Trends in high-risk human papillomavirus infection and cervical cytology of women in Karamay City, 2012–2021
Xiaoping Jia A , Min Jiang B , Jing Zhou C and Cailing Ma
D *
A
B
C
D
Abstract
To describe the changes in cervical lesions prevalence and high-risk human papillomavirus (HR-HPV) infections from 2012 to 2021, which have never been reported before, to provide direction for the effective implementation of cervical cancer prevention measures.
This retrospective study included women aged >25 years who received either organised or opportunistic cervical HR-HPV screening from January 2012 to December 2021 in Karamay Central Hospital, Karamay, China. The patients were split into four groups according to age 25–35, 36–45, 46–55 and >55 years, respectively. The Joinpoint Regression Program was used to analyse the trends of HR-HPV infection and the detection of cervical lesions.
Data from 85,429 women revealed a decline in HR-HPV infection rates across all age groups from 2012 to 2021. Although HR-HPV infection rates decreased, cervical lesion detection rates increased, although the proportion of cervical cancer in these lesions declined, likely due to enhanced awareness and HPV vaccination in Karamay. From 2012 to 2021, the prevalence of low-grade squamous intraepithelial lesions was 9.70%, and high-grade squamous intraepithelial lesions was 5.85%. HR-HPV infections were highest in the ≥55 years age group, with HPV52 (20.96%) being the most prevalent type.
In the past 10 years, the prevalence of HR-HPV infection has shown a decreasing trend, whereas the detection prevalence of cervical lesions has shown an upward trend among women in Karamay City. Importantly, particular emphasis should be placed on cervical cancer screening in women aged >55 years.
Keywords: cervical cancer, cervical lesions, high-grade squamous intraepithelial lesions, high-risk human papilloma virus, infection, Karamay, low-grade squamous intraepithelial lesions, prevalence.
References
1 Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021; 71(3): 209-49.
| Crossref | Google Scholar |
2 Duan R, Qiao Y, Clifford G, Zhao F. Cancer burden attributable to human papillomavirus infection by sex, cancer site, age, and geographical area in China. Cancer Med 2020; 9(1): 374-84.
| Crossref | Google Scholar | PubMed |
3 Arbyn M, Weiderpass E, Bruni L, de Sanjosé S, Saraiya M, Ferlay J, et al. Estimates of incidence and mortality of cervical cancer in 2018: a worldwide analysis. Lancet Glob Health 2020; 8(2): e191-e203.
| Crossref | Google Scholar |
4 Crosbie EJ, Einstein MH, Franceschi S, Kitchener HC. Human papillomavirus and cervical cancer. Lancet 2013; 382(9895): 889-99.
| Crossref | Google Scholar | PubMed |
5 Liverani CA, Di Giuseppe J, Giannella L, Delli Carpini G, Ciavattini A. Cervical cancer screening guidelines in the postvaccination era: review of the literature. J Oncol 2020; 2020: 8887672.
| Crossref | Google Scholar |
6 Arbyn M, de Sanjosé S, Saraiya M, Sideri M, Palefsky J, Lacey C, et al. EUROGIN 2011 roadmap on prevention and treatment of HPV-related disease. Int J Cancer 2012; 131(9): 1969-82.
| Crossref | Google Scholar | PubMed |
7 Zhao C, Zhao Y, Li J, Li M, Shi Y, Wei L. Opportunities and challenges for human papillomavirus vaccination in China. Hum Vaccin Immunother 2024; 20(1): 2329450.
| Crossref | Google Scholar | PubMed |
8 Zhao XL, Hu SY, Hu JW, Wang HH, Wen TM, Feng YS, et al. Tackling barriers to scale up human papillomavirus vaccination in China: progress and the way forward. Infect Dis Poverty 2023; 12(1): 86.
| Crossref | Google Scholar | PubMed |
9 Wheeler CM, Hunt WC, Cuzick J, Langsfeld E, Pearse A, Montoya GD, et al. A population-based study of human papillomavirus genotype prevalence in the United States: baseline measures prior to mass human papillomavirus vaccination. Int J Cancer 2013; 132(1): 198-207.
