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HPV

Distribution of HPV types among women with HPV-related diseases and exploration of lineages and variants of HPV 52 and 58 among HPV-infected patients in China: A systematic literature review

Meng Wanga Division of HIV/AIDS and Sex-Transmitted Virus Vaccines, WHO Collaborating Center for Standardization and Evaluation of Biologicals, State Key Laboratory of Drug Regulatory Science, NHC Key Laboratory of Research on Quality and Standardization of Biotech Products and NMPA Key Laboratory for Quality Research and Evaluation of Biological Products, Institute for Biological Product Control, National Institutes for Food and Drug Control (NIFDC), Beijing, ChinaView further author information
,
Haoyu Lianga Division of HIV/AIDS and Sex-Transmitted Virus Vaccines, WHO Collaborating Center for Standardization and Evaluation of Biologicals, State Key Laboratory of Drug Regulatory Science, NHC Key Laboratory of Research on Quality and Standardization of Biotech Products and NMPA Key Laboratory for Quality Research and Evaluation of Biological Products, Institute for Biological Product Control, National Institutes for Food and Drug Control (NIFDC), Beijing, ChinaView further author information
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Yue Yanb Merck Research Laboratories (MRL) Global Medical Affairs, MSD China, Shanghai, ChinaView further author information
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Rui Bianb Merck Research Laboratories (MRL) Global Medical Affairs, MSD China, Shanghai, ChinaView further author information
,
Weijin Huanga Division of HIV/AIDS and Sex-Transmitted Virus Vaccines, WHO Collaborating Center for Standardization and Evaluation of Biologicals, State Key Laboratory of Drug Regulatory Science, NHC Key Laboratory of Research on Quality and Standardization of Biotech Products and NMPA Key Laboratory for Quality Research and Evaluation of Biological Products, Institute for Biological Product Control, National Institutes for Food and Drug Control (NIFDC), Beijing, ChinaView further author information
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Xingxing Zhangb Merck Research Laboratories (MRL) Global Medical Affairs, MSD China, Shanghai, ChinaCorrespondence[email protected]
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Jianhui Niea Division of HIV/AIDS and Sex-Transmitted Virus Vaccines, WHO Collaborating Center for Standardization and Evaluation of Biologicals, State Key Laboratory of Drug Regulatory Science, NHC Key Laboratory of Research on Quality and Standardization of Biotech Products and NMPA Key Laboratory for Quality Research and Evaluation of Biological Products, Institute for Biological Product Control, National Institutes for Food and Drug Control (NIFDC), Beijing, ChinaCorrespondence[email protected]
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Article: 2343192 | Received 29 Dec 2023, Accepted 11 Apr 2024, Published online: 14 May 2024

ABSTRACT

To summarize the distribution of types of human papillomavirus (HPV) associated with HPV-related diseases and investigate the potential causes of high prevalence of HPV 52 and 58 by summarizing the prevalence of lineages, sub-lineages, and mutations among Chinese women. We searched PubMed, EMBASE, CNKI, and WanFang from January, 2012 to June, 2023 to identify all the eligible studies. We excluded patients who had received HPV vaccinations. Data were summarized in tables and cloud/rain maps. A total of 102 studies reporting HPV distribution and 15 studies reporting HPV52/HPV58 variants were extracted. Among Chinese women, the top five prevalent HPV types associated with cervical cancer (CC) were HPV16, 18, 58, 52, and 33. In patients with vaginal cancers and precancerous lesions, the most common HPV types were 16 and 52 followed by 58. For women with condyloma acuminatum (CA), the most common HPV types were 11 and 6. In Chinese women with HPV infection, lineage B was the most prominently identified for HPV52, and lineage A was the most common for HPV58. In addition to HPV types 16, which is prevalent worldwide, our findings revealed the unique high prevalence of HPV 52/58 among Chinese women with HPV-related diseases. HPV 52 variants were predominantly biased toward lineage B and sub-lineage B2, and HPV 58 variants were strongly biased toward lineage A and sub-lineage A1. Further investigations on the association between the high prevalent lineage and sub-lineage in HPV 52/58 and the risk of cancer risk are needed. Our findings underscore the importance of vaccination with the nine-valent HPV vaccine in China.

Introduction

Human papillomavirus (HPV) is a superfamily consisting of more than 200 members that have a preference for epithelial tissues. HPV types can be categorized into low- and high-risk categories based on their potential carcinogenicity. Currently, the 12 HPV types recognized as high-risk include HPV16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, and 59.Citation1 HPV infection has been implicated in nearly all cervical cancers (CCs) and squamous cell carcinomas of the anus, in 77.8% of vaginal cancers, 52.9% of penile cancers, 30% of oropharyngeal cancers, 25% of vulvar cancers, 2.3% of laryngeal cancers, and 2.1% of cancers of the oral cavity.Citation2,Citation3 Based on the most recent global cancer burden study, China bears a significant burden of HPV-related cancers, ranking second worldwide in both incidence (i.e., 110,000 new cases) and mortality rate (i.e., 59000 deaths) of cervical cancer.Citation4 Additionally, data from the National Cancer Center Registry in China indicate that head and neck cancers resulted in over 230,000 new cases and 78,000 deaths.Citation5

Notably, the distribution of high-risk HPV types in HPV-diseases vary across regions and countries. A recent review identified the five predominant high-risk HPV types in different countries that are associated with invasive cervical cancers (ICCs): HPV 16, 18, 33, 45, and 31 in Europe, HPV16, 18, 45, 31, and 33 in North America, and HPV16, 18, 45, 35, and 52 in Africa.Citation3 The most common oncogenic HPV types in other HPV-related diseases also vary in Africa, the Americas, Asia, Europe, and Oceania.Citation6 Similarly, the distribution of HPV types within China displays notable diversity across provinces and cities. Among patients with CC, the top three HPV types are HPV16, 58 and 52 in Beijing,Citation7 HPV58, 16, and 52 in Shanghai,Citation8 HPV16, 58, and 33 in Liaoning,Citation9 HPV16, 52, and 6 in Zhuhai,Citation10 and HPV16, 58, and 52 in Huaian.Citation11

The distribution of HPV types in distinct HPV-related diseases varies as well. For example, in Beijing, China, the top five high-risk HPV types found in the cytology of normal women were HPV52, 58, 16, 51 and 66. In women with cervical intraepithelial neoplasia (CIN), the predominant types were HPV58, 16, 52, 66, and 56, while in women with CC, HPV16, 58, 52, 59, and 18 predominated.Citation7 Research into other HPV-associated diseases like anal, vulvar and vaginal cancers, oropharyngeal cancer, recurrent respiratory papillomatosis (RRP) and genital warts is fragmented. We therefore carried out a systematic literature review to identify the distribution of HPV types among women with HPV-related diseases in diverse cities across China with the aim of supporting the development of optimal strategies for HPV surveillance, prevention, and control. It is widely recognized that HPV vaccines are effective in preventing genital warts and the majority of cervical cancers.Citation12 However, compared to the 117 countries worldwide that include HPV vaccines in their national immunization programs, with an average vaccination rate reaching 53%,Citation13,Citation14 the vaccination rate among eligible females aged 9–45 in China was generally low from 2018 to 2020.Citation15 It is noteworthy that although five types of HPV vaccines have been successively approved in China, their initial approval dates are considerably later than those in other countries.Citation16 Considering that most existing data are derived from unvaccinated individuals and to mitigate the impact of vaccination on genotype distribution, patients who had received HPV vaccination were excluded from this review.

Higher prevalence and attribution rates of HPV 52 and HPV58 in ICC have been observed in Eastern Asia compared with other regions.Citation17 Previous research has shown an association between viral genetic variants and cancer risk.Citation18–20 Within a certain HPV type,Citation21 it can be further classified into several lineages according to complete genome sequence identity.Citation19 The lineage B of HPV 52 is more prevalent in Asia than in other regions of the world.Citation17 Even though evidence suggests HPV lineages may explain in part the epidemiological characteristics of HPV-related diseases in China, data is limited. Therefore, another objective of our review is to explore the genetic variants of HPV 52 and 58, which may help to explain their high prevalence among Chinese women with HPV infection.

Methods

The systematic review was conducted per the Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) guidelines. The registration was completed in INPLASY (registration number 202280051). To validate the elevated prevalence of HPV52 and 58 in China, our primary objective is to elucidate the distribution of HPV types in the region. Subsequently, we endeavor to establish a foundational understanding and provide a potential explanation of the high prevalence of HPV52 and 58 by further investigating the distribution of lineages, sublineages, and mutations associated with these HPV types.

Search strategy

A comprehensive search of relevant studies published from January, 2012 to June, 2023 was retrieved from the PubMed and Embase databases for English literature and CNKI and Wanfang databases for Chinese literature. Detailed search strategies are shown in Supplementary Appendix 1.

Eligibility criteria

Inclusion Criteria

  1. Studies about the distribution of HPV types among Chinese women diagnosed with HPV-related diseases (CC and its precancerous lesions, anal cancer and its precancerous lesions, vaginal and vulvar cancers and their precancerous lesions, head and neck cancer and its precancerous lesions, recurrent respiratory papillomatosis (RRP) and genital warts) were included. The detection methods included hybriMax HPV gene array kit, HPV gene array test kit, flow cytometry-fluorescence hybridization test, “HR‐HPV genotyping real‐time PCR kit,” slan-96P real-time polymerase chain reaction (PCR) system assay and polymerase chain reaction-reverse dot blot (PCR-RDB). Study designs included cross-sectional studies.

  2. Studies about the variants of HPV52 and 58 and associated lineages, sublineages and mutations in Chinese women diagnosed with HPV infection were included.

  3. There was no limitation on age, stage of cancer, naïve treatment, recurrent disease, or other baseline characteristics.

