the surveyed Pacific Island countries and territories, with little variation and a statistically significant result from the Wilcoxon test.

Distribution of HPV prevalence among individuals with HSIL in Oceania countries

The HPV prevalence in HSIL cases varies across the countries, with the lowest observed values around 50% and the highest just above 70%. This indicates a relatively high prevalence of HPV in HSIL cases across these countries. Australia stands out with a notably lower prevalence of HPV in HSIL cases compared to other countries listed. This could indicate differences in HPV infection rates, screening practices, or healthcare interventions. While Fiji and New Zealand show high prevalence rates above 65%. The median HPV prevalence in HSIL cases is approximately 59.10%. This suggests that more than half of the HSIL cases in these Pacific countries have an HPV prevalence rate around this value.

Distribution of HPV prevalence among individuals with cervical cancer in Oceania countries

Papua New Guinea stands out with the highest HPV prevalence in cervical cancer cases among the countries listed, with a prevalence rate that appears to be close to 84%. This suggests that HPV is a major contributing factor to cervical cancer in this country. There is considerable variability in HPV prevalence rates among the countries in Oceania. This indicates that there may be diverse factors at play, such as differences in vaccination rates, screening practices, or sexual health education. The median HPV prevalence rate across the countries shown is approximately 76.60%. This median value suggests that over half of the countries have an HPV prevalence rate in cervical cancer cases that is quite high, emphasizing the need for effective HPV vaccination and screening programs in the region.

Remarks

  1. Summary

The analysis of HPV prevalence across various cervical conditions and countries reveals substantial variations in the burden of HPV-associated diseases. The median HPV prevalence differs significantly among different cervical conditions, ranging from 4.50% in normal cytology cases to 68.20% in cervical cancer cases. Furthermore, there are notable disparities in HPV prevalence across countries, indicating regional differences in the incidence and impact of HPV-related conditions. These findings underscore the importance of understanding the factors contributing to these variations and implementing targeted interventions to mitigate the burden of HPV-associated diseases.

  1. Significant insights

2.1 Variation in HPV prevalence

The examination of HPV prevalence in normal cytology cases highlights the presence of a considerable range, with rates ranging from minimal occurrences close to 0% to higher rates of approximately 7%. This suggests differences in HPV transmission and infection rates among the studied countries. Moreover, certain countries demonstrate considerably elevated HPV prevalence, potentially indicating shared geographical proximity or similar healthcare practices.

2.2 Disparities in HPV prevalence among cervical conditions

The analysis reveals notable disparities in HPV prevalence across different cervical conditions. The prevalence rates of HPV-associated LSIL display a wide range, from nearly 10% in Japan to approximately 80% in Myanmar. This indicates significant variability in the occurrence of HPV-associated LSIL across geographical regions. Similarly, HPV prevalence in HSIL cases exhibits considerable variation, with rates ranging from 27% to 65% among the majority of countries. Countries with notably high prevalence rates suggest the need for targeted public health interventions in these countries to address the heightened burden of HPV-associated LSIL and HSIL.

2.3 Correlation between HPV prevalence and cervical cancer cases

A significant positive correlation is observed between the percentage of HPV prevalence and the numerical value representing cervical cancer cases across the displayed countries. This finding suggests that as HPV prevalence increases, there is a corresponding increase in the burden of cervical cancer. The presence of outliers with exceptionally high HPV prevalence exceeding 80% highlights the need for targeted medical interventions or further investigation into the underlying factors contributing to such elevated prevalence rates.

  1. Recommendations

3.1 Strengthen HPV vaccination programs

Countries should focus on enhancing and promoting HPV vaccination programs, particularly in regions with higher HPV prevalence rates. Increasing vaccine coverage among the target population can effectively reduce HPV transmission and subsequent HPV-associated diseases, including cervical cancer.

3.2 Improve access to screening and early detection

Efforts should be directed towards improving access to cervical cancer screening programs, including regular Pap smears and HPV testing. Implementing population-based screening initiatives and ensuring adequate healthcare infrastructure can facilitate early detection and prompt treatment of HPV-associated conditions.

3.3 Comprehensive sexual education

Comprehensive sexual education programs should be integrated into school curricula and community health initiatives to raise awareness about HPV transmission, prevention methods, and the importance of regular screenings. Educating individuals about safe sexual practices and the benefits of HPV vaccination can contribute to reducing HPV prevalence and associated diseases.

3.4 Collaboration and data sharing

International collaboration among health organizations, governments, healthcare providers, and researchers is crucial for sharing best practices, exchanging data, and developing evidence-based strategies. Collaborative efforts can enhance surveillance systems, facilitate comparative analysis, and enable the identification of effective interventions tailored to specific regions.

3.5 Continued monitoring and evaluation

Ongoing monitoring and evaluation of HPV prevalence, cervical cancer incidence, and the impact of interventions are essential. Regular assessment of the effectiveness and outcomes of implemented strategies will aid in identifying areas of improvement, refining interventions, and adapting approaches based on evolving epidemiological patterns.

By implementing these recommendations, policymakers, healthcare providers, and stakeholders can work together to reduce the burden of HPV-associated diseases, promote early detection, and improve the overall health outcomes of individuals affected by HPV infection.

Reference

Bruni L, Albero G, Serrano B, Mena M, Collado JJ, Gómez D, Muñoz J, Bosch FX, de Sanjosé S. ICO/IARC Information Centre on HPV and Cancer (HPV Information Centre). Human Papillomavirus and Related Diseases in the World. Summary Report 10 March 2023.

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Wickham H, Averick M, Bryan J, Chang W, McGowan LD, François R, Grolemund G, Hayes A, Henry L, Hester J, Kuhn M, Pedersen TL, Miller E, Bache SM, Müller K, Ooms J, Robinson D, Seidel DP, Spinu V, Takahashi K, Vaughan D, Wilke C, Woo K, Yutani H (2019). “Welcome to the tidyverse.” Journal of Open Source Software, 4(43), 1686. doi:10.21105/joss.01686 https://doi.org/10.21105/joss.01686.

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Xie Y, Cheng J, Tan X (2024). DT: A Wrapper of the JavaScript Library ‘DataTables’. R package version 0.33, https://CRAN.R-project.org/package=DT.

Cheng J, Schloerke B, Karambelkar B, Xie Y (2024). leaflet: Create Interactive Web Maps with the JavaScript ‘Leaflet’ Library. R package version 2.2.2, https://CRAN.R-project.org/package=leaflet.

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