| Crossref | Google Scholar | PubMed |
10 Dareng EO, Ma B, Famooto AO, Adebamowo SN, Offiong RA, Olaniyan O, et al. Prevalent high-risk HPV infection and vaginal microbiota in Nigerian women. Epidemiol Infect 2016; 144(1): 123-137.
| Crossref | Google Scholar | PubMed |
11 Teka B, Gizaw M, Ruddies F, Addissie A, Chanyalew Z, Skof AS, et al. Population-based human papillomavirus infection and genotype distribution among women in rural areas of South Central Ethiopia. Int J Cancer 2021; 148(3): 723-730.
| Crossref | Google Scholar | PubMed |
12 Zhu Y, Qian F, Zou W, Wu X, Liu C, Shen G, et al. Prevalence and genotype distribution of human papillomavirus infection in Huzhou City, eastern China, 2018–2019. Trans R Soc Trop Med Hyg 2021; 115(1): 30-37.
| Crossref | Google Scholar | PubMed |
13 Yang J, Wang W, Wang Z, Wang Z, Wang Y, Wang J, et al. Prevalence, genotype distribution and risk factors of cervical HPV infection in Yangqu, China: a population-based survey of 10086 women. Hum Vaccin Immunother 2020; 16(7): 1645-52.
| Crossref | Google Scholar | PubMed |
14 Jiang L, Tian X, Peng D, Zhang L, Xie F, Bi C, et al. HPV prevalence and genotype distribution among women in Shandong Province, China: Analysis of 94,489 HPV genotyping results from Shandong’s largest independent pathology laboratory. PLoS ONE 2019; 14(1): e0210311.
| Crossref | Google Scholar | PubMed |
15 Zhang C, Cheng W, Liu Q, Guan Q, Zhang Q. Distribution of human papillomavirus infection: a population-based study of cervical samples from Jiangsu Province. Virol J 2019; 16(1): 67.
| Crossref | Google Scholar | PubMed |
16 Mai Q, Yang X, Cheng H, Wu G, Wu Z. Prevalence and genotype distribution of human papillomavirus among women with cervical lesions in Shenzhen city, China. Hum Vaccin Immunother 2021; 17(4): 965-71.
| Crossref | Google Scholar | PubMed |
17 Hao S, Wang C, Liu S, He J, Jiang Y. HPV genotypic spectrum in Jilin province, China, where non-vaccine-covered HPV53 and 51 are prevalent, exhibits a bimodal age-specific pattern. PLoS ONE 2020; 15(3): e0230640.
| Crossref | Google Scholar | PubMed |
18 Melnikow J, Nuovo J, Willan AR, Chan BK, Howell LP. Natural history of cervical squamous intraepithelial lesions: a meta-analysis. Obstet Gynecol 1998; 92(4 Pt 2): 727-35.
| Crossref | Google Scholar | PubMed |
19 Perkins RB, Wentzensen N, Guido RS, Schiffman M. Cervical cancer screening: a review. JAMA 2023; 330(6): 547-58.
| Crossref | Google Scholar | PubMed |
20 Tainio K, Athanasiou A, Tikkinen KAO, Aaltonen R, Cárdenas J, Hernándes, et al. Clinical course of untreated cervical intraepithelial neoplasia grade 2 under active surveillance: systematic review and meta-analysis. BMJ 2018; 360: k499.
| Crossref | Google Scholar | PubMed |
21 Wu W, Song L, Yang Y, Wang J, Liu H, Zhang L. Exploring the dynamics and interplay of human papillomavirus and cervical tumorigenesis by integrating biological data into a mathematical model. BMC Bioinformat 2020; 21(Suppl 7): 152.
| Crossref | Google Scholar |
22 Demarco M, Cheung LC, Kinney WK, Wentzensen N, Lorey TS, Fetterman B, et al. Low risk of cervical cancer/precancer among most women under surveillance postcolposcopy. J Low Genit Tract Dis 2018; 22(2): 97-103.
| Crossref | Google Scholar | PubMed |
23 Li M, Wei L, Sui L, Ma D, Kong B, Wu X, et al. Guidelines for cervical cancer screening in China. Gynecol Obstet Clin Med 2023; 3(4): 189-94.
| Crossref | Google Scholar |
24 Nie Y-W, Ma Y-H, Wang C-C, Tian M-Z, Jiang M, Yang Z, et al. Analysis of HPV infection characteristics and trend of cohort population in Karamay City, Xinjiang, 2010–2019 based on Joinpoint and APC Model. Mod Prevent Med 2022; 49(11): 1921-5.