Exclusion criteria

  1. Case reports, therapies, reviews and meta-analyzes, and clinical diagnostic methods;

  2. The quality of studies not meeting all items of the Joanna Briggs Institute (JBI) toolCitation22;

  3. Duplicate publications with the same patient population;

  4. Non-English or non-Chinese language studies;

  5. Lesions diagnosed among women who had received any HPV vaccine.

Study selection

Two qualified reviewers independently screened the abstracts and full texts for inclusion eligibility. All potentially relevant citations were requested and inspected in detail via the full-text paper. A third reviewer resolved any disagreement. A PRISMA flow diagram was generated to show the entire study selection process.

Outcomes

  1. The distribution of HPV types in Chinese women with HPV-related diseases;

  2. The variants of HPV52 and 58, including lineages/sublineages and mutations in Chinese women diagnosed with HPV infection. Lineages, sub-lineages and mutations were defined by the original study.

Data extraction

After screening and determining eligibility, data from each study were extracted independently by two reviewers using a standardized data abstraction form. The following data were extracted: author and year, study design, patient demographic information (age, gender, disease, HPV types, country, area), distribution of HPV types in HPV-related disease, distribution of HPV52 and 58, including lineages/sublineages and mutations. A third reviewer resolved any disagreement.

Assessment of study quality

Two independent authors assessed the quality of the included studies by using the JBI checklist for prevalence studies.Citation22 In summary, the tool rates the quality of selection, measurement, and the comparability of studies for prevalence studies.

Data synthesis

We tabulated the outcome results from each study in detail. Since the diagnosis and definition of precarious lesions in different studies vary, we decided to summarize the distribution of HPV types in two categoriesCitation23,Citation24: 1) CIN1, 2, and 3, 2) low-grade squamous intraepithelial lesion (LSIL) and high-grade squamous intraepithelial lesion (HSIL), based on the results extracted from included studies. The distribution information is summarized and presented in tables and cloud and rain maps. In the Cloud and rain maps, the prevalence data of each study is illustrated by dots, and the median and interquartile range are shown in bar charts. The distribution of HPV52 and 58, including lineages and sublineages in Chinese women diagnosed with HPV-related diseases is summarized and presented in tables.

Results

Study selection

A total of 4,639 studies were identified from the literature search that examined the distribution of HPV types in HPV-related diseases in China. Finally, 102Citation25–126 articles from this category were included for review after careful selection and assessment by two independent authors (). A total of 1,893 studies were identified from the literature search that investigated the distribution of HPV52 and 58, including lineages/sub-lineages and mutations in China. Fifteen articlesCitation16,Citation127−Citation140 from this category were ultimately included for review. (). The results of the quality of included studies are shown in Supplementary Tables S1 and S2.

Figure 1. The flow chart of the selection of the distribution of HPV types in HPV-related disease.

Figure 1. The flow chart of the selection of the distribution of HPV types in HPV-related disease.

Figure 2. Flow chart demonstrating the selection of the distribution of HPV 52 and 58, including lineages and sub-lineages.

Figure 2. Flow chart demonstrating the selection of the distribution of HPV 52 and 58, including lineages and sub-lineages.

Distribution of HPV types in HPV-related diseases

Basic characteristics of included studies

A total of 102 observational studies were included for the analysis of the distribution of HPV types in CIN1, CIN2, CIN3, LSIL, HSIL, CC, vaginal and vulvar cancers and its precancerous lesions, and condyloma acuminatum (CA). None of the studies reported anal cancer, head and neck cancer, or RRP. Most studies were from the East region (n = 42), Southwest region (n = 17), and North region (n = 13) of China. Rare studies described the age and race of included individuals. Among the 102 studies, 49Citation27,Citation28,Citation30,Citation32,Citation33,Citation35–38,Citation42–46,Citation49,Citation55–57,Citation59–61,Citation62–72,Citation77,Citation78,Citation82–84,Citation90–94,Citation101–103,Citation105,Citation107–110,Citation114–124 were published in Chinese, while the other 53Citation25,Citation26,Citation29,Citation31,Citation34,Citation39–41,Citation47,Citation48,Citation50–54,Citation58,Citation60,Citation63–67,Citation73–76,Citation79–81,Citation85–89,Citation95–100,Citation104,Citation106,Citation108,Citation109,Citation111–113,Citation115,Citation116,Citation118,Citation119,Citation125,Citation126 were published in English (). For the analysis of the distribution of HPV types in HPV-related diseases in China, 100,427 individuals for whom information about the HPV type was reported were included. A total of 24,556 patients were diagnosed with CIN1, 9,933 with CIN2, 14676 with CIN3, 9,665 with LSIL, 9,196 with HSIL 26,209 with CC (includes both cervical squamous cell carcinoma and cervical adenocarcinoma), 4,416 patients with vaginal and vulvar cancers and their precancerous lesions and 1,776 patients with CA.

Table 1. Basic characteristics of included studies for the distribution of HPV types in HPV-related disease.

Distribution of HPV types in HPV-related cervical cancer and precancerous lesions in Chinese patients

As shown in (Supplementary Figure S1), the five most common HPV types were 52, 16, 58, 53, and 51 for patients with CIN1. While for patients with CIN2 and CIN3 (; Supplementary Figures S2 and S3), the predominant 5 types were 16, 58, 52, 33 and 31. HPV16 played a dominant role in patients with CIN3. In cases of LSIL (; Supplementary Figure S4), HPV 52, 16, 58, 56 and 18 were the most prevalent. In cases of HSIL (; Supplementary Figure S5), the 5 most common HPV types were 16, 58, 52, 33, and 18. The prevalence of 16, 58, and 52 was distinctly higher than the other types. For patients with CC (; Supplementary Figure S6), HPV 16, 18, 58, 52, and 33 were the most prevalent.

Figure 3. The common HPV types in women.

(a) The common HPV types in women diagnosed with CIN1; (b) the common HPV types in women diagnosed with CIN2; (c) the common HPV types in women diagnosed with CIN3; (d) the common HPV types in women diagnosed with LSIL; (e) the common HPV types in women diagnosed with HSIL; (f) the common HPV types in women diagnosed with CC.
Notes: Cervical cancer includes both cervical squamous cell carcinoma and cervical adenocarcinoma. The graph above shows only the top 10 common HPV type.
Figure 3. The common HPV types in women.

Distribution of HPV types in HPV-related non-cervical sites in Chinese patients

Two studiesCitation25,Citation113 reported the distribution of HPV types in patients with vaginal cancer or precancerous lesions and reported the most prevalent HPV types were 16, 52, and 58. The distribution in patients with vulvar cancer was reported in another two studiesCitation81,Citation95 in which the most common HPV types were 16, 58, and 52. Among patients with CA, the prevalence of HPV types was investigated in 4 studiesCitation28,Citation92,Citation106,Citation111 that reported the predominant HPV types were HPV 11 and 6.

Distribution of HPV variants in HPV52 and 58 in Chinese patients

Basic characteristics of included studies

A total of 15 observational studiesCitation16,Citation127−Citation140 were included to analyze the distribution of HPV 52 and 58 variants. Three studiesCitation130,Citation132,Citation139 were published in Chinese, and twelve studiesCitation16,Citation127–129,Citation131–138,Citation140 were published in the English.

Variants of HPV 52 in Chinese patients

Eight studiesCitation16,Citation127–133 contributed data about the HPV52 variants (). Variants were detected in the E6 gene in 5 studies,Citation127–131 the E7 gene in 5 studies,Citation128–132 the L1 gene in 2 studies,Citation127,Citation128 and the long control region (LCR) gene in 3 studies.Citation16,Citation129,Citation132 One studyCitation133 reported variants in E6 and E7 jointly. Within the E6 gene segment, the most prominently identified lineage was lineage B (observed in 5 studies, ranging from 93.3% to 97.6%) and sublineage B2 (identified in 2 studies, with a prevalence ranging from 93.3% to 97.6%). Notably, the mutations G350T (identified in 4 studies, with a prevalence ranging from 96.4% to 100%) and A379G (identified in 3 studies, with a prevalence ranging from 93.3% to 97.6%) were identified as the prevailing mutations in the E6 gene. Similarly, lineage B (observed in 5 studies, ranging from 93.3% to 97.8%) and sublineage B2 (identified in 2 studies, with a prevalence ranging from 93.3% to 97.6%) were the most prevalent within the E7 gene segment. Moreover, 4 studies reported that the mutations C751T (with a prevalence ranging from 93.3% to 97.8%) and A801G (with a prevalence ranging from 98.6% to 100%) were the most prevalent mutations in the E7 gene. The variants in L1 and LCR are summarized in and Supplementary Table 3.

Table 2. Basic characteristics of included studies for the distribution of HPV 52, including lineages and sub-lineages.

Variants in HPV 58 in Chinese patients

HPV58 variants were reported in 9 studiesCitation16,Citation133–140 (). Five studiesCitation133,Citation136–139 presented the variants in the E6 and E7 gene segments, 4 studiesCitation136–139 reported E6 and E7 variants individually, and 1 studyCitation133 reported them jointly. Two studiesCitation134,Citation135 reported variants in the L1 gene, 1 studyCitation134 in the L2 gene, 1 studyCitation16 in the LCR gene, and 1 studyCitation140 reported variants in the entire genome. The most prominently identified lineage was lineage A (identified from 4 studies, with a prevalence ranging from 99.8% to 100%) in E6 and E7 genes. ublineage A1 was the most prevalent sublineage (with a prevalence ranging from 41.5% to 68.3%) in E6 (identified from 3 studies) and E7 genes (identified from 4 studies), followed by sublineages A2 and A3. Moreover, the mutations A388C (identified in 4 studies, with a prevalence ranging from 27.4% to 55.4%) and C307T (identified in 4 studies, with a prevalence ranging from 19.6% to 58.5%) were the prevailing mutations within the E6 gene. The mutations T744G (identified from 4 studies, with a prevalence ranging from 60.5% to 78.8%) and G761A (identified from 3 studies, with a prevalence ranging from 19.6% to 40.2%) were the most prevalent mutations in the E7 gene. The variants within L1, L2 and LCR are shown in and Supplementary Table 4.

Table 3. Basic characteristics of included studies for the distribution of HPV 58, including lineages and sub-lineages.

Discussion

We explored the distribution of HPV types among women in China with cervical and non-cervical HPV-related diseases. To the best of our knowledge, this review represents the first attempt to consolidate data on the prevalence of HPV types across various anatomical sites in Chinese women, identifying lineage B as the most prominently represented for HPV52, and lineage A as the most common for HPV58 in the Chinese population. This may provide clues for future investigations into the biological mechanisms underlying the high prevalence of HPV52 and HPV58 and the high disease burden associated with HPV52 and HPV58 in Chinese women.

Our findings demonstrate a pronounced disparity in the distribution of HPV genotypes associated with CC across different geographical regions. In line with global trends, HPV16 and 18 emerged as the predominant types among Chinese women with cervical cancer (CC) or precancerous lesions. Particularly, HPV58, 52, and 33 were more prevalent among Chinese women with CC, while in Europe, HPV 33, 45, and 31 were more commonly associated with CC, HPV 45, 31, and 33 were predominant in North America, and HPV 45, 35, and 52 more common in Africa.Citation3 As expected, our findings align consistently with previous studies demonstrating a higher prevalence of HPV52 and 58 in China when compared with other global regions.Citation141–145 Remarkably, these distinct patterns were steadily observed across a range of conditions, including cervical cancer, CIN1, CIN2, CIN3, and vaginal cancers. This observation may reflect that CIN of all grades could potentially progress to cancers over time, highlighting the need for vigilance across all CIN grades.Citation146,Citation147

The variability in the prevalence of HPV genotypes signifies a need for region-specific strategies to prevent HPV-related diseases. Each country and region should formulate tailored prevention and control strategies based on their specific HPV epidemiological characteristics. Preventing HPV-related diseases requires comprehensive strategies due to the numerous HPV types and their widespread prevalence. Higher-valency vaccines, like the nine-valent HPV vaccine, provide broad coverage, effectively preventing 92% of cervical cancer cases globally.Citation148 Simultaneously, the real-world impact of the nine-valent HPV vaccine has been a decrease in the incidence of precancerous lesions in the vulva, vagina, and anus,Citation149 a reduction in the occurrence of genital warts,Citation150 and a decline in the prevalence of oral HPV infections.Citation151 However, it should be noted that the nine-valent HPV vaccine does not encompass around 10% of genotypes linked to high-grade lesions, nor does it include HPV genotypes associated with a significant portion of other cervical neoplastic lesions in Chinese women. This may indicate to consider exploring further research into higher-valency vaccines in the future to better understand the potential positive effects they may offer. It is noteworthy that while HPV vaccination stands as one of the most effective measures in reducing the risk of HPV-associated diseases, such as CC and oropharyngeal cancer, its uptake in China has faced challenges, predominantly limited to adult women.Citation152 Financial barriers may hinder the uptake of the HPV vaccine in China, as it has not been integrated into the national immunization program. Nevertheless, certain regions have introduced initiatives that either reimburse or provide coverage for HPV vaccination among eligible girls, potentially enhancing uptake in this critical demographic.Citation153 Additionally, in settings where the cost of HPV vaccines remains prohibitive, the promising reports regarding the high efficacy of single-dose HPV vaccination among young women residing in resource-constrained areas is urgently needed.Citation154

Furthermore, in line with previous research, our study found that HPV52 is predominantly associated with lineage B, specifically B2, while HPV58 is primarily linked to lineage A, particularly A1.Citation155–158 In contrast to the Americas (78.2%), Europe (92.6%), and Africa (64.3%), where sub-lineage A1 exhibited predominantly higher prevalence, our results align with those from Asia (89.0%), where sub-lineage B2 was the most commonly observed sub-lineage.Citation17 Notably, it has been suggested a higher risk of cervical cancer associated with HPV52 lineage B than with lineage A, with an odds ratio (OR) of 5.46 (95% CI: 2.28–13.07).Citation17 This suggests that the higher prevalence of HPV52 in China may be attributed to the prevalence of lineage B, which carries a higher carcinogenic risk. The carcinogenic risk of the lineage A of HPV58 has yet to be fully understood, despite its high prevalence in HPV-related diseases. Differing from earlier studies that identified sub-lineage A2 as the dominant sub-lineage of HPV 58 in Europe (87.1%), the Americas (74.6%), Africa (46.4%), and Asia (45.8%), our research reveals that sub-lineage A1 is the prevailing sub-lineage in China.Citation159 In one study from the Taizhou area, sublineage A3 of HPV 58 was associated with higher-grade intraepithelial neoplasia (CIN2 or worse) than other sublineages (OR = 4.41, p < .05), and no association was found between HPV58 lineages or sublineages and cervical lesions.Citation138 Therefore, it would be valuable for future studies to explore whether the increased prevalence of HPV58 in HPV-related diseases in Chinese women, especially in patients with HSIL, is due to the higher oncogenic potential of lineage A, specifically sublineage A1.

Mutations in the E6 and E7 genes have been suggested to play a significant role in cervical carcinogenesis.Citation160 Studies have linked the A379G variation in HPV52 E6 to an increased risk of cervical lesions in Korean women but found no correlation in Chinese women.Citation157,Citation161 The A388C variation in HPV58 E6 has actually been associated with a reduced risk of HSIL in in HongkongCitation162 and Shanghai.Citation133 In our review, we identified prevalent mutations in HPV 52 (G350T E6, A379G E6, C751T E7, A801G E7) and HPV58 (C307T E6, A388C E6, G694A E7, T744G E7). Given the known association between nucleotide sequence mutations of HPV viruses and cancer risk,Citation163 these mutations in E6 and E7 genes of HPV52 and HPV58 may help explain their higher prevalence in Chinese women with HPV-related diseases, despite limited data. Further research is warranted to explore the influence of viral, host, and environmental factors on the distribution of HPV types.

Strengths and limitations

To our knowledge, this review represents the first comprehensive attempt to depict the prevalence of HPV types in Chinese women with HPV-related diseases. Additionally, it further explores the variations in HPV52 and 58 among these women with HPV infection. Through a systematic review of the available information derived from both English and Chinese databases, we identified specific gaps in our knowledge. While there is a wealth of epidemiological data regarding HPV in women, the focus is predominantly on cervical infections. Epidemiological data regarding the prevalence, distribution, and impact of HPV in other anatomic locations in women is scarce. Following our rigorous screening process, no references meeting our inclusion criteria were found that reported on the distribution of HPV types among women with anal cancer, head and neck cancer, or RRP. Because we exclusively analyzed data for women, research papers that did not differentiate by gender were excluded in our analysis. This limitation limits the generalizability of our results to broader populations. Several references that evaluated the distribution of HPV types among individuals with HPV-related diseases, regardless of gender, may provide relevant information for future analysis. For example, HPV16 and 58,Citation164,Citation165 HPV16 and 18,Citation143–169 and HPV11 and 6Citation170 were found to be the most prevalent in anal cancer, head and neck cancer, and RRP, respectively. Therefore, extensive research is imperative to delve into the epidemiological aspects of HPV in non-cervical sites, particularly with regard to HPV-related diseases, to bolster efforts to prevent and manage HPV-related non-cervical diseases in Chinese women. Furthermore, the results of this study primarily emphasize the distribution of individual genotypes’ infection risks within the population, without considering the impact of mixed infections on genotype distribution. This limitation underscores the need for future research to supplement the data by specifically addressing mixed infections. In addition, we aware that the included studies did not provide detailed information about the methodology used to generate phylogenetic trees. This may affect the transparency and reproducibility of our study and may have impact on the interpretation of our findings Another limitation of our review is that most of our results were descriptive. We did not perform meta-analysis due to the broad heterogeneity between studies, such as different methodologies and sampling used in the included studies. This may indicate that future studies should strive to standardize methodologies and sampling techniques to address heterogeneity and enable meaningful meta-analytical synthesis of data. Regarding the quality of included studies, 67% of the included studies providing data on variants of HPV52 and 58 did not explicitly report whether a standard and reliable way was used to measure participants, potentially affecting the validity, interpretability, generalizability, and implications of the results. Future research could benefit from providing clearer documentation in this regard to enhance the credibility of their study findings.

Clinical implications

This study offers important epidemiological evidence that can inform vaccine strategies in China. Moreover, gaining insights into the distribution of lineages, sub-lineages and mutations linked to high-risk HPV types is instrumental in evaluating cancer risks, guiding early cancer screening, and implementing preventive measures, ultimately leading to a reduction in the incidence of HPV-related cancers. Lastly, our research serves as a valuable point of reference for future monitoring HPV and tracking viral strain variations in China, thereby ensuring the continued efficacy of vaccination strategies as HPV infections continue to evolve.

Conclusion

The findings of this study underscore that HPV infections play a substantial role in the development of cervical cancer, vaginal cancer, and genital warts in Chinese women. Specifically, the high-risk HPV types, notably HPV16, 18, 52, and 58, are the predominant culprits responsible for cervical cancer, external genital cancers and precancers. The low-risk types, such as HPV6 and 11, are the most frequently associated with genital warts. Notably, the increased prevalence of HPV52 and 58 among Chinese women can potentially be attributed to the heightened oncogenic potential of lineage B of HPV 52 and lineage A of HPV 58. Further investigations that unravel the precise mechanisms by which these genetic variations influence disease progression and cancer risk will provide valuable insights for the development of targeted interventions and vaccination strategies aimed at reducing the burden of HPV-related diseases among Chinese women.