| Google Scholar |
25 Ronco G, Giorgi-Rossi P, Carozzi F, Confortini M, Dalla Palma P, Del Mistro A, et al. Efficacy of human papillomavirus testing for the detection of invasive cervical cancers and cervical intraepithelial neoplasia: a randomised controlled trial. Lancet Oncol 2010; 11(3): 249-57.
| Crossref | Google Scholar | PubMed |
26 Brisson M, Drolet M. Global elimination of cervical cancer as a public health problem. Lancet Oncol 2019; 20(3): 319-21.
| Crossref | Google Scholar | PubMed |
27 McCluggage WG, Singh N, Gilks CB. Key changes to the World Health Organization (WHO) classification of female genital tumours introduced in the 5th edition (2020). Histopathology 2022; 80(5): 762-78.
| Crossref | Google Scholar |
28 Ilic M, Ilic I. Cancer mortality in Serbia, 1991–2015: an age-period-cohort and joinpoint regression analysis. Cancer Commun 2018; 38(1): 10.
| Crossref | Google Scholar |
29 Wang J, Tang D, Wang K, Wang J, Zhang Z, Chen Y, et al. HPV genotype prevalence and distribution during 2009–2018 in Xinjiang, China: baseline surveys prior to mass HPV vaccination. BMC Women’s Health 2019; 19(1): 90.
| Crossref | Google Scholar |
30 Cohen PA, Jhingran A, Oaknin A, Denny L. Cervical cancer. Lancet 2019; 393(10167): 169-82.
| Crossref | Google Scholar |
31 Han X, Song G, Li Y, Dong Z, Yan X, Wang S, et al. Prevalence and genotype distribution of human papillomavirus infection among women aged 30–65 years in Xi’an, China: a population-based study of 14,655 women. Human Vaccin & Immunotherap 2021; 17(12): 5439-46.
| Crossref | Google Scholar |
32 Pan XF, Li R, Pan A, Larson H. Human papillomavirus vaccine approval in China: a major step forward but challenges ahead. Lancet Infect Dis 2016; 16(12): 1322-23.
| Crossref | Google Scholar | PubMed |
33 Franceschi S, Herrero R, Clifford GM, Snijders PJ, Arslan A, Anh PT, et al. Variations in the age-specific curves of human papillomavirus prevalence in women worldwide. Int J Cancer 2006; 119(11): 2677-84.
| Crossref | Google Scholar | PubMed |
34 de Sanjosé S, Diaz M, Castellsagué X, Clifford G, Bruni L, Muñoz N, et al. Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: a meta-analysis. Lancet Infect Dis 2007; 7(7): 453-59.
| Crossref | Google Scholar | PubMed |
35 Li P, Liu Q, Li W, Liu Z, Xing B, Wu S, et al. Characteristics of human papillomavirus infection among women with cervical cytological abnormalities in the Zhoupu District, Shanghai City, China, 2014-2019. Virol J 2021; 18(1): 51.
| Crossref | Google Scholar | PubMed |
36 Tang SY, Liao YQ, Hu Y, Shen HY, Wan YP, Wu YM. HPV prevalence and genotype distribution among women from Hengyang district of Hunan Province, China. Front Public Health 2021; 9: 710209.
| Crossref | Google Scholar | PubMed |
37 Luo Q, Lang L, Han N, Liang L, Shen L, Zhang H. Prevalence and genotype distribution of high-risk human papillomavirus infection among women with cervical cytological abnormalities in Chongqing, China, 2014–2020. Diagn Cytopathol 2021; 49(12): 1237-43.
| Crossref | Google Scholar | PubMed |
38 Wang R, Guo XL, Wisman GBA, Schuuring E, Wang WF, Zeng ZY, et al. Nationwide prevalence of human papillomavirus infection and viral genotype distribution in 37 cities in China. BMC Infect Dis 2015; 15: 257.
| Crossref | Google Scholar | PubMed |
39 Ogilvie GS, van Niekerk D, Krajden M, Smith LW, Cook D, Gondara L, et al. Effect of screening with primary cervical HPV testing vs cytology testing on high-grade cervical intraepithelial neoplasia at 48 months: the HPV FOCAL randomized clinical trial. JAMA 2018; 320(1): 43-52.