Abbreviations

HPV: Human papillomavirus; CCs: cervical cancers; ICCs: invasive cervical cancers; CIN: cervical intraepithelial neoplasia; RRP: recurrent respiratory papillomatosis; PRISMA: Preferred Reporting Items for Systematic reviews and Meta-Analyses; PCR: polymerase chain reaction; PCR-RDB: polymerase chain reaction-reverse dot blot; JBI: Joanna Briggs Institute; LSIL: low-grade squamous intraepithelial lesion; HSIL: high-grade squamous intraepithelial lesion; CA: condyloma acuminatum; LCR: long control region; OR: odds ratio.

Author contribution

Weijin Huang (WH), Jianhui Nie (JN), Rui Bian (RB), Xingxing Zhang (XZ), and Yue Yan (YY) designed the review protocol. Meng Wang (MW), Haoyu Liang (HL), XZ and YY conducted the literature search and data extraction. Statistical analyzes were performed by WH, JN, RB, MW, HL, and XZ. Authors MW, HL, RB, XZ, and YY critically reviewed and interpreted the results. The manuscript was drafted by MW and HL, with substantial input from all other authors during the writing, reviewing, and editing stages. All authors have read and approved the final manuscript.

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Acknowledgments

This work was partly supported by a grant from the major project of the Study on Pathogenesis and Epidemic Prevention Technology System (2021YFC2302500) by the Ministry of Science and Technology of China. The collection and assembly of data and statistical expertise were provided by Miss. Sai Zhao, Miss. Yang Zhang, and Dr. Sitong Dong from Systematic Review Solutions, Ltd. Margueritte White M.D. of Global Community Writer provided English language editing.

Disclosure statement

Authors Yue Yan, Rui Bian, and Xingxing Zhang are employed by MSD China.

The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Data availability statement

Data will be made available on request.

Supplementary material

Supplemental data for this article can be accessed on the publisher’s website at https://doi.org/10.1080/21645515.2024.2343192.

Additional information

Funding

The collection and assembly of data, statistical expertise and writing assistance were funded by MSD China.

References

  • Human papillomavirus vaccines: WHO position paper (2022 update). 2022.
  • de Martel C, Georges D, Bray F, Ferlay J, Clifford GM. Global burden of cancer attributable to infections in 2018: a worldwide incidence analysis. Lancet Global Health. 2020;8(2):180–26. doi:10.1016/S2214-109X(19)30488-7.
  • Kombe Kombe AJ, Li B, Zahid A, Mengist HM, Bounda GA, Zhou Y. Epidemiology and Burden of Human Papillomavirus and Related Diseases, Molecular Pathogenesis, and Vaccine Evaluation. Front Public Health. 2021;8:552028. doi:10.3389/fpubh.2020.552028.
  • Cao W, Chen HD, Yu YW, Li N, Chen WQ. Changing profiles of cancer burden worldwide and in China: a secondary analysis of the global cancer statistics 2020. Chin Med J. 2021;134(7):783–91. doi:10.1097/CM9.0000000000001474.
  • Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, Jemal A, Yu XQ, He J. Cancer statistics in China, 2015. CA Cancer J Clin. 2016;66(2):115–32. doi:10.3322/caac.21338.
  • Bruni L, Albero G, Serrano B, Mena M, Collado J, Gómez D, Muñoz J, Bosch F, De Sanjosé S. Human papillomavirus and related diseases in the world. Summary Report 10 March 2023. ICO/IARC Information Centre on HPV and Cancer (HPV Information Centre); 2023.
  • Zhu X, Wang Y, Lv Z, Su J. Prevalence and genotype distribution of high-risk HPV infection among women in Beijing, China. J Med Virol. 2021;93(8):5103–9. doi:10.1002/jmv.27013.
  • Zhu C, Diao W, Wang Q, Sui L. Analysis of HPV genotype distribution in 475 cases of cervical squamous intraepithelial lesions in Shanghai. Fudan J (Med Ed). 2016;43:447–52.
  • Yu Y, Liu H. Meta-analysis of distribution of cervical human papillomavirus types in women of Liaoning region. Chin Mod Doctor. 2021;59:108–13.
  • Zu Y, Ou Z, Wu D, Liu W, Liu L, Wu D, Zhao Y, Ren P, Zhang Y, Li W, et al. Genetic characteristics of human papillomavirus type 16, 18, 52 and 58 in southern China. Genomics. 2021;113(6):3895–906. doi:10.1016/j.ygeno.2021.09.006.
  • Xiang Y, Wang Q, Zhang B. Distribution of different subtypes of HPV in patients with high-grade cervical lesions. J Bengbu Med Coll. 2020;45:1407–9, 13.
  • Organization WH. Global strategy to accelerate the elimination of cervical cancer as a public health problem [EB/OL]. 2020 Sept 6. https://www.who.int/publications/i/item/9789240014107.
  • Organization WH. HPV vaccine global market study [EB/OL]. 2022 Sept 8. https://www.who.int/publications/m/item/who‑hpv‑vaccine‑global‑market‑study‑april‑2022.2022.
  • Bruni L, Saura-Lázaro A, Montoliu A, Brotons M, Alemany L, Diallo MS, Afsar OZ, LaMontagne DS, Mosina L, Contreras M, et al. HPV vaccination introduction worldwide and WHO and UNICEF estimates of national HPV immunization coverage 2010–2019. Prev Med. 2021;144:106399. doi:10.1016/j.ypmed.2020.106399.
  • Song Y, Liu X, Yin Z, Yu W, Cao L, Cao L, Ye J, Li L, Wu J. Human papillomavirus vaccine coverage among the 9–45-year-old female population of China in 2018–2020. Chin J Vaccines Immunization. 2021;27(5):570–5.
  • Yang Z, Zhang C, Luo P, Sun F, Mei B. Genetic diversity and functional implication of the long control region in human papillomavirus types 52, 58, and 16 from central China. Infect Genet Evol. 2023;112:105447. doi:10.1016/j.meegid.2023.105447.
  • Zhang C, Park JS, Grce M, Hibbitts S, Palefsky JM, Konno R, Smith-McCune KK, Giovannelli L, Chu T-Y, Picconi MA, et al. Geographical distribution and risk association of human papillomavirusgenotype 52–variant lineages. J Infect Dis. 2014;210(10):1600–4. doi:10.1093/infdis/jiu310.
  • Bernard HU. The clinical importance of the nomenclature, evolution and taxonomy of human papillomaviruses. J Clin Virol. 2005;32(Suppl 1):S1–6. doi:10.1016/j.jcv.2004.10.021.
  • Chen Z, Schiffman M, Herrero R, Desalle R, Anastos K, Segondy M, Sahasrabuddhe VV, Gravitt PE, Hsing AW, Burk RD, et al. Evolution and taxonomic classification of human papillomavirus 16 (HPV16)-related variant genomes: HPV31, HPV33, HPV35, HPV52, HPV58 and HPV67. PLOS ONE. 2011;6(5):e20183. doi:10.1371/journal.pone.0020183.
  • Clifford GM, Tenet V, Georges D, Alemany L, Pavón MA, Chen Z, Yeager M, Cullen M, Boland JF, Bass S, Steinberg M. Human papillomavirus 16 sub-lineage dispersal and cervical cancer risk worldwide: whole viral genome sequences from 7116 HPV16-positive women.Papillomavirus res (Amsterdam.Netherlands.2019;Vol. 7:pp. 67–74.
  • Chen Z, Schiffman M, Herrero R, DeSalle R, Anastos K, Segondy M, Sahasrabuddhe VV, Gravitt PE, Hsing AW, Chan PK, Burk RD, et al. Classification and evolution of human papillomavirus genome variants: Alpha-5 (HPV26, 51, 69, 82), Alpha-6 (HPV30, 53, 56, 66), Alpha-11 (HPV34, 73), Alpha-13 (HPV54) and Alpha-3 (HPV61). Virology. 2018;516:86–101. doi:10.1016/j.virol.2018.01.002.
  • Munn Z, Moola S, Riitano D, Lisy K. The development of a critical appraisal tool for use in systematic reviews addressing questions of prevalence. Int J Health Policy Manag. 2014;3(3):123–8. doi:10.15171/ijhpm.2014.71.
  • Eknoyan G, Levin A, Levin NW. K/DOQI clinical practice guidelines for bone metabolism and disease in chronic kidney disease. Am J Kidney Dis. 2003;42(4 Suppl 3):S1–201. doi:10.1016/S0272-6386(03)00905-3.
  • Schiffman M, Solomon D, Solomon CG. Clinical practice. Cervical-cancer screening with human papillomavirus and cytologic cotesting. N Engl J Med. 2013;369(24):2324–31. doi:10.1056/NEJMcp1210379.
  • Ao M, Zheng D, Wang J, Gu X, Xi M. A retrospective study of cytology and HPV genotypes results of 3229 vaginal intraepithelial neoplasia patients. J Med Virol. 2022;94(2):737–44. doi:10.1002/jmv.27311.
  • Baloch Z, Li Y, Yuan T, Feng Y, Liu Y, Tai W, Liu L, Wang B, Zhang A-M, Wu X, et al. Epidemiologic characterization of human papillomavirus (HPV) infection in various regions of Yunnan Province of China. BMC Infect Dis. 2016;16(1):228. doi:10.1186/s12879-016-1562-7.
  • Cai W, Wang H, Geng J, Xia L, Long X, Wang X. Distribution of HPV infection genotypes in normal cells of the uterine cervix and tissues of squamous cell carcinoma and adenocarcinoma of the uterine cervix. Chin J Clin Exp Path. 2014;30(8):854–7+62.
  • Chen Y. Study on the correlation between human papillomavirus genotypes and cervical lesions in Tianshui area. Chin Primary Health Care. 2013;27:42–4.
  • Chen W, Sun H, Molijn A, Zeng L, Kang L, Jenkins D, Zhang S, Cui J, Wu Z, Pirog E, et al. The variable characteristics of human papillomavirus in squamous cell carcinoma and adenocarcinoma of Cervix in China. J Low Genit Tract Dis. 2018;22(4):355–61. doi:10.1097/LGT.0000000000000408.
  • Chen Z, Zhen H, Huang L. Human papillomavirus infection and genotype distribution in women in. Wuhan: Jianghan University; 2019.
  • Chen G, Zheng P, Gao L, Zhao J, Wang Y, Qin W. Prevalence and genotype distribution of human papillomavirus in women with cervical cancer or cervical intraepithelial neoplasia in Henan province, central China. J Med Virol. 2020;92(12):3743–9. doi:10.1002/jmv.25670.
  • Chen L, Cheng H. HPV18 E7 antibody preparation, application and survey of HPV subtypes in patients with cervical lesions. Hangzhou (China): Zhejiang University; 2020.
  • Cui Y, Zhang P, Lu T, Huang X, Lv S. Human papillomavirus infection status and genotype analysis in women with cervical lesions in Xi’an. Chin J Woman Child Health Res. 2016;27:819–21.
  • Ding X, Liu Z, Su J, Yan D, Sun W, Zeng Z. Human papillomavirus type-specific prevalence in women referred for colposcopic examination in Beijing. J Med Virol. 2014;86(11):1937–43. doi:10.1002/jmv.24044.
  • Fan J, Xue M. Study on the relationship between HPV infection and cervical lesions and related risk factors. Changsha (China): Central South University; 2014.
  • Fan LY, Zhan P, Wang CY, Liu YF. Characteristics of HPV infection among 4 084 gynecological outpatients. J Army Med Univ. 2023;45:335–42.
  • Fang C. Analysis of human papillomavirus infection in 651 patients with squamous cervical cancer. Mod Pract Med. 2018;30:495–7.
  • Gao W, Gao D, Yu X, Xu Y. Distribution of human papillomavirus infection subtypes and its correlation with cervical lesions in Hefei women. J Pract Med. 2019;35:1785–8+93.
  • Gong P, Wang Z, Geng J, Tan X. Comparative study on detection and typing of human papillomavirus (HPV) Infection with microarray using paraffin-embedded specimens from squamous cell carcinoma and cervical precursor lesions. J Nanosci Nanotechnol. 2017;17(2):990–7. doi:10.1166/jnn.2017.12769.
  • Gu X, Long X, Yu Z, Xia S, Geng J. An analytical description of distributions of HPV genotypes patients with cervical precancerous lesions and squamous cell carcinoma in Zhejiang and Jiangsu area. Int J Clin Exp Med. 2017;10:6987–93.
  • He L, He J. Distribution of high-risk HPV types among women in Sichuan province, China: a cross-sectional study. BMC Infect Dis. 2019;19(1):390. doi:10.1186/s12879-019-4038-8.
  • Hou SN, Cheng WG, Lu HM, Li YY, Shen QY, C Y. High-risk HPV genotyping distribution and human papillomavirus E6/E7 expression in different degrees of cervical lesions. Med Lab Sci Clin. 2022;33:25–8,4.
  • Hu W, Fu Y. Clinical analysis of 519 cases of cervical lesions in middle-aged and elderly women without primary prevention of HPV vaccine. Changchun (China): Jilin University; 2021.
  • Hu X, Meng L, Gao Y, Man S, Ma Y, Jin C, Wang B, Ning Y, Li L. Current status of human papillomavirus infection and abnormal cervical cytology in a female medical examination population in Shenzhen. Chin J Epidemiol. 2021;42(7):1205–12. doi:10.3760/cma.j.cn112338-20210106-00007.
  • Huang Y, Zhou HZH. Study on HPV infection in cervical cancer screening population and its relationship with cervical lesions. Kunming (China): Kunming Medical University; 2019.