| Crossref | Google Scholar | PubMed |
40 Song L, Lyu Y, Ding L, Li X, Gao W, Wang M, et al. 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.
| Crossref | Google Scholar |
41 Lyu Y, Ding L, Gao T, Li Y, Li L, Wang M, et al. Influencing factors of high-risk human papillomavirus infection and DNA load according to the severity of cervical lesions in female coal mine workers of China. J Cancer 2019; 10(23): 5764-69.
| Crossref | Google Scholar | PubMed |
42 Zhang R, Xu W, Yang S, Hu D, Bai L, Xiang R, et al. Prevalence of high-risk human papillomavirus infection, associated risk factors, and relationship with cervical precancerous lesions in perimenopausal and older women in an area with high cervical cancer incidence in China. Cureus 2024; 16(4): e58081.
| Crossref | Google Scholar | PubMed |
43 Mboumba Bouassa RS, Nodjikouambaye ZA, Sadjoli D, Adawaye C, Péré H, Veyer D, et al. High prevalence of cervical high-risk human papillomavirus infection mostly covered by Gardasil-9 prophylactic vaccine in adult women living in N’Djamena, Chad. PLoS ONE 2019; 14(6): e0217486.
| Crossref | Google Scholar | PubMed |
44 Patel SJ, Mugo NR, Cohen CR, Ting J, Nguti R, Kwatampora J, et al. Multiple human papillomavirus infections and HIV seropositivity as risk factors for abnormal cervical cytology among female sex workers in Nairobi. Int J STD AIDS 2013; 24(3): 221-5.
| Crossref | Google Scholar | PubMed |
45 Molina-Pineda A, López-Cardona MG, Limón-Toledo LP, Cantón-Romero JC, Martínez-Silva MG, Ramos-Sánchez HV, et al. High frequency of HPV genotypes 59, 66, 52, 51, 39 and 56 in women from Western Mexico. BMC Infect Dis 2020; 20(1): 889.
| Crossref | Google Scholar | PubMed |
46 de Sanjose S, Quint WG, Alemany L, Geraets DT, Klaustermeier JE, Lloveras B, et al. Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol 2010; 11(11): 1048-56.
| Crossref | Google Scholar | PubMed |
47 Bruni L, Diaz M, Castellsagué X, Ferrer E, Bosch FX, de Sanjosé S. Cervical human papillomavirus prevalence in 5 continents: meta-analysis of 1 million women with normal cytological findings. J Infect Dis 2010; 202(12): 1789-99.
| Crossref | Google Scholar | PubMed |
48 Crow JM. HPV: The global burden. Nature 2012; 488(7413): S2-3.
| Crossref | Google Scholar | PubMed |
49 Li K, Li Q, Song L, Wang D, Yin R. The distribution and prevalence of human papillomavirus in women in mainland China. Cancer 2019; 125(7): 1030-37.
| Crossref | Google Scholar | PubMed |
50 Han C, Huang W, Ye M, Zou R, Lan J, Chen J, et al. HPV prevalence and genotype distribution in 2,306 patients with cervical squamous cell carcinoma in central and eastern China. Front Public Health 2023; 11: 1225652.
| Crossref | Google Scholar | PubMed |
51 Yang X, Li Y, Tang Y, Li Z, Wang S, Luo X, et al. Cervical HPV infection in Guangzhou, China: an epidemiological study of 198,111 women from 2015 to 2021. Emerg Microbes Infect 2023; 12(1): e2176009.
| Crossref | Google Scholar | PubMed |
52 Health Commission of Xinjiang Uygur Autonomous Region. Xinjiang’s 249-valent HPV vaccine basically realizes full coverage of all prefectures (states and cities) and key counties (cities and districts). Available at https://wjw.xinjiang.gov.cn/hfpc/xwxc1/202407/35196c05ebb84263ab5ac0275d223d9f.shtml
53 Ye J, Cao L, Yu W, Song Y, Yin Z. Reported routine immunization coverage with National Immunization Program vaccines in China, 2020–2021. Chinese J Vaccin Immuniz 2022; 28(5): 576-80.
| Google Scholar |