  • Jin L, Zhang X, Xiao L, Zhang L, Yang H, Zhang L. Analysis of cervical human papillomavirus genotyping in 116441 census women. J Bengbu Med Coll. 2018;43:462–7.
  • Jin R, Yang X, Bao J, Zhang W, Dou R, Yuan D, Jiang L, Yu H. The prevalence and genotype distribution of human papilloma virus in cervical squamous intraepithelial lesion and squamous cell carcinoma in Taizhou, China. Medicine (Baltimore). 2021;100(28):e26593. doi:10.1097/MD.0000000000026593.
  • Li H, Zhang J, Chen Z, Zhou B, Tan Y. Prevalence of human papillomavirus genotypes among women in Hunan province, China. Eur J Obstet Gynecol Reprod Biol. 2013;170(1):202–5. doi:10.1016/j.ejogrb.2013.05.010.
  • Li D, Xiao Z, Chen Y. Epidemiological survey of HPV in cervical cancer patients in a region. lab Med Clin. 2014;11:2423–4.
  • Li K, Yin R, Li Q, Wang D. Analysis of HPV distribution in patients with cervical precancerous lesions in Western China. Medicine (Baltimore). 2017;96(29):e7304. doi:10.1097/MD.0000000000007304.
  • Li K, Yin R, Wang D, Li Q. Human papillomavirus subtypes distribution among 2309 cervical cancer patients in West China. Oncotarget. 2017;8(17):28502–9. doi:10.18632/oncotarget.16093.
  • Li X, Wan X, Zheng F, Zhu H, Zhu X, Yu J. Comparison of human papillomavirus genotype distributions in cervical intraepithelial neoplasia and cervical cancer. Biomed Res (India). 2017;28:2284–9.
  • Yuanyue L, Baloch Z, Yasmeen N, Tao Y, Xiaomei W, Xueshan X. The distribution of human papillomavirus genotypes in cervical cancer and intraepithelial neoplasia lesions among Chinese women in Yunnan Province. J Infect Public Health. 2018;11(1):105–10. doi:10.1016/j.jiph.2017.06.012.
  • Li M, Du X, Lu M, Zhang W, Sun Z, Li L, Ye M, Fan W, Jiang S, Liu A, et al. Prevalence characteristics of single and multiple HPV infections in women with cervical cancer and precancerous lesions in Beijing, China. J Med Virol. 2019;91(3):473–81. doi:10.1002/jmv.25331.
  • Li C, Luo X, Li J. Characterization of HPV infection in women in Xiangxi autonomous prefecture. Jishou (China): Jishou University; 2019.
  • Li R, Yin X. Exploration of HPV distribution characteristics of high-grade cervical lesions and its application value in post-LEEP follow-up. China Med Pharm. 2019;9:85–8.
  • Li G, Liu G. Preliminary investigation on the role of HPV and PLOD2 in the progression of cervical intraepithelial neoplasia. Guangzhou (China): Nanfang Medical University; 2020.
  • Li Y, Wang H, Zhang Y, Jing X, Wu N, Hou Y, Hao C. Correlation between multi-type human papillomavirus infections and viral loads and the cervical pathological grade. Int J Gynaecol Obstet. 2021;152(1):96–102. doi:10.1002/ijgo.13406.
  • XJ L. Analysis of cervical cancer precancerous lesion, cervical cancer and human papillomavirus infection. Zhongguo Wei Sheng Jian Yan. 2023;33:853–7.
  • Liao L, Cheng H, Zeng F, Zhou W, Ding Y. Prevalence and distribution of human papillomavirus genotypes among women with high-grade squamous intraepithelial lesion and invasive cervical cancer in Ganzhou, China. J Clin Lab Anal. 2019;33(3):e22708. doi:10.1002/jcla.22708.
  • Liu Q. Association between different subtypes of HPV infection and cervical lesions. Clin Res Practicev. 2016;1:36–7.
  • Liu J, Zhang X, Luo M, Zhang Y, Wang Q, Zhang J Clinicopathological characteristics of cervical exfoliative cytology-negative genital tract high-risk human papillomavirus-positive patients. J Capital Med Univ. 2018;39(6):858–63.
  • Liu Y, Ang Q, Wu H, Xu J, Chen D, Zhao H, Liu H, Guo X, Gu Y, Qiu H, et al. Prevalence of human papillomavirus genotypes and precancerous cervical lesions in a screening population in Beijing, China: analysis of results from China’s top 3 hospital, 2009–2019. Virol J. 2020;17(1):104. doi:10.1186/s12985-020-01383-1.
  • Liu F, Chang L, Bai T, Liu X, Hu J. Association of human papillomavirus genotype distribution and cervical cytology: a cross-sectional study. Epidemiol Infect. 2021;149:e95. doi:10.1017/S0950268821000741.
  • Long W, Yang Z, Li X, Chen M, Liu J, Zhang Y, Sun X. HPV-16, HPV-58, and HPV-33 are the most carcinogenic HPV genotypes in Southwestern China and their viral loads are associated with severity of premalignant lesions in the cervix. Virol J. 2018;15(1):94. doi:10.1186/s12985-018-1003-x.
  • Ma Q, Hou M, Yang XF. Screening of the genital human papillomavirus infection among 8581 women in the first affiliated hospital of Xi’an Jiaotong university. Zhongguo Yi Xue Ke Xue Yuan Xue Bao. 2014;36(3):277–82. doi:10.3881/j.issn.1000-503X.2014.03.009.
  • Ma M, Zhu J, Yang Y, Wang X, Jin Y, Zhang J, Wu S. The distribution and pathogenic risk of non-9-valent vaccine covered HPV subtypes in cervical lesions. Cancer Med. 2022;11(6):1542–52. doi:10.1002/cam4.4532.
  • Meng J, Xu X, Lu Y, Fan Z, Cai G. Survey analysis of cervical exfoliative cell HPV infection subtypes among women in Shanghai from 2017 to 2020. J Diagn Concepts Pract. 2021;20:567–72.
  • Ou Y. Clinical analysis of human papillomavirus infection characteristics and relationship with cervical lesions in women in southern. Guangdong: Guangzhou Medical University; 2014.
  • Pang X, Mo L. Study on the relationship between different cervical lesions and HPV infection subtypes. Nanning (China): Guangxi Medical University; 2017.
  • Qin Y. Retrospective cohort study of focused ultrasound in the treatment of high-risk HPV infection with HSIL. Chongqing (China): ChongQing Medical University; 2022.
  • Qiu YT, Zhou JJ, Zhang JY. Epidemiological investigation and analysis of HPV infection and cervical intraepithelial neoplasia in women in pingxiang area. Med Innovation China. 2022;19:79–83.
  • Ren L, Shi Q, Wei Y. The relationship between human papillomavirus genotypes and cervical lesions. Chin Cancer Res Clin. 2016;28:107–11.
  • Shen Y, Gong JM, Li YQ, Gong YM, Lei DM, Cheng GM, Li XF. Epidemiology and genotype distribution of human papillomavirus (HPV) in women of Henan Province, China. Clin Chim Acta. 2013;415:297–301. doi:10.1016/j.cca.2012.11.005.
  • Singh S, Zhou Q, Yu Y, Xu X, Huang X, Zhao J, Han L, Wang K, Sun J, Li F. Distribution of HPV genotypes in Shanghai women. Int J Clin Exp Pathol. 2015;8(9):11901–8.
  • Song L, Lyu Y, Ding L, Li X, Gao W, Wang M, Hao M, Wang Z, Wang J. Prevalence and genotype distribution of high-risk human papillomavirus infection in women with abnormal cervical cytology: A population-based study in Shanxi Province, China. Cancer Manag Res. 2020;12:12583–91.
  • Sun D, Huang J, Geng J, Zhao G, Liu B, Wang C. Comparative analysis of HPV infection types in female genital tract diseases. Mil Med J Southeast China. 2022;24(2):128–32.
  • Tan Y, Xie L, Shi G, Yuan H, Liang J. Screening status and genotype analysis of 3632 human papillomavirus cases. Lab Med Clin. 2021;18:384–7.
  • Tang X, Jones TE, Jiang W, Austin M, He Y, Li L, Tong L, Wang C, Yang K, Yin R, et al. Extended human papillomavirus genotype distribution in cervical intraepithelial neoplasia and cancer: Analysis of 40 352 cases from a large academic gynecologic center in China. J Med Virol. 2023;95(1):e28302. doi:10.1002/jmv.28302.
  • Tao X, Zhang H, Zhang H, Xiao Y, Zhong F, Zhou X, Cong Q, Sui L, Zhao C. The clinical utility of extended high-risk HPV genotyping in risk-stratifying women with L-SIL cytology: A retrospective study of 8726 cases. Cancer Cytopathol. 2022;130(7):542–50. doi:10.1002/cncy.22573.
  • Tung H, Tang Y, Yang L, Huang H, Wu R, Pan Y, Jung S, Lin C, Wang C, Chao A, et al. Human papillomavirus genotype and long-term clinical outcomes of vulvar malignancies. Int J Gynecol Cancer. 2020;30:A75.
  • Wang L, Wu N. The value of TCT, HPV and DNA quantitative cytology in cervical lesions. Dalian (China): Dalian Medical University; 2013.
  • Wang X, Wang L. HPV genotype distribution and value of liquid-based cytology combined with HPV typing test and HPV16 DNA integration status in the screening and management of cervical lesions. Shijiazhuang (China): Hebei Medical University; 2013.
  • Wang H, Xie X. Distribution of HPV infection types in invasive cervical cancer and precancerous lesions in the Yangtze River Delta region of. China: Zhejiang University; 2014.
  • Wang L, Wu B, Li J, Chen L. Prevalence of human papillomavirus and its genotype among 1336 invasive cervical cancer patients in Hunan province, central south China. J Med Virol. 2015;87(3):516–21. doi:10.1002/jmv.24094.
  • Wang Y, Wang S, Shen J, Peng Y, Chen L, Mai R, Zhang G. Genotype distribution of human papillomavirus among women with cervical cytological abnormalities or invasive squamous cell carcinoma in a high-incidence area of esophageal carcinoma in China. Biomed Res Int. 2016;2016:1–6. doi:10.1155/2016/1256384.
  • Wang Z, Li Z, Li J, Wang C, Wang W, Hao M, Zhao C. Prevalence and distribution of HPV genotypes in 1387 women with cervical intraepithelial neoplasia 2/3 in Shanxi Province, China. J Cancer. 2018;9(16):2802–6. doi:10.7150/jca.25614.
  • Wang J, Tang D, Wang J, Zhang Z, Chen Y, Wang K, Zhang X, Ma C. Genotype distribution and prevalence of human papillomavirus among women with cervical cytological abnormalities in Xinjiang, China. Hum Vaccin Immunother. 2019;15(7):1889–96. doi:10.1080/21645515.2019.1578598.
  • Wang WP, An JS, Yao HW, Li N, Zhang YY, Ge L, Song Y, Wang MJ, Yuan GW, Sun YC, et al. Prevalence and attribution of high-risk HPV in different histological types of cervical cancer. Chin J Obstetrics Gynecology. 2019;54(5):293–300.
  • Wang J, Tang D, Wang J, Chen Y, Ma C. Survey on the prevalence and genotype distribution of human papillomavirus in patients with cervical squamous intraepithelial lesions and cervical cancer in Xinjiang. Chin J Hum Sex. 2020;29:35–8.
  • Wang L, He Y. Value of HPV typing test in the diagnosis of cervical lesions. Bengbu (China): Bengbu Medical College; 2020.
  • Wang XL, Sun H, Zhou QH, Chen YE, Fu JH, Li CM, Zhou A. Correlation between different HR-HPV subtypes and the severity of cervical lesions. J Cancer Control Treat. 2022;35(6):549–53.
  • Wu X, Zhao J, Cui X, Li Q, Tao H, Pan Q, Zhang X, Chen W, Li YP, Li RC, et al. [Prevalence of type-specific human papillomavirus infection among 18–45 year-old women from the general population in Liuzhou, Guangxi Zhuang autonomous region: a cross-sectional study]. Chin J Epidemiol. 2017;38(4):467–71. doi:10.3760/cma.j.issn.0254-6450.2017.04.011.
  • Wu Y, Wu X, Lv W, Zhang X, Zheng J. Clinical value of human papillomavirus genotyping in cervical lesions. J Molecular Diagnostics And Therapeutics. 2017;9:416–21.
  • Xiao X, Meng YB, Bai P, Zou J, Zhang Y, Bui Nguyen TM, Xiao J-G, Gao X-M, Wen B-F. Vulvar cancer in China: epidemiological features and risk analysis. J Cancer. 2017;8(15):2950–8. doi:10.7150/jca.20496.
  • Xu XX, Zhou JS, Yuan SH, Yu H, Lou HM. Distribution of HPV genotype in invasive cervical carcinoma and cervical intraepithelial neoplasia in Zhejiang Province, Southeast China: Establishing the baseline for surveillance. Int J Environ Res Public Health. 2015;12(9):10794–805. doi:10.3390/ijerph120910794.
  • Xu X, Feng T, Li D, Lou H, Lan H. Prevalent distribution and survival outcome of HPV infection in patients with early-stage cervical cancer in Hangzhou, China. BMC Infect Dis. 2022;22(1):941. doi:10.1186/s12879-022-07888-0.
  • Xu H, Chen Y, Zhao C, Wang Q, Tang M, Zhang W, Wang Q, Lou R, Liu T, Feng Y, et al. Bethesda system reporting rates, histological follow-up and HPV genotypes distribution of abnormal cytology in Anhui province of China: Analysis of 93,168 cervical liquid-based cytology test reports. Diagn Cytopathol. 2023;51(8):501–10. doi:10.1002/dc.25150.
  • Xue H, Gao H, Zheng J, Chen Y, Chen J, Pan D, Dong B, Sun P. Use of extended HR-HPV genotyping in improving the triage strategy of 2019 ASCCP recommendations in women with positive HR-HPV diagnosis and simultaneous LSIL cytology results. J Cancer. 2021;12(14):4332–40. doi:10.7150/jca.55826.
  • Yan H, Zhao J, Liu DJ, Chen GH. Analysis on human papillomavirus infection in 2 110 patients with cervical cancer in Henan province. Chin J Epidemiol. 2021;42(5):914–7. doi:10.3760/cma.j.cn112338-20200729-00992.
  • Yang H. Study of cervical HPV infection type and its significance in pre-cancer screening of the cervix. Chinese Medical Engineering. 2015;23:174+6.
  • Yang C, Xu Q, Zhang L, Wang J, Tian L, Zhan X. Analysis of 9227 cases of HPV infection status in naturally attending female patients in linyi people’s Hospital. Chin J Cancer Prev Treat. 2020;27:1113–18.
  • Yang T, Zhang W, Tan L, Gao Z, Ma L. Distribution characteristics of HPV subtypes in cervical intraepithelial neoplasia among ethnic minorities in kunming. Medicine And Pharmacy Of Yunnan. 2021;42:476–8.
  • You W, Li S, Du R, Zheng J, Shen A. Epidemiological study of high-risk human papillomavirus infection in subjects with abnormal cytological findings in cervical cancer screening. Exp Ther Med. 2018;15(1):412–8. doi:10.3892/etm.2017.5357.
  • Yu Z, Wang C, Geng J, Fan X, Zhang X, Xia L, Wang H, Long X, Zhao X. Distribution of HPV infection genotypes in cervical normal cells and cervical CIN grade III lesions and squamous cell carcinoma tissues. Maternal And Child Health Care Of China. 2015;30(31):5354–8.
  • Yuan H, Li R, Lv J, Yi G, Sun X, Zhao N, Zhao F, Xu A, Kou Z, Wen H. Epidemiology of human papillomavirus on condyloma acuminatum in Shandong Province, China. Hum Vaccin Immunother. 2023;19(1):2170662. doi:10.1080/21645515.2023.2170662.
  • Zhai Q, Wang X, Yu D, Fan Y, Li X, Ma Y, Meng Y, Li L, First Medical Center of PLA General Hospital. Distribution of high-risk human papillomavirus types and their prognosis in patients with high-grade cervical intraepithelial neoplasia. Zhonghua Yi Yuan Gan Ran Xue Za Zhi. 2021;31(10):1576–80.
  • Zhang ZM, Cui XQ, Li N, Zhang GJ, Zhao YH, Liu RR, Xie Q, Gao B. Human papillomavirus genotypes distribution in patients with cervical intraepithelial neoplasia and microinvasive cancer Chinese. Journal Of Xi’an Jiaotong University (Medical Sciences). 2016;37:697–702.
  • Zhang L, Bi Q, Deng H, Xu J, Chen J, Zhang M, Mu X. Human papillomavirus infections among women with cervical lesions and cervical cancer in Eastern China: genotype-specific prevalence and attribution. BMC Infect Dis. 2017;17(1):107. doi:10.1186/s12879-017-2223-1.
  • Zhang L, Xie F, Zhao D, Jiang L, Peng D, Wang B, et al. Analysis of human papillomavirus infection subtypes in female patients with condyloma acuminatum in Shandong Province. Chin J Hum Sex. 2018;27(9):105–9.
  • Zhang C, Huang C, Zheng X, Pan D. Prevalence of human papillomavirus among Wenzhou women diagnosed with cervical intraepithelial neoplasia and cervical cancer. Infect Agent Cancer. 2018;13(1):37. doi:10.1186/s13027-018-0211-8.
  • Zhang J, Zhang D, Yang Z, Wang X, Wang D. The role of human papillomavirus genotyping for detecting high-grade intraepithelial neoplasia or cancer in HPV-positive women with normal cytology: a study from a hospital in northeastern China. BMC Cancer. 2020;20(1):443. doi:10.1186/s12885-020-06935-w.
  • Zhang L, Wang Q, Zhang H, Xie Y, Sui L, Cong Q. Screening history in vaginal precancer and cancer: A retrospective study of 2131 cases in China. Cancer Manag Res. 2021;13:8855–63. doi:10.2147/CMAR.S335701.
  • Zhang QF, Wan ZQ, Tang JL. Characterization of HPV subtype distribution and analysis of risk factors in patients with cervical squamous intraepithelial lesion and cervical cancer. Mod Pract Med. 2022;34:1052–4+102.
  • Zhang R, Hong G, Liao C, Chen Z, Lin H, Yu L. High-risk human papillomavirus infection in Putian, China: a cross-sectional analysis of 98085 women. Journal Of The College Of Physicians And Surgeons–Pakistan: JCPSP. 2023;33:642–6.
  • Zhao XY, Kong WM, Jiao SM, Song D, Chen J, Shang RT. Prevalence and genotypes of human papilloma virus infection in CIN3 in Beijing, China. Transl Cancer Res. 2020;9(3):1978–84. doi:10.21037/tcr.2020.01.59.
  • Zheng S. Analysis of cervical HPV infection status and its correlation with vaginal microecology in 16324 women. Jinan (China): Shandong University; 2021.
  • Zhi HF, Yang LF, Ge J, Yang XT. The human papillomavirus infection characteristics for patients with cervical intraepithelial neoplasia in Yunnan, China: A sampling survey analysis. Infect Drug Resist. 2022;15:2843–51. doi:10.2147/IDR.S364763.
  • Zhong F, Li Z, Sun Y, Xiao Y, Li J, Zhou X, Cong Q, Sui L, Tao X, Zhao C. HPV genotyping of cervical histologic specimens of 61, 422 patients from the largest women hospital in China. Front Oncol. 2023;13:1161631. doi:10.3389/fonc.2023.1161631.
  • Zhou A, Du Y. Study on cervical cancer screening and influencing factors among rural women with household registration in. Wuhan: Huazhong University of Science and Technology; 2014.
  • Zhou Q, Shi Q, Zhao J, Wang D, Tang Z. Study on the genetic subtype distribution of human papillomavirus infection in patients with squamous and adenocarcinoma of the cervix in Gansu. Health Vocational Education. 2019;37:142–4.
  • Zhou J, Niaz M, Zhou Q, Wang P, Chen W, Li J. Analysis of the current status and influencing factors of HPV infection in cervical cancer patients in western China. Chinese Journal Of Clinical Obstetrics And Gynecology. 2020;21:13–16.
  • Zhou J, Xu H. Analysis of HPV infection status of cervical cancer screening population in wenshan prefecture. Yunnan Province: Baise (China): Yujiang Ethnic College of Medicine; 2020.
  • Zhu L, Guo J, Lv B, Zhang L, Li X. Analysis of the distribution of HPV infection genotypes in normal cervical tissue, cervical squamous cell carcinoma and adenocarcinoma tissue. Chin J Hum Sex. 2017;26:58–61.
  • Zhu C, Wang Y, Mao W, Zhang H, Ma J. Prevalence and distribution of HPV types in genital warts in Xi’an, China: a prospective study. BMJ Open. 2019;9(5):e023897. doi:10.1136/bmjopen-2018-023897.
  • Zhuang L, Xie X, Wang L, Weng X, Xiu Y, Liu D, Zhong L. Assessment of high-risk human papillomavirus infection characteristics in cervical squamous cell carcinoma and adenocarcinoma in china. Risk Manag Healthc Policy. 2022;15:2043–55. doi:10.2147/RMHP.S384342.
  • Gong Y, Wang Y, Zhou Q, Qu W, Chen F, Wang Y, Mo J, Zhang H, Lin L, Bi T, et al. The possible impact of novel mutations in human papillomavirus 52 on the infection characteristics. Microb Genomics. 2023;9(4). doi:10.1099/mgen.0.000962.
  • Wang X, Han S, Li X, Wang X, Wang S, Ma L. Prevalence and distribution of human papillomavirus (HPV) in Luoyang city of Henan province during 2015-2021 and the genetic variability of HPV16 and 52. Virol J. 2022;19(1):37. doi:10.1186/s12985-022-01759-5.
  • Song Z, Cui Y, Li Q, Deng J, Ding X, He J, Liu Y, Ju Z, Fang L. The genetic variability, phylogeny and functional significance of E6, E7 and LCR in human papillomavirus type 52 isolates in Sichuan, China. Virol J. 2021;18(1):94. doi:10.1186/s12985-021-01565-5.
  • Wang QY, Zhao XQ, Guo YC, Zhang L, Li XX, Wang Y. Relationship between E6 and E7 gene polymorphisms of human papillomavirus type 52 and cervical intraepithelial neoplasia. J Qingdao Univ. 2022;58:667–71.
  • Yang Z, He ZH, Zhang Y, Di XH, Zheng DF, Xu HH. Genetic variability in the E6 and E7 oncogenes of HPV52 and its prevalence in the Taizhou area, China. Virol J. 2022;19(1):194. doi:10.1186/s12985-022-01929-5.
  • Li Y, Zhou L, Liao Q, Liu H. Study of human papillomavirus type 52 genetic mutations and subtype classification collected in Beijing. Chin J Exp Clin Virol. 2016;30:558–61.
  • Zhao J, Zhan Q, Guo J, Liu M, Ruan Y, Zhu T, Han L, Li F. Phylogeny and polymorphism in the E6 and E7 of human papillomavirus: alpha-9 (HPV16, 31, 33, 52, 58), alpha-5 (HPV51), alpha-6 (HPV53, 66), alpha-7 (HPV18, 39, 59, 68) and alpha-10 (HPV6, 44) in women from Shanghai. Infect Agent Cancer. 2019;14(1):38. doi:10.1186/s13027-019-0250-9.
  • Chen Z, Jing Y, Wen Q, Ding X, Zhang S, Wang T, Zhang Y, Zhang J. L1 and L2 gene polymorphisms in HPV-58 and HPV-33: implications for vaccine design and diagnosis. Virol J. 2016;13(1):167. doi:10.1186/s12985-016-0629-9.
  • Wang Y, Han S, Wang X, Song S, Wang X. Characteristics of human papillomavirus infection among females and the genetic variations of HPV18 and HPV58 in Henan province, China. Sci Rep. 2023;13(1):2252. doi:10.1038/s41598-022-24641-4.
  • Chen Z, Jing Y, Wen Q, Ding X, Wang T, Mu X, Chenzhang Y, Cao M. E6 and E7 Gene Polymorphisms in Human Papillomavirus Types-58 and 33 Identified in Southwest China. PLOS ONE. 2017;12(1):e0171140. doi:10.1371/journal.pone.0171140.
  • Yang Z, Zhang C, Luo P, Ye M, Gong Q, Mei B. Genetic variability of E6 and E7 genes of human papillomavirus type 58 in jingzhou, Hubei Province of central China. Virol J. 2022;19(1):71. doi:10.1186/s12985-022-01801-6.
  • Yu JH, Shi WW, Zhou MY, Liu JM, Han QY, Xu HH. Genetic variability and oncogenic risk association of human papillomavirus type 58 E6 and E7 genes in Taizhou area, China. Gene. 2019;686:171–6. doi:10.1016/j.gene.2018.11.066.
  • Zhang S, Xu G, Ni H, Li S, Lv D. Distribution and variant spectrum of HPV58 infection in women with cervical infection in Ningbo. Zhonghua Yu Fang Yi Xue Za Zhi. 2017;18:91–6.
  • Liu Y, Pan Y, Gao W, Ke Y, Lu Z. Whole-genome analysis of human papillomavirus types 16, 18, and 58 isolated from cervical precancer and cancer samples in Chinese Women. Sci Rep. 2017;7(1):263. doi:10.1038/s41598-017-00364-9.
  • Jin R, Qian H, Zhang Y, Yuan D, Bao J, Zhou H, Chen M, Huang J, Yu H. The prevalence and genotype distribution of human papillomaviruses among women in Taizhou, China. Medicine (Baltimore). 2019;98(39):e17293. doi:10.1097/MD.0000000000017293.
  • Zhao S, Zhao X, Hu S, Lu J, Duan X, Zhang X, Chen F, Zhao F. Distribution of high-risk human papillomavirus genotype prevalence and attribution to cervical precancerous lesions in rural North China. Chin J C ancer R es. 2019;31(4):663–72. doi:10.21147/j.issn.1000-9604.2019.04.10.
  • Ni G, Huang K, Luan Y, Cao Z, Chen S, Ma B, Yuan J, Wu X, Chen G, Wang T, et al. Human papillomavirus infection among head and neck squamous cell carcinomas in southern China. PLOS ONE. 2019;14(9):e0221045. doi:10.1371/journal.pone.0221045.
  • Boon SS, Xia C, Lim JY, Chen Z, Law PTY, Yeung ACM, Thomas M, Banks L, Chan PKS. Human Papillomavirus 58 E7 T20I/G63S Variant Isolated from an East Asian Population Possesses High Oncogenicity. J Virol. 2020;94(8). doi:10.1128/JVI.00090-20.
  • Guan P, Howell-Jones R, Li N, Bruni L, de Sanjosé S, Franceschi S, Clifford GM. Human papillomavirus types in 115,789 HPV-positive women: a meta-analysis from cervical infection to cancer. Int J Cancer. 2012;131(10):2349–59. doi:10.1002/ijc.27485.
  • Orumaa M, Leinonen MK, Campbell S, Møller B, Myklebust T, Nygård M. Recent increase in incidence of cervical precancerous lesions in Norway: Nationwide study from 1992 to 2016. Int J Cancer. 2019;145(10):2629–38. doi:10.1002/ijc.32195.
  • McCredie MR, Sharples KJ, Paul C, Baranyai J, Medley G, Jones RW, Medley G, Jones RW, Skegg DC. Natural history of cervical neoplasia and risk of invasive cancer in women with cervical intraepithelial neoplasia 3: a retrospective cohort study. Lancet Oncol. 2008;9(5):425–34. doi:10.1016/S1470-2045(08)70103-7.
  • Kind AB, Pavelyev A, Kothari S, El Mouaddin N, Schmidt A, Morais E, Guggisberg P, Lienert F. Assessing the epidemiological impact on cervical cancer of switching from 4-valent to 9-valent HPV vaccine within a gender-neutral vaccination programme in Switzerland. BMC Public Health. 2020;20(1):671. doi:10.1186/s12889-020-08840-0.
  • Mix JM, Saraiya M, Senkomago V, Unger ER. High-Grade Vulvar, Vaginal, and anal precancers among U.S. Adolescents and young adults after human papillomavirus vaccine introduction. Am J Prev Med. 2022;62(1):95–9. doi:10.1016/j.amepre.2021.06.026.
  • Khawar L, McManus H, Vickers T, Chow EPF, Fairley CK, Donovan B, Machalek DA, Regan DG, Grulich AE, Guy RJ, et al. Genital warts trends in Australian and overseas-born people in Australia: A cross-sectional trend analysis to measure progress towards control and elimination. Lancet Reg Health West Pac. 2021;16:100251. doi:10.1016/j.lanwpc.2021.100251.
  • Diana G, Corica C. Human Papilloma virus vaccine and prevention of head and neck cancer, what is the current evidence? Oral Oncol. 2021;115:105168. doi:10.1016/j.oraloncology.2020.105168.
  • Zhao XL, Hu SY, Hu JW, Wang HH, Wen TM, Feng YS, Qiao Y-L, Zhao F-H, Zhang Y. Tackling barriers to scale up human papillomavirus vaccination in China: progress and the way forward. Infect Dis Poverty. 2023;12(1):86. doi:10.1186/s40249-023-01136-6.
  • Xie P, Zhao J, Li X, Zou X, Liu G, Han X. Preference for human papillomavirus vaccine type and vaccination strategy among parents of school-age girls in Guangdong province, China. Prev Med Rep. 2023;36:102463. doi:10.1016/j.pmedr.2023.102463.
  • Barnabas RV, Brown ER, Onono MA, Bukusi EA, Njoroge B, Winer RL, Galloway DA, Pinder LF, Donnell D, Wakhungu IN, et al. Durability of single-dose HPV vaccination in young Kenyan women: randomized controlled trial 3-year results. Nat Med. 2023;29(12):3224–32. doi:10.1038/s41591-023-02658-0.
  • Chan PK, Luk AC, Park JS, Smith-McCune KK, Palefsky JM, Konno R, Giovannelli L, Coutlée F, Hibbitts S, Chu T-Y, et al. Identification of human papillomavirus type 58 lineages and the distribution worldwide. J Infect Dis. 2011;203(11):1565–73. doi:10.1093/infdis/jir157.
  • Tenjimbayashi Y, Onuki M, Hirose Y, Mori S, Ishii Y, Takeuchi T, Tasaka N, Satoh T, Morisada T, Iwata T, et al. Whole-genome analysis of human papillomavirus genotypes 52 and 58 isolated from Japanese women with cervical intraepithelial neoplasia and invasive cervical cancer. Infect Agent Cancer. 2017;12(1):44. doi:10.1186/s13027-017-0155-4.
  • Choi YJ, Ki EY, Zhang C, Ho WC, Lee SJ, Jeong MJ, Chan PK, Park JS. Analysis of Sequence Variation and Risk Association of Human Papillomavirus 52 Variants Circulating in Korea. PloS One. 2016;11(12):e0168178. doi:10.1371/journal.pone.0168178.
  • Chang YJ, Chen HC, Lee BH, You SL, Lin CY, Pan MH, Chou Y-C, Hsieh C-Y, Chen YMA, Cheng Y-J, CBCSP-HPV Study Group. Unique variants of human papillomavirus genotypes 52 and 58 and risk of cervical neoplasia. Int J Cancer. 2011;129(4):965–73. doi:10.1002/ijc.25724.
  • Chan PKS, Luk ACS, Park J-S, Smith-McCune KK, Palefsky JM, Konno R, Giovannelli L, Coutlée F, Hibbitts S, Chu T-Y, et al. Identification of human papillomavirus type 58 lineages and the distribution worldwide. J Infect Dis. 2011;203(11):1565–73. doi:10.1093/infdis/jir157.
  • Pal A, Kundu R. Human papillomavirus E6 and E7: The cervical cancer hallmarks and targets for therapy. Front Microbiol. 2019;10:3116. doi:10.3389/fmicb.2019.03116.
  • Ding T, Wang X, Ye F, Cheng X, Ma D, Lu W, Xie X. Distribution of human papillomavirus 58 and 52 E6/E7 variants in cervical neoplasia in Chinese women. Gynecol Oncol. 2010;119(3):436–43. doi:10.1016/j.ygyno.2010.08.032.
  • Chan PKS, Lam CW, Cheung TH, Li WW, Lo KW, Chan MY, Cheung JL, Cheng AF. Association of human papillomavirus type 58 variant with the risk of cervical cancer. J Natl Cancer Inst. 2002;94(16):1249–53. doi:10.1093/jnci/94.16.1249.
  • Gillison ML, Koch WM, Capone RB, Spafford M, Westra WH, Wu L, Zahurak ML , Daniel RW, Viglione M, Symer DE, Shah KV et al. Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J Natl Cancer Inst. 2000;92(9):709–20. doi:10.1093/jnci/92.9.709.
  • de Sanjosé S, Serrano B, Tous S, Alejo M, Lloveras B, Quirós B, Clavero O, Vidal A, Ferrándiz-Pulido C, Pavón MA, et al. Burden of Human Papillomavirus (HPV)-Related Cancers Attributable to HPVs 6/11/16/18/31/33/45/52 and 58. JNCI Cancer Spectr. 2018;2(4):ky045. doi:10.1093/jncics/pky045.
  • Yhim HY, Lee NR, Song EK, Kwak JY, Lee ST, Kim JH, Kim J-S, Park HS, Chung I-J, Shim H-J, et al. The prognostic significance of tumor human papillomavirus status for patients with anal squamous cell carcinoma treated with combined chemoradiotherapy. Int J Cancer. 2011;129(7):1752–60. doi:10.1002/ijc.25825.
  • Wei W, Shi Q, Guo F, Zhang BY, Chen C, Zhang NS, Dong XP. The distribution of human papillomavirus in tissues from patients with head and neck squamous cell carcinoma. Oncol Rep. 2012;28(5):1750–6. doi:10.3892/or.2012.1990.
  • Xu Y, Liu S, Yi H, Wang J, Luo Y, Yin S. Low prevalence of human papillomavirus in head and neck squamous cell carcinoma in Chinese patients. J Med Virol. 2015;87(2):281–6. doi:10.1002/jmv.24052.
  • Huang H, Zhang B, Chen W, Zhou SM, Zhang YX, Gao L, Xu ZG, Qiao YL, Tang PZ. Human papillomavirus infection and prognostic predictors in patients with oropharyngeal squamous cell carcinoma. Asian Pac J Cancer Prev. 2012;13(3):891–6. doi:10.7314/APJCP.2012.13.3.891.
  • Huang SF, Li HF, Liao CT, Wang HM, Chen IH, Chang JT, Chen Y-J, Cheng A-J. Association of HPV infections with second primary tumors in early-staged oral cavity cancer. Oral Dis. 2012;18(8):809–15. doi:10.1111/j.1601-0825.2012.01950.x.
  • Zainura A, Yalkun Y, Wu M. The different experession of human papilloma viral types 6 and 11 in Uyghur and Chinese juvenile recurrent respiratory papillomatosis in a large pediatric population in Xinjiang. J clin Otolaryngol, Head, and Neck Surg. 2013;27:1205–7.
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